nonuniform changes in mri measurements of the thigh muscles after two hamstring strengthening...

TITLE

Non-uniform changes in MRI measurements of the thigh muscles following two hamstring strengthening exercises

Authors:

Jurdan Mendiguchia1, Mirian Aranzazu Garrues2, John Barry Cronin3,4, Bret Contreras3, Asier Los Arcos5, Nikos Malliaropoulos6, Nicola Maffulli7, Fernando Idoate8.

1. Zentrum rehab and performance Center.Department of Physical Therapy.Pamplona, Spain.

2. Public University of Navarre, Health Science Department .Graduate School for Health Sciences, Physical Therapy School, Tudela, Spain.

3. Sport Performance Research Institute New Zealand, AUT University, Auckland, New Zealand

4. School of Biomedical and Health Sciences, Edith Cowan University, Joondalup, Australia.

5. Club Atletico Osasuna.Pamplona. Spain.6. National Track & Field Centre, Sports Medicine Clinic of S.E.G.A.S., Thessaloniki,

Greece 7. The London School of Medicine and Dentistry Institute of Health Sciences

Education Centre for Sports and Exercise Medicine Mile End Hospital.8. Radiology Department, Clinica San Miguel, Pamplona, Spain

Corresponding Author:Jurdan Mendiguchia1

Zentrum rehab and performance CenterCalle B Nº 23Department of Physical TherapyPamplona, [email protected] 948229459

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Competing Interest

“ None to declare."

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Abstract

This study investigated the effects of the eccentric leg curl (LC) and lunge (L) on the

biceps femoris (BF), semitendinosus (ST), semimembranosus (SM), adductor magnus

(AM) and gluteus maximus (GM). Each leg of eleven male professional soccer

players were randomly assigned to an eccentric leg curl (LC) or lunge (L) exercise

protocol (3 sets of 6 repetitions). Functional magnetic resonance imaging (fMRI) of the

subjects’ thighs were performed before and 48 hours after the intervention. Fifteen

axial scans of the thigh interspaced by a distance of 1 / 15 of the length of the right

femur (Lf) were obtained from the level of 1/15 Lf to 15/15 Lf . The fMRI data were

analyzed for signal intensity (SI) changes. While no significant changes were observed

in absolute short tau inversion recovery (STIR) values for the semimembranosus and

gluteus maximus, significant changes for the semitendinosus (~21-45%) from sections 4

to 10, adductor magnus (~2-13%) at section 4, and biceps femoris (~ -3 vs 8%) at

section 7 were noted. These two hamstring exercises did not result in a uniform

response (training stimulus) for the same muscles and regions. The ELC exercise was

better suited for loading all regions of the ST muscle, while the L exercise was more

effective for loading the proximal regions of biceps femoris and adductor magnus.

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Introduction

Acute hamstring injuries are the most prevalent muscle injuries reported in sport,

accounting for 6 to 37% of all injuries in Australian Rules football, rugby union,

football, basketball, cricket and track sprinters. [1-8] Appropriate training and

strengthening of the hamstring muscles for many sports is a fundamental focus of

prevention and rehabilitation. Although selective strengthening of the hamstring

muscles has been recommended as a key component in the management of hamstring

injury, [9-13] only limited literature exists to guide clinicians in designing effective

strengthening programs.

The architectures and innervation patterns of the various muscles in the posterior aspect

of the thigh (the biceps femoris muscle long head (BFl), the biceps femoris short head

(BFs), the semimembranosus (SM), and semitendinosus (ST)) differ [14-16], and each

muscle has unique inherent functions. If this were indeed the case, it would be of value

to strength and conditioning coaches as well as clinicians to understand which exercises

preferentially activate different muscle groups, so as programming is guided to better

effect.

Functional magnetic resonance imaging (fMRI) may be a sensitive method for

displaying the physiological changes that occur in muscles activated during exercise, as

it provides detailed anatomical analysis of associated soft tissues, which is lacking in

electromyography (EMG) experiments.[17-22] The short tau inversion recovery (STIR)

sequence is a T2-weighted sequence that suppresses signals from fat and displays

sensitivity in enhancing differences between the water content of tissues. [19-22].

Exercise produces changes in the distribution of water both intra- and inter-cellularly.

