The Effects of Muscle Fatigue on and the Relationship of Arm ~omhance to Shoulder Proprioception

Transcription

1 The Effects of Muscle Fatigue on and the Relationship of Arm ~omhance to Shoulder Proprioception Michael I. Voight, DPT, PT, ATC, SCS, OCS' ). Allen Hardin, MS, PT, ATC2 Turner A. Blackburn, MEd, PT, ATC) Steve Tippett, MS, PT, ATC, SCS4 Gary C. Canner, MD5 S houlder proprioception and kinesthesia have recently come to light in physical therapy as sensory modalities that need to be addressed in rehabilitation of various pathologies. Proprioception is defined as the cumulative neural input to the central nervous system from specialized nerve endings called mechanoreceptors. These are located in the joint capsules, ligaments, muscles, tendons, and skin (16,19). Kinesthesia has been defined as the conscious awareness of joint position and movement, resulting from proprie ceptive input to the central nervous system (8.19). The concepts of proprioception and kinesthesia are often confused. Controversy exists as to the relative contribution of joint vs. muscle receptors (3). The traditional view is that sensations of joint position sense originate in the joint capsule. However, a more recent viewpoint suggests that muscle receptors play a significant role (2). Burgess et al found no evidence that the articular mechanoreceptors of any joint are important for the conscious awareness of joint position, although kinesthesia requires neural input to the central nervous system (5). Rather, muscle spindle receptors are believed It is hypothesized that proprioceptive information plays an important role in joint stabilization and that muscle fatigue may alter proprioceptive ability. The purpose of this study was to determine what effect shoulder muscle fatigue has on glenohumeral proprioception and to examine the relationship between arm dominance and shoulder proprioception. Eighty subjects without a history of glenohumeral pathology participated. Each was seated on an isokinetic dynamometer with a randomly selected shoulder positioned in 90" of abduction and elbow flexion. With vision blinded, the arm was passively positioned in 75" of external rotation for 10 seconds, then passively returned to the neutral starting position. Three trials each of active and passive repositioning (2%~) were recorded. Following a fatigue protocol, both active and passive repositioning were reassessed. Testing order was randomized. A significant difference was detected between pre- and post-fatigue scores. No significant difference was detected between dominant and nondominant extremities. No relationship between arm dominance and shoulder proprioception was established. It is concluded that shoulder proprioception is diminished in the presence of shoulder muscle fatigue, suggesting clinical rehabilitation protocols must emphasize increasing muscular endurance. Key Words: proprioception, fatigue, dominance, shoulder ' Co-Director, Berkshire lnstitute of Orthopedic and Spom Physical Therapy, 2201 Ridgewood Road, Suite 375, Wyomissing, PA Physical Therapist, Berkshire lnstitute of Orthopedic and Spom Physical Therapy, Wyomissing, PA ' Co-Director, Berkshire lnstitute of Orthopedic and Sports Physical Therapy, Wyomissing, PA ' Assistant Professor, Bradley University, Peoria, IL Berkshire Orthopedic Associates, Wyomissing, PA; Director, Eastem Spom Medicine and Orthopedic lnstitute, Wyomissing, PA to be most suited for conveying conscious awareness of joint position sense, which is essential for proper function in activities of daily living, occupational tasks, and sports (4,13, 16,17). This theory establishes the basis for the important role muscle receptors play in proprioception. Proprioception arises from a variety of sensory neurons in skin, muscle, and joint tissues, including capsular and ligamentous structures. The sensory end organs include the Pacinian corpuscle-like receptors, Rufini end organ-like receptors, Golgi tendon organ-like receptors, and free nerve endings. The Pacinian corpuscles respond to small changes in pressure and are considered rap idly adapting end organs. This type of end organ is stimulated in the initial and terminal stages of joint range of motion as well as during rapid changes in velocity and direction (1, Volume 23 Number 6 June 1996 JOSPT

