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Journal of Bodywork & Movement Therapies (2015) xx, 1e7
Available online at www.sciencedirect.com
ScienceDirect
journal homepage: www.elsevier.com/jbmt
EXERCISE PHYSIOLOGY: UNCONTROLLED CLINICAL TRIAL
The Pilates Method increases respiratory
muscle strength and performance as well as
abdominal muscle thickness*
Mateus Beltrame Giacomini, Msc a,
Antônio Marcos Vargas da Silva, DSc b,
Laura Menezes Weber, Physiotherapist, Specialist in Physical
Rehabilitation b, Mariane Borba Monteiro, DSc c,*
a
Rehabilitation and Inclusion, Centro Universitário Metodista IPA, Porto Alegre, RS, Brazil
Universidade Federal de Santa Maria, Santa Maria, RS, Brazil
c
Centro Universitário Metodista, IPA and Universidade Federal de Ciências da Saúde de Porto Alegre,
Porto Alegre, RS, Brazil
b
Received 14 July 2015; received in revised form 21 October 2015; accepted 30 October 2015
KEYWORDS
Pilates Method;
Abdominal muscles;
Respiratory muscles;
Women
Summary The aim of this study was to verify the effects of the Pilates Method (PM) training
program on the thickness of the abdominal wall muscles, respiratory muscle strength and performance, and lung function. This uncontrolled clinical trial involved 16 sedentary women who
were assessed before and after eight weeks of PM training. The thickness of the transversus
abdominis (TrA), internal oblique (IO) and external oblique (EO) muscles was assessed. The respiratory muscle strength was assessed by measuring the maximum inspiratory (MIP) and expiratory (MEP) pressure. The lung function and respiratory muscle performance were assessed by
spirometry. An increase was found in MIP (p Z 0.001), MEP (p Z 0.031), maximum voluntary
ventilation (p Z 0.020) and the TrA (p < 0.001), IO (p Z 0.002) and EO (p < 0.001) thickness
after the PM program. No alterations in lung function were found. These findings suggest that
the PM program promotes abdominal wall muscle hypertrophy and an increase in respiratory
muscle strength and performance, preventing weakness in abdominal muscles and dysfunction
in ventilatory mechanics, which could favor the appearance of illnesses.
ª 2015 Elsevier Ltd. All rights reserved.
*
Study developed at Centro Universitário Metodista, IPA, Porto Alegre, RS, Brazil.
* Corresponding author.
E-mail address: [email protected] (M.B. Monteiro).
http://dx.doi.org/10.1016/j.jbmt.2015.11.003
1360-8592/ª 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Giacomini, M.B., et al., The Pilates Method increases respiratory muscle strength and performance as
well as abdominal muscle thickness, Journal of Bodywork & Movement Therapies (2015), http://dx.doi.org/10.1016/j.jbmt.2015.11.003
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Introduction
The Pilates Method (PM) can be regarded as an exercise
technique with a focus on body awareness, where body self
perception is improved during its practice, thus connecting
the body and mind. PM based exercises have been used for
prevention, rehabilitation, physical conditioning (Andrade
et al., 2015), and enhancement in mindfulness, associated with wellness (Caldwell et al., 2013).
Initially, the PM took the name Contrology because its
creator Joseph Pilates believed that we should have a
conscious control of our body movements (Barbosa et al.,
2015). The PM is a comprehensive conditioning method
that embraces six fundamental and interrelated principles:
centering, concentration, control, precision, breathing and
movement flow (Muscolino and Cipriani, 2004).
Contrology is the complete coordination of body, mind
and spirit. It develops the body uniformly, corrects wrong
postures, restores physical activity, invigorates the mind,
and elevates the spirit (Muscolino and Cipriani, 2004).
Exercises based on PM principles have been widely used,
both with the aid of specific equipment or on the floor on a
Pilates Mat (Da Luz et al., 2013). The PM has become
popular in rehabilitation and fitness programs. The aims of
Pilates training are the improvement of general body
strength and flexibility, with an emphasis on the core, good
posture and alignment and breathing coordination with
movement (Guimarães et al., 2012).
