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Scand J Med Sci Sports 2015: 25: 301–307 © 2014 John Wiley & Sons A/S.

doi: 10.1111/sms.12205 Published by John Wiley & Sons Ltd

Evaluation of hamstring muscle strength and morphology after


anterior cruciate ligament reconstruction
Y. Nomura1, R. Kuramochi2, T. Fukubayashi3
1
Graduate School of Sport Sciences, Waseda University, Saitama, Japan, 2School of Health and Sport Science, Chukyo University,
Aichi, Japan, 3Faculty of Sport Sciences, Waseda University, Saitama, Japan
Corresponding author: Yumi Nomura, Graduate School of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa,
Saitama 359-1192, Japan. Tel: +81 4 2947 6879, Fax: +81 4 2947 6879, E-mail: yumi.nmr@gmail.com
Accepted for publication 1 February 2014

This study aimed to clarify the relationship between knee lation between the MRI findings and flexor strength was
flexor strength and hamstring muscle morphology after analyzed. Regenerated ST tendon was confirmed in 21 of
anterior cruciate ligament (ACL) reconstruction using the 24 patients, but muscle volume (87.6%) and muscle
the semitendinosus (ST) tendon and to determine the length (74.5%) of the ST in the operated limb were sig-
causative factors of decreased knee flexor muscle nificantly smaller than those in the normal limb. The
strength. Fourteen male and ten female patients who percentage of the knee flexion torque of the operated limb
resumed sports activities after surgery participated in the compared with that of the normal was apparently lower
experiment. Isometric knee flexion torque was measured at 105° (69.1%) and 90° (68.6%) than at 60° (84.4%).
at 30°, 45°, 60°, 90°, and 105° of knee flexion. Magnetic Tendon regeneration, ST muscle shortening, and ST
resonance imaging (MRI) was used to calculate ST muscle atrophy correlated with decreased knee flexion
muscle length and hamstring muscle volume, and to torque. These results indicated that preserving the mor-
confirm the status of ST tendon regeneration. The corre- phology of the ST muscle-tendon complex is important.

Using the semitendinosus (ST) tendon as a graft material is muscle volume (Nakamae et al., 2005; Nishino et al.,
the mainstream method for anterior cruciate ligament 2006; Ahlén et al., 2012), morphological changes in the
(ACL) reconstruction. The advantages of the surgical pro- ST muscle-tendon complex would affect knee flexor
cedure are that it is less likely to cause anterior knee pain strength. Because most sports activities require good
and that it ensures good recovery of thigh muscle strength knee joint flexion, deficits in deep knee flexion as a result
(Rosenberg & Deffner, 1997; Cooley et al., 2001). Despite of ACL reconstruction surgery can influence athletic per-
tendon harvest, most studies have shown almost full recov- formance, e.g., in active flexion while standing in gym-
ery of knee flexion torque compared with the uninjured nastics and dance, and in the hooking action during
limb during isokinetic strength testing; however, deficits in groundwork or pinning techniques in wrestling and judo.
deep knee flexion torque have been confirmed during iso- In addition, the contraction of the hamstring muscles
metric strength testing (Ohkoshi et al., 1998; Tashiro et al., prevents secondary trauma by producing posterior tibial
2003; Makihara et al., 2006). Because of the differences in shear forces and contributing to the reduction of stress on
morphological structure, the component muscles in the the ACL (Noyes et al., 2005).
hamstring muscle group have diverse functions; i.e., the The purpose of this study was to clarify the relation-
semimembranosus (SM) and the long head of the biceps ship between knee flexion torque and morphology of the
femoris (BF) are mainly responsible for the muscle hamstring muscle group after harvesting the ST tendon
strength exerted during lower degrees of knee flexion, and for ACL reconstruction and to determine the causative
the ST is mainly responsible for the muscle strength factors of decreased knee flexor muscle strength. Our
exerted during deep knee flexion (Herzog & Read, 1993). hypothesis was that tendon morphology, muscle length,
Naturally, if the ST is subjected to invasive surgery, deficits and muscle volume of the ST would change after
in deep knee flexion may occur. surgery, and that the magnitude of the morphological
Studies revealed that a resected ST tendon has a high changes of the ST muscle-tendon complex influences
probability to regenerate tendon-like tissue (Cross et al., hamstring strength weakness. To evaluate the magnitude
1992; Eriksson et al., 2001a, b; Okahashi et al., 2006). of the changes, we compared the ACL reconstructed
Meanwhile, owing to muscle shortening and decreased limb with the uninjured limb.

