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The effects of muscle fatigue on dynamic standing balance in people with and without patellofemoral pain syndrome
Gait & Posture 37 (2013) 336–339
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
The effects of muscle fatigue on dynamic standing balance in people with and without patellofemoral pain syndrome Hossein Negahban a, Malihe Etemadi a,*, Saeed Naghibi b, Anita Emrani c, Mohammad Jafar Shaterzadeh Yazdi a, Reza Salehi a, Aida Moradi Bousari b a b c
Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran Sport Science Research Center (SSRC), Tehran, Iran Department of Physical Therapy, School of Rehabilitation Sciences, Tehran University of Medical Sciences, Tehran, Iran
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 February 2012 Received in revised form 23 July 2012 Accepted 27 July 2012
The aim was to examine the effects of muscle fatigue of knee extensor and hip abductor muscles on dynamic standing balance of patients with patellofemoral pain syndrome (PFPS) compared to their healthy matched controls. Thirty participants (15 with PFPS, 15 controls) were recruited. Isolated muscle fatigue of two muscles was induced isokinetically in three separate sessions (one practice and two testing sessions) with a rest interval of at least 72 h. In each testing session, fatigue protocol of only one muscle group was performed for the both legs with a rest time of 30 min. After determining peak torque, participants were encouraged to perform continuous maximal concentric–eccentric contraction of the target muscle until the torque output dropped below 50% of peak value for 3 consecutive repetitions. Immediately after the completion of the fatigue protocol, balance testing of participants was undertaken during single leg standing using the Biodex stability system. Balance stability measures included the overall, anteroposterior and mediolateral stability indices (OSI, APSI and MLSI, respectively). Patients exhibited decreased balance stability in the sagittal plane (higher APSI) when compared to controls. Isolated muscle fatigue of the knee extensors and hip abductors reduced balance stability in both study groups. Fatigue of hip abductors was associated with greater balance instability (higher OSI and APSI) than fatigue of knee extensors. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Fatigue Standing balance Patellofemoral pain
1. Introduction Patellofemoral pain syndrome (PFPS) is a common musculoskeletal disorder [1,2] which occurs more frequently in athletes and in women compared to non-athletes and men, respectively [3–5]. Nearly 21% of knee complaints [6] and 10–25% of all patients referred to the physiotherapy clinics [7] are diagnosed with PFPS. Standing balance control is a key component of most daily and sports activities [8]. Balance can be evaluated in both static (force platform) and dynamic (moveable balance platform) conditions and during both double and single leg standing [8,9]. While several studies have extensively examined standing balance control of patients with different knee disorders such as anterior cruciate ligament injury [10–12], little is known on balance ability of patients with PFPS.
* Corresponding author. Tel.: +98 611 374 3101; fax: +98 611 374 3506. E-mail addresses: [email protected] (H. Negahban), [email protected] (M. Etemadi), [email protected] (S. Naghibi), [email protected] (A. Emrani), [email protected] (M.J. Shaterzadeh Yazdi), [email protected] (R. Salehi), [email protected] (A. Moradi Bousari). 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.07.025
Muscle fatigue, which is defined as the decline in force output capacity after repeated muscle contractions [8,13–15], is a common occurrence in most activities of daily living and sporting competitions [14,16,17]. Specifically, most sports injuries occur during the late stage of competitions in which muscles become fatigued [8]. It has been assumed that muscle fatigue is one of the main causes of impaired balance [13,15]. The post-fatigue impairment in balance control is often attributed to deficit in neuromuscular control resulting from altered somatosensory inputs [8,9,13]. Recently, the evaluation of balance control in the presence of isolated muscle fatigue has become a popular research focus [16]. The adverse effects of lower extremity muscle fatigue on balance performance have been reported in the young [8,15,17–19] and elderly [13] healthy populations and also in some pathological conditions such as chronic ankle instability (CAI) [9,16]. This study aimed to examine the effects of muscle fatigue of the knee extensor and hip abductor muscles on dynamic standing balance of patients with PFPS compared to healthy matched controls. From a clinical viewpoint, understanding the effects of muscle fatigue on balance performance may provide important insight into the role of muscle weakness in the development of PFPS. Also, it may help to assess
H. Negahban et al. / Gait & Posture 37 (2013) 336–339
the potential contribution of muscle strengthening exercises in the prevention and rehabilitation of patients with PFPS. Increased fatigability followed by muscle weakness is one of the primary symptoms of patients with different musculoskeletal disorders [19]. Knee extensor (quadriceps) weakness has been considered as a major contributing factor in the development of PFPS [4,5]. Strengthening exercise of this muscle is an important aspect in the management of this condition [20]. Furthermore, several studies have associated the reduction in cross-section area of the hip abductor (gluteus medius) with PFPS [1,4,5]. Improvement of pain and dysfunction in these patients has been attributed to strengthening exercises of this muscle [1]. Theoretically, gluteus medius weakness during single leg standing could result in dropping of the pelvis on the contra-lateral side, increased hip adduction/internal rotation, increased lateral patellar contact pressure, and thereby it may contribute to the development of PFPS [1,3–5]. It was hypothesized that PFPS patients would exhibit poor balance stability during single leg standing on a dynamic moveable platform, compared to controls. Furthermore, dynamic standing balance of patients would be more affected by fatigue of the knee extensor and hip abductor muscles, compared to healthy controls. 