Función del isquiosural durante la extensión de cadera

8/13/2019 Funcin del isquiosural durante la extensin de cadera

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Research in Sports Medicine , 19:4252, 2011Copyright Taylor & Francis Group, LLCISSN: 1543-8627 print/1543-8635 onlineDOI: 10.1080/15438627.2011.535769

Hamstring Functions During Hip-Extension Exercise Assessed With Electromyography and Magnetic Resonance Imaging

TAKASHI ONO and AYAKO HIGASHIHARA Department of Sports Orthopedics, Faculty of Sports Sciences,

Graduate School of Waseda University, Saitama, Japan

TORU FUKUBAYASHI Faculty of Sport Sciences, Waseda University, Saitama, Japan

The purpose of this study was to compare the recruitment pat-terns in hamstring muscles during hip extension exercise by electromyography (EMG) and muscle functional magnetic reso-nance imaging (mfMRI). Six male volunteers performed 5 sets of 10 repetitions of the hip extension exercise. Electromyography (EMG) activity during the exercise was recorded for the biceps

femoris long head (BFlh), semitendinosus (ST), and semimembra-nosus (SM) muscles; mfMRI T2 values and cross-sectional areas (CSAs) of the same muscles were measured at rest, immediately after, 2 and 7 days after the exercise. The study found that EMG of the BFlh and SM were signicantly higher than that of the ST. Immediately after the exercise, the T2 value and CSA changes inthe SM showed a signicant increase. It was concluded that the BFlh and SM were selectively recruited during the hip extensionexercise.

KEYWORDS pennate muscles, eccentric contraction, recruitment pattern, muscle strain

Received 5 August 2009; accepted 17 May 2010. Address correspondence to Takashi Ono, Department of Sports Orthopedics, Faculty

of Sports Sciences, Graduate School of Waseda University, 2-579-15 Mikajima, Tokorozawa,

Saitama 359-1192, Japan. E-mail: [email protected]


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Hamstring Function During Hip Extension 43

INTRODUCTION

Hamstring muscles, which include the biceps femoris long head (BFlh),semitendinosus (ST), and semimembranosus (SM) muscles, form a multiar-

ticular muscle group that cross the hip and knee joints. These muscles worksynergistically to produce hip extension and / or knee exion torque. It hasbeen demonstrated, however, that each hamstring muscle has inherent mor-phological features (Friederich and Brand 1990; Woodley and Mercer 2005),leading to different functional properties even in the case of a single jointmovement. Previous studies with electromyography (EMG) have revealedthe activation patterns of individual hamstring muscles during knee exionmovement (Makihara et al. 2006; Mohamed et al. 2002; Onishi et al. 2002).These reports showed that the EMG activity of each hamstring muscle dur-ing maximum knee exion varied with the knee angle, and the differencemight be due to the muscle morphological features, such as muscle fasciclelength, pennation angle, and moment arm.

Despite these detailed investigations of the hamstring muscle functionsduring knee exion movement, there is little information about the functionsof these muscles during hip extension. Worrell et al. (2001) investigated therelationship between the hip angle and the EMG activity of the hamstringmuscle during isometric hip extension in the prone position and at vari-ous hip angle positions and found that the activity was constant at all hipangles. The hamstring muscles, however, were examined as a single func-tional group by a single pair of electrodes, and the individual muscle whoseactivity had been detected was not precisely identied. In addition, the func-tions of the hamstring muscles during hip extension while standing, that is,the movement involving bending forward / backward from the hip joint, wasnot investigated.

It is generally known that the hamstring muscles frequently are injuredduring various sports activities, such as football, rugby, and track and eldevents, and that most acute cases of hamstring strains involve the BFlh, whereas the ST and SM muscles are less often injured (Brooks et al. 2006; Woods et al. 2004). Most of the injuries occur during the late-swing phase

and stance phase of sprinting (Montgomery et al. 1994; Verrall et al. 2001),and during these phases, the hamstring muscles contract eccentrically todecelerate the forward swing of the leg and concentrically to push off theground. Thus, it seems to be important to investigate the activation patternsof the hamstring muscles during eccentric and concentric hip extension toclarify the mechanism underlying hamstring injury.

