Arch Orthop Trauma Surg DOI 10.1007/s00402-016-2428-6
ARTHROSCOPY AND SPORTS MEDICINE
Gluteus maximus impairment in femoroacetabular impingement: a tensiomyographic evaluation of a clinical fact ´ lvarez-Dı´az1,2,4, • Roberto Seijas1,2 • Eduard Alentorn-Geli3 • Pedro A 5 • 1,2 • 6 • Miguel Marı´n Oscar Ares Andrea Sallent Xavier Cusco´1 • Ramo´n Cugat1,2,4
Received: 6 January 2016 Ó Springer-Verlag Berlin Heidelberg 2016
Abstract Introduction the aim of the present study is to evaluate the mechanical and contractile properties of the gluteus maximus (GM) muscle in patients with femoroacetabular impingement (FAI). Our hypothesis is that the clinical observation of GM pain would be evidenced by tensiomyographic impairment in muscle function. Materials and methods A prospective, cross-sectional, intra-group comparative study was conducted to assess the neuromuscular changes of lower extremity muscles in patients with FAI. Fifty-one patients with clinical and radiographic diagnosis of FAI for at least 3 months were included. The rectus femoris (RF), adductor magnus (AM), and GM of both lower extremities of all patients were evaluated with tensiomyography (TMG). The values of TMG of the affected lower extremity were compared to those of the healthy contralateral side. The parameters obtained in this study were maximal displacement (Dm), and contraction time (Tc).
& Roberto Seijas [email protected] 1
Fundacio´n Garcı´a-Cugat. Artroscopia GC, Hospital Quiro´n, Barcelona, Spain
2
Universitat Internacional de Catalunya, Barcelona, Spain
3
Department of Orthopaedic Surgery, Duke Sports Sciences Institute, Duke University, Durham, NC, USA
4
Mutualidad de Futbolistas, Federacio´n Espan˜ola de Futbol, Delegacio´n Catalun˜a, Barcelona, Spain
5
Department of Physical Medicine and Rehabilitation, Hospital Quiro´n, Barcelona, Spain
6
Department of Orthopaedic Surgery, Hospital Vall d’Hebron, Barcelona, Spain
Results The Tc of the injured GM was significantly higher compared to the healthy side (p = 0.01). There were no significant side-to-side differences in the Dm of the GM (p = 0.13), either in the Tc and Dm of the RF (p = 0.15 and p = 0.8, respectively) and AM (p = 0.25 and p = 0.75, respectively). Conclusions FAI is associated with impairment of contraction time in the GM of the injured compared to the healthy side. Impairment of the GM may be monitored to evaluate response to conservative or surgical treatment. Keywords Femoroacetabular impingement Gluteus maximus Tensiomyography Rectus femoris Adductor magnus
Introduction The diagnosis of femoroacetabular impingement (FAI) has increased in recent years [1, 2]. A better understanding of the etiopathogenesis of hip disorders along with improved diagnostic techniques have contributed to an increase in the identification of this hip disorder, especially in young adults [1, 2]. Common signs and symptoms of FAI include activity-related groin or hip pain exacerbated with hip flexion, mechanical hip symptoms, sitting difficulties, and limited hip flexion especially with internal rotation, among others [3]. It has also been observed that muscular impairment is a common finding in patients with hip osteoarthritis undergoing joint replacement, mainly expressed with weakness in flexors, extensors, abductors, and rotator muscles [4–7]. Painful trigger points in several muscle groups have been reported in relation to FAI, the gluteus maximus being a common region [2, 8, 9]. Thus, investigating the status of the gluteus maximus is
123
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warranted to evaluate this clinical observation. However, research to evaluate gluteus maximus impairment is scarce. Tensiomyography (TMG) is a non-invasive method used to evaluate skeletal muscle mechanical and contractile properties in response to electrical stimuli [10]. This method provides information of muscle stiffness, muscle contraction velocity, type of predominant skeletal muscle fibers, or muscle fatigue [10, 11]. This method has shown good-toexcellent inter-observer, intra-session, and between-day reliability for other muscle groups of the lower extremity [11–14]. The evaluation of gluteus maximus muscular impairment in patients with FAI, including the tensiomyographic characteristics, has not been reported to date. The purpose of this study was to evaluate the gluteus maximus mechanical and contractile properties in patients with FAI with gluteus maximus dysfunction. It was hypothesized that the clinical observation of gluteus maximus pain would be evidenced by tensiomyographic impairment in muscle function.