2. Materials and methods 2.1. Subjects Thirty participants (15 with PFPS, 15 controls) between the ages of 19 and 35 years were recruited. All participants provided a written informed consent prior to participation in this investigation. PFPS patients were recruited from orthopedic and physiotherapy clinics in Tehran, Iran. Inclusion criteria were: (1) non-traumatic anterior or retropatellar pain for more than 6 months [20]; (2) pain on palpation of the patellar facets [1] or facet compression; and (3) pain on at least two of the following activities: prolonged sitting with bent knees, squatting, kneeling, running, hopping/jumping, and ascending or descending stairs [1,2]. Patients were excluded if they had: (1) diagnosis of knee osteoarthritis, patellar tendonitis, or patellar dislocation/ subluxation [21]; (2) clinical evidence of knee ligament, meniscus, or tendon injuries [1,21]; (3) involvement of other joints affecting the lower extremities or the back in the past year; (4) history of any neurological deficit [21]; and (5) previous history of surgery including arthroscopy [21]. None of the patients was undergoing physical therapy in the 30 days preceding the study. All participants were asked to refrain from any strenuous exercise for 2 days before testing to prevent muscle fatigue [2]. In order to evaluate pain and disability, all patients completed a 10-cm visual analogue scale (VAS) [20] and the Kujala patellofemoral scale (KPS) [22]. Additionally, in order to match the activity level of patients and healthy subjects, the Tegner activity rating scale [23] was completed by both study groups. The scoring range of the VAS was 0–10, where 0 indicated no pain and 10 the worst pain [20]. The KPS is a 13-item, self completed instrument with different categories consisting of limping, weight bearing, walking, stairs, squatting, running, jumping, prolonged sitting, pain, swelling, painful patellar movements, muscle atrophy, and flexion deficiency [22]. The total score ranges from 0 to 100, with higher scores indicating lower levels of disability [22]. The Tegner activity scale is a one-item instrument that assesses activity levels for sports and occupational activities. It has 11 items with a scoring range of 0–10. Higher scores represent higher levels of
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physical activity [23]. Iranian-versions of the KPS [22] and the Tegner scale [23] have been validated for use in Iran. The selection of the control group was based on the same exclusion criteria as for the patient group. Healthy subjects were matched with patients according to gender (12 female, 3 male), age, height, body mass index, and activity level (Table 1). 2.2. Fatigue protocol This study was approved by the local Institutional Review Board. The fatigue protocol used in this investigation followed previously published protocols for studying balance control in the presence of fatigue of lower limb muscles [9,13,17–19]. Isolated muscle fatigue of knee extensor and hip abductor muscles was induced using a Biodex System yV isokinetic dynamometer (Biodex Inc., Shirley, NY, USA). Three separate sessions (one practice and two testing sessions) with a rest interval of at least 72 h were assigned to each subject in order to minimize possible learning and fatigue effects [8,19]. The practice session was used to allow familiarization with the equipment and procedure. During each testing session, only one muscle group was tested in both legs with a resting time of 30 min. The order of muscle group and side tested were randomly assigned for each participant. The involved leg of each patient was matched with the corresponding leg of a healthy control according to their dominant side. The leg used to kick a ball was defined as dominant [4,8]. At first, 3 practice trials of sub-maximal and 3 of maximal contractions were performed. After a 60 s rest and in order to determine peak torque, 3 repetitions of maximal concentric–eccentric contraction with no rest were performed at the speed of 608/s [9,18]. The highest torque achieved during the 3 repetitions was considered as peak torque. After 2–3 min, participants were instructed to perform continuous maximal concentric–eccentric contractions of the target muscle at 608/s until the torque output dropped below 50% of peak torque for 3 consecutive contractions. This definition of fatigued state has been used in previous studies on fatigue-balance [9,13,17–19]. Participants were given verbal encouragement throughout the isokinetic fatigue protocol [17,18]. Patient positioning in the isokinetic dynamometer was based on the guidelines provided by the manufacturer. Concentric–eccentric contraction of the quadriceps was performed through a range of motion from 908 to 308 knee flexion in the sitting position. As maximal knee extension in the open kinetic chain can increase the patellofemoral joint reaction force [20] and in order to reduce the patellofemoral stress to a minimum during the fatigue protocol, the last 308 of knee extension were excluded by the equipment. For the gluteus medius, participants were positioned side-lying in front of the isokinetic dynamometer [4] and concentric–eccentric contraction was performed within the available range of hip abduction. 2.3. Balance testing According to previous studies, fatigue recovery (i.e. return to above 80% of peak torque after fatigue) occurs within 2–4 min after the completion of the fatigue protocol [17]. Therefore, all balance testing of this investigation was completed immediately after fatigue [4,17]. The Biodex stability system (BSS) SD (Biodex Medical System Inc., Shirley. NY, USA) is used for the quantitative assessment of dynamic standing balance [17]. It consists of a circular moveable platform that provides up to 208 tilt in a range of 3608 [15]. The BSS measures stability ranging from 1 to 12 with higher scores corresponding to increased platform stability. All balance testing in this study was conducted on the moderate level of 4. Balance stability measures extracted from the BSS include the overall, anteroposterior and mediolateral stability indices (OSI, APSI and MLSI, respectively). These stability indices represent the mean angular displacement of the platform in degrees from a level, zero-point position [24–26]. Higher and lower stability indices correspond to greater and lesser movement of the
Table 1 Demographic and functional characteristics of PFPS and healthy groups. PFPS group (n = 15)
Healthy group (n = 15)
P value
Mean (SD)
Mean (SD)
(Mean differences)
Demographic data Age (year) Height (m) Body mass index (kg/m2) Duration of symptoms (month)
25.8 (4.41) 1.64 (10.8) 22.7 (3.78) 29.2 (20.7)
25.2 (5.17) 1.64 (10.4) 22.9 (3.87) N/A
0.73 0.97 0.88
Tegner activity score a Kujala patellofemoral scale b Visual analogue scale c (pain)
6.46 (1.35) 78.0 (7.74) 5.66 (1.11)
6.73 (1.16) N/A N/A
0.56
PFPS: patellofemoral pain syndrome; SD: standard deviation; N/A: not applicable. a Range of scores is from 0 to 10. b Range of scores is from 0 to 100. c Range of scores is from 0 to 10.
