KONISHI, Y., T. FUKUBAYASHI, and D. TAKESHITA. Possible mechanism of quadriceps femoris weakness in patients with ruptured anterior cruciate ligament. Med. Sci. Sports Exerc., Vol. 34, No. 9, pp. 1414–1418, 2002.
Purpose: The purpose of this study was to test the hypothesis that loss of afferent feedback due to rupture of anterior cruciate ligament (ACL) is the cause of quadriceps femoris (QF) weakness through gamma loop. Two experiments were designed to prove our hypothesis.
Methods: In experiment 1, the maximal voluntary contraction (MVC) of knee extension and integrated electromyogram (I-EMG) of vastus medialis (VM), vastus lateralis (VL), and rectus femoris (RF) were measured in 13 patients with ruptured ACL and 7 healthy volunteers before and after injection of anesthetic agent into the knee. In experiment 2, MVC of knee extension and I-EMG of the VM, VL, and RF were measured in 13 patients with ruptured ACL, 7 knee-anesthetized healthy subjects, and 12 normal subjects, before and after 20-min vibration stimulation applied to the infrapatellar tendon.
Results: The results of experiment 1 revealed that injection of anesthetic agent into the knee capsule resulted in significant decrease of MVC and I-EMGs. In experiment 2, the mean percentage change of MVC in the control group was significantly lower than that in the other two groups. There was no significant difference between knee-anesthetized group and patients with ruptured ACL. The mean percentage change of I-EMG showed a pattern similar to that of MVC.
Conclusion: Our results suggest that loss of feedback from mechanoreceptors in ACL is the underlying mechanism of weakness of QF in patients with ACL lesion. This conclusion is based on chronic suppression of recruitment of high-threshold motor units during voluntary contraction because ACL lesion leads to chronic reduction in Ia-feedback to muscles around the knee due to a lack of feedback from ACL to gamma motor neurons.
Department of Life Sciences, Graduate School of Arts and Science, University of Tokyo, Tokyo, JAPAN
Submitted for publication July 2001.
Accepted for publication May 2002.
Substantial weakness of quadriceps femoris (QF) has been observed in patients with ruptured anterior cruciate ligament (ACL) even in the absence of muscle atrophy, thus indicating that muscle atrophy is not the cause of QF weakness (11,14,17). Several investigators suggested that the loss of afferent feedback from ACL could contribute to this weakness (11,14,17), even though the exact mechanism of how QF weakness could lead to the loss of afferent feedback from ACL is uncertain.
Previous studies suggested that afferent feedback from knee joint structures (joint afferents) could only weakly affect alpha motor neurons (7). Therefore, it is unlikely that the ACL rupture could directly reduce the maximal voluntary contraction (MVC). In contrast, animal studies have shown that gamma motor neurons are markedly influenced by joint afferents. Because the activities of gamma motor neurons can influence alpha motor neurons through the gamma loop (16), a decrease in gamma efferent caused by loss of joint afferents might explain QF weakness in ACL lesions. To our knowledge, there are no studies that previously investigated whether attenuated joint afferents resulted in gamma loop dysfunction.
The purpose of our study was to investigate whether loss of afferent feedback due to ACL lesion could lead to prolonged weakness of QF through gamma loop in patients with ruptured ACL.
Thirteen patients (7 male, 6 female) with ruptured ACL (age 22.1 ± 8.1 yr, mean ± SD), and 19 healthy volunteers (14 male, 4 female, age 26.2 ± 3.1 yr) without a history of knee injury were enrolled in the present study. Patients with any other type of knee joint injury in addition to ACL rupture were excluded from this study. A clinical summary of participating patients is provided in Table 1. All subjects in this study had no pain or clinical signs of inflammation. In 7 of 19 healthy volunteers (6 male, 1 female, age 26.8 ± 2.6 yr), lidocaine was injected into the knee capsule at the time of the study. The remaining 12 healthy volunteers (8 male, 4 female, age 25.3 ± 3.77 yr) did not receive such treatment. All procedures were in accordance with the ethical standards of the Committee in Human Experimentation at the Department of Life Sciences, the University of Tokyo and informed written consent was obtained from subjects.
A dose of 5-mL lidocaine was injected into the knee capsule by a well-trained physician. In a preliminary study, we confirmed that effusion caused by the injected volume did not alter MVC or integrated electromyographic activity (I-EMG) of the QF muscle.
