Accepted Manuscript
Title: Local and widespread hyperalgesia in female runners
with patellofemoral pain are influenced by running volume
Author: Marcella Ferraz Pazzinatto Danilo de Oliveira Silva
Juliana Pradela Maira Bergamaschi Coura Christian Barton
Fábio Mı́colis de Azevedo
PII:
DOI:
Reference:
S1440-2440(16)30204-3
http://dx.doi.org/doi:10.1016/j.jsams.2016.09.004
JSAMS 1390
To appear in:
Journal of Science and Medicine in Sport
Received date:
Revised date:
Accepted date:
19-4-2016
10-8-2016
11-9-2016
Please cite this article as: Pazzinatto Marcella Ferraz, de Oliveira Silva Danilo,
Pradela Juliana, Coura Maira Bergamaschi, Barton Christian, de Azevedo Fábio
Mı́colis.Local and widespread hyperalgesia in female runners with patellofemoral
pain are influenced by running volume.Journal of Science and Medicine in Sport
http://dx.doi.org/10.1016/j.jsams.2016.09.004
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Local and widespread hyperalgesia in female runners with patellofemoral pain are
influenced by running volume
Marcella Ferraz Pazzinatto1, Danilo de Oliveira Silva1, Juliana Pradela1, Maira Bergamaschi
Coura1, Christian Barton2,3, Fábio Mícolis de Azevedo1
1
Physical Therapy Department, University of São Paulo State, School of Science and
Technology, Presidente Prudente, Brazil.
2
School of Allied Health, College of Science, Health and Engineering, La Trobe University,
Bundoora, Australia.
3
Centre for Sports and Exercise Medicine, Queen Mary University of London, London, UK.
Correspondence concerning about this article should be addressed to Fábio Mícolis de Azevedo,
Roberto Simonsen Street, 305, CEP 19060-900, Department of Physiotherapy FCT/UNESP,
Presidente Prudente (SP), Brazil. Phone: 3229-5820. E-mail: [email protected]
Objectives: To compare pressure pain threshold (PPT) around the knee (local hyperalgesia)
and at a site remote to the knee (widespread hyperalgesia) between female runners with and
without patellofemoral pain (PFP); and to evaluate the relationship between running volume,
self-reported knee function and PPT measures.
Design: Cross-sectional study.
Methods: Twenty female runners with PFP and twenty pain-free female runners participated in
the study. PPTs were measured using a handheld pressure algometer at four sites in the
patellar region: quadriceps tendon, medial patella, lateral patella and patellar tendon; and on the
contralateral upper limb. Additionally, all participants were asked to report their average weekly
1
running volume in a typical month and answer the anterior knee pain scale (AKPS)
questionnaire.
Results: For all sites, female runners with PFP presented lower PPT measures in comparison
with control group (P<0.017). There were negative correlations between AKPS and running
volume (ρ= -0.88; P<0.001) and between all PPTs and the running volume in the PFP group
with correlation (ρ) values ranging between -0.46 and -0.70 (P<0.022). There were positive
correlations between all PPTs and AKPS with correlation (ρ) value from 0.50 to 0.69 (P<0.030).
Conclusion: Lower PPTs locally and remote to the knee in female runners with PFP indicate
the presence of local and widespread hyperalgesia. Additionally, this hyperalgesia, which is
related to self-reported knee function, appears to be increased by greater running volumes.
Development and evaluation of non-mechanical interventions for the management of runningrelated PFP in females may be needed to address this apparent hyperalgesia.
Keywords: Patellofemoral joint; Anterior knee pain; Hyperalgesia secondary; Athlete; Knee;
Pain.
2
Introduction
Running is a very common and popular form of exercise due its low cost and ease of
access. However, there is a high incidence of lower extremity injuries among runners, with
estimates reaching as high as 79%, with the knee being the most commonly affected site1.
Patellofemoral pain (PFP) is the most common running-related knee injury2, and is particularly
common in females aged 18-35, with an estimated prevalence being 13%3. Symptoms often
become chronic and may reduce sports and daily activity participation, with chronicity
associated with PFP also thought to increase the risk of developing osteoarthritis in later life4.
