Does quadriceps atrophy exist in individuals with patellofemoral pain? A systematic literature review with meta-analysis.

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Journal of Orthopaedic & Sports Physical Therapy® Downloaded from www.jospt.org at Bibliotheque de l'Universite Laval on July 16, 2014. For personal use only. No other uses without permission. Copyright © 2013 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

LACHLAN S. GILES, PT1 • KATE E. WEBSTER, PhD2 • JODIE A. MCCLELLAND, PhD1 • JILL COOK, PhD3

Does Quadriceps Atrophy Exist in Individuals With Patellofemoral Pain? A Systematic Literature Review With Meta-analysis

P

atellofemoral pain (PFP) is a common source of knee pain experienced by adolescent and young-adult athletes. The incidence of PFP in people presenting to sports medicine clinics with knee pain has been reported to be 1 in 4 (25%),2,12,19 although the reported incidence between studies ranges from as low TTSTUDY DESIGN: Systematic literature review. TTOBJECTIVES: To investigate whether quad-

riceps atrophy is present in the affected limb of individuals with patellofemoral pain (PFP).

TTBACKGROUND: PFP is a common condition.

Atrophy of the quadriceps femoris, in particular the vastus medialis obliquus, is often assumed to be present by clinicians, and its resolution may underpin the reported effectiveness of quadriceps strengthening intervention in PFP rehabilitation.

TTMETHODS: A systematic search of the literature was conducted to identify studies that measured the size of the quadriceps in individuals with PFP. Meta-analyses were performed to determine whether quadriceps size in limbs with PFP differed from that in comparison limbs. Separate meta-analyses were performed for quadriceps size measured as girth and quadriceps size measured with imaging (thickness, cross-sectional area, and volume).

TTRESULTS: Ten studies were included in this review. The meta-analysis of girth measurements (3 studies) found no atrophy in limbs with PFP

(P = .638). The meta-analyses for imaging techniques (thickness, cross-sectional area, or volume measurements) showed atrophy in the limb with PFP compared to both the asymptomatic limb (3 studies) (P = .036) and limbs from a comparison group (3 studies) (P = .001). The single study that compared the vastus medialis obliquus and vastus lateralis in individuals with PFP found atrophy of both the vastus medialis obliquus and vastus lateralis but no significant difference in the amount of atrophy between them (P = .179).

TTCONCLUSION: Quadriceps muscle atrophy was shown to be present in PFP when analyzed by imaging, but not by girth measures. Insufficient data were available to determine if there was greater atrophy of the vastus medialis obliquus than the vastus lateralis. These findings support the rationale for use of quadriceps strengthening as part of a rehabilitation program for PFP. J Orthop Sports Phys Ther 2013;43(11):766-776. Epub 9 September 2013. doi:10.2519/jospt.2013.4833 TTKEY WORDS: girth, knee, strengthening, thigh,

vastus medialis

as 9% in students (7% of males and 10% of females) aged 17 to 21 years during 2 years of physical education training51 to as high as 43% in army recruits (38% of males and 58% of females) undertaking 6 weeks of training. 48 PFP is characterized by pain in the anterior knee region when performing activities such as sitting, stair climbing, running, and squatting.3,16,49 Although rehabilitation typically reduces the prevalence of persistent symptoms, Clark et al15 found that 60% of participants with PFP who undertook exercise programs continued to experience symptoms after 1 year, with symptoms of PFP often still present 5 years after diagnosis.6,27,43 Quadriceps-strengthening exercises have been shown to be an effective, commonly prescribed intervention to improve pain and function in individuals with PFP.15,18,47 Although these strengthening exercises are often provided to counteract the assumed quadriceps muscle atrophy and consequent weakness, there is limited information to support the existence of quadriceps atrophy in individuals with PFP. Previous studies that have measured the size of the quadriceps have reported

Department of Physiotherapy, School of Allied Health, Faculty of Health Sciences, La Trobe University, Bundoora, Australia. 2School of Allied Health, Faculty of Health Sciences, La Trobe University, Bundoora, Australia. 3Department of Physiotherapy, School of Primary Health Care, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Australia. Dr Cook was supported by the Australian Centre for Research Into Sports Injury and Its Prevention, which is one of the International Research Centres for Prevention of Injury and Protection of Athlete Health supported by the International Olympic Committee. The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or materials discussed in the article. Address correspondence to Lachlan S. Giles, Department of Physiotherapy, School of Allied Health, La Trobe University, Bundoora, Victoria 3086 Australia. E-mail: [email protected] t Copyright ©2013 Journal of Orthopaedic & Sports Physical Therapy® 1

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conflicting results; therefore, a systematic review of the literature is needed to evaluate and synthesize the evidence on quadriceps atrophy in individuals with PFP. A potential reason for the inconsistency of the findings of previous research may be the type of measurement used to evaluate quadriceps atrophy. Measurements made with magnetic resonance imaging (MRI) and ultrasound have demonstrated strong validity35,36; however, measures of muscle girth are more typical in clinical settings. Differences in sensitivity of these measurements may yield different findings; therefore, it is important for a systematic evaluation of the evidence of atrophy in PFP to be completed with reference to the type of measurement used. This review aimed to investigate whether quadriceps atrophy exists in the affected limb of individuals with PFP and whether the amount of atrophy differs between the vastus medialis obliquus (VMO) and vastus lateralis (VL).