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Nomura et al.
Materials and methods obtain hamstring muscle volume and ST tendon thickness, the
Subjects anatomical cross-sectional area (CSA) of each T1-weighted image
was calculated using Scion Image (Scion Corporation, Frederick,
In this study, 24 patients (14 men, 10 women; mean age, 21 ± 2 Maryland, USA). Muscle volume was determined by adding all
years) who successfully underwent primary ACL reconstruction the anatomical CSAs of the images and then multiplying the sum
were enrolled. The mean post-operative time was 27.7 ± 18.2 by 12 mm, which is the slice thickness plus the interslice gap. The
months (range 12–72 months). The inclusion criteria were (a) at hamstring muscles comprise the ST, SM, BF, and gracilis (G). The
least 12 post-operative months and (b) return to sports activities ST muscle length was defined as the length from the proximal
without any pain or restriction. All of the subjects were either musculo-tendinosus junction to the distal musculo-tendinosus
recreational or competitive athletes belonging to a high school, junction of the ST on proton destiny images. ST tendon regenera-
college, or recreational league team with sports activities classified tion was identified by an orthopedic surgeon and classified accord-
as level 1 or 2. Level 1 sports are described as jumping, pivoting, ing to the presence or absence of a regenerated tendon.
and hard cutting sports. Level 2 sports also involved lateral motion Regeneration failure was defined when a regenerated tendon could
but with less jumping or hard cutting than level 1 (Daniel et al., not be visualized in any view.
1994). However, their performance level was not always as high as
their pre-injury performance level (pre-injury: level 1, 23 patients;
level 2, 1 patient; post-surgery: level 1, 21 patients; level 2, 3
patients). Muscle strength testing
The present study was approved by the human research ethics Isometric knee flexion torque was measured using a dynamometer
committee of the School of Sport Sciences of Waseda University (Biodex System III, Biodex Co., New York, New York, USA).
and is consistent with their requirements for human experimenta- Subjects were instructed to take a prone position, with a hip flexion
tion (Approval No. 08–019). This study conforms to the Declara- angle of 0° and the lower body tightly secured to the seat (Fig. 1).
tion of Helsinki. Written informed consent statements were Before evaluation, compensation was performed to exclude the
obtained after participants read the volunteer information sheet effect of gravity on the measurement of torque. The isometric
and answered questions related to the study. contraction was performed at 30°, 45°, 60°, 90°, and 105° of knee
flexion with maximum voluntary effort. After the subject warmed
up and became familiarized with the procedure, measurements
Surgical technique and rehabilitation were performed twice with a 1-min interval. The normal limb was
Arthroscopically assisted reconstruction with an autogenous qua- tested before the operated limb. The peak torque value was nor-
drupled ipsilateral ST tendon was first described by Rosenberg malized to the body weight and assessed as the parameter.
et al. (1997). The same rehabilitation program was used for each
patient. After the acute phase, the patients were permitted to exer-
cise to promote increased range of motion, and isotonic knee Data management and analysis
extension and flexion exercises. The patients were allowed partial
Based on the power analysis study (Hoenig & Heisey, 2001), we
weight-bearing at 2 post-operative weeks and progress to full
estimated that to achieve 80% power with an alpha level of 0.05, a
weight-bearing at 3 post-operative weeks. Rehabilitation exercises
minimum of 21 subjects would be required. Each measurement
involved stationary bicycling and exercises with partial weight-
from the operated limb was expressed as a percentage relative
bearing at 3 weeks after surgery. Strengthening exercises for the
to that from the operated limb (% normal). To evaluate the rela-
isotonic quadriceps and hamstring muscle were initiated at 4
tionship between hamstring muscle strength and morphology, the
weeks. Until 8 weeks, restriction in range of motion was set for the
subjects were divided into three groups according to the morpho-
knee extension strengthening exercise. Jogging and full-speed
logical characteristics of the ST muscle-tendon complex in the
running were permitted after 12 and 16 post-operative weeks,
operated limb (Table 1). Group 2, which showed muscle shorten-
progressing to agility and sports-specific drills. Return to unlim-
ing despite the regenerated tendon, accounted for 13 of the 24
ited sports was allowed at 6–8 post-operative months.
patients, followed by group 1 patients, whose tendons were regen-
erated and muscle lengths were unchanged, accounting for 8
patients, and group 3 patients, who showed muscle shortening but
Magnetic resonance imaging (MRI) and measurements no tendon regeneration, accounting for 3 patients, the fewest
MRI was performed using a 1.5-T instrument (Signa EXCITE XI, among the three groups.
GE Healthcare, Tokyo, Japan), and T1-weighted images (repeti- A paired t-test was used to test for side-to-side differences in
tion time, 700 ms; echo time, 15 ms; slice thickness, 10.0 mm; CSA of the ST tendon, ST muscle length, and ST muscle volume.
interslice gap, 2.0 mm) and proton density images (repetition time, One-way analysis of variance was used to test for task differences
3000 ms; echo time, 10, 20, and 30 ms; slice thickness, 5.0 mm; in knee flexion torque, and for differences in each hamstring
interslice gap, 1.0 mm) were obtained on the axial planes. To muscle volume. The Pearson correlation coefficient analysis was

