Universidad Politécnica de Madrid
Facultad de Ciencias de la Actividad Física y el Deporte (INEF)
Termografía infrarroja y dolor de hombro en usuarios
de sillas de ruedas
Infrared thermography and shoulder pain in wheelchair
users
Tesis Doctoral con Mención Internacional / International PhD Thesis
Isabel Rossignoli Fernández
Licenciada y Máster en Ciencias de la Actividad Física y del Deporte
Master of Science in Adapted Physical Activity
Madrid, 2015
Isabel Rossignoli 2015
Isabel Rossignoli, 2015
Título: Termografía infrarroja y dolor de hombro en usuarios de sillas de ruedas. Infrared
thermography and shoulder pain in wheelchair users
Universidad Politécnica de Madrid 2015
Editorial: FUNDACIÓN GENERAL DE LA U.P.M.
www.fgupm.es
ISBN: 978-84 608-4845-5
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PhD thesis
DEPARTAMENTO DE SALUD Y RENDIMIENTO HUMANO
FACULTAD DE CIENCIAS DE LA ACTIVIDAD FÍSICA Y DEL DEPORTE (INEF)
Termografía infrarroja y dolor de hombro en usuarios
de sillas de ruedas
Infrared thermography and shoulder pain in wheelchair
users
Isabel Rossignoli Fernández
Licenciada y Máster en Ciencias de la Actividad Física y el Deporte
Master of Science in Adapted Physical Activity
DIRECTORES DE TESIS
Pedro José Benito Peinado
Azael Juan Herrero Alonso
PhD
PhD
Prof. Titular de Universidad
Prof. Titular de Universidad
Universidad Politécnica de
Madrid
Universidad Europea Miguel de
Cervantes
Madrid, 2015
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Isabel Rossignoli 2015
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PhD thesis
MIEMBROS DEL TRIBUNAL
Tribunal nombrado por el Magfco. y Excmo. Sr. Rector de la Universidad
Politécnica de Madrid, el día ____________________________________________________________
Presidente D. _____________________________________________________________________________
Vocal D. ___________________________________________________________________________________
Vocal D. ___________________________________________________________________________________
Vocal D. ___________________________________________________________________________________
Secretario D. _____________________________________________________________________________
MIEMBROS DEL TRIBUNAL SUPLENTES
Vocal D. ___________________________________________________________________________________
Vocal D. ___________________________________________________________________________________
Realizado el acto de defensa y lectura de Tesis el día _________________________________
en _________________________________________________________________________________________
Calificación: ______________________________________________________________________________
EL PRESIDENTE
LOS VOCALES
EL SECRETARIO
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Isabel Rossignoli 2015
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PhD thesis
A mi abuela ‘grande’
“El futuro tiene muchos nombres: para el débil es lo inalcanzable,
para el miedoso lo desconocido. Para el valiente, la oportunidad”
(Víctor Hugo)
"Valiente no es el que no tiene miedo, sino el que lucha y se enfrenta a sus miedos"
(Isabel Rossignoli)
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Isabel Rossignoli 2015
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PhD thesis
AGRADECIMIENTOS
Winston Churchill, político británico y premio novel Laureate, afirmó “success is the ability
to go from one failure to another with no loss of enthusiasm”. Allí donde el entusiasmo falla,
las fuerzas flaquean, o las zancadillas aparecen, es el punto de encuentro con muchas
personas, que intencional o fortuitamente me han echado una mano o directamente no han
dudado en sostenerme entre sus brazos. Al final de una tesis empieza una nueva etapa.
Espero compartirla de nuevo con vosotros.
Mi director, pero sobretodo mi amigo, Pedro J. Benito. Lo que no aparece en tu curriculum
es justo lo que más valor tiene, me quedo con tu ejemplo de honestidad, honradez y
perseverancia. Eres un referente para alumnos y profesores, pero sobretodo eres un modelo
como persona. Te estaré siempre agradecida por todo el apoyo recibido cuando más lo he
necesitado, por tu comprensión cuando perdía la serenidad, y por tus consejos humanos y
profesionales (me quedo con tu sabiamente repetida frase ante cualquier problema:
“seamos pragmáticos”).
Azael J. Herrero, muchísimas gracias por confiar en mí, sin conocerme me abriste las puertas
del CIDIF, me ofreciste todo tu equipo, y me aconsejaste en numerosas ocasiones. Gracias
también por presentarme a los compañeros del CIDIF, Juancho Martín, Héctor Alegre, Pedro
Marín, que me recibieron con los brazos abiertos y me brindaron todos sus conocimientos y
apoyo. Nunca disfruté y aprendí tanto en una toma de datos como esos intensos 5 meses en
Valladolid. Mi agradecimiento se extiende a todos los 55 sujetos que participaron
voluntariamente en la aventura de someterse a 11 test, ¡algunos hasta 2 veces! Tanto los
jugadores del MUPLI y de la Fundación Grupo Norte, como los residentes de ASPAYM
Castilla y León, gracias por vuestra generosidad y todas las conversaciones compartidas.
Manuel Sillero Quintana, el terremoto del INEF. Siempre dejando huella por donde pasas.
¿Cuántas personas habrán recibido tu ayuda en el INEF? Incontables. Incansable trabajador,
abierto a dar y recibir conocimiento de quien fuese. Muchísimas gracias por compartir tu
entusiasmo, energía, y por brindarme tu ayuda en numerosas ocasiones.
Aplicando el refrán, “dime con quién andas y te diré quién eres”, puedo enorgullecerme de
“andar” con lo mejorcito del INEF, y es que todos sus rincones me han regalado personas
fantásticas. Empezando por mi equipo de fabulosas y empollonas: Ana Paz Bermúdez, Ana
Belén Peinado, Cristina Vintaned, Marta Rodelgo y Rosa Mª Valera. Hemos compartido todas
las clases, prácticas, estudios, dudas, y cuando ya no quedaban años de clases, seguimos
compartiendo historias de novios, hijos, oposiciones, viajes… Os llevo con mucho cariño en
mi maleta. Rocío Cupeiro y Helena la chula, mis coaches particulares. Cada encuentro es una
charla de crecimiento, es un sincero abrir el corazón. Sin duda habéis caminado de la mano
de esta tesis y no sería igual sin vosotras. Mi rincón favorito del INEF, la biblioteca, donde
Minerva siempre me guarda un rato para una charla cariñosa y Gloria me pasaba los
artículos y compartía sueños de escaladas pirenaicas. El INEF tiene mucho que ofrecer no
solo en las clases, también en sus laboratorios, y he tenido la suerte de pasar mucho tiempo
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Isabel Rossignoli 2015
en varios. El laboratorio de Fisiología del Esfuerzo, donde Irma Lorenzo, Mercedes Galindo y
Javier Calderón transformaron las pruebas de esfuerzo en el más emocionante de los tests
deportes. Gracias por vuestras enseñanzas, amor a la ciencia y momentos compartidos.
Javier Brutragueño, tus palabras el día de tu defensa realmente me hicieron cambiar el chip
para conseguir disfrutar esta última etapa afrontando con alegría el estrés. El laboratorio de
termografía, antes pemaGroup y ahora ThermoHuman; Manolo me invitó a entrar y allí me
atraparon las risas, compañerismo y hospitalidad de Miguel ‘miarma’, Ismael Fernández,
Peter Gómez, Sergio ‘canicas’ Piñonosa y Javier Arnaiz. Empezamos de cero y el sueño
continua, gracias Javier por resucitarlo. Gracias Miguel por hacer el INEF un poco más
divertido y humano. Gracias Isma por tus palabras de ánimo y todo tu apoyo en esta última
etapa. Gracias Peter por tu ejemplo de liderazgo, por tus consejos, pero sobre todo, por tus
bromas. Clemens Ley y María Rato me inspirasteis en mis comienzos del doctorado siendo
modelo de solidaridad, esfuerzo, rigurosidad, e impulso para realizar los voluntariados en
deporte adaptado en Guatemala y Argentina. Gracias por presentarme al grupo DIM. Me
llevo con cariño las enseñanzas y el tiempo compartido con muchos profesores: Javier
Durán, Carlos Cordente, Alberto García, Jose Antonio García de Mingo, Javier Rojo,
Guadalupe Garrido, Alfonso López, Enrique López, José Aparicio, Vicente Gómez, Cristina
López, Isabel Rico, Isabel Martín, Mª José Gómez… Mil gracias Andrés desde secretaría por
salvar el pellejo de los alumnos todos los días. Gracias Gador, que has ejercido de madre en
el INEF empujándome a terminar pronto la tesis.
La tesis empezó en Madrid y decidió viajar. En el Erasmus Mundus Master in Adapted
Physical Activity aprendí de la mano de grandes profesores y científicos a nivel internacional,
sus enseñanzas y trabajos fueron fuente de inspiración para esta tesis. In particular, Sean
Tweedy thanks for trusting me and for supervising the master’s thesis in Australia, you
taught me to dream high and to see the international perspective of the Paralympic
Movement, many thanks for your teaching in the data collection of Kenya. Thanks Alice
Niewbouer for your patience, empathy and feedback to the master’s thesis. Viajar es el
mejor de los aprendizajes, el máster me regaló la oportunidad de recorrer varios países.
Empezando por Bélgica, donde tuve la suerte de tener por compañeras y buenas amigas a
Erika Ermacora, Andreea Dragos y Julie Jayapal, gracias por vuestra dulzura y cuidados;
Noruega me abrió un mundo de posibilidades en la utilización del deporte como medio de
rehabilitación, me permitió aplicar los conocimientos adquiridos, tratar a bellísimas
personas con diversidad de discapacidades que me dejaron “experimentar” a través del
deporte adaptado, y convivir con geniales compañeras que me ayudaron a progresar
profesionalmente: gracias Lieke de Vries, Kate Goble, Maud Rubinstein, y especialmente
Rinske de Jong, me llevo el mejor de los recuerdos. De las prácticas en Noruega salté a la
investigación aplicada en Australia. Thousand thanks Hedda Giorgi (Brooks) for the time
spent together in Brisbane, for taking care of my in the distance, for your advices and your
example as a researcher, let’s toast for future trips and projects together. After all your
feedback this thesis is also yours. Gracias Coni Galleguillos y Eva Madrid por vuestra especial
amistad, hicisteis Nueva Zelanda mucho más hogareña, sin duda me ayudó a trabajar en la
tesis.
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PhD thesis
Muchas más personas me apoyaron de alguna manera o fueron fuente de inspiración,
durante el máster de EMMAPA, el máster del INEF o en Magisterio de EF, así como durante
las clases en la UCJC y en la ENE. Me faltan palabras en estos agradecimientos y temo
dejarme a alguien en el tintero (que no en el corazón). Gracias Pablo González, Antonio Cala,
Rafita Blanco, Raúl Reina, Jorge Couceiro, Lola Moreno, Mª Jesús Perea, Margarita Alcaide,
Juan Camilo, César Uribe, Marga Gual, Rossina Colista, Javi Argüelles, Johanna P, Rebecca
Deuble, Virginia Zamorano, cada uno pusisteis un granito de esta tesis de muy diversas
formas.
Una tesis no se puede llevar a cabo sin la comprensión y apoyo de los más cercanos. La
personalidad, los valores, las virtudes y vicios de cada investigador dan también carácter a
alguna pieza del puzle que es la tesis. Muchas de las características personales se forman a
base de conversaciones con amigos grandes que te hace crecer. Porque “el viaje más largo
es el que se hace hacia el interior de uno mismo”, gracias por todas las charlas y tiempo
compartido Javier Martín de Villa, Eugenio Amor, Roberto Sayalero, Ero Silva, os debo parte
de lo que soy. Gracias a los que quedándose en España y desde la distancia, me habéis
enviado cariño y mimos vía Skype: Ana Alonso, Magda Trzpis, Kike Cantos, Floren Cano. Si el
Judo me hizo luchadora, la escalada me enseña que la vida comienza fuera de tu zona de
confort. Sin duda tengo que agradecer a este deporte el darme la oportunidad de
enfrentarme a mis límites. Gracias a mis amigos escaladores que me han acompañado en mi
mejor y mi peor faceta, y por saber comprender que tenía que aparcar la roca un tiempo
para poder terminar la tesis, pronto volveremos a compartir y acumular buenos ratos: Félix,
Marta, Vari, Hilá, Edu, Raph, Gerar, Bea, Pablo, Nuria, Itzi, Elena, Carlos, Juanan, Eli, Jorge,
Nick, Ryan, Tania, y todos los forestales: Jorge, Cris, Eva, Sergio, Asun, Luisa, Ibone, Maribel,
Sara… Especialmente gracias a Fred, que pacientemente ha escuchado la presentación de la
tesis.
Mi fuente de inspiración, la razón de por qué sigo investigando en el mundo del deporte
adaptado, son los propios atletas. Gracias por todo lo que enseñáis al mundo: Urko
Carmona, Pipo, Paula de la Calle, Juan Antonio Bellido, Simone Salvagnin, Francesca
Porcellato, Gema Hassen-bey, Raphael Nishimura, Ronnie Dickson, Bethany Hamilton…
Dentro de este grupo de excelentes deportistas, no puedo olvidar al equipo Fundosa ONCE,
quienes me ofrecieron su tiempo y esfuerzo para realizar los tests del estudio del DEA.
Argentina: donde me llamó el amor. Allí me encerré analizando termogramas durante
meses. Mis suegros, Liliana y Raúl, no dudaron ofrecerme su casa y hacer más fácil mi
estancia para poder analizar los datos en el mejor ambiente posible. Gracias por vuestra
comprensión y paciencia, sobretodo este verano. Me llevo en mi maleta bonaerense un
montón de buenos aprendizajes con los chicos de la Casa Ceferino, a quienes la vida les
golpeó en la calle y ellos le devuelven alegría. Buenos Aires está para siempre asociada a
facturas con dulce de leche, mate entre boulders, infinitas horas de subte…, pero sobre todo
tiene cara de amistad: Negro, Pauli, Gastón, Lu, William, Mateico, Pablo, Nati, Mamo,
Nobile, Richard, Marisa… nos vemos pronto.
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Isabel Rossignoli 2015
Mi casa durante dos años y medio tiene nombre alemán, Bonn. Trabajando como
responsable de investigación en el Comité Paralímpico Internacional (IPC) aprendí lo que los
libros no muestran ni las clases enseñan. Si la tesis tuvo que ser aparcada temporalmente,
fue para participar en otras numerosas investigaciones dentro del movimiento paralímpico.
Lo mejor sin duda fue conocer y aprender de atletas paralímpicos, entrenadores,
clasificadores, investigadores y muy especialmente de los miembros del Classification
Committee del IPC. It is impossible to mention everybody, but I would like to particularly
express my gratitude to my collagues from the Medical & Scientific Department: Peter Van
de Vliet, Greg Vice, Cris Gomes, Julia Rauw, Vanessa Webb, Bee O Callaghan. Thanks for your
unconditional friendship Heike, living in Bonn would be much more complicated without
you, thanks for making the complex German bureaucracy a little bit more understandable
and for your blind faith in myself. Alba Roldán, o el comienzo de una gran amistad,
espontaneidad y humildad, trabajadora como nadie, te mereces de lo bueno lo mejor. Anna
Sagarra, siempre dispuesta a echar un cable, gracias por rescatarme la noche anterior a mi
boda. Jose Gigante, mil gracias por tu hospitalidad y calurosa acogida. Gracias María
Carballeira por cada conversación compartida que me hizo crecer como persona. The best of
traveling is that you meet amazing people. Many of them have supported this thesis in a
direct or indirect way. Sash Ramírez-Hughes, thanks for teaching me a bit of your crappy
English and for your corrections. Steph La Hoz Theuer, a quién admiro por tu inteligencia y
tus ganas incansables de aprender. Chitro Chaudhuri, you’ll always be the strongest Indian in
Germany, thanks for your constant smile. Thanks all for your friendship: Vasily Kuznetsov,
Christopher Reeder, Nathan, Moremi, Jessica, Li, Lana, Pishum, Tina, Simon, Ulla, Roman,
Rosario, Sven, Vivien, y Sana. Thanks for your support when I have difficulties to combine my
job with my PhD work.
Después de mucho trotar, llenando la maleta de experiencias inolvidables y aprendizajes
que han hecho posible que hoy pueda defender esta tesis, por fin vuelvo a casa, donde están
aquellos a los que más tengo que agradecer, mi familia que siempre me espera. Gracias a
mis hermanos, Tomás, Javier, Susana, Pablo y Alberto, y a mis padres, por estar a mi lado
incluso (y sobretodo) en la distancia, por creer y confiar en mí. Gracias mamá por ser tan
luchadora y por aceptar que estos pies inquietos siempre quisiesen viajar. Gracias papá, por
recodarme que las personas van antes que todo lo demás, por tu bondad y comprensión,
gracias por nunca cortar mis alas.
Guille mi roca, todo paciencia y dulzura, no hay palabras para agradecer todo lo que has
hecho por mí, y como no te gustan las palabras, te lo agradeceré dedicándote todo el
tiempo que esta tesis nos ha robado.
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Dr. PEDRO JOSÉ BENITO PEINADO
Profesor Titular de Universidad
Departamento de Salud y Rendimiento Humano
Facultad de Ciencias de la Actividad Física y del Deporte
Universidad Politécnica de Madrid
PEDRO JOSÉ BENITO PEINADO, PROFESOR TITULAR DE LA UNIVERSIDAD
POLITÉCNICA DE MADRID, FACULTAD DE CIENCIAS DE LA ACTIVIDAD FÍSICA Y
DEL DEPORTE
CERTIFICA:
Que la Tesis Doctoral titulada “Termografía infrarroja y dolor de hombro en
usuarios de sillas de ruedas. Infrared thermography and shoulder pain in
wheelchair users” que presenta Dña. ISABEL ROSSIGNOLI FERNÁNDEZ al
superior juicio del Tribunal que designe la Universidad Politécnica de Madrid, ha
sido realizada bajo mi dirección durante los años 2009-2015, siendo expresión
de la capacidad técnica e interpretativa de su autora en condiciones tan
aventajadas que le hacen merecedora del Título de Doctor con Mención
Internacional, siempre y cuando así lo considere el citado Tribunal.
Fdo. Pedro José Benito Peinado
En Madrid, a 5 de Octubre de 2015
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Dr. AZAEL JUAN HERRERO
Profesor Titular de Universidad
Laboratorio de Fisiología
Facultad de Ciencias de la Salud
Universidad Europea Miguel de Cervantes
AZAEL JUAN HERRERO, PROFESOR TITULAR DE LA UNIVERSIDAD EUROPEA
MIGUEL DE CERVANTES, FACULTAD DE CIENCIAS DE LA SALUD
CERTIFICA:
Que la Tesis Doctoral titulada “Termografía infrarroja y dolor de hombro en
usuarios de sillas de ruedas. Infrared thermography and shoulder pain in
wheelchair users” que presenta Dña. ISABEL ROSSIGNOLI FERNÁNDEZ al
superior juicio del Tribunal que designe la Universidad Politécnica de Madrid, ha
sido realizada bajo mi dirección durante los años 2009-2015, siendo expresión
de la capacidad técnica e interpretativa de su autora en condiciones tan
aventajadas que le hacen merecedora del Título de Doctor con Mención
Internacional, siempre y cuando así lo considere el citado Tribunal.
Fdo. Azael Juan Herrero
En Madrid, a 5 de Octubre de 2015
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TABLE OF CONTENTS
LIST OF TABLES .............................................................................................................. XIX
LIST OF FIGURES ............................................................................................................ XXI
LIST OF ABBREVIATIONS ......................................................................................... XXIII
LIST OF PUBLICATIONS .............................................................................................XXIV
RESUMEN ......................................................................................................................... XXV
ABSTRACT .................................................................................................................... XXVII
1 INTRODUCTION ............................................................................................................ 1
1.1 WHEELCHAIR USER’S SHOULDER ........................................................................................... 2
1.1.1 Shoulder joint mobility and scapular stability ........................................................... 2
1.1.2 Pathologies related to wheelchair propulsion ............................................................ 3
1.1.3 Prevalence of shoulder pain in wheelchair users ...................................................... 5
1.1.4 Etiology of shoulder pain in wheelchair users ........................................................... 7
1.1.4.1
1.1.4.2
1.1.4.3
Wheelchair ambulation ................................................................................................................. 7
Wheelchair transfers ................................................................................................................... 14
Musculoskeletal causes of shoulder pain and excessive load ................................... 15
1.2 TOOLS FOR SHOULDER PAIN EVALUATION .................................................................... 18
1.3 INFRARED THERMOGRAPHY ................................................................................................. 20
1.3.1 Concept and types ............................................................................................................... 20
1.3.2 Infrared thermography applications ........................................................................... 24
1.3.3 Factors influencing the application of infrared thermography in humans.. 30
1.3.3.1 Specific factors influencing the application of infrared thermography in people
with disabilities ................................................................................................................................................. 32
1.3.4 Technique and protocol .................................................................................................... 33
1.3.5 Corporal symmetry and infrared thermography.................................................... 36
1.4 THERMOREGULATION .............................................................................................................. 39
1.4.1 Thermoregulation and exercise ..................................................................................... 40
1.4.2 Thermoregulation in people with spinal cord injury during exercise ........... 42
1.5 PHYSICAL ACTIVITY IN WHEELCHAIR USERS ................................................................ 47
1.6 OUTLINE OF THE PRESENT THESIS .................................................................................... 50
2 OBJECTIVES ................................................................................................................. 53
2.1
2.2
2.3
STUDY 1............................................................................................................................................ 53
STUDY 2............................................................................................................................................ 53
STUDY 3............................................................................................................................................ 53
3 MATERIAL AND METHODS .................................................................................... 54
3.1 STUDY DESIGN .............................................................................................................................. 54
3.2 SAMPLE ............................................................................................................................................ 54
3.2.1 Ethics norms followed in this study ............................................................................. 55
3.2.2 Inclusion and exclusion criteria ..................................................................................... 56
3.2.3 Demographic data of the studies 1 and 2................................................................... 56
3.2.4 Demographic data of the study 3 .................................................................................. 57
3.3 EQUIPMENT ................................................................................................................................... 57
3.3.1 Material for the thermographic evaluation............................................................... 57
3.3.2 Material for the shoulder pain evaluation ................................................................. 58
3.3.3 Material for the register of the kinematic variables .............................................. 59
3.4 RESEARCH PERSONNEL ............................................................................................................ 61
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3.5 PROCEDURES ................................................................................................................................. 62
3.5.1 Study 1: Infrared Thermal Imaging .............................................................................. 62
3.5.2 Study 2: Infrared Thermal Imaging and The Wheelchair User Shoulder Pain
Index…….. ................................................................................................................................................ 65
3.5.3 Study 3: Infrared Thermal Imaging, The Wheelchair User Shoulder Pain
Index and the wheelchair propulsion test T-CIDIF ............................................................... 66
3.6 VARIABLES ..................................................................................................................................... 68
3.7 STATISTICAL ANALYSIS ............................................................................................................ 69
3.7.1 Study 1 ...................................................................................................................................... 69
3.7.2 Study 2 ...................................................................................................................................... 69
3.7.3 Study 3 ...................................................................................................................................... 70
4 RESULTS ....................................................................................................................... 71
4.1 STUDY 1: Reliability of infrared thermography in skin temperature evaluation
of wheelchair users.................................................................................................................................. 71
4.1.1 Reliability of measurements ........................................................................................... 71
4.2 STUDY 2: Relationship between perceived shoulder pain and infrared
thermography in wheelchair athletes and nonathletes ........................................................... 76
4.2.1 Comparison of thermography values in nonathletic and athletic subjects . 76
4.2.2 Comparison of shoulder pain in athletic and nonathletic subjects ................. 80
4.2.3 Relationship between thermography and shoulder pain ................................... 80
4.3 STUDY 3: Relationship between shoulder pain and skin temperature measured
by infrared thermography in a wheelchair propulsion test ................................................... 81
5 DISCUSSION ................................................................................................................. 88
5.1 STUDY 1: Reliability of infrared thermography in skin temperature evaluation
of wheelchair users.................................................................................................................................. 88
5.2 STUDY 2: Relationship between perceived shoulder pain and infrared
thermography in wheelchair athletes and nonathletes ........................................................... 92
5.3 STUDY 3: Relationship between shoulder pain and skin temperature measured
by infrared thermography in a wheelchair propulsion test ................................................. 100
6 CONCLUSIONS ...........................................................................................................105
6.1
6.2
6.3
Conclusions study 1................................................................................................................... 105
Conclusions study 2................................................................................................................... 105
Conclusions study 3................................................................................................................... 106
7 LIMITATIONS ............................................................................................................108
8 FUTURE RESEARCH LINES....................................................................................111
9 REFERENCES .............................................................................................................113
10 APPENDIXES .............................................................................................................146
10.1
10.2
10.3
10.4
10.5
APPENDIX 1. Example of informed consent form ...................................................... 146
APPENDIX 2. Example of thermographic report ........................................................ 148
APPENDIX 4. Data collection information sheet for the subjects ........................ 150
APPENDIX 4. WUSPI test in English................................................................................. 152
APPENDIX 5. WUSPI test in Spanish................................................................................ 153
11 SUMMARIZED CV / CURRICULUM VITAE ABREVIADO ...............................155
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LIST OF TABLES
Table 1. Prevalence of current SP and SP since wheelchair ambulation ................... 6
Table 2. Number of subjects per group ................................................................................. 55
Table 3. Group subject characteristics from studies 1 and 2 expressed by
mean±Standard Deviation............................................................................................................ 56
Table 4. General characteristics of the weather station, model BAR-908-HG®
(Oregon Scientific, Portland, Oregon) ..................................................................................... 58
Table 5. Rolling resistance to overcome depending on the subject's mass ........... 61
Table 6. Variables and their values ......................................................................................... 68
Table 7. Descriptive maximum values of the skin temperature profile on day 1,
day 2 and between both the assessments of the analyzed area .................................. 72
Table 8. Descriptive average values of the temperature profile on day 1, day 2
and between both the assessments for each analyzed area .......................................... 74
Table 9. Interrater-reliability measures in terms of ICC and CV organized by
general areas ...................................................................................................................................... 75
Table 10. Mean maximal values of regional skin temperature °C (±) standard
deviations and absolute values of the side-to-side differences (ΔTsk) for the
different skin areas of the study subjects. Results of Student’s t-test for the two
measures .............................................................................................................................................. 75
Table 11. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the maximum basal values registered in ROIs. It is
showed the values of each body side (right vs. left) for each ROI .............................. 76
Table 12. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the average basal values registered in the ROI. It is
showed the values of each body side (right vs. left) for each ROI .............................. 77
Table 13. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the side-to-side differences (ΔTsk) of maximum values
between bilateral body areas in nonathletic and athletic subjects ............................ 79
Table 14. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the side-to-side differences (ΔTsk) of average values
between bilateral body areas in nonathletic and athletic subjects ............................ 79
Table 15. Descriptive values of the skin temperature (°C) of 22 ROIs in
wheelchair athletes; repeated measures ANOVA correlation ...................................... 82
Table 16. Descriptive values of the side-to side differences (°C) of the 26
measured ROIs in wheelchair athletes; repeated measures ANOVA correlation 83
Table 17. Spearman Rho correlations between bilateral ΔTsk and shoulder
pain…. .................................................................................................................................................... 84
Table 18. Descriptive values of the kinematic variables; Spearman Rho
correlations between kinematic variables and shoulder pain ..................................... 86
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Isabel Rossignoli 2015
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PhD thesis
LIST OF FIGURES
Figure 1. Shoulder anatomy. From Morphopedics (272) ................................................. 3
Figure 2. Supraspinatus tendon rupture (left) and supraspinatus impingement
and rotator cuff tendonitis (right). Adapted from ePainAssist (106) .......................... 4
Figure 3. Wheelchair propulsion technique parameters. The dots represent the
trayectory of the hand. EA = end angle (°); HC = hand contact; HR = hand release;
PA = push angle; SA = start angle. From Vanlandewijck et al. (422) ............................ 8
Figure 4. Mean muscle forces (only forces larger than 10 N) during the push
phase (left) and recovery phase (right). From Veeger et al. (427) ................................ 9
Figure 5. The relationship between force direction and calculated net joint
torques around shoulder and elbow. From Veeger et al. (432). .................................. 13
Figure 6. Sliding board (left) and sitting pivot transfer (right) for individuals
with spinal cord injury. From Gagnon (129) ....................................................................... 14
Figure 7. The first medical thermographic device developed by Schwamm and
Reeh in 1952, from Berz et al. (39) (above), and a modern high resolution
thermographic camera VarioCAM®, from Jenoptik (193) (below) ........................... 22
Figure 8. Thermogram of a patient with allergic rhinitis detected with an early
IRT camera, from Georgevici (136) (left), and a thermogram of a patient with
hypothyroidism and inflamed carotid artery detected with a modern IRT camera,
from Möhrke (271) (right) ........................................................................................................... 23
Figure 9. Thermograms with TotalVision™ Anatomy Software. From Möhrke
(271) ...................................................................................................................................................... 23
Figure 10. Classification of IRT-related factors in humans by Fernández (113) 30
Figure 11. Physiologic thermoregulation in humans. A, Increases in internal
and/or skin temperatures are identified by the preoptic/anterior hypothalamus
(PO/AH) and result in increased heat dissipation via cutaneous vasodilation and
sweating, which then corrects an increase in temperature. B, Decreased skin or
internal temperature causes reflex decreases in heat dissipation (cutaneous
vasoconstriction) and increased heat generation (through shivering) to correct a
decrease in temperature. CNS = central nervous system. From Charkoudian
(60)… ..................................................................................................................................................... 40
Figure 12. Thigh, Calf, Forearm, and Upper Arm skin temperatures for ablebodied (AB), paraplegic (PA), and tetraplegic (TP) athletes during prolonged
exercise and recovery in warm conditions. From Price (317) ..................................... 46
Figure 13. IRT camera T335 (FLIR® Systems, Sweden) ............................................... 57
Figure 14. Elite wheelchair athlete ready to perform the wheelchair propulsion
test (T-CIDIF) ..................................................................................................................................... 60
Figure 15. T-CIDIF. Left: detail of the linear position transducers integrated with
the fitness pulley. Right: detail of the gloves fixed to the forearm. ............................ 61
Figure 16. Thermographic analysis of an athlete (left) and a nonathlete (right)62
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Isabel Rossignoli 2015
Figure 17. A total of 16 areas on the front body were studied in the study 1.
Example from a wheelchair athlete ......................................................................................... 63