2 2,20). Pacinian afferents are also compression sensitive, excited by tissue deformation (18). These recep tors, classified as type I1 sensory end organs by Wyke, are located in the joint capsule at the junction of the synovial membrane and the fibrosum layer and include a low threshold response and code for acceleration (10,11,15). The Rufini end organ-like recep tors and Golgi tendon organ-like receptors are slow adapting and have been associated with a response to the relative positions of muscles and joints. They relay information on the actual or steady state joint position and changes related to joint rotation (1). Ruffini end organ-like receptors, or type I receptors, are found in the joint capsule and are characterized by low threshold response and coding for speed, acceleration, and direction. These afferents are stretch sensitive and are excited by capsule stresses associated with end range limits of motion (18). Golgi tendon organs, or type I11 receptors, are found in the fascia of muscle tendons and collateral ligaments in the joints of the extremities and are characterized by high threshold response and coding for tension, joint position, and direction (10,11,15). Free nerve endings are associated with pain sensation and are considered to be nonadapting nociceptors. They are characterized by high threshold response and are classified as type lv receptors, found in joint ligaments, capsules, and fat pads (10, 11,15). These afferents are excited by a forceful rotation into a limit of movement sufficient enough to produce a noxious stimulus (18). Joint mechanoreceptors consist of Rufini and Pacinian afferents as well as free nerve endings. Joint rotation will stretch the capsule on one side of the joint, while possibly compressing it against the underlying bone. As a result of this mechanical deformation, it is possible that the mechanoreceptors originating in JOSPT Volume 23 Number 6 June 1996 these joint tissues may have a role in proprioception (9). The muscle spindle, present in nearly all muscles, functions as a stretch receptor, sending sensory impulses over afferent axons concerning the length of the muscle spindle and the rate at which it is being stretched and providing information on joint position sense (12). The spindle also contains contractile fibers controlled by efferent nerve impulses, providing it with both afferent and efferent innervation (12). The spindle may be stretched via two mechanisms: 1) the muscle within which it lies is stretched or 2) the central portion of the spindle stretches due to the contractile elements at the end of the spindle shortening (12). The Golgi tendon organ is a sensory receptor in the muscle tendon sensitive to tension, whether generated by passive stretch or active muscle contraction. The Golgi tendon organ provides a direct tension feedback mechanism for either increases or decreases in muscle tension by inhibiting motor neurons to the same muscle and synergistic muscles and exciting motor neurons to antagonistic muscles (12). Cutaneous mechanoreceptors in the skin have been shown to encode joint movements via stretch-sensitive neurons, signaling joint position or motion. However, evidence from previous studies suggest that their contribution to proprioception is joint specific. Cutaneous contributions appear to be of less importance in proximal joints, such as the shoulder, than those of the more distal hand (9). Muscle mechanoreceptors appear to play an important role in proprioception. In an animal model, muscle afferents were found to provide an unidirectional signal of joint movement because the response of muscle spindle afferents is known to be a function of muscle length (18). When muscle afferents are excited alone (without the normal simultaneous activation of afferents located in peripheral structures), the result- ing proprioceptive acuity is very poor (18). Likewise, when single muscle afferents are excited, sensations of movement are infrequently reported (14). However, when sensory neurons in the joint and in the tissues outside the joint are anesthetized, proprioception is not lost, perhaps due to involvement of the muscle mechanoreceptors (6,7,18). In a recent study, Lephart et al have provided a comprehensive assessment of shoulder joint proprioception in normal, capsuloligamentous-injured, and postreconstructed groups (13). However, little data exist examining the role, if any, of muscle fatigue on shoulder joint propriocep tion. Barrack et al concluded proprioceptive information is essential in ,---. Proprioceptive information is essential in eliciting muscular reflexes that aid in protecting and stabilizing the knee joint. eliciting muscular reflexes that aid in protecting and stabilizing the knee joint (2). Skinner et al found passive repositioning ability of the knee joint to be significantly decreased following a fatigue protocol, concluding that patients who are fatigued may have altered proprioceptive abilities ( 17). Accordingly, the purpose of this study was to examine the conscious awareness of joint position sense through a joint repositioning protocol, to determine what effect muscle fatigue has on glenohumeral joint proprioception, and to examine the relationship between arm dominance and shoulder proprioception.