METHODS Search Strategy

T

his review was conducted according to the PRISMA guidelines.37 A single author performed the primary search of studies dating from inception to the dates specified in the following databases: MEDLINE (Ovid) (March 20, 2012), CINAHL (March 20, 2012), Embase (March 23, 2012), Cochrane (March 26, 2012), and PEDro (March 26, 2012). The search string was (quadricep* OR vastii OR vastus OR knee extens* OR VMO OR thigh) AND (atrophy OR wasting OR cross section* OR volume OR size OR measure* OR diameter OR girth OR bulk OR area OR morphology) AND (PFJ OR anterior knee pain OR chondromalacia OR patell* OR runners knee OR PFPS). Citation tracking and reference scanning were performed on all studies included in the review.

TABLE 1

Risk-of-Bias Checklist*

Item Title

Description

1

Representative of sample population (yes/no)

Either volunteer participants or greater than 80% of invited participants were included in the study

2

Comparison had similar characteristics (yes/no)

The comparison group had similar gender, age, and body composition to the PFP group

3

Measurer blinded to group allocation (yes/no)

The assessor was blinded to whether the assessed limb was symptomatic or asymptomatic

4

Justification of sample size (yes/no)

Calculations were performed to justify the sample size

5

Provides a measure of variability (yes/no)

Provides a measure of variability where a mean value is reported or the total population where a proportion is reported

6

Reliability of measurement assessed (yes/no)

The study reports the reliability of the measurement utilized

Abbreviation: PFP, patellofemoral pain. *Adapted from Chester et al14 and Downs and Black.21

Selection Criteria Studies published in full text in peerreviewed journals in English were included in the review. The participants included were diagnosed with PFP and had measurements of quadriceps muscle size (muscle thickness, cross-sectional area, girth, volume) taken of either individual quadriceps muscles (eg, just vastus medialis) or for total quadriceps muscle size. The included studies had to report the mean value of quadriceps muscle size or the proportion of participants who had quadriceps atrophy. Studies that only visually observed quadriceps muscle size were excluded. Studies with subjects with unilateral or bilateral PFP were included. Studies in which participants had bilateral PFP required a separate comparison group, whereas those with unilateral PFP were compared to either a separate comparison group or to the contralateral, asymptomatic limb. The presence of coexisting pathology in the PFP and comparison groups was determined for each study, and studies were excluded if participants had coexisting pathology (eg, previous anterior cruciate ligament tear, patellar dislocation/subluxation, patellofemoral osteoarthritis, meniscal injuries, or lower-limb surgery). Studies were included if no

mention was made of coexisting pathology, on the assumption that there was none. Studies were excluded if baseline data of muscle size were not reported before the start of interventions that might have affected quadriceps muscle size. Case reports were also excluded.

Data Collection and Analysis Selection of Studies All articles that met the key-word search were exported to EndNote X5 (Thomson Reuters, New York, NY). Subsequently, 2 authors independently excluded studies based on the title and abstract, according to the selection criteria. Full text was obtained of the remaining articles and reviewed, according to the same selection criteria, independently by the same 2 authors. Where there was disagreement or ambiguity, the 2 authors met to resolve the issue. Once selection was finalized, data were independently extracted from the included studies by the same 2 authors. Assessment of the Risk of Bias To assess risk of bias, a checklist containing 6 criteria was put together by using items from 2 existing sources (TABLE 1).14,21 This included calculation of the differences between groups for potential confounding factors (age, gender, and body weight) when not reported.13 To evaluate the validity of PFP diagnosis for each article, a

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TABLE 2

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Diagnostic Criteria for PFP*

Item Title

Description

1

Greater than 6 weeks of symptoms (yes/no/not stated)

Participants had symptoms for greater than 6 weeks in duration

2

Clear definition of symptom location (yes/no/not stated)

Specifically states that participants with PFP complained of pain in the peripatellar region

3

Insidious onset unrelated to trauma (yes/no)

Participants did not experience any trauma at the onset of symptoms

4

Symptoms consistent with diagnosis of PFP (yes/no)

Participants complained of pain with activities such as squatting, kneeling, running, or stairs

5

Excludes other sources of anterior knee pain (yes/no)

Excludes conditions such as patellar tendinopathy, fat-pad impingement, or osteoarthritis

6

Excludes major knee pathology (yes/no)

Excludes previous or concurrent knee issues such as ligament damage, subluxation, or past surgery

Abbreviation: PFP, patellofemoral pain. *Adapted from Barton et al.4

6-item checklist, adapted from Barton et al,4 was used (TABLE 2).