Materials and methods A cross-sectional, intra-group comparative study was conducted to assess the neuromuscular changes of lower extremity muscles in patients with FAI. All consecutive patients with clinical and radiographic diagnosis of FAI, Camtype, for a period of at least 3 months were included in the present study. All patients had positive C-sign and pain and/or weakness of the GM, and were diagnosed and followed by the same orthopedic surgeon specialist in joint-preserving hip disorders. Exclusion criteria included history of lumbar spine, pelvis, or hip surgery, neurological diseases, unrelated gait abnormalities, history of sciatica and other nerve root compression disorders of the proximal lower extremity. Before undergoing surgical treatment of FAI, the rectus femoris (RF), adductor magnus (AM), and gluteus maximus (GM) of both lower extremities of all patients were evaluated using TMG. The values of TMG for the muscles of the affected lower extremity were compared to those of the healthy contralateral side. An additional comparison was conducted depending on gender for each of the TMG parameters. The methodology for the TMG assessment was identical in all patients. This method uses a portable device that produces an electrical stimulus applied percutaneously that creates a muscular contraction detected by a digital transducer applied above the muscle belly [15]. TMG has demonstrated good-to-excellent inter-observer, intra-session, and between-day reliability for vastus medialis, vastus lateralis, RF, and biceps femoris [11–14]. The parameters obtained in this study were the maximal displacement (Dm) expressed in mm, and the contraction time (Tc) expressed in
123
ms. The Dm is the radial movement of the muscle belly after the application of the electrical stimulus. The Tc is the time between 10 and 90 % of Dm. Both parameters were obtained for the RF, AM, and GM of the healthy and affected lower extremity under the same conditions. The same researcher with experience in TMG collected all data. The measurement protocol has been previously described in detail [16–20], and was based on Rey et al. [11]. All measurements were obtained at rest in the supine position for the RF and AM, and in the prone position for the GM. For the supine position, a foam cushion was employed to keep the knee joint with a fixed angle of 608 of knee flexion [11], and the hip joint was kept at 308 flexion. To evaluate the GM in the prone position, a foam cushion was also employed to keep a hip flexion of approximately 308. The radial muscle displacement was measured perpendicular to the muscle belly with a digital transducer Dc–Dc Trans-TekÒ (GK 40, Panoptik d.o.o., Ljubliana, Slovenia). The TMG measurements were obtained in all patients under the following conditions [11]: (1) resting, with no previous strenuous exercise in 48 h; (2) no intake of energy drinks or supplements in the previous 48 h; (3) no alcohol or caffeine at least 3 h before measurements; and (4) no foot intake at least 2 h before measurements. The self-adhesive electrodes (Compex Medical SA, Ecublens, Switzerland) were placed equidistant to the measuring point, proximal (anode) and distal (cathode) to the sensor. Electrical stimulation was applied through a TMG-100 System electrostimulator (TMG-BMC d.o.o., Ljubljana, Slovenia) with a pulse of 1 ms and an initial amplitude of 50 mA. For each test, amplitude was progressively increased by 10 mA increments until there was no further increase in Dm or maximal stimulator output (110 mA). All muscles were tested twice; firstly to assure appropriate functioning of the TMG, and a second time was taken as the definitive value. All patients gave consent to participate in this study, which received Institutional Review Board approval. Statistical analysis Descriptive statistics were used to summarize all demographic characteristics as well as outcomes. A Shapiro– Wilk test was first conducted to assess for normal distribution of all the evaluated parameters. For variables with normal distribution, an unpaired Student’s t test was employed to compare the TMG values between both sides. This test was also used to compare side-to-side differences for each TMG parameter between males and females. For variables not following a normal distribution, a Mann– Whitney test was used for the comparison of TMG values between sides. A separate sample size calculation was conducted for the Tc and Dm parameters, and involved all muscle groups of a preliminary sample of 20 patients. The
Arch Orthop Trauma Surg
minimum sample size that was considered for the whole study was obtained from the comparison that elicited the highest value of sample size. The Tc corresponded to the result of calculating the highest number of patients needed for the study to compare the TMG values between both lower extremities. Considering a power of 80 % to detect statistically significant differences in the hypothesis testing through a two-tailed unpaired t test with an alpha level of 0.05, and assuming a difference in mean Tc values between the injured and healthy lower extremity of 2.3 ms, and a standard deviation of the healthy side of 5.6 ms, 47 patients were needed. All statistical analyses were conducted using the SPSS v.21 (SPSS, Inc. Chicago, IL, USA). The alpha level was set up at 0.05.