3 RESEARCH STUDY METHODS Subjects A total of 80 college-aged sub jects (37 males and 43 females) with a mean age of 23.7 years (SD = 2.8) and without history of glenohumeral pathology volunteered to participate in this study. All subjects signed informed consent documents approved by a University Institutional Review Board. All subjects were informed that they would be tested for their ability to reproduce joint angles in both shoulders. However, they were not given specific details of the study. Instrumentation/Subject Positioning Each subject was seated on a Biodex multi-joint isokinetic dynamometer (Biodex Medical Systems, Shirley, NY) with the randomly selected shoulder positioned in 90" of shoulder abduction, 90" of elbow flexion, and neutral pronation/supination. The arm was positioned so that it rested on a pad just proximal to the elbow. Prior to attachment, the lever arm was gravity compensated to diminish any feedback from the lever arm to the subject. A narrow padded strap was securely fastened around the forearm to be tested to stabilize the upper extremity. The subject was then blindfolded. Prior to testing, each subject revealed arm dominance through direct questioning concerning preference for tossing a ball. Procedure The arm was passively positioned by the examiner and held for 10 seconds at the reference angle, 75" of external rotation. The arm was then passively returned to the neutral starting position. The subject was instructed to actively reposition the shoulder at the reference angle until three trials were recorded, each beginning from the starting position. Following the three trials of active repositioning, the arm was again pas- sively positioned by the examiner at 75" of external rotation and held for 10 seconds. After returning to the starting position, passive movement of the dynamometer was initiated at SO/sec. The subject was instructed to stop the dynamometer with a stop button when the subject perceived the reference angle had been reached. Three separate trials of passive repositioning were performed. The order of the extremity tested as well as of active and passive testing was randomized. Following the baseline testing, the arm was exercised in the test position via active isokinetic internal and external rotation at 180 /sec until peak torque output of the external rotators dropped below 50% of the initial or maximal values for three consecutive repetitions. Both active and passive repositioning were immediately reassessed in random order as previously described. RESULTS Statistical analysis was conducted using the SPSS computer software system (SPSS Inc., Chicago, IL). Results of testing revealed that the test- ing method was reliable. An intraclass correlation coefficient was calculated for reliability and was found to be appropriate (ICC = 0.95). Based on pre- and post-fatigue active and passive repositioning values, a one-way analysis of variance found glenohumeral repositioning ability to be significantly altered in the presence of shoulder muscle fatigue (p < 0.001). A one-way analysis of variance revealed no statistical difference between the dominant and nondominant extremity in any test condition (p < 0.05). A relationship between shoulder proprioception and arm dominance was not established. The mean value scores in degrees from preset reference position and standard deviations are shown in Figures 1 and 2 and Tables 1 and 2, respectively. DISCUSSION ACT WE REPOSITIONING Group &arm FIGURE 1. Mean values in degrees from preset reference position. While differing views on the origin ofjoint position sense persist, the results of this study make a case for the importance of the role of muscle mechanoreceptors. The commonly held appreciation appeared to sup port static joint receptors as the pre- Volume 23 Number 6 June 1996 JOSF'T

4 RESEARCH STUDY PASSNE REPOSITIONING TABLE 1. Mean values and standard deviations (SDl in degrees from preset reference position. Nondominant Dominant TABLE 2. Mean values and standard deviations (SD) in degrees from preset reference position. Group Amrage FIGURE 2. Mean values in degrees from preset reference position. dominant receptors (15). However, our data would suggest that proprioceptive acuity was greatest with prefatigue active repositioning. This contraction-associated proprioceptive acuity supports the important role of the muscle receptors in the glenohumeral joint, which concurs with previous research (4). Conversely, the proprioceptive acuity in the shoulder was significantly hindered in the presence of fatigue. Several explanations may account for these alterations in proprioceptive ability, both actively and passively. It is a logical assumption that the fatigue protocol directly affects the contractile elements of the shoulder, presumably the muscles as well as the receptors which lie within. Therefore, the contractile elements (muscles) as well as their receptors may be inefticient and the ability to actively reproduce an established position inhib ited. The resultant effect may be a muscle or muscle group that is compromised or dysfunctional. Likewise, the components of the muscle (s), specifically the muscle spindle and the Golgi tendon organ, may be similarly dysfunctional. The dysfunctional muscle mechanoreceptors may offer a reasonable explanation for the results of our study concerning passive repositioning as well. First, by taking the joint to the end range of motion in external rotation during the fatigue protocol, the muscle mechanoreceptors sensitive to muscle tension may have desensitized and, therefore, accommodated to the stimulus. Second, the fatigued muscle and its components may have become dysfunctional, thus rendering the muscle receptors unable to detect the change in tension. These explanations may account for the inability to passively reposition the upper extremity accurately. These findings dispute the suggestions from previous studies that passive