Recently, magnetic resonance imaging (MRI) has been used for quan-titative assessment of the activity and responses of the skeletal musclesduring exercise (Adams et al. 1992; Foley et al. 1999; Kinugasa, Kawakami,& Fukunaga 2006). The MRI transverse relaxation time (T2), which reects

the detailed changes in the intramuscular water content, has been observed


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to increase proportionally in activated muscles with an increase in exerciseintensity. Adams et al. (1992) showed that changes in the muscle functionalMRI signal correlated with the integrated EMG activity in the case of bothconcentric and eccentric contractions in the biceps brachii. Further, using

this technique, detailed information regarding the morphological changes inindividual muscles can be obtained by calculating the physiological cross-sectional areas (CSAs) following exercise. In our previous study (Kubotaet al. 2007), we showed that the degree of response during intensive eccen-tric knee exion exercise was not uniform among the hamstring muscles,and the ST muscle might respond sensitively as it is selectively recruiteddue to its anatomy. There are no reports, however, on the application of MRI for assessment of hamstring muscle function and adaptation during hipextension exercise.

The purpose of this study was, rst, to clarify the recruitment patterns of

each hamstring muscle during hip extension exercise by EMG and, second,to clarify the differences in the time-course changes in the MRI measure-ments, such as the T2 values and CSAs, after the exercise. We hypothesizedthat the recruitment patterns and responses of the individual hamstringmuscles during the hip extension exercise were different.

METHODS

Subjects

Six healthy male volunteers (age: 20.7 0.7 years, height: 174.3 1.9 cm, weight: 64.8 1.6 kg, mean SE, respectively) were recruited. The subjects were screened for medical and orthopedic conditions that would precludethem from the hip extension exercise or MRI procedures. Additionally, weexcluded individuals who had participated in a weight-training program orthose who performed rigorous lower extremity exercises on a regular basis within the past 1 year. This study was approved by the Human ResearchEthics Committee of the School of Sports Sciences of Waseda University and was conducted in accordance with their guidelines for human exper-

imentation. This study also conforms to the Declaration of Helsinki. Allsubjects provided written informed consent prior to participation and wereinstructed to avoid sports activities and refrain from using ice packs oranti-inammatory medications 1 week before and during the experiment.

Experimental DesignOne week before the experiment (exercise) day, all subjects underwentmfMRI of the right limb (dominant limb in all subjects) at rest. On the exper-iment (exercise) day, the subjects spent 1015 minutes warming up: they

spent a few minutes jogging on a treadmill in a voluntary speed and static


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stretching of lower extremity muscles. After warming up, the subjects wereprepared for EMG measurement (the skin was cleaned with a razor, sand-paper, and ethanol to reduce the skinelectrode impedance), and the EMG values during 5 seconds isometric maximal voluntary contraction (MVC) of

the hamstring muscles were collected with the subject in a prone position.Next, the subjects performed a session of eccentric / concentric hip exten-sion exercise. Immediately (within 5 minutes) after performing the exercisesessions as well as 2 and 7 days after the exercise, the subjects underwentmfMRI of the right limb.

Exercise ProtocolThe subjects underwent a session of hip extension exercises: these exer-cises are generally called Stiff-leg deadlift. The session consisted of 5 setsof 10 repetitions of the exercise. As an initial position, the subjects wereinstructed to stand upright with their feet shoulder-width apart, torso erect(chest out, scapulae in an adducted position), and grasp a bar loaded at60% of their body weight. With the weight hanging at arms length, the sub-jects were instructed to bend forward from the hip over a 2 sec count tosmoothly lower the weight maintaining the torso rigid throughout the hipexion. Hip exion continued until the trunk was approximately parallelto the oor. From this position, the subjects smoothly returned to the ini-tial position over a 2 sec count maintaining a rigid torso. This exercise was

properly performed maintaining a at trunk and bending from the hip toa position where the trunk was parallel to the oor and the knees, fully extended. There was a 1-min rest between each set of 10 repetitions during which the subjects rested in a standing position without hanging the weight.

