IJSPT
ORIGINAL RESEARCH
THE ACTIVITY PATTERN OF THE LUMBOPELVIC MUSCLES DURING PRONE HIP EXTENSION IN ATHLETES WITH AND WITHOUT HAMSTRING STRAIN INJURY Mahnaz Emami, PT, MSc1 Amir Massoud Arab, PT, PhD2 Leila Ghamkhar, PT, MSc1
ABSTRACT Background: Altered muscular activation pattern has been associated with musculoskeletal disorders. Some previous studies have demonstrated muscle weakness or tightness in athletes who have sustained hamstring (HAM) injuries. However, no study has clinically investigated the muscular activity pattern in subjects with HAM strain injuries. Objective: To investigate the activity pattern of the ipsilateral erector spinae (IES), contralateral erector spinae (CES), gluteus maximus (GM), and medial and lateral HAM muscles during the prone hip extension (PHE) test in athletes with and without history of HAM strain injury. Design: Cross-sectional non-experimental study design. Participants: A convenience sample of 20 soccer athletes participated in the study. Subjects were categorized into two groups: those with history of HAM strain injury (n=10, mean age = 22.6 ± 3.74) and without history of HAM strain (n =10, mean age = 22.45 ± 3.77). Methods: Three repetitions of the PHE were performed by each subject, and the electromyographic (EMG) outputs of the IES, CES, GM, and HAM muscles were recorded, processed and normalized to maximum voluntary electrical activity (MVE). Independent ttests were used for comparing activation means of each muscle between athletes with and without history of HAM strain injury. Results: There were significant differences in EMG activity of the GM (p= 0.04) and medial HAM (p = 0.01) between two groups. No significant difference was found in EMG signals of the IES (p= 0.26), CES (= 0.33) and lateral HAM (p= 0.58) between the two groups. Greater although non-significant normalized EMG outputes of IES, CES and lateral HAM were seen in athletes with history of HAM strain compared to those without HAM strain. Conclusion: The findings of this study demonstrated greater normalized EMG activity of GM and medial HAM tested in athletes with history of HAM strain compared to those without HAM strain (altered activation pattern). Level Of Evidence: 3a Key Words: Electromyography, hamstring strain, movement pattern, prone hip extension.
1
University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran 2 Department of Physical Therapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran. Source of Support: Partially supported by the University of Social Welfare and Rehabilitation Sciences Institutional review board: Human subject committee of University of Social Welfare and Rehabilitation Sciences, Tehran, Iran Disclosures: None
CORRESPONDING AUTHOR Amir Massoud Arab, PT, PhD Associate Professor Department of Physical Therapy University of Social Welfare and Rehabilitation Sciences Evin, Koodakyar Ave., Tehran, Iran Zip Code: 1985713831 Tel: (98) 21 22180039 (Office) (98) 21 22358149 (Home) Fax: (98) 21 22180039 E-mail: [email protected]; [email protected]
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INTRODUCTION Hamstring injuries are frequently identified as a common soft tissue injury occurring in athletes who participate in sports involving rapid acceleration and frequent stopping and starting, like soccer.1-7 Hamstring strain injuries account for 12-16% of soccer injuries and the financial impact of this has been estimated to be 115.86 million dollars.4 A rate of five to six hamstring strain injuries per club per season has been observed, resulting in minimum of three and maximum of 15-21 matches missed per club per season on average.3 Hamstring muscle strain is a frustrating injury with persistent symptoms, often slow healing (at least 2-3 weeks), with a high re-injury rate.3 It has been reported that the re-injury rate of Australian football players who lost the entire season after the first hamstring injury was as high as 12-31%.1,4,5,7 Hamstring muscle dysfunction (weakness or tightness) has been frequently associated with hamstring muscle strain. Authors of previous studies describe hamstring muscle weakness or tightness in athletes with hamstring muscle injury.8,9 During the recent decades, the approach of assessment and treatment of musculoskeletal pain has been changed from exercises targeted at developing strength alone, toward modifying the motor system.10 Balance within the motor system is derived from coordinated activity of synergist and antagonist muscles. According to this point of view, change in muscle length and strength characteristics can lead to altered movement patterns, pain, and movement disorders.10 Increased or decreased muscle activity and delayed muscular activation can also change the normal movement pattern.11,12 Recently, several authors have suggested that the main focus of rehabilitation should be on modification of the altered movement patterns found in patients with musculoskeletal pain and disorders.12-14 Several authors have shown altered activation pattern of the certain lumbo-pelvic muscles such as the gluteal muscles, trunk extensor muscles, trunk flexor muscles, and hip extensors in people who suffer from lumbo-pelvic disorders.15-18 The prone hip extension (PHE) test is a commonly and widely accepted test used to assess muscular
activation patterns in the lumbo-pelvic area. In PHE, subjects lie in prone position and lift the chosen leg off the bed to 10 degrees of hip extension whilst keeping the knee straight.12 PHE is a muscle activity pattern that has been theorized to simulate those muscles used during functional movement patterns such as gait.11,14 It has been theorized that changes in the typical activity pattern can overstress the various structures such as joint, ligament, capsule and etc., resulting in pain during walking.19 Good reliability has been reported for PHE test.20 Both timing (onset time) and amplitude of muscle activity are commonly calculated using electromyography (EMG) to investigate muscular activation patterns in musculoskeletal disorders.21-24 During PHE, the investigator evaluates the activity pattern of the ipsilateral erector spinae (IES), contralateral erector spinae (CES), ipsilateral gluteus maximus (GM) and ipsilateral hamstring (HAM) muscles21. It is assumed that when a muscle responsible for a specific joint movement (the prime mover) is inhibited or weakened, the amplitude of activation is lowered and the synergistic muscles substitute and become overactive during the movement.17,21,23 When a muscle is tight, the irritability threshold of the muscle is believed to be decreased. With less slack to take up before contraction begins, the muscle is activated earlier than normal in a movement sequence.10 Thus, the patterns of tightness or weakness seen in the muscle imbalance process result in alteration of the normal movement pattern.10 Considering HAM muscle weakness or tightness that has been reported in athletes who have sustained HAM muscle strains,25-27 it is possible that altered muscular activation patterns exist during PHE in these subjects. According to Sahrmann, abnormal movement pattern during PHE could place unusual mechanical stresses on the structures in lumbo-pelvic area.10 Review of the literature revealed that previous studies have examined HAM muscle strength or tightness in athletes with HAM injuries. However, to the authors’ knowledge, no study has clinically investigated the muscular activity pattern of lumbo-pelvic muscles during PHE in athletes with HAM strain injuries. The purpose of this study was to investigate the amplitude of the activation of IES, CES, GM and medial and lateral
