Scand J Med Sci Sports 2015: 25: 301–307 doi: 10.1111/sms.12205
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Evaluation of hamstring muscle strength and morphology after anterior cruciate ligament reconstruction Y. Nomura1, R. Kuramochi2, T. Fukubayashi3 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: [email protected]
1
Accepted for publication 1 February 2014
This study aimed to clarify the relationship between knee flexor strength and hamstring muscle morphology after anterior cruciate ligament (ACL) reconstruction using the semitendinosus (ST) tendon and to determine the causative factors of decreased knee flexor muscle strength. Fourteen male and ten female patients who resumed sports activities after surgery participated in the experiment. Isometric knee flexion torque was measured at 30°, 45°, 60°, 90°, and 105° of knee flexion. Magnetic resonance imaging (MRI) was used to calculate ST muscle length and hamstring muscle volume, and to confirm the status of ST tendon regeneration. The corre-
lation between the MRI findings and flexor strength was analyzed. Regenerated ST tendon was confirmed in 21 of the 24 patients, but muscle volume (87.6%) and muscle length (74.5%) of the ST in the operated limb were significantly smaller than those in the normal limb. The percentage of the knee flexion torque of the operated limb compared with that of the normal was apparently lower at 105° (69.1%) and 90° (68.6%) than at 60° (84.4%). Tendon regeneration, ST muscle shortening, and ST muscle atrophy correlated with decreased knee flexion torque. These results indicated that preserving the morphology of the ST muscle-tendon complex is important.
Using the semitendinosus (ST) tendon as a graft material is the mainstream method for anterior cruciate ligament (ACL) reconstruction. The advantages of the surgical procedure are that it is less likely to cause anterior knee pain and that it ensures good recovery of thigh muscle strength (Rosenberg & Deffner, 1997; Cooley et al., 2001). Despite tendon harvest, most studies have shown almost full recovery of knee flexion torque compared with the uninjured limb during isokinetic strength testing; however, deficits in deep knee flexion torque have been confirmed during isometric strength testing (Ohkoshi et al., 1998; Tashiro et al., 2003; Makihara et al., 2006). Because of the differences in morphological structure, the component muscles in the hamstring muscle group have diverse functions; i.e., the semimembranosus (SM) and the long head of the biceps femoris (BF) are mainly responsible for the muscle strength exerted during lower degrees of knee flexion, and the ST is mainly responsible for the muscle strength exerted during deep knee flexion (Herzog & Read, 1993). Naturally, if the ST is subjected to invasive surgery, deficits in deep knee flexion may occur. Studies revealed that a resected ST tendon has a high probability to regenerate tendon-like tissue (Cross et al., 1992; Eriksson et al., 2001a, b; Okahashi et al., 2006). Meanwhile, owing to muscle shortening and decreased
muscle volume (Nakamae et al., 2005; Nishino et al., 2006; Ahlén et al., 2012), morphological changes in the ST muscle-tendon complex would affect knee flexor strength. Because most sports activities require good knee joint flexion, deficits in deep knee flexion as a result of ACL reconstruction surgery can influence athletic performance, e.g., in active flexion while standing in gymnastics and dance, and in the hooking action during groundwork or pinning techniques in wrestling and judo. In addition, the contraction of the hamstring muscles prevents secondary trauma by producing posterior tibial shear forces and contributing to the reduction of stress on the ACL (Noyes et al., 2005). The purpose of this study was to clarify the relationship between knee flexion torque and morphology of the hamstring muscle group after harvesting the ST tendon for ACL reconstruction and to determine the causative factors of decreased knee flexor muscle strength. Our hypothesis was that tendon morphology, muscle length, and muscle volume of the ST would change after surgery, and that the magnitude of the morphological changes of the ST muscle-tendon complex influences hamstring strength weakness. To evaluate the magnitude of the changes, we compared the ACL reconstructed limb with the uninjured limb.
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Nomura et al. Materials and methods Subjects In this study, 24 patients (14 men, 10 women; mean age, 21 ± 2 years) who successfully underwent primary ACL reconstruction were enrolled. The mean post-operative time was 27.7 ± 18.2 months (range 12–72 months). The inclusion criteria were (a) at least 12 post-operative months and (b) return to sports activities without any pain or restriction. All of the subjects were either recreational or competitive athletes belonging to a high school, college, or recreational league team with sports activities classified as level 1 or 2. Level 1 sports are described as jumping, pivoting, and hard cutting sports. Level 2 sports also involved lateral motion but with less jumping or hard cutting than level 1 (Daniel et al., 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). The present study was approved by the human research ethics committee of the School of Sport Sciences of Waseda University and is consistent with their requirements for human experimentation (Approval No. 08–019). This study conforms to the Declaration of Helsinki. Written informed consent statements were obtained after participants read the volunteer information sheet and answered questions related to the study.