The core is the main focus of the PM and is composed of
the abdominal muscles (rectus abdominis, internal and
external obliques, transversus abdominis, lumbar paravertebral muscles, quadratus lumborum), hip extensors
(gluteus maximus, hamstrings, adductor magnus), hip
flexors (iliopsoas, rectus femoris, satorius, tensor fasciae
latae), the pelvic floor musculature (perineal muscles) and
diaphragm, which are responsible for the static and dynamic stabilization of the body (Muscolino and Cipriani,
2004).
Breathing control is fundamental during the execution
of PM exercises, where the practitioner learns how to
breathe properly as an essential part of each exercise
through forceful exhaling followed by complete inhaling.
Thus, adequate breathing aids in controlling movements
(Pilates and Miller, 2010), and therefore, the method can
be regarded as an indirect strategy for respiratory muscle
training. It is known that poor control of breathing can
result in compensation and lung volumes and respiratory
muscle performance, with several factors involved. This is
consistent with the literature, as seen in Hackett et al.
(2013), showing a greater lung function in athletes when
compared with sedentary individuals. People who perform
physical activities regularly present greater respiratory
endurance (Martin and Stager, 1981), as well as superior
lung volume and inspiratory and expiratory flow rates than
the general population (Morrow et al., 1989).
Recent studies have demonstrated that the PM leads to
abdominal wall muscle hypertrophy, as assessed by magnetic resonance imaging (Dorado et al., 2012) and ultrasound (Critchley et al., 2011). In light of these findings, the
hypothesis that even without the use of a specific training
load on respiratory muscles, the PM can favor an increase in
M.B. Giacomini et al.
respiratory muscle strength and its performance appears
plausible. Still, the influence of the PM on the lung function
of healthy subjects needs further clarification, as the reports in healthy subjects are scarce and do not clearly state
its relation to lung function (Niehues et al., 2015).
To provide a wide evaluation of the performance of the
respiratory and abdominal muscles involved in the practice
of PM, the aim of this study was to verify the effects of a PM
Mat training program on abdominal wall muscles thickness,
respiratory muscle strength and performance, and lung
function in healthy women.
Methods
Subjects
This study is an uncontrolled clinical trial (register number
on REBEC e Brazilian Register of Clinic Trials: RBR-538g6x)
involving 16 voluntary women that are sedentary (not
engaged in regular physical activity for at least 6 months),
non-smoking, and inexperienced in PM, with no reports of
lumbar pain, physical limitations, cardiorespiratory or
musculoskeletal disease.The volunteers did not present a
medical history diagnosed for any of the previously stated
conditions, as well as any other which could interfere in the
execution of the training program or results of the study.
The recruitment of the volunteers occurred in a nonprobabilistic manner by convenience, through printing
press adds, online social network promotion, free search
for PM and posters placed in fitness gyms in the city of Santa
Maria e RS, Brazil.
The research was conducted at the Prana Academia gym
in Santa Maria e RS, Brazil. The project was approved by
the Research Ethics Committee of the research origin
institution under protocol number 271/2012, and all of the
subjects were informed of the study procedures and signed
the Free and Clarified Consent Term.
Assessments
All of the evaluations occurred before and after the 8 week
PM training period, including an ultrasound (US) for
measuring abdominal wall muscle thickness, a manovacuometry test for measuring respiratory muscle strength
and spirometry for assessing lung function and respiratory
muscle performance.
The abdominal wall US exam was conducted at a private company in Santa Maria/RS, where images were
collected measuring the thickness of the following
abdominal wall muscles: external oblique (EO), internal
oblique (IO) and abdominis transversus (TrA), all in a
resting position. The equipment used to verify muscle
thickness in millimeters (mm) was a model My Lab 50x
Vision, Esaote maker in B- Mode (Paris, France) with a
linear 10 Hz transducer. The US image collection after
training occurred 48 h after the last training session. The
exams were performed by the same doctor, licensed in the
US, who explained the exam procedures as the volunteer
lay in the supine position in a suitable stretcher. The images were obtained with the transducer positioned anterolaterally on the right abdomen, centered between the
Please cite this article in press as: Giacomini, M.B., et al., The Pilates Method increases respiratory muscle strength and performance as
well as abdominal muscle thickness, Journal of Bodywork & Movement Therapies (2015), http://dx.doi.org/10.1016/j.jbmt.2015.11.003
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The Pilates Method increases respiratory muscle strength
anterior iliac crest and the midaxillary line, and were
registered at the end of the expiratory phase on the level
of the air flow volume.
