Department of Orthopedic Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 300 Gumi-dong, Bundang-gu, Seongnam-si, Gyeonggi-do 463-707, Korea
Department of Orthopedic Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 300 Gumi-dong, Bundang-gu, Seongnam-si, Gyeonggi-do 463-707, Korea. T: +82-31-787-7198; F: +82-31-787-4056.
Tendon injury is a commonly encountered clinical entity that may result from trauma or arthritis. If tendon repair after injury is delayed, the muscle-tendon unit contracts and several pathologic changes occur in the muscle, including increased intramuscular connective tissue, decreased capillary density, Z-disc streaming, early muscle fiber necrosis, and decreased twitch tension, finally resulting in irreversible muscle contracture.1–4
When the muscle contracture has not become irreversible in a neglected tendon injury, direct repair or interpositional tendon grafting can be used. If the muscle contracture has become irreversible, however, these methods will not restore the muscle function, thus tendon transfer using a new motor is required to restore the lost function. For example, in cases of old ruptures of the Achilles or extensor pollicis longus tendons, many clinicians have used either tendon transfer5–7 or tendon grafting8–10 for their late reconstruction. If possible, restoring the continuity of the injured muscle-tendon unit is preferable to sacrificing another muscle by tendon transfer. The decision between tendon grafting and tendon transfer will depend on the expected functional recovery of the injured muscle; If the contracted muscle still retains considerable function or a potential to recover function after tendon repair, then tendon grafting will be possible.
Empirically, surgeons have estimated the degree of muscle contracture, without substantial evidence, by referring to the time between injury and operation, muscle length (tendon retraction) and passive muscle excursion at the time of operation. Concerning the muscle length and muscle excursion, Chung et al.11 showed in a rabbit soleus tenotomy model that muscle contracture occurred the least when maximal muscle length was preserved within 4 weeks of injury, but that after 4 weeks muscle contracture developed the least when half of its excursion was maintained by passive motion. We hypothesized that passive muscle excursion observed during surgery can be a prognostic indicator of muscle recovery after tendon repair in neglected tendon injuries. Although pathologic changes in muscle after tenotomy are recognized, recovery of muscle after delayed tendon repair has not been assessed previously. The purpose of this study was to observe the time-dependent changes of muscle excursion after a tendon injury, and to determine how much muscle recovery can be expected after tendon repair with the given muscle excursion observed during surgery in a rabbit soleus muscle model.
MATERIALS AND METHODS
Institutional animal care and use committee approval was obtained and experimentation was conducted in accordance with our institution's guidelines for the care and use of laboratory animals. Experiments were performed on 24 skeletally mature, New Zealand White male rabbits (average 24 weeks old, 3.5 ± 0.5 kg).
Eighteen animals were randomly assigned to three groups and the groups were defined based on the duration from injury (tenotomy) to operation (tendon repair). The operations in each animal were bilateral, thus the number of soleus muscles in each group was 12. Tendon repair was performed at 2 weeks (group A), 4 weeks (group B), and 6 weeks (group C) after tenotomy. Muscle excursions were measured at baseline, and at 2, 4, and 6 weeks after tenotomy in each group, and 8 weeks after tendon repair in all groups. Power analysis determined that 12 muscles were needed in each group to demonstrate a 10% difference in muscle excursion between the groups at an α level of 0.05 and a β value of 0.80.
Surgical Procedures and Measurement of Excursions
All animals were maintained in conventional plastic cages and fed ab libitum with laboratory food and tap water. Anaesthesia was induced with an intramuscular injection of 15 mg/kg of Zoletil 20 (Zoletil 20 mg/mL, Tiletamine 50 mg, and Zolazepam 50 mg, Virbac, Carros, France) and 5 mg/kg of Rompun (xylazine hydrochloride 23.32 mg/mL, Bayer Korea, Seol, South Korea) and maintained by inhalation anesthesia using enflurane, which provided approximately 30 min of adequate sedation. The hind limbs were shaved and animals were positioned prone with the knee in full extension and the ankle hanging free over the operating table. Under aseptic conditions, a longitudinal skin incision was made over the posterior side of the hind limb and the soleus was exposed. The tendinous portion of the soleus was separated from the conjoined achilles tendon and was transected in pattern of Z-plasty, which was to repair the tendon later without interposition tendon graft, from 1 to 3 cm above the insertion to the calcaneus (Fig. 1). Baseline excursion of the soleus muscle was measured by using a digital caliper. The normal excursion of the soleus tendon was defined as the distance that a point of its tendon moved from maximal ankle flexion to maximal ankle extension, based on that the amount of tendon excursion is related to the amount of joint motion.12
After tenotomy, group A had tendon repair at 2 weeks, group B at 4 weeks, and group C at 6 weeks. Before tendon repair in each animal, we released the proximal stump completely from the adhesion with surrounding tissue, and the excursions of the contracted soleus muscle were re-assessed by measuring the distance that the tenotomized proximal tendon end can move from the retracted position to the maximal pull of the tendon with a hemostat. The force of pulling applied by the operating surgeon was maximally set to the point when no apparent plastic deformation occurred by stretching of the tendon.