Figure 18. A total of 20 areas on the rear body were studied in the study 1.
Example from a wheelchair athlete ......................................................................................... 64
Figure 19. Measurements of the study 3. Pre-test, thermographic evaluation
before the wheelchair exercise test; Post-test, thermographic evaluation one
minute after completing the wheelchair exercise test; Post-10, thermographic
evaluation ten minutes after completing the wheelchair exercise test .................... 67
Figure 20. Day-to-day analysis of the reliability in all body areas measured ...... 73
Figure 21. Mean and standard deviation of the average and maximum basal skin
temperature (Tsk) values .............................................................................................................. 78
Figure 22. Mean and standard deviation of the average and maximum basal
side-to-side skin temperature (ΔTsk) values ........................................................................ 78
Figure 23. Manual drawing of the regions of interest ................................................. 108
Figure 24. The impact of different backrest on the thermal image. Backrest size
is dependent upon the impairment of the subject .......................................................... 110
XXII
PhD thesis
LIST OF ABBREVIATIONS
BMI
Body Mass Index
CRT
Circuit resistance-training
CV
Coefficient of Variation
FES
Functional electrical stimulation
ICC
Interclass Correlation Coefficient
IRT
Infrared Thermography
°C
Degrees Celsius
Pre-test
Thermographic evaluation before the wheelchair
exercise test
Post-test
Thermographic evaluation one minute after
completing the wheelchair exercise test
Post-10
Thermographic evaluation ten minutes after
completing the wheelchair exercise test
ROI
Region of Interest
SCI
Spinal Cord Injury
SD
Standard Deviation
SP
Shoulder pain
Tsk
Skin Temperature
WCUs
Wheelchair Users
WUSPI
Wheelchair Users Shoulder Pain Index
∆Tsk
Side-to-side skin temperature difference
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Isabel Rossignoli 2015
LIST OF PUBLICATIONS
The content of this thesis is included in the following articles:
I - Rossignoli I, Benito PJ, Herrero AJ. Reliability of infrared thermography in skin
temperature evaluation of wheelchair users. Spinal Cord. 2014;53:243-8.
II - Rossignoli I, Herrero AJ, Menéndez H, Sillero M, Benito PJ. Relationship
between perceived shoulder pain and infrared thermography in wheelchair
athletes and nonathletes. Disability and Health Journal. (Submitted)
III - Rossignoli I, Fernández-Cuevas I, Benito PJ, Herrero AJ. Relationship
between shoulder pain and skin temperature measured by infrared
thermography in a wheelchair propulsion test. Infrared Physics and Technology.
(Submitted)
XXIV
PhD thesis
RESUMEN
Las personas que usan la silla de ruedas como su forma de movilidad prioritaria
presentan una elevada incidencia (73%) de dolor de hombro debido al sobreuso
y al movimiento repetitivo de la propulsión. Existen numerosos métodos de
diagnóstico para la detección de las patologías del hombro, sin embargo la
literatura reclama la necesidad de un test no invasivo y fiable, y sugiere la
termografía como una técnica adecuada para evaluar el dolor articular. La
termografía infrarroja (IRT) proporciona información acerca de los procesos
fisiológicos a través del estudio de las distribuciones de la temperatura de la piel.
Debido a la alta correlación entre ambos lados corporales, las asimetrías
térmicas entre flancos contralaterales son una buena indicación de patologías o
disfunciones físicas subyacentes. La fiabilidad de la IRT ha sido estudiada con
anterioridad en sujetos sanos, pero nunca en usuarios de sillas de ruedas. Las
características especiales de la población con discapacidad (problemas de
sudoración y termorregulación, distribución sanguínea o medicación), hacen
necesario estudiar los factores que afectan a la aplicación de la IRT en usuarios
de sillas de ruedas.
La bibliografía discrepa en cuanto a los beneficios o daños resultantes de la
práctica de la actividad física en las lesiones de hombro por sobreuso en usuarios
de sillas de ruedas. Recientes resultados apuntan a un aumento del riesgo de
rotura del manguito rotador en personas con paraplejia que practican deportes
con elevación del brazo por encima de la cabeza. Debido a esta falta de acuerdo
en la literatura, surge la necesidad de analizar el perfil termográfico en usuarios
de sillas de ruedas sedentarios y deportistas y su relación con el dolor de
hombro. Hasta la fecha sólo se han publicado estudios termográficos durante el
ejercicio en sujetos sanos. Un mayor entendimiento de la respuesta termográfica
al ejercicio en silla de ruedas en relación al dolor de hombro clarificará su
aparición y desarrollo y permitirá una apropiada intervención.
El primer estudio demuestra que la fiabilidad de la IRT en usuarios de sillas de
ruedas varía dependiendo de las zonas analizadas, y corrobora que la IRT es una
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Isabel Rossignoli 2015
técnica no invasiva, de no contacto, que permite medir la temperatura de la piel,
y con la cual avanzar en la investigación en usuarios de sillas de ruedas.
El segundo estudio proporciona un perfil de temperatura para usuarios de sillas
de ruedas. Los sujetos no deportistas presentaron mayores asimetrías entre
lados corporales que los sedentarios, y ambos obtuvieron superiores asimetrías
que los sujetos sin discapacidad reportados en la literatura. Los no deportistas
también presentaron resultados más elevados en el cuestionario de dolor de
hombro. El área con mayores asimetrías térmicas fue hombro. En deportistas,
algunas regiones de interés (ROIs) se relacionaron con el dolor de hombro. Estos
resultados ayudan a entender el mapa térmico en usuarios de sillas de ruedas.
El último estudio referente a la evaluación de la temperatura de la piel en
usuarios de sillas de ruedas en ejercicio, reportó diferencias significativas entre
la temperatura de la piel antes del test y 10 minutos después del test de
propulsión de silla de ruedas, en 12 ROIs; y entre el post-test y 10 minutos
después del test en la mayoría de las ROIs. Estas diferencias se vieron atenuadas
cuando se compararon las asimetrías antes y después del test. La temperatura de
la piel tendió a disminuir inmediatamente después completar el ejercicio, e
incrementar significativamente 10 minutos después. El análisis de las asimetrías
vs dolor de hombro reveló relaciones significativas negativas en 5 de las 26 ROIs.
No se encontraron correlaciones significativas entre las variables de propulsión
y el cuestionario de dolor de hombro. Todas las variables cinemáticas
correlacionaron significativamente con las asimetrías en múltiples ROIs. Estos
resultados indican que los deportistas en sillas de ruedas exhiben una capacidad
similar de producir calor que los deportistas sin discapacidad; no obstante, su
patrón térmico es más característico de ejercicios prolongados que de esfuerzos
breves. Este trabajo contribuye al conocimiento de la termorregulación en
usuarios de sillas de ruedas durante el ejercicio, y aporta información relevante
para programas deportivos y de rehabilitación.
Palabras clave: extremidad superior; deportistas; discapacidad; temperatura de
la piel; dolor de hombro; deporte; termografía infrarroja.
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PhD thesis
ABSTRACT
Individuals who use wheelchairs as their main means of mobility have a high
incidence (73%) of shoulder pain (SP) owing to overuse and repetitive
propulsion movement. There are numerous diagnostic methods for the detection
of shoulder pathologies, however the literature claims that a noninvasive
accurate test to properly assess shoulder pain would be necessary, and suggests
thermography as a suitable technique for joint pain evaluation. Infrared
thermography (IRT) provides information about physiological processes by
studying the skin temperature (Tsk) distributions. Due to the high correlation of
skin temperature between both sides of the body, thermal asymmetries between
contralateral flanks are an indicator of underlying pathologies or physical
dysfunctions.
The reliability of infrared thermography has been studied in healthy subjects but
there are no studies that have analyzed the reliability of IRT in wheelchair users
(WCUs). The special characteristics of people with disabilities (sweating and
thermoregulation problems, or blood distribution) make it necessary to study
the factors affecting the application of IRT in WCUs.
Discrepant reports exist on the benefits of, or damage resulting from, physical
exercise and the relationship to shoulder overuse injuries in WCUs. Recent
findings have found that overhead sports increase the risk of rotator cuff tears in
wheelchair patients with paraplegia. Since there is no agreement in the
literature, the thermographic profile of wheelchair athletes and nonathletes and
its relation with shoulder pain should also be analysed. Infrared thermographic
studies during exercise have been carried out only with able-bodied population
at present. The understanding of the thermographic response to wheelchair
exercise in relation to shoulder pain will offer an insight into the development of
shoulder pain, which is necessary for appropriate interventions.
The first study presented in this thesis demonstrates that the reliability of IRT in
WCUs varies depending on the areas of the body that are analyzed. Moreover, it
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corroborates that IRT is a noninvasive and noncontact technique that allows the
measurement of Tsk, which will allow for advances to be made in research
concerned with WCUs.
The second study provides a thermal profile of WCUs. Nonathletic subjects
presented higher side-to-side skin temperature differences (ΔTsk) than athletes,
and both had greater ΔTsk than the able-bodied results that have been published
in the literature. Nonathletes also revealed larger Wheelchair Users Shoulder Pain
Index (WUSPI) score than athletes. The shoulder region of interest (ROI) was the
area with the highest ΔTsk of the regions measured. The analysis of the athletes’
Tsk showed that some ROIs are related to shoulder pain. These findings help to
understand the thermal map in WCUs.
Finally, the third study evaluated the thermal response of WCUs in exercise.
There were significant differences in Tsk between the pre-test and the post-10
min in 12 ROIs, and between the post-test and the post-10 in most of the ROIs.
These differences were attenuated when the ΔTsk was compared before and after
exercise. Skin temperature tended to initially decrease immediately after the
test, followed by a significant increase at 10 minutes after completing the
exercise. The ΔTsk versus shoulder pain analysis yielded significant inverse
relationships in 5 of the 26 ROIs. No significant correlations between propulsion
variables and the results of the WUSPI questionnaire were found. All kinematic
variables were significantly correlated with the temperature asymmetries in
multiple ROIs. These results present indications that high performance
wheelchair athletes exhibit similar capacity of heat production to able-bodied
population; however, they presented a thermal pattern more characteristic of a
prolonged exercise rather than brief exercise. This work contributes to improve
the understanding about temperature changes in wheelchair athletes during
exercise and provides implications to the sports and rehabilitation programs.
Key words: upper extremity; athletes; disability; skin temperature; shoulder
pain; exercise; sports; infrared thermography.
XXVIII
Introduction
1 INTRODUCTION
After London 2012, best Paralympic Games hitherto (187), adaptive sports and
attitudes towards people with impairment around the world changed forever.
Famous para-athletes are starring in multiple leading brand advertisements, and
wheelchair rugby chairs or running blades are seen merely as another type of
sports equipment. This proliferation of media commercials and mainstream
acceptance has meant a development in para-sports at all levels. Some
consequences have been an increase in para-sports participation by people with
disabilities, an improvement in accessibility, the diversification of sporting
disciplines and an increase in the number of scientific studies related to parasports.
The shift to a more active lifestyle for people with disabilities should imply an
enhancement of the quality of life (18, 98, 395), since exercise prevents other
secondary impairments (loss of cardiorespiratory, and muscular function,
metabolic alterations and systemic dysfunctions) and diminishes loss of mobility,
physical dependence and poor social integration (288). Nonetheless, the
particularities of some impairments can lead to overload injuries. More
concretely, upper extremity injuries are a limiting factor for the mobility and
independence of wheelchair users (WCUs). The repetitive and continuous
movement of wheelchair propulsion, added to the mechanical strain of lifting
tasks and transfers, compromise the upper body musculoskeletal system of this
population. Moroever, wheelchair-confinement forces WCUs to sedentarism – a
well-known metabolic risk factor, and while increasing the physical capacity
seems particularly necessary for WCUs, physical activity for this population is
inherently related to upper-body work. Thus, physical activity for WCUs will
likely further contribute to complications in the upper extremities. There is no
agreement in the literature about whether the exercise implies an additional
overload on the already burdened upper body or, on the contrary, trained joints
will be well protected with developed musculature.
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Isabel Rossignoli 2015
In the following review of the literature, an overview will be given of the
wheelchair ambulation implications on shoulder problems in WCUs. The most
commonly used tools for shoulder evaluation will then be introduced, with
special focus on the non-contact infrared thermography technique. Furthermore,
the specific characteristics of the thermoregulation of people with spinal cord
injury (SCI) will be described.
1.1 WHEELCHAIR USER’S SHOULDER
1.1.1 Shoulder joint mobility and scapular stability
The complex structure, limited muscle mass and wide movement possibilities of
the shoulder make for a joint that has a propensity to overuse injuries (32). The
tendons of the rotator cuff muscles (supraspinatus, subscapularis, infraspinatus,
and teres minor) are primarily responsible for glenohumeral joint stabilization
(41, 142), and together with the deltoid and long head of the biceps brachii
muscles, are the stabilizing components of the shoulder (Figure 1). External
rotators also decelerate the arm during various activities through eccentric
contraction (12). Since the shoulder’s mobility relies on its stability, this joint is
particularly exposed to the development of muscle imbalances (142). Individuals
who use wheelchairs as their main means of mobility have a high incidence of
shoulder pain due to the overuse of the shoulder stabilizing and the repetitive
propulsion movement (32).
2
Introduction
Figure 1. Shoulder anatomy. From Morphopedics (272)
1.1.2 Pathologies related to wheelchair propulsion
Nichols et al. assigned the name ‘wheelchair user’s shoulder’ to the shoulder
problems experienced by individuals who utilize manual wheelchairs for their
primary means of locomotion (284). In a study of 94 paraplegic individuals, a
third presented with shoulder pain, a condition that Nichols et al. designated ‘the
weight-bearing shoulder’ (32). Both names make reference to the same problem
in this joint, which is designed, in evolutionary terms, for mobility and not for
loading.
During the propulsive phase of the wheelchair propulsion, the active muscles
(internal shoulder rotators, adductors and flexors (275)) become stronger, while
muscles involved in the recovery phase remain at the same strength (12). With
years of wheelchair propulsion, this leads to an imbalance in the shoulder
muscles, characterized by stronger internal rotators than external rotators and
weaker shoulder adductor muscles (12, 53). It is the internal-external rotators
strength ratio that is primarily considered indicative of shoulder instability and
impingement (12).
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Isabel Rossignoli 2015
Many movements for WCUs occur at or above shoulder height, strengthening
shoulder abductors and flexors. This imbalance heightens the risk of
supraspinatus tendon impingement (because abductors pull the humeral head
upward within the glenoid cavity and into the subacromial space), which leads to
the development of inflammation and pain, and may prompt rotator cuff tears
(142) (Figure 2). Supraspinatus impingement syndrome with subacromial
bursitis is the most common cause (74%) of shoulder pain in this population (32,
303, 367). The soft tissues involved can suffer other disorders such as rotator
cuff tendinitis and tears (32, 108), supraspinatus tendinitis (100), bicipital
tendinitis (134, 366), myalgias and myofascial pain syndromes (100),
subacromial bursitis (32, 366), adhesive capsulitis (366), instability (100),
undiagnosed upper limb fractures (100), osteonecrosis of the humeral head,
osteolysis of the distal clavicle (100), osteoporosis and osteoarthritis of the
acromioclavicular and glenohumeral joints (366), and acromioclavicular joint
space narrowing and calcifications (30). Nerve entrapment causing median
nerve dysfunction at the carpal tunnel and ulnar neuropathy were the most
common entrapment of the wrist and forearm segments (55, 134). Degenerative
arthritis resulting from overuse injuries is less common, but has been also
reported in the literature, for example osteonecrosis of the head of the humerus
(31, 32) and glenohumeral joint degeneration (450).
Figure 2. Supraspinatus tendon rupture (left) and supraspinatus impingement
and rotator cuff tendonitis (right). Adapted from ePainAssist (106)
4
Introduction
1.1.3 Prevalence of shoulder pain in wheelchair users
The prevalence of shoulder pain in wheelchair users (WCUs) has been reported
to be from 26% to 71.2% in those who currently experiences shoulder pain and
from 30% to 85% in those who have experienced shoulder pain since becoming
a WCU (7, 30, 32, 50, 53, 80, 100, 120, 225, 284, 346, 366). The heterogeneity of
age, duration of injury, neurologic level and severity of injury among the
participants involved in these studies explain the wide variability in the
prevalence of current and previous shoulder pain (100). Shoulder pain entails
functional loss and a reduction in mobility, quality of life and social participation
(100, 154, 210).
Nichols et al. reported shoulder pain in 51.4% of 517 individuals with spinal
cord injury (SCI) (284), while Bayley et al. reported 31% of 94 individuals in a
more recent study (32). This percentage of upper extremity pain increased to
55% and 64% for a sample of individuals with tetraplegia and paraplegia,
respectively (366). From 451 interviewed individuals with SCI, Subbarao et al.
found that 68% suffered shoulder pain or wrist pain (389). A later review of the
literature reported a range of 30-73% of shoulder pain (100). An extension of
this review revealed a similar range with 26-71.2% reporting shoulder pain at
the present time, and 30-85% reported experiencing shoulder pain since
beginning to use the wheelchair (Table 1).
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Isabel Rossignoli 2015
Table 1. Prevalence of current SP and SP since wheelchair ambulation
Year Author
1979 Nichols
Current SP (%)
51.4
SP since WCUs (%)
51.4 (idem)
1987 Bayley
30.8
32.9
1988 Gellman
1988 Wylie
36.36
a) 34.5, b) 67.8
a) SP, b) UE
a) 18, b) 45
a) Athletes
b) Nonathletes
Women
1991 Pentland
73
1991 Waring
75 TP
1991 Silfverskiold
a) 78 TP, 35 PP
b) 33 TP, 35 PP
a) 55 TP, 64 PP
b) 46 TP, 36 PP
1992 Sie
1993 Burnham
26 PP
1994 Pentland
39 PP
1995 Subbarao
a) 35.6, b) 57.8
1996 Campbell
Notes
a) 6 months after SCI
b) 18 months after SCI
a) UE, b) SP
Athletes
58 PP
a) 11, b) 13
a) Only SP
b) SP and wrist pain
All sample with SP
a) Acute SP
b) Chronic SP
1997 Escobedo
69.56 PP
1999 Curtis
59 TP, 42 PP
78 TP, 59 PP
1999 Curtis
52
72
Female athletes
1999 Curtis
75
Female and male
1999 Dalyan
a) 32
b) 76 (31.57, 68.42)
a) SP
b) UE (athletes,
nonathletes)
2000 Ballinger
30
2001 Boninger
32 PP
36
2001 Russell
47
72
2003 Salisbury
a) 54, b) 85, c) 54 TP
2003 Fullerton
48, a) 66, b) 39
2004 Finley
29
2004 Samuelsson
a) SP before rehab
b) During rehab
c) After rehab
a) Nonathletes
b) Athletes
61.55
37.5
2008 Alm
40
2008 Brose
67
2010 Jain
67
24.5 untreated SP
35.4
2010 Akbar
67
2011 Akbar
71.2
Note: SP, shoulder pain; UE, upper extremity; TP, tetraplegic; PP, paraplegic.
6
Introduction
Shoulder pain has been reported to be higher in people with tetraplegia than
paraplegia (80, 107, 313, 346, 347), greater in higher levels of paraplegia
compared to lower SCI levels (372), and higher in women than in men (100, 154,
159, 191, 302), despite similar levels of physical activity between women and
men (154). There exists controversy in the literature regarding the incidence of
shoulder pain in inactive compared to active wheelchair users, which will be
discussed in section 1.5. Interestingly, Fullerton et al. argued that there are more
sedentary individuals with tetraplegia than paraplegia, because the tetraplegic
group tends to avoid physical activity due to shoulder pain and they have fewer
sporting opportunities (128).
The normal process of aging may accelerate the degeneration of the shoulder
joint and aggravate the pain (11, 191). In addition to age, other factors that
correlate with shoulder pain include time since injury (134, 191, 284), years or
hours per week of wheelchair usage (80), and body mass index (BMI) (47, 100).
In contrast to most studies, Subbarao et al. did not find statistical significances by
age, neurologic level or time since injury (389).
1.1.4 Etiology of shoulder pain in wheelchair users
Woude et al. highlighted propulsion technique, transfers, wheelchair design and
excessive load as the main causes of shoulder injuries in wheelchair ambulation,
and pointed to training protocols and wheelchair design as the preventive
measures on which to focus (414). Ambrosio et al. recommended that clinicians
implement two types of rehabilitation strategies: 1) stretching and strengthening
shoulder muscles to maintain the glenohumeral alignment and to augment the
resistance to fatigue of the shoulder; and 2) teaching proper wheelchair
propulsion techniques (12) such as the one described in the following section.
1.1.4.1 Wheelchair ambulation
There are two wheelchair propulsion phases (Figure 3): the push and the
recovery. The muscles acting during the push phase are the anterior deltoid,
pectoralis major, supraspinatus, infraspinatus, subscapularis, serratus anterior,
7
Isabel Rossignoli 2015
lower trapezius, rhomboid major and long head of biceps brachii (276) (Figure
4). For tetraplegic individuals, some of these muscles may have a slightly delayed
onset or may have greater recruitment than in paraplegics. The muscles involved
in the recovery include the middle and posterior deltoid, supraspinatus, upper
and middle trapezius and subscapularis (276).
Figure 3. Wheelchair propulsion technique parameters. The dots represent the
trayectory of the hand. EA = end angle (°); HC = hand contact; HR = hand release;
PA = push angle; SA = start angle. From Vanlandewijck et al. (422)
It is interesting to note that supraspinatus is active in both the push and
recovery phases. Moreover, subscapularis is employed by paraplegics during
recovery, but is actually utilised for the push phase in WCUs with tetraplegia, and
while tetraplegics use latissimus dorsi for push work, its activation in the push
and recovery phases is inconsistent in paraplegics. Finally, the activity of the
infraspinatus is lower in WCUs with tetraplegia than paraplegia (276). Mulroy et
al. (275) indicated that the muscles most vulnerable to fatigue in paraplegics
were pectoralis major, supraspinatus and the recovery muscles, and that the
push phase is the most intense period of muscle activity.
8
Introduction
Figure 4. Mean muscle forces (only forces larger than 10 N) during the push phase
(left) and recovery phase (right). From Veeger et al. (427)
The repetitive and continuous activity of wheelchair ambulation is the main
stressor that leads to the development of activity-related musculoskeletal
problems in WCUs. The fact that wheelchair propulsion leads to upper-body
musculoskeletal disorders necessitates an ergonomic and integrative approach
to all of the components involved in this task (414, 431). There are three factors
that play an important role in the efficiency of wheelchair propulsion: the
wheelchair design, the wheelchair user and the wheelchair-user interaction.
Wheelchair design
There has been an evolution of the hand-rim wheelchairs from chromium-plated
wheelchairs used in the sixties to the high-tech, task-specific and self-tuned
wheelchairs of the present day. This progression reflects improvements in the
durability and safety of the wheelchairs and health of the WCUs. The rolling
resistance, air drag, and internal friction of the wheelchair (416, 418), its weight
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Isabel Rossignoli 2015
(47, 414), the rear wheel position (349), the effect of camber (249), the seat
position and angle (139, 220, 349, 373), the rim radius or gear ratio (121, 416)
and the material and deformation of the frame are some of the mechanical
components that must be considered for improving wheelchair ergonomics and
attaining the best wheeling conditions, and thus avoiding shoulder pain in WCUs.
For example, changes in seat position or handrim diameter will have an effect on
the elbow angle, subsequently impacting the constrained movement of the arms
during the push phase (428). A higher seat position is associated with upperextremity pathologies (250), and handrim size is recommended depending on
the functional capacity and preferences of the users (430).
Wheelchair weight, rear wheel location and wheelchair width were designed
prior to the 1980s in such a way that individuals had to push using a pattern of
shoulder abduction, internal rotation and extension. Additionally, wheelchair
seats that were parallel to the floor with tall backrests forced a spinal flexion
posture with forward head and shoulder positions (158). Configuration has
changed over the years resulting in different propulsion techniques, and people
using old wheelchair designs have been shown to present better shoulder pain
scores 15 years after injury due to changes in configuration (158).
Wheelchair user
Factors associated with the user including overweight (43, 47), duration of
disability (55) and time spent in the wheelchair per week (55) contribute to the
incidence of upper-extremity injuries in WCUs. Furthermore, the physical work
capacity, training status and propulsion technique should be addressed (414) in
order to achieve the optimal functioning of the musculoskeletal system. Strength
training should be specific for manual wheelchair propulsion, but shoulder
strength itself does not guarantee an improvement of the wheelchair ambulation
(12). A study of the electromyographic activity of shoulder muscles during
wheelchair propulsion recommended endurance training to prevent the fatigue
of the pectoralis major, supraspinatus and muscles involved in the recovery
phase (275). Fatigue in these muscles has been associated with a shift in joint
power from the shoulder to the elbow and wrist (339), increasing the risk of
10
Introduction
overload injuries in these distal joints. Therefore, the implications for joint injury
could be different for endurance-trained WCUs.
The alignment of the trunk and its stabilization are important factors for
shoulder function (456) and can be achieved through changes in the wheelchair
configuration. Hastings et al. highlighted postural alignment as a good
prevention of shoulder pain based on the authors’ experience. An optimal
balance must be found between stabilization possible mobility, as usually one
works to the detriment of the other. A more stable posture, such as one that
includes a posterior pelvic tilt and flexed spine, for example, will not allow great
mobility (158). In individuals with paraplegia, the absence of innervated trunk
musculature means that the external support system (the wheelchair) together
with the forces of gravity dictate the posture of the trunk (158). It has been
shown that in individuals with a SCI without trunk control presented a higher
intensity of shoulder pain than in those with trunk control (456), because of an
increased biomechanical stress on the upper limbs, which are also required for
stabilization to avoid falling and also collapsing into a “C” spinal sitting posture
(158).
In people with tetraplegia, the shoulder is not fully innervated, which
accentuates the shoulder muscle imbalance. For example, people with a C6 level
SCI have innervated rotator cuff muscles, rhomboids and deltoid, but pectorals
major and dorsal are not fully innervated resulting in a shoulder muscle
imbalance (158). In addition, tetraplegics are not able to properly grip with their
hands, so they must provide an extra-internal rotation force to provide some
friction on the wheel to move it. A lack of sternal pectoralis major innervation
precipitates an increase of the use of humeral depressors to reduce the risk of
impingement in the shoulder, and the anterior deltoid and serratus anterior
must perform additional work to compensate the smaller clavicular pectoralis
major in high SCI (276). A reliance on smaller or weaker muscles for shoulder
movements typically achieved (in able-bodied persons) by muscles that do not
receive full innervation in people with SCI can lead to shoulder injuries.
11
Isabel Rossignoli 2015
Generally, the higher the level of injury the higher the prevalence of shoulder
disorders (372).
The wheelchair-user interaction
The most effective propulsion technique involves pushing on the wheel with a
greater push angle and spending a longer period of time on the pushrim,
allowing for a decreased pushing cadence (12, 46). It is important to reduce the
cadence since increased movement repetition is related to an increased
predisposition for median nerve injury (43). The hand is held below the pushrim
during the recovery phase of the propulsion stroke. This technique is called the
semicircular pattern. The literature recommends that WCUs are trained to let
their hand drift down naturally when letting go of the pushrim to achieve the
semicircular motion (46). Sport propulsion techniques, such as the butterfly
technique (64, 148, 423), have rarely been the subject of scientific studies, and
bilateral symmetry during wheelchair propulsion has been identified as another
important aspect that requires further research (148, 183, 377).
Finally, the appropriate wheelchair-user interface determines the efficiency of
power transfer from the user to the wheelchair. This interaction depends on the
combined adjustment of movement pattern of the arm and trunk, timing
parameters (such as number of pushes, duration of the hand-to-rim contact,
push range or angle, work per cycle), force generation (75, 234, 427), muscle
activation of arms and shoulders (412), wheelchair configuration (rim size
(429), gear ratio (254), rim tube diameter (181), seat height and position (415)),
type and position of the propulsion mechanism (levers, rims, arm-cranks or hubcranks) (413, 416, 417), as well as individual characteristics (138, 235, 273, 284,
416). Propulsion technique varies between WCUs depending on the type of
wheelchair used, activity (daily propulsion, type of wheelchair sport), the
individual functional capacity of the user, level of expertise and how well suited
the wheelchair is to the user (90, 91, 414, 416). Veeger et al concluded that the
combination of lower handrim velocity and larger propulsive torque was
beneficial to the efficiency of wheelchair propulsion (429). In addition, they
12
Introduction
affirmed that the most efficient direction of force application was tangential to
the rims (Figure 5).
Figure 5. The relationship between force direction and calculated net joint
torques around shoulder and elbow. From Veeger et al. (432).
In summary, the most efficient wheelchair propulsion entails a combination of a
proper and individualised wheelchair design that reduces rolling resistance and
fits the user; a good level of physical fitness to counteract the forced physically
inactive lifestyle; and an ergonomic manner of propulsion that neutralises the
low mechanical efficiency of handrim wheelchair propulsion (431), which is the
product of the discontinuous movement, the particular muscles used (430) with
their low muscle mass, the position of the arms and the synchronicity of the arm
13
Isabel Rossignoli 2015
movements (140). An overview of the three factors that determine the efficiency
of wheelchair propulsion (wheelchair design, user and wheelchair-user
interaction) has been given, nevertheless, other individual (posture, fitness,
physical characteristics), environmental (exposure to cold, vibration, overhead
reaching) and work (transfers, pressure reliefs, driving, upper body dressing,
ramps or inclines) factors should be considered to reduce the risk of shoulder
injury and to allow the WCU to carry out activities of daily living, exercises
during physical therapy and physical training safely and with the correct
technique.
1.1.4.2 Wheelchair transfers
We have included a specific section for transfers since transferring to and from
the wheelchair has been reported as the second most painful activity for the
upper limbs of WCUs after wheelchair propulsion (32, 78, 158). The technique of
transfers has evolved from an overhead trapeze bar to techniques such as pivot
transfers or devices such as sliding boards or poles (Figure 6). Trapeze transfers
demand shoulder flexion, abduction and internal rotation placing the shoulder in
an impingement-prone position (158). This activity generates an intra-articular
pressure in the shoulder that exceeds the arterial pressure by two and a half
times, which, combined with the abnormal distribution of stress transmitted
across the subacromial area during the transfer, contributes to the high
prevalence of shoulder pain (32).
Figure 6. Sliding board (left) and sitting pivot transfer (right) for individuals with
spinal cord injury. From Gagnon (129)
14
Introduction
There is a lack of documentation of transfer technique in the literature. It is
necessary to have a clear definition of the correct technique before
biomechanical analyses of the various transfer techniques may be performed.
Transfer techniques will differ depending on the lesion level. For example,
tetraplegic individuals, who do not have innervation to their triceps muscles,
must lift themselves using flexion and adduction of the shoulder (157). Shoulder
pain can also be modified by the technique of the transfers; in a study with 23
WCUs, the 13 subjects with shoulder impingement performed transfers with
reduced thoracic flexion and increased scapular and humeral internal rotation
(119). This study also compared transfers towards the involved or dominant
side (lead limb transfer) to transfers towards the instrumented or non-dominant
side (trail limb transfer). The instrumented limb transfer showed reduced
upward scapular rotation and posterior tip and lower trapezius and serratus
anterior muscle activity than in the lead limb transfer (119). Ultimately, and in
support of the benefits of exercise in WCUs, the residual musculature should be
maintained to be able to do the transfers.
1.1.4.3 Musculoskeletal causes of shoulder pain and excessive load
The main shoulder pathologies of WCUs – subacromial impingement and rotator
cuff disorders – have, to this point, been discussed. These pathologies are
primarily caused by a narrowing of the impingement zone, that is, the space
through which the supraspinatus tendon passes. Some reasons for these
pathologies in WCUs have also been reviewed, including wheelchair ambulation
and transfers, however the most common causes of shoulder pain are due to
musculoskeletal disorders. Shoulder pain in WCUs may originate both from
structures intrinsic and also extrinsic to the shoulder joint complex. Other causes
of shoulder pain, impingement syndrome and rotator cuff pathologies, reported
by the literature, include:

Overuse (19, 32, 284, 313)

Repetitive overhead activities, such as reaching from a wheelchair
position (6, 8, 19, 108, 225, 389)
15
Isabel Rossignoli 2015

Time since injury (134)

Reflex neurovascular disorders of the shoulder, arm and hand, known as
‘shoulder-hand syndrome’ (294)

Weakness of abductors and/or muscle strength imbalance of abductorsadductors (53, 100, 269)

Weakness of rotator cuff (specifically external rotators) and axial
musculature that influences humeral head depression (53, 269)

Level of the spinal lesion (269)

Referred pain from the neck (19, 366) or degenerative changes at the
cervical spine (100)

Orthopedic origin (366)

Mechanical impingement, which is responsible for the rotator cuff
disease (32, 273)

Acute trauma when the humeral head is forced against the acromion,
such as when the arm is used to brace a fall (19)

Calcification
of
the
coracoacromial
ligament
with
subsequent
impingement and acromioclavicular joint arthritis (19)

Ligamentous laxity (100)

Nerve root entrapment (100)

Complex regional pain syndrome type II (100)

Frozen shoulder (19)

Joing instability (19)

Infection (19)

Myocardial infarction (19)

Syringomyelia (101)

Heterotopic ossification (101)

Spasticity (100)
It is generally accepted that the musculotendinous-type overuse injuries are the
most common cause of rotator cuff injuries (100). Excessive shoulder joint
loading through the support of body weight has been related to pushrim forces
and median nerve function (43); weight loss may probably prevent this injury in
manual WCUs (75). In support of this, several authors found that BMI may play a
16
Introduction
roll in shoulder injuries in WCUs because of its direct relation to the amount of
physical strain experienced during transfers and propulsive work done during
wheelchair propulsion (43, 47, 100, 192).
A number of causes of shoulder pain exist, therefore, in addition to factors
related specifically to wheelchair ambulation and transfers. Many of these have
musculoskeletal origins and are related to the high mechanical load on the upper
limbs, during handrim wheelchair propulsion, as a result of the repetitive and
continuous nature of this activity, the relatively small muscle mass involved, the
relatively large peak force required and the specific direction of force application
involved, and finally the complexity of the shoulder joint, particularly with
regard to stabilizing the glenohumeral joint.
17
Isabel Rossignoli 2015
1.2 TOOLS FOR SHOULDER PAIN EVALUATION
Assessment of the specific location or cause of shoulder pain in WCUs is
complicated, and treatment may be inappropriate without an accurate
evaluation. Arthrography (32, 57), radiography (5, 7, 30, 47, 57, 152, 229, 447,
450), imaging and arthrographic magnetic resonance (6, 7, 44, 47, 108, 312) or
computed tomography (152, 435) are considered accurate and reliable
techniques to diagnose the causes of shoulder pain. Nevertheless, these
assessments are expensive and usually not available to many researchers (152,
396). Particularly, magnetic resonance arthrography is an invasive technique
and the required intraarticular injections for this technique pose a risk to the
joint (451). Moreover, the effectiveness of these evaluative tools are dependent
on the experience of the radiologist (152), and some techniques are better suited
to specific types of shoulder injury (152, 160). For example, arthrography is not
helpful in detecting partial tears of the tendons (211). Other evaluation
implements, that are cheaper and less time-consuming for assessing shoulder
pain in WCUs, are: physical examination (47, 50, 57, 229, 312), specifically the
Physical Examination of the Shoulder Scale (50, 400); inclinometer (27, 202,
388); dynamometer (16, 44, 266, 330, 388) – the hand-held dynamometer
(HHD) is the most frequently used; electromyography (EMG) (37, 119, 266, 274276); ultrasound (50, 152, 419); and questionnaires (49, 81).
It has been reported that self-report questionnaires are the most frequently
employed, non-imaging evaluation tool for shoulder pain (49). Of all of these
tools, the most commonly used in the assessment of shoulder pain in WCUs is the
questionnaire (49, 59, 226, 284, 300), with the Wheelchair Users Shoulder Pain
Index (WUSPI) (23, 78, 80-83, 354, 372) and Shoulder Pain and Disability Index
(17, 40, 52, 105, 170, 241, 337, 446) being the two most popular. Other shoulder
pain questionnaires include the ShoulderQ, designed for hemiplegic shoulder
pain (405), the Shoulder Disability Questionnaire (285) and the visual analog
scale for pain (7, 285). The WUSPI test is the one used in this thesis and will be
explained in section 3.4.2.
18
Introduction
Thurston et al. (400) claimed the need for a noninvasive, but accurate test to
appropriately evaluate shoulder pain. They pointed to thermography as a wellestablished technique used for the evaluation of the back, neck and shoulder
pain (38, 400). This technique will be described in the following section.
19
Isabel Rossignoli 2015
1.3 INFRARED THERMOGRAPHY
1.3.1 Concept and types
Infrared Thermography (IRT) is a noninvasive method that detects and records
the infrared radiation in the long-infrared range of the electromagnetic spectrum
emitted by any body, and allows the interpretation of the distribution of surface
temperature (77, 216). The amount of radiation emitted by an object increases
with temperature, hence, thermography enables the assessment of variations in
temperature.
In
humans,
this
technique
provides
information
about
physiological processes related to blood perfusion, through the examination of
skin temperature (Tsk) distributions (167, 204). The maximum flux of blackbody
radiation at human skin temperature (30-36°C) is in the infrared part of the
spectrum (9–10 µm). Accordingly, clinical thermography must use detection
systems sensitive to that range of the infrared spectrum (15). In contrast to other
regions of the infrared spectrum, skin is >98% emissive in the 9-10µm range.
When skin is partly reflective, as it is below 8 µm, the detected infrared emission
may represent the infrared radiation originating from other sources in the
environment (15). Because of this low energy and intensity of the Tsk infrared
radiation, telethermometry was not available for clinical usage until the advent
of more sensitive and precise (<1% precision) detectors of infrared radiation
such as the photon or quantum detectors (15). Another requirement of the
application of thermal imaging to Tsk is a spatial resolution that allows the
distinction between two points less than 1 mm apart and differing in
temperature by 0.1°C. Factors that determine the temperature distributions on
body surface must be considered, including the temperature of internal organs,
heat conductivity of muscular and adipose tissue and heat emissivity of the skin.
Thus, the temperature on the surface of the skin is dependant on the
temperature of internal organs and the heat properties of the tissues that lie
between the organs and the body surface. It must be remembered that IRT only
measures heat convections at a depth of 0.5 cm.
20
Introduction
The methods of measuring infrared radiation utilize either contact and
noncontact devices. Contact devices are characterized by liquid crystal
thermography or LCT, where cholesteric crystals are embedded in rubber sheets
and the layers of crystals are mounted in a frame. Those crystals selectively
reflect polarized light in a narrow region of wavelength; therefore they change
their colour when applied to the surface of the body (216). The colour
distribution represents the Tsk distribution that is photographed to have a hard
copy of the image or thermogram (15). Other contact devices for measuring
temperature include thermometers, thermistors, and thermocouples.
The advent of the quantum physics allowed the development of noncontact
infrared equipment. There are a number of the different contact-free
thermography techniques, including infrared or electronic thermography (IRT),
computer-assisted
image
analysis,
area
telethermometry,
infrared
telethermography (ITT), and digital infrared telethermographic imaging (DITI)
(15). Electronic thermography involves scanning mirrors that reflect the infrared
radiation on an infrared transducer, and the infrared pattern is displayed on a
cathode ray tube from which it can be photographed (216). Telethermometry, or
radiation thermometry, measures Tsk at a single spot, remotely, and
telethermography, or area telethermometry, provides quantitative information
on the Tsk of a large area (15). Dynamic area telethermometry (DAT) measures
the time dependence of Tsk, that is, the modulation of the temperature when the
Tsk changes non-uniformly over the surface.
Because a thermal imaging camera allows for the distinction between warm
objects against cooler backgrounds, it is possible to use this type of camera to
monitor Tsk. Thermographic cameras provide a thermal map of the skin surface
measuring the heat radiation emitted, however the literature recommended not
comparing Tsk results that have been measured with different types of
thermographic cameras (conducted vs. infrared) (36, 96). Thermographic
cameras produce a visual display of the radiation called a thermal image or
thermogram. Early models of infrared cameras had low thermal and geometric
resolutions, stability issues and low reproducibility or accuracy, as well as a high
21
Isabel Rossignoli 2015
cost. Due to these limitations, IRT was rapidly substituted by other more precise
diagnostic techniques (39). Currently, with the advent of modern infrared
cameras (Figure 7) and improved data acquisition and processing techniques, it
is now possible to have real-time high-resolution thermographic images (198,
227, 381, 411) (Figure 8). Such high-speed images with high thermal and spatial
resolutions can be rapidly processed with modern software and standardized
protocols (see Figure 9, for example).
Figure 7. The first medical thermographic device developed by Schwamm and
Reeh in 1952, from Berz et al. (39) (above), and a modern high resolution
thermographic camera VarioCAM®, from Jenoptik (193) (below)
22
Introduction
Figure 8. Thermogram of a patient with allergic rhinitis detected with an early IRT
camera, from Georgevici (136) (left), and a thermogram of a patient with
hypothyroidism and inflamed carotid artery detected with a modern IRT camera,
from Möhrke (271) (right)
Some advantages to using thermal imaging cameras include immediacy of
results, mobility and adaptability, easy comparison of images, rapidity in the
millisecond range facilitating measuring of moving targets, and there is the
option to record a thermal video as well. Moreover, given that thermal imaging
cameras are noninvasive and contact-free, they allow for the measurement of
dangerous or physically inaccessible bodies and the risk of contamination to be
avoided, there is no interference with and no energy lost from the target, and
there is no mechanical effect on the surface of the object (145, 208).
Figure 9. Thermograms with TotalVision™ Anatomy Software. From Möhrke (271)
23
Isabel Rossignoli 2015
1.3.2 Infrared thermography applications
Fernández divided the main areas in which IRT is applied into two groups: IRT
for objects and IRT for living beings (112). The first group includes diverse
domains, such as engineering, construction, the military, industry, the
environment andastronomy, that which a long history of the use of, and strong
market for, IRT. The application of IRT in these domains include, for example, the
location of the base of a fire through the smoke by firefighters, the detection of
building fissures in historic structures and diagnosis of buildings safety; nondestructive testing of structures; the positioning of overheating joints and
sections of power lines; the location of gas and heat leaks in defective thermal
insulation to improve the efficiency of heating and air-conditioning units; the
inspection procedures for and optimization of the experimental set-up in the
aerospace industry; mapping of surface temperature in temperature-dependent
manufacturing processes; night vision, missile guidance and surveillance
cameras in the military industry; surface crack detection on concrete surface and
masonry bridges; the control the process, cost reduction and safety
improvements in steel industry and high voltage facilities; the protection of
flowers and trees; or monitoring and water pollution (26, 29, 71, 89, 110, 150,
208, 240, 244, 262, 287, 359, 402, 436).
Infrared thermography also has many direct applications in humans and
animals. The majority of studies of IRT in veterinary medicine are focused on its
utility as a diagnostic tool in equine health to detect locomotion injuries (e.g.
quantify inflammatory process) and to monitor the health status of horses (252,
324, 375, 382, 386). Moreover, in recent years, IRT has been directed to the
exercise training and thermoregulation of racehorses (135, 168, 371, 379, 454)
and animal behavior (208). The main source of error in IRT animal studies is due
to variation in emissivity, evaporative cooling and radiative heating of an
animal’s coat. Their hairy skin hinders the measures and it makes necessary to
wait for the seasonal shedding of fur (252). Another methodological limit is the
skin thickness. The literature on thermography in equine medicine recommends
that the examination be performed when the horse is at rest and before training
24
Introduction
to avoid the changes in body heat balance and blood circulation related to
working muscles (379). Horses are the most studied animal with respect to IRT,
however birds, foxes, bats, rats, marine mammals, cattle, sheep, dogs and wolves
have also benefited from this technology (126, 228, 255, 256, 301, 382).
From all the usages of IRT, we are obviously more interested in human
applications. The utilization of IRT in the clinical field in humans dates back to
the 1960s, although it started to become more accessible in the 1970s with the
development of computerized processing that allowed the storage and
quantification of images (332). Some physiological changes in human beings can
be monitored with IRT during clinical diagnostics testing. Kobrossi et al. affirmed
that this is an ideal technique for diagnosis because of its noninvasive and safe
nature and because it can be frequently applied (216) (other imaging techniques
cannot be used so frequently because of their potential to be harmful to
humans). However, these authors limited thermographic evaluation to
cutaneous circulation and pathological conditions that influence the superficial
blood flow, and confined its use for soft tissue injuries assessment (216). In spite
of IRT limitations as a diagnostic tool, Bertmaring et al. also recommends the use
of IRT to evaluate and identify injuries and musculoskeletal disorders (38). Some
of the most representative applications, in the medical and physiological
environment, where thermography is being used successfully are (39, 151, 203,
227, 267, 332):

Anaesthesia:
- Pain management: neuropathic pain
microcirculatory
sympathetic
due to
dysfunction,
perivascular
radicular
pain
syndromes, reflex sympathetic dystrophy, complex regional
syndrome, myofascial pain, and nociceptive pain (99, 125, 163165, 169, 172-174, 184, 222, 223, 230, 328, 361, 401).

Neurology:
- Neuromusculoskeletal disorders (4, 24, 35, 74, 308, 343, 400, 408,
420, 458, 460).

Traumatology:
- Detection of entrapment of peripheral nerves (196, 197, 311);
25
Isabel Rossignoli 2015
- Rehabilitation medicine, pain detection and location of the
neurological level of paralysis in individuals with SCI (92, 179, 180,
188, 189, 340, 342, 361, 362, 463, 464);
- Musculoligamentous injuries (332) of the spine (207), shoulder
(270, 299, 394), trapezius (310) and forearm (360), including
arthritis, bursitis and tendinitis (92, 151, 364, 399).

Evaluation of vascular disorders and measurement of the skin blood
perfusion (96):
- Evaluation of patients at high risk for lower extremity peripheral
arterial disease (176);
- Detection of deep vein thrombosis (194);
- Detection of entrapment of blood vessels, and vascular occlusion
predictive of CVA (206);
- Histamine skin test evaluation (409);
- Detection of tissue death in instances of frostbite, diabetic ulcers,
and burns (309).

Oncology (133, 162, 267, 449), especially breast cancer screening (22, 39,
215, 246, 282, 295).

Neonatal physiology (65, 156).

Surgery: appendicitis diagnosis (104), shoulder surgery (217, 296, 455),
flap tissue viability (239, 397), breast reconstruction (444), location of
perforator vessels (296), plastic surgery (267).

Dermatological disorders (70, 95, 268):
- Diagnosis of skin tumours: hyperthermic detection of cutaneous
melanoma;
- Cosmetic field: evaluation of aging skin to prevent photo-aging.

Microangiopathies:
- Study of skin circulation in systemic diseases such as progressive
systemic sclerosis, diabetes (127, 357, 380, 390, 461) and arterial
hypertension;
- Locoregional diseases such as occupational radiodermitis and
occupational Raynaud’s syndrome (332).

Assessment of the effectiveness of different therapies:
26
Introduction
- Ice burn and cryotherapy (358);
- Whiplash injury treatment (232);
- Trigger point treatment (74, 242, 393);
- Anterior cruciate ligament therapy (305);
- Coccygodynia therapy (448).

Diagnosis of thyroid gland disease (161).

Facial IRT applied in dentistry (15, 149).

Gynaecology (224).

Allergy detection (267)

Tuberculosis (123)

Effects of vasoactive drugs (corticosteroids) (332)

Others: kidney transplantation, heart, rheumatic diseases, orthopaedics,
fever screening for swine flu detection in airports (42, 62), and brain
imaging.
The use of IRT by VU University Medical Center in Amsterdam was presented in
at the XIII European Association of Thermology Congress: “Thermology in
Medicine: Clinical Thermometry and Thermal imaging”, in 2015. In this clinic,
IRT is widely used to monitor vital functions (heart rate, breathing, perfusion,
oxygenation and temperature), to discriminate diseased from healthy tissue
(pre-cancerous tissue, inflammation and tissue damage such as eczemas), and
for treatment monitoring of dermatology allergy testing (even allergic reactions
not recognized by visual inspection). Several of the clinic’s research studies were
introduced at the congress that exemplify the diverse application of IRT,
including the assessment of stress recovery by thermography, the oxygenation of
the fetal brain in the final stage of childbirth, the quantification of inflammation
in Graves’ orbitopathy, the examination for hypothermia in high altitude and the
study of Temporomandibular disorders, along with many other interesting
applications in the sport field: thermographic evaluation of swimming
techniques, different thermal models of warm-up for decathlon athletes, for
aerobic and anaerobic training and analysis of the hamstring muscles during
static stretching.
27
Isabel Rossignoli 2015
The most common areas of research regarding IRT and people with disabilities
are:

The improvement of communication with people unable to speak, IR
thermal video detects the movements of the mouth, and therefore IRT
substitutes conventional less hygienic devices that require the mouth to
direct objects (258-260);

The design of cushions for avoiding pressure-ulcers (116, 117);

The Tsk responses in lower limbs in children with cerebral palsy (466);

The Tsk inside prostheses as rest does not provide thermal relief (214);

The study of the autonomous nervous system with skin vasomotor
responses to cold stimuli in individuals with severe motor and intellectual
disabilities (392);

The study of postural adjustment in leg length differences (1);

The evaluation of autonomic function in animals and humans with SCI
(99, 186, 228, 439, 464);

The detection of the neurological level of paralysis in SCI people, which is
useful in emergency diagnosis and therapy for accident victims (340).
Moreover, the principal areas of interest in IRT application in the sport sciences
include:

Sport injury prevention and monitoring (33, 34, 114, 130, 131, 146, 167,
168, 368), specifically in knee injuries, epicondylitis, ankle sprain, tibial
shin splints and stress fractures (151), patellofemoral syndrome, Osgood
Schlatter’s disease, bicipital tendonitis, entrapment neuropathies, spinal
injuries, and reflex sympathetic dysfunction;

Monitoring thermoregulation during exercise and recovery (2, 264, 265,
298, 351, 378, 442);

Evaluation of mechanical load on the muscles of upper limb during
wheelchair driving (248, 251, 365);