Fig. 1. Measurement position for hamstring muscle strength. Left: Knee flexion at 30°. Right: Knee flexion at 90°.

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Hamstring muscle strength and morphology

Fig. 3. Hamstring muscle volume in the operated limb shown as


a percentage of that in the normal limb. **P < 0.01, compared
with the normal limb. BF, biceps femoris; G, gracilis; SM, semi-
membranosus; ST, semitendinosus.

Table 2. Isometric knee flexion torque shown as a percentage of body


weight

Knee flexion angle Normal limb Operated limb

F30 129.3 ± 18.0 117.9 ± 28.0


F45 115.8 ± 18.7 102.6 ± 26.6
F60 105.5 ± 18.0 88.3 ± 21.8**
Fig. 2. Axial magnetic resonance image of the semitendinosus F90 73.9 ± 19.0 50.1 ± 16.0**
tendon (arrow): (a) regenerated; (b) undetected. F105 61.9 ± 16.7 44.1 ± 14.7**

Table 1. Morphology of the semitendinosus muscle F30, isometric knee flexion torque at 30°.
**P < 0.01, compared with the normal limb.
Normal limb Operated limb

CSA of the semitendinosus 0.10 ± 0.02 0.27 ± 0.13** G volumes in the operated limb were approximately the
tendon (cm2) same as those in the normal limb (P < 0.01) (Table 1;
Muscle length of the 27.7 ± 0.3 24.2 ± 0.4**
semitendinosus (cm)
Fig. 3).
Muscle volume of the 178.9 ± 55.1 132.8 ± 44.3**
semitendinosus (cm3)
Muscle strength testing
The values are mean ± SD.
The isometric knee flexion torque in the operated limb
**P < 0.01, compared with the normal limb.
was significantly lower than that in the normal limb
at 60° (88 ± 21% of body weight; %BW), 90° (50 ±
performed to determine the relationship between measurements 16%BW), and 105° (44 ± 14%BW), respectively (P <
and the causative factors of decreased knee flexion torque. Statis- 0.01); however, the difference was not significant at 30°
tical significance was set at P < 0.05. A post-hoc test was per- (117 ± 28%BW) and 45° (102 ± 26%BW) (Table 2).
formed for each variable to determine statistical power. The percentage of the isometric knee flexion torque of
Descriptive data are expressed as mean and standard deviation the operated limb compared with that of the normal limb
(SD) values.
was significantly lower at 90° (68 ± 23%; P < 0.01) and
105° (69 ± 23%; P < 0.01) than at 30° (91 ± 22%;
P < 0.01) (Fig. 4).
Results
MRI and measurements
In 21 of the 24 patients, ST tendon regeneration was Relationship between hamstring muscle strength and
confirmed (Fig. 2). The ST muscle length in the operated morphology
limb (24.2 ± 0.38 cm) was significantly shorter than that We found a significant correlation between ST muscle
in the normal limb (27.7 ± 0.25 cm, P < 0.001). The length and knee flexion torque at 60° (r = 0.458,
CSA of the ST tendon in the operated limb (0.10 ± P = 0.042; Table 3). ST muscle volume was significantly
0.02 cm2) was significantly larger than that in the normal correlated with knee flexion torque at 30° (r = 0.427,
limb (0.27 ± 0.13 cm2, P < 0.001) (Table 1). The ST P = 0.047), 45° (r = 0.432, P = 0.045), and 60° (r =
volume in the operated limb was significantly smaller 0.611, P < 0.01). Figures 5 and 6 summarize for each of