Statistical Analysis Quadriceps Muscle Size When muscle

size was reported from measurements at multiple locations (eg, mid thigh, distal thigh, patellar level), the measurement closest to the mid thigh was selected for inclusion in the statistical analysis. When muscle size was also measured with multiple techniques, the data from only 1 measurement technique were chosen, based on the following order of preference: volume, cross-sectional area, thickness, girth. The mean and standard deviation for quadriceps muscle size of the PFP limb (unilateral or bilateral symptoms) and comparison limb (from a separate comparison group or the contralateral limb) were extracted from the article and imported to Comprehensive Meta-Analysis Version 2 (Biostat, Inc, Englewood, NJ) for statistical analysis. Heterogeneity was assessed with the I2 test, and, based on the results, a random-effects model was used to perform 3 meta-analyses: imaging measures (thickness, cross-sectional area, and volume) of the symptomatic limb compared to the asymptomatic limb, imaging measures of the symptomatic limb compared to the limb of an asymptomatic comparison group, and girth measures of

the symptomatic limb compared to the combined data of the limb of an asymptomatic comparison group and the asymptomatic limb. Data from studies that did not report the size of the quadriceps muscles but reported the proportion of participants with PFP with quadriceps atrophy, based on predetermined criteria, were used.

VMO/VL Ratio The data from 1 study40 that reported the size of the individual VMO and VL quadriceps muscles (VMO/VL ratio) were extracted.

RESULTS Characteristics of the Included Studies

T

he search identified 3169 articles, of which 10 were included in the final review (FIGURE 1). Of these, 2 were randomized controlled trials11,41 and 8 were cross-sectional studies (TABLE 3).1,10,20,22,26,29,32,40 The primary aim of 5 studies was to assess quadriceps muscle size.10,22,26,29,40 The remaining studies measured quadriceps muscle size as anthropometric data or as a secondary measurement of impairment associated with PFP.1,11,20,32,41 The data from 7 studies were included in meta-analyses, as they reported the mean and standard

] deviation of the size of the quadriceps musculature.10,20,22,26,29,40,41 Two studies reported the proportion of participants with quadriceps atrophy,1,32 and therefore were not included in the meta-analyses. One further study was not included in the meta-analyses because this study required quadriceps atrophy for a diagnosis of PFP11 and selecting a subgroup of patients with PFP based on quadriceps atrophy as a criterion for diagnosis might introduce bias. Of the 7 studies that reported mean muscle size, quadriceps muscle size was compared to the asymptomatic limb in 2 studies,22,29 to a separate comparison group in 4 studies,20,26,40,41 and to both in 1 study.10 In terms of the size of individual quadriceps muscles, the size of the VMO was analyzed in 2 studies, with 1 measuring the size of both the VMO and VL40 and the other measuring only the VMO.26 Five studies measured thigh girth with a tape measure,1,20,22,32,41 1 study measured muscle thickness using ultrasound,22 4 studies measured cross-sectional area (2 using ultrasound10,11 and 2 using MRI29,40), and 2 studies measured muscle volume using MRI.26,29 One study measured the volume of the entire quadriceps muscle group,29 another measured the volume of just the VMO,26 5 studies performed the measures at the mid thigh,10,11,20,22,40 and 4 studies performed measures at the distal thigh.1,32,40,41

Methodological Quality Risk of Bias Where risk-of-bias and diagnostic items were combined, studies satisfied between 3 and 10 criteria out of a possible 12 (TABLE 4). No study satisfied more than 4 of the 6 items on the riskof-bias checklist (TABLE 5). The gender, age, and body weight of participants in the comparison group were similar to those in the PFP group in all but 1 study, in which the gender and body weight of the participants were not reported.20 Attempts were made to demonstrate that the sample of participants was representative of the related population in 3 studies.22,26,41



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Diagnosis of PFP All items for the diagnosis of PFP were satisfied in 2 studies (TABLE 6).10,11 The diagnosis of PFP required pain with stair climbing, squatting, running, or long sitting in 5 studies,10,11,26,32,40 whereas 2 studies did not specify that participants had to have pain in the anterior knee region.29,41 In contrast to all other studies, the diagnosis of PFP in the study by Callaghan et al11 required participants to have quadriceps atrophy.