The effectiveness of compression stockings in running (322).
Early detection of overuses injuries and minor trauma in athletes is crucial to
avoiding injuries, thus the application of IRT in sport injury prevention has been
suggested as one of the most beneficial and promising applications (167, 168).
28
Introduction
This demands the investigation of different thermal patterns by group i.e., sport
and discipline, and by injury, particularly with regard to the evolution of the
injury. The stage of injury development will be reflected as hyperthermia in
acute injuries, inflammatory processes that result in higher skin blood flow such
as in infections, tendinitis, bursitis, bone fractures, arthritis, tennis elbow,
compartment syndrome and ankle sprain; and a hypothermic pattern in chronic,
compression, poor perfusion and degenerative injuries including nerve damage,
reflex sympathetic dystrophy, Raynaud’s phenomenon, avascular tissues and
vein occlusion (113, 130). A proper diagnostic procedure should accompany the
thermographic analysis of an injury, in which information about previous
injuries, diseases and surgeries is obtained for a correct interpretation of the
thermograms. The application of IRT in prevention of injuries is based on the
concept of corporal symmetry, which will be described in the section 1.3.5.
IRT and pain
Of all the applications of the thermography, the interaction with pain
management in connection to sport injury prevention is particularly interesting.
Wheelchair users may experience pain in their muscles joints, bones, ligaments,
and nerves, and in some cases an individual may feel pain in areas distant from
the injury, which is called ‘referred pain’. The zones of the referred pain are a
somatocutaneous sympathetic response, which is usually presented with
hyperthermia due to decreased sympathetic function. That response can be
located with thermography (34). BenEliyahu (1990) showed that IRT findings
correlated with the painful areas reported by their subjects, and although
thermography is not a picture of pain, it is a picture of autonomic dysfunction that
correlates well with pain (34). The literature is in agreement with this
relationship between thermography and pain or tisular damage (10, 455), and
suggests that IR imaging could be a valid technique for detecting soreness.
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1.3.3 Factors influencing the application of infrared thermography in humans
An extensive review of the factors that influence the application of IRT on the
human body was conducted by Fernández et al. (113). They classified these
factors in the following groups (see Figure 10):
1. Environmental factors, including room size, ambient temperature,
relative humidity, atmospheric pressure, and source radiation (297, 363);
2. Technical factors, such as validity, reliability, protocol, camera features,
ROI selection, software, and statistical analysis;
3. Individual factors:
a. Intrinsic factors, for example, sex, age, anthropometry, circadian
rhythm, hair density, skin emissivity, medical history, metabolic
rate, skin blood flow and genetic and emotional influences;
b. Extrinsic factors, such as intake factors (substancies that are
ingested), application (topical creams and oilments), therapies and
physical activity (137, 174, 308, 332).
Figure 10. Classification of IRT-related factors in humans by Fernández (113)
30
Introduction
Alternatively, the factors that must be considered in the evaluation of the human
body using IRT can alternately be classified as natural, artificial and sportsrelated. In the group of natural factors, atmospheric pressure, relative humidity
and air temperature, as well as reflectivity or reflected radiation of surrounding
objects, must be controlled for during IRT measurements (297, 363).
Furthermore, it is recommended that artificial factors such as the ingest of
medications that affect the cardio-vascular system are avoided, and likewise,
nicotine (137, 308) and alcohol, large meals and the consumption of tea, coffee
and sugar should be avoided (174). It is also recommended that creams and
ointments are not applied prior to the IRT analysis being done (36), and that the
skin is not exposed to sunlight for prolonged periods or treatment with
ultraviolet rays. Sweat can also change the skin surface temperature (36, 459).
Electrotherapy,
ultrasound,
thermotherapy,
cryotherapy,
massage
and
hydrotherapy treatments must be avoided because their thermal effects can last
from 4 to 6 hours (332). Moreover, circadian rhythm affects Tsk due to the loss of
heat through the limbs (270); circadian effect can be avoided by testing each
subject at the same time as their previous test. The temperature variation of
female breast, which is affected by individual development of the mammary
gland, the distribution of veins in the breast and the period of catamenia (65),
should be considered if the pectoral region of women is to be evaluated. Physical
exercise should not be performed within 4-6 hours before IRT analysis, as a
number of sports-related factors may influence the results, including the type of
sport, playing position, dominant side use, state of rest or fatigue (and the
specific activity in the most recent session), composition of muscle fibres, density
of capillary nets, thickness of skin and body fat, nutrition, sex (menstrual period)
and clinical history (e.g., injuries, lipid profile and infectious processes) (38, 113,
143, 369, 370, 462).
We will not enter in more detail since the literature extensively explains them.
Though, we will review the studies that applied IRT in people with disabilities,
and we will propose a few recommendations.
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Isabel Rossignoli 2015
1.3.3.1 Specific factors influencing the application of infrared thermography in
people with disabilities
There are a number of disability-specific characteristics that can influence the
efficacy of IRT in people with those disabilities. For example, a steady body
posture must be maintained during IRT evaluation. Persons with cerebral palsy
or with SCI may present involuntary muscle contractions and these spasms may
start or increase with changes of posture. Emergence of these movements can be
avoided with muscle relaxant drugs (although the effect of anti-spasticity
medicaments in IRT evaluation is yet unknown), by minimising or avoiding
posture changes altogether or slowing the speed of changes to body posture.
Calancie reported that spasmic contractions did not occur unless the hips and
knees were extended, such as when the subjects were supine (56).
Multiple sclerosis is a chronic and progressive neurological disease
characterized by inflammation and demyelination of nerve cells (87, 304). The
lesions of multiple sclerosis are restricted to the central nervous system and
hence they arise from disruption of central sudomotor pathways (290) and can
result in autonomic dysfunction (304). Subjects with multiple sclerosis may
present abnormal thermoregulatory sweating resulting from a lesion in the
central or preganglionic sympathetic nervous system (290, 410). A case reported
by Ueno et al. found a high-intensity lesion involving the left hypothalamus with
a consequent over-activity in the sweat glands of the right forehead and shoulder
(410). Although the literature reports cases of hyperhidrosis, a more common
response is decreased sweating and regional anhydrosis, or total anhydrosis in
the most advanced cases of multiple sclerosis (177, 304). These abnormalities in
thermoregulatory sweating may impact the effectiveness of IRT. Furthermore,
during exercise, people with multiple sclerosis may present impairments in the
autonomic control of cardiovascular (reduced elevations in blood pressure) and
thermoregulatory function. Moreover, 80% of subjects with multiple sclerosis
developed a variety of neurological signs (e.g., amblyopia) during hyperthermia,
60% of which had not been previously experienced (153). Heat also increases
weakness and spasticity in 62% vs. 14% of deterioration after cold exposure
(153). It is recommended to do physical exercise in early morning or after sunset
32
Introduction
to minimize heat exposure; it is also suggested to precool the head and neck
(304).
Scar tissue can influence Tsk (174, 203, 335, 363), which may be particularly
pertinent when using IRT in individuals with amputations or SCI due to
accidents who may have significant scarring located in specific part of the spinal
column. Moreover, some people with disabilities may experience problems with
the peripheral circulation in the distal parts of the body (459), as a consequence
of obliterating artery disease, malignancies, varicose veins or inflammatory
processes. This local change in blood flow can affect the Tsk (441) and
subsequently, the results of IRT. Finally, and of particular interest to this thesis,
people with SCI also present thermoregulation problems that can influence the
success of IRT techniques (319). These will be discussed in further detail in
section 1.4.2.
1.3.4 Technique and protocol
Thermography requires standardized protocols and careful interpretation of
thermograms (173, 204). According to Ring and Ammer, the thermographic
evaluation should follow these steps (332):
1. Ensure that the location, the assessment room, is of a satisfactory (or
particular) temperature, equipment for the image processing and the
cubicle for the participant;
2. Image system: infrared cameras, reference temperatures, image
monitoring, installation of the cameras and processing of the
thermograms;
3. Participant: previous information, balance and positioning of the
image and vision field;
4. Report generation: colour and temperature scales, processing and
archiving of the thermograms.
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In addition to the recommendations from Ring and Ammer (332), other
internationally recognized guidelines for thermographic evaluation include the
“Thermology Guidelines. Standards and protocols in Clinical Thermography
Imaging” from the International Academy of Clinical Thermology (185) and “The
Glamorgan Protocol for recording and evaluation of thermal images of the
human body” by Ammer (2008) (13).
For the optimization and reliability of the assessments, all tests must be
conducted in an air-conditioned room that is free of drafts, with a recommended
dimension of minimum 2x3 m (332). The literature advocates a temperature
range of between 18 and 25°C (332), 22.5°C (38), and between 23 and 26°C
(407), oscillating one or two degrees depending on the weather. Importantly, the
highest degree of emissivity in humans is achieved at 21°C. It is interesting to
know that inflammatory injuries are more visible in cold environments (20°C),
but for the evaluation of the limbs, a warm environment has been suggested, i.e.,
around 22-24°C (332). In any case, the Tsk is more homogeneous under warm
conditions (96). Humidity was recommended to be between 45 and 60% (407).
The use of thermography requires that the skin is free of clothing and jewelry for
10-15 minutes prior to the measurement, and the subject must be at rest to
acclimatize the skin and the blood pressure. Moreover, the participant should
avoid tight clothing and bending the arms or legs during this period. If this
resting time is extended to 30 minutes, some body temperature changes will be
observed as a result of thermal asymmetries in the two sides of the body (332)
due to vasoconstriction, for example, specially in subjects with SCI (see 1.4.2).
The selected body position for the measurement has to be consistent when interand intra-individual comparisons are to be made, otherwise the body surface
area exposed to ambient temperature might differ, i.e., two thermograms taken
in different positions - standing up, sitting down or lying down - cannot be
compared.
Participants should abstain from smoking (137, 332) prior to thermographic
images being taken, as well as from drinking coffee, tea or alcohol, which will
34
Introduction
increase Tsk due to skin vasodilatation (109, 248, 257). Taking medication (216)
should also be avoided, as certain drugs may influence the cardio-vascular
system and affect the Tsk (332). Eating heavy meals on the day of the
examination (86) and participating in physical activity within 8 hours before the
IRT evaluation (113, 201) can affect the results and so participants should
refrain from these. Wearing cosmetics or ointments can change the emissivity of
the skin (332, 384) and so should be avoided prior to testing, as should
treatments such as electrotherapy, ultrasound, heat treatment, cryotherapy,
massages and hydrotherapy, since the thermal effects on the Tsk will last for up
to 6 hours (216, 332). Some studies exclude subjects with a body fat content
greater than the 50 percentile, because of the insulating effect of adipose tissue
in the thermal data (38, 353). Larger variations of Tsk distributions have been
found as body fat mass increases (238). Finally, it is necessary to know a
person’s clinical history since some surgeries, scars and pathologies leave
permanent changes to the skin that can incorrectly modify the skin temperature
distribution.
External light over the camera lens can alter the thermograms, which should be
considered when calculating the angle between the camera and subject, and can
be avoided with curtains or reflectors. The proximity of the infrared camera with
respect to the subject depends on the area of study or region of interest (ROI).
Bertmaring et al. positioned the camera 0.5 m from the shoulder when
investigating this joint specifically (38), but other ROIs require 2 m to include the
trunk and upper limbs. Furthermore, it is recommended that the distance be
fixed when replicating the test in future registrations, as a change in the field of
view of the same subject could lead to false Tsk data. To avoid an angle of
inclination of the camera above horizontal, and hence ensure reliable and valid
measurement, it is recommended that a tripod with vertical adjustment be used;
one with wheels, for fast changes in position, may also be beneficial (332).
Moreover, the temperature behind the subject should be controlled using a white
or black background that will provide a uniform temperature. With regard to the
image system itself, the new generation of infrared cameras use new techniques
of data processing that can quantify the thermograms. Most thermal imaging
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Isabel Rossignoli 2015
cameras have an internal reference temperature and perform auto-calibrations;
hence the technician does not need to do external calibration (336).
1.3.5 Corporal symmetry and infrared thermography
There is a direct relation between the increment of temperature and the
emission of infrared radiation. Furthermore, there is a direct relation between
the increment of temperature from a body part that has been overloaded
because of training or competition and the risk of injury (167). Infrared
thermography can measure this increase of temperature, and bilateral, localised
Tsk differences can be identified by monitoring the evolution of the temperature
changes in the thermograms (comparing one side of the body with its
contralateral) and used to detect the presence of pathologies (28, 111, 167, 350).
Jones et al. indicated that changes of a few degrees Celsius in core body
temperature is a sign of physical dysfunction (204). A normal thermogram of the
limbs should show a symmetrical heat emission (216). In healthy subjects, the
cutaneous temperature difference between the sides of the body (ΔTsk) was
reported to be only 0.24±0.073°C (406). On the contrary, a temperature
difference of at least 1°C between the right and left sides of the body for more
than 25% of a specific body region is classified as asymmetrical or an
abnormality (4, 38, 111, 361, 400, 406, 460). With the improvement in the
thermal imaging cameras’ accuracy, the limit for left-to-right-side asymmetries
has been reduced to 0.5°C for clinical significance for healthy normalised ΔTsk
(28, 286, 407, 426). Subsequent studies of athletes saw a reduction in the normal
ΔTsk to 0.4±0.37°C (54), 0.4±0.22°C (459), and 0.3±0.61°C (167). This limit was
reduced even further in a recent study (424) in which the ΔTsk was equal to
0.19±0.2°C. The standard deviation providesve information about the presence
of abnormalities; it has been proposed that a ΔTsk exceeding 3 SD from the mean
is not normal (286).
Thermographic data of healthy subjects are scarce, notwithstanding a database
of normal Tsk patterns distribution is under construction (333). Many efforts
have been made to develop this database using data from different people of
36
Introduction
various ethnic backgrounds, including healthy Brazilians (245), Chinese (462),
Finnish (459), Taiwanese (286), Mexican children (218), and Portuguese (425).
Thermal references allow for the evaluation of normal Tsk and ΔTsk in different
ROIs. Therefore, it would also be interesting to include data from studies
regarding the ΔTsk in people with specific impairments or pathologies. An
example of one such study is that of Sherman et al. in which skin temperature
was compared between an area with normal sensations and an area without
sensation or with abnormal sensations in subjects with complete and incomplete
SCI. The differences were 1.5±0.62°C and 0.58±0.29°C for the participants with
complete and incomplete SCI, respectively (362). Since some nociceptive and
most neuropathic pain pathologies are associated with an alteration of the
thermal distribution (173), a more recent study on the assessment of pain
through IRT proposed statistical computations and distance measures between
comparable regions to assess the degree of asymmetry between contralateral
ROIs (165). In another example with patients with peripheral nerve injury, the
Tsk in the area innervated by the damaged nerve deviated an average of 1.55°C
from the undamaged areas (406). There are many other examples of ΔTsk
description in pathology samples (51, 293, 345, 406, 441). Some of these
asymmetries may remain for long periods, for example, for the first 90 days of an
injury in the peripheral nerves the Tsk of the affected side is elevated, and
following this, a reduction in the Tsk appears, which may last for years (38).
Varicose veins may also present long-term alterations of the Tsk (227). Cold
stress, common in northern countries, can increase the ΔTsk (459).
The effect of left- and right-side dominance, and factors associated with it, on
skin temperature is unclear. The literature reported no consistent relative
hyperthermia in the dominant extremity, no definitive thermal asymmetries and
no systematic pattern related to handedness (111, 151, 459). Gross et al. added
that asymmetrical temperature distribution patterns are caused by unilateral
pathologies rather than dominance (151). Smith et al. indicated there are no
significant differences between the dominant and the non-dominant limb on the
patterns of temperature distribution (374). They explained the presence of ΔTsk
in healthy subjects is because of better vascularization in the dominant side as a
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Isabel Rossignoli 2015
consequence of physiological adaptations resulting from repetitive unilateral
activities performed in some sports or occupations (374), and not because of an
increased muscular mass in the dominant side. However, other studies suggested
that hyperthermia in the dominant side is caused by greater vascularity, strength
and muscle fiber composition (38). Further, Sillero et al. suggested that
differences found on the dominant leg might be due to a different contraction
pattern (369). Nevertheless, regardless of the precise mechanism, it is generally
agreed that temperature comparisons between bilateral body areas can be
employed to detect symptomatology and abnormal patterns in Tsk distribution
(407).
38
Introduction
1.4 THERMOREGULATION
The body’s thermoregulatory system acts maintaining the normal body
temperature during challenges to thermal homeostasis. The thermoregulatory
system is under the command of the hypothalamus, which prevents overheating
or overcooling by detecting changes to different central and peripheral stimuli,
such as blood temperature, blood pressure and level of metabolic activity, and
regulating blood flow (61). The sympathetic function of the hypothalamus is
responsible for thermal emission and thermal microcirculation. Reflex
sympathetic innervation of the circulation of the skin incorporates the
sympathetic noradrenergic vasoconstrictor system and the non-noradrenergic
active vasodilator system. Cutaneous sympathetic vasoconstrictor and
vasodilator systems also participate in the baroreflex control of blood pressure.
The constant vasomotor tone of the peripheral arterioles and precapillary
sphincters and the consequent vasoconstricted state of the dermal vessels allows
inhibits excess heat loss from the core (34). Figure 11 summarizes the
thermoregulation process.
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Isabel Rossignoli 2015
Figure 11. Physiologic thermoregulation in humans. A, Increases in internal
and/or skin temperatures are identified by the preoptic/anterior hypothalamus
(PO/AH) and result in increased heat dissipation via cutaneous vasodilation and
sweating, which then corrects an increase in temperature. B, Decreased skin or
internal temperature causes reflex decreases in heat dissipation (cutaneous
vasoconstriction) and increased heat generation (through shivering) to correct a
decrease in temperature. CNS = central nervous system. From Charkoudian (60).
1.4.1 Thermoregulation and exercise
During heat stress and exercise, a large percentage of cardiac output is directed
to the skin and the active vasodilator system is initiated (61). Increased blood
flow to the skin plays an essential roll in preventing overheating. It facilitates
perspiration to cool the skin by evaporation and allows for a reduction in body
heat and blood heat by convection, when the air is colder than the skin (61).
Therefore, the two thermoregulatory mechanisms that are employed in response
to an elevated core body temperature during exercise are cutaneous
vasodilatation and active sweat secretion (200, 209). Fernández presented a
overview of studies that analyzed the influence of exercise on Tsk before, during
and after exercise using IRT (112).
40
Introduction
Of the total metabolic energy generated only 30% is converted to mechanical
energy and the rest should be dissipated to the environment through the skin
(233). At the beginning of exercise, the blood flow of the muscles increases
causing reflex vasoconstriction in the skin and metabolically inactive areas and
vasodilatation in the working muscles (61, 199). Heat transfer between the body
and the external environment occurs bi-directionally through convection,
conduction and radiation, whereby the transfer of heat is driven by the
temperature gradient between the skin and the environment. Heat is also
transferred uni-directionally through evaporation - heat is dissipated only from
the skin to the environment. Evaporation is the primary (>80%) means of heat
removal from the body (233).
The literature reports different skin temperature reactions subsequent to the
initial reactions described above depending on the type and duration of the
exercise (72, 168, 212, 265, 465). Increments in exercise load usually imply
increases of Tsk, quantitative and qualitative changes in the Tsk distribution and
homogenization of the Tsk during the recovery (73). Prolonged exercise at a
constant load raises the core temperature and this heat must be transferred to
the skin to be dissipated ouside the body, therefore an initial decrease of Tsk is
followed by an increase of the Tsk due to the reflex neurogenic skin vasodilation
(72, 118, 168, 171, 182, 237, 411, 437, 457). At some point during prolonged
exercises sweating ceases and the core temperature increases considerably.
Brief and intense, graded, intermittent or maximal exercises experiment this
initial decrease that is maintained across the full exercise while the working
muscles demand blood. This is due to an increase in catecholamine and
vasoconstrictor hormones as exercise intensity increases (212). Therefore, tests
of a short duration result in decreased Tsk caused by the blood redistribution
(264, 265, 404). The higher the intensity of the exercise, the more delayed the
onset of cutaneous vasodilation (61). Coh et al. concluded that IRT is an
important method for monitoring loading conditions resulting from different
training means or exercise intensities (73).
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Isabel Rossignoli 2015
When measuring the Tsk it should be considered that sweat changes the radiant
heat characteristics of the skin and can influence measurements and
underestimating the Tsk results. For this reason, some authors avoid using IRT
during exercises of longer duration because of the increased interference from
sweat (28). It is noteworthy to indicate that in cooler conditions (23 and 28°C)
such as the settings selected during IRT evaluations, the only reason for an onset
of sweating is related to a positive rate of oesophageal temperature variation,
while the Tsk level remains low and stable (243). This is in contrast to the
response following exercise in warm conditions (36.5 to 50°C), where the onset
of sweating is related to Tsk (243).
The literature reports some differences between the thermoregulation in trained
versus untrained individuals. For example, trained individuals have improved
skin thermal control, better vasoconstriction capability during the initial phase
of muscle work and a superior heat dissipation capability via the skin, because
the onset of vasodilation occurs at lower core temperatures and demonstrates
greater sensitivity to changes in temperature (264, 338). While it has been
reported that trained people have a more efficient thermoregulatory system
corresponding to greater levels of skin blood flow and sweating (61), the relation
between muscular effort and Tsk is still unknown. Interestingly, a very recent
study that assessed the relationship between neuromuscular activation and Tsk
during incremental cycle exercise found that participants with larger changes in
neuromuscular activation in the vastus lateralis muscle presented with a better
adaptive response of their thermoregulatory system, observed by smaller
increases in Tsk after exercise (321). This finding is supported by previous
studies that also showed a decrease in Tsk after the onset of the muscle work in
trained individuals (2) and a larger increase in Tsk after a prolonged exercise in
fit players (66).
1.4.2 Thermoregulation in people with spinal cord injury during exercise
People with SCI exhibit bradycardia, orthostatic hypotension, autonomic
dysreflexia, thermo-dysregulation and sweating disturbances as a result of
42
Introduction
impaired autonomic nervous system (221). All of these present important
applications for this population, however of particular importance to the
application of IRT are 1) the interruption of the neural transmission of
thermoregulatory signals; 2) the loss of autonomic nervous control for
vasomotor and sudomotor responses that leads to an inability to vasodilate and
sweat in regions below the level of the spinal cord lesion (175, 355); and 3) a
reduced thermoregulatory effector response for a given core temperature (314,
355). The three main phenomena linked with thermal dysregulation in SCI are:
poikilothermia, acute hyperthermia and exercise-induced hyperthermia (186).
Due to their poikilothermic behaviour, or the inability to regulate body
temperature in ambient conditions (453), people with SCIs show a lower core
temperature in the cold and a higher core temperature in the heat when
compared with able-bodied people (25), because of the lack of peripheral
circulation control (453). Consequently, people with SCI have a reduced ability to
tolerate thermal extremes (355), a greater heat storage within the lower body
(314) and a tendency to sweat less (314, 317). The acute hyperthermia related to
SCI, when it is not associated with infections or other such recognizable causes,
is called ‘quad fever’ and appears in the first weeks of months following the SCI
(186).
During exercise, the decreased sensitivity for thermoregulation as a result of SCI
translates to a greater increase in Tsk and skin blood flow in comparison with
healthy people (248). Circulatory responses during heat exposure, and also fluid
losses during exercise and heat retention during passive recovery from exercise
are related to lesion level (314, 453). This insufficiency in temperature
regulation makes Tsk very changeable from one day to another. Moreover, some
cardiovascular responses to exercise, for example, the increase of blood flow to
active muscles and vasoconstriction in inactive tissues, may be distorted (141).
Finally, the absence of a venous muscle pump, which limits the venous return
(140) must not be disregarded.
All of the complications described above are amplified in individuals with
tetraplegia compared to paraplegics (314) due to the alteration of sweating
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Isabel Rossignoli 2015
capacity. Although people with a low level of SCI can have up to a 50% reduction
in perspiration capacity compared to able-bodied individuals, being this
reduction proportional to their skin area available for sweating (178, 314).
Thijssen et al. found a significant disturbance of the circadian variation in core
temperature in tetraplegics, whereas paraplegics presented a comparable
circardian variation to their able-bodied counterparts (398). It has been
reported that people with tetraplegia have higher risk of hypo- and
hyperthermia than individuals with a thoracic-level injury (48, 213), and they
also have little to no sweating response as the injury level is above the
sympathetic outflow (155, 443). A study of the sympathetic sudomotor skin
activity in SCIs found that the manifestation or not of sympathetic skin responses
after stimulation at the palmar and dorsal wrist skin was dependent on the level
of the lesion and the location of the stimulation (327).
It has been suggested that the sixth thoracic vertebrae is the limit above which
individuals with SCIs experience a greater thermal strain (155). Gass et al. found
greater increase in the calf Tsk of subjects with T12-T11 injury level in
comparison with higher lesions indicating that the neural pathway responsible
for vasodilation may be located at or below T10 (132). Despite the increase in
thermal strain, it is interesting to note that Yaggie et al. observed a compensation
for the decreased sweating in regions affected below the level of the SCI by way
of greater perspiration in regions innervated above the injury level (452). In
general, people with tetraplegia have a much greater difficulty regulating
temperature (319). Michael J Price, one of the main contributors to the field of
thermoregulation in SCI explained that “A relationship between the available
muscle mass for heat production and sweating capacity appears evident for the
maintenance of thermal balance. During recovery from exercise, decreases in aural
temperature, Tsk and heat storage were greatest for the able-bodied athletes with
the greatest capacity for heat loss and lowest for the tetraplegic athlete with the
smallest capacity for heat loss” (317).
It is encouraging to note that despite impaired thermoregulation in people who
have SCIs, exercise training has been shown to alleviate the complications. In
44
Introduction
fact, the literature reports a greater capacity for the dissipation of heat in the
trained individuals with SCI (88, 122) compared to those who are not trained.
Moreover, similar increases in core temperature in cool and warm conditions
have been reported in trained low-level paraplegics and able-bodied people
(317), and similar decreases in Tsk from resting values followed by a plateau in
trained paraplegic and able-bodied individuals (88).
Lastly, it is important to highlight the regional Tsk responses experienced by
individuals with SCIs (Figure 12). This population is characterized by cold and
blue lower limbs with cooler thigh and calf Tsk than the rest of the body at rest
(175, 315). Conversely, there are almost no differences in Tsk values between
able-bodied and SCI subjects. Another interesting response observed in people
who have a SCI and associated disrupted sympathetic nervous system is the
increase in calf Tsk during prolonged arm exercise (132, 315-317). This
phenomenon has been attributed to heat storage within the lower body (315318), and for this reason Price et al. concluded that cooling the lower body
during arm exercise in hot conditions is more effective in reducing physiological
and thermal strain than cooling the upper body (320). The greater heat storage
in the lower body results in a reduced ability to lower the core temperature of
SCI during recovery periods (434), however this increase in thigh and calf Tsk is
necessary to stabilize the active upper body. These observations should be
considered when evaluating Tsk in SCI subjects with IRT.
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Isabel Rossignoli 2015
Figure 12. Thigh, Calf, Forearm, and Upper Arm skin temperatures for able-bodied
(AB), paraplegic (PA), and tetraplegic (TP) athletes during prolonged exercise and
recovery in warm conditions. From Price (317)
46
Introduction
1.5 PHYSICAL ACTIVITY IN WHEELCHAIR USERS
The literature generally agrees on the positive influence of physical exercise on
WCUs, specifically in people with SCI (115, 279). Amongst this population,
individuals actively involved in sports have higher employment rates than those
who are physically inactive, and physical activity has been identified as the
principal determinant of quality of life (18, 385). Recreational and therapeutic
exercise has been found to improve the physical and emotional wellbeing of
participants with SCI (279). Moreover, quality of life is closely related with
independent living, and it is a crucial outcome when evaluating the success of
rehabilitation (288). In a 9-month randomized control trial study, exercisers
reported greater quality of life and less stress and pain than non-exercisers; the
study highlighted the need to continue exercise adherence to maintain these
positive effects (98). Another study with paraplegics revealed the positive effects