than that in the normal limb; however, the SM, BF, and the three groups the measurement results of knee flexion

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Nomura et al.
Table 3. Correlation coefficients (r) between knee flexion torque and hamstring morphology

Hamstring morphology F30 F45 F60 F90 F105

CSA of the semitendinosus tendon 0.242 0.188 0.129 0.041 0.379


Muscle length of the semitendinosus 0.250 0.292 0.458* 0.234 0.220
Muscle volume of the semitendinosus 0.427* 0.432* 0.611** 0.027 0.135

F30, isometric knee flexion toque at 30°. CSA, cross-sectional area.


*P < 0.05, **P < 0.01.

Fig. 6. Results of semitendinosus (ST) muscle volume in the


operated limb regarding the morphology of the semitendinosus
muscle-tendon complex (% normal).
Fig. 4. Isometric knee flexion torque i n the operated limb
shown as a percentage of that in the normal limb. **P < 0.01,
compared with the normal limb.
Discussion
This study was designed to assess the strength and mor-
phological changes in the hamstring muscle group after
harvesting the ST tendon for ACL reconstruction and to
evaluate the relationship between the morphology of the
ST muscle-tendon complex and post-operative recovery
of hamstring muscle strength.
In several studies, it has been reported that the ST
tendon regenerates several years after surgery, with
similar macroscopic and histological features as those of
the original tendon (Eriksson et al., 1999; Papandrea
et al., 2000; Ferretti et al., 2002). Tadokoro et al. (2007)
observed regenerated ST tendon on MRI in 79% of
cases. Rispoli et al. (2001) and Choi et al. (2012) con-
firmed the regenerated ST tendon in MRIs obtained at
the level of the tibial plateau and superior pole of the
Fig. 5. Results of knee flexion torque regarding the morphology patella, respectively. However, the location of the
of the semitendinosus muscle-tendon complex (% normal). musculo-tendinosus junction shifted proximally when
compared with the normal limb. In our study, ST tendon
regeneration was confirmed in approximately 88% of
torque and ST muscle volume in the operated limb rela- patients after ACL reconstruction surgery, and the CSA
tive to those in the normal limb (% normal). In group 1, in the operated side was enlarged by a mean of approxi-
the knee flexion torque and ST muscle volume in the mately 2.7 times that in the normal side. Meanwhile,
operated limb were the same as those in the normal limb compared with the normal side, the ST muscle length in
(86 ± 10%, muscle volume; 100 ± 31%, flexion torque at the operated side was shortened by a mean of approxi-
30°). However, in groups 2 and 3, the knee flexion torque mately 3.5 cm and the muscle volume was also reduced
in the operated limb was lower than that in the normal by approximately 74%. This finding was similar to that
limb (88 ± 12%, group 2; 78 ± 3%, group 3). Moreover, of previous studies (Simonian et al., 1997; Nishino et al.,
the ST muscle volume in the operated limb was smaller 2006; Choi et al., 2012).
than that in the normal limb (71 ± 11%, group 2; In the muscle volume measurement conducted in this
52 ± 3%, group 3). study, the G, a knee flexor muscle, was assessed in