Articles located and imported to EndNote, n = 3169

After duplicates removed, n = 1923

After excluding by title and abstract, n = 89 Articles excluded for not being journal articles, n = 10

Quadriceps Size and PFP Meta-analysis of girth measures revealed no significant difference in quadriceps muscle size between limbs affected by PFP and comparison limbs (average standardized mean difference, –0.084; 95% confidence interval: –0.435, 0.267; P = .638) (FIGURE 2). Standardized mean differences were of similar magnitude for all 5 studies, with all but 1 study reporting a trend toward quadriceps atrophy in individuals with PFP.20 Meta-analysis of the imaging measurements of the symptomatic limb of individuals with PFP compared to the contralateral asymptomatic limb revealed a significantly smaller quadriceps muscle size on the side of PFP (average standardized mean difference, –0.442; 95% confidence interval: –0.855, –0.029; P = .036) (FIGURE 3). Meta-analysis of imaging measurements of the symptomatic limb of individuals with PFP compared to the asymptomatic limb of a comparison group also demonstrated a statistically significant difference, indicating that quadriceps muscle size is reduced in the limb with PFP (average standardized mean difference, –0.463; 95% confidence interval: –0.734, –0.192; P = .001) (FIGURE 4).

Prevalence Proportion of Quadriceps Atrophy in PFP Two studies1,32 reported the proportion of patients with PFP who had quadriceps atrophy. Each used different criteria to determine quadriceps atrophy. When atrophy was defined as a difference in

Inclusion and exclusion criteria applied, n = 79 Excluded, n = 69 • Quadriceps not measured, n = 50 • Not written in English, n = 6 • Participants did not have patellofemoral pain, n = 6 • Did not contain a comparison group, n = 2 • Did not provide results of comparison-limb measures, n = 5 Included in review, n = 10 FIGURE 1. Search strategy.

girth between sides of 0.5 cm or greater, 57.1% of those with unilateral PFP had quadriceps atrophy on the involved side1; when atrophy was defined as a difference of greater than 2 cm, 32.0% had quadriceps atrophy.32

VMO/VL Ratio There were insufficient data to perform a meta-analysis for the relative difference in size of the VMO and VL in the involved limb of individuals with PFP. One study found significantly smaller muscle cross-sectional area in limbs with PFP compared to the limbs of a comparison group for the VL at the mid thigh and for the VMO at the distal thigh.40 In that study, at mid thigh the VL was 10.5% smaller than the same measurements for the comparison group. Measurements

made at the distal thigh region indicated that the VMO was 5.4% smaller and the VL 8.9% smaller than those in the comparison group. The ratio of the size of the VMO to that of the VL (distal thigh measurement) was not significantly different between limbs with PFP and the limbs of a comparison group (P = .197).

DISCUSSION

T

his review of 10 papers examined the relationship between quadriceps muscle size and PFP. Meta-analyses for imaging measurements of quadriceps muscle size demonstrated that quadriceps atrophy is present in the involved limb of individuals with PFP, when compared to their asymptomatic limb and to a comparison group.



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TABLE 3


Study, Design, Comparison Group

Characteristics of the Included Studies Comparison Group Characteristics

Measurement Method

Unilateral symptoms, n = 49; age, gender, and body weight not stated

Same as PFP group (asymptomatic limb)

Tape measure applied 5 cm above patella

cm

Difference of 0.5 cm or more in girth was classified as quadriceps atrophy; 28 of 49 participants had atrophy

To compare results of 2 types of electrical stimulation for PFP

All participants had quadriceps atrophy (required for diagnosis)

Same as PFP group (asymptomatic limb)

Ultrasound measurement of quadriceps crosssectional area at mid thigh

cm2

Difference greater than 4% between sides considered as quadriceps atrophy; atrophy was a requirement for inclusion in this study

Callaghan and Oldham,10 cross-sectional study, separate comparison group and asymptomatic limb

To determine if quadriceps atrophy existed in PFP

n = 57; mean  SD age, 34.4  11.5 y; 22 male, 35 female; BMI, 26.0  5.2 kg/m2

Group 1: same as PFP group (unaffected limb) Group 2 (comparison group): n = 10; 4 male, 6 female; age, 30.6  5.2 y; BMI, 23.6  3.2 kg/m2

Ultrasound measurement of quadriceps crosssectional area at mid thigh

cm2

Mean  SD PFP, 18.06  4.6; group 1 (asymptomatic limb), 18.32  4.40; group 2 (dominant limb), 20.08  5.1; group 2 (nondominant limb), 19.87  5.2

Doucette and Goble,20 cross-sectional study (pretest/ posttest), separate comparison group

To determine the effect of exercise on lateral patellar tracking

Improved-symptoms group: n = n = 5; mean age, 16 y; gender and BMI not 43; mean age, 22.9 y; gender stated and weight not stated No-improvement-in-symptoms group: n = 8; mean age, 21.7 y; gender and weight not stated