The method of vibration described by Kouzaki et al. (10) was used in the present study. Briefly, subjects sat on the seat of an isokinetic exercise machine (Myolet, ASICS Co., Tokyo) with their legs hanging down from edge of the seat; they were asked to relax their thighs as much as possible during the application of vibration. Vibration stimulation was applied manually using the Hit Masser (Kinesio Co., Tokyo) (Fig. 1) to the mid-portion of the infrapatellar tendon to induce attenuation of Ia through tonic vibration reflex of the quadriceps muscle. The frequency, amplitude, force of application, and duration of vibration stimulation were modified in this study. Theoretically, induction of Ia discharge is necessary to induce effective attenuation of the Ia afferent. However, the vibrating protocol of Kouzaki et al. is less effective in inducing Ia discharge than that used in previous studies (2,3,5,12,13). Therefore, we conducted a pilot study to design a protocol that could effectively result in reduction MVC and I-EMG. The selected vibration frequency was 50 Hz, which resulted in 1.5-mm displacement. The force and duration of application were approximately 30 N and 20 min, respectively.
Electromyography (EMG) of the vastus medialis oblique (VMO), vastus lateralis (VL), and the rectus femoris (RF) was recorded during MVC measurement at a sampling rate of 1 kHz. The surface EMG was recorded using bipolar silver-silver chloride electrodes with a cup diameter of 5 mm. These electrodes were placed on the belly of the VM, VL, and RF. The interelectrode distance was 20 mm. The ground electrode for EMG was placed on the center of the patella. The electrodes were connected to a preamplifier and a differential amplifier with a bandwidth of 5 Hz–1 kHz (1253A, NEC Medical System, Tokyo). To obtain the I-EMG signal, the EMG obtained during 1-s period of MVC was full wave rectified and integrated.
Subjects learned to perform MVC in a practice session before measurements were conducted. All subjects were asked to perform MVC of knee extension three times at 90° knee-flexion position before vibration. During measurement, the subject was in a sitting position, with the upper body and thigh kept tightly secured to the seat of the isokinetic exercise machine (Myolet, ASICS Co.) by belts (Fig. 2). The I-EMG of all muscles was simultaneously measured during MVC measurement. After finishing torque and I-EMG measurements, 20 min of vibration stimulation was applied. Immediately after finishing vibration stimulation, the MVC of knee extension and I-EMG were measured again using the same method as that used for previbration.
This experiment was designed to determine whether attenuation of joint afferents influences the MVC in the QF. MVC and I-EMG were measured in all participating subjects to establish the preinjection data. Then, lidocaine was injected into the knee capsule. We then examined the knee for any symptoms and signs and subjects complaining of any abnormal feeling or pain were excluded from further analysis. Five minutes after injection, the MVC and I-EMG measurements were repeated to assess the effect of feedback from knee mechanoreceptors on MVC and I-EMG.
This experiment was designed to determine whether the function of gamma efferent is altered by the loss of joint afferent from ACL. MVC and I-EMG was measured in all subjects to establish the baseline. This was followed by 20-min vibration stimulation. Immediately after completion of vibration stimulation, the MVC of knee extension and I-EMG were recorded again as described above.
All data were expressed as mean ± SD. A P-value less than 0.05 denoted the presence of a statistically significant difference.
Differences in MVIC and I-EMG data between baseline and postinjection were tested by paired Student’s t-test.
The mean percentage change in MVC and I-EMG after vibration stimulation was calculated by [(previbration value − postvibration value)/previbration value × 100]. Single-factorial ANOVA was used to determine differences between the mean percentage change of MVC and I-EMG between groups. Scheffe’s F-test was used as post hoc test.
Mean MVC and I-EMG values before and after lidocaine injection.
The mean MVC measured after lidocaine injection (229 ± 35 Nm) was significantly lower than the preinjection value (251 ± 29 Nm). The mean I-EMGs measured after lidocaine injection (VL: 0.22 ± 0.18; VM: 0.29 ± 0.28; RF: 0.19 ± 0.26) were significantly lower than the respective baseline I-EMG (VL: 0.29 ± 0.16; VM: 0.35 ± 0.31; RF: 0.23 ± 0.13).
Mean percentage change of MVC and I-EMG after vibration stimulation.