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Hamstring muscle strength and morphology
addition to the BF, SM, and ST, which were studied by ST muscle decreases and the function of the tendon to
Nishino et al. (2006). It has been also shown that ST convey the torque-generating capacity of the ST muscle
muscle atrophy was not accompanied by a compensatory to the tibia could also decline.
hypertrophy of the BF and SM. In addition, our experi- Nevertheless, the fact remains that the hamstring
mental results confirmed the absence of a compensatory tendon graft is the mainstream method for ACL recon-
hypertrophy of the G, which is a fusiform muscle like the struction. It is also true that satisfactory result was
ST. These findings show that ST muscle atrophy is obtained in most of patients. This could be because the
impossible to compensate, even by knee flexor muscles function of the hamstring is more important at extended
of the same category. Although we mention details later, or slightly knee flexed position. Considering the advan-
this ST muscle atrophy could be a causative factor of tages and disadvantages of the hamstring tendon graft
knee flexion deficits. and other graft, we think that choosing the best proce-
An isometric knee flexion torque allowed for a recov- dure for ACL reconstruction depends on the types of
ery of approximately 90% at a 30° or 45° knee joint athletic activity in which athletes participate. Therefore,
flexion but showed a significant decrease at a 60°, 90°, or a more active rehabilitation for hamstring is needed to
105° knee joint flexion. Like the findings reported by minimize hamstring muscle weakness and maximize
Tashiro et al. (2003), our results suggest that deficits in athletic performance, when we use hamstring tendon
deep knee flexion torque occurred after ST tendon resec- graft. The hamstring muscle rehabilitation in this study
tion. Meanwhile, by obtaining MRI scans using the did not include strengthening exercises at deep knee
tagging snapshot technique, Hioki et al. (2003) observed flexion. Kubota et al. (2007) observed the regional dif-
the dynamics of the ST muscle during knee joint flexion ferences of MRI measurements in the hamstring follow-
and confirmed the equal movements of the operated and ing knee-eccentric flexion exercise. Consequently, CSA
normal sides. Likewise, Takeda et al. (2006) also mea- and transverse relaxation times of the ST were increased
sured the T2 value (the transverse relaxation time) of the significantly compared with those of the BF or SM. This
hamstring muscle group after knee flexion tasks and result indicated that ST muscle responds to knee-
confirmed that the latter was functional in the normal eccentric flexion exercise by strengthening only pararell
and operated sides, regardless of the state of regenera- fibered muscles. We are currently conducting new
tion. It has been recognized that the regenerated tendon research that assesses the effects of the Nordic ham-
is considered to function similar to the original ST string, which is simple eccentric hamstring exercise.
tendon when generating knee joint torque. However, the Further research may reveal how we can prevent ham-
exercise challenges performed in the previous studies string muscle weakness after tendon harvest.
consisted of a 0°–45° concentric contraction of the knee A limitation of this study was the large variation in
joints in the prone position and an isokinetic contraction post-operative time. The mean ± SD post-operative time
in the sitting position, and because both challenges were was 27.7 ± 18.2 months (range 12–72 months) after
not performed in the prone position/deep knee flexion, in reconstruction. This variability shows that the sample of
which the ST is greatly involved, the decline in the patients with ACL reconstruction was heterogeneous in
function of the ST is believed to have not occurred. relation to post-operative time. Eriksson et al. (1999)
Consistent with the findings of Tadokoro et al. (2007) revealed that ST tendon is gradually remodeled into a
regarding the relationship between hamstring strength tendon-like structure. This time-based phenomenon may
and morphology, no relationship was found between the correspond to morphological changes in ST muscle-
CSA of the regenerated ST tendon and the knee flexion tendon complex. We found that morphological changes
torque; however, the volume and length of the ST muscle in the ST correlated with hamstring weakness; it could
showed a positive correlation with knee flexion torque. be influenced by recovery of the ST muscle-tendon
That is, the decrease in knee flexion torque occurs when complex. Therefore, further research is needed to assess
muscle shortening and muscle atrophy are present. Com- morphology and strength at different post-operative
pared with groups 2 and 3, group 1 was less likely to times.
have decreased ST muscle volume and length, and knee Despite the limitation, the information provided
flexion torque. These findings suggest that because ST is herein might provide insight for better understanding of
a fusiform muscle, it undergoes muscle length shorten- several morphological and functional behaviors of the
ing, as in the case of groups 2 and 3, and causes an hamstring muscle group after harvesting the ST tendon.
equivalent shortening of the muscle fibers. When muscle Based on a series of considerations, morphological
fibers are shortened in relation to their original state, the changes (tendon regeneration, muscle shortening, and
relationship between muscle force and length is likely to muscle atrophy) that accompany ST tendon resection
change and the ST muscle may also show functional were indicated to be the cause of knee flexion deficits. In
changes. In addition, when ST muscle shortening occurs addition, the results pertaining to the hamstring muscle
in the absence of a regenerated ST tendon (as in the case volume show that tendon function could not be compen-
of group 3) and when the muscle has no site of attach- sated by muscles other than the ST muscle. Therefore,
ment to the tibia, the torque-generating capacity of the prevention of muscle shortening and muscle atrophy is