Tape measure applied to midthigh region

cm

Mean  SD group 1, 49.3  3.87; group 2, 54.4  4.89; comparison, 49.4  2.67

Same as PFP groups (unaffected limb)

Thickness measured by ultrasound at the mid-thigh level

cm

Mean  SD males, 2.81  0.46; females, 2.48  0.43; comparison males, 3.21  0.44; comparison females, 2.86  0.63

n = 54; mean  SD age, 40.6  9.6 y; 13 male, 41 female; 57.9 kg

Ultrasound measurement of VMO volume at and below patella level

cm3

Mean  SD PFP, 1.8  1.5; comparison, 3.0  2.2

Aim of Study

PFP Group Characteristics

al-Rawi and Nessan,1 cross-sectional study, contralateral limb as comparison

To determine the relationship between joint hypermobility and PFP

Callaghan et al,11 randomized controlled trial, contralateral limb as comparison

Doxey,22 cross-sectional To determine via ultrasound the validity of study, contralateral assessing quadriceps limb bulk with girth measurements

Male group: n = 26; mean  SD age, 28.6  5.9 y; 80.2 kg Female group: n = 18; mean  SD age, 26  7.3 y; 64.2 kg

Outcome Results

Jan et al,26 case-control/cross-sectional study, separate comparison group

To determine the difference n = 54; mean  SD age, 40.8  9.3 y; 13 male, 41 female; in VMO morphology be58.4 kg tween PFP and healthy subjects

Kaya et al,29 crosssectional study, contralateral limb

To determine if women with PFP have quadriceps volume and strength deficits

n = 24; mean age, 41 y; 24 female; 69 kg

Same as PFP group (unaffected limb)

MRI of whole quadriceps volume

cm3

Mean  SD PFP, 938.7  210.1; comparison, 993.7  205.9

Leslie and Bentley,32 cross-sectional study, contralateral limb

To analyze the arthroscopic findings in participants with chondromalacia patellae

n = 78; mean age, 21.9 y; 26 male, 52 female; weight not stated

Same as PFP group (unaffected limb)

Tape measure applied 5 cm above the patella

cm

Difference greater than 2 cm classified as atrophy; 25 participants had atrophy

Pattyn et al,40 crosssectional study, separate comparison group

To determine if VMO atrophy exists in PFP

n = 46; mean  SD age, 25  7.4 y; 21 male, 25 female; mean  SD BMI, 22.8  3.4 kg/m2

n = 30; mean  SD age, 21.6  4.5 y; 13 male, 17 female; mean  SD BMI, 22.1  2.9 kg/m2

MRI measurement of cross-sectional area of each quadriceps muscle, patellar level and mid thigh

cm2

Mean  SD (total quadriceps) PFP, 67.0  15.1; comparison, 70.8  15.3

Peeler and Anderson,41 To determine the effects of stretching on PFP randomized controlled trial, separate comparison group

n = 40; mean  SD age, 31  7.9 y; 16 male, 24 female; mean  SD body mass, 24.9  3.7 kg

n = 43; mean  SD age, 28 Tape measure applied at the  7 y; 13 male, 30 fedistal thigh male; mean  SD body mass, 24.3  3.3 kg

cm

Mean  SD PFP, 38  3.3; comparison, 39  2.4

Abbreviations: BMI, body mass index; MRI, magnetic resonance imaging; PFP, patellofemoral pain; VMO, vastus medialis obliquus.



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TABLE 4

Total Score for Risk-of-Bias and Diagnostic Criteria*


Author

Score

al-Rawi and Nessan1

5

Callaghan et al11

8 10

Callaghan and Oldham10 Doucette and Goble20

3

Doxey22

6

Jan et al26

9

Kaya et al29

6

Leslie and Bentley32

5

Pattyn et al40

9

Peeler and Anderson41

6

*Score is out of 12.

When using girth measurements, no quadriceps atrophy was noted. The finding of quadriceps atrophy in the involved side of individuals with PFP may provide a rationale for the efficacy of strengthening exercises in reducing pain and improving function in this population,16,47 which suggests that assessing quadriceps strength may be a worthwhile clinical parameter. The finding of quadriceps atrophy in the involved limb of individuals with PFP contributes to understanding the mechanisms behind quadriceps weakness found previously in this population.5,28,29 The reduced force output of the quadriceps could be due to pain limiting force production, pain-induced inhibition of the quadriceps musculature, or physiological changes of the quadriceps musculature. If, contrary to the findings of this review, no difference were present in quadriceps size between PFP and comparison limbs, it would indicate that there is no physiological change in the quadriceps, and therefore interventions aimed purely to relieve pain may be sufficient to restore quadriceps strength. However, the finding of quadriceps atrophy in this review supports the notion that there is a physiological change within the quadriceps in this population, and, as quadriceps size has a strong correlation to quadriceps strength, 33,44 it is unlikely that normal