Single-factorial ANOVA detected significant differences in MVC among the three groups (P < 0.01). Significant differences could be detected in the mean percentage change of MVC between the control (−10% ± 5%) and ACL (4 ± 4%) groups, and between the control and anesthesia group (Table 2). However, there was no significant difference between ACL and anesthesia group (5 ± 8%).
Single-factorial ANOVA detected significant differences in I-EMG of each muscle among the three groups (P < 0.01). Significant differences could be detected in the mean percentage change in I-EMG of VL, VM and RF in between control ACL groups (Table 3), as well as between anesthetized and control group (Table 3). However, there was no difference in relative change in I-EMGs between ACL and anesthetized groups (Table 3).
Attenuation of joint afferents as a possible mechanism of MVC reduction in QF.
Our results showed that injection of local anesthetic agent into the knee joint cavity reduced MVC and I-EMG in normal subjects. Because the injection of local anesthetic agent into the knee joint cavity selectively attenuates the afferent signals from structures inside the joint cavity without attenuation of α-motor neurons, the decline of MVC and I-EMG caused by the anesthetic agent suggest that attenuation of joint afferents compromises the function of α-motor neurons innervating the QF. Furthermore, this result also suggested that ACL lesion could be the cause of QF weakness because such lesion could lead to the loss of joint afferents from ACL as well as the injection of local anesthetic agent into the knee joint cavity.
On the other hand, it is unlikely that attenuation of joint afferents due to ACL rupture and injection of local anesthetic agent would directly result in reduced MVC and I-EMG of QF because joint afferents only weakly affect α-motor neurons (7). Although joint afferent are unlikely to directly affect α-motor neurons, previous studies suggested that joint afferents could influence α-motor neurons through gamma loop because such afferents played an important role in regulating gamma efferents (6–9,15). Therefore, we assessed the gamma efferent function, which forms part of the gamma loop, in experiment 2. For this purpose, we tested the effect of vibration stimulation on the MVC and I-EMG in the quadriceps of subjects with ACL rupture and in a group of uninjured subjects.
Presence of abnormal gamma loop in the QF in patients with ACL lesion and anesthetized subjects.
Prolonged vibration simulation attenuates Ia afferent due to either neurotransmitter depletion, a heightened threshold of Ia fiber, or presynaptic inhibition of the Ia terminal (10) because the selective activation of Ia afferent evoked by vibration stimulation lasts for a long period of time (3,10,12,13). Therefore, the significant decreases of MVC and I-EMG in the control group represent normal responses to vibration stimulation (10). However, the mean percentage change of MVC and I-EMG of patients with ruptured ACL and knee-anesthetized subjects following prolonged vibration stimulation were significantly different from those of normal subjects.
In fact, the Ia discharge sufficient to lead to either neurotransmitter depletion or a heightened threshold of Ia fiber must be evoked by vibration stimulation to induce the normal response of MVC and I-EMG (10). Therefore, this change in response to prolonged vibration could be due to abnormality in gamma efferent because the gamma efferent functions to maintain Ia discharge caused by mechanical stimulation such as vibration stimulation at normal level (16). Indeed, previous studies demonstrated that abnormality in gamma efferent could be caused by attenuation of joint afferents (6–9,15). Therefore, the abnormal response to prolonged vibration noted in our patients with ruptured ACL and knee-anesthetized subjects suggests that attenuation of joint afferent caused the abnormality in gamma efferent.
The results of present study indicated that attenuation of joint afferents disturbs the function of both gamma efferent and α-motor neuron. Because joint afferents directly affect to the gamma loop but only weakly affect α-motor neurons, the results of this study provide evidence that attenuation of afferents from the knee joint results in failure of MVC of QF through the gamma loop. Previous studies also demonstrated that attenuation of Ia afferents induced by a decrease in gamma efferent could hinder the recruitment of high-threshold motor units (1,2,4,10). Therefore, we conclude that attenuation of joint afferents caused by ACL lesion is a possible mechanism of QF weakness. We summarize our hypothesis in Figure 3.
Conflict of interest: The results of the present study do not constitute endorsement of the product by the authors or ACSM.
Address for correspondence: Toru Fukubayashi, M.D., Ph.D., Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, 3-8-1 Komaba, Tokyo, Japan 153-8902; E-mail: email@example.com.
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