movement and position sense were exclusively detected by changes in tension in the joint capsule (15). There appears to be no relationship between arm dominance and shoulder proprioceptive ability. The subjects appeared to have no kinesthetic or proprioceptive difference when the dominant shoulder was compared with the nondominant contralateral shoulder. These find- ings are supported in previous research involving the upper and lower extremities in both normal and athletic groups (13). Any effects of a learning curve were diminished through randomization of all facets of data collection. This was shown by the fact that the ability to reproduce a preestablished position, both actively and passively, following the baseline data collection was significantly decreased. These findings support the notion that muscle mechanoreceptors or afferents are, in fact, most suited for conveying conscious awareness of joint position sense in the shoulder. The point must be made, however, that the ability to reposition the extremity at a reference angle is but one aspect of proprioception, presumably quantifying conscious proprioception. Quantifying the threshold to detection of passive movement is equally important, presumably rep resenting yet another measure of conscious proprioception. This was not addressed in our study, secondary to limitations of the testing equip ment. This measure should be addressed concerning effects of muscular fatigue in future studies. Likewise, future research addressing the restorative time of muscle receptors following fatigue may be of significance. JOSF'T Volume 23 Number 6 June 1996

5 The clinical implications from this study are three-fold. First, this study showed that the testing method was reliable, establishing a protocol for future proprioceptive testing and rehabilitation. Second, results showed glenohumeral proprioceptive ability to be decreased in the presence of shoulder muscle fatigue. Therefore, clinical rehabilitation protocols should emphasize increasing muscular endurance to produce a more fatigue-resistant muscle or muscle group. Lastly, limb dominance was - - Clinical rehabilitation protocols should emphasize increasing muscular endurance to produce a more fatigue-resistant muscle or muscle group. shown to have no effect on proprioceptive ability. This finding estab lishes validity for using the uninvolved limb as a control or baseline for testing and rehabilitation to aid in establishing discharge criteria. CONCLUSION This study concludes that glenohumeral proprioception is significantly altered in the presence of shoulder muscle fatigue. This conclusion is drawn from the inability of subjects to both actively and passively reposition the upper extremity accurately following a fatigue protocol. A relationship between shoulder proprioception and arm dominance was not established. JOSPT ACKNOWLEDGMENTS The authors would like to acknowledge John Guido, PT, SCS, CSCS, John D. Kidder, PTA, Brooks Applegate, PhD, and Morgen C. Hardin for their technical assistance. REFERENCES 1. Barrack RL, Skinner HB: The sensory function of knee ligaments. In: Daniel D (ed), Knee Ligament Structure, Function, Injury, and Repair, pp New York: Raven Press, Ltd., Barrack RL, Skinner HB, Buckley SL: Proprioception in the anterior cruciate deficient knee. Phys Sportsmed 1 l(6): 1-6, Barrack RL, Skinner HB, Cook SD: Proprioception of the knee joint: Paradoxical effect of training. Am J Phys Med 63(4): , Borsa PA, Lephart SM, Kocher MS, Lephart SP: Functional assessment and rehabilitation of shoulder proprioception for glenohumeral instability. J Sport Rehab 3(1):84-104, Burgess PR, Wei JY, Clark F), Simon J: Signaling of kinesthetic information by peripheral sensory receptors. Annu Rev Neurosci 5: , Gandevia SC, McClosky Dl: Joint sense, muscle sense, and their combination as position sense, measured at the distal interphalangeal joint of the middle finger. J Physiol (Lond) 260: , Gandevia SC, McCloskey DI, Burke D: Kinaesthetic signals and muscle contraction. Trends Neurosci l5(2):62-65, Garn SN, Newton RA: Kinesthetic awareness in subjects with multiple ankle sprains. Ph ys Ther 68: , Grigg P: Peripheral neural mechanisms in proprioception. J Sport Rehab 3(1): 2-17, lhara H, Nakayama A: Dynamic joint control training for knee ligament injuries. Am J Sports Med 1 WMO9-3 15, Johansson H, Sjolander P, Sojka P: A sensory role for the cruciate ligaments. Clin Orthop 268: , Lehmkuhl LD, Smith LK: Some aspects of muscle physiology and neurophysiology. In: Brunnstrom's Clinical Kinesiology, pp Philadelphia: F.A. Davis Company, Lephart SM, Fu FH, Borsa PA, Harner CD, Safran MR, Warner J)P: Proprioception of the knee and shoulder joints in normal, athletic, capsuloligamentous injured, and post-surgical individuals: A model for the measurement of joint proprioception characteristics. Presented at the annual conference of the American Academy of Orthopedic Surgeons, Pittsburgh, PA, April, Macefield G, Gandevia SC, Burke D: Perceptual responses to microstimulation of single afferents innervating joints, muscles, and skin of the human hand. J Physiol (Lond) 239:27-28, Newton RA: Joint receptor contributions to reflexive and kinesthetic responses. Phys Ther 62(1):22-29, Rowinski MJ: Afferent neurobiology of the joint. In: Gould JA (4, Orthopaedic and Sports Physical Therapy, pp St. Louis: C.V. Mosby Company, Skinner HB, Wyatt MP, Hodgdon DW, Conard DW, Barrack RL: Effect of fatigue on joint position sense of the knee. J Orthop Res 4: , Strasmann T, van der Wal J, Halata Z, Drukker J: Functional topography and ultrastructure of periarticular mechanoreceptors in the lateral elbow region of the rat. Acta Anat 138:l-14, Wilkerson GB, Nitl A): Dynamic ankle stability: Mechanical and neuromuscular interrelationships. J Sport Rehab 3(1):43-57, Zimny ML, Schutte M, Dabezies E: Mechanoreceptors in the human anterior cruciate ligament. Anat Rec 214: , Volume 23 Number 6 June 1996 JOSPT