The manovacuometry test, validated by American
Thoracic Society/European Respiratory Society (2002),
was carried out using a digital manovacuometer (MVD 300,
Microhard System, Globalmed, Porto Alegre, Brazil),
following the Guidelines for Lung Function Tests from the
Brazilian Society of Pneumology (Souza, 2002), with the
volunteer in seated position with a nasal clip. To determine
the inspiratory muscle strength, the maximum inspiratory
pressure (MIP) obtained with the forced maximum inspiration maneuver from the residual volume was measured. The
expiratory muscle strength was assessed by the maximum
expiratory pressure (MEP), with a forced maximum expiration from the total lung capacity. The maneuvers were
performed five times, with a one-minute interval in between each maneuver. The highest MIP and MEP values
were registered when the difference between the two
highest measures was lower than 10% (Souza, 2002). The
predicted values were considered as proposed by Neder
et al. (1999).
The lung function and respiratory muscle performance
were assessed by spirometry using a portable spirometer
(Spirobank II, Medical International Research, Rome,
Italy). The predicted values were considered to be normal
according to Pereira (2002). The volunteers remained
seated and were advised to rest for five minutes prior to the
test. Afterwards, the volunteers carried out a maximum
inhalation inspiration, followed by a maximum expiration,
sustaining the breath through the mouthpiece of the device
until the observer determined the interruption. As recommended by the American Thoracic Society and the European
Respiratory Society (2006) and based on the reproducibility
and acceptability criteria, three exercises were performed
(variability <5%) and the best curve was considered for the
study. The data obtained from this process included the
forced vital capacity (FVC), forced expiratory volume in one
second (FEV1), FEV1/FVC relation (FEV1/FVC), peak expiratory flow (PEF) and forced expiratory flow between 25 and
75% of the FVC curve (FEF25e75%). The respiratory muscle
performance was estimated by the maximum voluntary
ventilation (MVV) measure, with the individual being
instructed to inhale and exhale repeatedly through the
spirometer mouthpiece with the greatest possible effort for
10 s. The values were registered in absolute measurement
units and as a percentage of the predicted values.
Pilates Method training
The PM lessons occurred in two weekly sessions, 60 min per
lesson, for eight weeks, with a maximum three volunteers
per session. All of the lessons were administered by the
same professional who had experience with and was qualified on the method and coached the individuals during all
exercises, ensuring thus an adequate execution of all
movements. The Original PM training protocol was carried
out in the following manner: the sessions began with PM
fundaments (breathing, imprinting, pelvic bowl, knee sway,
knee folds/stirs, leg slides, spinal bridging, prone hip
extension, cervical nod, nose circles, head float, ribcage,
rotation arms, torso twist, flight, cat, bowing), which seek
3
greater body awareness through primary movements that
are executed along with before-Pilates exercises (the
hundred, roll down, roll up, single leg circles, rolling like a
ball, single leg stretch, double leg stretch, spine stretch
forward). Afterwards, the basic and intermediate level
phase exercises began (the hundred, the rollup, single leg
circles, rolling like a ball, single leg stretch, double leg
stretch, single straight leg, double straight leg, criss cross,
spine stretch forward, open leg rocker, corkscrew, saw,
neckroll, single leg kicks, double leg kicks, neck pull,
sidekicks series, small circles, teaser, seal), always taking
into account the principles of the method and the biological
individuality of each participant. Throughout the exercises,
the volunteers were advised to associate conscious
breathing to movement through the command to inhale
during the preparation/initial position phase and, as the
movement progressed during the execution of the exercise,
slow exhaling was suggested. Some exercises were
repeated from one phase to the other and differed by the
modulating elements, where the exercise progressed or
regressed modifying articular amplitudes of the lever arm
and the support basis on the Mat (floor).
All of the volunteers performed the same training protocol, with the same exercises and PM fundaments, with an
average of 20 exercises per training session and 3 to 10
repetitions per exercise progression. All of the sessions
were instructed by the same professional qualified by the
Pilates Brazilian Association (ABP) and by Metacorpus
Pilates. The attendance was noted, and any absence level
over 25% was representative of sample loss.
The design of the study is presented in Fig. 1.