quadriceps function would return in PFP without targeted strengthening exercises. It is difficult to determine why people with PFP have quadriceps atrophy, as data were taken after the onset of symptoms and, therefore, it is not known whether atrophy was a predisposing factor or developed after the onset of PFP. A literature review of prospective risk factors for the development of PFP found only 1 study that measured quadriceps muscle size31; girth measurements were used and no difference was found between those who developed PFP and those who did not.34 However, quadriceps weakness has been identified as a predisposing factor for PFP,9,51 and it cannot be ruled out that quadriceps atrophy might accompany this identified weakness. Further prospective research using validated measurement methods is required to determine whether quadriceps atrophy is a predisposing factor for PFP. The VMO and VL were both assessed in only 1 study.40 Further high-quality research using validated measurement methods is required to determine if a difference exists between the amount of atrophy in the VMO and VL in individuals with PFP. Currently, there is insufficient evidence to support VMO/VL muscle size imbalance as a reason to prescribe exercises to isolate VMO activation in rehabilitation programs.

When compared to the asymptomatic comparison group, those with PFP showed an atrophy of the quadriceps of the involved limb that was not as great in comparison to their contralateral limb, as indicated by the magnitude of the standardized mean differences between groups. These data suggest that quadriceps atrophy may not only be present in the affected limb, but that the unaffected limb may also be atrophied or of reduced size compared to the quadriceps in an asymptomatic population. Further research is required to determine if a difference exists between the unaffected limb in those with PFP and the limbs of healthy populations. Analysis of PFP data compared to limbs of a comparison group may provide a more accurate measure of the extent of quadriceps atrophy in those with PFP than data from the contralateral limb, which could be subject to similar patterns of reduced loading or muscle inhibition as found in the affected limb. Girth may not provide an accurate measure of quadriceps muscle size, as girth measures have lower validity than other measures in estimating quadriceps muscle size.22 It is therefore difficult to extrapolate the finding of similar thigh girth in PFP and comparison limbs to the actual quadriceps muscle size in PFP. Girth measures have been moderately correlated to thickness measures in PFP (females, r = 0.61; males, r = 0.64),22 and thickness measures have been highly correlated to muscle volume (r = 0.881).36 The clinical utility of girth measures in estimating quadriceps muscle size is questionable, as differences in size between affected and unaffected limbs are likely to be small, and minor errors in measurement may affect the results; therefore, it is preferable to use alternative measures with higher validity. Ultrasound measurement of muscle thickness is often clinically available and has high validity in estimating quadriceps muscle size.3 Data on the proportion of participants with PFP with quadriceps atrophy demonstrated that quadriceps atrophy was



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TABLE 5

Assessment of Risk of Bias

Measurer Blinded

Justification of Sample Size

Provides a Measure of Variability

Reliability of Measurement Assessed

Score*

No

No

Yes

No

2

Yes

No

No

Yes

No

2

Yes

No

Yes

Yes

Yes

4

Representative of Population

Comparison Group Similar

al-Rawi and Nessan1

No

Yes

Callaghan et al11

No

Callaghan and Oldham10

No

Study

Doucette and Goble20

No

No

No

No

Yes

No

1

Doxey22

Yes

Yes

No

No

Yes

Yes

4

Jan et al26

Yes

Yes

No

No

Yes

Yes

4

Kaya et al29

No

Yes

No

Yes

Yes

No

3


No

Yes

No

No

Yes

No

2

Pattyn et al40

No

Yes

Yes

No

Yes

Yes

4


Yes

Yes

Yes

No

Yes

No

4

Score*

*Score is out of 6.

TABLE 6

Diagnostic Items for Patellofemoral Pain Greater Than 6 wk of Symptoms

Symptom Location

Insidious Onset

Symptoms Consistent With Diagnosis

Excludes Other Sources

Excludes Major Pathology

al-Rawi and Nessan1

Yes

Yes

Yes

No

No

No

3

Callaghan et al11

Yes

Yes

Yes

Yes

Yes

Yes

6

Callaghan and Oldham10

Yes

Yes

Yes

Yes

Yes

Yes

6


Yes

Yes

No

No

No

No

2

Doxey22

Yes

Yes

No

No

No

Yes

3

Jan et al26

No

Yes

Yes

Yes

Yes

Yes

5

Kaya et al29

Yes

No

No

No

Yes

Yes

3


Yes

Yes

No

Yes

No

No

3

Pattyn et al40

Yes

Yes

No

Yes

Yes

Yes

5


No

No

Yes

No

No

Yes

2

Study

*Score is out of 6.