Results Fifty-one patients were finally included in the present study. Mean age (SD) was 44.7 (12.4) years old. The left lower extremity was the affected side in 27 patients, and the right lower extremity in 24 patients. There were 24 women and 27 men. The comparison of TMG parameters between the injured and healthy sides for all muscle groups is shown in Table 1. The Tc for the GM was significantly higher in the injured compared to the healthy side (p = 0.01). There were no significant side-to-side differences for Tc and Dm in the RF (p = 0.88 and p = 0.5, respectively), for Tc and Dm in the AM (p = 0.9 and p = 0.45, respectively), and for Tc and Dm in the GM (p = 0.72 and p = 0.22, respectively) between males and females.
Discussion The main finding of the present research was that the GM showed poorer mechanical and contractile properties in the injured side of patients affected of FAI compared to the healthy side. In contrast, the RF and AM demonstrated similar TMG characteristics between both sides in the same cohort of patients.
Table 1 Comparison of the tensiomiography parameters between the injured and healthy sides for all muscle groups
Parameter/side
The GM is one of the biggest muscles in the human body, with broad origin and insertion including the ilium, the sacrotuberous ligaments, the sacrum and the coccyx [21]. Eighty percent of the insertion is found in the iliotibial band and gluteal tuberosity. This muscle is a powerful hip extensor and significantly contributes to hip external rotation [22]. It has a major role in physical activities involving sprinting, squatting and climbing a steep hill [23]. The relationship between impairment in the contractility or function of the GM and different hip or lumbar disorders has already been described [21, 24]. FAI produces pain in the lateral and posterior aspect of the hip joint and in the lumbosacral area [2, 8, 9]. While worsening of GM function in neurologic injuries has been well demonstrated [25], the status of the GM in patients with FAI has not been yet described. Therefore, the quantification or measurement of this clinical observation (pain in the GM area) seems timely. Values of Tc above 30 ms have been related to a predominance of slow-twitch (type I muscle fibers) muscle type [26]. According to the present results, the RF and AM would predominantly be fast and powerful muscles whereas the GM would be slow and endurance muscles. This is in accordance to autopsy data where it was demonstrated that RF and GM had a predominance of fasttwitch (type II) and slow-twitch (type I) muscles fibers, respectively [27]. However, the AM has been reported to predominantly be a slow-contraction muscles with 53.5 % of type I muscle fibers [27], whereas in the present study the mean Tc was 25 ms. In the side-to-side comparison, the decrease in Tc of the GM of the injured compared to the healthy side may indicate that the disorder causes a decreased contraction speed of the muscle [11, 15]. Therefore, the GM of the injured side would decrease its ability to rapidly generate strength during contraction [11]. The differences in Tc between the injured and healthy GM could be explained by the injury, as it clinically correlates with a painful area in FAI. In addition, no differences between both lower extremities for Tc and Dm of vastus medialis, vastus lateralis, RF, biceps femoris, gastrocnemius medialis and gastrocnemius lateralis in healthy individuals have been identified [19]. However, differences of
Rectus femoris
Adductor magnus
Gluteus maximus Mean (SD)
Mean (SD)
p value
Mean (SD)
p value
Tc injured
28.7 (4.6)
0.15
26.6 (8.5)
0.25
Tc healthy
27.6 (3.2)
Dm injured Dm healthy
8.8 (2.7) 8.6 (3)
24.8 (6.5) 0.8
4.3 (2.3) 4.6 (2.6)
37 (9.5)
p value 0.01
32.9 (7.2) 0.75
6 (3.4) 5 (3)
0.13
Dm maximal displacement, Tc contraction time
