Effects of Age and ACL Reconstruction on Quadriceps Gamma Loop Function
Richardson, Michael S
Background and Purpose: Both aging and anterior cruciate ligament (ACL) reconstruction are associated with strength deficits, which can in turn influence performance of activities of daily living. Thus it is informative to understand mechanisms underlying strength deficits. Age-related declines in strength follow reductions in muscle fiber numbers and size, whereas strength deficits following ACL reconstruction may be caused by the loss of intraligamentous mechanoreceptors. A common link between these conditions is the gamma spindle system, or the gamma loop. Appropriately applied vibration can affect the gamma loop by causing disruption of afferent feedback to a muscle and result in decreased force capabilities. We investigated the effect of age and ACL reconstruction on gamma loop function. Methods: Maximal isometric strength (MVC) and electromyography (EMG) of the quadriceps were quantified before and after vibration stimulation of the infrapatellar tendon of 3 groups: young healthy (n=14; mean age=23.8 yrs), young ACL reconstructed (n=7; mean age=22.4 yrs), and older healthy (n=14; mean age=66.1 yrs) individuals. Results: The quadriceps MVC, vastus lateralis EMG, vastus medialis EMG, and rectus femoris EMG declined significantly in the young healthy group following vibration stimulation to the infrapatellar tendon, which indicated an intact gamma loop. There were no changes in these variables for the old healthy and ACL reconstructed groups. Conclusion: Gamma loop function was impaired in both the older and ACL reconstructed groups possibly due to either decreased muscle spindle sensitivity or the loss of mechanoreceptors.
Key Words: gamma loop, muscular vibration, reflex sensitivity, aging
Significant muscular strength reductions occur as individuals age and when individuals experience anterior cruciate ligament (ACL) reconstruction; however, the loss of strength is multifactorial involving the loss of muscle fibers (age related sarcopenia), muscle atrophy (inactivity or injury), and the inability to recruit existing motor units. A common link between age and injury reductions in strength appears to be related to the gamma spindle system, or the gamma loop.
It is well documented that the ACL contains neural elements that allow for a sensory function in individuals with healthy knees.1 For an ACL that has been reconstructed following a tear, the afferent feedback from the ACL can be disrupted. Researchers have shown that the afferent feedback from the ACL neural elements aids in the maintenance of muscle tension around the knee,2,3 not by altering alpha motor neurons directly, but rather by the gamma loop.3 A disruption of gamma loop function associated with ACL deficiency therefore could be part of the underlying mechanism of decreased maximal voluntary contraction of the quadriceps femoris muscles of these subjects.4-6
There are many complex processes that can result in strength declines. Older individuals experience a decline in muscle mass related to decreased anabolic stimuli, such as decreases in circulating growth hormone and testosterone levels, as well as increased catabolic factors like myostatin, interleukin-1 and -6, and tumor necrosis factor.7 Changes in the central and peripheral neural systems can also play a role in the loss of muscle mass and the inability to activate existing motor units. Corden and Lippold reported that reflex actions for which the gamma loop is responsible become impaired as individuals age, possibly due to a reduced reflex sensitivity of the muscle spindle, and may ultimately contribute to age related muscle atrophy.8
Vibration stimulation can be used to determine the effect of age on gamma loop function and to further define the role of the gamma loop in quadriceps femoris weakness associated with ACL deficiency. For example, if the gamma loop is functional, then vibration stimulation should result in a decrease in maximal voluntary contraction (MVC) and electromyographic activity (EMG) of the muscles surrounding the affected joint by inhibiting feedback from la afferents that are required for the complete recruitment of Type II muscle fibers.4,9,10 Therefore, if the gamma loop were functional in subjects who have had ACL reconstruction and those who are aging, we would expect their postvibration response of MVC and EMG activity to be similar to that of young healthy subjects.
The purpose of this study was to investigate the effect of age and ACL reconstruction on the function of the gamma loop. To that end, the MVC and EMG of the quadriceps were quantified both before and after vibration stimulation was applied to the infrapatellar tendon of 3 groups: young healthy, young ACL reconstructed, and older healthy. We hypothesized that gamma loop function would be diminished with ACL reconstruction or aging due to the disruption of various gamma loop components. Therefore, we expected that MVC and EMG of the quadriceps to be attenuated more following vibration stimulation in the young healthy group than in the young ACL reconstructed and older healthy groups.