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platform away from the central reference point, respectively [24,26]. Therefore, higher score indicates a greater difficulty maintaining the platform in a stable position, hence poor balance stability. Conversely, lower scores represent better stability and, therefore, better balance [8,15,25–27]. The reliability of these stability measures has been reported in several studies, with intra-class correlation coefficients of 0.60–0.99 during single leg standing on the platform [8,17,27]. Participants were asked to place one leg on the central region of the platform while the other leg was in a position of slight hip flexion/abduction and 908 of knee flexion [17]. The foot coordinates were recorded for the first time and were maintained throughout the testing trials of each participant [8,15]. Participants were asked to look straight ahead and place their arms crossed over the chest [15,17] and to keep the platform as motionless as possible for 20 s. Balance testing consisted of 3 trials before the fatigue protocol and 2 trials immediately after fatigue with a rest interval of 20 s between trials [8]. The first trial before fatigue was a practice one. The average of the pre- and post-fatigue balance testing was used for further analysis. 2.4. Statistical analysis A separate 2 2 2 2 (2 groups; 2 muscles; 2 times; 2 legs) mixed model of analysis of variance (ANOVA) test was used to determine main effects and interactions of these factors for each of the balance stability measures (OSI, APSI, MLSI) [28]. An alpha level of 0.05 was used for all statistical analyses.
3. Results The mean (SD; standard deviation) pain level of patients was 5.66 (1.11) for most painful functional activities during the previous 2 weeks. The mean (SD) disability level of patients was 78 (7.74). Table 2 shows the mean and SD for pre-fatigue and post-fatigue measurements of all balance stability measures. The results of ANOVA showed that the only significant interaction was seen for the interaction of group by leg in the sagittal plane (F1, 28 = 10.9, P < 0.01 for APSI). Further analysis by independent t-test showed that there were between-group differences for APSI only when the patients were standing on the involved leg and were compared with the corresponding leg of the healthy group (P < 0.01). When comparison was made between the uninvolved leg of patients and corresponding leg of healthy group, no significant differences were seen (P > 0.05). The main effect of time (pre-fatigue vs. post-fatigue measurement) was significant, indicating that fatigue had a significant effect on all stability measures (F1, 28 = 13.0, P < 0.01 for OSI;
F1, 28 = 7.15, P = 0.01 for APSI; F1, 28 = 5.55, P = 0.02 for MLSI). The main effect of muscle (hip abductor vs. knee extensor) was significant for OSI (F1, 28 = 8.49, P < 0.01) and APSI (F1, 28 = 7.48, P = 0.01), indicating that fatigue of the hip abductors led to greater changes in stability indices compared to fatigue of the knee extensors.