MeasurementsELECTROMYOGRAPHY

Electromyographic activities in the right limb were recorded during the exer-

cise at a sampling rate of 1 kHz. The surface EMG was recorded from themidbellies of the BFlh, ST, and SM muscles with bipolar surface electrodes(ME6000, Mega Electronics Ltd, Finland) with an interelectrode distance of 30mm. The positions of the surface electrodes were determined by palpation of each muscle belly during isometric contraction. The skin was cleaned with arazor, sandpaper, and ethanol to reduce the skinelectrode impedance. Thedigital hip joint exion angle signal was recorded using a digital goniometer(NIHON MEDIX Co., Ltd, Japan). The digital EMG signals were full-waverectied and integrated (iEMG) over each period of eccentric and concentriccontraction (10 repetitions 5 sets = 50 for each muscle in total), which was

determined by the digital signal markers recorded with the EMG signals. The


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iEMG values were normalized with the iEMG values collected during a 5-secisometric maximal voluntary contraction (MVC) for each subject (NiEMG =iEMG/ MVC (%)).

MUSCLE FUNCTIONAL MAGNETIC RESONANCE IMAGING

The T2 value in the MRI was measured to evaluate the degree of musclerecruitment during the exercise. All the MRI scans of the participants thighs were obtained using a 1.5-T MR imaging system with a body coil (SignaEXCITE XI ver. 11.0; GE Yokogawa Medical Systems, Japan). The subjects were placed in the supine position with their knees fully extended. TransverseT2-weighted spin echo images were subsequently obtained with the followingparameters: repetition time = 3000 ms, echo times (TEs) = 25, 50, 75, and100 ms, matrix = 160 256, eld of view = 260 mm, slice thickness = 10 mm,and interslice gap = 10 mm. The MRI data were evaluated for the T2 relaxationtime (T2 value) and the muscle volume of the hamstring muscles. The MR images were transferred to a personal computer in the digital imaging andcommunications in medicine (DICOM) le format. An image manipulationandanalysis software (OSIRIS: University Hospital of Geneva, Switzerland) wasused to measure the signal intensity (SI) and CSAs of each hamstring muscle(BFlh, ST, and SM). The region of interest was dened by tracing the muscleoutline, taking care to avoid visible aponeurosis, vessels, fat, membranes,and the femur. The same examiner performed these tracings throughout theexperiment at 5 levels within the muscles, namely, at 30, 40, 50, 60, and 70% of the thigh length from the upper border of the ischial tuberosity (0%) relativeto the lower border of the tibial plateau (100%). The SI was measured fromthe same region for all 4 TEs. A T2 measurement sequence with 4 TEs wasapplied to measure the absolute T2 value. Images taken at different TEs weretted to a monoexponential time curve to extract the T2 values based on theformula: SI = M 0 exp (TE/ T2), where SI represents the signal intensity at a given TE and M0 is the original MRI signal intensity. The same personperformed the MRI scan and the T2 calculation. The time-course changes inthe T2 values for each muscle were evaluated using the average values of

all 5 levels (T2 mean value), and the muscle volumes were evaluated usingthe sum total of the CSA values of all the 5 levels. For comparison purposes,the average T2 mean value and the volume of each muscle were computedas the percentage change relative to the value measured at the pre-exercisestage.

Statistical Analysis All statistical analyses were conducted using a statistical analysis softwareprogram (SPSS ver. 14.0; SPSS, Japan, Tokyo, Japan). All the descriptive

data, namely, the NiEMG, T2 value, and muscle volume were expressed


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as mean standard error (SE), and the differences between the values inthe case of each muscle (NiEMG, T2 value) and the differences over thesubsequent days (T2 value and muscle volume) were evaluated using one- way analysis of variance (ANOVA) with repeated measures. If the differences

were signicant by ANOVA, Bonferronis post-hoc test was performed. Thelevel of signicance was set at P < 0.05.

