Comparison of Gluteus Medius Muscle Activation in Women With and Without Patellofemoral Pain

Key Points

• Women with patellofemoral pain had reduced activation of the gluteus medius muscle.

• Identifying the presence of inhibition may be useful for clinicians to determine the most appropriate treatment techniques.

Patellofemoral pain (PFP) affects as much as 7.3% of all patients who seek care from an orthopaedic physician in the United States.¹ Patellofemoral pain accounts for approximately 25% of all knee injuries among physically active populations,² and the prevalence of PFP in women is twice that in men.¹ Patellofemoral pain commonly presents as diffuse pain across the anterior knee that increases with activities such as running, squatting, and walking up and down stairs.³ The etiology of PFP is multifactorial, because numerous underlying factors are associated with development and progression of this condition, including but not limited to muscle weakness, abnormal motor activation patterns, abnormal joint kinematics, and abnormal joint stress.^3–5

Clinicians and researchers place a large focus on the gluteus medius in the evaluation and management of PFP. The gluteus medius is an important stabilizer muscle, functioning to maintain neutral alignment of the lower extremity in the frontal plane during dynamic movement.⁶ To prevent excessive lower extremity malalignment in the frontal plane, adequate strength and activation of the gluteus medius are important. However, deficits in strength and activation are common in individuals with PFP.^6–10 It has been theorized that abnormal gluteus medius muscle function is related to excessive hip adduction and internal rotation, causing dynamic knee valgus and contributing to the development of PFP.¹¹

Although current treatment strategies aim to improve hip musculature function, there are inconsistent findings in how these strategies lead to improved strength or movement patterns.^12–14 The lack of improvements in strength or movement patterns for some individuals with PFP may imply additional underlying neuromuscular factors that should be considered in the evaluation and management of PFP. Therefore, it would be beneficial to investigate additional assessment tools that could detect specific deficits in hip function beyond strength and movement patterns.

One underlying explanation for abnormal gluteus medius activation in individuals with PFP could be related to muscle inhibition. An inhibited muscle is not capable of recruiting all available motor units, resulting in reduced force output. One suggested explanation for inhibition occurring in the gluteus medius is disrupted neural signaling transmission.¹⁵ This is suggested to occur when mechanoreceptors located inside the tissues of a strained joint are excessively activated, which in the case of PFP could be caused by excessive hip adduction. This heightened joint afference leads to an inhibitory response to the surrounding musculature, reducing its voluntary activation.¹⁵ The superimposed-burst (SIB) technique is commonly used to measure muscle voluntary activation and is quantified as the central activation ratio (CAR).^16–18 The CAR indicates the level of voluntary activation of a specific muscle, ranging from 0% to 100%. Although the CAR is a valid and reliable measure in individuals with PFP, this has been limited to the quadriceps.^16,17 Hart et al found that patients with anterior knee pain had 78.6% quadriceps inhibition and suggested this may lead to muscle weakness and kinematic changes.¹⁶ Researchers recently provided initial evidence that the CAR is a valid and reliable measure of gluteus medius and maximus activation in a healthy cohort.¹⁸ Gluteal CAR has been assessed in a small cross-sectional study but has not been compared directly with a healthy cohort.¹⁹ Determining the gluteal CAR for women with PFP could assist in investigating the lack of improvements in strength sometimes found after rehabilitative treatment. Therefore, the purpose of this study was to compare the gluteus medius CAR of women with and without PFP. We hypothesized that women with PFP would present with reduced CAR in comparison with the pain-free controls.

METHODS

The STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) checklist for case-control studies was used to assist in providing quality methodology.²⁰ In this case-control study, we compared group differences between women with PFP and pain-free controls. The independent variable was group (PFP, control). The dependent variables were CAR of the gluteus medius and maximal voluntary isometric contraction (MVIC) of the gluteus medius.

Participants

Twenty-eight female participants volunteered for this study: 13 pain-free controls and 15 with PFP. As an interinstitutional collaborative study, participants with PFP were collected from 2 universities and surrounding communities. Both the University of Nevada, Las Vegas, and University of Toledo obtained institutional review board approval. Before data collection, participants were screened for inclusion and exclusion criteria (Table 1) adhering to the International Patellofemoral Pain Consensus Statement.²¹ Once a participant’s eligibility was confirmed, written informed consent was acquired. All participants with PFP were screened by a licensed athletic trainer with 10+ years of clinical experience to confirm diagnosis based on their symptoms. Any participant who reported PFP bilaterally was instructed to self-select their most symptomatic side to be used for testing.