4. Discussion To our knowledge, this investigation was the first to examine dynamic standing balance in patients with PFPS. The results showed that, irrespective of fatigue effects and during standing on the involved leg, patients exhibited decreased balance stability in the sagittal plane (higher APSI) when compared to healthy controls. A deficit in knee proprioception followed by patellofemoral pain [29] could be proposed as a major contributing factor contributing to poor balance stability in this patient population. Additionally, direction-specific balance instability in the patients could be attributed to the fact that PFPS is a musculoskeletal disorder that affects stability mainly in the sagittal plane. Isolated muscle fatigue of the knee extensor and hip abductor muscles reduced balance stability in both study groups. These findings are consistent with previous investigations that examined the effects of lower limb muscle fatigue induced by either isokinetic [17–19] or functional [8] methods on balance control of healthy young subjects using a static [18] or a dynamic moveable platform [9,17]. Fatigue of the hip abductors was associated with greater balance instability (higher OSI and APSI) than fatigue of the knee extensors. Previous studies on the relative contributions of the proximal (hip) and distal (ankle) muscles in maintaining single leg stance in a fatigued state showed that fatigue in the proximal muscles caused greater impairment in balance stability than fatigue induced to distal muscles [8,9,17]. This could be attributed to the assumption that proximal muscles of the lower extremity have a crucial role in maintaining balance under more challenging dynamic conditions [9,17]. Contrary to these findings, Reimer and Wikstrom [8] found that functional fatigue of the ankle and hip muscles caused similar impairments in single leg stance as measured by balance stability indices obtained from the BSS. This inconsistency could be explained by the fact
Table 2 Mean (standard deviation) of the overall, AP and ML stability indexes for two levels of pre- and post-fatigue in two groups of PFPS and healthy participants. Fatigue levels
Pre-fatigue PFPS
Fatigue protocol on knee extensors Standing on the involved leg (and its matched leg in the control group) Overall stability index 4.32 (1.80) AP stability index* 2.77 (1.58) ML stability index 2.80 (1.30) Standing on the uninvolved leg (and its matched leg in the control group) Overall stability index 3.72 (1.19) AP stability index 2.19 (0.80) ML stability index 2.60 (1.22) Fatigue protocol on hip abductors Standing on the involved leg (and its matched leg in the control group) Overall stability index 4.75 (1.77) AP stability index* 2.89 (1.40) ML stability index 3.34 (1.29) Standing on the uninvolved leg (and its matched leg in the control group) Overall stability index 4.28 (1.68) AP stability index 2.75 (1.37) ML stability index 2.84 (1.15)
Post-fatigue Healthy
PFPS
Healthy
3.56 (1.46) 2.06 (1.00) 2.40 (1.45)
5.20 (3.16) 3.26 (2.01) 3.57 (2.60)
3.71 (1.87) 1.94 (1.05) 2.69 (1.81)
4.09 (0.86) 2.48 (1.07) 2.70 (1.22)
4.12 (1.52) 2.45 (1.08) 2.78 (1.63)
3.95 (1.44) 2.48 (1.08) 2.58 (1.50)
3.70 (1.27) 2.17 (0.78) 2.50 (1.50)
5.43 (1.77) 3.13 (1.01) 3.81 (2.14)
4.19 (1.51) 2.50 (0.76) 2.84 (1.78)
3.85 (1.04) 2.48 (0.84) 2.52 (1.17)
5.00 (1.99) 3.20 (1.80) 3.06 (1.63)
4.78 (1.38) 3.41 (1.01) 2.82 (1.67)
AP: anteroposterior; ML: mediolateral; PFPS: patellofemoral pain syndrome. * Indicates significance: irrespective of fatigue effects and during standing on the involved leg, patients exhibited decreased balance stability in the sagittal plane (higher APSI) when compared to their healthy controls.
H. Negahban et al. / Gait & Posture 37 (2013) 336–339
that, in contrast to isokinetic fatigue induced by an open kinetic chain, functional fatigue induced by closed kinetic chain exercises incorporates activation of all muscle groups (and not isolated muscles) [8]. Therefore, it is not possible to compare the relative contribution of isolated muscle fatigue on balance performance. Similar effects of muscle fatigue on dynamic standing balance between the two study groups were found in this study. This is in contrast to the study of Gribble et al. [9] in which isokinetic fatigue of the hip, knee, and ankle resulted in a smaller reach distance value in the CAI patients than their healthy matched controls. These authors used the star excursion balance test (SEBT) as a measure of functional balance in their study. Similarly, Hosseinimehr et al. [16] found that sports-related fatigue of the lower extremity resulted in a significant decrease in the reach distance of patients with CAI relative to healthy controls as measured by SEBT. The inconsistent results of these studies compared to ours may partially relate to the different patient populations (CAI vs. PFPS) and the different measures of balance (SEBT vs. BSS) used in these studies. Therefore, it seems that the SEBT is a more sensitive measure to detect different effects of muscle fatigue on balance performance of two study groups and we recommend its uses in future studies. In addition, as the disability level of our patients, as measured by the KPS, was low it is probable that patients with severe disability level exhibit different fatigue effects when compared to healthy controls. Thus, we recommend selection of patients with a higher level of disability for future investigations. Our study had some limitations. Firstly, the isolated fatigue induced by isokinetic methods is not representative of muscle fatigue occurring during functional activities or sports. Therefore, the results may not be generalized to functional activities. However, previous studies showed that both isokinetic and functional fatigue protocols caused similar impairments in standing balance performance [8]. The second limitation is that due to the relatively small number of subjects, the results should be considered as preliminary. In conclusion, patients with PFPS exhibited decreased balance stability in the sagittal plane when compared to controls. Therefore, balance training should be incorporated in the rehabilitation of these patients. Moreover, muscle fatigue had an adverse effect on balance performance but these effects were not different between the two study groups. Source of support This work was part of M.Sc thesis of Mrs. Etemadi and was supported by a Master thesis grant (no: pht-8901) in Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran. Acknowledgement We thank Dr. Mazaheri and Dr. Latifi for their assistance with study design and statistical advice, respectively. Conflict of interest None of the authors have any financial or other interests relating to the manuscript to be submitted for publication in Gait & Posture. References [1] Boling MC, Padua DA, Creighton RA. Concentric and eccentric torque of the hip musculature in individuals with and without patellofemoral pain. Journal of Athletic Training 2009;44:7.