Surgical technique and rehabilitation Arthroscopically assisted reconstruction with an autogenous quadrupled ipsilateral ST tendon was first described by Rosenberg et al. (1997). The same rehabilitation program was used for each patient. After the acute phase, the patients were permitted to exercise to promote increased range of motion, and isotonic knee extension and flexion exercises. The patients were allowed partial weight-bearing at 2 post-operative weeks and progress to full weight-bearing at 3 post-operative weeks. Rehabilitation exercises involved stationary bicycling and exercises with partial weightbearing at 3 weeks after surgery. Strengthening exercises for the isotonic quadriceps and hamstring muscle were initiated at 4 weeks. Until 8 weeks, restriction in range of motion was set for the knee extension strengthening exercise. Jogging and full-speed running were permitted after 12 and 16 post-operative weeks, progressing to agility and sports-specific drills. Return to unlimited sports was allowed at 6–8 post-operative months.
Magnetic resonance imaging (MRI) and measurements MRI was performed using a 1.5-T instrument (Signa EXCITE XI, GE Healthcare, Tokyo, Japan), and T1-weighted images (repetition time, 700 ms; echo time, 15 ms; slice thickness, 10.0 mm; interslice gap, 2.0 mm) and proton density images (repetition time, 3000 ms; echo time, 10, 20, and 30 ms; slice thickness, 5.0 mm; interslice gap, 1.0 mm) were obtained on the axial planes. To
obtain hamstring muscle volume and ST tendon thickness, the anatomical cross-sectional area (CSA) of each T1-weighted image was calculated using Scion Image (Scion Corporation, Frederick, Maryland, USA). Muscle volume was determined by adding all the anatomical CSAs of the images and then multiplying the sum by 12 mm, which is the slice thickness plus the interslice gap. The hamstring muscles comprise the ST, SM, BF, and gracilis (G). The ST muscle length was defined as the length from the proximal musculo-tendinosus junction to the distal musculo-tendinosus junction of the ST on proton destiny images. ST tendon regeneration was identified by an orthopedic surgeon and classified according to the presence or absence of a regenerated tendon. Regeneration failure was defined when a regenerated tendon could not be visualized in any view.
Muscle strength testing Isometric knee flexion torque was measured using a dynamometer (Biodex System III, Biodex Co., New York, New York, USA). Subjects were instructed to take a prone position, with a hip flexion angle of 0° and the lower body tightly secured to the seat (Fig. 1). Before evaluation, compensation was performed to exclude the effect of gravity on the measurement of torque. The isometric 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 were performed twice with a 1-min interval. The normal limb was tested before the operated limb. The peak torque value was normalized to the body weight and assessed as the parameter.
Data management and analysis Based on the power analysis study (Hoenig & Heisey, 2001), we estimated that to achieve 80% power with an alpha level of 0.05, a minimum of 21 subjects would be required. Each measurement from the operated limb was expressed as a percentage relative to that from the operated limb (% normal). To evaluate the relationship between hamstring muscle strength and morphology, the subjects were divided into three groups according to the morphological characteristics of the ST muscle-tendon complex in the operated limb (Table 1). Group 2, which showed muscle shortening despite the regenerated tendon, accounted for 13 of the 24 patients, followed by group 1 patients, whose tendons were regenerated and muscle lengths were unchanged, accounting for 8 patients, and group 3 patients, who showed muscle shortening but no tendon regeneration, accounting for 3 patients, the fewest among the three groups. A paired t-test was used to test for side-to-side differences in CSA of the ST tendon, ST muscle length, and ST muscle volume. One-way analysis of variance was used to test for task differences in knee flexion torque, and for differences in each hamstring 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, semimembranosus; ST, semitendinosus. Table 2. Isometric knee flexion torque shown as a percentage of body weight
Fig. 2. Axial magnetic resonance image of the semitendinosus tendon (arrow): (a) regenerated; (b) undetected. Table 1. Morphology of the semitendinosus muscle
Normal limb CSA of the semitendinosus tendon (cm2) Muscle length of the semitendinosus (cm) Muscle volume of the semitendinosus (cm3)
Operated limb
0.10 ± 0.02
0.27 ± 0.13**
27.7 ± 0.3
24.2 ± 0.4**
178.9 ± 55.1
132.8 ± 44.3**
The values are mean ± SD. **P < 0.01, compared with the normal limb.
performed to determine the relationship between measurements and the causative factors of decreased knee flexion torque. Statistical significance was set at P < 0.05. A post-hoc test was performed for each variable to determine statistical power. Descriptive data are expressed as mean and standard deviation (SD) values.