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HAM muscles during PHE in male athletes with and without history of HAM strain injury. METHODS Subjects A cross-sectional non-experimental observational study was used to compare the muscle activity pattern during PHE in two groups of male professional soccer athletes with history of HAM strain (N = 10, average age: 22.6 [SD = 3.74] years old, average height: 180 [SD = 0.04] cm, average weight: 75.8 kg [SD = 7.49] kg) and athletes with no history of HAM strain (N = 10, average age: 104 22.45 [SD = 3.77] years old, average height: 177 [SD = 0.07] cm, average weight: 74.1 [SD = 8.02] kg). Athletes with history of HAM strain were referred for participation in the study by orthopedic specialists and physiotherapy clinics. The patients were included if they had a history of HAM strain during the year before the time of the study. They could not have sustained a hamstring strain in the month before the study date.3,27 All players with history of HAM strain reported localized posterior thigh pain at the time of injury that resulted in missed training and/or playing time (at least one match). Athletes who sustained contact injuries (direct trauma) were excluded. The healthy players were included if they had no history of HAM strain and were matched for age, height, weight and BMI. The exclusion criteria in both groups were history of hip pain, dislocation or fracture of the lower extremity, history of lumbar spine surgery, history of knee ligament injury or rupture, history of anterior knee pain, history of pain or injury in lumbar area in the prior three months, recent episodes of ankle sprain 3 month prior to the study, leg length difference of more than one centimeter, inability to perform active PHE without pain, shortness of hip flexors (by Thomas Test), or positive neurological symptoms. Each eligible subject was enrolled after signing an informed consent form approved by the human subjects committee at the University of Social Welfare and Rehabilitation Sciences. Ethical approval for this study was granted from the internal ethics committee at the University of Social Welfare and Rehabilitation Sciences. The injured leg of the injured subjects and dominant leg of healthy subjects were chosen for investigation.
The raw EMG activity pattern of IES, CES, GM and HAM muscles during PHE was collected using the MIE-MT8 Telemetry EMG instrument (MIE-Medical, Leeds, UK). A preamplifier with a gain of (4000×), band pass filter (6-500 HZ) and A-D convertor (sampling rate = 1000 HZ) were used to process the EMG signal. The subjects were asked to lie prone with their arms at their side and head in mid line. The skin was shaved, rubbed, and cleaned with alcohol. To record muscle activity, disposable, bipolar, self-adhesive Ag/Agcl electrodes (In Vivo Metric, Healdsburg, CA, USA) were placed in pairs with distance of 1.5-2 cm from each other and parallel to the muscle fibers.25 Electrode placement to collect EMG signals were as follow: for the ES muscles, bilaterally at least 2 cm lateral to spinous process of L3 parallel to the vertebral column on the muscle belly; for the GM, at the midpoint of a line running from S2 to the greater trochanter; for the lateral HAM, laterally on the mid distance between gluteal and popliteal fold; and for the medial HAM, medially on the mid distance between gluteal and popliteal fold. Figure 1 depicts the electrode placement for EMG assessment of the muscles. The maximum voluntary electrical activity (MVE) for each muscle was calculated for use during normalization. Testing procedure to calculate MVE were similar to those described for manual muscle testing of the muscles, as described by Kendall et al.28 The pelvis was secured to the bed with a sling to prevent pelvic motion substitution only during MVE testing. For the ES muscles the subject was asked to bring up their trunk against the maximum resistance applied
Figure 1. Electrode placement for EMG assessment of the muscles.
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below the scapula. For the GM, the hip joint was placed in an extended position with the knee flexed to 90 degrees, and resistance was applied to the distal aspect of posterior portion of thigh. For the HAM muscles, the hip joint was placed in extension position of zero degrees, the knee was flexed to nearly 70 degrees, and resistance was applied to the distal aspect of the posterior portion of the shank during knee flexion with medial rotation for medial HAM and with lateral rotation for lateral HAM. Each contraction was repeated 2 times and held 5 seconds. One-minute rest was given between contractions. An average of the two MVC contractions was used for calculations. Before testing, the subjects were familiarized with the standard position and movement. All subjects were asked to lift the chosen leg off the bed to 10 degrees of hip extension whilst keeping the knee straight, as soon as they heard the command “lift”. An adjustable bar was placed at this level and the subjects were asked to extend their hip until the calcaneus touched the bar. The subjects were instructed only to reach the adjustable bar and were not instructed to press against the bar with the distal segment of the lower extremity. This was repeated three times for each individual. Figure 2 presents an example of the raw EMG signals for tested muscles. The raw data were processed into the root mean square (RMS). The EMG signals collected during hip extension were normalized to MVC expressed as percentage of the calculated mean RMS of MVE (%MVE). The muscle activity pattern was characterized by maximal amplitude of normalized voluntary activity.
Figure 2. Example of data recording from the tested muscles.