Statistical analysis
The data were analyzed in the Sigma Stat v. 3.1 statistic
program for Windows and are expressed as the
average standard deviation (SD). The data distribution
was assessed via ShapiroeWilk test. The comparison of the
before and after training data were assessed with Student’s
t-test for dependent samples or the Wilcoxon test (variables with asymmetrical distribution). The significance
level was 5% (p < 0.05).
Results
Twenty-six volunteers were studied, eight of whom were
excluded for not completing 75% attendance to the training
sessions, one for reporting lumbar spine pain during some
exercises and one for pregnancy. The analyzed sample
consisted of 16 volunteers, aged 32.4 10.4 years old, who
had a body mass index (BMI) of 23.1 3.00 kg/m2.
Table 1 presents the results of the abdominal wall
muscles thickness and respiratory muscle strength
measured by MIP and MEP. The TrA thickness increased in
42.3%, IO in 21% and EO in 53% of the participants, all with a
significant difference. A significant increase of 19.5% on MIP
and 8.7% on MEP was also found.
A significant improvement in the respiratory muscle
performance was found, with an increase of 11.5% on MVV,
which presented an asymmetrical distribution. The PEF also
increased by 7.4% after PM. No significant differences were
Please cite this article in press as: Giacomini, M.B., et al., The Pilates Method increases respiratory muscle strength and performance as
well as abdominal muscle thickness, Journal of Bodywork & Movement Therapies (2015), http://dx.doi.org/10.1016/j.jbmt.2015.11.003
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M.B. Giacomini et al.
Volunteers
Table 2 Respiratory muscle performance and lung function before and after the PM training.
Before
Respect the
Inclusion and
Exclusion Criteria
No
Removal
from the
study
Yes
Invitation and Signature of
the FCCT.
Assessment: Form,
Spirometry,
Manovacuometry and
Ultrasound.
8 weeks
Assessment: Spirometry,
Manovacuometry and
Ultrasound.
Results Analysis
Study design.
Table 1 Abdominal wall muscle thickness and respiratory
muscle strength before and after the PM training.
Before
TrA resting (mm)
IO resting (mm)
EO resting (mm)
MIP (cmH2O)
MIP (%pred)
MEP (cmH2O)
MEP (%pred)
3.7
6.3
3.7
80.8
86.3
98.9
104.7
After
0.8
0.7
0.9
18.1
22.4
25.1
30.9
114.1
102.7
3.7
105.6
3.1
102.2
6.7
96.5
3.5
13.9
12.3
0.5
17
0.5
14.9
0.8
12.6
0.9
90.6 21.2
84.2 6.7
101.4 6.7
127.2
114.6
3.7
103.7
3.1
99.1
7.2
102.9
3.3
Value
of p
13.5
12.2
0.5
13.3
0.4
10.8
0.9
15.4
0.8
0.020
0.019
0.888
1.000
0.517
0.693
0.004
0.005
0.845
85.4 21.1
0.764
77.5 21.1
99.3 8.9
0.354
0.821
MVV: Maximum Voluntary Ventilation; FVC; Forced Vital Capacity; FEV1: forced expiratory volume in one second; PEF: Peak
Expiratory Flow; FEF25e75%: forced expiratory flow between 25
and 75% of the FVC curve; FEV1/FVC: FEV1/FVC relation; %pred:
percentage of predicted value.
PM Traininig Protocol
Figure 1
MVV (L/min)
MVV (%pred)
FVC (L)
FVC (%pred)
FEV1 (L)
FEV1 (%pred)
PEF (L/s)
PEF (%pred)
FEF25e75% (L/
s)
FEF25e75%
(%pred)
FEVF1/FVC
FEV1/FVC
(%pred)
After
5.3
7.6
5.6
96.5
103.1
107.5
113.4
p
0.9
1.6
1.3
23.8
28.4
16.4
23.5
<0.001
0.002
<0.001
0.001
0.001
0.031
0.029
TrA: transversus abdominis; IO: internal oblique; EO: external
oblique; MIP: maximum inspiratory pressure; MEP: maximum
expiratory pressure.
found for the FVC, FEV1, FEV1/FVC and FEF25e75%. All of the
participants presented lung function data within the normal
range, with values close to 100% of the expected values
(Table 2).
Discussion
The main findings in our study demonstrated an increase in
the strength and respiratory muscle performance and in the
abdominal wall muscle thickness after eight weeks of PM
training in healthy women.