Results MRI and measurements In 21 of the 24 patients, ST tendon regeneration was confirmed (Fig. 2). The ST muscle length in the operated limb (24.2 ± 0.38 cm) was significantly shorter than that in the normal limb (27.7 ± 0.25 cm, P < 0.001). The CSA of the ST tendon in the operated limb (0.10 ± 0.02 cm2) was significantly larger than that in the normal limb (0.27 ± 0.13 cm2, P < 0.001) (Table 1). The ST volume in the operated limb was significantly smaller than that in the normal limb; however, the SM, BF, and
Knee flexion angle
Normal limb
Operated limb
F30 F45 F60 F90 F105
129.3 ± 18.0 115.8 ± 18.7 105.5 ± 18.0 73.9 ± 19.0 61.9 ± 16.7
117.9 ± 28.0 102.6 ± 26.6 88.3 ± 21.8** 50.1 ± 16.0** 44.1 ± 14.7**
F30, isometric knee flexion torque at 30°. **P < 0.01, compared with the normal limb.
G volumes in the operated limb were approximately the same as those in the normal limb (P < 0.01) (Table 1; Fig. 3). Muscle strength testing The isometric knee flexion torque in the operated limb was significantly lower than that in the normal limb at 60° (88 ± 21% of body weight; %BW), 90° (50 ± 16%BW), and 105° (44 ± 14%BW), respectively (P < 0.01); however, the difference was not significant at 30° (117 ± 28%BW) and 45° (102 ± 26%BW) (Table 2). The percentage of the isometric knee flexion torque of the operated limb compared with that of the normal limb 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). Relationship between hamstring muscle strength and morphology We found a significant correlation between ST muscle length and knee flexion torque at 60° (r = 0.458, P = 0.042; Table 3). ST muscle volume was significantly correlated with knee flexion torque at 30° (r = 0.427, P = 0.047), 45° (r = 0.432, P = 0.045), and 60° (r = 0.611, P < 0.01). Figures 5 and 6 summarize for each of 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 Muscle length of the semitendinosus Muscle volume of the semitendinosus
0.242 0.250 0.427*
0.188 0.292 0.432*
0.129 0.458* 0.611**
0.041 0.234 0.027
0.379 0.220 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.
Fig. 5. Results of knee flexion torque regarding the morphology of the semitendinosus muscle-tendon complex (% normal).
torque and ST muscle volume in the operated limb relative to those in the normal limb (% normal). In group 1, the knee flexion torque and ST muscle volume in the operated limb were the same as those in the normal limb (86 ± 10%, muscle volume; 100 ± 31%, flexion torque at 30°). However, in groups 2 and 3, the knee flexion torque in the operated limb was lower than that in the normal limb (88 ± 12%, group 2; 78 ± 3%, group 3). Moreover, the ST muscle volume in the operated limb was smaller than that in the normal limb (71 ± 11%, group 2; 52 ± 3%, group 3).
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Discussion This study was designed to assess the strength and morphological 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) confirmed the regenerated ST tendon in MRIs obtained at the level of the tibial plateau and superior pole of the patella, respectively. However, the location of the musculo-tendinosus junction shifted proximally when compared with the normal limb. In our study, ST tendon regeneration was confirmed in approximately 88% of patients after ACL reconstruction surgery, and the CSA in the operated side was enlarged by a mean of approximately 2.7 times that in the normal side. Meanwhile, compared with the normal side, the ST muscle length in the operated side was shortened by a mean of approximately 3.5 cm and the muscle volume was also reduced by approximately 74%. This finding was similar to that of previous studies (Simonian et al., 1997; Nishino et al., 2006; Choi et al., 2012). In the muscle volume measurement conducted in this study, the G, a knee flexor muscle, was assessed in
Hamstring muscle strength and morphology addition to the BF, SM, and ST, which were studied by Nishino et al. (2006). It has been also shown that ST muscle atrophy was not accompanied by a compensatory hypertrophy of the BF and SM. In addition, our experimental results confirmed the absence of a compensatory hypertrophy of the G, which is a fusiform muscle like the ST. These findings show that ST muscle atrophy is impossible to compensate, even by knee flexor muscles of the same category. Although we mention details later, this ST muscle atrophy could be a causative factor of knee flexion deficits. An isometric knee flexion torque allowed for a recovery of approximately 90% at a 30° or 45° knee joint flexion but showed a significant decrease at a 60°, 90°, or 105° knee joint flexion. Like the findings reported by Tashiro et al. (2003), our results suggest that deficits in deep knee flexion torque occurred after ST tendon resection. Meanwhile, by obtaining MRI scans using the tagging snapshot technique, Hioki et al. (2003) observed the dynamics of the ST muscle during knee joint flexion and confirmed the equal movements of the operated and normal sides. Likewise, Takeda et al. (2006) also measured the T2 value (the transverse relaxation time) of the hamstring muscle group after knee flexion tasks and confirmed that the latter was functional in the normal and operated sides, regardless of the state of regeneration. It has been recognized that the regenerated tendon is considered to function similar to the original ST tendon when generating knee joint torque. However, the exercise challenges performed in the previous studies consisted of a 0°–45° concentric contraction of the knee joints in the prone position and an isokinetic contraction in the sitting position, and because both challenges were not performed in the prone position/deep knee flexion, in which the ST is greatly involved, the decline in the function of the ST is believed to have not occurred. Consistent with the findings of Tadokoro et al. (2007) regarding the relationship between hamstring strength and morphology, no relationship was found between the CSA of the regenerated ST tendon and the knee flexion