The soleus tendon was repaired to the distal conjoined Achilles tendon with its proximal tendon being at the half of its excursion and with the ankle in neutral extension, using the augmented Becker method.13 After tendon repair, both limbs were immobilized in a short leg cast to prevent ankle extension for 4 weeks, and then the animals were allowed to move freely after cast off for another 4 weeks.
Eight weeks after tendon repair, all animals were re-examined for the excursion of the repaired soleus muscles. The repaired soleus tendon was cut and its excursion was measured using the same method as was done during tendon repair procedure.
Two animals developed complications, that is, 1 case of infection and 1 case of early death. These animals were replaced with new animals and the same protocol was applied to them, thus a total of 20 animals were used for the study, and 36 soleus muscles in 18 animals were examined.
Time-dependent changes of muscle excursion of each group (N = 12) were assessed by using the Friedman test. Comparisons of muscle excursion among three groups at each time of tenotomy, tendon repair, and 8 weeks after tendon repair were done by the Kruskal–Wallis test. The Mann Whitney test was performed for post hoc analysis and the level of significance was set at p = 0.01 to adjust for multiple comparison.
Multiple regression analysis was used to find the explanatory variables that significantly affected muscle recovery (%) in a total of 36 limbs. Univariate analyses were performed initially. Pearson's correlation coefficient was used to assess the relationship between the muscle recovery and explanatory variables. Potential explanatory variables consisted of baseline muscle excursion (mm), muscle excursion at the time of tendon repair (%), and timing of repair (weeks). Variables significant at p = 0.1 in the univariate study were included as an explanatory variable in the relevant multiple regression, and backward stepwise method was used for analysis. A study of the residuals was performed, and goodness-of-fit was presented as an adjusted R2 value. The significance level was set at p = 0.05 in multiple regression. The SPSS software package (version 13.0, SPSS, Inc., Chicago, IL) was used and statistical significance was accepted at p = 0.05 other than post hoc analysis.
Our first purpose was to observe the time-dependent changes of muscle excursion after tendon injury. At baseline, the average excursion of all the soleus muscles were 13.6 mm (N = 36). After tenotomy, the mean excursion decreased to 9.6 mm (73%) by 2 weeks (group A, N = 12), to 7.6 mm (54%) by 4 weeks (group B, N = 12), and further to 6.9 mm (50%) by 6 weeks (group C, N = 12). The decrease of muscle excursion was significant between the groups (p < 0.001, Kruskal–Wallis test). Post hoc analysis of the side-to-side differences between the groups indicated that the amount of decrease was significantly larger during the first 2 weeks (from 100% to 73%) and during the second 2 weeks (from 73% to 54%) than during the last 2 weeks (from 54% to 50%), indicating that the decrease of muscle excursion occurs mostly during the first 4 weeks after tenotomy (Table 1).
The second purpose of this study was to determine how much muscle recovery in terms of muscle excursion can be expected after tendon repair with the given muscle excursions observed during surgery. Eight weeks after tendon repair, the average muscle excursion of the soleus muscles was 11.6 mm (89% of the baseline, 16% increase after repair) in group A, 9.8 mm (69% of the baseline, 15% increase after repair) in group B, and 7.3 mm (51% of the baseline, 1% increase after repair) in group C. Percentage of recovery was significantly larger in group A and B than group C (all p < 0.001) (Table 1).
Multiple regression analysis was used to find how much the explanatory variables affected the recovery of muscle excursion, and identified that both the muscle excursion at the time of tendon repair and the timing of repair independently affected muscle recovery significantly, explaining 94% of the variance (Table 2). The muscle excursion recovery (%) increased on average by 0.6% as the muscle excursion at the time of tendon repair increased by 1% after adjusting for the timing of repair, that is, the muscle excursion recovered in proportion to the percentage of the observed muscle excursion at the time of repair.
Table 2. Factors Affecting Muscle Recovery (%)
A study of the residuals in multiple regression analysis indicated that the assumptions of normality and homogeneity of variance were satisfied.