The STIR sequence has previously shown to be valuable in the investigation of signal

intensity (SI) changes in muscles after exercise. [19-22]

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MRI has also been used to assess muscle damage following intensive exercise. [23,24]

The T2 value increased following eccentric exercise [18,25-30], and was positively

correlated with plasma creatine kinase (CK) activity, reflecting exercise-induced muscle

damage.[18,23,26,31] Furthermore, previous studies have investigated the intermuscle

differences and intramuscle regional differences of the T2 value between proximal and

distal regions of the muscles of interest. [18,29,32] For example, Kubota et al. [18]

reported that although all hamstring muscles and regions displayed a T2 increase

immediately following eccentric knee-flexion exercise (prone leg-curl machine), the

relationship between the changes of the plasma CK activity and the T2 value of the ST

was not statistically significant until the second day following exercise , which may be

indicative of severe localised muscle damage. These findings have interesting

implications in terms of the time course and effects of different exercises on the

hamstrings.

Some exercises are used to prevent hamstring injuries in elite athletes, [9,11-13]

but fMRI to our knowledge, has not been used to date to investigate muscle damage and

intermuscle and intramuscle regional differences in STIR values. This study assessed SI

changes in the upper thigh muscles using fMRI at 48 hours following a lunge and

eccentric leg curl exercises.

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Materials and Methods

Subjects

Eleven male professional soccer players participated in this study. Participants were

excluded if they had an injury to their legs or back in the preceding 12 months or if they

were unsuitable for fMRI because of foreign metal bodies, electronic implants or

claustrophobia. Before the start of the investigation, each participant’s height, weight,

age, regular exercise program and any previous injuries to the legs were recorded (see

Table 1). Subjects were instructed to avoid strength training activities

for the lower legs and not to use icing or anti-inflammatory

medication for the week preceding and the week of the experiment.

Our institutional Ethics Committee approved the study and all participants gave

informed consent to participate in the study.

Insert Table 1 about here

GENERAL INITIAL CHARACTERISTICS

n MEAN SDHEIGHT(m) 11 1.80 0.05

WEIGHT(kg) 11 74.6 4.5

AGE(years) 11 22.1 1.8

Table 1: Initial characteristics of subjects.

Procedures

The left and right legs of the subjects were randomly assigned to an eccentric leg curl

(LC) or lunge (L) exercise protocol. The protocol involved 3 sets of 6 repetitions

with at least a two-minute rest between sets. Following the

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completion of the exercise protocol for one leg (e.g LC), a two

minutes rest was taken before starting the second exercise (e.g. L) for

the other leg.

Exercise Protocol

For the L exercise, subjects were instructed to step forward a predetermined distance

marked on the floor whilst the trunk remained upright. The length of the step was

standardized for each subject and was equal to the distance from the greater trochanter

to the floor as measured with the subject standing. This normalized distance was chosen

based on pilot testing, in which a comfortable L step length was determined. Subjects

were asked to lower their trunk by flexing their lead and trailing knees simultaneously

to a point where the trail knee was approximately 2 to 3 cm short of contacting the

ground. The lunge was completed when the subjects returned to the starting position.

For the ELC exercise, subjects performed eccentric hamstring curls (Prone Leg Curl

Technogym, Italy) at 120% of their one repetition maximum (1RM). The ELC 1RM

was quantified via a typical incremental load to failure protocol. Once the subject could

not complete two concentric leg curls at the set load this was determined as their 1RM

to which a 20% load, which resulted in the 120% 1RM eccentric load. Subjects were

instructed to lower the weight from a knee-flexed position (100°) to a knee-extended

position (0°) in 3 seconds, maintaining a constant lowering velocity. The subjects kept

their ankle plantar flexed to reduce the contribution of the gastrocnemius muscle.

Subjects were verbally encouraged to exert maximal force at the starting position and to

resist maximally against the knee-extending action throughout the range of motion. The

weight was raised after each eccentric repetition by an examiner, thereby rendering the

exercise an eccentric-only task for the subject.

Imaging Technique

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MR imaging was performed using a 1 T whole body imager (Magnetom Impact Expert;

Siemens-Erlangen, Germany), with the subjects supine with their knee extended

immediately before and 48 hours after the exercise. Once the subject was positioned

inside the magnet, the thighs of both legs were kept parallel to the MRI table and the

feet were strapped together to prevent rotation. The length of the right femur (Lf), taken

as the distance from the intercondylar notch of the femur to the superior boundary of the

femoral head, was measured in the coronal plane.

