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1Institute of Orthopaedic Research and Biomechanics, University of Ulm, Ulm; 2Department of Neurology, University of Freiburg, Freiburg; and 3Department of Trauma and Reconstructive Surgery, University Hospital Rechts der Isar of the Technical University of Munich, Munich, Germany
Submitted 17 May 2006; accepted in final form 18 August 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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; Johansson et al. 1990; More et al. 1993). Moreover, the ACL with a tensile strength of 
2.000 N (Woo et al. 1991) not only has a mechanical function but, as was shown in histological studies (Freeman and Wyke 1967; Haus and Halata 1990; Schutte et al. 1987; Sjolander et al. 1989; Zimny et al. 1986), also contains different types of mechanoreceptors, most of which are located close to the ligament insertion sites (Raunest et al. 1998). Animal experiments provided the first evidence of a specific reflex arc between the ACL and the hamstrings and suggested a contribution of the ACL in the neuromuscular stabilization of the knee (Johansson et al. 1991; More et al. 1993; Solomonow et al. 1987). More recent studies on humans were able to demonstrate such a reflex arc between the knee and the hamstrings after electrical stimulation (Dyrhe-Poulsen and Krogsgaard 2000; Miyatsu et al. 1993; Tsuda et al. 2003) and under functional conditions (Beard et al. 1993; Bruhn 1999; Friemert et al. 2005a). In addition, Friemert et al. (2005a) provided evidence that this reflexive muscle response consisted of a monosynaptic reflex of the hamstrings (short-latency response, SLR), mediated by group I afferents and a later second presumably polysynaptic reflex (medium-latency response, MLR).
Clinical tests such as the angle reproduction test, posturography, and gait analysis revealed pathological changes after ACL rupture (Beard et al. 2000, 2001; Hogervorst and Brand 1998; Jerosch and Prymka 1996). Despite successful ACL surgery, patients report, for example, symptoms of knee instability and complain of a feeling of "giving way" that may arise from loss of proprioception and altered stretch reflex excitability. There are, however, also patients who have mechanical instability (no surgery) but no "giving way" symptoms. In addition, it is still unclear whether the "giving way" phenomenon is associated with mechanical knee instability. Beard et al. (1994) and Bruhn (1999) mechanically induced posterior–anterior tibial translation in patients with ACL rupture during standing and reported a significant increase in the latency of the ACL–hamstring reflex. These studies and that of Wojtys et al. (1994) for the first time provided evidence for the presence of altered stretch reflex excitability. However, they did not describe the possible underlying neurophysiological mechanisms and its connection with the kinematic characteristics of tibial translation. An understanding of these qualitative aspects, however, is of primary importance in planning the therapeutic intervention. The authors of these studies also failed to draw conclusions concerning the clinical relevance (e.g., indication for surgery) for patients with or without "giving way" symptoms.
The objective of this study was to assess quantitatively hamstring activity and the mechanical characteristics of posterior–anterior tibial movement in response to mechanically induced tibial translation in patients with ACL rupture. To identify possible differences in sensorimotor knee function within the patient population, the subjects were divided into a group with "giving way" symptoms and compared with a group without "giving way" symptoms. The aim was to investigate whether the subjective feeling of "giving way" is related to any objective difference in hamstring reflexes. Accordingly, the hypothesis of the study was that giving way symptoms are rather associated with alterations in sensorimotor function than with increased mechanical instability. Furthermore, we presume that this disturbed sensorimotor function is related to significant changes in the hamstring reflex excitability.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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A total of 21 patients (mean age: 25 ± 4.5 yr; height: 180 ± 7.5 cm; weight: 83.5 ± 15.2 kg) with isolated ACL ruptures took part in the study. Patients with effusion, pain, blockade, additional capsuloligamentous injuries, and meniscus or cartilage injuries were excluded, whereas 83 patients with clinically suspected ACL injury were screened. Objective measures were MRI of the knee before classification as coper or noncoper to ensure the isolated injury. Fifty-eight patients had to be excluded after MRI of the knee because of additional injuries. The remaining 25 patients underwent the experimental procedure the day before arthroscopy. After reflex measurements arthroscopy was performed and again four of 25 patients were excluded from the analysis because of additional knee injuries. The way that classification was performed in our study was aimed to strictly identify only patients with isolated ACL ruptures as copers, who never had experienced any "giving way" symptom after the acute injury symptoms had been resolved (i.e., after they were free of pain and effusion and had regained full range of knee motion). Patients were asked four questions (see Table 1) and only if all were answered in the direction of copers, they were classified as copers. Accordingly, from a functional perspective copers in our study were in daily life without "subjective" symptoms. All the remaining patients were classified as noncopers even if they reported only a single subjective feeling of "giving way."