Data Analysis Statistical analysis was performed using SPSS Version 17. Multivariate analysis was used to compare the maximal amplitude of normalized voluntary activity of the tested muscles between athletes with and without history of HAM strain. Statistical significance was defined as a p-value less than 0.05. RESULTS The demographic data for each are displayed in Table 1. There was no statistically significant difference in subjects’ age, height, weight and BMI between the two groups. The maximal amplitude of normalized electrical activity of the IES, CES, GM and medial and lateral HAM muscles during PHE test in athletes with and without history of HAM strain are presented in Table 2. There was significant difference in EMG activity of the GM (F=3.48, p=0.04) and medial HAM (F=5.26, p = 0.01) between the two groups. However, no significant difference was found in EMG activity of the IES (F=1.39, p= 0.26), CES (F=1.14, p= 0.33) and lateral HAM (F=0.54, P= 0.58) among the two groups. The results indicated that normalized electrical activity of the IES, CES, and lateral HAM muscles is greater during PHE, (although not statistically significantly) in athletes with history of HAM injury compared to those without HAM injury. DISCUSSION The current study compared muscular activation patterns between individuals with and without history of HAM strain. The results of this study showed higher maximal amplitude of normalized electrical activity of the tested muscles in athletes with history of HAM strain compared to those without history of HAM. However, only the difference in EMG activity of medial HAM and GM were statistically significantly different between the two groups. These findings demonstrate that a difference exists in the muscular activity pattern during PHE in athletes with history of HAM strain compared with healthy, uninjured subjects. Many factors affect absolute EMG amplitudes, such as thickness of tissues overlying the muscle and skin impedance. To obtain an EMG output that is independent of these factors, the EMG amplitude must be normalized to the amplitudes obtained in MVE.
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Table 1. Demographic data of the subjects in each group With Hamstring strain (n=10)
Without Hamstring strain (n=10)
Average (SD)
Mean
Average (SD)
Mean
Variables
Age (years)
(3.74)
22.6
(3.77)
22.45
Weight (kg)
(7.49)
75.8
(8.02)
74.1
Height (cm)
(0.04)
180
(0.07)
177
BMI (kg/m2)
(1.81)
23.23
(1.28)
23.44
SD = Standard Deviaon BMI = Body Mass Index
Table 2. Electromyographic activity of the muscles during prone hip extension in subjects with and without Hamstring strain Muscle acvity
Without Hamstring strain
With Hamstring strain
p-value
IES
28.20(16.59)
41.60 (23.77)
0.26
CES
36.40(14.09)
44.90(17.97)
0.33
GM
18.33(12.08)
27.83(23.84)
0.04
Med HAM
40(16.92)
72(23.81)
0.01
Lat HAM
51.08(23.72)
60.40(19.66)
0.58
(%MVE)
Values are Mean (SD), bold p-values indicate stascal significance IES: Ipsilateral erector spinae; CES: Contralateral erector spinae; GM: Gluteus maximus; Med HAM: Medial hamstring; Lat HAM: Lateral hamstring
However, this procedure may not be appropriate for subjects who have sustained injury because they may be unwilling or not able to perform maximum contractions due to pain or fear of re-creating pain. Normalization to sub maximal contractions is not a good method because the EMG amplitudes during these contractions will be affected similarly during the activities to be studied. In the current study, MVE method was used because subjects had no pain during the test and none of the subjects reported that pain was a limiting factor to perform the PHE test. Thus the direct effects of pain can be minimized. Investigators have attributed the HAM strain to various factors, such as muscle weakness, reduced flexibility or tightness, fatigue, and muscle imbalance. Some investigators have demonstrated HAM muscle
weakness or tightness and muscle imbalance in athletes with HAM muscle strain injury.8,9 The concept of muscle imbalance has been explained by different authors.10-12,28-30 In its simplest form it is defined as the ratio between the strength or flexibility of the agonist and antagonist muscles around a joint. However, more in-depth descriptions of muscle imbalance define the altered movement pattern in musculoskeletal disorders. When a muscle is weakened or inhibited, the synergistic muscle substitute and become overactive to perform the movement. Thus, the pattern of tightness or weakness seen in the muscle imbalance process result in alteration of the normal movement pattern.10 Hence, contemporary treatment focus has shifted to modification of the altered movement pattern in patients with musculoskeletal pain and disorders.12-14
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To the authors’ knowledge, this is the first study to investigate the muscular activation pattern in a specified movement pattern (PHE) in athletes with HAM strain injury. The difference in the normalized EMG activity of the muscles between individuals with and without HAM strain found in the current study complements the results of authors which indicated that muscle imbalance is associated with HAM strain injury and could be considered as an important risk factor. The current data revealed a significant difference in activity pattern of medial HAM (p = 0.01) while there was no significant difference in lateral HAM activity (p= 0.58) between athletes with and without history of HAM strain. This discrepancy may be due to the site of injury in the HAM muscles in the participants with hamstring strain. Different parts of the HAM muscles (medial vs. lateral) vary from each other with respect to muscle architecture, e.g. fascicular length, physiological cross-sectional area, length of the proximal and distal free tendons, extent of the intramuscular tendons and flexion moments.31,32 In this study, medial side of hamstring was mostly commonly affected in the subjects with hamstring strain. Controversy exists regarding the most common site of strain injury (medial vs. lateral) in HAM muscles. In this study, most of the subjects had strain injury in the medial portion of the HAM muscles. Change in medial-lateral HAM muscle activation ratio has been previously reported in other musculoskeletal disorders including lumbo-pelvic and low back pain.33 The current data showed a significant difference in EMG activity of the GM between the athletes with and without history of HAM strain. GM provides powerful hip extension during sprinting. The hamstrings are thought to act as transducers of power. HAM muscle dysfunction followed by strain injury may cause the GM to be overactive. Both of these two actions may predispose an athlete to re-injury. Lumbo-pelvic dysfunction and disorders has been associated with HAM strain.34 Some investigators have shown an altered muscular activation pattern of the erector spinae, gluteal maximus, and hamstring muscles during PHE subjects with and without low back pain.21,24 Considering the association between HAM strain and lumbo-pelvic abnormality or dysfunction, the current findings are in accordance