Subsequently, 15 axial scans of the thigh interspaced by a distance of 1 / 15 Lf were

obtained from the level of 1/15 Lf to 15/15 Lf . Every image obtained was labelled at its

location (i.e. slice 4 being closer to the coxofemoral joint and slice 12 closer to the

knee). Great care was taken to reproduce the same individual Lf each time by using the

appropriate anatomical landmarks [33] For the final calculation of the signal intensity

of each muscle, slices 4 / 15 – 12 / 15 were used for all muscles examined; the two

cranial slices (closer to the hip) and the three distal slices (closer to the knee) were

discarded given the presence of image artifacts. Then fast STIR MR axial images

[repetition time (TR) = 5,300 ms, echo time (TE) = 60ms, inversion time (TI) 115 ms,

flip angle (FA): 180] were collected using a 256 x 256 image matrix, with a 350 mm

field of view and 10-mm slice thickness using a body coil.

The MRI data were evaluated for SI of each hamstring muscle (BF, ST and SM),

adductor magnus (AM) and gluteus maximus (GM). The MR images were transferred to

a personal computer in the Digital Imaging and Communications in Medicine (DICOM)

format and analysed using image manipulation and analysis software (OSIRIX,

University Hospital of Geneva, Switzerland). Individual baseline SI readings, analysed

with a standardized radius of interest (ROI), were established with the preliminary scan

for each participant. The ROI was placed in the same position within the muscle for

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each measurement, avoiding blood vessels and bone, which may have affected the

analysis of the intensity changes. The SI was measured in a circular region of interest

(ROI, 10-30 mm2) within each muscle assessed before and after exercise and a

percentage difference was calculated. The same technician (FIS) performed the MR

imaging scan and the SI measures.

Statistical Analysis

The STIR absolute values were reported as mean ± SD. Given the differences between

exercises utilized in this study, the principal comparison of interest was the within

exercise pre-post changes in absolute values of STIR of the muscles (BF, SM, ST, AM

and GM) for all the different sections (3, 4, 5, 6, 7, 8, 9, 10,11 and 12). To disentangle

the main effects a two factor (time x section) repeated measures ANOVA with post hoc

contrasts was used to determine significant differences between sections. Paired t-tests

were used to determine significant pre-post exercise changes in L and ELC and for the

relative change between the ELC and L exercises. Statistical significance was set at p <

0.05.

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Results

Typical STIR of the right (ELC) and left (L) before and after exercise can be observed

in Figure 1. No statistical differences (p < 0.05) were found in any muscle or section

between left and right legs in the pre-exercise MRI’s. The changes in absolute values

pre and post exercise of the different muscles (BF, SM, ST, AM and GM) and sections

3 to 12 for the ELC and L exercises can be observed in Table 2. The following is a

summary of the main findings from these tables.

Insert Figure 1 about here.

Insert Table 2 about here.

STIR Absolute Values for ELC and L before and after exerciseELC L

ANOVA RM p

Muscle and Section

TIME n Mean +SDT-

TESTp

Muscle and Section

TIME n Mean +SDT-

TEST P

ST4 Before 11 128.09 15.33 0.048 ST4 Before 11 133.4 13.0 0.718 0.033After 11 189.00 89.37 After 11 131.00 14.3

ST5 Before 11 134.45 10.71 0.021 ST5 Before 11 132.3 12.3 0.068 0.019After 11 267.36 165.25 After 11 139.9 13.4

ST6 Before 11 146.27 20.70 0.005 ST6 Before 11 132.00 15.1 0.057 0.004After 11 342,45 186,45 After 11 143.7 18.0

ST7 Before 11 135,91 18,66 0,007 ST7 Before 11 126.3 15.9 0.085 0.005After 11 321,45 183,13 After 11 136.3 16.4




BF7 Before 11 157,27 45,35 0,260 BF7 Before 11 147.3 40.2 0.110 0.048After 11 152,00 41,05 After 11 162.1 43.6

AM4 Before 10 137,10 8,69 0,047 AM4 Before 9 142.1 9.9 0.042 0.152After 10 145,10 9,71 After 9 164.2 23.5


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Table 2: STIR absolute values of muscles before and after exercise. ST= semitendinosus, BF = biceps femoris, AM= adductor magnus. The number after the muscle represents the section. ELC= eccentric leg curl. L =Eccentric Lunge, RM= repeated measures. Significant differences are marked in cursive.