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, who accepted even one episode of giving way for copers. This "subjective self-assessment" of the patient was the unique criterion and was performed before the reflex measurement. Because the aim of the study was to discern only on the basis of the subjective feeling of giving way being ever present to classify as a noncoper, the additional physical scores used in other studies were not used for the prospective classification because even a good score would have not led to a classification as coper. Based on the questionnaire we classified nine patients as copers and 12 patients as noncopers. The classification was performed after a mean of 77 ± 53 days (range 19–211) after the trauma. There were no differences between copers (75 ± 32 days, range 41–128) and noncopers (79 ± 64 days, range 19–211, P = 0.27). Before the tests, the patients had given their written informed consent. The study was approved by the ethics committee of the University of Ulm. Experimental setup
The patients were examined in bipedal stance bearing full body weight (at 30° of knee flexion and 5° of external rotation). There was no significant difference in the hamstring baseline EMG activity between the injured and the uninjured legs and there was also no significant difference in the baseline activity between copers and noncopers. A force of 300 N was applied to the proximal section of the lower leg (10 cm below the popliteal fossa) parallel to the tibial plateau to induce posterior–anterior tibial translation in the healthy and injured legs. Before measurements, the height of the patella-supporting plate was individually adjusted to achieve the knee flexion angle of 30°. The patella was pressed against a supporting plate to ensure isolated movement of the tibia relative to the femur and prevent movement of the entire leg. A linear potentiometer (independent linearity: 0.25 ± 0.0075%, repeatability: 0.002 mm; Novotechnik, Ostfildern, Germany) was placed on the tibial tuberosity and measured (functional) tibial translation. The onset of tibial movement was used as a trigger signal for the measurement of reflex latency (Fig. 1). To reduce the variability of individual measurements we performed in each patient a total of 50 single measurements in 10 trials, each of which consisted of five single measurements. In addition, KT1000 arthrometer measurements (MEDmetric, San Diego, CA) were conducted to assess anterior tibia translation. Although the reliability of this device has been questioned in the literature (Wroble et al. 1990), the more recent studies indicate that KT1000/KT2000 measurements have a sufficient reliability to assess anterior tibia translation during lying as performed in the present study (e.g., Huber et al. 1997; Myrer et al. 1996). Knee joint stability was determined in the healthy and injured legs performing three measurements in each leg. To ensure reliability of testing, all measurements were performed by the same investigator, who is an orthopedic surgeon and has ample experience in KT1000 measurements.
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Reflex activity in the hamstring muscles and the vastus medialis was measured using surface EMG. Pairs of self-adhesive bipolar electrodes (interelectrode distance 2 cm, Arbo Ag/AgCl sensor; Tyco Healthcare, Neustadt, Germany) were arranged longitudinally on the muscle bellies in the middle between the knee joint gap and buttocks gap of the femoral biceps muscle (lateral hamstring) and the semimembranosus/semitendinous muscle (medial hamstring). The m. vastus medialis was recorded 2–3 cm medially and 5 cm proximally from the upper patella rim. The reference electrode was placed on the medial malleolus. The skin was shaved, abraded, and cleaned with alcohol before the electrodes were attached. A commercially available EMG measuring and evaluation software (Daisy Lab Biovision, Weilheim, Germany) was used for recording and analyzing the muscular activity of the hamstrings (band-pass filter: 10–700 Hz, sixth-order Butterworth, preamplification: 1,000, sampling rate: 5,000 Hz). For further analysis, the EMG signals were rectified and averaged. Normally the recordings of the medial hamstrings were taken for analysis because it was previously shown that there are no significant differences between the lateral and medial hamstrings with respect to the onset latencies of SLR and MLR (Friemert et al. 2005a,b). As a result of artifacts or technical difficulties for the medial hamstring recordings of three subjects, the EMG activity of the lateral hamstrings was analyzed.