Subjects and Research Design
An effect size of 1.04 was determined using data from a previous study,6 requiring a minimum of 13 subjects for each group to achieve a statistical power of 0.80 for our study.11 Unfortunately, it was very difficult to recruit the young ACL group, hence the smaller sample size compared to the other 2 groups. In total, 35 men (n = 13) and women (n = 22) between the ages of 19 and 72 years volunteered to participate in this study. Subjects were grouped into 3 groups according to age and ACL status:young healthy (n = 14), old healthy (n = 14), and young ACL (n = 7) reconstructed. Subjects were eligible to be classified into the young healthy group if they were between the ages of 18 and 35 years and had no history of knee injury. The criteria for inclusion into the old healthy group were an age range of 60-75 years and no history of knee injury or cardiovascular problems. To be eligible for the young ACL group, subjects were required to be between the ages of 18-35 years and to have had an ACL reconstruction between 6 and 12 months prior to participation in the study. Each subject provided a written informed consent, which was approved by the University of Oklahoma Institutional Review Board. Individuals in the young ACL group were required to obtain approval from their operating physician prior to participating in the study. Subjects completed a short questionnaire regarding their current physical activity level. All subjects indicated that they felt that they were at about the same level of physical activity when compared to their age and gender matched cohorts, both at work and leisure. All subjects were required to attend only one testing session during which anthropometric measures (weight, height) and MVC and EMG data were collected.
Isometric MVC Assessment
Prior to engaging in the isometric MVC assessment, each subject was instructed to warm-up by stretching the quadriceps muscles for a period of 1 minute, then the Biodex System 3® (Shirley, NY) was used to obtain isometric strength of the right quadriceps. Prior to testing, the Biodex dynamometer was initialized and set to a 75° right knee flexion angle to ensure consistency between subjects and maximal force values. The subject was seated in the Biodex chair and the torso was secured using the restraint belts. The Biodex chair was then adjusted so that the subject’s right knee center of rotation was aligned with the center of rotation of the Biodex dynamometer and the shin pad located and secured by padded straps just proximal to the subject’s ankle. Next, the subjects were informed of the testing protocol commands that would be given during all isometric testing. After initiating EMG collection and giving the verbal command (3,2,1, Go!), the subject exerted a maximal voluntary contraction of the right quadriceps while pushing against the stationary dynamometer arm for 3 seconds. At the completion of the 3 second contraction the subject was instructed to ‘relax’ and was allowed 30 seconds of rest before performing another 3 second contraction. This procedure was repeated for a total of 3 contractions. Following the third contraction, vibration stimulation was applied to the subject’s infrapatellar tendon for a period of 20 minutes. Immediately following the 20-minute vibration application the subject performed 3 more contractions with the same commands and timing that were used during the previbration contractions. The highest isometric peak torque (MVC) for each of the pre- and postvibration trials was then determined and recorded for further analyses.
Bipolar surface electrode (Biopac, EMG/ECG electrodes) arrangements were placed along the longitudinal axes of the vastus lateralis, vastus medialis, and rectus femoris muscles (Figure 2). For the vastus lateralis, electrodes were placed along the lateral border of the quadriceps at 5 and 15 cm from the superior edge of the patella on the lateral border of the quadriceps. For the vastus medialis, electrodes were located 5 and 15 cm from the superior border of the patella on the medial border of the quadriceps. For the rectus femoris, electrodes were located on the central line of the quadriceps at a distance of 12 and 20 cm from the superior edge of the patella. To ensure proper adhesion and electrode contact, the skin was prepared by abrading with an alcohol prep pad. A small amount of conductive gel was placed on the contact side of the electrodes, which were then placed on the muscles. The EMG signals (recorded in millivolts, mV) were preamplified (gain=1000x) using a differential amplifier (EMG100C, Biopac Systems Inc., Santa Barbara, Calif; bandwith=1-500 Hz).
The analog EMG (mV) signals were sampled at a frequency of 1 KHz, stored on a personal computer, and expressed as root mean square (rms) values by custom software (LabVIEW 7.0, National Instruments, Austin, Tex) as suggested by Basmajian.12 The EMG signals were bandpass filtered (4th-order Butterworth filter) at 10-500 Hz. All subsequent analyses used the filtered EMG (mVrms) values for each muscle (vastus lateralis, vastus medialis, and rectus femoris) that were recorded during the highest pre- and postvibration MVC measurements.
Vibration stimulation was applied to the infrapatellar tendon using the Foredom Percussion Hammer (Bethel, Conn) (Figure 1). The Foredom Percussion Hammer applies a vibration with a frequency from 0 to 233 Hz and a displacement of 1.5 mm. Based on previously published research, the vibration frequency was set at 50 Hz.6 The force and duration of vibration was 30 N and 20 minutes, respectively. The location of vibration application was 1 cm below the inferior border of the patella, directly on the infrapatellar tendon. The percussion hammer was secured to the subject’s leg using Velcro(TM) straps around the handle and head of the hammer (Figure 2). In order to ensure that 30 N of force was placed on the infrapatellar tendon, 6.75 lbs. of force (or approximately 30 N) was applied to one end of the Velcro(TM) strap before securing it to the other side. This was accomplished using a Shimano instrument scale (Irvine, Calif) attached to the end of the Velcro(TM) strap and pulling until the scale registered 6.75 lbs. The strap was then secured,ensuring a constant force of vibration to the infrapatellar tendon.