torque; however, the volume and length of the ST muscle showed a positive correlation with knee flexion torque. That is, the decrease in knee flexion torque occurs when muscle shortening and muscle atrophy are present. Compared with groups 2 and 3, group 1 was less likely to have decreased ST muscle volume and length, and knee flexion torque. These findings suggest that because ST is a fusiform muscle, it undergoes muscle length shortening, as in the case of groups 2 and 3, and causes an equivalent shortening of the muscle fibers. When muscle fibers are shortened in relation to their original state, the relationship between muscle force and length is likely to change and the ST muscle may also show functional changes. In addition, when ST muscle shortening occurs in the absence of a regenerated ST tendon (as in the case of group 3) and when the muscle has no site of attachment to the tibia, the torque-generating capacity of the
ST muscle decreases and the function of the tendon to convey the torque-generating capacity of the ST muscle to the tibia could also decline. Nevertheless, the fact remains that the hamstring tendon graft is the mainstream method for ACL reconstruction. It is also true that satisfactory result was obtained in most of patients. This could be because the function of the hamstring is more important at extended or slightly knee flexed position. Considering the advantages and disadvantages of the hamstring tendon graft and other graft, we think that choosing the best procedure for ACL reconstruction depends on the types of athletic activity in which athletes participate. Therefore, a more active rehabilitation for hamstring is needed to minimize hamstring muscle weakness and maximize athletic performance, when we use hamstring tendon graft. The hamstring muscle rehabilitation in this study did not include strengthening exercises at deep knee flexion. Kubota et al. (2007) observed the regional differences of MRI measurements in the hamstring following knee-eccentric flexion exercise. Consequently, CSA and transverse relaxation times of the ST were increased significantly compared with those of the BF or SM. This result indicated that ST muscle responds to kneeeccentric flexion exercise by strengthening only pararell fibered muscles. We are currently conducting new research that assesses the effects of the Nordic hamstring, which is simple eccentric hamstring exercise. Further research may reveal how we can prevent hamstring muscle weakness after tendon harvest. A limitation of this study was the large variation in post-operative time. The mean ± SD post-operative time was 27.7 ± 18.2 months (range 12–72 months) after reconstruction. This variability shows that the sample of patients with ACL reconstruction was heterogeneous in relation to post-operative time. Eriksson et al. (1999) revealed that ST tendon is gradually remodeled into a tendon-like structure. This time-based phenomenon may correspond to morphological changes in ST muscletendon complex. We found that morphological changes in the ST correlated with hamstring weakness; it could be influenced by recovery of the ST muscle-tendon complex. Therefore, further research is needed to assess morphology and strength at different post-operative times. Despite the limitation, the information provided herein might provide insight for better understanding of several morphological and functional behaviors of the hamstring muscle group after harvesting the ST tendon. Based on a series of considerations, morphological changes (tendon regeneration, muscle shortening, and muscle atrophy) that accompany ST tendon resection were indicated to be the cause of knee flexion deficits. In addition, the results pertaining to the hamstring muscle volume show that tendon function could not be compensated by muscles other than the ST muscle. Therefore, prevention of muscle shortening and muscle atrophy is
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Nomura et al. important to suppress decreased knee flexion torque as a result of ACL reconstruction surgery. A future study on surgical techniques, rehabilitation, and exercises is necessary to further investigate and improve approaches to prevent morphological changes the ST muscle-tendon complex. Our results suggest that ST tendon regeneration, ST muscle shortening, and ST muscle atrophy were significantly correlated with hamstring muscle strength. Consequently, preservation of ST morphology after ACL reconstruction is important. Perspectives Considering all the possible morphological evaluation variables (tendon regeneration, CSA, and muscle length and volume) and the isometric strength test results in this study, the most important finding is that the morphological changes after harvesting the ST tendon correlated with hamstring muscle strength. Moreover, this strength deficit remained even after subjects returned to their previous sports activities and completed the rehabilitation program. This study revealed that the causative
factors of decreased hamstring muscle strength were (a) absence of a regenerated ST tendon; (b) ST muscle shortening; and (c) ST muscle atrophy. In fact, ST tendon regeneration and ST muscle shortening were dependent on the surgical technique used in harvesting the ST tendon, suggesting that the management approach for ST muscle atrophy is especially important in the rehabilitation after ACL reconstruction, which tend to overemphasize hamstring exercises. A further direction of this study will be to develop the surgical technique for harvesting a graft and to examine a more active rehabilitation for the hamstring muscle, such as deep knee flexion or eccentric hamstring exercises. Key words: Anterior cruciate ligament, semitendinosus, flexion torque, muscle volume, MRI.
Acknowledgements The authors gratefully acknowledge A. Nishino and A. Sanada for their assistance in the preparation of this research. The authors also thank Waseda University and all the participants in this study for their cooperation.