with other studies showing alteration in muscular activity patterns in patients with low back pain.21,25,35 However, in this study, none of participants had low back pain. Subjects in the current study with HAM strain had non-statistically significant higher EMG activity of the IES, CES, and lateral HAM muscles during PHE compared with those without HAM injury (Table 2). However, the reason that no statistical differences were found between groups may be explained by the relatively small sample size. Therefore, it is essential to continue to investigate using a larger sample size in order to obtain the answers of the research questions more precisely. Additionally, in this study, the severity of strain injuries was mild and moderate and athletes with severe or acute HAM strain were not included in order to lessen the direct effects of pain as an important limiting factor. Some investigators stated that muscle dysfunction in subjects with musculoskeletal disorders might be related to pain, called “pain interference”.35-37 They believed that ability of voluntary contraction in all muscles during a movement is reduced because of the pain sensation. In this study, none of the subjects reported that pain was a limiting factor when producing hip extension. If a study is performed using athletes with severe injuries, muscular activity patterns may be significantly different between athletes with and without HAM strain injury due to muscle inhibition from pain or inflammation. The authors acknowledge several limitations. One of the limitations and a weakness of this study was the sample size. Subjects with severe and acute HAM strain were excluded in order to assess the muscle activity pattern in a more homogenous population. So, the accessible population, that is athletes with mild and moderate HAM strain injury and no other type of strain injury, was limited to a relatively small group of patients that were available during the time frame that this study was conducted. The authors’ suggest that this study could be repeated on subjects with different types and varied acuity of HAM strain to provide more insight regarding the muscular activity pattern in athletes with greater variety of HAM strain injury. It should also be noted that EMG measurements do not always guarantee the actual magnitude of force production or and objective measure of actual muscle
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strength.. In some cases, an inhibited muscle may work harder than a normal one in order to produce the required force for a particular task. Thus, the timing of the onset of muscle activity in addition to normalized EMG amplitude could provide additional useful information regarding the muscular activation pattern. CONCLUSION The results of this study indicate that there was statistically significantly greater normalized EMG activity of the medial HAM and GM in athletes with history of HAM strain injury compared to healthy subjects during the PHE test. REFERENCES 1. Bing Yu RMQ ANA, Yu Liu, Claude T. Moorman, William E. Garrett. Hamstring muscle kinematics and activation during overground sprinting. J Biomech. 2008;41:3121-3126. 2. Chumanov E TD. Hamstring strain injuries: recommendations for diagnosis, rehabilitation, and injury Prevention. J Orthop Sports Phys Ther. 2010;40(2):67-81. 3. Engebretsen A MG, Holme I, Engebretsen L, Bahr R. 2010;38(6):1147-1153. Intrinsic risk factors for hamstring injuries among male soccer players. Am J Sports Med. 2010;38(6):1147-1153. 4. Hoskins W PH. The management of hamstring injury--Part 1: Issues in diagnosis. Man Ther. 2005;10(2):96-107. 5. Hunter D SC. The assessment and management of chronic hamstring/posterior thigh pain Best Pract Res Clin Rheumatol. 2007;21(2):261-277. 6. Page P FC, Lardner R. Assessment and Treatment of muscle Imbalance. Human Kinetics. 2010. 7. Petersen J HP. Evidence based prevention of hamstring injuries in sport. Br J Sports Med. 2005;39(6):319-323. 8. Askling C ST, Thorstensson A. Type of acute hamstring strain affects flexibility, strength, and time to return to pre-injury level. Br J Sports Med. 2006;40(1):40-44. 9. Silder A TD, Heiderscheit BC. Effects of prior hamstring strain injury on strength, flexibility, and running mechanics. Clin Biomech. 2010;25:681-686. 10. Sahrmann. S. Diagnosis and treatment of movement impairment syndrome: 1th ed. St Louis: Mosby. 2002. 11. Sahrmann. S. Posture and muscle imbalance. Physiotherapy. 1992;78:13-20. 12. V. J. On the concept of postural muscles and posture in man. Aust J Physiother. 1983;29(3):83.
13. O’Sullivan P PD TL, Allison G. Evaluation of specific stabilizing exercise in the treatment of chronic low back pain with radiologic diagnosis of spondylolysis or spondylolisthesis. Spine. 1997;22(24):2959. 14. V. J. Pain in the locomotor system-A broad approach. Aspects of Manipulative Therapy Melbourne: Churchill Livingstone. 1985:148-151. 15. Hodges P MG. Pain and motor control of the lumbopelvic region: effect and possible mechanisms. J Electromyogr Kinesiol. 2003;13:36-70. 16. Hungerford B GW, Hodges P. Evidence of altered lumbopelvic muscle recruitment in the presence of sacroiliac joint pain. Spine. 2003;28:1593-1600. 17. Leinonen V KM, Airaksinen O, Hanninen O. Back and hip extensor activities during trunk flexion/ extension: Effects of low back pain and rehabilitation. Arch Phys Med Rehabil. 2000;81:32-37. 18. Newcomer K JT, Gabriel D, Larson D, Brey R, An K. Muscle activation patterns in subjects with and without low back pain. Arch Phys Med Rehabil 2002;83:816-821. 19. Vogt L PK, Banzer W. Neuromuscular control of walking with chronic low-back pain. Man Ther. 2003;8:21-28. 20. Murphy D BD, Mccarthy P, Humphreys K, Gregory A, Rochon R. Interexaminer reliability of the hip extension test for suspected impaired motor control of the lumbar spine. J Manipulative Physiol Ther. 2006;29:374-377. 21. Bruno P BJ. An investigation into motor pattern differences used during prone hip extension between subjects with and without low back pain. Clinical Chiropractic. 2007;10:68-80. 22. Lehman G LD, Tresidder B, Rayfield B, Poschar M. Muscle recruitment patterns during the prone leg extension. BMC Musculoskelet Disord. 2004;5(1):3. 23. Lewis C SS. Muscle activation and movement patterns during prone hip extension exercise in women. J Athl Train. 2009;44(3):238-248. 24. Sakamoto A T-SL, de Paula-Goulart F, de Morais Faria C, Guimarães C. Muscular activation patterns during active prone hip extension exercises. J Electromyogr Kinesiol. 2009;19(1):105-112. 25. Arab AM GL, Emami M, Nourbakhsh MR. Altered muscular activation during prone hip extension in women with and without low back pain. Chiropr Man Therap. 2011;19:18-24. 26. DLC. BJ. Muscle alive: their functions revealed by electromyography. Baltimore: Williams and Wilkins. 1985:Links.432. 27. Franklin BA. Balady GJ BK, Golding LA, Gordon N, Mahler DA Myers JN, and Sheldhal LM, ACSM’s.