Table 1.Inclusion and Exclusion Criteria

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Procedures

Participants reported to the research laboratory for a single data collection session. For pain-free controls, the dominant extremity (ie, preferred leg to kick a ball) was chosen for testing.

During the session, 2 measures were collected: hip-abduction MVIC force (F_MVIC) and MVIC force with a SIB of electrical stimulation (F_SIB). Before testing, participants completed a 5-minute walking warm-up on a treadmill at their preferred walking speed with 0% incline. Then, two 5- × 9-cm adhesive electrodes (Axelguard) were placed over the participant’s gluteus medius, with one placed directly inferior to the iliac crest and the second directly superior to the greater trochanter.¹⁸ Assessment of hip-abduction strength was performed with the participant in a standing position. The dynamometer axis of rotation was lined up with the anterior superior iliac spine while the arm of the dynamometer was attached to the leg approximately 5 cm proximal to the lateral femoral condyle. The Biodex chair was positioned to assist with stabilizing trunk motion. The chair height was adjusted so that a bolster placed on the chair would be at the level of the participant’s contralateral hip to prevent trunk and pelvic motion (Figure 1). When testing was being completed, participants were instructed to stand up straight with their arms held across their chest.

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As described previously, to acclimate participants to the task, they performed a sequence of submaximal isometric contractions at 25%, 50%, and 75% of their self-determined maximal ability with a 1-minute rest between trials.¹⁸ Participants were instructed to perform these contractions by ramping up to the defined intensity and holding for 3 to 5 seconds. Participants were then instructed to perform 2 contractions of maximal effort, while also being given verbal feedback from the investigator and visual feedback on a computer monitor. The verbal and visual feedback were provided to encourage the participant to perform at true maximal effort. The visual feedback was a line graph representing the amount of force the participant was producing in real time. The participant then performed 6 MVICs with a superimposed electrical burst stimulation. The first 3 trials were performed with maximal contraction and with submaximal stimulus amplitude at 25%, 50%, and 75%. The last 3 trials were performed with a 100% SIB stimulation applied with a stimulus-isolation unit. This produced a 100-millisecond train of 10 square-wave pulses at an intensity of 125 V (pulse duration = 600 microseconds, frequency = 100 Hz).¹⁸ The SIB stimulus was administered when the investigator saw a plateau in the real-time torque display. One minute of rest was given between trials. The last 3 trials of maximal contractions were used as F_MVIC and F_SIB.

RESULTS

The participant demographics and characteristics are presented in Table 2. The results of the general linear model demonstrated a statistically significant main effect of group (F_1,26 = 10.4, P = .004). Women with PFP had a lower gluteus medius CAR than women without PFP even after accounting for age (P = .29), mass (P = .24), and hip-abduction MVIC (P = .29). We confirmed that results of the analysis possessed no outliers, and collinearity between predictor variables was in the appropriate range. The estimated differences between groups were −0.28 gluteus medius CAR (95% CI = −0.45, −0.1; average control gluteus medius CAR = 0.72; average gluteus medius CAR PFP = 0.44). Back transformation of the estimated mean group difference equated to 2.5% gluteus medius CAR (average control gluteus medius CAR = 98.4%, PFP = 95.9%, estimated effect size = 1.35; 95% CI = 0.39, 2.3; large effect). Overall, after controlling for participant age, mass, and hip-abduction MVIC, the PFP group had an average gluteus medius CAR score 2.5% lower than that of the pain-free control group. Figure 2 shows the results found for the gluteus medius CAR and gluteus medius MVIC.

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Table 2.Participant Characteristics

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DISCUSSION

The purpose of this study was to determine if individuals with PFP have a lower CAR for the gluteus medius when compared with pain-free controls. The main observation of this study indicated that women with PFP have a significantly lower CAR than pain-free controls. It is important to note that, although a difference was found, the gluteus medius activation levels ranged from 74% to 99% within the PFP group. This is not surprising, because PFP is multifactorial, with numerous underlying factors associated with the development and progression of the condition, resulting in a patient population that presents with a diverse range of symptoms and functional abnormalities. Both findings, including the reduced CAR and varied activation levels, agree with the first study conducted that examined whether females with PFP exhibited lower gluteal muscle activation.¹⁹ This study used the same methodology for the CAR assessment of the gluteus medius with a smaller cohort of females with PFP.¹⁹

