Aspects of shoulder function in relation to exposure demands and fatigue – a mini review

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Abstract

Objective. To discuss the literature on control and function of multiple muscle systems with special focus on shoulder and upper extremity under submaximal conditions.

Design. The paper is a mini review based on 31 studies.

Background. Control mechanisms underlying the recruitment and gradation of muscle activity in complex multiple muscle systems during various voluntary exertions is still not fully understood. Load sharing principles may be influenced by several factors like work demand, fatigability, metabolic factors etc.

Methods. Several methods, e.g., electromyography, intramuscular pressure, and tissue oxygenation are used. The definition of fatigue is discussed.

Results and conclusion. A relatively fixed load sharing of the shoulder muscles has been found at low load levels, submaximal speeds and with a limited range of movements of the arms for healthy subjects. However, the load sharing of the shoulder muscles can be changed to some extent in response to fatigue, mental demands, visual feedback and in patients suffering from disorders in the upper extremities. It is hypothesized that lack of ability to redistribute muscle activation pattern in the shoulder region or the upper extremity increases the risk of development of work related symptoms.

Introduction

One goal of biomechanical modeling is to estimate and predict forces on structures of the shoulder in order to get more insight into the static as well as the dynamic shoulder function. Biomechanical models can be based on the assumption of load sharing principles (e.g., minimize a cost function) [1], [2], [3] or measurements of myoelectric activity [4] in combination with anthropometric data. Large uncertainties exist regarding these data, although major improvements have been accomplished during the last decade. Most anthropometric studies are based on in vitro measurements from few cadavers [5]. However, new scan techniques such as ultrasound and MRI have recently been considered to comprise promising methods that allow individual in vivo measurements of especially muscle anthropometrics to be included in future models, see e.g., [6], [7].

The shoulder constitutes a complex system where most muscles are activated simultaneously to some extent during movements of arm and shoulder. The general knowledge regarding mechanical muscle function at the individual muscle level is well established, e.g., force/velocity relations and stress/strain relations. In contrast, the control mechanisms underlying the recruitment and gradation of muscle activity in complex multiple muscle systems during various voluntary exertions is still not fully understood. From a physiological point of view, load-sharing principles may be influenced by several factors like work demand, fatigability, metabolic factors etc.

The present paper discusses the control and function of multiple muscle systems as, e.g., the shoulder muscle region, when performing submaximal contractions. Factors of significance for the coordination of the activity in healthy non-fatigued muscles as well as in painful muscles are presented.

During static conditions shoulder muscle activation patterns in non-fatigued shoulder muscles are generally task dependent but with a relatively fixed load sharing for each task [4], [8]. But also for a dynamic task (paper and pencil) performed at different speed and precision demands, a rather fixed activity pattern has been documented [9]. This task specific activity pattern showed different levels of activity for the different shoulder muscles, but the activity levels were scaled similarly by changes in speed and precision demands. Thus, a difference in function between deep shoulder muscles (the rotator-cuff muscles) and the more superficial shoulder muscles could not be documented in such a task. The increased level of muscle activation with increasing speed could only in part be explained by increasing demands of acceleration and deceleration of the arm. Co-activation of antagonistic muscles was demonstrated and suggested to be partly responsible for the increased muscle activity [9]. Further, indirect evidence for the load sharing can be obtained by mapping the shoulder rhythm during different shoulder positions. The effect of different submaximal hand loads on the shoulder rhythm showed that the shoulder rhythm in abducted positions was not influenced by external loads up to 2.9 kg applied to the wrist [10], [11]. Thus, these studies indicate a relatively fixed load sharing of the shoulder muscles at low load levels, submaximal speeds and within a limited range of movements of the arms.

However, as mentioned above, the relative muscle activity during a certain task varies between muscles [9]. This may be a crucial point for the shoulder activity leading to fatigue or exhaustion in some of the active muscles, if the task is performed for long periods of time.

Muscle fatigue has been defined as failure to maintain the required or expected force or power while other researchers ascribe to the definition that muscle fatigue is a decrease in the force generating capacity [12], [13], [14], [15]. One advantage about the latter definition is that it allows a differentiation between fatigue and exhaustion. Point of exhaustion occurs when the required force or exercise intensity can no longer be maintained whereas fatigue develops gradually from the beginning of the exercise. The definition of muscle fatigue as defined by Vøllestad and Sejersted [14] is closely related to the capacity of muscle force and valuable in e.g., muscle preparation experiments where the exerted force is measured directly at the individual muscle level or at the single muscle fiber level. However, these definitions do not mirror all the mechanical variables relevant for muscle performance in general, which also include measures such as the ability to exert a precise and steady force or to perform a precise movement in space [16], [17], [18]. Muscle performance in humans is therefore highly dependent on the activity pattern among muscles or in other terms load sharing between muscles. A more broad definition of fatigue also including measures of precision of force and precision in space during movements seems to be more valuable and useful in ergonomics, rehabilitation, sport etc. It is therefore suggested to define contraction related muscle fatigue as any impaired mechanical muscle performance.