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Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
The effects of muscle fatigue on dynamic standing balance in people with and without patellofemoral pain syndrome Hossein Negahban a, Malihe Etemadi a,*, Saeed Naghibi b, Anita Emrani c, Mohammad Jafar Shaterzadeh Yazdi a, Reza Salehi a, Aida Moradi Bousari b a b c
Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran Sport Science Research Center (SSRC), Tehran, Iran Department of Physical Therapy, School of Rehabilitation Sciences, Tehran University of Medical Sciences, Tehran, Iran
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 February 2012 Received in revised form 23 July 2012 Accepted 27 July 2012
The aim was to examine the effects of muscle fatigue of knee extensor and hip abductor muscles on dynamic standing balance of patients with patellofemoral pain syndrome (PFPS) compared to their healthy matched controls. Thirty participants (15 with PFPS, 15 controls) were recruited. Isolated muscle fatigue of two muscles was induced isokinetically in three separate sessions (one practice and two testing sessions) with a rest interval of at least 72 h. In each testing session, fatigue protocol of only one muscle group was performed for the both legs with a rest time of 30 min. After determining peak torque, participants were encouraged to perform continuous maximal concentric–eccentric contraction of the target muscle until the torque output dropped below 50% of peak value for 3 consecutive repetitions. Immediately after the completion of the fatigue protocol, balance testing of participants was undertaken during single leg standing using the Biodex stability system. Balance stability measures included the overall, anteroposterior and mediolateral stability indices (OSI, APSI and MLSI, respectively). Patients exhibited decreased balance stability in the sagittal plane (higher APSI) when compared to controls. Isolated muscle fatigue of the knee extensors and hip abductors reduced balance stability in both study groups. Fatigue of hip abductors was associated with greater balance instability (higher OSI and APSI) than fatigue of knee extensors. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Fatigue Standing balance Patellofemoral pain
1. Introduction Patellofemoral pain syndrome (PFPS) is a common musculoskeletal disorder [1,2] which occurs more frequently in athletes and in women compared to non-athletes and men, respectively [3–5]. Nearly 21% of knee complaints [6] and 10–25% of all patients referred to the physiotherapy clinics [7] are diagnosed with PFPS. Standing balance control is a key component of most daily and sports activities [8]. Balance can be evaluated in both static (force platform) and dynamic (moveable balance platform) conditions and during both double and single leg standing [8,9]. While several studies have extensively examined standing balance control of patients with different knee disorders such as anterior cruciate ligament injury [10–12], little is known on balance ability of patients with PFPS.
* Corresponding author. Tel.: +98 611 374 3101; fax: +98 611 374 3506. E-mail addresses: [email protected] (H. Negahban), [email protected] (M. Etemadi), [email protected] (S. Naghibi), [email protected] (A. Emrani), [email protected] (M.J. Shaterzadeh Yazdi), [email protected] (R. Salehi), [email protected] (A. Moradi Bousari). 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.07.025
Muscle fatigue, which is defined as the decline in force output capacity after repeated muscle contractions [8,13–15], is a common occurrence in most activities of daily living and sporting competitions [14,16,17]. Specifically, most sports injuries occur during the late stage of competitions in which muscles become fatigued [8]. It has been assumed that muscle fatigue is one of the main causes of impaired balance [13,15]. The post-fatigue impairment in balance control is often attributed to deficit in neuromuscular control resulting from altered somatosensory inputs [8,9,13]. Recently, the evaluation of balance control in the presence of isolated muscle fatigue has become a popular research focus [16]. The adverse effects of lower extremity muscle fatigue on balance performance have been reported in the young [8,15,17–19] and elderly [13] healthy populations and also in some pathological conditions such as chronic ankle instability (CAI) [9,16]. This study aimed to examine the effects of muscle fatigue of the knee extensor and hip abductor muscles on dynamic standing balance of patients with PFPS compared to healthy matched controls. From a clinical viewpoint, understanding the effects of muscle fatigue on balance performance may provide important insight into the role of muscle weakness in the development of PFPS. Also, it may help to assess
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the potential contribution of muscle strengthening exercises in the prevention and rehabilitation of patients with PFPS. Increased fatigability followed by muscle weakness is one of the primary symptoms of patients with different musculoskeletal disorders [19]. Knee extensor (quadriceps) weakness has been considered as a major contributing factor in the development of PFPS [4,5]. Strengthening exercise of this muscle is an important aspect in the management of this condition [20]. Furthermore, several studies have associated the reduction in cross-section area of the hip abductor (gluteus medius) with PFPS [1,4,5]. Improvement of pain and dysfunction in these patients has been attributed to strengthening exercises of this muscle [1]. Theoretically, gluteus medius weakness during single leg standing could result in dropping of the pelvis on the contra-lateral side, increased hip adduction/internal rotation, increased lateral patellar contact pressure, and thereby it may contribute to the development of PFPS [1,3–5]. It was hypothesized that PFPS patients would exhibit poor balance stability during single leg standing on a dynamic moveable platform, compared to controls. Furthermore, dynamic standing balance of patients would be more affected by fatigue of the knee extensor and hip abductor muscles, compared to healthy controls. 