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28. 29. 30. 31.
32. 33.
General Principles of Exercise Prescription Guidelines for exercise testing and prescription. 6th ed. Phyladelfia, Lippincot Williams & Willkins. 2004:137-164. Kendall F ME PP. Muscles Testing and Function. Baltimore MD: Williams & Wilkins. 1993. 81:20-31. NC. Spinal stabilisation 4. Muscle imbalance and the low back. Physiotherapy 1995;81:20-31. C. N. The Muscle debate. J Bodyw Mov Ther. 2004;4:232-235. Garrett WE RF, Nickolaou PK, et al. Computed tomography of hamstring muscle strains. Med Sci Sports Exerc. 1989;21:506-514. Woodley SJ MS. Hamstring muscles: architecture and innervation. Cells Tissues Organs 2005;179:125-141. Hubley-Kozey CL DK, Landry SC, McNutt JS, Stanish WD. Neuromuscular alterations during walking in
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persons with moderate knee osteoarthritis. J Electromyogr Kinesiol. 2006;16:365-378. Hennessey L WA. Flexibility and posture assessment in relation to hamstring injury. Br J Sports Med 1993;27:243-246. Moseley GL HP. Are the changes in postural control associated with low back pain caused by pain interference? Clin J Pain. 2005;21:323-329. Hodges PW MG, Gabrielsson A. Evidence for a direct effect of pain on postural recruitment of the trunk muscles in pain free humans. Exp Brain Res. 2004. Zedka M PA, Knight B, et al. Voluntary and reflex control of human back muscles during induced pain. J Physiol (Lond). 1999;520:591-604.
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ORIGINAL RESEARCH
THE ACTIVITY PATTERN OF THE LUMBOPELVIC MUSCLES DURING PRONE HIP EXTENSION IN ATHLETES WITH AND WITHOUT HAMSTRING STRAIN INJURY Mahnaz Emami, PT, MSc1 Amir Massoud Arab, PT, PhD2 Leila Ghamkhar, PT, MSc1
ABSTRACT Background: Altered muscular activation pattern has been associated with musculoskeletal disorders. Some previous studies have demonstrated muscle weakness or tightness in athletes who have sustained hamstring (HAM) injuries. However, no study has clinically investigated the muscular activity pattern in subjects with HAM strain injuries. Objective: To investigate the activity pattern of the ipsilateral erector spinae (IES), contralateral erector spinae (CES), gluteus maximus (GM), and medial and lateral HAM muscles during the prone hip extension (PHE) test in athletes with and without history of HAM strain injury. Design: Cross-sectional non-experimental study design. Participants: A convenience sample of 20 soccer athletes participated in the study. Subjects were categorized into two groups: those with history of HAM strain injury (n=10, mean age = 22.6 ± 3.74) and without history of HAM strain (n =10, mean age = 22.45 ± 3.77). Methods: Three repetitions of the PHE were performed by each subject, and the electromyographic (EMG) outputs of the IES, CES, GM, and HAM muscles were recorded, processed and normalized to maximum voluntary electrical activity (MVE). Independent ttests were used for comparing activation means of each muscle between athletes with and without history of HAM strain injury. Results: There were significant differences in EMG activity of the GM (p= 0.04) and medial HAM (p = 0.01) between two groups. No significant difference was found in EMG signals of the IES (p= 0.26), CES (= 0.33) and lateral HAM (p= 0.58) between the two groups. Greater although non-significant normalized EMG outputes of IES, CES and lateral HAM were seen in athletes with history of HAM strain compared to those without HAM strain. Conclusion: The findings of this study demonstrated greater normalized EMG activity of GM and medial HAM tested in athletes with history of HAM strain compared to those without HAM strain (altered activation pattern). Level Of Evidence: 3a Key Words: Electromyography, hamstring strain, movement pattern, prone hip extension.