Data analysis
Two of the authors analyzed the EMG data of all subjects. Both were blinded as to whether the subjects had been classified as copers or noncopers. Onset latencies and the integrated EMGs (iEMGs) of the hamstring muscles were assessed manually on the computer using two cursors. The onset latency of the first response was defined as the time window from the beginning of tibial translation to the first significant muscular activity. In the case of superimposed responses (first response: monosynaptic reflex = SLR, second response: polysynaptic reflex = MLR), the evaluation algorithm introduced by Friemert et al. (2005a) was used to ensure valid data analysis and to clearly differentiate between SLR and MLR. The MLR evaluation window was defined as a 30-ms period beginning with the onset of the MLR. The iEMG (SLR and MLR) was calculated as the area under the rectified signal. Additionally, the iEMG activity in hamstring and vastus muscles was assessed during the 30 ms before the beginning of tibia translation. Maximum tibia translation was determined on the basis of the tibial translation curves (Fig. 1).
Statistical analysis
All values are means ± SDs. Differences between healthy and injured legs were analyzed using a paired Student's t-test. The statistical significance of comparisons between the noncopers and the copers was calculated using Wilcoxon's nonparametric test. A P value of <0.05 was considered statistically significant. The Pearson correlation coefficient was calculated to identify a correlation between anterior tibial translation during stance and MLR latency of all injured patients.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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There was no significant difference in SLR onset latencies between the healthy legs (19.1 ± 3.5 ms) and the injured legs (19.9 ± 3.3 ms) (P = 0.21; Fig. 2A). By contrast, significantly longer MLR onset latencies (P < 0.001) were measured for the injured legs (56.3 ± 13.3 ms) compared with those for the healthy legs (35.8 ± 3.8 ms). An ACL injury had no significant effect on the integrals for SLRs (P = 0.12) and MLRs (P = 0.35). A significant increase in tibial translation, which gives an indirect measure of mechanical joint stability in the posterior–anterior direction, was noted for the injured legs. Whereas during stance a maximum tibial translation of 6.4 mm (±1.5) was measured for healthy legs, a tibia translation of 8.5 mm (±2.5) was noted for injured legs (P < 0.001). Likewise, the KT1000 test showed a significant increase in posterior–anterior joint instability in the injured leg compared with that in the healthy leg (5.6 ± 1.8 vs. 9.7 ± 2.2 mm; P < 0.001; Fig. 2B). There was also no relationship between tibial translation during stance and MLR response latency if all injured legs were considered (r2 = 0.22, Fig. 3). No difference in the ratio of the iEMG activity 30 ms before the tibia translation of the hamstring and quadriceps (vastus medialis) muscles between the unaffected leg and the affected leg was found (1.39 ± 1.32 vs. 1.45 ± 0.87, P = 0.86). In addition, there was also no statistically significant difference if the absolute iEMG of the quadriceps (P = 0.215) or the hamstrings (P = 0.236) was compared between the healthy and the injured legs.
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A comparison between the healthy legs of copers and noncopers revealed no significant differences in MLR onset latency (36 ± 4.1 vs. 35.8 ± 3.9 ms; P = 0.81), maximum tibial translation (P = 0.59), or the KT1000 test (P = 0.67). A significantly longer MLR onset latency, however, was measured for the injured legs of the noncopers (P = 0.01; Fig. 4A). Whereas the copers had an MLR onset latency of 47.9 ± 8.1 ms, the noncopers showed a reflex response after anterior tibial translation that occurred considerably later (62.6 ± 13.2 ms). Neither the KT1000 test (P = 0.97) nor functional posterior–anterior tibial translation (P = 0.31) showed significant differences between the two groups (Fig. 4B). The integrals revealed no significant between-group differences, for either the healthy legs (SLR P = 0.95, MLR P = 0.37) or the injured legs (SLR, P = 0.18; MLR, P = 0.78). We found no difference in the iEMG hamstrings/quadriceps ratio for the patients classified as copers and noncopers (1.46 ± 0.77 vs. 1.44 ± 1.07, P = 0.62). Finally, there was no difference in the mechanical stability (assessed by both KT1000 and by maximum tibia translation during stance) between these two groups, although there was a clear increase of tibia translation in the affected legs compared with that in the unaffected legs in both copers and noncopers.