Statistical analyses were performed using SPSS® for Windows® (version 11.5). Descriptive statistics were performed for all measures to describe each group’s physical attributes and neuromuscular responses to vibration stimulation. Differences (absolute and percentage) between the groups’ responses to vibration were summarized descriptively (Table 2). Percent changes were calculated as (previbration value – postvibration value) divided by the previbration value, then multiplied by 100. Thereafter, a 3 (group) by 2 (condition) mixed model analysis of variance (ANOVA) was conducted. Bonferroni paired samples procedure was used as a post-hoc test when significant group or interaction effects were found. All measures are presented as Mean ± SE and statistical significance was set at P
The mean and standard error for age (years), standing height (cm), and body weight (kg) are given for each group in Table 1. The age range for the young healthy and ACL groups was 18-35 years, while the age range for the old healthy group was 60-75 years. There were no significant differences (P > 0.05) between groups for standing height or body weight.
Descriptive statistics for MVC of the right quadriceps and EMG for the vastus lateralis, vastus medialis, and rectus femoris for each of the 3 groups are presented in Table 2. Only the young healthy group had a significant decline in MVC following vibration which averaged 7.2%. In the same manner, only the young healthy group had significant declines in EMG activity for each of the 3 muscle groups (11.1% for the vastus lateralis, 15.2% for the vastus medialis, and 8.9% for the rectus femoris). The MVC and EMG activity for the young ACL reconstructed and old healthy groups remained either unchanged or increased slightly, following application of vibration to the infrapatellar tendon.
For the dependent variable, MVC, there was no significant condition effect (P- 0.273), however, there was a significant group (P= 0.028) and group by condition interaction (P- 0.001) (Table 3). Only the young healthy group’s MVC force following vibration decreased significantly (P = 0.001).
The EMG responses for each of the 3 muscle groups are presented in Table 3. The vastus lateralis and rectus femoris muscle groups demonstrated a significant group and group by condition interaction, while the vastus medialis muscle group had only a significant group by condition interaction. There was no significant condition effect (P = 0.490) for the vastus lateralis, only a significant group (P = 0.009) and group by condition interaction (P = 0.001). The young healthy group’s postvibration vastus lateralis EMG activity declined significantly (P = 0.012), while there was essentially no change for the other 2 groups.
The EMG for the vastus medialis demonstrated no significant condition (P = 0.192) or group effect (P – 0.069), however, a significant group by condition interaction was present (P= 0.001). Following vibration, the young healthy group’s vastus medialis EMG declined significantly (P = 0.002), whereas the old healthy (P = 0.638) and young ACL (P = 0.064) groups showed no significant change.
Finally, the EMG for the rectus femoris resulted in no significant condition effect (P = 0.304) but there was a significant group effect (P = 0.001) and group by condition interaction (P = 0.009). Not surprisingly, it was found that the postvibration rectus femoris EMG of the young healthy group decreased significantly from the previbration values (P = 0.003) while there was no significant change in the old healthy (P= 0.918) or young ACL (P = 0.254) groups.
The observed power of each main effect and interaction from the ANOVA analyses are presented in Table 3, The statistical power for the group main effects and the group by condition interactions for each of the dependent variables were close to the expected value of 0.80. The average power for the group effects was 0.70 while the average power for the interaction effects was 0.93. There were no significant condition main effects for any of the variables although the average power value was quite low (0.18).
This study examined the effect of age and ACL reconstruction on the function of the gamma loop. To that end, the difference between the MVC and quadriceps EMG of young healthy, young ACL reconstructed, and older healthy individuals was quantified both before and after vibration stimulation was applied to the infrapatellar tendon of the right knee. A limitation to the current study was the small sample size for the young ACL reconstructed group when compared to the young healthy and old healthy groups. Even so, statistical power for the group main effects remained high for each dependent variable and averaged 0.70.
The significant decline in postvibration MVC and EMG of the quadriceps muscle in the young healthy group represents the expected and normal response following vibration stimulation applied to the infrapatellar tendon.10 The results show, however, that the young ACL reconstructed group’s response to vibration was dissimilar from that of the young healthy groups. This is in support of the findings of Konishi et al6 who reported significant reductions in MVC as well as reductions in vastus lateralis and vastus medialis EMG following vibration to the infrapatellar tendon in young control subjects but not in young ACL reconstructed subjects. The fact that the young healthy group had declines in the dependent variables following vibration while the other 2 groups either had small increases or no change would account for the lack of statistical significance for the main effect of condition (before and after vibration).