2. Materials and methods 2.1. Subjects Thirty participants (15 with PFPS, 15 controls) between the ages of 19 and 35 years were recruited. All participants provided a written informed consent prior to participation in this investigation. PFPS patients were recruited from orthopedic and physiotherapy clinics in Tehran, Iran. Inclusion criteria were: (1) non-traumatic anterior or retropatellar pain for more than 6 months [20]; (2) pain on palpation of the patellar facets [1] or facet compression; and (3) pain on at least two of the following activities: prolonged sitting with bent knees, squatting, kneeling, running, hopping/jumping, and ascending or descending stairs [1,2]. Patients were excluded if they had: (1) diagnosis of knee osteoarthritis, patellar tendonitis, or patellar dislocation/ subluxation [21]; (2) clinical evidence of knee ligament, meniscus, or tendon injuries [1,21]; (3) involvement of other joints affecting the lower extremities or the back in the past year; (4) history of any neurological deficit [21]; and (5) previous history of surgery including arthroscopy [21]. None of the patients was undergoing physical therapy in the 30 days preceding the study. All participants were asked to refrain from any strenuous exercise for 2 days before testing to prevent muscle fatigue [2]. In order to evaluate pain and disability, all patients completed a 10-cm visual analogue scale (VAS) [20] and the Kujala patellofemoral scale (KPS) [22]. Additionally, in order to match the activity level of patients and healthy subjects, the Tegner activity rating scale [23] was completed by both study groups. The scoring range of the VAS was 0–10, where 0 indicated no pain and 10 the worst pain [20]. The KPS is a 13-item, self completed instrument with different categories consisting of limping, weight bearing, walking, stairs, squatting, running, jumping, prolonged sitting, pain, swelling, painful patellar movements, muscle atrophy, and flexion deficiency [22]. The total score ranges from 0 to 100, with higher scores indicating lower levels of disability [22]. The Tegner activity scale is a one-item instrument that assesses activity levels for sports and occupational activities. It has 11 items with a scoring range of 0–10. Higher scores represent higher levels of
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physical activity [23]. Iranian-versions of the KPS [22] and the Tegner scale [23] have been validated for use in Iran. The selection of the control group was based on the same exclusion criteria as for the patient group. Healthy subjects were matched with patients according to gender (12 female, 3 male), age, height, body mass index, and activity level (Table 1). 2.2. Fatigue protocol This study was approved by the local Institutional Review Board. The fatigue protocol used in this investigation followed previously published protocols for studying balance control in the presence of fatigue of lower limb muscles [9,13,17–19]. Isolated muscle fatigue of knee extensor and hip abductor muscles was induced using a Biodex System yV isokinetic dynamometer (Biodex Inc., Shirley, NY, USA). Three separate sessions (one practice and two testing sessions) with a rest interval of at least 72 h were assigned to each subject in order to minimize possible learning and fatigue effects [8,19]. The practice session was used to allow familiarization with the equipment and procedure. During each testing session, only one muscle group was tested in both legs with a resting time of 30 min. The order of muscle group and side tested were randomly assigned for each participant. The involved leg of each patient was matched with the corresponding leg of a healthy control according to their dominant side. The leg used to kick a ball was defined as dominant [4,8]. At first, 3 practice trials of sub-maximal and 3 of maximal contractions were performed. After a 60 s rest and in order to determine peak torque, 3 repetitions of maximal concentric–eccentric contraction with no rest were performed at the speed of 608/s [9,18]. The highest torque achieved during the 3 repetitions was considered as peak torque. After 2–3 min, participants were instructed to perform continuous maximal concentric–eccentric contractions of the target muscle at 608/s until the torque output dropped below 50% of peak torque for 3 consecutive contractions. This definition of fatigued state has been used in previous studies on fatigue-balance [9,13,17–19]. Participants were given verbal encouragement throughout the isokinetic fatigue protocol [17,18]. Patient positioning in the isokinetic dynamometer was based on the guidelines provided by the manufacturer. Concentric–eccentric contraction of the quadriceps was performed through a range of motion from 908 to 308 knee flexion in the sitting position. As maximal knee extension in the open kinetic chain can increase the patellofemoral joint reaction force [20] and in order to reduce the patellofemoral stress to a minimum during the fatigue protocol, the last 308 of knee extension were excluded by the equipment. For the gluteus medius, participants were positioned side-lying in front of the isokinetic dynamometer [4] and concentric–eccentric contraction was performed within the available range of hip abduction. 2.3. Balance testing According to previous studies, fatigue recovery (i.e. return to above 80% of peak torque after fatigue) occurs within 2–4 min after the completion of the fatigue protocol [17]. Therefore, all balance testing of this investigation was completed immediately after fatigue [4,17]. The Biodex stability system (BSS) SD (Biodex Medical System Inc., Shirley. NY, USA) is used for the quantitative assessment of dynamic standing balance [17]. It consists of a circular moveable platform that provides up to 208 tilt in a range of 3608 [15]. The BSS measures stability ranging from 1 to 12 with higher scores corresponding to increased platform stability. All balance testing in this study was conducted on the moderate level of 4. Balance stability measures extracted from the BSS include the overall, anteroposterior and mediolateral stability indices (OSI, APSI and MLSI, respectively). These stability indices represent the mean angular displacement of the platform in degrees from a level, zero-point position [24–26]. Higher and lower stability indices correspond to greater and lesser movement of the
Table 1 Demographic and functional characteristics of PFPS and healthy groups. PFPS group (n = 15)
Healthy group (n = 15)
P value
Mean (SD)
Mean (SD)
(Mean differences)
Demographic data Age (year) Height (m) Body mass index (kg/m2) Duration of symptoms (month)
25.8 (4.41) 1.64 (10.8) 22.7 (3.78) 29.2 (20.7)
25.2 (5.17) 1.64 (10.4) 22.9 (3.87) N/A
0.73 0.97 0.88
Tegner activity score a Kujala patellofemoral scale b Visual analogue scale c (pain)
6.46 (1.35) 78.0 (7.74) 5.66 (1.11)
6.73 (1.16) N/A N/A
0.56
PFPS: patellofemoral pain syndrome; SD: standard deviation; N/A: not applicable. a Range of scores is from 0 to 10. b Range of scores is from 0 to 100. c Range of scores is from 0 to 10.