For the semitendinosus, significant changes (~21-45%, Table 2) in the STIR values for

the ELC exercise were noted along the length of the ST belly from sections 4 to 10 (see

Figure 2A); whereas only section 8 was found to differ significantly (p<0.028) from

pre-testing for the L exercise (see Figure 2B). In terms of the adductor magnus,

significant changes were observed for the L exercise proximally (sections 4 to 7,

Figures 3A) (~2-13%) whereas a significant increase in STIR was only found for

section 4 for the ELC exercise (See Figure 3B).

Insert Figure 2A-2B, 3A-3B.

In terms of biceps femoris, significant differences (p=0,048, see figure 4A and 4B) were

found post exercise for the ELC and L exercise at section 7 (~ -3 vs 8%). No significant

changes were observed in absolute STIR values for the semimembranosus and gluteus

maximus.

Insert Figure 4A and 4B about here.

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Discussion

This study measured whether the hamstring muscles responded in a uniform manner to

two different exercises, as quantified by the absolute changes in the STIR values of

fMRI. It has been assumed previously that during hamstring strengthening exercises,

individual hamstring muscles are activated in a similar manner. However, this is not the

case, as we observed that each hamstring muscle responded differently during the L and

ECL exercises respectively. The mechanics of the exercises used in this investigation

differ in many ways: 1) the ELC is an open kinetic chain exercise with differences in

hip flexion and tibial rotation [34,35] compared to the L which is a closed kinetic chain

exercise;[36,37] 2) the ELC is principally a monoarticular exercise, whereas the L is

biarticular; 3) as a result, the moments around the joints as well as the

length-tension/torque angle relationship of individual muscles will differ; 4) there is no

concentric component in the ELC which is not the case for the L; and, 5) the ELC is

supramaximally loaded at 120% 1RM which is not the case for the L. Given these

differences, it is difficult to ascertain whether a given exercise is ‘superior’ to the other,

and we shall focus on the site specific activation of each exercise and how each exercise

may be used for the conditioning of the hamstring muscle group.

With regards to the ST, it appears that the greatest changes in the MRI measurements

followed the ELC loading, in agreement with previous research. [18,38] The changes

in fMRI measurements of the ST may relate to its architectural characteristics as it has

the longest fascicle length and smallest physiological cross-sectional area (PSCA) of the

hamstring muscles [16], and it is a fusiform muscle compared with more pennate BF

and SM muscles. Muscles containing long fascicles produce forces over large length

ranges and at high shortening speeds, because they have a large number of

simultaneously contracting, serially arranged sarcomeres. [39] Such morphological

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properties of ST may be selectively used to perform eccentric knee flexion more

efficiently.

The region-specific activation within the proximal, middle and distal regions of the

same muscle found in this study were in contrast to the Kubota et al. [18] findings,

where significant differences between proximal and distal regions were detected. This

was explained by the fact that the ST is the only hamstring muscle that was

anatomically partitioned as defined by its architecture and innervation [16]. In addition,

this division into partitions was augmented by the presence of a tendinous inscription

with each partition receiving innervation from one muscle nerve, or from a primary

branch of the nerve [16]. The differences between ours and Kubota et al.’s findings [18]

could be attributed to methodological differences, as we divided the thigh into fifteen

regions while they only divided the thigh into three regions. Only in one instance did

one section (Section 8) of the ST show changes after the lunge exercise.

In the AM, significant changes (section 4,~12%; section 5, ~19%; section 6, ~22%; and

section 7, ~14%s) were observed for the L exercise proximally (sections 4 to 7), as

compared to section 4 ( 5%) for the ELC exercise. The greater evidence of

intramuscular changed of the AM during lunges may result from greater hip extension

moments when the hip is flexed. The large hip extension moment arm in addition to

adduction has been noted previously for this muscle. [40,41] The lesser involvement of

the AM during the ELC may be due to a fixed hip angle position (15º) during the

exercise.