These results lend support for a theory of functional impairment of the gamma loop in subjects with a history of ACL reconstruction.6 It appears to be physiologically impossible to exert a true MVC without gamma loop feedback since adequate Ia afferent neuron output is required for the comprehensive recruitment of Type Il motor units.4,10,12 According to previous studies, mechanoreceptors within the ACL are important because they enhance the response and discharge of the gamma motor neurons.2,3 With ACL reconstruction, the mechanoreceptors of the ACL are lost, resulting in impaired gamma loop function and an inability to fully contract the quadriceps due to incomplete Type Il motor unit recruitment.
The mechanism of quadriceps weakness described above also supports the findings from studies that reported selective atrophy of the Type Il muscle fibers in subjects with a history of ACL reconstruction.13,14 The loss of Ia afferent input to the gamma loop of ACL injured subjects could cause prolonged disuse of the Type Il muscle fibers due to a reduced activation of the high-threshold α-motor neurons, which would result in a loss of strength in the affected quadriceps muscle.
The results of the current study also showed that there was an age difference in the postvibration responses for MVC and quadriceps EMG. The older group’s response to vibration did not differ significantly from that of the young ACL reconstructed group. More specifically, the older healthy group’s MVC and quadriceps EMG values did not decline following vibration stimulation applied to the infrapatellar tendon, indicating impaired gamma loop function. The first possibility is that the gamma loop does not function as efficiently in older individuals due to a reduced number and size of Type Il muscle fibers.15-17 Considering that the Ia afferent neurons assist in the recruitment of fast-twitch motor units, a reduction in Type Il muscle fibers would result in decreased MVC of the quadriceps following vibration to the infrapatellar tendon. The second, and more likely mechanism for reduced gamma loop function in older individuals, is a reduced sensitivity of the muscle spindle.8,18 The muscle spindle’s role in the function of the gamma loop is vital. The muscle spindles are innervated by gamma motor neurons that cause responsive changes in the spindle following muscle stretch. The spindles then send afferent information back to the high-threshold α-motor neurons via the Ia afferent neuron. Age-related alterations to the structure and function of the muscle spindle can cause reduced sensitivity to gamma motor neuron activation, and in turn, could result in a reduced Ia afferent discharge and an inability to maximally recruit highthreshold motor units. Therefore, if the muscle spindles of older individuals are less sensitive to muscle stretch, then vibration of the infrapatellar tendon will have less of an attenuating effect on MVC and EMG of the quadriceps muscle.
If reduced spindle sensitivity is, in fact, the cause of impaired gamma loop function in older individuals, then its effect on the well-documented decrease in muscle mass associated with increasing age cannot be ignored.19,20 As mentioned previously, it is possible that the gamma loop interruption experienced by ACL reconstruction patients causes a selective atrophy of Type Il muscle fibers due to reduced Ia afferent influence on fast-twitch motor units. Assuming that the reduced sensitivity of muscle spindles is responsible for gamma loop impairment in older individuals, this same mechanism of a reduced influence of the la afferents may also affect the elderly. It would be difficult, however, to differentiate the effects of the impaired gamma loop on Type Il muscle fibers from other possible causes of Type Il fiber atrophy, such as the neuropathic processes within the muscle21 and physical inactivity associated with increasing age.22
In conclusion, it is assumed that gamma loop function was affected by ACL reconstruction and increased age which resulted in a decreased ability for the quadriceps to exert force. Although the mechanisms by which the gamma loop affects strength are not clear, it seems to be due to the loss of ligamentous mechanoreceptors or decreased muscle spindle sensitivity. Increased knowledge of strength deficits associated with ACL reconstruction and aging can lead to better rehabilitation techniques as well as to an improved quality of life for affected individuals, since the ability to exert maximal force is dependent on more than just the quantity of the muscle mass involved but also the ability to activate the existing muscle mass. Therefore, rehabilitative techniques for ACL reconstructed individuals, as well as for older individuals, need to include activities to improve neural coordination and reflexes as well as exercises for improving strength.
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Michael S. Richardson, MS;’ Joel T. Cramer, PhD;1 Debra A. Bemben, PhD;1 Randa L. Shehab, PhD;2 John Glover, DO;3 Michael G. Bemben, PhD1
1 Department of Health and Exercise Science, University of Oklahoma, Norman, OK
2 School of Industrial Engineering, University of Oklahoma, Norman, OK
3 Department of Osteopathic Manipulative Medicine, Touro University – California, Vallejo, CA
Address correspondence to: Michael G. Bemben, University of Oklahoma, Department of Health and Exercise Science, Neuromuscular Research Laboratory, 1401 Asp Avenue, Norman, OK 73019, Ph:405-325-2717, Fax:405-325-0594 (firstname.lastname@example.org).
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