A recent systematic review with meta-analysis5 reported that athletes had higher pain
thresholds when measured using a variety of methods, including pressure pain threshold
(PPT)6, in comparison with normally active controls. This may be protective against
hyperalgesia7 associated with conditions such as PFP8,9. Moreover, Hoffman and colleagues10
reported that greater running volume per week leads to reduced pressure pain perception
compared with smaller running volumes. These findings indicate higher PPT relate to more
active runners without pathology5,10.
Although higher physical activity levels appear to protect against pain sensitization in
uninjured runners, it is unclear if this same relationship exists in injured runners. It is well
established that females with PFP present local and widespread hyperalgesia8,9 measured by
PPT. However, PPTs in female runners with PFP are yet to be evaluated in the literature.
Therefore, it is unclear whether high levels of activity (i.e. running volume) in female runners
with PFP provides protection against pain sensitivity, has no effect on sensitization, or in fact
increases sensitization in the presence of pathology. The latter is highly plausible since
sensitization and hyperalgesia are thought to be contributed by the persistent presence of pain
and symptoms11, which is frequently aggravated by running in PFP12. If true, this may have
particularly important implications for the management of PFP, including the possible need to
3
incorporate pain neuroscience education alongside current evidence based biomechanical and
strength targeted treatments in female runners with PFP13,14.
The aims of this study were to (i) compare PPTs around the knee (local hyperalgesia)
and at a site remote to the knee (widespread hyperalgesia) between female runners with and
without PFP; and (ii) evaluate correlations between running volume (i.e. number of kilometers
run per week), self-reported knee function and PPT measures in female runners with and
without PFP. Due to impaired endogenous pain inhibitory mechanism previously reported in
females with PFP15 we hypothesized that female runners with PFP would also (i) present with
lower PPTs compared to female runners without PFP; and (ii) running volume would be
negatively correlated with PPTs and self-reported knee function would be positively correlated
with PPTs in female runners with PFP.
Methods
Reporting of this cross-sectional study is in accordance to STROBE guideline
recommendations. Twenty female runners with PFP (PFP group - PFPG) aged 18-35 and
twenty asymptomatic female runners (Control group - CG) were recruited via advertisements in
fitness centres and public places for physical activity, between September 2015 and February
2016. All participants had been running at least 15 km per week prior to enrolment for the
minimum period of six months16. Power calculations for this study were performed based on a
pilot data (n = 8 for each group). Conservatively, we chose the PPT of patellar tendon, because
it was the variable with higher standard deviation and lower detectable difference. Sample size
was determined on the basis of predicted power to detect a difference of 1.27kgf (SD 1.22) in
PPT of patellar tendon between groups, considering an α level of .05 and a power of 80%.
Based on the calculations performed with SamplePower software a minimum sample size of 14
participants per group was indicated.
4
Runners with PFP were included if they had (1) symptoms of insidious onset and
duration of at least 3 months; (2) anterior knee pain during at least 2 of the following activities:
prolonged sitting, squatting, kneeling, climbing stairs, and jumping; (3) anterior knee pain during
running; and (4) worst pain level in the previous month at least 3cm on a 10cm VAS17,18. To be
included in the CG participants could not present any signs, symptoms or historical of PFP or
other current musculoskeletal injury. Exclusion criteria for both groups were: events of patellar
subluxation or dislocation, lower limb inflammatory process, lower limb surgery, patellar tendon
or meniscus tears, bursitis, ligament tears or the presence of neurological diseases. The
inclusion and exclusion criteria were verified following consensus from two experienced clinical
physiotherapists (> 5 years' experience). The study was approved by the Local Ethics
Committee and each participant gave written informed consent prior to participation. The
participants included were asked to avoid pain medications on the day of their evaluation (none
of the participants reported use of any medications).
PPTs were measured using a handheld pressure algometer (Wagner FPX™ 25,
Greenwich, CT, USA) with a probe of 1cm2 placed perpendicular to the skin. Participants were
instructed to indicate when the sensation changed from a sensation of pressure to the first
sensation of pain.