No significant changes in fMRI were observed for the BF after ECL loading. In

contrast, significant absolute changes in STIR values were observed at one region

(Section 7) for the BF after L loading. As T2 values are more sensitive to eccentric

exercise [18,25-30] compared to concentric exercise[26] this study may support

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previous findings where a very short and rapid period of eccentric hamstring contraction

during the forward lunge has been documented .[36,37] Hamstring length depends on

both knee and hip joint angles since the hamstrings are biarticular muslces. The angle of

the hip has more impact on the length of the biceps femoris than the angle of the knee,

[42,43] given the longer moment arm at the hip, and this relationship increases with

increasing knee angle. Hip flexion-extension exercise resulted in greater BF activation

as measured by MRI compared with a hip fixed exercise .[18,38] Given this

information and based on muscle mechanics and physiology, greater BF damage during

lunges may arise from larger internal hip extension moments when the hip is flexed.

It is difficult to ascertain which variables differ between exercises to produce site

specific activation differences. However, greater proximal activation (section 5, 23%;

section 6, 10%; section 7, 8%; and section 8, 7%) is present after the L exercise ( see

figure 3) while minimal or negative changes after ELC exercise (section 5, 11%; section

6, -3%; section 7, -3%; and section 8, -4%) are evident. It is possible that exercise

intensity accounts for the finding that only one region showed significant changes for

the BF. Exercise-induced changes in fMRI vary according to exercise intensity:

previous studies have reported greater SI changes after maximal loads compared to

lower loads. [19,21,22,44-46] To better define this load effect, more research is needed

investigating whether a loaded lunge produces greater changes across the proximal BF

in comparison to the bodyweight lunge.

This study used fMRI to assess the relative damage to lower leg muscles after two

different exercises. Different exercises can increase hamstring strength, [11,47] but

various hamstring exercises do not result in a uniform response, and therefore training

stimulus, for the same muscles and the same regions of the muscles. Because hamstring

strains affect different hamstring muscles, proper exercise selection is crucial to target

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the desired muscle/s. When the goal of a therapeutic intervention is to specifically

strengthen the ST, AM, and/or BF, a progressive resistive training program that

incorporates ELC or L is indicated, as these exercises selectively and effectively

activate the aforementioned muscles. In conclusion, the present study demonstrates that

the ELC exercise is better suited for loading all regions of ST muscle and the L exercise

is more effective for loading the proximal regions of biceps femoris and adductor

magnus.

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References

1. Garrett WE Jr.Muscle strain injuries. Am J Sports Med. 1996: 24(6 Suppl): S2-

8. Garrett WE Jr. Am J Sports Med. 1996;24(6 Suppl):S2-8.

2. Woods C, Hawkins RD, Maltby S, et al. The Football Association Medical

Research Programme: an audit of injuries in professional football--analysis of

hamstring injuries. Br J Sports Med. 2004: 38(1): 36-41.

3. Orchard J, Seward H. Epidemiology of injuries in the Australian Football

League, seasons 1997-2000. Br J Sports Med. 2002: 36(1): 39-44.

4. Meeuwisse WH, Sellmer R, Hagel BE. Rates and risks of injury during

intercollegiate basketball. Am J Sports Med. 2003: 31(3): 379-85.

5. Croisier JL. Factors associated with recurrent hamstring injuries. Sports Med.

2004: 34(10): 681-95.

6. Brooks JH, Fuller CW, Kemp SP, et al. Epidemiology of injuries in English

professional rugby union: part 1 match injuries. Br J Sports Med. 2005: 39(10):

757-66.

7. Brooks JH, Fuller CW, Kemp SP, et al. Epidemiology of injuries in English

professional rugby union: part 2 training Injuries. Br J Sports Med. 2005:

39(10): 767-75.

8. Ekstrand J, Hägglund M, Waldén M.Epidemiology of Muscle Injuries in

Professional Football (Soccer). Am J Sports Med. Published online first:

February 18, 2011.

9. Askling C, Karlsson J, Thorstensson A. Hamstring injury occurrence in elite

soccer players after preseason strength training with eccentric overload. Scand J

Med Sci Sports. 2003;13(4):244-50.

16

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323

324

325

326

327

328

329

330

331

332

333

334

335

336

337

338

339

340

341

16

10. Croisier JL, Ganteaume S, Binet J, Genty M, Ferret JM .Strength imbalances

and prevention of hamstring injury in professional soccer players: a prospective

study. Am J Sports Med. 2008; 36(8):1469-75.