The PM promoted a significant increase in the parameters related to respiratory muscle function, as represented
by an increase in MIP, MEP and MVV. The improvement in
respiratory muscle strength has been reported in some
studies that evaluated the effects of different physical
exercise protocols on patients with cystic fibrosis (Dassios
et al., 2013), in healthy subjects (Dunham and Harms,
2012) and in athletes (Hackett et al., 2013).
The increase in MIP and MEP may be attributed to a total
improvement of the respiratory muscle system, the development of strength in respiratory muscles may be influenced by the mechanical characteristics of the chest and
abdominal wall, just as the recruitment of the diaphragm
along with other respiratory muscles contribute to stabilizing the trunk and it supplies stimulation for the increase
in respiratory muscle strength (Hackett et al., 2013).
Other current reports demonstrated that specific programs for respiratory muscle training also improved the
respiratory muscle strength in patients with heart failure
(Plentz et al., 2012), quadriplegics (Tamplin and Berlowitz,
2014), and obese (Edwards et al., 2012) and healthy individuals (Enright and Unnithan, 2011). Such data support
our findings; however, no previous studies have evaluated
the effects of PM on respiratory muscle strength.
During the PM training, the volunteers were constantly
stimulated to execute an active respiratory pattern through
the abdominal deflation maneuver (MEA), which is the action of “pulling” the abdomen towards the spine. Approximately 200 active respiratory cycles were made in each
session, which may explain the improvement in respiratory
muscle function, even without using a specific respiratory
muscle training method.
Please cite this article in press as: Giacomini, M.B., et al., The Pilates Method increases respiratory muscle strength and performance as
well as abdominal muscle thickness, Journal of Bodywork & Movement Therapies (2015), http://dx.doi.org/10.1016/j.jbmt.2015.11.003
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The Pilates Method increases respiratory muscle strength
There still is a lack of consensus in regards to the amount
of effort for obtaining gains in respiratory muscle functions.
Dassios et al. (2013) suggests that a minimum of three
forty-five minute workouts per week of moderate to
vigorous intensity is adequate do exert beneficiary effects
on respiratory muscle strength.
Our results may also be attributed to respiratory reeducation via the PM with a direct interference in respiratory muscle action and work (Forgiarini et al., 2007). Our
findings are also consistent with a study that adopted Yoga
respiratory exercises, also without specific loads to the
respiratory muscles, to promote MIP, MEP and MVV in
elderly people (Cebrià et al., 2013).
All of the volunteers presented normal lung function
with no alterations, except an increase in PEF, in response
to the PM. Some studies report that lung function does not
change during respiratory muscle training (Tamplin and
Berlowitz, 2014) or would occur only with high training
loads (80% MIP) (Enright and Unnithan, 2011). This effect
was not the aim of our investigation because lung function
evaluation was a control variable and we did not hypothesize that alterations would occur in response to the PM
training. Up to the present moment there have not been
found any reports of an improvement in PEF due to the PM.
Given that the PEF results from the expiratory muscle potency, its increase may be secondary to the improvement in
respiratory muscle strength and performance as well as
muscle thickness.
The present study found an increase on EO, IO and TrA
muscle thickness during rest. In similar study (Critchley
et al., 2011) identified an increase in TrA thickness after
PM training only during the “Hundreds A” exercise, but
without alterations in any of the abdominal wall muscles
during rest. In such study, the volunteers received verbal
instructions from a physiotherapy undergraduate student
along, with texts and pictures about the exercises which
were then made without individual supervision and executed
in training sessions at home in a 45-min programme, twice a
week, for eight weeks. Positive results, however, were found
in Dorado’s study (Dorado et al., 2012), where after 36 weeks
of PM equipment training coached by a licensed instructor
with groups of 4 participants, an increase in the rectus
abdominis was found along with a reduction of pre-existing
asymmetries of the abdominal wall muscles in women;
however, this study, similar to ours, also lacks a control
group.
Our results demonstrated that the increase in the
abdominal wall muscle thickness was greater than that
observed in similar studies, perhaps due our protocol that
included a higher number of exercises than other studies.
Furthermore, the floor exercises were executed following
the PM principles and were supervised during the entire
time session to ensure correct execution.