of an exercise programme using a seated double-poling ergometer in reducing
musculoskeletal and neuropathic pain (291).
Pain is the first indication of an overload injury and, as it increases, the WCU
reduces their performance of daily life activities, resulting in a reduction of their
physical capacity and a subsequent increment of the overloading risk (348).
Therefore, it seems obvious to prescribe exercise to wheelchair-dependent
individuals. In a cross-sectional and longitudinal survey, it was found that the
shoulder was the most frequently reported site of pain (195). More recent
studies have indicated that lower quality of life and physical activity scores are
significantly related to higher levels of shoulder pain (154) and vice versa (63,
210). The majority of studies concur in indicating that the longer the duration of
injury and the older the wheelchair users are, the higher the shoulder pain.
Quadriplegics are also reported to have more shoulder pain than people with
paraplegia, as are women compared to men.
The literature is, to this point, inconclusive regarding the effect of physical
activity on shoulder pain. Some authors assert that the shoulder pain does not
increase or decrease with sports (120), while other authors argue that shoulder
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Isabel Rossignoli 2015
pain decreases with exercise (83, 85, 128, 277, 395, 450), and one study found
slightly higher shoulder pain in those using a powered-wheelchair than those in
manual-wheelchairs (190). On the other hand, some studies support the ‘overuse
theory’ described by Wing et al. (447), where a greater number of injuries have
been associated with an increase in sports participation, particularly overhead
sports (8); a larger number of training hours per week (79); a higher level of
wheelchair activity (225, 229); and musculoskeletal overuse (32, 284). One
study reported simply that wheelchair sports generate shoulder pain (389).
There are a number of studies that have addressed the incidence of shoulder
pain and/or shoulder injuries with various modes of physical activity. An
investigation of wheelchair rugby players (mostly quadriplegics) found an
adductor strength deficit linked to shoulder pain, probably due to the level of the
SCI, in contrast to the common weak abductors in able-bodied athletes (269). An
interesting study analyzed five wheelchair-based circuit resistance-training
(CRT) exercises (overhead press, lat pull-down, chest press, row and rickshaw)
and how they placed the shoulder at risk for subacromial mechanical
impingement. The rickshaw was shown to be the most dangerous exercise with
respect to this type of injury (329). Similarly, Nash et al. examined the effects of a
CRT on muscle strength, endurance, anaerobic power, and shoulder pain in
middle-aged men with paraplegia. They concluded that CRT improves muscle
strength, endurance, and anaerobic power of the paraplegia sample while
significantly reducing their shoulder pain (280). Conversely, a primary fitness
program using arm crank ergometry had no effect on shoulder pain in 23 SCI
WCUs (102), possibly because of the less harmful type of wheelchair exercise.
Hettinga et al. presented functional electrical stimulation (FES) as an alternative
to increase the upper body muscle mass to avoid the risk of shoulder overuse
injury. In this review, the benefits of three FES modalities were shown, including
FES-assisted cycling, FES-cycling combined with arm cranking (FES-hybrid
exercise) and FES-rowing; all have been suggested as candidates for
cardiovascular training in SCI (166). Burnham et al. compared paraplegic
athletes, 26% of whom had rotator cuff impingement syndrome, whith healthy
athletes. Stronger shoulders in all directions were shown for the paraplegic
48
Introduction
group, as well as a higher strength ratio of shoulder abduction:adduction (53).
Shoulder pain intensity was inversely related to physical activity in a study with
80 WCUs with shoulder pain (154). In this study, women reported higher levels
of shoulder pain, but men and women had similar levels of physical activity. The
same inverse correlation was found by Fullerton et al. (128). While Wylie et al.
reported that moderate joint activity protected shoulders from degeneration
after finding 45% of inactive paraplegics with degenerative changes in
comparison with 18% of the actives; an interview to 88 individuals with thoracic
SCI found shoulder pain in 47% of the wheelchair athletes compared to 33% of
the sedentary WCUs (11). Taken together, these studies show that, according to
literature, the effect of exercise in WCUs is yet unclear. The comparison of results
between the studies is difficult due to a lack of standardization and consensus
with respect to the technologies and methodologies applied. Added to this are
relatively small sample sizes and large inter-individual variations that limit the
application of the results.
49
Isabel Rossignoli 2015
1.6 OUTLINE OF THE PRESENT THESIS
This review of literature identified that injuries to the shoulder are particularly
prevalent in people who use wheelchairs. The propulsion activity for ambulation
in handrim wheelchair activity itself causes muscle imbalances and
complications due to overloading of the upper limbs. However, it is not clear
whether sedentariness prevents shoulder injuries or whether shoulder pain
impedes sedentary WCUs from participating in physical activity and sports.
Some studies support a protective role for physical activity in the shoulder joint,
precluding degeneration of the involved structures. Given the positive outcomes
associated with habitual physical activity for people with SCIs, including
improvements in health, functional ability, quality of life and vocational
opportunities (115), as well as the higher rates and earlier onset of
cardiovascular diseases in this population, preventive strategies for shoulder
pain and shoulder injuries must be developed. Some of the solutions that require
further investigation are the development of educational programs teaching
alternative techniques for transfers and other daily activities, training endurance
capacity, optimizing posture, stretching and strengthening the upper limbs and
individualised fitting of the wheelchair to its user. Another solution that is of
particular interest to the current thesis is the adoption of injury prevention
strategies for the early identification of shoulder pain and injury risk factors in
WCUs. Infrared thermography may be a useful tool for this early-identification
process. This technique’s advantage, and the primary reason for its selection in
the present work, is that non-invasive. Although its application is promising in
this regard, it is important to bear in mind that IRT is not a diagnostic tool. Yet,
encouragingly, IRT allows for the detection of changes in skin temperature that
may be an indication of inflammatory responses contributing to injury
processes. Before its use in WCUs, it is necessary to measure the reliability of the
thermal
imaging
camera
in
this
population,
especially
given
the
thermoregulatory particularities of people with SCIs. Therefore, the first study of
the present thesis is an investigation of the reliability of the IRT in WCUs. The
aim of the second study is to ascertain the resting thermal profiles of wheelchair
athletes and nonathletes in regions that are involved in their ambulation and
50
Introduction
that are related to shoulder pain. The final study examines the thermal pattern of
wheelchair athletes after a 30 second maximal intensity wheelchair propulsion
test. Given that there is little agreement in the literature about the benefits or
harm to the shoulder joint during wheelchair exercise, the aim of the current
thesis is conduct the foundation studies to begin to understand whether
wheelchair exercise increase the load to the shoulder joint, and hence cause
shoulder pain, or will it build a strong and stable joint to propel the wheelchair
without pain.
51
Isabel Rossignoli 2015
52
Objectives
2 OBJECTIVES
2.1 STUDY 1
- To examine the reliability of infrared thermography in wheelchair users.
2.2 STUDY 2
- To compare the temperature profile of athletic and nonathletic
wheelchair users.
- To differentiate the shoulder pain of athletic and nonathletic wheelchair
user.
- To relate shoulder pain with upper body skin temperature in wheelchair
athletes and nonathletes.
2.3 STUDY 3
- To analyse the skin temperature measured by infrared thermography
before and after a maximal wheelchair propulsion test in athletes.
- To evaluate the relationship between shoulder pain and skin temperature
after a wheelchair propulsion test.
- To analyze the relationship of the shoulder pain with the kinematic
variables of the wheelchair propulsion test.
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Isabel Rossignoli 2015
3 MATERIAL AND METHODS
3.1 STUDY DESIGN
We designed a reliability study to analyse the IRT in WCUs, and an observational
and descriptive study (cross-sectional or transversal) to analyse the relation of
Tsk and shoulder pain in different groups of WCUs: athletes and nonathletes. It
was a test retest reliability design.
During one month, the same researcher visited the rehabilitation center where
the nonathletic WCUs received treatment (the Rehabilitation Center of ASPAYM
Castilla y León) or the sport facilities where the athletic WCUs trained (in
Valladolid and Palencia) to perform thermographic analysis in basal state on two
consecutive days to each subject, with the objective to analyse the IRT technique.
In those days two physical activity questionnaires specific for people with
disabilities were distributed, including The Physical Activity and Disability
Survey (PADS) (331) and The Physical Activity Scale for Individuals with
Physical Disabilities (PASIPD) (440). Posteriorly, all subjects attended one
session at the laboratory of the Research Centre for Physical Disabilities (CIDIF)
to be evaluated on the following battery of tests: a shoulder pain questionnaire
(the Wheelchair Users Shoulder Pain Index or WUSPI); a wheelchair propulsion
test (T-CIDIF) (261); and two additional thermograms taken before, one minute
after and ten minutes after the T-CIDIF. The section 3.5 details each of those
measures. Experiments were performed on their own daily wheelchair.
3.2 SAMPLE
A total of 54 manual WCUs participated voluntarily in the initial data collection
of this thesis (Table 2). From the 32 nonathletic WCUs, 15 were male (age:
45.1±12.2 years; height: 177±0.09 cm; weight: 76.7±10.2 kg; IMC: 24.4±3.1 kg·m2)
and 17 female (age: 42.4±10.5 years; height: 161±0.05 cm; weight: 56.4±10.3
54
Material & Methods
kg; IMC: 21.7±4.1 kg·m-2). The 22 male wheelchair athletes belonged to the
wheelchair basketball teams: Fundación Grupo Norte from Valladolid and
Minusválidos Unidos por la Integración (MUPLI) from Palencia. The season of the
data collection (2009-2010), the Fundación Grupo Norte team was the winner of
the “European Cup Willi Brinkmann”; second position in the European League;
third position in the “Copa de S.M. El Rey”; and fourth position in the Spanish
League honour division as well as champion of fourth different Spanish
tournaments; being champion of the Spanish League in the following season.
MUPLI team competed in first division and trained 2 hours 3 days per week, vs.
the 2 hours and 6 days per week of the Fundación Grupo Norte team.
Table 2. Number of subjects per group
Lesion
Sport
Sex
Paraplegic Tetraplegic Others Total
Nonathlete Men
Women
Total
1
Athlete A
Men
Total
Athlete B2 Men
Total
6
10
16
1
1
10
10
5
1
6
4
6
10
10
10
1
1
All
1 Athletes
2 Athletes
15
17
32
11
11
11
11
54
that use the wheelchair only for sport
that use the wheelchair for sport and daily live
3.2.1 Ethics norms followed in this study
Prior to the investigation, subjects were fully familiarized with testing
procedures and informed about the risks and benefits of the study, and signed an
institutionally approved informed consent document. The protocol was
approved by the Ethics Committee of the Technical University of Madrid
following the principles outlined by the World Medical Declaration of Helsinki
(445). Moreover, all procedures used in this study conformed to the Spanish law
for Protection of Personal Data 15/1999.
55
Isabel Rossignoli 2015
3.2.2 Inclusion and exclusion criteria
All participants have propelled their own manual wheelchair for at least one
year, and use a wheelchair for at least 50% of home and community mobility. In
addition, they must be over 18 years old. Subjects were classified as athletes if
they were involved in organized, competitive wheelchair sports of recreational
to elite levels of competition, had participated in at least three competitions per
year and if they trained at least 3 h·wk-1 (120). The vast majority of athletes
involved in the study, being at an elite level of competition, far exceeded these
requirements.
3.2.3 Demographic data of the studies 1 and 2
In the first and second studies, experimental data were collected from 24
experienced manual WCUs, 22 men and 2 women. 19 were manual wheelchair
dependent and 5 were wheelchair independent (use of wheelchair only to
practice sport), 14 were subjects with paraplegia, 3 with tetraplegia and 7
presented other disabilities (amputation, multiple sclerosis, and poliomyelitis).
From all, 13 were nonathletes (11 males and two females) and 11 were male
athletes. Table 2 summarizes the number of subjects that belongs to each group
and Table 3 the main characteristics of the sample.
Table 3. Group subject characteristics from studies 1 and 2 expressed by
mean±Standard Deviation
Sport
Nonathletes
Athletes
All
Gender n
Age (yr)
Height (cm) BMI (kg·m-2)
Male
11 45.1±11.6 177.6±9.1
Female 2 44.5±3.5 158.0±1.4
Male
11 32.3±6.4 173.4±8.7
23.2±2.5
25.9±5.3
24.7±3.8
24 39.2±10.9 174.0±9.9
24.1±3.3
n, number of subjects; BMI, body mass index.
56
Material & Methods
3.2.4 Demographic data of the study 3
Twelve male wheelchair athletes (age: 32.58±6.16 years; height: 173.58±8.34
cm; body mass: 74.24±12.73 kg; body mass index: 24.61±3.66 kg/m2) recruited
from the elite and the recreational wheelchair basketball teams, volunteered to
participate in this study.
3.3 EQUIPMENT
3.3.1 Material for the thermographic evaluation
The three studies used the same common instruments for the IRT analysis.
Infrared thermal imaging of the upper extremities and the trunk were recorded
using a thermal camera (FLIR T335, FLIR® Systems, Danderyd, Sweden), with a
thermal sensitivity of 50 mK, an object temperature range from -20°C to +120°C,
a length spectrum range of 7.5-13 μm, an infrared spectral band of 320 x 240
pixels FPA (Focal Plane Array), a IR resolution of 320 x 240 pixels and an
accuracy of ±2% or 2% of the measurement (Figure 13). The temperature data
was extracted and the IRT images were analyzed with specific software
(ThermaCAM Reporter, version 8, FLIR® Systems, Danderyd, Sweden).
Figure 13. IRT camera T335 (FLIR® Systems, Sweden)
57
Isabel Rossignoli 2015
The camera was calibrated before each trial using an external temperature
reference source (thermistor PT-100, Telemeter Electronic®, Donauworth,
Germany) and was turn on 20’ before to avoid calibration problems. The wall
behind body figures was covered with a white “Roll-up” 125x206 cm (in the
study 1 and 2) and a black background (in the study 3) to create a homogeneous
background behind body figures and to avoid any kind of reflection or radiation
emitted by other objects. A fixed area of the black background was taken as the
reference temperature. Images were obtained assuming skin emissivity of 0.98
(383). A tripod Hama Omega Premium II (Hama®, Monheim, Germany) was
used to hold the camera during the data collection. The environmental
conditions in the testing room were monitored by a portable weather station
(BAR-908-HG® model, Oregon Scientific®, USA). The table 4 shows the
characteristics of this weather station.
Table 4. General characteristics of the weather station, model BAR-908-HG®
(Oregon Scientific, Portland, Oregon)
Characteristics of the portable weather station
Weight
370 grams.
Dimensions
188 x 120 x 86 mm. (height x width x depth
Temperature
Interior (-5 / + 50%)
Humidity
Interior and exterior (25 – 95%)
Atmospheric pressure
Numeric value; 500 – 1050 mb/hPa.
Resolution
1 mb/hPa
Indicators
Trends and comfort zones
Others
- Evolution charts of the atmospheric pressure in the last 24h
- Weather forecast with symbols
3.3.2 Material for the shoulder pain evaluation
The WUSPI is a questionnaire with a maximum total score of 150 which
integrates a series of visual analogue scales (consisting of 10-cm lines anchored
by ‘no pain’ and ‘worst pain ever experienced’) to provide an accumulated index
of the intensity of shoulder pain suffered during the previous week while
performing 15 different daily activities. Due to individual characteristics, not all
the activities listed on the WUSPI were performed by the subjects in their daily
58
Material & Methods
routines. Consequently, the Performance-Corrected score (PC-WUSPI) was
calculated by dividing the total raw score by the number of activities executed
and multiplied by 15 (80, 83). The WUSPI and the PC-WUSPI has been shown to
be both reliable and valid for people with SCI (82). We used the Spanish version
of this questionnaire validated by Arroyo et al. (23) (see Appendix 4 for the
English version and Appendix 5 for the Spanish version of the WUSPI).
3.3.3 Material for the register of the kinematic variables
The Research Centre for Physical Disability developed a test to analyze the
wheelchair propulsion; it was called the T-CIDIF and has been recently validated
(261) (Figure 14). It correlated well with pain and strength in the shoulder joint
of WCUs.
59
Isabel Rossignoli 2015
Figure 14. Elite wheelchair athlete ready to perform the wheelchair propulsion
test (T-CIDIF)
Each subject placed his wheelchair over two rollers located one meter from a
wall, in which there was a fitness pulley (En-TREEPulley, Enraf-Nonius,
Rotterdam, Holland) and two linear position transducers (Sportmetrics,
Valencia, Spain). Each transducer was attached to the subject’s arm through a
glove. A cable connected each glove with the correspondent pulley to provide
resistance to the movement (Figure 15).
60
Material & Methods
Figure 15. T-CIDIF. Left: detail of the linear position transducers integrated with
the fitness pulley. Right: detail of the gloves fixed to the forearm.
The load of the pulley was selected according to the body mass of each subject
(see Table 5). Kinematic data were collected bilaterally at a registration
frequency of 200Hz. It was obtained the number of propulsions, mean and
maximum peak power, and mean and maximum velocity of each arm.
Table 5. Rolling resistance to overcome depending on the subject's mass
Selected pulley mass Real mass transmitted to the forearm
Subject mass (kg)
(kg)
anchorage* (kg)
< 65
6
1.43
66-75
10
2.57
76-85
14
3.63
86-95
18
4.77
> 96
22
6.2
*Mass calculated trough placing a load cell (KERN HCB 200K100, Kern & Sohn GmbH,
Balingen, Germany) in the cable that is connected to the glove. The pulley system gears
down the initially selected load.
3.4 RESEARCH PERSONNEL
All the tests were carried out by the thermographic specialist, supported by the
technicians from the laboratory of the CIDIF formed of Sport Science experts.
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Isabel Rossignoli 2015
3.5 PROCEDURES
3.5.1 Study 1: Infrared Thermal Imaging
Two thermographic photographs corresponding to the anterior and posterior
upper body were performed over two days with an interval of one day. Skin
temperature of 16 and 20 body areas or ROIs of the front and rear upper body
respectively, were measured using IRT. All images were taken and analyzed by
the same observer. Images were taken with the subject’s own daily wheelchair in
anatomical position. The camera was positioned perpendicular to the ground,
and the distance between the subject and the infrared camera was from 2 m to 3
m, depending on the height of subjects, as the aim was to match the center of the
image with the geometric center of the area to be evaluated. A transparent
template helped the technician on the placement of the camera (Figure 16).
Figure 16. Thermographic analysis of an athlete (left) and a nonathlete (right)
Each image was manually divided into different body areas (Figure 17) based on
previous proposals (13, 147, 406, 407), and on the areas corresponding to the
62
Material & Methods
main muscles involved in the wheelchair propulsion task (341). Uematsu et al.
selected the ROIs coinciding with the dermatomes, which are skin areas
innervated by the major peripheral nerves (407). In this way, it is possible to
associate the ROIs’ data with the corresponding nerves. In our case, we
substitute the squares used by other authors for areas more similar to the real
muscles; it increased the drawing difficulty but gained in accuracy (Figures 17
and Figure 18).
5
1
4
6
13
7
3
2
1
8
12
11
9
10 14
0
15
16
1. Left anterior forearm
2. Flexor of the left elbow
3. Left anterior arm
4. Left anterior shoulder
5. Left anterior trapezius
6. Anterior neck
7. Left pectoral
8. Left side of the abdomen
9. Abdomen
10. Right side of the abdomen
11. Right pectoral
12. Right anterior trapezius
13. Right anterior shoulder
14. Right anterior arm
15. Flexor of the right elbow
16. Right anterior forearm
Figure 17. A total of 16 areas on the front body were studied in the study 1.
Example from a wheelchair athlete
63
Isabel Rossignoli 2015
21
20
22
30
23 29
24
19
32
33
28
25
27
18
17
31
34
35
26
36
17. Left posterior forearm
18. Left elbow
19. Left posterior arm
20. Left posterior shoulder
21. Left posterior trapezius
22. Left supraspinatus
23. Left central posterior
trapezius
24. Left infraspinatus
25. Left dorsal
26. Lumbar
27. Right dorsal
28. Right infraspinatus
29. Right central posterior
trapezius
30. Posterior neck
31. Right posterior trapezius
32. Right infraspinatus
33. Right posterior shoulder
34. Right posterior arm
35. Right elbow
36. Right posterior forearm
Figure 18. A total of 20 areas on the rear body were studied in the study 1.
Example from a wheelchair athlete
Several body areas were eliminated from the analysis: the lumbar area was
hidden by the wheelchair; the abdomen and both flanks were not considered a
relevant muscular area as many subjects with SCIs do not have muscle tone in
that area; elbows and cubital fosses areas are not important for the propulsion of
the wheelchair; the pectoral data of women were discarded due to the influence
of the bra.
64
Material & Methods
The circadian rhythm effect over Tsk (270) was avoided by always testing each
subject at the same hour of the day. During the first session, the subject
responded verbally to a demographic and medical questionnaire. Before every
thermographic examination subjects were instructed to refrain from the
following in the 24 hours before the test: applying creams or perfume, smoking,
drinking alcohol or coffee, sunbathing, showering, receiving treatment, therapy,
massage or undertaking exercise. All subjects postponed their weekly therapies
after the thermographic tests, and they were asked not to push their wheelchairs
before the test more than was strictly necessary. Prior to the assessment,
subjects were asked to remain at rest, without clothes and jewelry on the upper
body for at least 10 minutes before being photographed. This acclimatization
period allowed the subjects’ Tsk to stabilize (332). Every test was performed
under equal conditions and in the same room, in which the temperature was
fixed at 23°C and drafts were eliminated.
3.5.2 Study 2: Infrared Thermal Imaging and The Wheelchair User Shoulder Pain
Index
For the second study, subjects attended one session at the laboratory and two
thermograms corresponding to the anterior and posterior subject’s upper body
were taken. Therefore the basal Tsk was studied in the same day, instead of over
two days such as the study 1. Another difference with the previous protocol was
the number of ROIs studied, which was reduced from 36 to 22 ROIs. In the study
2, Tsk of 8 anterior and 14 posterior ROIs of the upper body were measured,
which were left and right: anterior and posterior Arm, Shoulder, Pectoral,
anterior and posterior Trapezius, Dorsal, Infraspinatus, Supraspinatus, Central
Trapezius. The rest of the procedure remained equal to the precedent data
collection regarding position of the camera, room conditions, instructions to the
subjects, and same researcher performing the tests.
After thermographic examination, each subject completed the Wheelchair User
Shoulder Pain Index (WUSPI).
65
Isabel Rossignoli 2015
3.5.3 Study 3: Infrared Thermal Imaging, The Wheelchair User Shoulder Pain
Index and the wheelchair propulsion test T-CIDIF
The Tsk of the body ROIs was obtained from thermographic images following the
same criteria described by Rossignoli et al. (342). The Tsk analysis included the
following 26 ROIs (left and right): anterior and posterior Arm, anterior and
posterior Shoulder, anterior and posterior Forearm, Pectoral, anterior and
posterior Trapezius, Dorsal, Infraspinatus, Supraspinatus and Central Trapezius.
The ROIs were manually drawn on the basis of previous studies (13, 342, 406,
407). Three sets of 4 thermographs for each subject in anatomical position were
taken and analyzed by the same previously trained observer. Subjects were
instructed to remove clothes and jewelry from their upper body and remain 10
min at rest in a conditioned room (23°C±1.9°C). After the acclimatization period
and before the wheelchair propulsion test, four thermograms were recorded
including two images each (trunk/upper limbs) of the anterior and posterior
sides of the body (pre-test); right after performing the T-CIDIF, the subject
placed his wheelchair in the same location of the previous IRT analysis and
another four thermograms were recorded (post-test); 10 min after the post-test
two new thermograms were taken (post-10) (Figure 19).
The camera was placed perpendicular to the ground, at 2-3 m away from the
subject’s skin to match the center of the image with the geometric center of the
area to be evaluated. A transparent template was affixed to the camera screen to
ensure the correct placement of the camera during the session.
Before the assessment, subjects were instructed to avoid consuming alcohol or
caffeine, using any type of cream or perfume, smoking, sunbathing, showering,
receiving treatment, therapy, massage or performing vigorous exercise in the 24
h preceding the measurements (same instruction than in the studies 1 and 2).
After the basal thermographic data collection, the subjects performed a
maximum wheelchair propulsion test (T-CIDIF) (261). The subject completed a
10 min warm-up period, consisting on 6 min propelling their wheelchair at a
high speed, followed by 4 min of progressions of 20s propelling and 20s resting.
66
Material & Methods
Two minutes after the warm-up period, the subject was asked to propel his
wheelchair as fast as possible during 30s.
Figure 19. Measurements of the study 3. Pre-test, thermographic evaluation
before the wheelchair exercise test; Post-test, thermographic evaluation one
minute after completing the wheelchair exercise test; Post-10, thermographic
evaluation ten minutes after completing the wheelchair exercise test
67
Isabel Rossignoli 2015
3.6 VARIABLES
Table 6 show the dependent, independent and control variables considered in
the studies of this thesis:
Control
Independent
Dependent
Table 6. Variables and their values
Name/Abbreviation
Type
Values
Skin temperature (Tsk)
Continuous (interval)
Celsius degrees (°C)
Asymmetries or side-to-side
skin temperature (ΔTsk)
Shoulder pain questionnaire
(WUSPI and PC-WUSPI)
Number of propulsions
Mean peak torque
Mean power
Maximum velocity
Average maximum velocity
Total work
Age
Height
Body Mass Index
Weight
Continuous (interval)
Celsius degrees (°C)
Continuous (interval)
Pain score (0 to 150
points)
Group
Time
Dichotomous
Ordinal
Regions of interest (ROI)
Body areas
Nominal
Nominal
Room temperature
Continuous (interval)
Humidity
Atmospheric pressure
Continuous (ratio)
Continuous (interval)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
Continuous (ratio)
68
Watt (W)
Watt (W)
(m·s-1)
(m·s-1)
Watt (W)
Years
Cm
Kg/m2
Kg
Athletes / nonathletes
Before exercise (pretest), one minute after
exercise (post-test),
after 10 minutes (post10); day 1 and day 2
ROI (left and right)
ROI (right minus left)
Celsius degrees (°C)
%
Mb/hPa
Material & Methods
3.7 STATISTICAL ANALYSIS
The statistical treatment of data was performed using SPSS 19.0 software for
Windows (SPSS Inc., Chicago, IL, USA). The level of significance was always set at
α ≤ .05 for all statistical analyses. The specific calculations for each section are
described in the following points.
3.7.1 Study 1
After applying the Kolmogorov-Smirnov tests with the Lilliefors correction,
asymmetry and kurtosis, ±1 and ±2 respectively (58, 247), the normality of the
dependent variables was verified and parametric statistics were therefore
applied.
Intraclass Correlation Coefficient (ICC) was used to analyze the reliability and
Coefficient of Variation (CV) (SD*100/mean) to analyze the dispersion data. ICC
was characterized as follows (69): Poor reproducibility: 0–0.39, Fair
reproducibility:
0.40–0.59,
Good
reproducibility:
0.60–0.74,
Excellent
reproducibility: 0.75–1.0. Descriptive statistics were used (mean ± SD) to
describe, organize and summarize the data for the number of assessments (day 1
and day 2). Side-to-side skin temperature differences (ΔTsk) were calculated for
each area by subtracting the mean temperature of the maximum values of the
right side from that of the left side. The minimum difference was calculated for
all the body areas to study the relevancy of day-to-day Tsk. Student-T Test for
related samples was used to ascertain whether there were any differences across
the two measures.
3.7.2 Study 2
The bilateral skin temperature difference (ΔTsk) was calculated by subtracting
the temperature of the right side from that of the left side. The normality of the
thermographic values was analysed with the Shapiro-Wilk test. If normality was
assumed, the independent student t test was used to compare thermographic
69
Isabel Rossignoli 2015
values between nonathletic and athletic subjects. If normality was not assumed,
the U Mann-Whitney test was used for this comparison. The comparison
between athletes and nonathletes in relation with WUSPI and PC-WUSPI was
done with the U Mann-Whitney test. The relation between thermographic values
and WUSPI or PC-WUSPI was analysed with the Spearman rho. Thermographic
values are expressed as mean ± Standard Deviation and WUSPI and PC-WUSPI
values are expressed as median ± Interquartile Range.
3.7.3 Study 3
The interside temperature difference (ΔTsk) was calculated for each ROI by
subtracting the temperature of the right side from that of the left side. Bilateral
ΔTsk more than 0.5°C was considered abnormal (54).
The normality of the thermographic values and the variables obtained in the TCIDIF was tested with the Shapiro-Wilk tests. If normality was assumed, the
repeated measures ANOVA test was used to compare the absolute levels of ΔTsk
before (pre), after one minute (post1) and after 10 minutes (post-10) the TCIDIF. The post hoc applied was the least significant difference, due to the
reduced number of participants. If normality was not assumed, the Friedman’s
test with the Bonferroni procedure was applied for this comparison.
The relations between the T-CIDIF variables and WUSPI or PC-WUSPI, likewise
between thermographic values and WUSPI or PC-WUSPI, were analysed with the
Spearman rho, since WUSPI or PC-WUSPI are ordinal variables. The correlation
between thermographic values and T-CIDIF variables was analysed with the
Spearman rho coefficient.
70
Results
4 RESULTS
4.1 STUDY 1: RELIABILITY OF INFRARED THERMOGRAPHY IN SKIN
TEMPERATURE EVALUATION OF WHEELCHAIR USERS
4.1.1 Reliability of measurements
A total of 1728 images for the trunk and upper extremities were recorded from
24 subjects. By comparing the assessment of day 1 and day 2 for the temperature
profile, no significant differences were observed in any of the 36 zones, or in the
mean or maximum values. The only differences were observed in the average Tsk
of the right posterior arm (P=0.041), with a difference of 2.05°C between day 1
and day 2.
The best maximum Tsk values of ICC were found in the left anterior forearm,
right posterior forearm, left posterior arm and left anterior trapezius, with 0.76,
0.77, 0.77, 0.79, respectively (see Table 7).
For the average values the highest ICC was the following: left posterior forearm,
0.80; right posterior arm, 0.88; right dorsal, 0.79; right pectoral, 0.95; left
supraspinatus, 0.76 (see Table 8). Some zones presented a poor reproducibility:
right anterior forearm, 0.22; left anterior forearm, 0.24; left anterior arm, 0.18;
left posterior arm, 0.23; left anterior shoulder, 0.15; left pectoral, 0.39; left
posterior trapezius, 0.38. Hence, IRT in WCUs showed a poor to excellent
reliability for the left posterior arm and right posterior arm (ICC= 0.15 and 0.95,
respectively). For a graphical view of the day-to-day analysis of reliability see
Figure 20.
71
Isabel Rossignoli 2015
Table 7. Descriptive maximum values of the skin temperature profile on day 1,
day 2 and between both the assessments of the analyzed area
Day 1
Day 2
Day 1 and 2
ROIs
Mean ± SD
Mean ± SD
CV
ICC
Scale
R A Forearm
L A Forearm
R A Arm
L A Arm
A Neck
R A Shoulder
L A Shoulder
R Pectoral
L Pectoral
R A Trapezius
L A Trapezius
R P Forearm
L P Forearm
R P Arm
R P Arm
P Neck
R Dorsal
L Dorsal
R P Shoulder
L P Shoulder
R P Infraspinatus
L P Infraspinatus
R P Supraspinatus
L P Supraspinatus
R P Central Trapezius
L P Central Trapezius
R P Trapezius
L P Trapezius
33.31 ± 1.36
33.10 ± 1.17
33.96 ± 0.75
33.50 ± 0.72
33.67 ± 0.84
34.15 ± 0.65
33.90 ± 0.72
34.29 ± 0.62
34.19 ± 0.61
34.12 ± 0.71
33.91 ± 1.01
32.94 ± 1.53
33.06 ± 1.68
32.63 ± 0.83
32.55 ± 1.28
33.54 ± 0.76
33.01 ± 0.99
33.01 ± 0.69
32.81 ± 1.09
33.17 ± 0.72
33.14 ± 0.88
33.27 ± 0.86
33.27 ± 0.75
33.45 ± 0.82
33.85 ± 0.77
33.72 ± 0.89
33.58 ± 0.79
33.61 ± 0.92
33.38 ± 1.16
33.00 ± 1.13
33.97 ± 0.99
33.53 ± 0.92
33.79 ± 0.77
34.21 ± 0.83
33.85 ± 1.19
34.39 ± 0.83
34.24 ± 1.00
33.93 ± 1.36
33.98 ± 1.17
33.15 ± 1.65
33.20 ± 1.47
32.90 ± 1.04
32.69 ± 1.20
33.61 ± 0.91
33.07 ± 1.22
33.10 ± 1.20
32.70 ± 1.73
33.24 ± 1.03
33.35 ± 1.22
33.42 ± 1.15
33.47 ± 0.99
33.53 ± 1.05
33.91 ± 0.95
33.75 ± 1.01
33.62 ± 1.01