RESULTS

NiEMG values during the exercise are shown in Figure 1. During the eccen-tric phases, the NiEMG values of the BFlh and SM muscles were signicantly higher than that in the case of the ST muscle ( P < 0.01), and the activity of the SM muscle was also higher than that of the BFlh muscle ( P < 0.01).During the concentric phases, the activity of the BFlh and SM muscles werestill signicantly higher than that of the ST muscle ( P < 0.01), but no sig-nicant difference was observed between BFlh and SM muscle activities.

Typical T2-weighted MR images of the right thigh before and after theexercise are shown in Figure 2. Figure 3 presents changes in average T2 values of each muscle as a function of time. The averaged T2 mean valueimmediately after evaluation increased only in the case of the SM muscle(12.5% 1.9%, P < 0.05) and no signicant change was identied in thecase of the other muscles. There was no signicant change in any muscle at

2 and 7 d after the exercise.Figure 4 displays the time course of the changes in the CSAs of eachmuscle. Immediately after the exercise no signicant change was detected

0

5

10

15

20

25

30

35

40

45

50

concentriceccentric

N i E M G ( %

M V C )

BFlh ST SM

*

* *

FIGURE 1 NiEMG activities in eccentric and concentric phases of hip-extension exercise. Values are means SE; P < 0.01 vs ST, P < 0.01 vs the other muscles; BFlh, biceps femoris

long head; ST , semitendinosus; SM , semimembranosus.


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2D 7D

BFlhST

SM

PRE POST

FIGURE 2 T2-weighted magnetic resonance images (TR = 3000 ms, TE = 25 ms) of themiddle region (50% of the thigh length) of the thigh at rest (PRE), immediately after (POST),and 2 (2D) and 7 (7D) days after the exercise. Images were obtained from 1 representativesubject. BFlh, biceps femoris long head; ST , semitendinosus; SM , semimembranosus.

2

0

2

4

6

8

10

12

14

16

7D2DPOST

P e r c e n

t a g e c h a n g e o

f T 2 ( % P R E )

BFlh ST SM

FIGURE 3 Average change in the T2 value of each muscle with time. Values are thepercentage change compared with the value at rest (PRE, at rest); P < 0.05 vs PRE.

in any muscle, but 2 and 7 d after the exercise, a signicant increase wasidentied only in the case of the SM muscle (28.5% 11.2%; 26.7% 7.7%,respectively; P < 0.05), and no signicant change was identied in the other

muscles.


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5

0

5

10

15

20

25

30

35

40

45

7D2DPOST P e r c e n

t a g e c h a n g e o

f C S A

s ( % P R E )

BFlh ST SM

FIGURE 4 Average change in the CSAs of each muscle with time. Values are the percentagechange compared with the value at rest (PRE, at rest); P < 0.05 vs PRE.

DISCUSSION

In this study, we examined the recruitment patterns of each hamstring mus-cle during a hip extension exercise and the difference in the time-coursechanges of the MRI measurements after the exercise. The NiEMG values of the BFlh and SM muscles were signicantly higher than those in the case of the ST muscle during both the eccentric and concentric phases. This resultsuggested that the recruitment patterns of each hamstring muscle during hipextension were not uniform among the hamstring muscles, and the BFlhand SM muscles were selectively recruited to a greater extent. Immediately after the exercise, the T2 mean value increased, especially in the case of the SM muscle. As Kinugasa and Akima (2005) reported, the MRI signal cor-related with EMG activity during repetitive exercise, and the relationships were associated with both neuromuscular and metabolic factors during theexercise. Hence, the T2 increase in the present study is in accordance with

the EMG data, and it supports this data from the metabolic viewpoint in vivo.In our previous study (Kubota et al. 2007), we have shown that theST muscle might respond sensitively to eccentric knee exion load. Therationale behind the selective recruitment of this muscle was that the mor-phological property of this muscle is such that it can effectively deal withthe strain during this type of exercise. The ST muscle possesses long berscontaining many sarcomeres in series, illustrating its notable potential tocontract quickly over large distances (Heron and Richmond 1993). In con-trast, during the hip extension exercise, the degree of activation was higherin the case of the BFlh and SM muscles than in the case of the ST muscle

in both the eccentric and concentric phases. The BFlh and SM muscles are


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50 T. Ono et al.