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both lower extremities for the AM and GM were not assessed in the study by Alvarez-Diaz et al. [19]. The absence of pre-injury TMG values does not allow to strongly concluding that the observed side-to-side differences are explained by the injury. FAI produces gait changes due to pain and limited hip motion that would likely explain the observed impairment of the GM. Further investigations with pre-injury data are needed to better elucidate the effects of FAI in GM and other muscle groups. Furthermore, some authors have defended the role of conservative treatment of FAI over surgical treatment [28–31]. Therefore, a therapeutic pre and post-study evaluating the effects of conservative or surgical treatment on TMG modifications of GM should be performed. The Dm represents muscle stiffness. Some authors have related Dm to contraction velocity (Tc) and muscle fatigue (relaxation time, or Tr) [32, 33]. Kokkonen et al. suggested that lower muscle stiffness (higher Dm values) in the musculotendinous unit would induce a decrease of strength and muscle power, thus reducing contraction velocity (increase in Tc) [32]. These conclusions cannot be applied to the present study, as the Dm was not significantly different in any of our comparisons. The relationship between muscle fatigue (Tr) and Dm cannot be either established in the present study as Tr was not evaluated. To our knowledge, there are no similar studies evaluating GM TMG changes in patients with FAI or other hip disorders. Alvarez-Diaz et al. reported on TMG changes of the vastus medialis, vastus lateralis, RF, biceps femoris, gastrocnemius medialis and gastrocnemius lateralis after anterior cruciate ligament injury and subsequent reconstruction in soccer players [18, 20]. Anterior cruciate injury caused a decrease in contraction velocity, resistance to fatigue and muscle tone/stiffness of the quadriceps, hamstrings and gastrocnemius medialis [18], which was corrected with ligament reconstruction and subsequent physical therapy [20]. These data cannot be extrapolated to FAI as they deal with a different disorder. Several limitations should be considered when reviewing the present study. First, the absence of pre-injury data prevents us from elaborating strong conclusions on the effects of FAI in the observed GM impairment. However, there is not definitive reason to assume that side-to-side differences for this muscle group would be observed in healthy conditions. In addition, GM impairment seems to clinically correlate with pain or weakness in this muscle area. Second, this study provides no data on the length of symptoms or current physical activity level, both of which may influence TMG values. Third, no correlation was conducted between the present findings and the pain or range of motion. Further studies are needed to evaluate the correlation of TMG values of the GM and the presence/
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absence and location of hip pain, especially in the posterior aspect of the joint.
Conclusions FAI is associated with impairment of contraction time (Tc) in the GM of the injured compared to the healthy side. Impairment of the GM may be monitored to assess response to either conservative or surgical treatment of FAI. Compliance with ethical standards Conflict of interests The authors declare no conflict of interests or financial aid for the present investigation.
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Arch Orthop Trauma Surg 14. Simunic B (2012) Between-day reliability of a method for noninvasive estimation of muscle composition. J Electromyogr Kinesiol 22:527–530 15. Valencic V, Knez N (1997) Measuring of skeletal muscle’s dynamic properties. Artif Organs 21:240–242 16. Alentorn-Geli E, Alvarez-Diaz P, Ramon S et al (2015) Assessment of neuromuscular risk factors for anterior cruciate ligament injury through tensiomyography in male soccer players. Knee Surg Sports Traumatol Arthrosc 23(9):2508–2513 17. Alentorn-Geli E, Alvarez-Diaz P, Ramon S (2015) Assessment of gastrocnemius tensiomyographic neuromuscular characteristics as risk factors for anterior cruciate ligament injury in male soccer players. Knee Surg Sports Traumatol Arthrosc 23(9):2502–2507 18. Alvarez-Diaz P, Alentorn-Geli E, Ramon S et al (2014) Effects of anterior cruciate ligament injury on neuromuscular tensiomyographic characteristics of the lower extremity in competitive male soccer players. Knee Surg Sports Traumatol Arthrosc [Epub ahead of print] 19. Alvarez-Diaz P, Alentorn-Geli E, Ramon S et al (2014) Comparison of tensiomyographic neuromuscular characteristics between muscles of the dominant and non-dominant lower extremity in male soccer players. Knee Surg Sports Traumatol Arthrosc [Epub ahead of print] 20. Alvarez-Diaz P, Alentorn-Geli E, Ramon S et al (2015) Effects of anterior cruciate ligament reconstruction on neuromuscular tensiomyographic characteristics of the lower extremity in competitive male soccer players. Knee Surg Sports Traumatol Arthrosc 23(11):3407–3413 21. Reiman MP, Bolgla LA, Loudon JK (2012) A literature review of studies evaluating gluteus maximus and gluteus medius activation during rehabilitation exercises. Physiother Theory Pract 28:257–268 22. Delp SL, Hess WE, Hungerford DS, Jones LC (1999) Variation of rotation moment arms with hip flexion. J Biomech 32:493–501 23. Neumann DA (2010) Kinesiology of the hip: a focus on muscular actions. J Orthop Sports Phys Ther 40:82–94
24. Oh JS (2014) Effects of Pelvic Belt on Hip Extensor Muscle EMG Activity during Prone Hip Extension in Females with Chronic Low Back Pain. J Phys Ther Sci 26:1023–1024 25. Maguire C, Sieben JM, Erzer F et al (2012) How to improve walking, balance and social participation following stroke: a comparison of the long term effects of two walking aids—canes and an orthosis TheraTogs—on the recovery of gait following acute stroke. A study protocol for a multicentre, single blind, randomised control trial. BMC Neurol 12:18 26. Dahmane R, Valencic V, Knez N, Erzen I (2001) Evaluation of the ability to make non-invasive estimation of muscle contractile properties on the basis of the muscle belly response. Med Biol Eng Comput 39:51–55 27. Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18:111–129 28. Dooley PJ (2008) Femoroacetabular impingement syndrome: nonarthritic hip pain in young adults. Can Fam Physician 54:42–47 29. Emara K, Samir W, el Motasem H, Ghafar KA (2011) Conservative treatment for mild femoroacetabular impingement. J Orthop Surg (Hong Kong) 19:41–45 30. Palmer AJ, Ayyar-Gupta V, Dutton SJ (2014) Protocol for the Femoroacetabular Impingement Trial (FAIT): a multi-centre randomised controlled trial comparing surgical and non-surgical management of femoroacetabular impingement. Bone Joint Res 3:321–327 31. Palmer AJ, Thomas GE, Pollard TC et al (2013) The feasibility of performing a randomised controlled trial for femoroacetabular impingement surgery. Bone Joint Res 2:33–40 32. Kokkonen J, Nelson A, Cornwell A (1998) Acute muscle stretching inhibits maximal strength performance. Res Q Exerc Sport 69:411–415 33. Krizaj D, Simunic B, Zagar T (2008) Short-term repeatability of parameters extracted from radial displacement of muscle belly. J Electromyogr Kinesiol 18:645–651
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ARTHROSCOPY AND SPORTS MEDICINE
Gluteus maximus impairment in femoroacetabular impingement: a tensiomyographic evaluation of a clinical fact ´ lvarez-Dı´az1,2,4, • Roberto Seijas1,2 • Eduard Alentorn-Geli3 • Pedro A 5 • 1,2 • 6 • Miguel Marı´n Oscar Ares Andrea Sallent Xavier Cusco´1 • Ramo´n Cugat1,2,4
Received: 6 January 2016 Ó Springer-Verlag Berlin Heidelberg 2016
Abstract Introduction the aim of the present study is to evaluate the mechanical and contractile properties of the gluteus maximus (GM) muscle in patients with femoroacetabular impingement (FAI). Our hypothesis is that the clinical observation of GM pain would be evidenced by tensiomyographic impairment in muscle function. Materials and methods A prospective, cross-sectional, intra-group comparative study was conducted to assess the neuromuscular changes of lower extremity muscles in patients with FAI. Fifty-one patients with clinical and radiographic diagnosis of FAI for at least 3 months were included. The rectus femoris (RF), adductor magnus (AM), and GM of both lower extremities of all patients were evaluated with tensiomyography (TMG). The values of TMG of the affected lower extremity were compared to those of the healthy contralateral side. The parameters obtained in this study were maximal displacement (Dm), and contraction time (Tc).