33.61 ± 1.03
Total X
1.56
1.23
1.36
1.14
1.13
1.17
1.51
1.05
1.5
1.5
1.12
1.54
1.8
1.62
1.44
1.31
1.57
1.51
2.04
1.41
1.44
1.47
1.27
1.37
1.47
1.49
1.26
1.48
0.6
0.76
0.52
0.58
0.56
0.52
0.49
0.59
0.39
0.53
0.79
0.77
0.69
0.46
0.77
0.53
0.59
0.54
0.6
0.54
0.67
0.6
0.65
0.59
0.49
0.52
0.64
0.58
Good
Excellent
Fair
Fair
Fair
Fair
Fair
Fair
Poor
Fair
Excellent
Excellent
Good
Fair
Excellent
Fair
Fair
Fair
Good
Fair
Good
Good
Good
Fair
Fair
Fair
Good
Fair
1.42
0.59
Fair
Abbreviations: CV, coefficient of variation; ICC, coefficient of intraclass correlation;
Scale, scale of reproducibility of Cicchetti (1981); X, average. ROI, Regions of interest. L,
left side. R, right side. A, anterior. P, posterior.
The CV between day 1 and day 2 ranged between 1.05% (right pectoral
maximum values) and 6.18% (left posterior trapezius average values). Table 7
shows the variability and the reliability of each variable (maximum values) and
Table 8 presents the same descriptive values for variables that describe average
72
Results
Tsk values. The mean of the average values of all the areas studied was:
31.83±2.04; CV, 2.80%; ICC, 0.56, with a ΔTsk between day 1 and 2 of 0.08°C. The
analysis of the main body areas (see Table 9) allows appreciating a lower Tsk in
the limbs (31.63±1.97) than in the trunk (31.98±1.79), and a lower Tsk in the
distal extremities (forearms colder than arms, arms colder than shoulders).
Figure 20. Day-to-day analysis of the reliability in all body areas measured
73
Isabel Rossignoli 2015
Table 8. Descriptive average values of the temperature profile on day 1, day 2 and
between both the assessments for each analyzed area
Day 1
Day 2
Day 1 and 2
ROIs
Mean ± SD
Mean ± SD
CV
ICC
Scale
R A Forearm
L A Forearm
R A Arm
L A Arm
A Neck
R A Shoulder
L A Shoulder
R Pectoral
L Pectoral
R A Trapezius
L A Trapezius
R P Forearm
L P Forearm
R P Arm
R P Arm
P Neck
R Dorsal
L Dorsal
R P Shoulder
L P Shoulder
R P Infraspinatus
L P Infraspinatus
R P Supraspinatus
L P Supraspinatus
R P Central Trapezius
L P Central Trapezius
R P Trapezius
L P Trapezius
31.26 ± 2.54
31.28 ± 2.63
32.42 ± 0.96
30.93 ± 4.20
32.44 ± 1.21
33.09 ± 0.87
33.01 ± 0.80
31.14 ± 2.91
31.99 ± 1.57
32.54 ± 3.00
30.65 ± 5.51
31.04 ± 3.62
30.95 ± 3.91
29.21 ± 4.35
29.89 ± 3.12
32.53 ± 0.91
30.98 ± 3.62
31.27 ± 1.82
31.13 ± 2.92
32.12 ± 0.83
32.28 ± 1.10
32.48 ± 0.91
32.64 ± 0.92
32.15 ± 1.91
31.90 ± 1.95
32.79 ± 0.86
32.92 ± 0.83
31.57 ± 3.96
31.40 ± 2.35
31.19 ± 2.45
32.19 ± 1.25
32.19 ± 1.15
32.84 ± 1.21
33.24 ± 0.96
32.10 ± 3.94
31.47 ± 2.89
31.91 ± 2.06
31.29 ± 5.13
31.08 ± 5.49
31.55 ± 2.72
30.95 ± 3.68
31.25 ± 1.35
30.44 ± 2.49
32.73 ± 1.05
30.28 ± 4.13
31.22 ± 2.43
29.97 ± 4.91
32.11 ± 1.16
32.48 ± 1.29
32.60 ± 1.21
32.89 ± 1.13
31.95 ± 2.48
32.12 ± 2.14
32.92 ± 1.16
32.90 ± 1.10
31.43 ± 4.06
Total X
3.56
3.65
1.58
3.14
1.63
1.45
4.14
1.61
2.39
4.66
4.84
2.74
2.48
1.38
5.17
1.59
3.59
3.16
5.14
1.66
2.01
1.65
1.34
2.23
2.06
1.79
1.47
6.18
0.24
0.24
0.57
0.18
0.67
0.56
0.15
0.95
0.62
0.6
0.69
0.66
0.8
0.88
0.23
0.46
0.79
0.5
0.58
0.51
0.51
0.55
0.68
0.76
0.73
0.47
0.63
0.38
Poor
Poor
Fair
Poor
Good
Fair
Poor
Excellent
Good
Good
Good
Good
Excellent
Excellent
Poor
Fair
Excellent
Fair
Fair
Fair
Fair
Fair
Good
Excellent
Good
Fair
Good
Poor
2.80
0.56
Fair
Abbreviations: CV, coefficient of variation; ICC, coefficient of intraclass correlation;
Scale, scale of reproducibility of Cicchetti (1981); X, average. ROI, Regions of interest.
L, left side. R, right side. A, anterior. P, posterior.
The maximum Tsk values were taken as references to calculate the ΔTsk between
symmetrical sides of the body. Table 10 shows the absolute values of mean±SD;
the first and second columns are referred as ΔTsk between both sides of the body
on day 1 and day 2, respectively; the third column is related to ΔTsk between the
74
Results
days. The ΔTsk did not show any consistent pattern related to the handedness of
the subjects.
Table 9. Interrater-reliability measures in terms of ICC and CV organized by
general areas
Average values
Maximum values
Body areas
Mean±SD
CV
ICC
CV
ICC
Arm
31.32±2.09
2.96
0.48
1.46
0.64
Shoulder
32.10±1.86
3.10
0.45
1.53
0.54
Trapezius
31.80±3.25
4.29
0.57
1.34
0.63
Pectoral
31.63±2.26
2.00
0.79
1.28
0.49
Back
32.07±1.67
2.23
0.62
1.45
0.58
Neck
32.63±0.97
1.61
0.56
1.22
0.54
Abbreviations: CV, coefficient of variation; ICC, coefficient of intraclass correlation.
Table 10. Mean maximal values of regional skin temperature °C (±) standard
deviations and absolute values of the side-to-side differences (ΔTsk) for the
different skin areas of the study subjects. Results of Student’s t-test for the two
measures
ΔTsk Day 1 ΔTsk Day 2
ΔTsk between days
Body areas
r
P
Mean±SD
Mean±SD
Mean±SD
P
A forearm
A arm
A shoulder
Pectoral
A trapezius
P forearm
P arm
Dorsal
P shoulder
Infraspinatus
Supraspinatus
P central Trapezius
P trapezius
0.12 ± 0.66
0.42 ± 0.41
0.24 ± 0.30
0.13 ± 0.29
0.18 ± 0.72
0.05 ± 0.61
0.17 ± 0.78
0.00 ± 0.48
0.40 ± 1.06
0.13 ± 0.47
0.18 ± 0.48
0.12 ± 0.33
0.08 ± 0.29
0.39 ± 0.65
0.35 ± 0.49
0.16 ± 0.29
0.07 ± 0.38
0.01 ± 0.28
0.05 ± 0.59
0.22 ± 0.74
0.03 ± 0.36
0.31 ± 1.07
0.07 ± 0.50
0.06 ± 0.43
0.12 ± 0.30
0.07 ± 0.33
0.27 ± 0.75
0.07 ± 0.43
0.08 ± 0.20
0.06 ± 0.27
0.17 ± 0.74
0.01 ± 0.53
0.05 ± 0.72
0.03 ± 0.42
0.09 ± 0.35
0.06 ± 0.29
0.12 ± 0.38
0.02 ± 0.25
0.15 ± 0.38
Total X
0.17 ± 0.53
0.15 ± 0.49
0.09 ± 0.44
0.117
0.479
0.081
0.287
0.283
0.969
0.752
0.737
0.237
0.335
0.137
0.745
0.078
0.352
0.540
0.778
0.703
0.146
0.609
0.553
0.536
0.946
0.821
0.648
0.679
0.269
0.583
Abbreviations: A, anterior; P, posterior; r, Pearson correlation coefficient; X, average.
NOTE: Diagnostic accuracy of IRT using thermographic asymmetry.
*P<0.05.
†P<0.001.
75
0.118
0.008*
0.001†
0.001†
0.517
0.003*
0.006*
0.007*
0.001†
0.001†
0.001*
0.001†
0.226
Isabel Rossignoli 2015
4.2 STUDY 2: RELATIONSHIP BETWEEN PERCEIVED SHOULDER PAIN AND
INFRARED THERMOGRAPHY IN WHEELCHAIR ATHLETES AND
NONATHLETES
4.2.1
Comparison of thermography values in nonathletic and athletic subjects
The analysis of the maximum Tsk values in nonathletes and athletes ranged from
32.13±1.84 to 34.07±0.90°C and from 31.89±0.69 to 33.69±0.60°C, respectively.
No statistical difference was observed between both groups for any ROI (Table
11).
Table 11. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the maximum basal values registered in ROIs. It is
showed the values of each body side (right vs. left) for each ROI
ROIs
Nonathletes
Athletes
R A Arm
L A Arm
R A Shoulder
L A Shoulder
R Pectoral
L Pectoral
R A Trapezius
L A Trapezius
R P Arm
L P Arm
R Dorsal
L Dorsal
R P Shoulder
L P Shoulder
R P Infraspinatus
L P Infraspinatus
R P Supraspinatus
L P Supraspinatus
R P Central Trapezius
L P Central Trapezius
R P Trapezius
L P Trapezius
33.45
33.15
34.02
33.54
34.07
33.95
33.55
33.60
32.35
32.40
32.58
32.70
32.13
32.78
32.54
32.92
32.62
32.83
33.17
32.93
32.98
32.92
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.87
0.99
0.96
1.47
0.90
0.95
1.09
1.36
1.02
1.18
1.47
1.30
1.84
1.47
1.36
1.49
1.33
1.56
1.42
1.43
1.35
1.35
33.41
32.88
33.43
32.97
33.49
33.46
33.69
33.56
31.89
32.12
32.27
32.36
32.06
32.41
32.05
32.38
32.30
32.53
33.10
33.17
32.94
33.07
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.63
0.75
0.74
0.81
0.89
0.90
0.60
0.66
0.69
0.77
1.12
1.19
1.00
0.95
1.16
1.13
1.06
0.91
1.06
0.98
0.96
0.84
Total X ROI
33.05
±
1.28
32.80 ±
0.90
P
Dif.
0.888
0.476
0.107
0.268
0.129
0.209
0.701
0.933
0.226
0.510
0.594
0.542
0.923
0.481
0.373
0.353
0.537
0.587
0.900
0.637
0.925
0.746
-0.13%
-0.83%
-1.77%
-1.70%
-1.71%
-1.45%
0.41%
-0.11%
-1.43%
-0.87%
-0.95%
-1.03%
-0.19%
-1.15%
-1.52%
-1.64%
-0.98%
-0.91%
-0.20%
0.75%
-0.14%
0.47%
Dif. = Difference between both groups calculated as: ([athletes-nonathletes / (athletes
+ nonathletes) / 2]·100%)
R, right; L, left; A, anterior; P, posterior; X, average.
76
Results
The analysis of the average Tsk values in nonathletes and athletes ranged from
30.13±2.89 to 33.43±1.08°C and from 29.93±0.80 to 32.77±0.76°C, respectively.
No statistical difference was observed between both groups for any ROI (Table
12).
Table 12. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the average basal values registered in the ROI. It is
showed the values of each body side (right vs. left) for each ROI
ROIs
Nonathletes
Athletes
R A Arm
L A Arm
R A Shoulder
L A Shoulder
R Pectoral
L Pectoral
R A Trapezius
L A Trapezius
R P Arm
L P Arm
R Dorsal
L Dorsal
R P Shoulder
L P Shoulder
R P Infraspinatus
L P Infraspinatus
R P Supraspinatus
L P Supraspinatus
R P Central Trapezius
L P Central Trapezius
R P Trapezius
L P Trapezius
31.63
31.61
32.98
32.80
30.84
31.30
33.29
33.43
30.59
30.20
31.71
30.13
31.69
31.78
31.99
32.34
32.08
32.36
31.12
32.27
32.37
32.44
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
1.42
0.78
1.14
1.42
3.39
2.40
0.86
1.08
1.24
0.99
1.67
2.89
1.53
1.50
1.44
1.46
1.45
1.70
2.49
1.40
1.49
1.63
31.58
31.68
32.56
32.25
30.89
31.23
32.77
32.72
29.93
30.06
30.97
31.08
31.08
31.31
30.89
31.48
31.65
31.87
31.23
31.93
32.29
32.35
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
1.12
0.96
0.74
0.79
1.97
1.10
0.76
0.77
0.80
0.81
1.12
1.08
1.07
1.01
1.15
1.21
1.09
1.06
1.33
0.92
0.99
0.96
Total X ROI
31.86
±
1.61
31.54
±
1.04
P
0.927
0.854
0.314
0.290
0.964
0.931
0.192
0.107
0.158
0.732
0.261
0.347
0.302
0.388
0.062
0.151
0.425
0.449
0.895
0.502
0.888
0.891
Dif.
-0.15%
0.22%
-1.26%
-1.69%
0.17%
-0.21%
-1.58%
-2.15%
-2.19%
-0.45%
-2.36%
3.11%
-1.94%
-1.50%
-3.50%
-2.68%
-1.37%
-1.52%
0.35%
-1.08%
-0.23%
-0.26%
Dif. = Difference between both groups calculated as: ([athletes-nonathletes / (athletes
+ nonathletes) / 2]·100%)
R, right; L, left; A, anterior; P, posterior; X, average.
The Figure 21 and Figure 22 represents the mean and standard deviation of the
average and maximum basal temperature values, Tsk and ΔTsk respectively, in all
ROIs. A ΔTsk of 0.5°C was considered the threshold for abnormal asymmetries.
77
Isabel Rossignoli 2015
34.5
Nonathetes
Temperature (ºC)
34
Athletes
33.5
33
32.5
32
31.5
31
30.5
30
Tsk maximum
Tsk average
Figure 21. Mean and standard deviation of the average and maximum basal skin
temperature (Tsk) values
Nonathetes
Asymmetries (ºC)
1.5
Athletes
1
0.5
0
ΔTsk maximum
ΔTsk average
Figure 22. Mean and standard deviation of the average and maximum basal sideto-side skin temperature (ΔTsk) values
The side-to-side differences of maximum and average values in nonathletes and
athletes are presented in Tables 13 and 14. No statistical difference was
observed between both groups for any body area.
78
Results
Table 13. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the side-to-side differences (ΔTsk) of maximum values
between bilateral body areas in nonathletic and athletic subjects
Body areas
Nonathletes
Athletes
P
0.223
0.722
0.164
0.953
0.134
0.161
0.165
0.318
0.104
0.268
0.791
A Arm
A Shoulder
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
0.38
0.61
0.38
0.28
0.53
0.38
0.73
0.53
0.39
0.36
0.22
±
±
±
±
±
±
±
±
±
±
±
0.28
0.51
0.37
0.33
0.57
0.35
0.86
0.26
0.30
0.40
0.23
0.52
0.51
0.19
0.22
0.25
0.20
0.35
0.39
0.25
0.15
0.19
±
±
±
±
±
±
±
±
±
±
±
0.26
0.82
0.23
0.15
0.24
0.20
0.23
0.36
0.30
0.14
0.23
Total X ΔTsk
0.43
± 0.41
0.29
± 0.29
Dif. = Difference between both groups calculated as: ([athletesnonathletes/(athletes+nonathletes)/2]·100%)
A, anterior; P, posterior; X, average.
Table 14. Results of unpaired t-test in nonathletic and athletic subjects. Mean °C
(±) Standard Deviation of the side-to-side differences (ΔTsk) of average values
between bilateral body areas in nonathletic and athletic subjects
Body areas
Nonathletes
Athletes
A Arm
A Shoulder
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
0.84
0.39
1.11
0.23
0.13
1.25
0.42
0.53
0.38
1.26
0.25
±
±
±
±
±
±
±
±
±
±
±
1.14
0.25
1.46
0.15
0.12
2.07
0.19
0.41
0.23
1.61
0.31
0.67
0.26
0.78
0.14
0.25
0.25
0.28
0.68
0.26
0.75
0.17
±
±
±
±
±
±
±
±
±
±
±
1.08
0.20
0.98
0.10
0.22
0.19
0.20
0.96
0.19
1.40
0.14
Total X ΔTsk
0.62
± 0.72
0.41
± 0.51
Dif. = Difference between both groups calculated as: ([athletesnonathletes/(athletes+nonathletes)/2]·100%)
A, anterior; P, posterior; X, average.
79
P
0.735
0.191
0.762
0.160
0.291
0.217
0.119
0.527
0.291
0.438
0.475
Isabel Rossignoli 2015
4.2.2 Comparison of shoulder pain in athletic and nonathletic subjects
The WUSPI and PC-WUSPI scores were 8.7±20.3 (0.0, 38.49) and 9.1±20.4 (0.0,
52.81), respectively. The nonathletic group presented a higher WUSPI score
(11.9±28.4) in comparison to the athletic group (1.1±13.5, p=0.034). Likewise,
the nonathletic group presented a significantly higher PC-WUSPI score
(17.8±29.8) compared to the athletic group (1.3±13.5, p=0.022).
4.2.3 Relationship between thermography and shoulder pain
The Spearman Rho test revealed that there was no correlation between WUSPI
or PC-WUSPI and the basal temperatures of the different body regions in the
nonathletic group. Athletes presented a significant correlation between WUSPI
score and the Tsk maximum values in the following ROIs: Left Anterior Shoulder
(r=-0.622; p<0.05), Right Posterior Central Trapezius (r=-0.591; p<0.05), Left
Posterior Central Trapezius (r=-0.684; p<0.05); and between PC-WUSPI score
and the Tsk maximum values of these ROIs: Left Anterior Shoulder (r=-0.664;
p<0.05), Right Posterior Central Trapezius (r=-0.563; p<0.05), and Left Posterior
Central Trapezius (r=-0.647; p<0.05).
Considering the asymmetries, only the WUSPI and PC-WUSPI of the athletic
subjects were related with the ΔTsk of the average values of the Anterior Arm
(r=0.729 and r=0.729; p<0.05).
80
Results
4.3 STUDY 3: RELATIONSHIP BETWEEN SHOULDER PAIN AND SKIN
TEMPERATURE MEASURED BY INFRARED THERMOGRAPHY IN A
WHEELCHAIR PROPULSION TEST
The mean WUSPI and PC-WUSPI scores were 5.49±6.57 (0.0, 16.58) and
5.58±6.59 (0.0, 16.58), respectively. The maximum and average Tsk and ΔTsk was
compared before (pre-test), one minute after (post-test), and 10 min after (post10) the T-CIDIF. The thermal results and ROIs with significant differences are
showed in the Tables 15 and 16.
81
Isabel Rossignoli 2015
Table 15. Descriptive values of the skin temperature (°C) of 22 ROIs in wheelchair
athletes; repeated measures ANOVA correlation
Maximum Tsk values
ROI
R A Arm
L A Arm
R A Shoulder
L A Shoulder
R Pectoral
L Pectoral
R A Trapezius
L A Trapezius
R P Arm
L P Arm
R Dorsal
L Dorsal
R P Shoulder
L P Shoulder
R P Infraspinatus
L P Infraspinatus
R P Supraspinatus
L P Supraspinatus
R P Central Trapezius
Average Tsk values
L P Central Trapezius
R P Trapezius
L P Trapezius
R A Arm
L A Arm
R A Shoulder
L A Shoulder
R Pectoral
L Pectoral
R A Trapezius
L A Trapezius
R P Arm
L P Arm
R Dorsal
L Dorsal
R P Shoulder
L P Shoulder
R P Infraspinatus
L P Infraspinatus
R P Supraspinatus
L P Supraspinatus
R P Central Trapezius
L P Central Trapezius
R P Trapezius
L P Trapezius
Total maximum Tsk
Total average Tsk
Pre-test
Mean
±
SD
33.51
33.12
33.91
33.44
34.06
33.93
33.90
33.96
32.08
32.12
32.76
32.82
32.13
32.73
32.46
32.92
32.63
32.88
33.52
33.39
33.26
33.26
31.54
31.76
32.93
32.66
31.24
31.68
33.11
33.21
30.23
30.10
31.33
31.08
31.45
31.65
31.36
32.09
32.03
31.73
31.33
32.33
32.66
32.64
33.13
31.57
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.62
0.78
0.67
1.06
0.70
0.69
0.41
0.70
0.81
0.97
1.13
1.17
1.39
1.11
1.20
1.29
1.03
1.19
0.94
0.90
0.84
0.82
1.32
0.75
0.73
0.99
2.44
1.57
0.45
0.69
1.05
0.74
1.26
1.60
1.26
1.27
1.42
1.41
1.07
1.74
1.41
0.82
0.93
0.93
0.93
1.21
Post-test
Mean
±
SD
33.59
32.94
33.90
33.38
34.04
33.84
33.90
33.73
32.23
32.30
32.20
32.29
32.25
32.66
32.13
32.58
32.31
32.80
33.13
32.87
32.98
32.96
31.78
31.42
32.55
32.35
30.99
31.55
32.96
32.88
30.50
30.40
30.90
31.18
31.18
31.44
31.08
31.57
31.65
30.69
30.63
31.14
32.18
31.88
32.95
31.17
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.92
1.02
1.44
1.36
1.04
0.87
1.14
1.29
1.18
1.18
0.91
0.97
1.38
1.37
1.13
1.51
1.34
1.50
1.49
1.45
1.28
1.27
1.03
1.13
1.43
1.34
2.34
1.61
1.27
1.39
1.12
1.19
1.18
1.21
1.44
1.46
1.40
1.66
1.31
2.61
1.71
1.80
1.26
1.40
1.23
1.48
Post-10
a
a
#
#
Mean
±
SD
34.29
33.90
34.48
34.36
34.69
34.58
34.64
34.49
33.15
33.09
32.90
32.95
32.97
33.32
32.87
33.12
32.99
33.37
33.74
33.57
33.63
33.58
32.82
32.29
33.37
33.39
31.66
32.43
33.78
33.59
31.46
31.26
31.48
31.52
31.87
32.10
31.59
32.23
32.38
31.63
31.23
31.91
32.78
32.78
33.67
31.87
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.75
0.91
1.27
1.25
1.16
0.90
1.08
1.03
1.12
0.72
0.99
0.90
1.54
1.29
1.48
1.51
1.44
1.49
1.24
1.28
1.28
1.28
1.18
1.23
1.47
1.38
2.37
1.47
1.17
1.31
1.23
1.12
1.34
1.24
1.61
1.54
1.64
1.62
1.50
2.09
1.70
1.71
1.35
1.56
1.18
1.52
ab
ab
#∞
b
ab
ab
∞
ab
ab
∞
∞
∞
ab
ab
∞
b
∞
∞
b
b
b
ab
#b
b
ab
∞
#b
∞
∞
ab
ab
∞
b
#b
b
b
∞
∞
b
b
b
F
P
10.670
12.185
2.385
1.686
3.879
5.215
5.415
3.221
8.883
12.606
3.179
2.709
3.267
5.284
8.067
2.833
3.824
2.949
2.503
3.272
3.903
3.756
5.606
5.380
4.808
5.792
2.443
4.219
2.648
2.545
11.850
10.155
2.472
0.524
5.505
4.819
1.369
3.671
4.591
1.841
1.026
5.391
4.632
6.630
0.001
0.002
0.143
0.208
0.036
0.014
0.012
0.093
0.001
0.000
0.066
0.094
0.090
0.013
0.003
0.083
0.038
0.073
0.127
0.057
0.035
0.040
0.031
0.016
0.034
0.011
0.141
0.046
0.130
0.106
0.000
0.005
0.116
0.601
0.012
0.018
0.276
0.044
0.022
0.201
0.338
0.013
0.021
0.007
Note: ROI, region of interest; Tsk, skin temperature; A, anterior; P, posterior; R, right; L, left; (a), significantly
82
Results
different with respect to pre-test at p<0.05; (b), significantly different with respect to post-test at p<0.05; (#),
tendency to significance with respect to pre-test p<0.1; (∞), tendency to significance with respect to post-test
p<0.1.
Table 16. Descriptive values of the side-to side differences (°C) of the 26 measured
ROIs in wheelchair athletes; repeated measures ANOVA correlation
ROI
A Arm
A Shoulder
Maximum ΔTsk values
A Forearm
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Forearm
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
A Arm
A Shoulder
Average ΔTsk values
A Forearm
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Forearm
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
Total average ΔTsk
values
Pre-test
Mean ± SD
Post-test
Mean ± SD
0.47
0.40
0.37
0.27
0.20
0.25
0.32
0.40
0.61
0.35
0.13
0.10
0.22
0.35
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.25
0.35
0.53
0.28
0.14
0.23
0.20
0.22
0.56
0.33
0.20
0.11
0.17
0.21
0.62
0.43
0.27
0.22
0.30
0.48
0.10
0.53
0.49
0.80
0.55
0.17
0.12
0.13
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.38
0.25
0.23
0.08
0.36
0.40
0.06
0.25
0.55
0.50
0.49
0.14
0.13
0.10
0.33
0.28
0.63
0.15
0.23
0.23
0.33
0.31
0.48
0.18
0.10
0.22
±
±
±
±
±
±
±
±
±
±
±
±
0.23
0.18
0.93
0.10
0.19
0.24
0.26
0.21
0.54
0.18
0.11
0.17
0.27
0.25
0.20
0.22
0.22
0.25
0.32
0.37
0.47
0.45
1.02
0.43
±
±
±
±
±
±
±
±
±
±
±
±
0.18
0.19
0.15
0.16
0.18
0.25
0.23
0.15
0.36
0.29
1.24
0.37
0.29
±
0.27
0.35
±
0.30
Post10
Mean ± SD
#
a
a
a
#
a
#
0.37
0.33
0.30
0.12
0.13
0.37
0.13
0.37
0.28
0.62
0.65
0.22
0.17
0.35
±
±
±
±
±
±
±
±
±
±
±
±
±
±
0.29
0.24
0.19
0.15
0.12
0.23
0.08
0.45
0.29
0.44
0.37
0.20
0.23
0.30
0.38
0.46
0.23
0.15
0.27
0.27
0.48
0.28
0.58
0.45
1.02
0.30
±
±
±
±
±
±
±
±
±
±
±
±
0.34
0.56
0.19
0.14
0.15
0.31
0.48
0.23
0.36
0.39
1.20
0.17
0.40
±
0.37
F
a∞
b
b
#
P
1.988
0.621
0.257
0.004
0.241
0.038
0.260
0.750
5.126
3.582
2.466
1.193
0.815
4.142
0.161
0.547
0.668
0.996
0.788
0.963
0.774
0.428
0.015
0.047
0.108
0.322
0.413
0.036
0.235
1.498
0.290
1.617
1.048
0.018
0.119
1.181
0.288
3.470
0.158
2.416
0.793
0.250
0.645
0.226
0.371
0.983
0.888
0.328
0.631
0.087
0.707
0.118
Note: ROI, region of interest; ΔTsk, difference between right and left skin temperature; A, anterior; P, posterior;
(a), significantly different with respect to pre-test at p<0.05; (b), significantly different with respect to posttest at p<0.05; (#), tendency to significance with respect to pre-test p<0.1; (∞), tendency to significance with
respect to post-test p<0.1.
83
Isabel Rossignoli 2015
Table 17. Spearman Rho correlations between bilateral ΔTsk and shoulder pain
Maximum ΔTsk values
Average
ΔTsk values
Post-test
Average ΔTsk values
Pre-test
Maximum ΔTsk values
ROI
A Arm
A Shoulder
A Forearm
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Forearm
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
A Arm
A Shoulder
A Forearm
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Forearm
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
A Arm
A Shoulder
A Forearm
Pectoral
A Trapezius
P Arm
Dorsal
P Shoulder
P Forearm
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
A Arm
A Shoulder
A Forearm
Pectoral
A Trapezius
WUSPI
PC-WUSPI
P
r
-0.22
-0.52
-0.21
-0.12
0.28
0.33
-0.15
-0.58 *
0.22
-0.06
-0.19
-0.27
-0.05
0.36
-0.61 *
0.50
-0.24
-0.33
-0.15
0.30
-0.20
0.05
-0.04
-0.05
-0.15
-0.34
-0.04
0.03
0.18
0.47
0.01
0.10
0.53
0.22
-0.18
-0.07
-0.33
-0.22
0.03
0.42
0.06
-0.52
-0.22
0.08
0.49
0.09
0.53
0.72
0.37
0.30
0.68
0.05
0.49
0.87
0.56
0.40
0.88
0.28
0.05
0.14
0.48
0.34
0.66
0.43
0.56
0.89
0.90
0.89
0.66
0.34
0.91
0.93
0.60
0.12
0.98
0.77
0.12
0.49
0.57
0.83
0.29
0.49
0.94
0.23
0.85
0.10
0.52
0.81
84
r
-0.22
-0.54 #
-0.21
-0.13
0.32
0.34
-0.18
-0.56 #
0.18
-0.04
-0.14
-0.23
-0.03
0.36
-0.65 *
0.50
-0.32
-0.33
-0.15
0.26
-0.22
-0.04
-0.12
0.04
-0.11
-0.36
-0.06
0.04
0.18
0.42
-0.03
0.08
0.48
0.20
-0.23
-0.13
-0.29
-0.20
0.09
0.42
0.06
-0.52
-0.26
0.05
P
0.49
0.07
0.53
0.68
0.30
0.28
0.62
0.06
0.58
0.90
0.65
0.48
0.94
0.28
0.03
0.14
0.34
0.34
0.66
0.50
0.52
0.91
0.73
0.91
0.75
0.31
0.85
0.89
0.60
0.17
0.92
0.79
0.16
0.54
0.48
0.68
0.36
0.52
0.79
0.23
0.85
0.10
0.45
0.87
Results
ROI
r
0.14
-0.16
0.11
-0.08
-0.06
-0.48
-0.61 *
-0.48
0.20
A Shoulder
Maximum ΔTsk values
Average ΔTsk values
PC-WUSPI
P
P
0.67
0.68
0.74
0.82
0.86
0.11
0.04
0.16
0.53
r
0.14
-0.16
0.11
-0.13
-0.10
-0.45
-0.59 *
-0.51
0.17
0.67
0.68
0.74
0.71
0.75
0.14
0.04
0.13
0.59
0.24
0.46
0.29
0.36
A Forearm
0.21
0.54
0.21
0.54
Pectoral
0.07
0.83
0.08
0.81
A Trapezius
-0.10
0.75
-0.08
0.81
P Arm
-0.06
0.85
-0.09
0.79
Dorsal
-0.71 *
0.02
-0.71 *
0.02
P Shoulder
-0.32
0.31
-0.37
0.24
P Forearm
-0.35
0.27
-0.37
0.24
P Infraspinatus
-0.30
0.34
-0.35
0.26
P Supraspinatus
-0.35
0.27
-0.32
0.32
P Central Trapezius
-0.25
0.44
-0.23
0.47
P Trapezius
-0.24
0.45
-0.23
0.48
A Arm
0.52
0.15
0.52
0.15
A Shoulder
0.46
0.13
0.41
0.18
A Forearm
-0.07
0.84
-0.07
0.84
Pectoral
0.21
0.54
0.17
0.62
A Trapezius
0.55
0.10
0.62 *
0.05
P Arm
0.11
0.75
0.11
0.75
Dorsal
-0.54
0.13
-0.45
0.22
P Shoulder
-0.48
0.11
-0.49
0.10
P Forearm
0.09
0.80
0.03
0.93
P Infraspinatus
-0.49
0.11
-0.51
0.09
P Supraspinatus
-0.22
0.52
-0.17
0.63
-0.64 *
0.02
-0.63 *
0.03
0.24
0.47
0.20
0.56
P Arm
Dorsal
P Shoulder
P Forearm
P Infraspinatus
P Supraspinatus
P Central Trapezius
P Trapezius
A Arm
Post-10
WUSPI
P Central Trapezius
P Trapezius
Note: ROI, region of interest; ΔTsk, difference between right and left skin temperature;
WUSPI, Wheelchair Users Shoulder Pain Index; PC-WUSPI, Performance Corrected WUSPI; A,
anterior; P. posterior; (*), significant difference (p<0.05); (#), Tendency to significance
p<0.1.
Significant inverse relationships between changes in ΔTsk in the Shoulder ROI
and the results from the shoulder pain questionnaire were found before the
85
Isabel Rossignoli 2015
wheelchair propulsion test (Table 17); while Posterior Central Trapezius ROI
presented significant inverse correlation with the questionnaire in the post-test
and post-10. In addition, negative relationships were verified between the Dorsal
ROI and both WUSPI and PC-WUSPI, as well as the Anterior Trapezius ROI with
the PC-WUSPI (Table 17). Those inverse correlations imply that the higher the
shoulder pain the lower the thermal asymmetry and vice versa.
No significant correlations were observed between the kinematic variables and
the shoulder pain questionnaire (Table 18).
Table 18. Descriptive values of the kinematic variables; Spearman Rho
correlations between kinematic variables and shoulder pain
WUSPI
PC-WUSPI
Variables
Mean ± SD
r
P
r
P
46.75 ± 19.42
-0.02 0.96 -0.01 0.98
Number of propulsions
217.05 ± 102.28 0.41 0.19
0.44 0.15
Mean peak torque (W)
81.48 ± 26.63
0.33 0.30
0.38 0.23
Mean power (W)
7.00 ± 1.29
-0.18 0.58 -0.15 0.64
Maximum velocity (m·s-1)
-1
5.60 ± 1.38
0.04 0.90
0.09 0.79
Average maximum velocity (m·s )
1182.08 ± 401.69 0.25 0.43
0.29 0.36
Total work (W)
Note: significant difference (p<0.05); r = coefficient of correlation Spearman Rho between both
arms.
There were found the following significant differences between the kinematic
variables and the thermographic data (ΔTsk). The number of propulsions
correlated with the maximum values of the Dorsal ROI (r=0.778, p=0.008) and
the anterior Forearm (r=-0.862, p<0.001) in the pre-test.
The mean peak torque correlated with the average values of the Pectoral (r=0.578, p=0.063), Infraspinatus (r=-0.565, p=0.056) and Central Posterior
Trapezius (r=-0.716, p=0.009) ROIs, as well as maximum values of the
Infraspinatus (r=-0.637, p=0.026) in the post-test; and with the average values of
the Arm (r=0.667, p=0.050) and Central Posterior Trapezius (r=-0.730, p=0.007)
ROIs, as well as the maximum values of the anterior Forearm (r=0.734, p=0.010)
and Infraspinatus (r=-0.637, p=0.026) in the post-10.
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Results
Mean power was the variable with higher number of correlated ROI, being for
pre-test: anterior Forearm (r=0.695, p=0.026) average values; for post-test:
Infraspinatus average (r=-0.668, p=0.018) and maximum values, and average
values of Central Posterior Trapezius (r=-0.688, p=0.013) and posterior
Trapezius (r=-0.737, p=0.015); for post-10: average values of anterior Trapezius
(r=-0.820, p=0.004), posterior Shoulder (r=-0.660, p=0.020), and Central
Posterior Trapezius (r=-0.575, p=0.050), and maximum values of Infraspinatus
(r=-0.688, p=0.013) and Central Posterior Trapezius (r=-0.596, p=0.041).
The maximum velocity correlated with average values of posterior Arm
(r=0.718, p=0.013) in pre-test; maximum values of Infraspinatus (r=-0.633,
p=0.027) in post-test and anterior Forearm (r=0.706, p=0.0153) in post-10.
Average maximum velocity present correlations with posterior Arm (r=0.662,
p=0.026) and Infraspinatus (r=-0.667, p=0.025) average values in pre-test;
posterior Forearm (r=-0.5633, p=0.056) and Infraspinatus (r=-0.601, p=0.039)
maximum values, and pectoral (r=-0.799, p=0.003) average values in post-test;
and maximum values of anterior Forearm (r=0.678, p=0.022) in post-10.
Finally, total work showed correlations in pre-test with the ROIs: average values
of anterior Forearm (r=0.800, p=0.005), and maximum values of anterior
Trapezius (r=0.593, p=0.042) and Dorsal (r=-0.673, p=0.033); in post-test with
the ROIs: maximum values of Infraspinatus (r=-0.615, p=0.033), and average
values of Infraspinatus (r=-0.547, p=0.065), Central Posterior Trapezius (r=0.663, p=0.019) and posterior Trapezius (r=-0.712, p=0.021); in post-10 with the
ROIs: average values of anterior Trapezius (r=0.712, p=0.021), posterior
Shoulder (r=-0.695, p=0.012), and maximum values of Infraspinatus (r=-0.713,
p=0.009) and Central Posterior Trapezius (r=-0.635, p=0.027).
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5 DISCUSSION
5.1 STUDY 1: RELIABILITY OF INFRARED THERMOGRAPHY IN SKIN
TEMPERATURE EVALUATION OF WHEELCHAIR USERS
Before establishing the efficacy of IRT as a tool for assessing the evolution of
pain, it is necessary to evaluate its reliability in order for it to be implemented on
populations with diverse characteristics. The main contribution of this study is
that its reliability is highly dependent on the area to be analyzed; IRT in WCUs
had a variable ICC and CV; and IRT demonstrated a poor to excellent reliability
(ICC: left anterior shoulder=0.15; right pectoral=0.95). This range of reliabilities
must be taken into account when interpreting thermographic data.
To our knowledge, there is only one study investigating IRT and skin
temperature evaluation of WCUs (365). It found that the temperature in the
palm, forearm, pectoral major and shoulder tended to increase during
wheelchair propulsion compared to other parts of the trunk. In the posterior
trunk the warmest areas corresponded to the trapezius and forearms (365). Our
results are similar, since the trunk was warmer than the limbs, and the forearm
and shoulder were warmer than the anterior trunk, but it is not possible to
compare both investigations since our measurements were undertaken while
the subjects were at rest.
There are no previous studies about reliability of IRT as a means of assessing
body temperature in WCUs, although some researchers have studied the IRT
reliability of non-WCUs. Our study is focused on works that studied similar areas
than us (the upper body except the hands, wrists and lumbar areas). A study by
Littlejohn et al. reached thermal ICC values for the forearm ranged from 0.190.85 (236). The intra-examiner reproducibility of a study by Zaproudina et al.
varied from poor in the fingertips to moderately high in the core areas, with a
mean ICC of 0.47 (459). Most of their areas with low ICC are coincident with our
study, whereupon it is necessary to pay attention to those relevant areas
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Discussion
(trapezius, forearm and shoulder). Burnham et al. compared the reliability of
three thermometers, finding that the infrared skin device was the most
responsive (ICC of 0.97) for the hand, forearm, shoulder, thigh, shin and foot
(54). Several studies (93, 253, 297, 306) about paraspinal Tsk discovered a fair to
excellent intraexaminer reproducibility (ICC 0.51-0.98). However, the surface of
some analyzed areas differs slightly between studies, and consequently, some
areas with the same name in each study (54, 459) corresponded to different
areas. Some studies only measured specific skin spots, because they used an
infrared skin thermometer (54), a handheld thermographic scanner (297), or a
handheld infrared paraspinal instrument (93) instead of an infrared camera.
Furthermore, Plaugher et al.’s research was undertaken with contact
thermography, whereas IRT is non-contact thermography (306). Their research
(306) relied on the examiner’s interpretation instead of a computerized reading
of data while other studies, including ours, manually measured the body areas
and compared one graph to another.
Injury processes of some body areas are the main explanation for the
fluctuations in the reliability, since the temperature varies depending on the type
and moment of the injury (post-traumatic pain syndrome and sympathetic nerve
involvement result in vasoconstriction and a colder area; acute and
inflammatory injury increase metabolism, blood flow and dermal temperatures)
(350). The particular characteristics of people with disabilities may have also
influenced the reliability, such as the thermoregulation problems presented by
the subjects with SCI (319) and sweating characteristics of multiple sclerosis
subjects (410). People with SCI have a loss of autonomic nervous system control
for vasomotor and sudomotor responses below the level of SCI, and a reduced
thermoregulatory effector response for a given core temperature (314, 355). As
a consequence of their poikilothermic behavior, they have a reduced ability to
tolerate thermal extremes (355); they have increased heat storage within the
lower body (314); and they tend to sweat less (314). This imbalance in
temperature regulation (most pronounced in individuals with tetraplegia rather
than paraplegia) makes skin temperature very changeable from one day to
another, influencing the reliability of our data. Other factors that may locally
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change the blood flow and the skin temperature are the variation of the
peripheral circulation in the distal parts of the body (459), obliterating artery
disease, malignancies, varicose veins or inflammatory processes (441).
The distribution of the upper body temperature of our study was similar to the
literature (54, 462). Central sites were warmer than peripheral sites, and this
may be explained by blood distribution (462). Unlike Zhu et al. (462), subjects in
our study had slightly higher ventral body temperature (31.92±2.22) than dorsal
body temperature (31.77±1.92). Commonly the ventral area has greater skin
thickness than the dorsal area, and subcutaneous fat in the area is known to
influence thermal readings (236).
The mean ICC for average values (Table 8) is 0.56 (fair). When areas with lower
ICC values are removed (the forearm, arm, shoulder and trapezius) the mean ICC
augments to 0.64 (good). For the maximum values (Table 7) the mean ICC is 0.59
(fair) and without the most troubled area, the pectoral, the mean ICC becomes
0.60 (good). These sensitive areas to error are involved in wheelchair
propulsion; we suggest the participant is carried to the room to avoid doing any
exercise before the testing. The average values have a greater number of areas
with poor ICC than the maximum values. When regions of interest are manually
drawn certain limits can go out of the boundary and encompass part of the
background picture, and hence the average temperature of this area would be
lower. The maximum values are not affected by extreme values, and thus they
are more congruent; therefore, they were chosen as references to calculate the
ΔTsk between symmetrical sides of the body.
Burnham et al. affirmed that side-to-side temperature comparisons could be
used as a measure of an instrument’s reliability (54). Most of the articles found
ΔTsk or thermal asymmetry of around 0.5°C (54, 286), 0.4°C (459) and 0.3°C
(167, 407). Our data showed a ΔTsk for maximum values of: 0.17±0.53°C and
0.15±0.49°C in days 1 and 2, respectively; with a ΔTsk between both days of
0.09±0.44°C. SD values over 2.5-3 indicate a Tsk abnormality of certain part of
their bodies (286). There were no significant differences between day 1 and day
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Discussion
2. The correlation was good for anterior and posterior arm, posterior forearm,
dorsal, supraspinatus, and central trapezius; and excellent for anterior and
posterior shoulder, pectoral and infraspinatus. The average correlation was
moderate (r=0.583). Low correlation was found in the anterior forearm, anterior
and posterior trapezius. Previous literature proposes different reasons that
could cause these variations, such as Owens et al., who suggested that changes
could be explained due to physiological variations rather than equipment error
(297).
In summary, this is the first study examining the reliability of IRT, in particular
when incorporating the FLIR T335 thermal imaging camera, the ThermaCAM
Reporter (v.8) software and the selection protocol for the regions of interest, to