pennate muscles, which have large CSAs and are more suitable for torqueproduction than fusiform muscles are (Koulouris and Connell 2005; Lieberand Friden 2000; Woodley and Mercer 2005). Architecturally, these 2 musclesoriginate from the ischial tuberosity and control the movement of the pelvis

and torso. Furthermore, the architecture of the SM muscle is unique. The SMmuscle possesses the longest proximal tendon of all the hamstring muscles, which originates beneath the common tendon of the BFlh and ST mus-cles. The belly of the SM muscle overlaps that of the ST muscle, and thismuscle inserts into the medial tibial condyle as a distal tendon. Thus, theSM muscle has a relatively small moment arm at the hip joint and a largemoment arm at the knee joint. On the basis of those morphological andarchitectural properties, our nding suggested that the BFlh and SM musclesare selectively recruited in order to deal with the hip joint movements duringstanding, bending forward, and extending backward from the hip, as these

movements demand a high muscle torque.The CSAs values revealed that the SM muscle exhibited a conspicuous

response following hip extension exercise, and it was assumed that this mus-cle was recruited and stimulated during repetitive eccentric and concentrichip extension exercise. There were no signicant changes, however, in theT2 values in any muscles 2 and 7 days after the exercise, which indicatedthat there was no muscle damage. To explain this result, i.e., the unchangedT2 values, it was assumed that the activities of the hamstring muscles duringthe exercise were not so high relative to those during MVC, especially duringthe eccentric phase; even the highest values in the case of the SM muscle were approximately 30% of the MVC value.

From the results of this study and our previous study (Kubota et al. 2007;Ono, Okuwaki, & Fukubayashi 2010), we found that each hamstring musclefunction during hip extension and knee exion movement was different andthe BFlh and SM muscles were selectively recruited in order to deal withthe hip joint movements during standing, bending forward, and extendingbackward from the hip. In contrast, it is generally known that most acutehamstring strains involve the BFlh, whereas the ST and SM muscles areless often injured (Brooks et al. 2006; Woods et al. 2004) and most of the

injuries occur during the late-swing phase and stance phase of sprinting(Montgomery et al. 1994; Verrall et al. 2001) during which the hamstringmuscles contract eccentrically to decelerate the forward swing of the legand concentrically to push off the ground. In light of these considerations, we suggest that most of the acute cases of hamstring strains that involve theBFlh would happen during the stance phase of sprinting during which thehamstring muscles contract concentrically to push off the ground, producinghip extension torque. Further studies should clarify the activation pattern of each hamstring muscle and kinematics in sprinting on the ground, and if it was claried, we could understand the mechanism of hamstring muscle

strain injuries and more practical training to prevent them.


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This study had several limitations, the rst of which was a small sampleof untrained subjects. This means that the results cannot necessarily be gen-eralized, and further studies of athletes are required to determine whetherthese results would still stand. Another limitation was that we did not con-

trol strictly the involvement of any other muscles except hamstrings for hipextension movement. In this study, we examined the activation pattern of each of the hamstring muscles during hip extension exercise. Rather thanuse an external xation device, extraneous trunk and / or lower leg move-ment was controlled by instructing subjects to maintain the torso rigid andthe knee extended throughout the hip exion.

In conclusion, the activation pattern of each of the hamstring muscles isdifferent, and the BFlh and SM muscles are selectively recruited during hipextension exercise. The difference in activation patterns might be due to themorphological and functional properties of these muscles. Thus, the BFlh

and SM muscles are recruited since hip joint movement during standing,bending forward, and extending backward from the hip demands a highmuscle torque production.

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Función del isquiosural durante la extensión de cadera