not present in all individuals with PFP. It is unclear exactly how common quadriceps atrophy is, because the 2 studies reported different proportions.1,32 This difference most likely reflects the disparity in how quadriceps atrophy was defined. al-Rawi and Nessan1 considered a 0.5-cm difference in girth as quadriceps atrophy; this small difference could have categorized participants with similarsized quadriceps as having atrophy due to error in measurement. The finding that not all people with PFP have quadriceps atrophy may help to explain why some people with PFP respond more favor-

ably to strengthening interventions than others.24 For those without quadriceps atrophy, it is possible that interventions targeting hip kinematics may be more appropriate than quadriceps-strengthening exercises.42 The results of these meta-analyses should be approached with caution, as all of the included studies had potential for bias. It is important to note that although the risk of bias was assessed individually for each study, bias was not accounted for in the synthesis of the results. Scores on the risk of bias varied, which may be due to many of the studies not hav-

ing quadriceps muscle measurement as their primary aim. Many of these studies recorded quadriceps muscle size for use as demographic data, without intending to investigate its relationship to PFP. It is unlikely that these studies made stringent attempts to control factors affecting quadriceps muscle size (age, sex, weight). Specific reporting of diagnostic criteria was not present in many of the included studies, of which only 2 met all items on the diagnosis of PFP and many did not require pain with activities such as stair negotiation, squatting, or prolonged sitting to establish a diagnosis.



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Sample Size, n

Statistics for Each Study

Study

Subgroup Within Study

PFP

Comparison

SMD (95% CI)

P Value

Relative Weight


Mid thigh group 1

43

5

–0.016 (–0.942, 0.910)

.973

11.93


Mid thigh group 2

8

5

.055

7.56

Doxey22

Mid thigh female

18

18

–0.061 (–0.714, 0.593)

.856

20.46

Doxey22

Mid thigh male

26

26

–0.157 (–0.702, 0.387)

.571

26.13


Distal thigh

40

43

–0.349 (–0.782, 0.085)

.115

33.91

–0.084 (–0.435, 0.267)

.638

Total

1.180 (–0.026, 2.386)

SMD and 95% CI

–2.50 –1.25

0.00

Favors quadriceps atrophy

1.25

2.50

Favors quadriceps hypertrophy

Abbreviations: CI, confidence interval; PFP, patellofemoral pain; SMD, standardized mean difference. Heterogeneity, I2 = 28.2.

FIGURE 2. Forest plot of girth measurements of quadriceps muscle size in patellofemoral pain. Squares represent SMDs, the size of the square represents relative weight, lines represent 95% CI. The center of the diamond represents pooled SMDs, and the tips of the diamond represent pooled 95% Cl.

Sample Size, n Study


Callaghan and Oldham10 Contralateral limb


PFP

Comparison

SMD (95% CI)

P Value

Relative Weight

57

57

–0.058 (–0.425, 0.309)

.758

32.31

Doxey22

Female thickness

18

18

–0.742 (–1.417, –0.066)

.031

20.09

Doxey22

Male thickness

26

26

–0.889 (–1.458, –0.319)

.002

23.77

Kaya et al29

Volume

24

24

–0.264 (–0.833, 0.304)

.362

23.83

–0.442 (–0.855, –0.029)

.036

Total

SMD and 95% CI

–2.50 –1.25

0.00


1.25

2.50


Abbreviations: CI, confidence interval; PFP, patellofemoral pain; SMD, standardized mean difference. Heterogeneity, I2 = 58.6.

FIGURE 3. Forest plot of imaging measures of quadriceps muscle size in unilateral patellofemoral pain, with the asymptomatic limb as comparison. Squares represent SMDs, the size of the square represents relative weight, lines represent 95% CI. The center of the diamond represents pooled SMDs, and the tips of the diamond represent pooled 95% Cl.

Sample Size, n Study


Callaghan and Oldham10 Comparison ND


PFP

Comparison

SMD (95% CI)

P Value

Relative Weight

57

10

–0.386 (–1.061, 0.289)

.262

16.16

Jan et al26

Volume VMO

54

54

–0.637 (–1 024, –0.251)

.001

49.28

Pattyn et al40

Total quads

46

30

–0.250 (–0.712, 0.211)

.288

34.56

–0.463 (–0.734, –0.192)

.001

Total

SMD and 95% CI

–2.50 –1.25

0.00


1.25

2.50


Abbreviations: CI, confidence interval; ND, nondominant; PFP, patellofemoral pain; SMD, standardized mean difference; VMO, vastus medialis obliquus. Heterogeneity, I2 = 0.0.