& Roberto Seijas [email protected] 1
Fundacio´n Garcı´a-Cugat. Artroscopia GC, Hospital Quiro´n, Barcelona, Spain
2
Universitat Internacional de Catalunya, Barcelona, Spain
3
Department of Orthopaedic Surgery, Duke Sports Sciences Institute, Duke University, Durham, NC, USA
4
Mutualidad de Futbolistas, Federacio´n Espan˜ola de Futbol, Delegacio´n Catalun˜a, Barcelona, Spain
5
Department of Physical Medicine and Rehabilitation, Hospital Quiro´n, Barcelona, Spain
6
Department of Orthopaedic Surgery, Hospital Vall d’Hebron, Barcelona, Spain
Results The Tc of the injured GM was significantly higher compared to the healthy side (p = 0.01). There were no significant side-to-side differences in the Dm of the GM (p = 0.13), either in the Tc and Dm of the RF (p = 0.15 and p = 0.8, respectively) and AM (p = 0.25 and p = 0.75, respectively). Conclusions FAI is associated with impairment of contraction time in the GM of the injured compared to the healthy side. Impairment of the GM may be monitored to evaluate response to conservative or surgical treatment. Keywords Femoroacetabular impingement Gluteus maximus Tensiomyography Rectus femoris Adductor magnus
Introduction The diagnosis of femoroacetabular impingement (FAI) has increased in recent years [1, 2]. A better understanding of the etiopathogenesis of hip disorders along with improved diagnostic techniques have contributed to an increase in the identification of this hip disorder, especially in young adults [1, 2]. Common signs and symptoms of FAI include activity-related groin or hip pain exacerbated with hip flexion, mechanical hip symptoms, sitting difficulties, and limited hip flexion especially with internal rotation, among others [3]. It has also been observed that muscular impairment is a common finding in patients with hip osteoarthritis undergoing joint replacement, mainly expressed with weakness in flexors, extensors, abductors, and rotator muscles [4–7]. Painful trigger points in several muscle groups have been reported in relation to FAI, the gluteus maximus being a common region [2, 8, 9]. Thus, investigating the status of the gluteus maximus is
123
Arch Orthop Trauma Surg
warranted to evaluate this clinical observation. However, research to evaluate gluteus maximus impairment is scarce. Tensiomyography (TMG) is a non-invasive method used to evaluate skeletal muscle mechanical and contractile properties in response to electrical stimuli [10]. This method provides information of muscle stiffness, muscle contraction velocity, type of predominant skeletal muscle fibers, or muscle fatigue [10, 11]. This method has shown good-toexcellent inter-observer, intra-session, and between-day reliability for other muscle groups of the lower extremity [11–14]. The evaluation of gluteus maximus muscular impairment in patients with FAI, including the tensiomyographic characteristics, has not been reported to date. The purpose of this study was to evaluate the gluteus maximus mechanical and contractile properties in patients with FAI with gluteus maximus dysfunction. It was hypothesized that the clinical observation of gluteus maximus pain would be evidenced by tensiomyographic impairment in muscle function.
Materials and methods A cross-sectional, intra-group comparative study was conducted to assess the neuromuscular changes of lower extremity muscles in patients with FAI. All consecutive patients with clinical and radiographic diagnosis of FAI, Camtype, for a period of at least 3 months were included in the present study. All patients had positive C-sign and pain and/or weakness of the GM, and were diagnosed and followed by the same orthopedic surgeon specialist in joint-preserving hip disorders. Exclusion criteria included history of lumbar spine, pelvis, or hip surgery, neurological diseases, unrelated gait abnormalities, history of sciatica and other nerve root compression disorders of the proximal lower extremity. Before undergoing surgical treatment of FAI, the rectus femoris (RF), adductor magnus (AM), and gluteus maximus (GM) of both lower extremities of all patients were evaluated using TMG. The values of TMG for the muscles of the affected lower extremity were compared to those of the healthy contralateral side. An additional comparison was conducted depending on gender for each of the TMG parameters. The methodology for the TMG assessment was identical in all patients. This method uses a portable device that produces an electrical stimulus applied percutaneously that creates a muscular contraction detected by a digital transducer applied above the muscle belly [15]. TMG has demonstrated good-to-excellent inter-observer, intra-session, and between-day reliability for vastus medialis, vastus lateralis, RF, and biceps femoris [11–14]. The parameters obtained in this study were the maximal displacement (Dm) expressed in mm, and the contraction time (Tc) expressed in