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Nomura et al.
important to suppress decreased knee flexion torque as a factors of decreased hamstring muscle strength were (a)
result of ACL reconstruction surgery. A future study absence of a regenerated ST tendon; (b) ST muscle
on surgical techniques, rehabilitation, and exercises is shortening; and (c) ST muscle atrophy. In fact, ST
necessary to further investigate and improve approaches tendon regeneration and ST muscle shortening were
to prevent morphological changes the ST muscle-tendon dependent on the surgical technique used in harvesting
complex. the ST tendon, suggesting that the management
Our results suggest that ST tendon regeneration, ST approach for ST muscle atrophy is especially important
muscle shortening, and ST muscle atrophy were signifi- in the rehabilitation after ACL reconstruction, which
cantly correlated with hamstring muscle strength. Con- tend to overemphasize hamstring exercises. A further
sequently, preservation of ST morphology after ACL direction of this study will be to develop the surgical
reconstruction is important. technique for harvesting a graft and to examine a more
active rehabilitation for the hamstring muscle, such as
Perspectives deep knee flexion or eccentric hamstring exercises.

Considering all the possible morphological evaluation Key words: Anterior cruciate ligament, semitendinosus,
variables (tendon regeneration, CSA, and muscle length flexion torque, muscle volume, MRI.
and volume) and the isometric strength test results in this
study, the most important finding is that the morphologi-
cal changes after harvesting the ST tendon correlated Acknowledgements
with hamstring muscle strength. Moreover, this strength
The authors gratefully acknowledge A. Nishino and A. Sanada for
deficit remained even after subjects returned to their their assistance in the preparation of this research. The authors also
previous sports activities and completed the rehabilita- thank Waseda University and all the participants in this study for
tion program. This study revealed that the causative their cooperation.

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