FIGURE 4. Forest plot of imaging measures of quadriceps muscle size in patellofemoral pain, separate comparison group. Squares represent SMDs, the size of the square represents relative weight, lines represent 95% CI. The center of the diamond represents pooled SMDs, and the tips of the diamond represent pooled 95% Cl.



10/16/2013 4:49:07 PM


[ Of the 5 studies that did not require an insidious onset of symptoms, 2 did not specify patellar dislocation/subluxation as an exclusion criterion; however, these studies made no mention of dislocation or subluxation being present in their cohort with PFP.20,22 Although there may be enhanced risk for misdiagnosis in these studies, it is likely that the factors mentioned were a consideration but not a requirement to establish a diagnosis. The heterogeneity in diagnostic criteria between studies may reflect the fact that PFP is diagnosed by a set of signs and symptoms and is not ruled in or out by a single test.16

Clinical Relevance A visual assessment of quadriceps size is often performed in a clinical setting by comparing the size of the VMO between limbs. From this comparison, it is often inferred that VMO atrophy is present, and this is used as a justification for performance of exercises attempting specific activation of the VMO. Results of this review found that it is the total volume of the quadriceps that is atrophied in the symptomatic limb of individuals with PFP, and a difference in the ratio of the VMO to VL has not been established. The 1 study that did assess this ratio found no difference between symptomatic and comparison limbs.40 Therefore, the results of this review suggest that, at present, perceived differences in quadriceps size from visual inspection should not be assumed to be isolated VMO atrophy. Recent research has led many clinicians to shift their focus toward more proximal factors in PFP rehabilitation. Altered kinematics of the hip joint45,46 and reduced strength of the muscles surrounding the hip joint7,8 have been identified in PFP and proposed to increase lateral patellofemoral joint pressure.42 Further, interventions that target hip muscle strength23,25,30 and kinematics39,50 have been shown to be effective in improving pain and function in PFP. Research surrounding the hip joint in PFP is promising; however, assessment and treatment of the quadriceps femoris

research report still have clinical relevance. Similar outcomes from quadriceps-strengthening and hip muscle–strengthening interventions have been reported.47 The findings of this review that suggest quadriceps atrophy is present in some people with PFP, along with the results of a literature review that suggest that reduced quadriceps strength is a risk factor for PFP,31 indicate that quadriceps-strengthening exercises may still be an important consideration in this population.

Limitations Due to the paucity of research on quadriceps muscle size in individuals with PFP and the lack of a standard procedure to measure quadriceps muscle size, it was not possible to ensure that all included studies used the same measurement method. Considerable heterogeneity was present in the measurement of the quadriceps muscle or its components (girth, thickness, cross-sectional area, volume) and the location of the measurement along the quadriceps. Many studies performed measurements at the distal thigh, in contrast to evidence from MRI crosssections suggesting that the mid thigh is the best measurement location when correlating measurements made in 1 location to the total quadriceps muscle volume.17,38 It is possible that quadriceps atrophy may occur asymmetrically or affect different sections (eg, the VMO) of the quadriceps differently. Including studies in the meta-analysis regardless of the quadriceps muscle(s) measured or the location of the quadriceps measurement presents a risk that the results may not reflect the true quadriceps muscle size in these participants. Changes in quadriceps muscle size due to PFP are likely to be small; it is therefore important that the measurement of quadriceps muscle size be reliable and valid to detect change. Quadriceps volume is considered the gold standard in estimating muscle size,38 but was only assessed in 2 studies. Measures of thickness and cross-sectional area have a high correlation to volume (r = 0.88136 and r

] = 0.964,38 respectively) and are therefore likely to provide valid results. Despite only a moderate correlation between girth and thickness measures,22 girth is a common clinical measurement of quadriceps muscle size, and these studies were included to assess all the available literature on quadriceps muscle size.

CONCLUSION

T

his review showed that quadriceps atrophy exists in the involved limb of individuals with PFP when compared by imaging techniques to either the asymptomatic limb or a separate comparison group. Insufficient evidence exists to determine whether there is a difference in atrophy between different sections of the quadriceps, such as the VMO and VL. Further high-quality research utilizing valid measurement techniques is required to further validate these findings and to determine if a specific section of the quadriceps is most affected. t

KEY POINTS FINDINGS: This review of 10 studies found

quadriceps atrophy in the involved limb of individuals with PFP when measured with imaging techniques (MRI and ultrasound) but not with girth measures. Limited evidence that is currently available suggests that there is no difference in the amount of atrophy of the VMO and VL. IMPLICATIONS: The results of this review provide a rationale for the inclusion of quadriceps-strengthening exercises for individuals with PFP. CAUTION: This review does not reveal whether quadriceps atrophy is a cause or a result of PFP. Considerable heterogeneity existed in methodological, population, and procedural details within and between many of the studies included in the review.



10/16/2013 4:49:08 PM


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