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© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Evaluation of hamstring muscle strength and morphology after anterior cruciate ligament reconstruction Y. Nomura1, R. Kuramochi2, T. Fukubayashi3 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: [email protected]
1
Accepted for publication 1 February 2014
This study aimed to clarify the relationship between knee flexor strength and hamstring muscle morphology after anterior cruciate ligament (ACL) reconstruction using the semitendinosus (ST) tendon and to determine the causative factors of decreased knee flexor muscle strength. Fourteen male and ten female patients who resumed sports activities after surgery participated in the experiment. Isometric knee flexion torque was measured at 30°, 45°, 60°, 90°, and 105° of knee flexion. Magnetic resonance imaging (MRI) was used to calculate ST muscle length and hamstring muscle volume, and to confirm the status of ST tendon regeneration. The corre-
lation between the MRI findings and flexor strength was analyzed. Regenerated ST tendon was confirmed in 21 of the 24 patients, but muscle volume (87.6%) and muscle length (74.5%) of the ST in the operated limb were significantly smaller than those in the normal limb. The percentage of the knee flexion torque of the operated limb compared with that of the normal was apparently lower at 105° (69.1%) and 90° (68.6%) than at 60° (84.4%). Tendon regeneration, ST muscle shortening, and ST muscle atrophy correlated with decreased knee flexion torque. These results indicated that preserving the morphology of the ST muscle-tendon complex is important.
Using the semitendinosus (ST) tendon as a graft material is the mainstream method for anterior cruciate ligament (ACL) reconstruction. The advantages of the surgical procedure are that it is less likely to cause anterior knee pain and that it ensures good recovery of thigh muscle strength (Rosenberg & Deffner, 1997; Cooley et al., 2001). Despite tendon harvest, most studies have shown almost full recovery of knee flexion torque compared with the uninjured limb during isokinetic strength testing; however, deficits in deep knee flexion torque have been confirmed during isometric strength testing (Ohkoshi et al., 1998; Tashiro et al., 2003; Makihara et al., 2006). Because of the differences in morphological structure, the component muscles in the hamstring muscle group have diverse functions; i.e., the semimembranosus (SM) and the long head of the biceps femoris (BF) are mainly responsible for the muscle strength exerted during lower degrees of knee flexion, and the ST is mainly responsible for the muscle strength exerted during deep knee flexion (Herzog & Read, 1993). Naturally, if the ST is subjected to invasive surgery, deficits in deep knee flexion may occur. Studies revealed that a resected ST tendon has a high probability to regenerate tendon-like tissue (Cross et al., 1992; Eriksson et al., 2001a, b; Okahashi et al., 2006). Meanwhile, owing to muscle shortening and decreased
muscle volume (Nakamae et al., 2005; Nishino et al., 2006; Ahlén et al., 2012), morphological changes in the ST muscle-tendon complex would affect knee flexor strength. Because most sports activities require good knee joint flexion, deficits in deep knee flexion as a result of ACL reconstruction surgery can influence athletic performance, e.g., in active flexion while standing in gymnastics and dance, and in the hooking action during groundwork or pinning techniques in wrestling and judo. In addition, the contraction of the hamstring muscles prevents secondary trauma by producing posterior tibial shear forces and contributing to the reduction of stress on the ACL (Noyes et al., 2005). The purpose of this study was to clarify the relationship between knee flexion torque and morphology of the hamstring muscle group after harvesting the ST tendon for ACL reconstruction and to determine the causative factors of decreased knee flexor muscle strength. Our hypothesis was that tendon morphology, muscle length, and muscle volume of the ST would change after surgery, and that the magnitude of the morphological changes of the ST muscle-tendon complex influences hamstring strength weakness. To evaluate the magnitude of the changes, we compared the ACL reconstructed limb with the uninjured limb.
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Nomura et al. Materials and methods Subjects In this study, 24 patients (14 men, 10 women; mean age, 21 ± 2 years) who successfully underwent primary ACL reconstruction were enrolled. The mean post-operative time was 27.7 ± 18.2 months (range 12–72 months). The inclusion criteria were (a) at least 12 post-operative months and (b) return to sports activities without any pain or restriction. All of the subjects were either recreational or competitive athletes belonging to a high school, college, or recreational league team with sports activities classified as level 1 or 2. Level 1 sports are described as jumping, pivoting, and hard cutting sports. Level 2 sports also involved lateral motion but with less jumping or hard cutting than level 1 (Daniel et al., 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). The present study was approved by the human research ethics committee of the School of Sport Sciences of Waseda University and is consistent with their requirements for human experimentation (Approval No. 08–019). This study conforms to the Declaration of Helsinki. Written informed consent statements were obtained after participants read the volunteer information sheet and answered questions related to the study.