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Previous studies agree that an ACL rupture leads to a loss of proprioception in the knee-stabilizing muscles of the thigh (Hogervorst and Brand 1998), but they fail to identify the cause of this neurophysiological disorder. Di Fabio et al. (1992) reported changes in hamstring activity in subjects with ACL insufficiency. After an anterior–posterior sway no hamstring activity was found in the compensatory leg EMG activity in healthy legs, whereas they found hamstring activity in the ACL-deficient leg after 100 ms coupled with the automatic postural responses of quadriceps and tibialis muscle. Moreover, reflex activity of muscles was significantly increased in the ACL-deficient leg in unilateral stance, indicating an integration of the capsular-hamstring reflex in postural control to stiffen the knee joint after ACL rupture (Di Fabio et al. 1992). The authors suggested that a capsular-hamstring reflex is integrated into the existing structure of a preprogrammed postural synergy to compensate for ligamentous laxity. Accordingly, increased knee laxity seems to modulate central programming to compensate joint laxity and to maintain erect posture. If this is the case for long-loop reflexes it may also be the case for the MLRs with shorter latencies. Beard et al. (1993) and Bruhn (1999) found during stance a significant increase in the latency of the hamstring reflex induced by anterior tibia translation, which may be induced by a deficient proprioception. Our results confirm these studies and show that only the second component of the response (e.g., MLR), which is probably mediated by secondary muscle spindle (group II) afferents as shown in the soleus muscle during stance and gait (Grey et al. 2001; Schieppati et al. 1997), plays a major role in the sensorimotor function of the knee joint. Onset latencies of the MLR on the affected side with values around 63 ms could be close to the fastest long-latency responses (LLRs). For the soleus (Taube et al. 2006) as well as for the tibialis anterior muscle (Christensen et al. 2001; Petersen et al. 1998) the fastest transcortical responses have been shown to be earliest at around 85 ms. Given the longer travel distance of 2 x 30–45 cm (i.e., 60–90 cm) one may expect the fastest transcortical responses in the hamstrings 10–15 ms earlier (i.e., earliest at 70–75 ms). Accordingly, a transcortical component cannot be excluded for the upper range of the response latencies classified as "MLR" latencies. However, it seems unlikely that some of the noncopers show delayed MLR responses and no "fast" LLRs, whereas other noncopers show only fast LLRs. It seems more likely that this is a continuous delay of the MLRs. On the other hand, if it should be the case that in the noncopers the MLRs are suppressed and this is associated with the subjective feeling of instability, then one may still hypothesize that the MLR may play a major role for this subjective knee joint stability.
Dhaher et al. (2003) were able to show that in healthy subjects a mechanical valgus stimulation consistently elicits reflex responses in knee joint muscles with a latency of 83–92 ms, whereas stretch reflexes of the same target muscles showed latencies around 30 ms. They hypothesized that the muscle responses may originate from mechanoreceptors lying in periarticular tissues such as joint ligaments and capsule. A more recent study of the same group indicates that excitation of such reflexes from periarticular tissue afferents results in a significant increase of the joint adduction–abduction stiffness (Dhaher et al. 2005). They discussed that this reflex stiffness may have significance during functional tasks. The reflexes investigated in the present study showed onset latencies clearly <80 ms, even in the noncoper group. Accordingly, they can also contribute to the knee joint stiffness. The fact that the onset latency in the noncopers was obviously delayed compared with the copers and even more delayed compared with subjects with healthy knees may indicate a disturbance or delay in the processing of the afferent information arising from the knee during posterior–anterior tibia translation. This may be interpreted as a disturbance of the sensorimotor integration associated with isolated ACL injury. Because the subjective feeling of "giving way" was reported only by noncopers (i.e., patients with a rather long delay of the MLR response, whereas the copers showed only a moderate delay), one may hypothesize that this delay in MLR may also affect knee joint stiffness.