11. Jönhagen S, Ackermann P, Saartok T.J. Forward lunge: a training study of

eccentric exercises of the lower limbs. Strength Cond Res. 2009;23(3):972-8.

12. Holcomb WR, Rubley MD, Lee HJ, Guadagnoli MA. Effect of hamstring-

emphasized resistance training on hamstring:quadriceps strength ratios. J

Strength Cond Res. 2007; 21(1):41-7.

13. Mjølsnes R, Arnason A, Østhagen T, Raastad T, Bahr R. A 10-week randomized

trial comparing eccentric vs. concentric hamstring strength training in well-

trained soccer players. Scand J Med Sci Sports. 2004 ;14(5):311-7.

14. Friederich JA, Brand RA .Muscle fiber architecture in the human lower limb. J

Biomech. 1990;23(1):91-5.

15. Wickiewicz TL, Roy RR, Powell PL, Edgerton VR. Muscle architecture of the

human lower limb. Clin Orthop Relat Res. 1983 ;(179):275-83.

16. Woodley SJ, Mercer SR. Hamstring muscles: architecture and innervation. Cells

Tissues Organs. 2005;179(3):125-41.

17. Kubota J, Ono T, Araki M, Tawara N, Torii S, Okuwaki T, Fukubayashi T.

Relationship between the MRI and EMG measurements. Int J Sports Med.

2009 ;30(7):533-7.

18. Kubota J, Ono T, Araki M, Torii S, Okuwaki T, Fukubayashi T Non-uniform

changes in magnetic resonance measurements of the semitendinosus muscle

following intensive eccentric exercise. Eur J Appl Physiol. 2007 ;101(6):713-20.

17

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346

347

348

349

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352

353

354

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356

357

358

359

360

361

362

363

364

17

19. Horrigan JM, Shellock FG, Mink JH, Deutsch AL. Magnetic resonance imaging

evaluation of muscle usage associated with three exercises for rotator cuff

rehabilitation. Med Sci Sports Exerc. 1999;31(10):1361-6.

20. Takeda Y, Kashiwaguchi S, Endo K, Matsuura T, Sasa T. The most effective

exercise for strengthening the supraspinatus muscle: evaluation by magnetic

resonance imaging. Am J Sports Med. 2002;30(3):374-81.

21. Green RA, Wilson DJ. A pilot study using magnetic resonance imaging to

determine the pattern of muscle group recruitment by rowers with different

levels of experience. Skeletal Radiol. 2000;29(4):196-203.

22. Baczkowski K, Marks P, Silberstein M, Schneider-Kolsky ME. A new look into

kicking a football: an investigation of muscle activity using MRI. Australas

Radiol. 2006;50(4):324-9.

23. LeBlanc AD, Jaweed M, Evans H. Evaluation of muscle injury using magnetic

resonance imaging. Clin J Sport Med. 1993;3(1):26-30.

24. Chen YW, Hubal MJ, Hoffman EP, Thompson PD, Clarkson PM. Molecular

responses of human muscle to eccentric exercise. J Appl Physiol.

2003 ;95(6):2485-94.

25. Jayaraman RC, Reid RW, Foley JM, Prior BM, Dudley GA, Weingand KW,

Meyer RA. MRI evaluation of topical heat and static stretching as therapeutic

modalities for the treatment of eccentric exercise-induced muscle damage. Eur J

Appl Physiol. 2004;93(1-2):30-8.

26. Larsen RG, Ringgaard S, Overgaard K. Localization and quantification of

muscle damage by magnetic resonance imaging following step exercise in young

women. Scand J Med Sci Sports. 2007;17(1):76-83.

18

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387

388

18

27. Prior BM, Jayaraman RC, Reid RW, Cooper TG, Foley JM, Dudley GA, Meyer

RA. Biarticular and monoarticular muscle activation and injury in human

quadriceps muscle. Eur J Appl Physiol. 2001;85(1-2):185-90.

28. Yanagisawa O, Niitsu M, Takahashi H, Itai Y. Magnetic resonance imaging of

the rotator cuff muscles after baseball pitching. J Sports Med Phys Fitness.

2003 ;43(4):493-9.

29. Segal RL, Song AW. Nonuniform activity of human calf muscles during an

exercise task. Arch Phys Med Rehabil. 2005;86(10):2013-7.