All measurements were performed in the same period of the day and by the same
trained rater to a pressure rate of 0.50kgf/s19. The assessor was blinded concerning groups. All
evaluations were performed with participants in a standardized position, supine with slightly
flexed knees at 20º20. For PFPG, we evaluated the symptomatic knee and for CG, we chose the
knee of the dominant leg. Four sites in the patellar region were selected to investigate local
hyperalgesia: quadriceps tendon (QT), medial patella (MP), lateral patella (LP) and patellar
tendon (PT)21; and on a contralateral upper limb (UL) to reflect widespread hyperalgesia (the
lesser tubercle of the humerus)9. PPT was measured twice at each site with a 30-second period
between testing, and the average was used for analysis8,9,20.
5
Half of the participants (Ten female runners with PFP and ten asymptomatic female
runners) were invited to return at the lab for repeat the evaluation with an interval of 2 to 7 days
of the first evaluation to calculate the intra-rater reliability using the intraclass correlation
coefficient (ICC2,k) with a confidence interval of 95%, standard error of measurement (SEM) and
the minimal detectable change with a confidence level of 95% (MDC95) for PPT measures. All
PPT measures demonstrated satisfactory reliability with ICC values ranging between 0.79 to
0.93 for CG (UL and PT, respectively) and 0.67 to 0.91 for PFPG (UL and QT, respectively).
Additionally, the measures presented values of SEM ranging between 1.1% to 22.7% and
values of MDC95 ranging between 0.17 to 2.27 (Supplementary material).
Prior to the PPT measurements, all participants were asked to rate their worst knee pain
intensity during the last 4 weeks, and current pain measured on a 0–10 visual analogue scale
(VAS). Additionally, symptom duration (months), self-reported knee function (Anterior Knee Pain
Scale – AKPS) and running volume (number of kilometers run per week in a typical month) were
recorded. The AKPS is a 13-item questionnaire that evaluates subjective symptoms and
functional limitations associated with PFP. The questionnaire score ranges from 0 to 100, with
the maximum total score of 100 indicating no disability. This tool has been validated for subjects
with PFP and has been reported to demonstrate high test–retest reliability22.
All analyses were performed using Statistical Package for the Social Sciences software
program (version 18.0, SPSS, INC., Chicago, IL) with an a priori level of significance of 0.05.
Normality and variance homogeneity of data were tested using the Shapiro-Wilk and Levene
tests, respectively. Data for normally distributed variables were reported as mean (SD) and for
non-normally distributed variables were reported as median (interquartile range).
Independent t-tests were used to compare the characteristics including age, height, body
mass and running volume of the participants between groups. Due to non-normal distribution of
data, the Mann-Whitney U test was used to assess the group differences for each dependent
variable (PPTs and VAS). The data reported were the U, z, p and effect size (r) values. Besides,
6
Spearman correlation coefficients were used to correlate PPTs with running volume and selfreported knee function.
Results
No differences between groups for age, height, body mass and weekly running distance
were identified; the AKPS scores were lower in the PFPG (Table 1). For all sites, the PFPG had
lower PPT measures in comparison with CG: QT (U= 71; z= -3.639; P< 0.001; r= -0.58), MP (U=
118.5; z= -2.392; P= 0.017; r= -0.38), LP (U= 51; z= -4.171; P< 0.001; r= -0.66); PT (U= 100.5;
z= -2.885; P= 0.004; r= -0.46) and UL (U= 93; z= -3.005; P= 0.002; r= -0.48) (Figure 1).
There were negative correlations between self-reported knee function and running
volume in the PFPG (ρ= -0.88; P<0.001) and among all PPT measures and the running volume
per week in the PFPG, indicating lower PPTs were associated with higher running volumes. The
correlations for PFPG were: QT (ρ= -0.56; P= 0.006), MP (ρ= -0.70; P< 0.001), LP (ρ= -0.46; P=
0.020), PT (ρ= -0.46; P= 0.022), UL (ρ= -0.48; P= 0.015). There were positive correlations
among PPT measures and self-reported knee function in the PFPG, indicating lower PPTs were
associated with poorer knee function. The correlations for PFPG were: QT (ρ= 0.52; P= 0.030),
MP (ρ= 0.69; P= 0.003), LP (ρ= 0.52; P= 0.028), PT (ρ= 0.50; P= 0.034), UL (ρ= 0.52; P=
0.028). No significant correlations were identified in the CG (p > 0.213). Figure 2 depicts all
significant correlations found in the PFPG.