1
University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran 2 Department of Physical Therapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran. Source of Support: Partially supported by the University of Social Welfare and Rehabilitation Sciences Institutional review board: Human subject committee of University of Social Welfare and Rehabilitation Sciences, Tehran, Iran Disclosures: None
CORRESPONDING AUTHOR Amir Massoud Arab, PT, PhD Associate Professor Department of Physical Therapy University of Social Welfare and Rehabilitation Sciences Evin, Koodakyar Ave., Tehran, Iran Zip Code: 1985713831 Tel: (98) 21 22180039 (Office) (98) 21 22358149 (Home) Fax: (98) 21 22180039 E-mail: [email protected]; [email protected]
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INTRODUCTION Hamstring injuries are frequently identified as a common soft tissue injury occurring in athletes who participate in sports involving rapid acceleration and frequent stopping and starting, like soccer.1-7 Hamstring strain injuries account for 12-16% of soccer injuries and the financial impact of this has been estimated to be 115.86 million dollars.4 A rate of five to six hamstring strain injuries per club per season has been observed, resulting in minimum of three and maximum of 15-21 matches missed per club per season on average.3 Hamstring muscle strain is a frustrating injury with persistent symptoms, often slow healing (at least 2-3 weeks), with a high re-injury rate.3 It has been reported that the re-injury rate of Australian football players who lost the entire season after the first hamstring injury was as high as 12-31%.1,4,5,7 Hamstring muscle dysfunction (weakness or tightness) has been frequently associated with hamstring muscle strain. Authors of previous studies describe hamstring muscle weakness or tightness in athletes with hamstring muscle injury.8,9 During the recent decades, the approach of assessment and treatment of musculoskeletal pain has been changed from exercises targeted at developing strength alone, toward modifying the motor system.10 Balance within the motor system is derived from coordinated activity of synergist and antagonist muscles. According to this point of view, change in muscle length and strength characteristics can lead to altered movement patterns, pain, and movement disorders.10 Increased or decreased muscle activity and delayed muscular activation can also change the normal movement pattern.11,12 Recently, several authors have suggested that the main focus of rehabilitation should be on modification of the altered movement patterns found in patients with musculoskeletal pain and disorders.12-14 Several authors have shown altered activation pattern of the certain lumbo-pelvic muscles such as the gluteal muscles, trunk extensor muscles, trunk flexor muscles, and hip extensors in people who suffer from lumbo-pelvic disorders.15-18 The prone hip extension (PHE) test is a commonly and widely accepted test used to assess muscular
activation patterns in the lumbo-pelvic area. In PHE, subjects lie in prone position and lift the chosen leg off the bed to 10 degrees of hip extension whilst keeping the knee straight.12 PHE is a muscle activity pattern that has been theorized to simulate those muscles used during functional movement patterns such as gait.11,14 It has been theorized that changes in the typical activity pattern can overstress the various structures such as joint, ligament, capsule and etc., resulting in pain during walking.19 Good reliability has been reported for PHE test.20 Both timing (onset time) and amplitude of muscle activity are commonly calculated using electromyography (EMG) to investigate muscular activation patterns in musculoskeletal disorders.21-24 During PHE, the investigator evaluates the activity pattern of the ipsilateral erector spinae (IES), contralateral erector spinae (CES), ipsilateral gluteus maximus (GM) and ipsilateral hamstring (HAM) muscles21. It is assumed that when a muscle responsible for a specific joint movement (the prime mover) is inhibited or weakened, the amplitude of activation is lowered and the synergistic muscles substitute and become overactive during the movement.17,21,23 When a muscle is tight, the irritability threshold of the muscle is believed to be decreased. With less slack to take up before contraction begins, the muscle is activated earlier than normal in a movement sequence.10 Thus, the patterns of tightness or weakness seen in the muscle imbalance process result in alteration of the normal movement pattern.10 Considering HAM muscle weakness or tightness that has been reported in athletes who have sustained HAM muscle strains,25-27 it is possible that altered muscular activation patterns exist during PHE in these subjects. According to Sahrmann, abnormal movement pattern during PHE could place unusual mechanical stresses on the structures in lumbo-pelvic area.10 Review of the literature revealed that previous studies have examined HAM muscle strength or tightness in athletes with HAM injuries. However, to the authors’ knowledge, no study has clinically investigated the muscular activity pattern of lumbo-pelvic muscles during PHE in athletes with HAM strain injuries. The purpose of this study was to investigate the amplitude of the activation of IES, CES, GM and medial and lateral
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HAM muscles during PHE in male athletes with and without history of HAM strain injury. METHODS Subjects A cross-sectional non-experimental observational study was used to compare the muscle activity pattern during PHE in two groups of male professional soccer athletes with history of HAM strain (N = 10, average age: 22.6 [SD = 3.74] years old, average height: 180 [SD = 0.04] cm, average weight: 75.8 kg [SD = 7.49] kg) and athletes with no history of HAM strain (N = 10, average age: 104 22.45 [SD = 3.77] years old, average height: 177 [SD = 0.07] cm, average weight: 74.1 [SD = 8.02] kg). Athletes with history of HAM strain were referred for participation in the study by orthopedic specialists and physiotherapy clinics. The patients were included if they had a history of HAM strain during the year before the time of the study. They could not have sustained a hamstring strain in the month before the study date.3,27 All players with history of HAM strain reported localized posterior thigh pain at the time of injury that resulted in missed training and/or playing time (at least one match). Athletes who sustained contact injuries (direct trauma) were excluded. The healthy players were included if they had no history of HAM strain and were matched for age, height, weight and BMI. The exclusion criteria in both groups were history of hip pain, dislocation or fracture of the lower extremity, history of lumbar spine surgery, history of knee ligament injury or rupture, history of anterior knee pain, history of pain or injury in lumbar area in the prior three months, recent episodes of ankle sprain 3 month prior to the study, leg length difference of more than one centimeter, inability to perform active PHE without pain, shortness of hip flexors (by Thomas Test), or positive neurological symptoms. Each eligible subject was enrolled after signing an informed consent form approved by the human subjects committee at the University of Social Welfare and Rehabilitation Sciences. Ethical approval for this study was granted from the internal ethics committee at the University of Social Welfare and Rehabilitation Sciences. The injured leg of the injured subjects and dominant leg of healthy subjects were chosen for investigation.
The raw EMG activity pattern of IES, CES, GM and HAM muscles during PHE was collected using the MIE-MT8 Telemetry EMG instrument (MIE-Medical, Leeds, UK). A preamplifier with a gain of (4000×), band pass filter (6-500 HZ) and A-D convertor (sampling rate = 1000 HZ) were used to process the EMG signal. The subjects were asked to lie prone with their arms at their side and head in mid line. The skin was shaved, rubbed, and cleaned with alcohol. To record muscle activity, disposable, bipolar, self-adhesive Ag/Agcl electrodes (In Vivo Metric, Healdsburg, CA, USA) were placed in pairs with distance of 1.5-2 cm from each other and parallel to the muscle fibers.25 Electrode placement to collect EMG signals were as follow: for the ES muscles, bilaterally at least 2 cm lateral to spinous process of L3 parallel to the vertebral column on the muscle belly; for the GM, at the midpoint of a line running from S2 to the greater trochanter; for the lateral HAM, laterally on the mid distance between gluteal and popliteal fold; and for the medial HAM, medially on the mid distance between gluteal and popliteal fold. Figure 1 depicts the electrode placement for EMG assessment of the muscles. The maximum voluntary electrical activity (MVE) for each muscle was calculated for use during normalization. Testing procedure to calculate MVE were similar to those described for manual muscle testing of the muscles, as described by Kendall et al.28 The pelvis was secured to the bed with a sling to prevent pelvic motion substitution only during MVE testing. For the ES muscles the subject was asked to bring up their trunk against the maximum resistance applied
Figure 1. Electrode placement for EMG assessment of the muscles.