The average gluteus medius CAR for women with PFP was 95.9%, whereas the average for pain-free controls was 98.4%. Our findings for gluteus medius activation were slightly higher for both groups compared with prior research, wherein the CAR was between 96.1% and 96.6% for healthy women¹⁸ and 90.5% for women with PFP.¹⁹ These previous studies differed in that one had a smaller cohort of female participants with PFP (n = 7) and did not include a healthy cohort for direct comparison,¹⁹ and the other assessed only a healthy cohort (n = 20) with both males and females to establish validity and reliability of the CAR for the gluteal muscles.¹⁸

One interesting finding was that the PFP group in our study had similar hip-abduction torque (1.36 N·m/kg) when compared with the control group (1.15 N·m/kg). This could indicate that, although the PFP group had similar hip-abduction strength, due to decreased activation of the gluteus medius, they may have relied on other muscles to compensate and generate the abduction torque (ie, tensor fasciae latae, gluteus maximus). The gluteus medius is an important stabilizer muscle functioning to maintain neutral alignment of the lower extremity in the frontal plane during dynamic movement.⁶ During functional activities, such as running, the demand on the gluteus medius was found to peak at an activation at 112.4% of MVIC and to average 81.4% of MVIC in a group of women with PFP, which was not significantly different from the comparison healthy control group.²⁵ However, female participants with PFP did display gluteus medius activation that was delayed and shorter in duration during running.²⁵ This provides another example to illustrate the importance of using specific assessment tools to examine different aspects of neuromuscular control.²⁵

Although a standard of care exists for the treatment and rehabilitation of PFP, the long-term outcomes are poor, resulting in abnormal findings such as persistent pain,^26–28 restrictions in both daily^26,27 and physical^26–28 activities, and no improvements in hip^29,30 and quadriceps³¹ strength. A recent theoretical model suggests some of these abnormal findings, specifically a lack of improved strength, could be related to an underlying influence of muscle inhibition, which provided the motivation for the current study.¹⁵ The findings from our study could provide some insight to explain why some individuals with PFP may be unresponsive to strengthening of the gluteus medius. For example, our study had 4 participants with a CAR less than 95%, suggesting altered gluteus medius muscle function for these individuals. This also indicates that not all individuals with PFP exhibit impaired gluteus medius voluntary activation, but some do. This heterogeneous symptomology provides justification to consider adjusting our current practice for evaluation and treatment of PFP for individuals identified with reduced voluntary activation.

One way to address heterogeneous symptomology could be subgrouping patients by their prominent impairment, such as impaired voluntary activation, and then designing their treatment with interventions focused on the prominent impairment. Subgrouping of individuals with PFP has been suggested and studied with success and improved outcomes.^32,33 The wide range in gluteus medius activation found in our study (74% to 99%) would support the concept of subgrouping.

Subgrouping was recommended after it was determined that one-third of patients in a randomized controlled clinical trial were unresponsive to a strengthening protocol,³⁰ and 3 subgroups³³ were first suggested after 127 patients were evaluated for similarities. Current clinical practice for PFP does not involve specific approaches to address inhibition, which could mean clinicians are not able to provide optimal treatment. In addition, there currently is not a clinician-friendly approach to determine if a patient has muscle inhibition because very specific equipment is necessary to assess the CAR. Therefore, it could be suggested that a subgroup should be created for patients who are unresponsive to strengthening protocols to attempt to determine if this is related to impaired voluntary activation. Future researchers could evaluate nonresponders to determine if muscle inhibition may explain their lack of success with a traditional strengthening protocol. Establishing muscle inhibition’s connection to nonresponders could lead to research that could determine effective treatment strategies for individuals with PFP who demonstrate inhibition of the gluteus medius. Disinhibitory modalities, such as focal joint cooling or conventional transcutaneous electrical nerve stimulation to the knee joint, have been used for treating inhibition; however, clinicians should be aware these interventions have only been evaluated for quadriceps inhibition and not for gluteal inhibition.³⁴ Before tailored rehabilitation for individuals with gluteal inhibition can be recommended, future researchers should compare potential interventions that have been successful at addressing inhibition of other muscles.

CONCLUSIONS

Women with PFP had reduced voluntary activation of the gluteus medius and presented with a wide range of gluteus medius activation levels. Moreover, inhibition was not present in all women with PFP, indicating further that assessment of gluteus medius voluntary activation should occur in patients with PFP to determine the most effective treatment strategies.

FINANCIAL DISCLOSURE

Dr Lee reports grants from the Department of Defense, grants from the National Institutes of Health, and personal fees from the Symposium on Advanced Wound Care outside the submitted work; in addition, Dr Lee has a patent to Method and Apparatus for Performing Timed Up-And-Go Test issued.