Discussion
Female runners diagnosed with PFP, in this study, presented with lower PPTs locally
and remote to the knee when compared with asymptomatic female runners, indicating the
presence of local and widespread hyperalgesia. Lower PPTs were also associated with poorer
7
self-reported knee function and greater running volume in the PFPG. Put together, these
findings highlight the potential importance of load management to control symptoms and reduce
hyperalgesia in female runners with PFP.
Previous studies8,9 comparing PPTs in females with PFP and asymptomatics have
reported mean differences of 1.56kgf (range= 0.83 to 2.19) around the knee and 1.45kgf
(range= 0.80 to 2.44) at a remote site to the knee. Findings from our study of female runners
with PFP are comparable, with differences of 1.38kgf and 1.53kgf, locally and remote to the
knee, respectively. Based on these findings, it appears that similar hyperalgesia deficits may
exist in both running and non-running female PFP populations, indicating the potential need for
non-mechanical interventions such as pain neuroscience education in both populations.
According to our hypothesis, similar reductions in PPTs found in female runners with
PFP to those in more general PFP populations8,9 indicate exercise induced analgesia is lost in
the presence of pathology. This apparent exercise induced analgesia represented by higher
PPTs7,23 is thought to be facilitated by activation of the endogenous opioid system7,24. Based on
findings of this study, it appears that this potentially protective mechanism against hyperalgesia
in asymptomatic runners may be impaired in female runners with PFP, not just locally, but also
remote to the knee.
Greater running volume was also found to be associated with local and remote
hyperalgesia, and also with poorer self-reported knee function in female runners with PFP in
this study, which is contrary to previous findings reported in asymptomatic runners10. This
widespread hyperalgesia, consistent with other research on this topic in including thermal,
tactile and vibration thresholds in individuals with PFP25,26, may point to the possible presence of
central sensitization, characterized by malfunctioning of descending pain inhibitory pathways
and subsequent dysfunctional endogenous analgesic control11. This malfunctioning of
descending pain inhibitory pathways associated with a chronic overstressing of the endogenous
8
opioid system by heightened activation levels, during high intensity exercises, may eventually
result in exhaustion over time. Such exhaustion may result in disinhibition of pain processing7.
Activities that load patellofemoral joint during weight bearing on a flexed knee as stair
climbing and running are responsible to aggravate the PFP symptoms12. Our findings
demonstrated that presence of hyperalgesia is associated with poorer self-reported knee
function, which was also associated with higher weekly running volumes. In other words, greater
running volume may lead to poorer self-reported knee function and hyperalgesia. According to
Dye and colleagues27, altered pain perception in individuals with PFP with certain loading
activities can therefore be viewed as an overt biologic indicator that the joint is being loaded out
of its envelope of function (load acceptance capacity of the joint). Consideration of this possible
phenomenon may have important implications for management, with the potential need to
monitor and control running volume and activity levels in the presence of PFP in order to
manage hyperalgesia effectively. Further research is needed to develop and evaluate
interventions in this regard.
Some limitations of this study should be acknowledged (i) we evaluated females in the
age group most affected by PFP, limiting extrapolation of findings to males with PFP, or older
participants with PFP; (ii) PPTs were not evaluated immediately following a bout of running,
preventing us establishing the acute effects of exercise on the endogenous analgesic control
and potential influence on widespread hyperalgesia; (iii) we did not evaluate a non-running
female population with PFP, and therefore cannot determine if there are differences between
runners and non-runners with PFP, however, it could be further explored in future studies; (iv)
the power calculation was performed using PPT of the patella tendon as in our pilot data it was
the site we found the smallest difference between groups with the greatest standard deviation.