evaluate the skin temperature in WCUs. The range of reliabilities must be taken
into account when interpreting thermographic data and it is being attributable to
the accuracy characteristics of IRT equipment; the measurement environment
and technique; as well as the greater physiological variability of the blood flow in
subjects with SCI than healthy population. We can conclude that the IRT
technique has the potential to be an objective quantifiable indicator of
autonomic disturbances, which was fast, easy to use and was shown to be
adequately reliable to monitor skin temperature in wheelchair users.
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5.2 STUDY 2: RELATIONSHIP BETWEEN PERCEIVED SHOULDER PAIN AND
INFRARED THERMOGRAPHY IN WHEELCHAIR ATHLETES AND
NONATHLETES
The main findings of the study show that: (i) nonathletic and athletic WCUs
present a similar profile of body temperature; (ii) the side-to-side differences of
body temperature are similar in nonathletic and athletic subjects; (iii) shoulder
pain is greater in nonathletic subjects in respect to athletic subjects; and (iv) in
athletes the temperature of some body regions are negatively related with
shoulder pain.
To the best of our knowledge, there is no previous study that facilitates a general
or local thermal profile of WCUs that could work as a reference thermal pattern
for this population, except in our preceding research (342) where data of mean
Tsk and bilateral ΔTsk of the main body ROIs was provided. Few studies have
applied IRT technique for the evaluation of the Tsk particularly in wheelchair
users (340, 365, 434, 464). Any of these studies can be compared with our data
because of: different infrared technology used (434) since the Tsk obtained with
IRT is lower than that obtained with contact thermometry (286); time since
injury (464) as subjects with SCI after 6 months from the onset of the injury
adjust their thermoregulatory set point in the presence of an external ambient
stressor (25); ROIs analysed (340, 464); the subjects’ position (464); or the lack
of data provided (365). Until now no studies have applied this technique for the
comparison of the Tsk in athletic and nonathletic WCUs. Only one IRT study has
been undertaken which compares the Tsk of trained and untrained subjects, and
this analysed only the lower body (124). Interestingly, they discovered a faster
thermoregulation response in sportspeople than in sedentary people. However,
their results cannot be compared with ours since they did not study the upper
body.
The higher Tsk of our work is found in the anterior trapezius, pectoral and
anterior shoulder and the lower in posterior arm, dorsal and posterior shoulder.
The temperature pattern of the body regions nearly coincides with the literature
in able-bodied individuals, being higher in the ventral side compared to the
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Discussion
dorsal and higher in the central regions than in the extremities mainly in our
maximum values (286, 462). When comparing our results with thermographic
data from healthy population we found different ROIs selected by each study. We
have compared the following similar ROIs: anterior and posterior arm, anterior
and posterior shoulder, pectoral or upper trunk, and superior back. Although
there were not significant differences between the Tsk of nonathletes and
athletes the Tsk average values of the anterior and posterior arm and shoulder
ROIs approximate Marins et al. (245), Niu et al. (286) and Zaproudina et al. (458)
being slightly higher in nonathletes than athletes, and finding lower values in
upper trunk and back. The results were lower than the values presented by Zhu
et al. (462) and Kolosovas et al. (218) in all the compared ROIs. Differences in
race of the subjects (462), age (218) or type of camera used (283) may explain
the variation in the Tsk. It is interesting to find that core area presented lower
average values than any other study, since the central regions usually have
higher Tsk than the extremities. The poor thermoregulation system as well as
trunk activity of SCI subjects might influence in their low core Tsk values.
Thermography offers information about the status and disturbances of the
sympathetic vasomotor tone (458), evaluating the vasomotor activity of the
sympathetic nerve fibers and detecting sympathetic dysfunctions (400). So et al.
affirmed that Tsk values with a SD over 2.5 to 3 are indication of abnormal Tsk in
patients suspect to have autonomic dysfunction (376). Our maximum Tsk values
in wheelchair athletes and nonathletes and the average Tsk values in athletic
subjects do not present more than 2 SD, although high SD was found in the
average Tsk values of nonathletic subjects in the following ROIs: right pectoral
(3.39 SD); left pectoral (2.40 SD); left dorsal (2.89 SD) and right central trapezius
(2.49 SD). In general, the Tsk profile in WCUs presents much higher SD than the
profiles of able-bodied individuals found in the literature. The reason may be the
peculiarity of each impairment, e.g. two people with the same level of SCI, same
degree of involvement, and similar respiratory and cardiovascular parameters
may have different levels of functional sensitive-motor capacity and
thermoregulatory responses (97). In addition, the affected area may present a
warmer or colder pattern depending on whether there is a complete or partial
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interruption of the nerve fibers (406), therefore a complementary examination
of the patient should accompany the thermographic evaluation. Most of our
subjects present SCI, a condition that may imply autonomic nervous system
disruption, peripheral blood flow disturbances, and poikilothermic behavior that
is characterized by a poor body temperature regulation (25, 314). The
autonomic nervous system is one of the main factors that influence the Tsk; it
controls dilation and contraction of capillaries. In subjects with a SCI above the
6th thoracic vertebrae thermoregulation is affected since the neural pathway to
the hypothalamus is interrupted (314), disturbing autonomic responses such as
blood pressure. As a consequence, these subjects have impaired ability to reduce
body temperature by vasodilatation and sweat production (314), presenting
hypohidrosis below the level of the lesion and hyperhidrosis above and below
the level of the lesion (205). Their disturbed sweat production is translated in
hyperthermia in the affected skin area that evolves to hypothermia after 4-6
months (323). The normal thermal pattern of nerve fiber irritation or root
compression syndromes in the spine was described by Pochaczevsky et al. (308),
it may present changes due to inflammation or infection of vertebral or
paravertebral areas as well as 94 usculoligamentous injuries resulting in
hyperthermic zones anywhere along the spine or torso (308). A recent review
(14) confirmed the no-consensus and contradictory data in the literature on the
pattern of the healthy back, as well as the Tsk profile of various spinal
pathologies. They concluded that different spinal disorders might generate a
similar
thermal
pattern.
Further
development
of
the
knowledge
in
thermographic studies of the spinal disorders is needed.
Bilateral ΔTsk values over 0.3-1.8°C (35, 111, 218, 245, 407, 458, 462), are
considered abnormal and may be an indication of dysfunction in the assessed
ROI such as disturbances in the autonomic nervous system (165), peripheral
blood flow (167, 356) as well as pain syndromes (10, 458) or overuse injuries
(167). In our study we have considered 0.5°C as the threshold for abnormal
asymmetries. The results in the Table 13 show that absolute ΔTsk of maximum
values exceeded 0.5°C in the following areas of the athletic subjects: anterior arm
(0.52) and anterior shoulder (0.51); as well as the next areas of the nonathletic
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Discussion
subjects: posterior shoulder (0.73), anterior shoulder (0.61), posterior arm
(0.53), and infraspinatus (0.53). These areas with bilateral thermal imbalance
coincide with our WUSPI’s results, where WUSPI scores of nonathletic subjects
are higher than in athletic subjects, especially in the shoulder ROI that presents
the highest ΔTsk values. Ammer et al. found that healthy people have a much
lower ΔTsk than patients with peripheral nerve injury, 0.24 vs 1.55°C
respectively (14).
When we compare our ΔTsk with the literature of healthy subjects our average
values of ΔTsk of the ventral arm, pectoral (or upper trunk) as well as upper back
were higher than the literature (218, 286, 407, 459, 462), being higher in
nonathletic than athletic subjects. Our dorsal arm ΔTsk average values were
similar than Marins et al. (245) and Zaproudina et al. (459) but lower than the
rest of studies, either in athletes or nonathletes. The ventral shoulder ΔTsk
average values were similar to Kolosovas et al. (218) and Zhu et al. (462) but
higher than Uematsu et al. (407). Finally, the dorsal shoulder ΔTsk average values
in nonathletic subjects approximate the values published, being lower in athletic
subjects. Part of the interside ΔTsk may be explained by the dominant side
hyperthermia due to the higher muscle mass (21, 38, 144, 374), however the
bilateral propulsion of the wheelchair may compensate this asymmetry in WCUs
(377); even the athletic group, who perform unilateral repetitive sport gestures
with the dominant arm, presented a more symmetrical side-to-side Tsk than the
nonathletic group. This result may have been caused by the better wheelchair
propulsion technique of the athletes and the bilateral workout exercises that
they perform. The higher ΔTsk values of the nonathletic group can be explained
by the shoulder rotator muscle imbalance (292, 344) as well as the weakness of
the shoulder adductors (53, 372), as it is reflected in the WUSPI score and it is
highly studied in the literature (53, 94, 100, 219, 292, 344, 372).
The literature is not conclusive about whether wheelchair exercisers have a
higher or lower prevalence of shoulder pain than non-exercising WCUs (8, 45,
79, 120, 128, 225, 229, 387, 450). In our study, nonathletic WCUs have the
highest ΔTsk values, coinciding with the highest WUSPI score. The Tsk and ΔTsk
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Isabel Rossignoli 2015
results both showed asymmetric values that reflect the muscle imbalance around
the shoulder developed by WCU population. Sports could have a positive effect in
WCUs preventing shoulder pain, however multiple factors responsible of the
shoulder joint impairment, such as wheelchair propulsion technique (325, 326)
or over-the-head reaching from a wheelchair position (8, 103) should be
considered.
Thermography has been rarely used for the assessment of shoulder disorders
(38, 232, 270, 394, 400, 426). The literature differentiates two groups of
patients, with hypothermic and hyperthermic pattern in the involved side, where
the hypothermic group has more restriction in the movement of the shoulder
(299, 426). A study of the circadian rhythm of impaired shoulders showed that
shoulders tendinitis did not significantly change their Tsk on the day of study in
comparison with normal shoulders or cuff tear shoulders that reduce their Tsk at
night, due to the inflammation of the subacromial bursal tissues of the tendinitis
shoulders versus the lower inflammation process of the rotator cuff tears (270).
Hypothermia has been linked to degenerative process and chronic injuries (111,
307, 308), vessel occlusion such as thrombosis, nervous damage, reflex
sympathetic dystrophy, nerve root injury, Raynaud phenomenon, or avascular
tissues such from wounds or burns (334), abnormal activity of the sympathetic
nervous system (323, 400), as well as muscle atrophy (299), and decreased ROM
(299). Hypothermic patterns do not correlate with pain since in chronic phases
the movement is avoided and consequently the pain is reduced. However, Ring et
al. affirm that pain is present in both responses (334). A new study confirms that
long-term injuries exhibit the lower asymmetry between bilateral sides (370).
On the contrary, hyperthermia has been associated with inflammatory process
(299, 334) in the painful side (111), arthritis, skin reactions (334), disorders
related to increased blood flow in the skin (such as infections, tendinitis, bursitis,
bone fractures, tennis elbow, acute muscular injuries and other degenerative or
traumatic injuries in an acute phase) (307, 308, 334), also decreased
sympathetic tone to the skin due to the inflammatory response after a
sympathetic fibers’ injury (310), or other impaired sympathetic function (323).
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Discussion
In a study with 94 individuals with paraplegia was found that one third of the
subjects had shoulder pain, 75% of them had impingement and subacromial
bursitis and 65% had rotator cuff tear (32). After this preliminary study, other
investigations unveiled that the most common cause of shoulder pain is overuse
injuries of the rotator cuff (7, 32, 53, 100, 134, 158, 229, 284, 303, 366).
However, the shoulder impingement syndrome cannot be detected by IRT due to
its hidden location of the supraspinatus tendon in the coracoacromial arch and
subacromial space (299). This may explain the lack of correlation between IRT
and WUSPI test in nonathletes, and also the non-consistent patterns in shoulder
Tsk in rotator cuff tendinitis found by Vecchio et al. (426), who justify their
findings because of the low grade of inflammatory process. Since we did not
perform a clinical evaluation of the subjects’ shoulders, we cannot specify which
type of impairment they may have (whether both shoulders are affected
resulting in false-negative results) or in which phase of the development it is (as
each phase is characterized by a different thermal response). Despite the
absence of correlation between Tsk and WUSPI score in nonathletic subjects, the
higher WUSPI score and the higher ΔTsk values than in the athletes make suspect
a larger number of shoulder disorders in the nonathletic group. In addition,
Pogrel et al. assured that it is possible to have thermal asymmetry and not have
corporal pain (310). ΔTsk is a major distinctive factor than the absolute Tsk
between normal and abnormal conditions, as many studies show thermograms
of control group with symmetrical patterns (310). We consider a limitation of
the WUSPI score the fact that it does not discriminate between shoulders;
therefore, our correlation could have been stronger if the IRT of the shoulder ROI
had been compared with the specific painful shoulder. Additionally, the WUSPI
test is applied to just one ROI, the shoulder, while the IRT in this study includes
all the ROI involved in wheelchair propulsion. Another possible explanation for
the moderate correlation is the low intensity of the shoulder pain as it is
reflected in smaller WUSPI score than the literature (50, 101, 277). The score
range encompasses from 0 to 150 cm and our higher value was 52.81 cm.
Pulst et al. describes the microcirculation evolution of entrapment neuropathies,
from initial vasoconstriction caused by irritation of the sympathetic fibers;
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Isabel Rossignoli 2015
posterior vasodilatation fruit of sympathetic denervation consequence of the
compression; and, ending with vasoconstriction, results of the postdenervation
hypersensitivity of the blood vessels to circulation (323). Suprascapular nerve
entrapment is a common nerve compression syndrome in WCUs; its irritation
may produce a sympathetic vasoconstriction reflex resulting in decreased Tsk
(408, 458). Our results are in agreement with these authors since we found a
negative correlation between the temperature of some ROIs and shoulder pain in
athletic subjects. Probably the higher basal metabolic rate and muscle mass in
wheelchair athletes (the group with less shoulder pain) justify the greater heat
emission and consequently major Tsk (238, 353), since the muscle is an active
metabolic tissue responsible of the heat production to keep the body warm (76).
Their better vasculature and strength due to exercise allows an improved blood
flow (represented by higher Tsk) and lowers the risk of injury (38). It may be the
reason of lower pain with higher temperature experimented by the athletes.
Nonathletes possibly have more adipose tissue, which better isolates body
temperature irradiating less heat (113), adding to higher pain and muscle
imbalance. Moreover, recent studies have found that brown adipose tissue, a
metabolically active tissue specialized in generating heat through the
thermogenesis process, is also present in human adults. This highly capilarized
tissue, stimulated by the sympathetic nervous system, is mainly located in the
supraclavicular region, anterior neck, paravertebral area, and upper chest (281)
ROIs of our study. Brown fat is inversely correlated with BMI (84), and is
reduced in most overweight or obese subjects (421). It can partially explain why
this correlation is present only in wheelchair athletes. In summary, the heat
emitted by the musculature at rest (231), the articular protection that muscles
provide (38) linked to lower pain thanks to a better load distribution, greater
percentage of muscle mass and fat-free mass in athletes, offers a possible
explanation to our findings. Physical activity is used in osteoarthritis
rehabilitation programs to prevent and treat pain thanks to the muscle mass
augmentation. We encourage WCUs to practice sports to prevent shoulder
injuries, especially at low angles as it improves blood flow patterns and avoids
impingement syndromes (38). From a practical point of view, our findings help
to understand the thermal map in WCUs and call for future studies to further
98
Discussion
examine the thermoregulation response of WCUs in exercise. The great
methodological differences between the studies that research the thermal Tsk
pattern in upper body differ in such a way that disturbs the comparison between
them. In order to avoid it, we recommend using the same standard room
temperature for future studies (21-25°C, no lower than 22°C when working with
SCI subjects) and to select the same ROIs for WCUs, which should be the same
areas used for wheelchair propulsion. Furthermore, it is advocated to reduce the
acclimatization period to no more of 10 minutes for subjects with SCI
characterized by poikilothermic behaviour, to prevent from discomfort and
hypothermia.
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5.3 STUDY 3: RELATIONSHIP BETWEEN SHOULDER PAIN AND SKIN
TEMPERATURE MEASURED BY INFRARED THERMOGRAPHY IN A
WHEELCHAIR PROPULSION TEST
Our study focuses on the response of the Tsk to a maximal wheelchair propulsion
test and its relation (pre-test, post-test, post-10) with shoulder pain in WCUs.
Most the studies in which the subjects were exposed to constant and prolonged
exercise resulted in an increased Tsk (72, 118, 124, 168, 171, 182, 237, 411, 433,
437, 438, 457). In contrast, graded, intermittent or maximal exercises normally
performed for brief period, resulted in decreased Tsk (9, 20, 66-68, 263-265, 278,
403). Based on this trend our short test should produce a reduction of the Tsk
once it finalized. Our Tsk values in Table 15 clearly show a tendency to initially
decrease immediately after the test (in 81.81% of the ROIs, average values) and
next a significant increase after 10 minutes of completing the T-CIDIF (in 86.36%
of the ROIs, average values). These results are more common of prolonged
exercises.
In WCUs, it seems primordial to transfer the metabolic heat from the core to the
skin as it is reflected by the prompt increase of Tsk. Another possible explanation
could be the SCI condition presented by most of our sample, this population may
present cardiovascular limitations, and patients with compromised cardiac
function are characterized by a higher extent of vasoconstriction in comparison
with healthy (168), which could explain the initial reduction of the Tsk. Another
characteristic of paraplegic athletes is to have a larger heat storage in the lower
body that ends in a diminished ability to reduce their core temperature during
the recovery phase (314), that may explain the rise of Tsk in the reduced body
surface area for active thermoregulation even in brief exercises. Price et al. found
that lower body Tsk augmented during prolonged upper body exercise due to the
increased heat storage in that region (314, 315). Gass et al. also found an initial
decrease of the Tsk (measured with thermistors) followed by an increase in the
arm ROI during a prolonged wheelchair exercise with trained paraplegic men
(132). Normell indicated that there is a large individual variation of the
cutaneous thermoregulatory vasomotor response, specially at the lower spinal
lesion levels, highlighting differences in the somatosensory and sympathetic
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Discussion
pathways, in the sympathetic outflow response, and in the type and degree of
reinnervation (289). The extent of vasodilation and sweating depend on the
lowermost intact portion of the sympathetic chain, level and completeness of SCI
(132), in other words, fluid losses during exercise and heat retention during
passive recovery from exercise are related to lesion level (314). Probably the
findings would be different with a higher number of subjects having the same
level of injury. For example, five of our subjects have a lesion level above T10,
which implies a lack of sympathetic innervation to the splanchnic area and
therefore may not have the ability to redirect blood flow from an inactive area to
the active areas. In subjects with extended skin regions denervated, the loss of
sympathetic vasomotor afferent fibers results in microcirculation changes that
are reflected in locally increase of the blood flow and Tsk.
Because of each subject performed the T-CIDIF in their own daily wheelchair, the
differences in the wheelchair design and seating position could have influenced
the venous return dynamics, and thus impact the blood distribution.
The lack of significant differences between the pre-test and post-test Tsk in
contrast with the amount of differences respect to post-10 could be due to the
short duration of the T-CIDIF; 30 seconds normally is not enough time to activate
the thermoregulation system, as the hypothalamus starts to respond after 6-7
minutes of the exercise’s onset (314). Most of the IRT studies chose longer
exercise protocols with the exception of Adamczyk et al., who found similar
results than our study: a decrease of the lower limbs Tsk (1.44°C) right after
finishing the exercise and a posterior rise during the recovery period (3).
However, we have chosen the T-CIDIF for being a validated test for WCUs (261)
and because of its characteristics allow trained as well as untrained participants
to perform it.
The thermal pattern can also be influenced by the fitness level; trained subjects
present better cooling capacity during exercise and faster recovery (264) thanks
to an improved thermoregulation system and greater vascularization of the
musculature compared with non-trained (2, 61, 124). The muscles of our highly
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skilled sample may present earlier and more responsive skin blood flow
responses, consequently the onset of vasodilation would occur at lower internal
temperatures (338) and the Tsk would start growing sooner than in a less fit
sample. This finding is in agreement with previous thermal study of a martial art
comparing skilled and novice physically active females, where the skilled group
presented higher post-exercise Tsk values than the novice group (237). The
opposite will happen with a sample with greater fat percentage, as adipose tissue
has lower thermal conductivity preventing the transfer of the heat from the
muscles to the skin (238). Future studies could compare the thermoregulation
response at exercise of athletes vs. nonathletes wheelchair users, in order to
know whether the athletes’ rise of Tsk is not only happening earlier (more
responsive) than in nonathletes but also during a shorter period (faster
recovery), as it happens in able-bodied population (2, 66, 321).
A previous research of skin temperature measurement during wheelchair
exercise (365) found that the ROIs with higher Tsk under exercise (Shoulder,
upper Pectoral major, anterior and posterior Forearm, Palm, anterior and
posterior Trapezius) showed marked increase in Tsk during the first 15 min
recovery phase, and coincided with the areas of raised activity in EMG under
wheelchair driving. Interestingly, the ROI with lower EMG was the upper arm.
Shin-ichi et al. concluded that the surface temperature could be an index of
muscle activity during exercise (365). They also found a great body surface
temperature difference depending on the body fat percentage of the subject, with
higher drop of the Tsk during the test and larger Tsk variations between the prettest, during wheelchair driving and recovery in the fat subject.
According to the Table 16, the ΔTsk is statistically modified by exercise increasing
in post-test respect to pre-test in 5 ROIs (anterior Arm, Infraspinatus,
Supraspinatus, anterior and posterior Trapezius); rising in anterior Arm ROI and
decreasing in two ROIs (posterior forearm and Infraspinatus) in post-10 respect
to post-test; growing in one ROI (posterior Central Trapezius) and diminishing in
another ROI (posterior forearm) in post-10 respect to pre-test.
102
Discussion
There is not a consistent tendency of the growth or decrement of the ΔTsk after
the T-CIDIF, although both average (0.29±0.27 vs 0.35±0.30) and maximum
(0.31±0.27 vs. 0.39±0.29) total ΔTsk values increased in post-test respect to pretest. The clear trend in Tsk vs. the no-tendency in ΔTsk make suspect of different
influence of exercise in each ROIs, and/or different implication of each muscle in
the wheelchair propulsion test. On one side, there is a different percentage of
involvement of the several muscles used during the wheelchair propulsion task,
and different wheelchair propulsion techniques applied (e.g. depending on their
impairment type and the size of the wheelchair). Any of the SCI participants have
tetraplegia, hence their upper extremities are fully innervated, and also, all of
them trained the same number of hours per week and same load of training, so
they have similar upper body work capabilities. On the other side, the initial
cutaneous vasoconstriction response needs dynamic activity by a significant
musculature, not being effective for smaller muscle groups (199). It is also
known that dominant side has a higher capacity to loss temperature and better
thermoregulation (374), getting cold in response to the onset of the activity
because of the vasoconstriction effect. This is not reflected in our results and it
can be due to the bilateral propulsion of the wheelchair that may compensate
this asymmetry in WCUs (377). Finally, Shin-ichi et al. found a non-uniform
distribution of the temperature in the bust rising heterogeneously during both
wheelchair exercise and recovery (365), which is consistent with our lack of
pattern in ΔTsk after exercise. Although the thermographic results are not
conclusive enough to make definitive assumptions, they provide an insight in the
thermal pattern of WCUs at exercise.
In Table 17 is observed an inverse correlation between shoulder pain and the
ΔTsk of the anterior and posterior Shoulder ROIs prior to T-CIDIF. One minute
after the wheelchair propulsion test, it is detected a negative relationship
between shoulder pain and the ΔTsk of the Central Posterior Trapezius. Ten
minutes after the test the ΔTsk of the Dorsal ROI correlates negatively with
shoulder pain, while the ΔTsk of the Central Posterior Trapezius and the Anterior
Trapezius correlate positively with shoulder pain. These are only a few
correlations in comparison with the amount of ROIs measured. Most of them
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were negative; hence higher WUSPI or PC-WUSPI scores are related with lower
ΔTsk. Previous studies of the author found several negative relationships
between the shoulder pain test and the Tsk of 6 ROIs, but only one correlation
with the bilateral differences (342). These findings could be explained because of
the low shoulder pain experienced by our sample, our WUSPI and PC-WUSPI
scores were no higher than 6 cm in comparison with the range of the scale from
0 to 150 cm.
Our study has not found any correlation between shoulder pain and the
kinematic variables of the T-CIDIF (Table 18). This results are opposite of
previous findings that reported significant inverse relationships between the
kinematic variables of the T-CIDIF and the PC-WUSPI test (261). The reason
could be also the low shoulder pain score of our subjects. Moreover, they were
very disposed to give their best during the test due to their athletic and
competitive attitude, thereby they may have propelled at their maximum in spite
of their shoulder pain.
The findings show multiple correlations (mostly negative) between all the
kinematic variables of the T-CIDIF and the ΔTsk of many ROIs. Although it was
not part of our aims, we provide information of the relation between the exercise
and the thermographic variables. Menéndez et al. discovered high positive
correlations between the variables of the T-CIDIF and the peak torque, total
work, mean power, and mean of the peak torques of the internal and external
shoulder rotators obtained in a maximum isokinetic strength test (261). Based
on this outcome, they affirmed that T-CIDIF could be used as an alternative of the
isokinetic strength test. Consequently, the inverse correlations found between
the kinematic variables and the thermal data in our study could be translated to
the isokinetic dynamometer, such as, higher torque and power may also
correlate with lower ΔTsk. This is good reason to promote the strengthening of
the shoulder joint between WCUs. Additionally, the isokinetic strength test
performed by them did not correlate with the shoulder pain questionnaire,
implying that the pain is limited to functional gestures more than maximum
strength.
104
Conclusions
6 CONCLUSIONS
6.1 CONCLUSIONS STUDY 1
The conclusions derived from the achievement of the first study’s objective are:
- The reliability of infrared thermography in wheelchair users depends
on the analyzed region of the body. The regions of interest with higher
intraclass correlation coefficient for average temperature when
measurements were compared on separate days, and hence, the more
reliable ROIs were the left posterior forearm (0.80), right posterior arm
(0.88), right dorsal (0.79), right pectoral (0.95), left supraspinatus
(0.76). The ROIs with a lower ICC for average temperatures, and were
therefore less reliable, were the right anterior forearm (0.22), left
anterior forearm (0.24), left anterior arm (0.18), left posterior arm
(0.23), left anterior shoulder (0.15), left posterior trapezius (0.38).
- The reliability of the maximum temperature values improved when
compared from one day to the next. Those which showed an excellent
reproducibility were the left anterior forearm (0.76), right posterior
forearm (0.77), left posterior arm (0.77) and left anterior trapezius
(0.79). The left pectoral was the only region to show poor
reproducibility (0.39) for maximum temperature.
6.2 CONCLUSIONS STUDY 2
The conclusions to the first objective of the study 2 are:
- Nonathletic wheelchair users were shown to have a similar skin
temperature and a greater bilateral skin temperature than wheelchair
athletes in most regions of interest. Furthermore, both athletic and
nonathletic wheelchair users presented with a higher bilateral skin
temperature than able-bodied results published in the literature.
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Isabel Rossignoli 2015
- In particular, nonathletes have higher skin temperature and bilateral
skin temperature differences in the anterior and posterior shoulder
than athletes.
The conclusion to the second objective of the study 2 is:
- The nonathletic group presented with higher shoulder pain in
comparison to the athletic group.
The conclusions to the third objective of the study 2 are:
- In athletic wheelchair users the analysis of the skin temperature could
be important since some regions of interest are related to shoulder
pain. The regions of interest, in which a relationship between
maximum skin temperature and pain was shown, were the left
anterior shoulder, the right posterior central trapezius, and the left
posterior central trapezius; and for the average bilateral skin
temperature differences: the anterior arm.
6.3 CONCLUSIONS STUDY 3
The conclusions to the first objective of the study 3 are:
- The thermal pattern of the wheelchair athletes observed after exercise
showed a decrease in skin temperature immediately after completing
a 30 second all-out wheelchair propulsion test, followed by an
increase at ten minutes after the test. The thermal pattern presented
significant differences between the skin temperature before the test
and 10 minutes after the maximal test in 12 regions; and between the
skin temperature measured in the minute immediately following the
test and at 10 minutes afterwards in most of the regions of interest.
- In contrast to the absolute skin temperature pattern, there were very
few significant differences in left-right asymmetries at the two timepoints following the wheelchair test. The differences between the leftright skin temperature asymmetries were smaller than the differences
106
Conclusions
between the absolute values of skin temperature before and after the
wheelchair test.
The conclusions to the second objective of the study 3 are:
- After a 30 seconds maximum wheelchair propulsion test the bilateral
skin temperature difference of the posterior central trapezius, the
dorsal and the anterior trapezius was inversely related with shoulder
pain.
-
The bilateral skin temperature difference of the regions of interest is
inversely related to the performance in the wheelchair propulsion
test.
The conclusion to the third objective of the study 3 is:
-
No correlation was found between shoulder pain and the kinematic
variables of the wheelchair test.
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Isabel Rossignoli 2015
7 LIMITATIONS
There are several aspects of this research that were necessarily foregone and
that must be considered when interpreting the results and applying them in
practical situations.