The physiological signs of fatigue precede the mechanical failure where the expected performance can no longer be maintained. Changes in the electromyographic activity (decrease in the mean power frequency and/or an increase in the EMG-amplitude) during standardized voluntary contractions are frequently used as indicators of muscle fatigue [19], [20], [21]. EMG mainfestations of fatigue provide useful information on the status of the electrical excitation of the muscle. Therefore, EMG measurements recorded during endurance type tasks are not suitable as force estimate input to biomechanical models, since the level of the EMG amplitudes relative to muscle force change gradually, implying that load sharing in a muscle synergy cannot be obtained from the EMG measurements when fatigue is involved. Intramuscular pressure may be a better indirect measure of muscle force here since the intramuscular pressure correlates linearly with contraction force at any specific position. However, the magnitude of the intramuscular pressure varies with catheter position [22]. During a 30° arm abduction maintained until exhaustion a tendency to a decrease in intramuscular pressure in the supraspinatus muscle (first min: 53 mmHg, 29th min: 30 mmHg) was found despite a 100% increase in the myoelectric activity. The individual values of the intramuscular pressure suggest that some of the subjects were able to reorganize the shoulder muscle activation strategy in order to maintain the arm abduction [23]. Also forearm muscle activity pattern has been found to be influenced by fatigue. Thus, sudden changes in activity pattern among the forearm muscles have been documented for some subjects during a prolonged isometric wrist extension maintained until exhaustion. Further, the prolonged wrist extension was accompanied by increasing force variability as the contraction proceeded [18].

Reorganization of muscle activation strategy in response to prolonged exertions is assumed to be a compensatory mechanism to prevent overloading of the muscles, minimizing fatigue, and postponing point in time of the exhaustion. It could therefore be hypothesized that lack of ability to redistribute the muscle activation pattern in the shoulder region or in the upper extremity, as seen for some subjects, increases the risk of developing work related soft tissue symptoms and disorders.

Few studies have investigated the activity pattern of muscles in healthy subjects compared to patients suffering from soft tissue injuries. This means that knowledge about the potential functional consequences of symptoms in the shoulder and upper extremity is lacking. Michaud et al. [24] examined the electrical activity of the supraspinatus muscle and the deltoid muscle during submaximal isometric arm abductions in healthy subjects and of patients suffering from supraspinatus tendinitis. In contrast to their expectations no differences in the recruitment profile (EMG relative to torque and angle of abduction) for the supraspinatus muscle was found between the patients and the healthy subjects. However, EMG from the deltoid muscle showed a lower activity level in the abducted position for the patients compared to the healthy subjects. This is suggested to be a compensatory mechanism within the synergistic action of the muscles to decrease the compression of the supraspinatus insertion site between the humeral head and the acromion [24]. This study again emphasizes the importance of focusing on the function of the whole muscle synergy and not only on each muscle separately.

Another aspect related to load sharing, is the specific timing of the muscle activity among synergistic muscles during dynamic contractions. The temporal activity pattern of the arm muscles was studied during standardized tennis strokes in a group of tennis players suffering from tennis elbow [25]. Tennis elbow is an overuse syndrome of the forearm extensor muscles, primary the extensor carpi radialis muscle. The patient group was compared to a group of healthy tennis players. In this tennis elbow study a change in the temporal activity pattern was documented in the patient group compared to the healthy group. The patient group activated their forearm extensor muscles earlier, longer, and attained greater levels than their healthy controls. In contrast no significant differences in temporal activity pattern were found between the two groups for the forearm flexor muscles and the triceps muscle. Thus, differences in activity pattern were only documented in the affected muscle group. It is, however, not clear whether the differences in activity pattern are a cause or a response. In other words, is the development of tennis elbow related to unfavorable muscle activation pattern or do the patients change the activity pattern due to pain. This remains an open question that needs further research to be answered. A study by Veiersted contributes to the discussion. In a prospective study of industrial chocolate packer's shoulder muscle activity (m. trapezius) during work was investigated. One year later some of the chocolate packers had developed work related symptoms in the shoulder region. Analysis of the recorded EMG showed that chocolate packers with few EMG gaps (activity level <0.5% EMGmax for at least 200 ms) had an increased risk of developing work related shoulder symptoms [26], [27].

This study indicates that specific muscle activity patterns and thereby possibe load sharing may predispose to an increased risk of development of musculoskeletal symptoms.

Finally, it has been found that load sharing can be influenced by use of visual feedback techniques and by mental demands during work. In a study by Palmerud et al. [28] subjects were positioned with the arm elevated and with online visual EMG feedback. The subjects were instructed to minimize the activity of the trapezius, the deltoid, the infraspinatus and the supraspinatus muscle while maintaining the arm positions. The results showed that in one of the investigated muscles, the trapezius muscle, the activity could be reduced voluntarily by 22–47% in different static arm postures indicating voluntary redistribution of the shoulder muscle activity. These findings are suggested to be due to overstabilization of the shoulder [28]. Also various feedback modes on musculoskeletal performance may per se elicit different muscle involvement [29].

Furthermore, certain types of mental demands such as motivation and continuing attention demands have been shown to increase the muscle activity in certain muscles, e.g., [30]. In a recent study forearm muscle activity was measured during intermittent handgrip (5 s on/5 s off) contractions while solving attention demanding problems. Despite of a fully supported forearm and hand a rather high level of activity was found in the resting periods between the contractions, where no external force was exerted, indicating a contribution of the mental demand to the muscle activity [31].

Section snippets

Conclusion

A relatively fixed load sharing of the shoulder muscles was found at low load levels, submaximal speeds and with a limited range of movements of the arms for healthy subjects. However, the load sharing of the muscles can be changed to some extent in response to fatigue, mental demands, visual feedback and in patients suffering from disorders in the upper extremities.

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