Surgical technique and rehabilitation Arthroscopically assisted reconstruction with an autogenous quadrupled ipsilateral ST tendon was first described by Rosenberg et al. (1997). The same rehabilitation program was used for each patient. After the acute phase, the patients were permitted to exercise to promote increased range of motion, and isotonic knee extension and flexion exercises. The patients were allowed partial weight-bearing at 2 post-operative weeks and progress to full weight-bearing at 3 post-operative weeks. Rehabilitation exercises involved stationary bicycling and exercises with partial weightbearing at 3 weeks after surgery. Strengthening exercises for the isotonic quadriceps and hamstring muscle were initiated at 4 weeks. Until 8 weeks, restriction in range of motion was set for the knee extension strengthening exercise. Jogging and full-speed running were permitted after 12 and 16 post-operative weeks, progressing to agility and sports-specific drills. Return to unlimited sports was allowed at 6–8 post-operative months.
Magnetic resonance imaging (MRI) and measurements MRI was performed using a 1.5-T instrument (Signa EXCITE XI, GE Healthcare, Tokyo, Japan), and T1-weighted images (repetition time, 700 ms; echo time, 15 ms; slice thickness, 10.0 mm; interslice gap, 2.0 mm) and proton density images (repetition time, 3000 ms; echo time, 10, 20, and 30 ms; slice thickness, 5.0 mm; interslice gap, 1.0 mm) were obtained on the axial planes. To
obtain hamstring muscle volume and ST tendon thickness, the anatomical cross-sectional area (CSA) of each T1-weighted image was calculated using Scion Image (Scion Corporation, Frederick, Maryland, USA). Muscle volume was determined by adding all the anatomical CSAs of the images and then multiplying the sum by 12 mm, which is the slice thickness plus the interslice gap. The hamstring muscles comprise the ST, SM, BF, and gracilis (G). The ST muscle length was defined as the length from the proximal musculo-tendinosus junction to the distal musculo-tendinosus junction of the ST on proton destiny images. ST tendon regeneration was identified by an orthopedic surgeon and classified according to the presence or absence of a regenerated tendon. Regeneration failure was defined when a regenerated tendon could not be visualized in any view.
Muscle strength testing Isometric knee flexion torque was measured using a dynamometer (Biodex System III, Biodex Co., New York, New York, USA). Subjects were instructed to take a prone position, with a hip flexion angle of 0° and the lower body tightly secured to the seat (Fig. 1). Before evaluation, compensation was performed to exclude the effect of gravity on the measurement of torque. The isometric 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 were performed twice with a 1-min interval. The normal limb was tested before the operated limb. The peak torque value was normalized to the body weight and assessed as the parameter.
Data management and analysis Based on the power analysis study (Hoenig & Heisey, 2001), we estimated that to achieve 80% power with an alpha level of 0.05, a minimum of 21 subjects would be required. Each measurement from the operated limb was expressed as a percentage relative to that from the operated limb (% normal). To evaluate the relationship between hamstring muscle strength and morphology, the subjects were divided into three groups according to the morphological characteristics of the ST muscle-tendon complex in the operated limb (Table 1). Group 2, which showed muscle shortening despite the regenerated tendon, accounted for 13 of the 24 patients, followed by group 1 patients, whose tendons were regenerated and muscle lengths were unchanged, accounting for 8 patients, and group 3 patients, who showed muscle shortening but no tendon regeneration, accounting for 3 patients, the fewest among the three groups. A paired t-test was used to test for side-to-side differences in CSA of the ST tendon, ST muscle length, and ST muscle volume. One-way analysis of variance was used to test for task differences in knee flexion torque, and for differences in each hamstring 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, semimembranosus; ST, semitendinosus. Table 2. Isometric knee flexion torque shown as a percentage of body weight
Fig. 2. Axial magnetic resonance image of the semitendinosus tendon (arrow): (a) regenerated; (b) undetected. Table 1. Morphology of the semitendinosus muscle
Normal limb CSA of the semitendinosus tendon (cm2) Muscle length of the semitendinosus (cm) Muscle volume of the semitendinosus (cm3)
Operated limb
0.10 ± 0.02
0.27 ± 0.13**
27.7 ± 0.3
24.2 ± 0.4**
178.9 ± 55.1
132.8 ± 44.3**
The values are mean ± SD. **P < 0.01, compared with the normal limb.
performed to determine the relationship between measurements and the causative factors of decreased knee flexion torque. Statistical significance was set at P < 0.05. A post-hoc test was performed for each variable to determine statistical power. Descriptive data are expressed as mean and standard deviation (SD) values.