The adjusted R2 was 0.939.
Excursion at tendon repair (%)
Timing of repair (weeks)
In this study, we assessed if the muscle excursion observed during surgery can be a prognostic indicator of muscle excursion recovery after tendon repair in neglected tendon injuries. The results indicated that muscle excursion changes according to the time between injury and surgery, and that the amount of muscle excursion recovery depends independently on the timing of surgery and on the muscle excursion observed during surgery, suggesting that muscle excursion can be a prognostic indicator.
This information, if extrapolated to clinical practices, can be useful in that surgeons may estimate how much muscle excursion recovery will occur after delayed tendon repair by measuring the muscle excursion during operation, as average excursions of the human muscles are known, although there can be individual variations.14 For example, if we repair an old extensor pollicis longus rupture and the measured excursion during operation is 3.5 cm, it is 60% of the normal excursion of the muscle, which is 5.8 cm according to Curtis.15 Thus we can expect 36% (60 × 0.6%) recovery from the current muscle excursion 8 weeks postoperatively, which is about 1.3 cm (3.5 cm × 36%). The final muscle excursion at 8 weeks will be 4.8 cm (3.5 cm + 1.3 cm), which is considered to be clinically long enough for thumb extension function.
The time between injury and operation and muscle length (tendon retraction) can also be the reference. However, the timing of injury depends on patients' memory and the muscle length (tendon retraction) may depend on the adherence of the tendon to the surrounding tissue. Moreover, there are some controversies regarding the time between injury and operation and irreversible muscle atrophy. In an experimental study, Józsa et al.16 demonstrated that if there is delay in suturing a tendon after injury more than 6 weeks after tenotomy, then muscle atrophy and intramuscular fibrosis will persist and complete regeneration will never be possible. This was supported by our study that the excursion improved by only 1% when the repair was done after 6 weeks of tenotomy. On the contrary, Magnell et al.9 reported satisfactory outcome of interpositional mini tendon graft in patients with up to 21 weeks of treatment delay, suggesting that muscle contractures appeared to be reversible. Saur et al.10 also successfully reconstructed the ruptured extensor pollicis longus tendon using a tendon graft, and the time between tendon rupture and reconstruction ranged to even 40 weeks. However, the good results obtained in those studies after a long delay of treatment may be because the proximal tendon retraction was limited by adhesion and thus some muscle excursion was retained somehow by the passive joint motion.
In this study, we used different methods in measuring the muscle excursion. We measured the baseline muscle excursion by moving the maximum range of ankle motion, and then measured the decreased excursion in the subsequent operations by retracting the tendon distally. It was because we thought that these methods are more relevant to the clinical situation of delayed tendon repair; we know the average normal excursion of a muscle from the data obtained by measuring tendon movement during joint motion (as in the method we used for the baseline excursion measurement), and we actually measure the excursion of an injured muscle during tendon repair by pulling the proximally retracted tendon (as in the method we used for the subsequent measurements).
The present study has several limitations that require consideration. First, we studied for only 8 weeks after tendon repair and had no information of further change with time. There is a possibility of further muscle recovery or delayed initiation of muscle recovery. Second, we only evaluated muscle excursion in the assessment of muscle recovery. Other histological or functional aspects such as muscle fibrosis, muscle volume, muscle power, or electrophysiologic assessment should have been informative. Third, we did not have a sham operation group in which animals had immediate tendon repair and casting to know how much this would have reduced the excursion. However, we believe the effects of surgery itself and casting are minimal, considering that Group A had improvement of nearly 90% of the excursion. Forth, this study was conducted only on soleus muscle, thus the results obtained from this muscle cannot represent general muscle physiology, as most studies have demonstrated that some changes are partly dependent on the muscular profile.17 Moreover, the soleus muscle has a postural function and its tendon is short and strong, compared with clinically relevant hand muscles which have a long and weak tendon. Lastly, we performed the same intervention on both limbs in each rabbit and counted them as independent limb. Although this should have reduced the number of sacrifice of the animals, it might be the defect in that both limbs usually have very similar data.
In summary, this study demonstrated that in a rabbit soleus muscle, muscle excursion at the time of tendon repair was a prognostic indicator of muscle excursion recovery 8 weeks postoperatively. Further clinical studies looking at this relationship may help physicians estimate the potential of muscle recovery by assessing the muscle excursion in cases of delayed tendon repair.
This work was supported in part by the Institution's Basic Research Fund (03-2008-011). We thank Dr. Moon Seok Park for his advice on statistics, and Mr. Suk Hyun Lim for his excellent illustration of Figure 1. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subjects of this article.