30. Sesto ME, Radwin RG, Block WF, Best TM. Anatomical and mechanical

changes following repetitive eccentric exertions. Clin Biomech (Bristol, Avon).

2005 Jan;20(1):41-9.

31. Schwane JA, Buckley RT, Dipaolo DP, Atkinson MA, Shepherd JR. Plasma

creatine kinase responses of 18- to 30-yr-old African-American men to eccentric

exercise. Med Sci Sports Exerc. 2000;32(2):370-8.

32. Akima H, Takahashi H, Kuno SY, Katsuta S. Coactivation pattern in human

quadriceps during isokinetic knee-extension by muscle functional MRI. Eur J

Appl Physiol. 2004;91(1):7-14.

33. Häkkinen K, Pakarinen A, Kraemer WJ, Häkkinen A, Valkeinen H, Alen M.

Selective muscle hypertrophy, changes in EMG and force, and serum hormones

during strength training in older women. J Appl Physiol. 2001;91(2):569-80.

34. Kwak SD, Ahmad CS, Gardner TR, Grelsamer RP, Henry JH, Blankevoort L,

Ateshian GA, Mow VC. Hamstrings and iliotibial band forces affect knee kinematics

and contact pattern. J Orthop Res. 2000;18(1):101-8.

19

389

390

391

392

393

394

395

396

397

398

399

400

401

402

403

404

405

406

407

408

409

410

411

19

http://www.ncbi.nlm.nih.gov/pubmed/11457767


35. Mesfar W, Shirazi-Adl A. Knee joint biomechanics in open-kinetic-chain flexion

exercises. Clin Biomech (Bristol, Avon). 2008;23(4):477-82.

36. Pincivero DM, Aldworth C, Dickerson T, Petry C, Shultz T. Quadriceps-

hamstring EMG activity during functional, closed kinetic chain exercise to

fatigue Eur J Appl Physiol. 2000;81(6):504-9.

37. Jönhagen S, Halvorsen K, Benoit DL. Muscle activation and length changes during

two lunge exercises: implications for rehabilitation. Scand J Med Sci Sports.

2009;19(4):561-8.

38. Ono T, Okuwaki T, Fukubayashi T. Differences in activation patterns of knee flexor

muscles during concentric and eccentric exercises. Res Sports Med. 2010 ;18(3):188-

98

39. Blazevich AJ. Effects of physical training and detraining, immobilisation, growth and

aging on human fascicle geometry. Sports Med. 2006;36(12):1003-17. Review.

40. Neumann DA. Kinesiology of the hip: a focus on muscular actions. J Orthop Sports

Phys Ther. 2010;40(2):82-94.

41. Ward SR, Winters TM, Blemker SS. The architectural design of the gluteal muscle

group: implications for movement and rehabilitation. J Orthop Sports Phys Ther.

2010;40(2):95-102.

42. Visser JJ, Hoogkamer JE, Bobbert MF, Huijing PA. Length and moment arm of

human leg muscles as a function of knee and hip-joint angles. Eur J Appl Physiol

Occup Physiol. 1990;61(5-6):453-60.

20

412

413

414

415

416

417

418

419

420

421

422

423

424

425

426

427

428

429

430

431

432

20



43. Hawkins D, Hull ML. A method for determining lower extremity muscle-tendon

lengths during flexion/extension movements. J Biomech. 1990;23(5):487-94.

44. Shellock F, Fleckenstein J. Muscle physiology and pathophysiology: magnetic

resonance imaging evaluation. Semin Musculoskelet Radiol 2000; 4: 459–79.

45. Fleckenstein JC, Parkey R, Peshock R. Acute effects of exercise on MR imaging of

skeletal muscle in normal volunteers. AJR 1988;15: 231–87.

46. Adams GR, Duvoisin, MR, Dudley GA. Magnetic resonance imaging and

electromyography as indexes of muscle function. J Appl Physiol 1992; 73: 1578-83.

47. Potier TG, Alexander CM, Seynnes OR. Effects of eccentric strength training on

biceps femoris muscle architecture and knee joint range of movement. Eur J Appl

Physiol. 2009 Apr;105(6):939-44

21

433

434

435

436

437

438

439

440

441

442

443

444

445

446

447

448

449

450

451

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nonuniform changes in mri measurements of the thigh muscles after two hamstring strengthening...

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