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below the scapula. For the GM, the hip joint was placed in an extended position with the knee flexed to 90 degrees, and resistance was applied to the distal aspect of posterior portion of thigh. For the HAM muscles, the hip joint was placed in extension position of zero degrees, the knee was flexed to nearly 70 degrees, and resistance was applied to the distal aspect of the posterior portion of the shank during knee flexion with medial rotation for medial HAM and with lateral rotation for lateral HAM. Each contraction was repeated 2 times and held 5 seconds. One-minute rest was given between contractions. An average of the two MVC contractions was used for calculations. Before testing, the subjects were familiarized with the standard position and movement. All subjects were asked to lift the chosen leg off the bed to 10 degrees of hip extension whilst keeping the knee straight, as soon as they heard the command “lift”. An adjustable bar was placed at this level and the subjects were asked to extend their hip until the calcaneus touched the bar. The subjects were instructed only to reach the adjustable bar and were not instructed to press against the bar with the distal segment of the lower extremity. This was repeated three times for each individual. Figure 2 presents an example of the raw EMG signals for tested muscles. The raw data were processed into the root mean square (RMS). The EMG signals collected during hip extension were normalized to MVC expressed as percentage of the calculated mean RMS of MVE (%MVE). The muscle activity pattern was characterized by maximal amplitude of normalized voluntary activity.
Figure 2. Example of data recording from the tested muscles.
Data Analysis Statistical analysis was performed using SPSS Version 17. Multivariate analysis was used to compare the maximal amplitude of normalized voluntary activity of the tested muscles between athletes with and without history of HAM strain. Statistical significance was defined as a p-value less than 0.05. RESULTS The demographic data for each are displayed in Table 1. There was no statistically significant difference in subjects’ age, height, weight and BMI between the two groups. The maximal amplitude of normalized electrical activity of the IES, CES, GM and medial and lateral HAM muscles during PHE test in athletes with and without history of HAM strain are presented in Table 2. There was significant difference in EMG activity of the GM (F=3.48, p=0.04) and medial HAM (F=5.26, p = 0.01) between the two groups. However, no significant difference was found in EMG activity of the IES (F=1.39, p= 0.26), CES (F=1.14, p= 0.33) and lateral HAM (F=0.54, P= 0.58) among the two groups. The results indicated that normalized electrical activity of the IES, CES, and lateral HAM muscles is greater during PHE, (although not statistically significantly) in athletes with history of HAM injury compared to those without HAM injury. DISCUSSION The current study compared muscular activation patterns between individuals with and without history of HAM strain. The results of this study showed higher maximal amplitude of normalized electrical activity of the tested muscles in athletes with history of HAM strain compared to those without history of HAM. However, only the difference in EMG activity of medial HAM and GM were statistically significantly different between the two groups. These findings demonstrate that a difference exists in the muscular activity pattern during PHE in athletes with history of HAM strain compared with healthy, uninjured subjects. Many factors affect absolute EMG amplitudes, such as thickness of tissues overlying the muscle and skin impedance. To obtain an EMG output that is independent of these factors, the EMG amplitude must be normalized to the amplitudes obtained in MVE.
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Table 1. Demographic data of the subjects in each group With Hamstring strain (n=10)
Without Hamstring strain (n=10)
Average (SD)
Mean
Average (SD)
Mean
Variables
Age (years)
(3.74)
22.6
(3.77)
22.45
Weight (kg)
(7.49)
75.8
(8.02)
74.1
Height (cm)
(0.04)
180
(0.07)
177
BMI (kg/m2)
(1.81)
23.23
(1.28)
23.44
SD = Standard Deviaon BMI = Body Mass Index
Table 2. Electromyographic activity of the muscles during prone hip extension in subjects with and without Hamstring strain Muscle acvity
Without Hamstring strain
With Hamstring strain
p-value
IES
28.20(16.59)
41.60 (23.77)
0.26
CES
36.40(14.09)
44.90(17.97)
0.33
GM
18.33(12.08)
27.83(23.84)
0.04
Med HAM
40(16.92)
72(23.81)
0.01
Lat HAM
51.08(23.72)
60.40(19.66)
0.58
(%MVE)
Values are Mean (SD), bold p-values indicate stascal significance IES: Ipsilateral erector spinae; CES: Contralateral erector spinae; GM: Gluteus maximus; Med HAM: Medial hamstring; Lat HAM: Lateral hamstring
However, this procedure may not be appropriate for subjects who have sustained injury because they may be unwilling or not able to perform maximum contractions due to pain or fear of re-creating pain. Normalization to sub maximal contractions is not a good method because the EMG amplitudes during these contractions will be affected similarly during the activities to be studied. In the current study, MVE method was used because subjects had no pain during the test and none of the subjects reported that pain was a limiting factor to perform the PHE test. Thus the direct effects of pain can be minimized. Investigators have attributed the HAM strain to various factors, such as muscle weakness, reduced flexibility or tightness, fatigue, and muscle imbalance. Some investigators have demonstrated HAM muscle
weakness or tightness and muscle imbalance in athletes with HAM muscle strain injury.8,9 The concept of muscle imbalance has been explained by different authors.10-12,28-30 In its simplest form it is defined as the ratio between the strength or flexibility of the agonist and antagonist muscles around a joint. However, more in-depth descriptions of muscle imbalance define the altered movement pattern in musculoskeletal disorders. When a muscle is weakened or inhibited, the synergistic muscle substitute and become overactive to perform the movement. Thus, the pattern of tightness or weakness seen in the muscle imbalance process result in alteration of the normal movement pattern.10 Hence, contemporary treatment focus has shifted to modification of the altered movement pattern in patients with musculoskeletal pain and disorders.12-14