A manual system was used to draw the limits of each region of interest
when analysing the thermograms (Figure 23). Consequently, the
demarcation lines of the examined area could vary slightly from one
image to the next influencing the skin temperature measurements.
Figure 23. Manual drawing of the regions of interest

The skin temperature data may have been affected by temporary injuries
in some participants, as a prior physical examination was not conducted.
In the first study, the time interval between the two infrared
thermographic measurements was reduced to one day to minimize the
thermal evolution of potential lesions, given that initial warm areas may
quickly return to normal temperatures (406).
108
Limitations

An attempt was made to control for the natural 24-hour circadian
variation in skin temperature by testing at the same time of the day.
However, a time interval of 24 hours gives the highest error of reliability
acceptable. Taking thermal images on the same day aims to isolate the
daily skin temperature (352) and skin blood flow (391) variations from
other factors. In the second study, thermographic data was collected
twice on the same day to avoid any day-to-day variation.

Individual characteristics that can affect skin temperature values, such as
the physiological variability of the blood flow, thermoregulation
problems, hormonal changes, medication intake, scars and body fat,
should be given particular considerations when making infrared
thermograpy measurements. Constraints of time and resources meant
that not all of these characteristics could be accounted for during the
studies of this thesis.

It would be preferable to use a standard wheelchair when assessing the
skin temperature in a group of wheelchair users to normalize the
backrest heights (Figure 24). However, in the third study, all subjects
used their own wheelchair to perform the exercise test, which meant that
they could propel their wheelchair without having to change their
propulsion style.
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Isabel Rossignoli 2015
Figure 24. The impact of different backrest on the thermal image. Backrest size is
dependent upon the impairment of the subject

The results of the third study suggested that 10 minutes may not be
enough time following a 30 second all-out push test for the skin
temperature to return to its pre-exercise level. A longer period spent
evaluating post-exercise skin temperature, perhaps up to 30 minutes,
may be beneficial in future studies to properly understand the thermal
response to this type of exercise.

The WUSPI test was chosen for this thesis due to its specificity for the
wheelchair using population. However, it is limited to the fact that it
focuses only on the shoulders and none of the other regions of interest
investigated in the present studies. These additional regions were
selected because of their associated musculature, which is also involved
in the wheelchair propulsion task. Moreover, the WUSPI refers only to
pain in the shoulder during the previous week; a longer clinical history
should be sought because of the potential implications for previous
injuries on the skin and the measurement of skin temperature.
110
Future Research Lines
8 FUTURE RESEARCH LINES
A number of possible research lines have emerged from the investigations of this
thesis. In the first instance, a more comprehensive evaluation of the reliability
and validity of thermographic imaging would require a range of time intervals
between the capture of images, other indoor settings, exercise modes and
athletes of various sports. Longitudinal prospective studies of infrared
thermography reliability on specific health conditions with larger and more
homogeneous samples could help to explore the clinical application of infrared
thermography on those pathologies. Future research should aim to study the
potential association between skin temperatures of the muscles involved in
wheelchair propulsion with the pain in those areas in an effort to prevent
situations of injury risk. Moreover, infrared thermography could help to detect
hypo- and hyperthermia that warn medical professionals and coaches about
potential injuries (350).
The investigations in this thesis act as a starting point to establishing more direct
relationships between skin temperature and pain and injury processes and,
eventually, perhaps employing infrared thermography within the array of injury
monitoring tools. While the correlations between skin temperature and shoulder
pain are not sufficient to support infrared thermography as a diagnostic tool for
shoulder pain (and much less, for shoulder injuries), it could be reasoned that an
increase in skin temperature may be indicative of the inflammatory process and
that without treatment, strengthening and stretching and modifications to the
daily and/or sporting tasks, the accumulative effect of the inflammatory
response could be a shoulder injury. The conclusions supports the use of
infrared thermography as one of the tools for medical professionals and sports
coaches to monitor wheelchair users in preventing overuse injuries.
Future studies would benefit from larger sample sizes and broader populations.
More participants with different levels of SCI would allow for a differentiation
between these levels of injury. Specifically, it would be possible to verify the
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Isabel Rossignoli 2015
differences of skin blood flow between subjects with SCI above and below T10
vertebrae, a crucial level in the sympathetic innervation, as well as above and
below T6 vertebrae, which is also implicated with thermoregulation.
The exercise test performed in the third study of the present thesis was a 30
second maximal intensity wheelchair propulsion test. Interestingly, Rodgers et
al. affirmed that there is a power shift in wheelchair propulsion from the
shoulder to the elbow and wrist with increasing fatigue (339). Ambrosio et al.
theorizes that this shift will not be so predominant in endurance-trained
individuals (12). One direction for future research could be identifying a
correlation between skin temperatures of the muscles involved in wheelchair
propulsion and shoulder pain following prolonged exercise. It will not only allow
time for the activation of the hypothalamus, but may also enable a possible
correlation between skin temperature and pain in other regions (such as elbow
and wrist) to be observed, which may only develop during fatigue or in
untrained wheelchair users. In this and other research that might investigate
skin temperatures in the entire upper body, more generic pain scales will need to
be employed (other than the WUSPI scale for shoulder pain used in this thesis) to
point to the regions where pain is being experienced, in real time.
112
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464. Zivcak J, Kneppo P, Hudak R, editors. Methodics of IR Imaging in SCI
Individuals Rehabilitation. IEEE-EMBS 2005 27th Annual International
Conference of the Engineering in Medice and Biology Society; 2005 Sept. 14, 2005; Shanghai, China. IEEE.
465. Zontak A, Sideman S, Verbitsky O, Beyar R. Dynamic thermography:
analysis of hand temperature during exercise. Ann Biomed Eng. 1998 NovDec;26(6):988-93.
466. Zurek G, Dudek K, Pirogowicz I, Dziuba A, Pokorski M. Influence of
mechanical hippotherapy on skin temperature responses in lower limbs in
children with cerebral palsy. J Physiol Pharmacol. 2008 Dec;59 Suppl
6:819-24.
145
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10 APPENDIXES
10.1 APPENDIX 1. EXAMPLE OF INFORMED CONSENT FORM
In the following page it is presented an example of the informed consent form
distributed to the study’s participants.
146
Confidencialidad y revisión de documentos
Usted comprende y es consiente que, con el fin de garantizar la fiabilidad de los
datos recogidos en este estudio, será preciso que representantes del Centro de
Investigación en Discapacidad Física (CIDIF), la Universidad Politécnica de
Madrid (UPM) y eventualmente las autoridades sanitarias y/ o miembros del
Comité Ético de Investigación Clínica, tengan acceso a sus datos
comprometiéndose a la más estricta confidencialidad.
De acuerdo con la Ley Orgánica 15/1999, de 13 de diciembre, de Protección de
Datos de Carácter Personal, los datos personales que se le requieren (imágenes
incluidas) serán objeto de tratamiento automatizado y se incorporan a un fichero
propiedad de ASPAYM Castilla y León, debidamente registrado en la Agencia
Española de Protección de Datos. En ninguno de los informes del estudio
aparecerá su nombre y su identidad no será revelada a persona alguna salvo
para cumplir con fines investigadores o docentes, y en caso de urgencia médica o
requerimiento legal. Cualquier información de carácter personal que pueda ser
identificable será conservada y procesada bajo condiciones de seguridad, con el
propósito de determinar los resultados del estudio. Éstos podrán ser
comunicados a las autoridades sanitarias y eventualmente, a la comunidad
científica a través de congresos y/ o publicaciones.
El abajo firmante declara haber sido informado de los riesgos e implicaciones
que conlleva la participación en el presente estudio, y autoriza la realización de
la batería de pruebas físicas y cuestionarios sobre su persona. Tras haber sido
resueltas las dudas que le hayan surgido referentes a su colaboración, manifiesta
que realiza voluntariamente dichas pruebas.
Firma del informado
Firma del testigo
DNI:_________________
DNI: _________________
Dtor. del Estudio
DNI: __________________
Valladolid, a ……… de ……… de 2010.
Centro de Investigación en Discapacidad Física, ASPAYM CASTILLA Y LEÓN
C/ Severo Ochoa, 33. Urbanización Las Piedras. 47130, Simancas, Valladolid, España.
 983 591 044 // Fax 983 591 101 //  [email protected]
Isabel Rossignoli 2015
10.2 APPENDIX 2. EXAMPLE OF THERMOGRAPHIC REPORT
148
Appendixes
149
Isabel Rossignoli 2015
10.3 APPENDIX 4. DATA COLLECTION INFORMATION SHEET FOR THE
SUBJECTS
150
Appendixes
151
Isabel Rossignoli 2015
10.4 APPENDIX 4. WUSPI TEST IN ENGLISH
The Wheelchair Users Shoulder Pain Index developed by Curtis et al. (81):
ANEXO 1. Wheelchair Users Shoulder Pain Index
Place an “X” on the scale to estimate your level of pain with the following activities. Check box at right if
the activity was not performed in the past week.
Based on your experiences in the past week, how much shoulder pain do you experience when:
1. Transferring from a bed to a wheelchair?
not performed
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
2. Transferring from a wheelchair to a car
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
3. Transferring from a wheelchair to a tub or shower?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
4. loading your wheelchair into a car?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
5. pushing your chair for 10 minutes or more?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
6. pushing up ramps or inclines outdoors?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
7. lifting objects down from an overhead shelf?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
8. putting on pants?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
9. putting on a t-shirt or pullover?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
10. putting on a button down shirt?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
11. washing your back?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
12. usual daily activities at work or school?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
13. driving?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
14. performing household chores?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
15. sleeping?
No pain [ ] _________________________________________________ Worst Pain Ever Experienced [ ]
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Appendixes
10.5 APPENDIX 5. WUSPI TEST IN SPANISH
The Wheelchair Users Shoulder Pain Index validated to Spanish by Arroyo-Aljaro
et al. (23):
ANEXO 2. Wheelchair Users Shoulder Pain Index (Castellano)
Coloque una “X” en la escala para estimar su nivel de dolor con las siguientes actividades. Marcar la caja “[
]” de la derecha si no ha realizado la actividad en la pasada semana.
Basado en su experiencia de la semana pasada, con qué intensidad le ha dolido el hombro cuando estaba:
1. pasando desde una cama a una silla de ruedas?
No realizado
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
2. pasando desde una silla de ruedas a un coche?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
3. pasando desde una silla de ruedas a un baño o ducha?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
4. cargando una silla de ruedas en el coche?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
5. empujando una silla durante 10 minutos o más?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
6. empujando una silla hacia arriba en rampas o pendientes exteriores?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
7. bajando objetos desde un estante situado por encima de la cabeza?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
8. colocándose los pantalones?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
9. colocándose una camiseta o jersey?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
10. colocándose una camisa de botones?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
11. lavándose la espalda?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
12. en actividades habituales diarias en el trabajo, el colegio o la universidad?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
13. conduciendo?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
14. realizando las tareas del hogar?
Sin dolor [ ] _________________________________________________ Peor dolor que nunca ha
experimentado [ ]
15. durmiendo?
Sin dolor [ ] __________________________________________________Peor dolor que nunca ha
experimentado [ ]
153
Isabel Rossignoli 2015
154
Curriculum Vitae
11 SUMMARIZED CV / CURRICULUM VITAE ABREVIADO
1. ACTIVIDAD LABORAL
2015-2016
2015
2012-2015
2014-2015
2011-2012
2010-2012
2010-2012
2010-2012
2010-2011
2009-2010
2009-2010
2008
2008-2012
2008
2004, 2007,
2010-2012
Profesor Asociado de la Universidad Isabel I de Castilla. Asignatura: Actividad Física
y Discapacidad Física.
Asesor y miembro de la Comisión de Clasificación del Comité Paralímpico Español
(CPE), España.
IPC Classification Research Manager, International Paralympic Committee (IPC),
Alemania.
Ponente en: la Universidad Complutense de Madrid (UCM), Facultad de Medicina,
asignatura “Valoración del daño funcional”; en la Universidad Politécnica de Madrid
(UPM), Facultad de Ciencias de la Actividad Física y el Deporte (INEF), asignatura de
doctorado “Diseño de Experimentos”, conferencia “Investigación en el Movimiento
Paralímpico”; en la Universidad Europea Miguel de Cervantes, conferencia: “Del
INEF al Comité Paralímpico Internacional”.
Profesor Asociado de la Universidad Camilo José Cela (UCJC). Asignatura: Educación
Física y su Didáctica (Troncal).
Investigador colaborador del Laboratorio de Fisiología del Esfuerzo Humano del
Departamento Salud y Rendimiento, INEF, UPM.
Investigador colaborador del Centro de Investigación en Discapacidad Física (CIDIF),
ASPAYM Castilla y León.
Investigador colaborador en la empresa spin off pemaGROUP (Prevención de
Lesiones mediante termografía infrarroja), empresa ganadora del 4º premio en la
VII de actúaUPM, concurso de creación de empresas de la UPM, Diciembre 2010; y 1º
premio del VIII concurso de creación de empresas CIADE de la Universidad
Autónoma de Madrid, Diciembre 2010; premio al Mejor Plan de Empresa Madri+d,
2011.
Profesor Ponente de la UPM. Asignatura: Actividades y Deportes de Montaña
(Optativa).
Profesor Asociado de la Universidad Camilo José Cela (UCJC). Asignatura: Educación
Física y su Didáctica (Troncal).
Profesor Ponente de la UPM. Asignatura: Deportes Adaptados a Personas con
Discapacidad Física (Obligatoria).
Terapeuta deportivo en el Hospital Beitostolen Helsesportsenter (Noruega).
Profesor de Deportes Adaptados de la Federación Española de Atletismo, curso de
Entrenador Nacional de Atletismo, Escuela Nacional de Entrenadores de Atletismo.
Ponente y organizador del curso de “Deporte Adaptado” ofrecido en colaboración con
la Dirección General de Educación Física de Guatemala.
Personal técnico de apoyo en las pruebas de esfuerzo máximo del Laboratorio de
Fisiología del Esfuerzo del INEF, UPM.
2. FORMACIÓN
2008-2009
Erasmus Mundus Master in Adapted Physical Activity por la Katholieke Universiteit
Leuven (Bélgica), European Comission Education & Training, Beitostølen
Helsesportsenter (Noruega), University of Queensland (Australia).
155
Isabel Rossignoli 2015
2006-2008
2005-2007
2005-2006
2005-2006
2004-2005
2000-2005
156
Máster Oficial de Postgrado en Investigación en Ciencias de la Actividad Física y el
Deporte. Diploma de Estudios Avanzados (DEA) INEF, UPM.
Diplomada en Magisterio de Educación Física en la UCM.
Certificado de Aptitud Pedagógica (C.A.P.) en el INEF, UPM.
Entrenador Nacional de Atletismo, por la Real Federación Española de Atletismo.
Entrenador Superior de Natación, por la Real Federación Española de Natación.
Licenciada en Ciencias de la Actividad Física y el Deporte en el INEF, UPM.
Especialidades: judo, natación y hockey. Maestrías en Natación y Deportes Adaptados
de Alto Rendimiento. Itinerarios: Educación e Investigación en Deporte Adaptado.
3. ACTIVIDAD INVESTIGADORA
Comunicaciones y póster en congresos
2015, 3-5
septiembre
2014, 25
noviembre
2013, 1-4
mayo
2012, 3-5
septiembre
2011, 15
diciembre
2011, 4-8
julio
2010, 6-8
mayo
2008, 9-11
octubre
2008, 2-5
abril
“Infrared Thermography and Shoulder Pain in Wheelchair Users”. Autores: Isabel
Rossignoli, Manuel Sillero-Quintana, Azael J Herrero. Congreso: XIII Congress of the
European Association of Thermology, INEF Madrid 2015.
"Reliability of Infrared Thermography in Skin Temperature Evaluation of Wheelchair
Users". Autores: Isabel Rossignoli, Pedro J Benito, Azael J Herrero. Journal: Spinal
Cord. 2014 Nov 25;53:243-8. doi:10.1038/sc.2014.212.
“Relationship between perceived shoulder pain and kinematic analysis of wheelchair
propulsion in sedentary and active wheelchair users”. Autor: Isabel Rossignoli.
Congreso: VISTA 2013 Scientific Conference – Equipment & Technology in
Paralympic Sports, International Paralympic Committee, Bonn (Germany).
“Risk factors of shoulder pain and shoulder functionality in athletes and sedentary
wheelchair users”. Autores: Azael Herrero, Isabel Rossignoli, Héctor Menéndez, Juan
Martín, Cristina Ferrero, Pedro J. Marín. Congreso: International Spinal Cord Society,
51ST Annual Scientific Meeting, ISCOS 2012 – Advances in Spinal Cord Injury
Management. Londres (Inglaterra).
“Factores de riesgo del dolor y de la funcionalidad en la articulación del hombro en
usuarios en silla de ruedas sedentarios y deportista”. Autores: Azael J. Herrero, Isabel
Rossignoli1, Héctor Menéndez, Juan Martín, Cristina Ferrero y Pedro J. Marín.
Congreso: CIDA 2011, III Conferencia Internacional sobre Deporte Adaptado,
Fundación Andalucía Olímpica. Málaga (España).
“Infrared Thermography in people with disabilities: a comparison between athletes
and sedentary wheelchair users”. Autores: Isabel Rossignoli, Azael Herrero, Pedro J
Benito. Congreso: 18th International Symposium on Adapted Physical Activity,
International Federation of Adapted Physical Activity. París (Francia)
“Pilot Evaluation of Methods for Measuring Sports-Specific Coordination”. Autores:
Isabel Rossignoli, Sean Tweedy, Alice Neiuwboer. Congreso: European Congress of
Adapted Physical Activity 2010 / Finish Congress of Adapted Physical Activity,
University of Jyväskylä and Finnish Society of Sport Sciences. Jyväskylä (Finlandia).
“Direct and on-court measurement of maximal aerobic performance of elite
wheelchair basketball players”. Autores: Isabel Rossignoli, Javier Pérez. Congreso:
European Congress of Adapted Physical Activity 2008 / Congress of EUFAPA,
Universita Degu Studi Di Torino. Torino (Italia)
"Medición directa en campo de la potencia aeróbica máxima de jugadores de
baloncesto en silla de ruedas de alto nivel". Autores: Isabel Rossignoli, Javier Pérez,
Pedro J Benito. Congreso: IV Congreso Internacional y XXV Nacional de Educación
Física, Facultad de Ciencias de la Educación, Universidad de Córdoba. Córdoba
(España).
156
Curriculum Vitae
2006, 16-20
mayo
2005, 19-22
octubre
“Shoulder Pain in Spanish Wheelchair Basketball Players: a pilot study”. Autores:
Javier Pérez, Isabel Rossignoli, Raquel Martínez. Congreso: 15 Congreso Europeo de
Medicina Física y Rehabilitación/44 Congreso Nacional de la Sociedad Española de
Rehabilitación y Medicina Física, Physical Medicine and Rehabilitation Department;
University of Medicine (UCM); Hospital Clínico San Carlos (Madrid); Departamento
de Medicina Física y Rehabilitación de la Facultad de Medicina (UCM); Hospital
Clínico San Carlos (Madrid). Madrid (España).
“Análisis biomecánico y muscular de la impulsión en silla de ruedas”. Autor/es: Isabel
Rossignoli, José Artacho, Javier Pérez. Congreso: I Congreso Internacional sobre
Deporte Adaptado, Facultad del Deporte de Toledo – Fundación del Hospital Nacional
de Parapléjicos de Toledo para la Investigación y la Integración. Toledo (España).
Participación en proyectos de investigación
2014
2013-2014
2013-2014
2013
2013
2010-2011
2010
2010-2012
2009-2011
2008-2009
Colaboración en el proyecto del Comité Paralímpico Internacional (IPC) y Anglia
Ruskin University: “IPC Shooting Classification Research Project”, organización toma
de datos y supervisión del proyecto.
Colaboración en el proyecto del IPC y Vrije Universitet Amsterdam: “IPC Swimming
Classification Research Project”, toma de datos durante los Campeonatos del Mundo
de Natación adaptado en Eindhoven, Holanda; organización de meetings de expertos;
supervisión del proyecto.
Colaboración en el proyecto del IPC, Salzburg University, University of Tübingen, y
University of Jÿvaskyla: “IPC Nordic Skiing Classification Research Project”, toma de
datos durante los Campeonatos del Mundo de Esquí Nórdico adaptado en Sollefteå,
Suecia; organización de meetings de expertos; supervisión del proyecto.
Colaboración en el proyecto del IPC y University of Queensland: “IPC Atletics
Classification Research Project”, toma de datos en Nairobi, Kenia.
Colaboración en el proyecto del IPC: “IPC Para-snowboard Classification Research
Project”, toma de datos en Cooper Mountain y Lake Tahoe, USA; organización de
meeting de expertos.
Investigador principal en el proyecto del CIDIF y UPM: “Factores de riesgo del dolor y
de la funcionalidad en la articulación del hombro en usuarios de silla de ruedas
sedentarios y deportistas”.
Colaboración en el proyecto del Grupo “PemaSiP” del Departamento de Deportes en
el INEF y CSD: “Aplicación de la termografía como medio para la prevención de
lesiones en deportistas de alto rendimiento (THERMOPREVENT)”.
Colaboración en el proyecto del INEF, Ministerio de Ciencia e Innovación, Federación
Española de Gimnasia, Asociación de Padres y Familiares de Minusválidos Psíquicos
y Sensoriales, Servicio Deportivo Munical de Leganés, Getafe FC SAD, Federación de
Autismo de Madrid, Álava Ingenieros S.A., Rayo Vallecano CF SAD: “La termografía
como medio de detección, prevención y seguimiento de problemas y lesiones
derivados de la actividad físico-deportiva en poblaciones especiales
(THERMOSPEC)”.
Proyecto I+D: con el Departamento de Salud y Rendimiento Humano del INEF, UPM;
el Instituto de Investigación Marqués de Valdecilla – Universidad de Cantabria; y el
Servicio de Nutrición, IDIPAZ, Hospital Universitario de la Paz: “PRONAF PROgramas
de Nutrición y Actividad Física para el tratamiento de la obesidad”. Ministerio de
Ciencia e Innovación. DEP2008-06354-C04-01.
Proyecto del master en la Universidad de Queensland, Australia: “Towards Evidence
Based Classification In Paralympic Athletics: Pilot Evaluation Of Methods For
Measuring Sports-Specific Coordination”. En colaboración con el IPC.
157
Isabel Rossignoli 2015
2007-2008
2007
2004-2005
158
Proyecto para la elaboración del Diploma de Estudios Avanzados (DEA) en el INEF,
UPM: “Valoración funcional en deportistas con discapacidad física de alto nivel:
evaluación de la salud, tests de laboratorio y de campo”.
Proyecto del CSD y el Laboratorio de Fisiología del Esfuerzo del INEF, UPM:
“Valoración de las variables fisiológicas en competición al equipo nacional de lucha”.
Proyecto de promoción del Deporte Adaptado “Hospisport en Madrid”, INEF, UPM.
Publicaciones científicas

Rossignoli I, Benito PJ, Herrero AJ. Reliability of infrared thermography in skin
temperature evaluation of wheelchair users. Spinal Cord. 2014;53:243-8.

Rossignoli I, Herrero AJ, Menéndez H, Sillero M, Benito PJ. Relationship between
perceived shoulder pain and infrared thermography in wheelchair athletes and
nonathletes. Disability and Health Journal. (Submitted)

Rossignoli I, Fernández-Cuevas I, Benito PJ, Herrero AJ. Relationship between
shoulder pain and skin temperature measured by infrared thermography in a
wheelchair propulsion test. Infrared Physics and Technology. (Submitted)
Estancias predoctorales en el extranjero

Centro: Faculty of Kinesiology and Rehabilitation Sciences, Katholieke Universiteit
Leuven. Localidad: Leuven, Bélgica. Duración: agosto-octubre 2008 y enero 2009, 4
meses.

Centro: The Norweigan School of Sport Science, The Norwegian University of Sport
and Physical Education. Localidad: Beitostolen, Noruega. Duración: noviembrediciembre 2009, 2 meses.

Centro: School of Human Movement Studies, University of Queensland. Localidad:
Brisbane, Australia. Duración: febrero-abril y agosto 2009, 4 meses.
4. OTROS DATOS DE INTERÉS

Premio de investigación 2008 del Convenio INEF-Consejo Superior de Deportes
(CSD) por el Diploma de Estudios Avanzados (DEA). Proyecto: "Valoración funcional
en deportistas de alto rendimiento con discapacidad física: evaluación de la salud,
test de laboratorio y de campo" realizado en el INEF, UPM.

Miembro del grupo de investigación internacional: European Research Group in
Disability Sport (ERGiDS).

Amplio historial deportivo en competiciones de Judo desde 1992 al 2007.

Miembro del equipo alpino internacional: The Mountain Academy, patrocinado por
Mountain Hardware y Black Diamond.

Compitiendo en escalada deportiva desde 2011, siendo en la actualidad Campeona
de España Universitaria de Escalada 2015.
158
Facultad de Ciencias de la Actividad Física y el
Deporte – INEF: 11
Isabel Rossignoli Fernández
2015