Results MRI and measurements In 21 of the 24 patients, ST tendon regeneration was confirmed (Fig. 2). The ST muscle length in the operated limb (24.2 ± 0.38 cm) was significantly shorter than that in the normal limb (27.7 ± 0.25 cm, P < 0.001). The CSA of the ST tendon in the operated limb (0.10 ± 0.02 cm2) was significantly larger than that in the normal limb (0.27 ± 0.13 cm2, P < 0.001) (Table 1). The ST volume in the operated limb was significantly smaller than that in the normal limb; however, the SM, BF, and
Knee flexion angle
Normal limb
Operated limb
F30 F45 F60 F90 F105
129.3 ± 18.0 115.8 ± 18.7 105.5 ± 18.0 73.9 ± 19.0 61.9 ± 16.7
117.9 ± 28.0 102.6 ± 26.6 88.3 ± 21.8** 50.1 ± 16.0** 44.1 ± 14.7**
F30, isometric knee flexion torque at 30°. **P < 0.01, compared with the normal limb.
G volumes in the operated limb were approximately the same as those in the normal limb (P < 0.01) (Table 1; Fig. 3). Muscle strength testing The isometric knee flexion torque in the operated limb was significantly lower than that in the normal limb at 60° (88 ± 21% of body weight; %BW), 90° (50 ± 16%BW), and 105° (44 ± 14%BW), respectively (P < 0.01); however, the difference was not significant at 30° (117 ± 28%BW) and 45° (102 ± 26%BW) (Table 2). The percentage of the isometric knee flexion torque of the operated limb compared with that of the normal limb 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). Relationship between hamstring muscle strength and morphology We found a significant correlation between ST muscle length and knee flexion torque at 60° (r = 0.458, P = 0.042; Table 3). ST muscle volume was significantly correlated with knee flexion torque at 30° (r = 0.427, P = 0.047), 45° (r = 0.432, P = 0.045), and 60° (r = 0.611, P < 0.01). Figures 5 and 6 summarize for each of 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 Muscle length of the semitendinosus Muscle volume of the semitendinosus
0.242 0.250 0.427*
0.188 0.292 0.432*
0.129 0.458* 0.611**
0.041 0.234 0.027
0.379 0.220 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.
Fig. 5. Results of knee flexion torque regarding the morphology of the semitendinosus muscle-tendon complex (% normal).
torque and ST muscle volume in the operated limb relative to those in the normal limb (% normal). In group 1, the knee flexion torque and ST muscle volume in the operated limb were the same as those in the normal limb (86 ± 10%, muscle volume; 100 ± 31%, flexion torque at 30°). However, in groups 2 and 3, the knee flexion torque in the operated limb was lower than that in the normal limb (88 ± 12%, group 2; 78 ± 3%, group 3). Moreover, the ST muscle volume in the operated limb was smaller than that in the normal limb (71 ± 11%, group 2; 52 ± 3%, group 3).
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Discussion This study was designed to assess the strength and morphological 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) confirmed the regenerated ST tendon in MRIs obtained at the level of the tibial plateau and superior pole of the patella, respectively. However, the location of the musculo-tendinosus junction shifted proximally when compared with the normal limb. In our study, ST tendon regeneration was confirmed in approximately 88% of patients after ACL reconstruction surgery, and the CSA in the operated side was enlarged by a mean of approximately 2.7 times that in the normal side. Meanwhile, compared with the normal side, the ST muscle length in the operated side was shortened by a mean of approximately 3.5 cm and the muscle volume was also reduced by approximately 74%. This finding was similar to that of previous studies (Simonian et al., 1997; Nishino et al., 2006; Choi et al., 2012). In the muscle volume measurement conducted in this study, the G, a knee flexor muscle, was assessed in
Hamstring muscle strength and morphology addition to the BF, SM, and ST, which were studied by Nishino et al. (2006). It has been also shown that ST muscle atrophy was not accompanied by a compensatory hypertrophy of the BF and SM. In addition, our experimental results confirmed the absence of a compensatory hypertrophy of the G, which is a fusiform muscle like the ST. These findings show that ST muscle atrophy is impossible to compensate, even by knee flexor muscles of the same category. Although we mention details later, this ST muscle atrophy could be a causative factor of knee flexion deficits. An isometric knee flexion torque allowed for a recovery of approximately 90% at a 30° or 45° knee joint flexion but showed a significant decrease at a 60°, 90°, or 105° knee joint flexion. Like the findings reported by Tashiro et al. (2003), our results suggest that deficits in deep knee flexion torque occurred after ST tendon resection. Meanwhile, by obtaining MRI scans using the tagging snapshot technique, Hioki et al. (2003) observed the dynamics of the ST muscle during knee joint flexion and confirmed the equal movements of the operated and normal sides. Likewise, Takeda et al. (2006) also measured the T2 value (the transverse relaxation time) of the hamstring muscle group after knee flexion tasks and confirmed that the latter was functional in the normal and operated sides, regardless of the state of regeneration. It has been recognized that the regenerated tendon is considered to function similar to the original ST tendon when generating knee joint torque. However, the exercise challenges performed in the previous studies consisted of a 0°–45° concentric contraction of the knee joints in the prone position and an isokinetic contraction in the sitting position, and because both challenges were not performed in the prone position/deep knee flexion, in which the ST is greatly involved, the decline in the function of the ST is believed to have not occurred. Consistent with the findings of Tadokoro et al. (2007) regarding the relationship between hamstring strength and morphology, no relationship was found between the CSA of the regenerated ST tendon and the knee flexion torque; however, the volume and length of the ST muscle showed a positive correlation with knee flexion torque. That is, the decrease in knee flexion torque occurs when muscle shortening and muscle atrophy are present. Compared with groups 2 and 3, group 1 was less likely to have decreased ST muscle volume and length, and knee flexion torque. These findings suggest that because ST is a fusiform muscle, it undergoes muscle length shortening, as in the case of groups 2 and 3, and causes an equivalent shortening of the muscle fibers. When muscle fibers are shortened in relation to their original state, the relationship between muscle force and length is likely to change and the ST muscle may also show functional changes. In addition, when ST muscle shortening occurs in the absence of a regenerated ST tendon (as in the case of group 3) and when the muscle has no site of attachment to the tibia, the torque-generating capacity of the