In a recent study, it was shown by intraoperative direct mechanical stimulation of the ACL that receptors within the ACL may be able to contribute to the hamstring MLR, although this contribution may be weak (Friemert et al. 2005b). However, there is a discrepancy between the latencies (SLR, MLR) of the present study as well as in our previous study (Friemert et al. 2005a) and those measured after intraoperative ACL stimulation (Friemert et al. 2005b) in healthy legs. A reason for the observations may be that intraoperative stimulation took place distal of the femur by direct mechanical stimulation of the ACL, whereas in the present experiments and in our previous study (Friemert et al. 2005a) the stimulation was an anterior tibia translation that affects the hamstring muscles to the knee, i.e., not only the muscle spindles in the distal but also in the proximal part of the muscle are stimulated at the same time. Accordingly, the distance from the afferent sensor to the spinal cord may be on average 25 cm shorter than during isolated stimulation of the ACL. If the conduction velocity of the contributing afferents was 60 m/s and one postulates that the information from the ACL is also mediated by afferents with similar conduction velocity, this would mean that the onset latency can be expected to be about 4 ms shorter. The changes in onset reflex latency observed in the present study are most probably the result of changes in the sensorimotor integration of this reflex component on the spinal level. This is particularly noteworthy because information from these afferent pathways arising from the hamstring muscle spindles is additionally modulated by the CNS by gamma motor neurons (Johansson et al. 1990). It is therefore possible that appropriate training stimuli may induce motor learning and, consequently, may improve knee sensorimotor function. These findings confirm previous assumptions about a supraspinal integration of this reflex (Fischer-Rasmussen et al. 2002; Johansson et al. 1990; Krauspe et al. 1992; Sojka et al. 1989). Beard et al. (1994) reported that the onset latencies of hamstring reflexes that were increased after ACL lesions improved after a 12-wk physiotherapy program. This may indicate that sensorimotor training, rehabilitative weight training, or functional training can help to restore sensorimotor control of the knee as recommended by Chmielewski et al. (2005b). Such beneficial effects were shown in a study by Friemert et al. (2006), where postoperative functional training within the first postoperative week significantly decreased the proprioceptive deficit.
Giving way
It is important to note that the criteria described in METHODS ensured that only patients who reported never to have experienced any symptoms of "giving way" were classified as copers. Our results on "giving way" of the knee provide quantitative evidence for the first time that the subjective feeling of instability is directly associated with the disturbance of the MLR pathway, whereas the SLR pathway is not affected and the mechanical stability of the knee was similar in copers and noncopers. This indicates that the altered stretch reflex excitability may be more important for the development of "giving way," than the mechanical instability of the knee. Kennedy et al. (1982) also postulated that a proprioceptive deficit rather than primary instability of the knee was the cause of "giving way." Although Beard et al. (1993) already reported a connection between "giving way" and loss of proprioception, they did not investigate whether there was also a correlation between instability and altered stretch reflex excitability. Using a passive angle reproduction test, Roberts et al. (1999) were able to detect significantly poorer proprioception in patients with "giving way" symptoms. By contrast, they found no differences in proprioception between symptomatic and asymptomatic patients in the active and visual angle reproduction tests. Our results support the findings reported by Kaalund et al. (1990). They described an altered timing of the hamstring activity under functional conditions when ACL-deficient patients walked uphill. A disturbed or delayed timing of the MLR may induce changes in the activation pattern.
It has been argued that there are changes in sensorimotor integration after ACL lesions on the basis of altered sensorimotor evoked potentials (SEPs) (Valeriani et al. 1996) and, in a small number of patients, it has been argued that differences in strategies of hamstring activation between copers and noncopers may be a result of changes in somatosensory integration (Courtney et al. 2005). Although in the present study the changes in MLR onset latency were significantly more marked in noncopers, the study of Courtney et al. (2005) found changes in SEPs in only one of four copers, although in all three noncopers they investigated. Unfortunately, it is not stated whether the changes were located in the periphery or the CNS and, furthermore, the patients were investigated 7–214 mo after the lesion, i.e., they were rather chronic patients. Future studies will have to investigate both MLRs and SEPs in the same patient at the same time to elucidate this question. Apart from SEPs, aberrant muscle recruitment and a decrease in quadriceps activity have also been described in noncopers, which may contribute to their instability of the knee (Chmielewski et al. 2005a; Williams et al. 2005). Our results suggest that the subjective feeling of instability (e.g., "giving way" symptom) is not associated with an increase in knee joint laxity. It is more likely that the "giving way" symptoms are related to alterations in stretch reflex excitability. This relationship should be considered in future evaluation of patients with knee instability and in the measurement of patient satisfaction, for example, on the basis of knee scores such as Tegner activity level and Lysholm score (Tegner and Lysholm 1985) and the International Knee Documentation Committee (IKDC) knee rating system (Hefti et al. 1993).
In conclusion, our study shows that ACL rupture causes considerable changes in stretch reflex excitability. "Giving way" of the knee is not simply related to the decrease in mechanical joint stability, but is closely associated with altered stretch reflex excitability that most probably takes place on the spinal level. Because sensorimotor function may be influenced by appropriate training stimuli, sensorimotor training early after ACL rupture with a focus on neuromuscular training may be promising for a rapid restoration of joint function.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. Faist, Department of Neurology, University of Freiburg, Breisacher Strasse 64, 79106 Freiburg, Germany (E-mail: faist{at}nz11.ukl.uni-freiburg.de)
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