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platform away from the central reference point, respectively [24,26]. Therefore, higher score indicates a greater difficulty maintaining the platform in a stable position, hence poor balance stability. Conversely, lower scores represent better stability and, therefore, better balance [8,15,25–27]. The reliability of these stability measures has been reported in several studies, with intra-class correlation coefficients of 0.60–0.99 during single leg standing on the platform [8,17,27]. Participants were asked to place one leg on the central region of the platform while the other leg was in a position of slight hip flexion/abduction and 908 of knee flexion [17]. The foot coordinates were recorded for the first time and were maintained throughout the testing trials of each participant [8,15]. Participants were asked to look straight ahead and place their arms crossed over the chest [15,17] and to keep the platform as motionless as possible for 20 s. Balance testing consisted of 3 trials before the fatigue protocol and 2 trials immediately after fatigue with a rest interval of 20 s between trials [8]. The first trial before fatigue was a practice one. The average of the pre- and post-fatigue balance testing was used for further analysis. 2.4. Statistical analysis A separate 2 2 2 2 (2 groups; 2 muscles; 2 times; 2 legs) mixed model of analysis of variance (ANOVA) test was used to determine main effects and interactions of these factors for each of the balance stability measures (OSI, APSI, MLSI) [28]. An alpha level of 0.05 was used for all statistical analyses.
3. Results The mean (SD; standard deviation) pain level of patients was 5.66 (1.11) for most painful functional activities during the previous 2 weeks. The mean (SD) disability level of patients was 78 (7.74). Table 2 shows the mean and SD for pre-fatigue and post-fatigue measurements of all balance stability measures. The results of ANOVA showed that the only significant interaction was seen for the interaction of group by leg in the sagittal plane (F1, 28 = 10.9, P < 0.01 for APSI). Further analysis by independent t-test showed that there were between-group differences for APSI only when the patients were standing on the involved leg and were compared with the corresponding leg of the healthy group (P < 0.01). When comparison was made between the uninvolved leg of patients and corresponding leg of healthy group, no significant differences were seen (P > 0.05). The main effect of time (pre-fatigue vs. post-fatigue measurement) was significant, indicating that fatigue had a significant effect on all stability measures (F1, 28 = 13.0, P < 0.01 for OSI;
F1, 28 = 7.15, P = 0.01 for APSI; F1, 28 = 5.55, P = 0.02 for MLSI). The main effect of muscle (hip abductor vs. knee extensor) was significant for OSI (F1, 28 = 8.49, P < 0.01) and APSI (F1, 28 = 7.48, P = 0.01), indicating that fatigue of the hip abductors led to greater changes in stability indices compared to fatigue of the knee extensors.