123
ms. The Dm is the radial movement of the muscle belly after the application of the electrical stimulus. The Tc is the time between 10 and 90 % of Dm. Both parameters were obtained for the RF, AM, and GM of the healthy and affected lower extremity under the same conditions. The same researcher with experience in TMG collected all data. The measurement protocol has been previously described in detail [16–20], and was based on Rey et al. [11]. All measurements were obtained at rest in the supine position for the RF and AM, and in the prone position for the GM. For the supine position, a foam cushion was employed to keep the knee joint with a fixed angle of 608 of knee flexion [11], and the hip joint was kept at 308 flexion. To evaluate the GM in the prone position, a foam cushion was also employed to keep a hip flexion of approximately 308. The radial muscle displacement was measured perpendicular to the muscle belly with a digital transducer Dc–Dc Trans-TekÒ (GK 40, Panoptik d.o.o., Ljubliana, Slovenia). The TMG measurements were obtained in all patients under the following conditions [11]: (1) resting, with no previous strenuous exercise in 48 h; (2) no intake of energy drinks or supplements in the previous 48 h; (3) no alcohol or caffeine at least 3 h before measurements; and (4) no foot intake at least 2 h before measurements. The self-adhesive electrodes (Compex Medical SA, Ecublens, Switzerland) were placed equidistant to the measuring point, proximal (anode) and distal (cathode) to the sensor. Electrical stimulation was applied through a TMG-100 System electrostimulator (TMG-BMC d.o.o., Ljubljana, Slovenia) with a pulse of 1 ms and an initial amplitude of 50 mA. For each test, amplitude was progressively increased by 10 mA increments until there was no further increase in Dm or maximal stimulator output (110 mA). All muscles were tested twice; firstly to assure appropriate functioning of the TMG, and a second time was taken as the definitive value. All patients gave consent to participate in this study, which received Institutional Review Board approval. Statistical analysis Descriptive statistics were used to summarize all demographic characteristics as well as outcomes. A Shapiro– Wilk test was first conducted to assess for normal distribution of all the evaluated parameters. For variables with normal distribution, an unpaired Student’s t test was employed to compare the TMG values between both sides. This test was also used to compare side-to-side differences for each TMG parameter between males and females. For variables not following a normal distribution, a Mann– Whitney test was used for the comparison of TMG values between sides. A separate sample size calculation was conducted for the Tc and Dm parameters, and involved all muscle groups of a preliminary sample of 20 patients. The
Arch Orthop Trauma Surg
minimum sample size that was considered for the whole study was obtained from the comparison that elicited the highest value of sample size. The Tc corresponded to the result of calculating the highest number of patients needed for the study to compare the TMG values between both lower extremities. Considering a power of 80 % to detect statistically significant differences in the hypothesis testing through a two-tailed unpaired t test with an alpha level of 0.05, and assuming a difference in mean Tc values between the injured and healthy lower extremity of 2.3 ms, and a standard deviation of the healthy side of 5.6 ms, 47 patients were needed. All statistical analyses were conducted using the SPSS v.21 (SPSS, Inc. Chicago, IL, USA). The alpha level was set up at 0.05.
Results Fifty-one patients were finally included in the present study. Mean age (SD) was 44.7 (12.4) years old. The left lower extremity was the affected side in 27 patients, and the right lower extremity in 24 patients. There were 24 women and 27 men. The comparison of TMG parameters between the injured and healthy sides for all muscle groups is shown in Table 1. The Tc for the GM was significantly higher in the injured compared to the healthy side (p = 0.01). There were no significant side-to-side differences for Tc and Dm in the RF (p = 0.88 and p = 0.5, respectively), for Tc and Dm in the AM (p = 0.9 and p = 0.45, respectively), and for Tc and Dm in the GM (p = 0.72 and p = 0.22, respectively) between males and females.
Discussion The main finding of the present research was that the GM showed poorer mechanical and contractile properties in the injured side of patients affected of FAI compared to the healthy side. In contrast, the RF and AM demonstrated similar TMG characteristics between both sides in the same cohort of patients.