However, it may be a possible bias for between groups difference in other sites.
Previous research evaluating potential deficits in runners with PFP have tended to focus
on mechanical variables such as kinematics, kinetics and muscle function28,29. As a result, the
9
majority of the current research and subsequent evidence base for managing runners with PFP
has been focused on addressing these mechanical deficits13,30. However, findings from our
study indicate that female runners with PFP may also require non-mechanical interventions in
order to focus on components aimed at pain neuroscience education14. The relationship
between greater running volume and hyperalgesia also indicates that education and guidance to
decrease loading within a joint’s current diminished envelope of function27 may also be vitally
important to tackling this non-mechanical phenomenon. A number of considerations have been
previously recommended to address CS associated with chronic musculoskeletal pain14,24.
These include a conservative approach when prescribing initial exercise loads; cautious
progression of load to prevent symptom flaring, including exercise of non-painful areas of the
body (e.g. upper limbs); and allowing only small increases in pain during and shortly following
exercise, but avoiding increased pain intensity over time14,24. Further research to develop and
evaluate interventions related to addressing hyperalgesia, and providing education on training
load and activity modification are needed.
Conclusion
Lower PPTs locally and remote to the knee in female runners with PFP indicate the
presence of local and widespread hyperalgesia in this common patient presentation.
Additionally, this hyperalgesia appears to be increased by greater running volumes and
associated with poorer self-reported knee function. Put together these findings highlight the
need to further develop and evaluate non-mechanical interventions including load management
to treat running-related PFP in females.
Practical Implications
- Female runners with patellofemoral pain presented signs of local and widespread
hyperalgesia. Additionally, greater running volume and poorer self-reported function were found
10
to be associated with increased local and widespread hyperalgesia in female runners with
patellofemoral pain.
- The relationship between greater running volume and hyperalgesia also indicates that
education and guidance to maintain runners with PFP in their envelope of function may also be
vitally important to tackling this non-mechanical phenomenon.
- A conservative approach with cautious progression of load to prevent symptom flaring and
avoiding increased pain intensity over time is encouraged to manage this disorder.
- Female runners with PFP may also require non-mechanical interventions in order to address
potential pain neuroscience deficits.
Acknowledgments
This research was supported by a grant (2014/24939-7) and two scholarships
(2014/10839-0 and 2015/15574-8 authors MFP and JP, respectively) from São Paulo Research
Foundation (FAPESP). The financial sponsors played no role in the design, execution, analysis
and interpretation of data, or writing of the study.
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Figure Legends
Figure 1. Box-plots of the PPT measures for CG and PFPG. Abbreviation: CG – control group;
PFPG – patellofemoral pain group; QT - quadriceps tendon; MP - medial patella; LP – lateral
patella; PT – patellar tendon; UL – upper limb; * - represents statistical difference between
groups.
Figure 2. A) Correlation graphs for PPT (pressure pain threshold) measures and running volume
per week for PFPG (patellofemoral pain group). B) Correlation graphs for PPT measures and
self-reported knee function by Anterior Knee Pain Scale (AKPS). C) Correlation graph for AKPS
and running volume per week.
16
Fig 1
17
Fig 2
18
Table 1. Characteristics of participants
CG
PFPG
P-value
Age (years)
27.00 (5.58)
25.62 (4.05)
0.518
Height (m)
1.62 (0.04)
1.63 (0.06)
0.444
Body mass (kg)
60.00 (7.35)
58.33 (6.89)
0.662
Weekly running distance (km)
20.75 (4.17)
19.75 (4.47)
0.591
Previous month
0 (0)
4.81 (1.54)
<0.001
During evaluation
0 (0)
1.15 (1.50)
NA
NA
37.69 (49.31)
NA
100.0 (0)
80.45 (4.55)
<0.001
VAS
Symptoms duration (months)
AKPS
Abbreviations: CG – control group; PFPG – patellofemoral pain group; VAS – visual analogue
scale; AKPS – anterior knee pain scale; NA – Not applicable. The values are showed in mean
(standard deviation).
19