4. Discussion To our knowledge, this investigation was the first to examine dynamic standing balance in patients with PFPS. The results showed that, irrespective of fatigue effects and during standing on the involved leg, patients exhibited decreased balance stability in the sagittal plane (higher APSI) when compared to healthy controls. A deficit in knee proprioception followed by patellofemoral pain [29] could be proposed as a major contributing factor contributing to poor balance stability in this patient population. Additionally, direction-specific balance instability in the patients could be attributed to the fact that PFPS is a musculoskeletal disorder that affects stability mainly in the sagittal plane. Isolated muscle fatigue of the knee extensor and hip abductor muscles reduced balance stability in both study groups. These findings are consistent with previous investigations that examined the effects of lower limb muscle fatigue induced by either isokinetic [17–19] or functional [8] methods on balance control of healthy young subjects using a static [18] or a dynamic moveable platform [9,17]. Fatigue of the hip abductors was associated with greater balance instability (higher OSI and APSI) than fatigue of the knee extensors. Previous studies on the relative contributions of the proximal (hip) and distal (ankle) muscles in maintaining single leg stance in a fatigued state showed that fatigue in the proximal muscles caused greater impairment in balance stability than fatigue induced to distal muscles [8,9,17]. This could be attributed to the assumption that proximal muscles of the lower extremity have a crucial role in maintaining balance under more challenging dynamic conditions [9,17]. Contrary to these findings, Reimer and Wikstrom [8] found that functional fatigue of the ankle and hip muscles caused similar impairments in single leg stance as measured by balance stability indices obtained from the BSS. This inconsistency could be explained by the fact
Table 2 Mean (standard deviation) of the overall, AP and ML stability indexes for two levels of pre- and post-fatigue in two groups of PFPS and healthy participants. Fatigue levels
Pre-fatigue PFPS
Fatigue protocol on knee extensors Standing on the involved leg (and its matched leg in the control group) Overall stability index 4.32 (1.80) AP stability index* 2.77 (1.58) ML stability index 2.80 (1.30) Standing on the uninvolved leg (and its matched leg in the control group) Overall stability index 3.72 (1.19) AP stability index 2.19 (0.80) ML stability index 2.60 (1.22) Fatigue protocol on hip abductors Standing on the involved leg (and its matched leg in the control group) Overall stability index 4.75 (1.77) AP stability index* 2.89 (1.40) ML stability index 3.34 (1.29) Standing on the uninvolved leg (and its matched leg in the control group) Overall stability index 4.28 (1.68) AP stability index 2.75 (1.37) ML stability index 2.84 (1.15)
Post-fatigue Healthy
PFPS
Healthy
3.56 (1.46) 2.06 (1.00) 2.40 (1.45)
5.20 (3.16) 3.26 (2.01) 3.57 (2.60)
3.71 (1.87) 1.94 (1.05) 2.69 (1.81)
4.09 (0.86) 2.48 (1.07) 2.70 (1.22)
4.12 (1.52) 2.45 (1.08) 2.78 (1.63)
3.95 (1.44) 2.48 (1.08) 2.58 (1.50)
3.70 (1.27) 2.17 (0.78) 2.50 (1.50)
5.43 (1.77) 3.13 (1.01) 3.81 (2.14)
4.19 (1.51) 2.50 (0.76) 2.84 (1.78)
3.85 (1.04) 2.48 (0.84) 2.52 (1.17)
5.00 (1.99) 3.20 (1.80) 3.06 (1.63)
4.78 (1.38) 3.41 (1.01) 2.82 (1.67)
AP: anteroposterior; ML: mediolateral; PFPS: patellofemoral pain syndrome. * Indicates significance: irrespective of fatigue effects and during standing on the involved leg, patients exhibited decreased balance stability in the sagittal plane (higher APSI) when compared to their healthy controls.
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that, in contrast to isokinetic fatigue induced by an open kinetic chain, functional fatigue induced by closed kinetic chain exercises incorporates activation of all muscle groups (and not isolated muscles) [8]. Therefore, it is not possible to compare the relative contribution of isolated muscle fatigue on balance performance. Similar effects of muscle fatigue on dynamic standing balance between the two study groups were found in this study. This is in contrast to the study of Gribble et al. [9] in which isokinetic fatigue of the hip, knee, and ankle resulted in a smaller reach distance value in the CAI patients than their healthy matched controls. These authors used the star excursion balance test (SEBT) as a measure of functional balance in their study. Similarly, Hosseinimehr et al. [16] found that sports-related fatigue of the lower extremity resulted in a significant decrease in the reach distance of patients with CAI relative to healthy controls as measured by SEBT. The inconsistent results of these studies compared to ours may partially relate to the different patient populations (CAI vs. PFPS) and the different measures of balance (SEBT vs. BSS) used in these studies. Therefore, it seems that the SEBT is a more sensitive measure to detect different effects of muscle fatigue on balance performance of two study groups and we recommend its uses in future studies. In addition, as the disability level of our patients, as measured by the KPS, was low it is probable that patients with severe disability level exhibit different fatigue effects when compared to healthy controls. Thus, we recommend selection of patients with a higher level of disability for future investigations. Our study had some limitations. Firstly, the isolated fatigue induced by isokinetic methods is not representative of muscle fatigue occurring during functional activities or sports. Therefore, the results may not be generalized to functional activities. However, previous studies showed that both isokinetic and functional fatigue protocols caused similar impairments in standing balance performance [8]. The second limitation is that due to the relatively small number of subjects, the results should be considered as preliminary. In conclusion, patients with PFPS exhibited decreased balance stability in the sagittal plane when compared to controls. Therefore, balance training should be incorporated in the rehabilitation of these patients. Moreover, muscle fatigue had an adverse effect on balance performance but these effects were not different between the two study groups. Source of support This work was part of M.Sc thesis of Mrs. Etemadi and was supported by a Master thesis grant (no: pht-8901) in Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran. Acknowledgement We thank Dr. Mazaheri and Dr. Latifi for their assistance with study design and statistical advice, respectively. Conflict of interest None of the authors have any financial or other interests relating to the manuscript to be submitted for publication in Gait & Posture. References [1] Boling MC, Padua DA, Creighton RA. Concentric and eccentric torque of the hip musculature in individuals with and without patellofemoral pain. Journal of Athletic Training 2009;44:7.
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