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To the authors’ knowledge, this is the first study to investigate the muscular activation pattern in a specified movement pattern (PHE) in athletes with HAM strain injury. The difference in the normalized EMG activity of the muscles between individuals with and without HAM strain found in the current study complements the results of authors which indicated that muscle imbalance is associated with HAM strain injury and could be considered as an important risk factor. The current data revealed a significant difference in activity pattern of medial HAM (p = 0.01) while there was no significant difference in lateral HAM activity (p= 0.58) between athletes with and without history of HAM strain. This discrepancy may be due to the site of injury in the HAM muscles in the participants with hamstring strain. Different parts of the HAM muscles (medial vs. lateral) vary from each other with respect to muscle architecture, e.g. fascicular length, physiological cross-sectional area, length of the proximal and distal free tendons, extent of the intramuscular tendons and flexion moments.31,32 In this study, medial side of hamstring was mostly commonly affected in the subjects with hamstring strain. Controversy exists regarding the most common site of strain injury (medial vs. lateral) in HAM muscles. In this study, most of the subjects had strain injury in the medial portion of the HAM muscles. Change in medial-lateral HAM muscle activation ratio has been previously reported in other musculoskeletal disorders including lumbo-pelvic and low back pain.33 The current data showed a significant difference in EMG activity of the GM between the athletes with and without history of HAM strain. GM provides powerful hip extension during sprinting. The hamstrings are thought to act as transducers of power. HAM muscle dysfunction followed by strain injury may cause the GM to be overactive. Both of these two actions may predispose an athlete to re-injury. Lumbo-pelvic dysfunction and disorders has been associated with HAM strain.34 Some investigators have shown an altered muscular activation pattern of the erector spinae, gluteal maximus, and hamstring muscles during PHE subjects with and without low back pain.21,24 Considering the association between HAM strain and lumbo-pelvic abnormality or dysfunction, the current findings are in accordance
with other studies showing alteration in muscular activity patterns in patients with low back pain.21,25,35 However, in this study, none of participants had low back pain. Subjects in the current study with HAM strain had non-statistically significant higher EMG activity of the IES, CES, and lateral HAM muscles during PHE compared with those without HAM injury (Table 2). However, the reason that no statistical differences were found between groups may be explained by the relatively small sample size. Therefore, it is essential to continue to investigate using a larger sample size in order to obtain the answers of the research questions more precisely. Additionally, in this study, the severity of strain injuries was mild and moderate and athletes with severe or acute HAM strain were not included in order to lessen the direct effects of pain as an important limiting factor. Some investigators stated that muscle dysfunction in subjects with musculoskeletal disorders might be related to pain, called “pain interference”.35-37 They believed that ability of voluntary contraction in all muscles during a movement is reduced because of the pain sensation. In this study, none of the subjects reported that pain was a limiting factor when producing hip extension. If a study is performed using athletes with severe injuries, muscular activity patterns may be significantly different between athletes with and without HAM strain injury due to muscle inhibition from pain or inflammation. The authors acknowledge several limitations. One of the limitations and a weakness of this study was the sample size. Subjects with severe and acute HAM strain were excluded in order to assess the muscle activity pattern in a more homogenous population. So, the accessible population, that is athletes with mild and moderate HAM strain injury and no other type of strain injury, was limited to a relatively small group of patients that were available during the time frame that this study was conducted. The authors’ suggest that this study could be repeated on subjects with different types and varied acuity of HAM strain to provide more insight regarding the muscular activity pattern in athletes with greater variety of HAM strain injury. It should also be noted that EMG measurements do not always guarantee the actual magnitude of force production or and objective measure of actual muscle
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strength.. In some cases, an inhibited muscle may work harder than a normal one in order to produce the required force for a particular task. Thus, the timing of the onset of muscle activity in addition to normalized EMG amplitude could provide additional useful information regarding the muscular activation pattern. CONCLUSION The results of this study indicate that there was statistically significantly greater normalized EMG activity of the medial HAM and GM in athletes with history of HAM strain injury compared to healthy subjects during the PHE test. REFERENCES 1. Bing Yu RMQ ANA, Yu Liu, Claude T. Moorman, William E. Garrett. Hamstring muscle kinematics and activation during overground sprinting. J Biomech. 2008;41:3121-3126. 2. Chumanov E TD. Hamstring strain injuries: recommendations for diagnosis, rehabilitation, and injury Prevention. J Orthop Sports Phys Ther. 2010;40(2):67-81. 3. Engebretsen A MG, Holme I, Engebretsen L, Bahr R. 2010;38(6):1147-1153. Intrinsic risk factors for hamstring injuries among male soccer players. Am J Sports Med. 2010;38(6):1147-1153. 4. Hoskins W PH. The management of hamstring injury--Part 1: Issues in diagnosis. Man Ther. 2005;10(2):96-107. 5. Hunter D SC. The assessment and management of chronic hamstring/posterior thigh pain Best Pract Res Clin Rheumatol. 2007;21(2):261-277. 6. Page P FC, Lardner R. Assessment and Treatment of muscle Imbalance. Human Kinetics. 2010. 7. Petersen J HP. Evidence based prevention of hamstring injuries in sport. Br J Sports Med. 2005;39(6):319-323. 8. Askling C ST, Thorstensson A. Type of acute hamstring strain affects flexibility, strength, and time to return to pre-injury level. Br J Sports Med. 2006;40(1):40-44. 9. Silder A TD, Heiderscheit BC. Effects of prior hamstring strain injury on strength, flexibility, and running mechanics. Clin Biomech. 2010;25:681-686. 10. Sahrmann. S. Diagnosis and treatment of movement impairment syndrome: 1th ed. St Louis: Mosby. 2002. 11. Sahrmann. S. Posture and muscle imbalance. Physiotherapy. 1992;78:13-20. 12. V. J. On the concept of postural muscles and posture in man. Aust J Physiother. 1983;29(3):83.
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