Table 1 Comparison of the tensiomiography parameters between the injured and healthy sides for all muscle groups
Parameter/side
The GM is one of the biggest muscles in the human body, with broad origin and insertion including the ilium, the sacrotuberous ligaments, the sacrum and the coccyx [21]. Eighty percent of the insertion is found in the iliotibial band and gluteal tuberosity. This muscle is a powerful hip extensor and significantly contributes to hip external rotation [22]. It has a major role in physical activities involving sprinting, squatting and climbing a steep hill [23]. The relationship between impairment in the contractility or function of the GM and different hip or lumbar disorders has already been described [21, 24]. FAI produces pain in the lateral and posterior aspect of the hip joint and in the lumbosacral area [2, 8, 9]. While worsening of GM function in neurologic injuries has been well demonstrated [25], the status of the GM in patients with FAI has not been yet described. Therefore, the quantification or measurement of this clinical observation (pain in the GM area) seems timely. Values of Tc above 30 ms have been related to a predominance of slow-twitch (type I muscle fibers) muscle type [26]. According to the present results, the RF and AM would predominantly be fast and powerful muscles whereas the GM would be slow and endurance muscles. This is in accordance to autopsy data where it was demonstrated that RF and GM had a predominance of fasttwitch (type II) and slow-twitch (type I) muscles fibers, respectively [27]. However, the AM has been reported to predominantly be a slow-contraction muscles with 53.5 % of type I muscle fibers [27], whereas in the present study the mean Tc was 25 ms. In the side-to-side comparison, the decrease in Tc of the GM of the injured compared to the healthy side may indicate that the disorder causes a decreased contraction speed of the muscle [11, 15]. Therefore, the GM of the injured side would decrease its ability to rapidly generate strength during contraction [11]. The differences in Tc between the injured and healthy GM could be explained by the injury, as it clinically correlates with a painful area in FAI. In addition, no differences between both lower extremities for Tc and Dm of vastus medialis, vastus lateralis, RF, biceps femoris, gastrocnemius medialis and gastrocnemius lateralis in healthy individuals have been identified [19]. However, differences of
Rectus femoris
Adductor magnus
Gluteus maximus Mean (SD)
Mean (SD)
p value
Mean (SD)
p value
Tc injured
28.7 (4.6)
0.15
26.6 (8.5)
0.25
Tc healthy
27.6 (3.2)
Dm injured Dm healthy
8.8 (2.7) 8.6 (3)
24.8 (6.5) 0.8
4.3 (2.3) 4.6 (2.6)
37 (9.5)
p value 0.01
32.9 (7.2) 0.75
6 (3.4) 5 (3)
0.13
Dm maximal displacement, Tc contraction time
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both lower extremities for the AM and GM were not assessed in the study by Alvarez-Diaz et al. [19]. The absence of pre-injury TMG values does not allow to strongly concluding that the observed side-to-side differences are explained by the injury. FAI produces gait changes due to pain and limited hip motion that would likely explain the observed impairment of the GM. Further investigations with pre-injury data are needed to better elucidate the effects of FAI in GM and other muscle groups. Furthermore, some authors have defended the role of conservative treatment of FAI over surgical treatment [28–31]. Therefore, a therapeutic pre and post-study evaluating the effects of conservative or surgical treatment on TMG modifications of GM should be performed. The Dm represents muscle stiffness. Some authors have related Dm to contraction velocity (Tc) and muscle fatigue (relaxation time, or Tr) [32, 33]. Kokkonen et al. suggested that lower muscle stiffness (higher Dm values) in the musculotendinous unit would induce a decrease of strength and muscle power, thus reducing contraction velocity (increase in Tc) [32]. These conclusions cannot be applied to the present study, as the Dm was not significantly different in any of our comparisons. The relationship between muscle fatigue (Tr) and Dm cannot be either established in the present study as Tr was not evaluated. To our knowledge, there are no similar studies evaluating GM TMG changes in patients with FAI or other hip disorders. Alvarez-Diaz et al. reported on TMG changes of the vastus medialis, vastus lateralis, RF, biceps femoris, gastrocnemius medialis and gastrocnemius lateralis after anterior cruciate ligament injury and subsequent reconstruction in soccer players [18, 20]. Anterior cruciate injury caused a decrease in contraction velocity, resistance to fatigue and muscle tone/stiffness of the quadriceps, hamstrings and gastrocnemius medialis [18], which was corrected with ligament reconstruction and subsequent physical therapy [20]. These data cannot be extrapolated to FAI as they deal with a different disorder. Several limitations should be considered when reviewing the present study. First, the absence of pre-injury data prevents us from elaborating strong conclusions on the effects of FAI in the observed GM impairment. However, there is not definitive reason to assume that side-to-side differences for this muscle group would be observed in healthy conditions. In addition, GM impairment seems to clinically correlate with pain or weakness in this muscle area. Second, this study provides no data on the length of symptoms or current physical activity level, both of which may influence TMG values. Third, no correlation was conducted between the present findings and the pain or range of motion. Further studies are needed to evaluate the correlation of TMG values of the GM and the presence/
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absence and location of hip pain, especially in the posterior aspect of the joint.
Conclusions FAI is associated with impairment of contraction time (Tc) in the GM of the injured compared to the healthy side. Impairment of the GM may be monitored to assess response to either conservative or surgical treatment of FAI. Compliance with ethical standards Conflict of interests The authors declare no conflict of interests or financial aid for the present investigation.
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