ST muscle decreases and the function of the tendon to convey the torque-generating capacity of the ST muscle to the tibia could also decline. Nevertheless, the fact remains that the hamstring tendon graft is the mainstream method for ACL reconstruction. It is also true that satisfactory result was obtained in most of patients. This could be because the function of the hamstring is more important at extended or slightly knee flexed position. Considering the advantages and disadvantages of the hamstring tendon graft and other graft, we think that choosing the best procedure for ACL reconstruction depends on the types of athletic activity in which athletes participate. Therefore, a more active rehabilitation for hamstring is needed to minimize hamstring muscle weakness and maximize athletic performance, when we use hamstring tendon graft. The hamstring muscle rehabilitation in this study did not include strengthening exercises at deep knee flexion. Kubota et al. (2007) observed the regional differences of MRI measurements in the hamstring following knee-eccentric flexion exercise. Consequently, CSA and transverse relaxation times of the ST were increased significantly compared with those of the BF or SM. This result indicated that ST muscle responds to kneeeccentric flexion exercise by strengthening only pararell fibered muscles. We are currently conducting new research that assesses the effects of the Nordic hamstring, which is simple eccentric hamstring exercise. Further research may reveal how we can prevent hamstring muscle weakness after tendon harvest. A limitation of this study was the large variation in post-operative time. The mean ± SD post-operative time was 27.7 ± 18.2 months (range 12–72 months) after reconstruction. This variability shows that the sample of patients with ACL reconstruction was heterogeneous in relation to post-operative time. Eriksson et al. (1999) revealed that ST tendon is gradually remodeled into a tendon-like structure. This time-based phenomenon may correspond to morphological changes in ST muscletendon complex. We found that morphological changes in the ST correlated with hamstring weakness; it could be influenced by recovery of the ST muscle-tendon complex. Therefore, further research is needed to assess morphology and strength at different post-operative times. Despite the limitation, the information provided herein might provide insight for better understanding of several morphological and functional behaviors of the hamstring muscle group after harvesting the ST tendon. Based on a series of considerations, morphological changes (tendon regeneration, muscle shortening, and muscle atrophy) that accompany ST tendon resection were indicated to be the cause of knee flexion deficits. In addition, the results pertaining to the hamstring muscle volume show that tendon function could not be compensated by muscles other than the ST muscle. Therefore, prevention of muscle shortening and muscle atrophy is
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Nomura et al. important to suppress decreased knee flexion torque as a result of ACL reconstruction surgery. A future study on surgical techniques, rehabilitation, and exercises is necessary to further investigate and improve approaches to prevent morphological changes the ST muscle-tendon complex. Our results suggest that ST tendon regeneration, ST muscle shortening, and ST muscle atrophy were significantly correlated with hamstring muscle strength. Consequently, preservation of ST morphology after ACL reconstruction is important. Perspectives Considering all the possible morphological evaluation variables (tendon regeneration, CSA, and muscle length and volume) and the isometric strength test results in this study, the most important finding is that the morphological changes after harvesting the ST tendon correlated with hamstring muscle strength. Moreover, this strength deficit remained even after subjects returned to their previous sports activities and completed the rehabilitation program. This study revealed that the causative
factors of decreased hamstring muscle strength were (a) absence of a regenerated ST tendon; (b) ST muscle shortening; and (c) ST muscle atrophy. In fact, ST tendon regeneration and ST muscle shortening were dependent on the surgical technique used in harvesting the ST tendon, suggesting that the management approach for ST muscle atrophy is especially important in the rehabilitation after ACL reconstruction, which tend to overemphasize hamstring exercises. A further direction of this study will be to develop the surgical technique for harvesting a graft and to examine a more active rehabilitation for the hamstring muscle, such as deep knee flexion or eccentric hamstring exercises. Key words: Anterior cruciate ligament, semitendinosus, flexion torque, muscle volume, MRI.
Acknowledgements The authors gratefully acknowledge A. Nishino and A. Sanada for their assistance in the preparation of this research. The authors also thank Waseda University and all the participants in this study for their cooperation.
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