The trunk flexion movement in the PM is a common action that uses eccentric and concentric muscle contractions
in combination with isometric contractions, thus maintaining a flexed trunk while moving the extremities (Dorado
et al., 2012), with a support from the gluteus and lumbar
paravertebral muscles, which are responsible for the static
and dynamic stabilization of the body (Muscolino and
Cipriani, 2004). Eccentric and isometric muscle contractions may provoke substantial muscle hypertrophy and may
5
occur early in a training program (Defreitas et al., 2011),
which considering our volunteers’ sedentary condition, may
explain the expressive increment in abdominal muscle
trophism, as well as in any other report of increased
abdominal strength and endurance after strength training
in sedentary women (Sekendiz et al., 2010).
Another factor that may considerably interfere with the
PM training is the MEA, which is the adequate contraction of
the TrA during the exercises that helps to stabilize the spine
(Pilates and Miller, 2010). Some reports claim that if the
MEA is executed properly, an improvement in the TrA muscle thickness is possible, as much during the execution of
the exercises as after the PM and static stabilization programs (Herrington and Davies, 2005; Stevens et al., 2007).
The TrA muscle and diaphragm act both over posture control
as over breathing, presenting an opposite action on the
chest and abdomen as mechanical consequence of this
contraction, however, the result of the combined activation
of these muscles supplies a mechanism for the central
nervous system to coordinate breathing and spine control
during the movements (Hodges and Gandevia, 2000).
The proper execution of the MEA was one of the priorities during the PM sessions in our study, which may have
carried a fundamental role in the abdominal muscle hypertrophy of our volunteers.
Our results may be justified through adaptations to
physical exercise, allowing the generation of alterations in
the contractile, morphologic and metabolic properties of
the muscle fibers, modifying the length, diameter, strength
and type of fiber (Verdijk et al., 2009; Polito et al., 2010).
The muscle adaptations occur due to muscle tension stimuli, and they materialized themselves as the activation
factor for satellite cells, for these stimuli (tension) induce
the liberation of nitric oxide hepatocyte growth factors,
signalling the establishment of DNA synthesis and the
consequential musculoskeletal tissue (Tatsumi and Allen,
2004).
The presented adaptations may also be tied to a higher
recruitment of muscle fibers and motor units (Galvan and
Cataneo, 2007) as well as a better synchronism and triggering frequency of these units (Komi, 1986), leading to an
increase in strength production.
These physiologic alterations on the skeletal muscle fibers of the abdominal wall may have increased the muscle
contraction capacity of the abdomen muscles, facilitating
the realization of movements with a greater control and
concentration in execution. Therefore, the volunteers were
able to coordinate the breathing pattern during each
movement.
Our study presented some limitations, such as the
absence of a control group and an inability to blind the
assessors. The participants presented similar characteristics; however, the application of the intervention protocol
and the outcome variable measurements were not conducted by the same researcher. The assessors of the respiratory capacity and ultrasound were experienced, and
the data collection techniques were carefully standardized,
thus qualifying the study and minimizing errors in evaluating the images and data.
The Mat PM promoted the improvement of respiratory
muscle strength and performance as well as the hypertrophy of abdominal wall muscles in healthy sedentary
Please cite this article in press as: Giacomini, M.B., et al., The Pilates Method increases respiratory muscle strength and performance as
well as abdominal muscle thickness, Journal of Bodywork & Movement Therapies (2015), http://dx.doi.org/10.1016/j.jbmt.2015.11.003
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women. These variables have been presented as a therapeutic target in many studies and are related to relevant
outcomes, such as functional capacity and life quality.
Therefore, this method may promote positive effects on
subjects with or without respiratory muscle strength
reduction, but should be tested in populations with
different chronic diseases.
The set of findings observed in our study may influence
the prevention of functional abdominal muscle disabilities
and, possibly, minimize the risks of musculoskeletal and
ventilatory dysfunction. Furthermore, the use of Mat PM
may be used as a potentially useful therapeutic instrument
in several populations suffering from respiratory pathologies. Therefore, the effects of Mat PM in special populations, may be recommended in clinical practice.
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+
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Please cite this article in press as: Giacomini, M.B., et al., The Pilates Method increases respiratory muscle strength and performance as
well as abdominal muscle thickness, Journal of Bodywork & Movement Therapies (2015), http://dx.doi.org/10.1016/j.jbmt.2015.11.003