Factors involved in strain-induced injury in skeletal muscles and outcomes of prolonged exposures
Introduction
Muscle and tendon disorders are frequent in the work-place, resulting in loss of work and sometimes lead to disability [114]. Based on ergonomic assessment of the workplace and epidemiology of work-related musculoskeletal disorders, it is commonly believed that tissue intolerance to repeated loading plays a role in the etiology of cumulative trauma disorders and can actually lead to tendon pathology [65] and perhaps even tendinitis [89]. The reason for this is that the tissues involved are often in series with one another (bone to tendon to muscle to tendon to bone) or in parallel (muscle, nerve, and fascia). Therefore, additional loading of the attachments of the muscle could result if the muscle lost the ability to attenuate strains as a result of muscle pathology. Thus, the tissue initially responsible for the disorder (e.g. muscle) goes unrecognized as the source of the problem because site of pain occurs proximal or distal to the original tissue injury. Only a small part of the muscle, perhaps just one fascicle, needs to be fibrotic (stiff) for the muscle to behave as a tendon transmitting more force to the tendon of origin and to the attachment site where most of the pain receptors are found (e.g. periosteum).
Although many factors contribute to cumulative trauma disorders, this discussion will focus on how skeletal muscles lose the ability to resist externally applied forces which results in strain injury and the consequences of chronic exposure to repeated strains. Most detailed information comes from animal studies where entire muscles can be removed for functional and morphological assessments. The other advantage of animal studies is that the parameters used to produce strain injury, such as velocity, acceleration and range of motion, can be precisely controlled. However, unlike most human activities using low loads and high repetitions, the animal muscles are maximally activated by electrical stimulation so that 100% of the myofibers are active prior to the strain. The advantage of this approach is the responses seen (e.g. force deficit) are larger than would be expected for submaximal activities, while the disadvantage is that they are not typical of work-place exposure, except when high loads and high repetitions are used.
Section snippets
Strain injury: loss of strength (weakness) and power
A prolonged loss of strength (maximal isometric force) [33] not caused by neural and metabolic factors [29] and not recovering after one hour of rest [97]—a time normally sufficient for muscles to recover from fatigue [97]—is considered to be the hallmark of muscle strain injury (Fig. 1). The loss of power has also been reported for human muscles [90] as would be expected if maximal force declined. The loss of muscle strength or power from repeated strains (stretches of active muscles) can be
Strain injury: histopathologic changes
Injury can also be defined by counting the number of myofibers that have lost their cellular integrity (e.g. albumin positive myofibers [37], [60], [103]) or suffered intracellular protein degradation (desmin negative myofibers [6], [55], [97]). However, histopathologic changes do not correlate well with the magnitude of the strength loss [53], [63], [97], [110] or the time course of the force deficits [24], [56]. The reason for this lack of correlation is that the loss of strength is due to
Risk factors for muscle strain injury
When an active muscle or myofiber is stretched to produce a muscle strain (eccentric muscle action [17], lengthening contraction [62], pliometric contraction [47]), an immediate loss of force or torque results [14]—the muscle injury. The various factors that contribute to muscle injury from muscle strains producing subsequent force deficits or weakness are discussed below.
Peak stretch force
Job activities requiring high forces have been associated with upper extremity injuries [84], [85]. Not surprisingly then, the most important factor involved in the strength loss from muscle strain injury in animals was observed to be peak stretch force. When an active muscle is stretched, increased force or extra tension can be produced beyond the isometric maximum (Fig. 3) [46], [66]. The magnitude of the peak stretch force correlates with the amount of muscle injury [63], [106]. In contrast,
Number of stretches or strains
The next major factor involved in isometric force deficits from repeated strains is strain number or repetition. In a series of repeated stretches or strains, the amount of strength loss continues to increase with each subsequent strain thus providing indirect evidence of increased injury with increasing stretch number (Fig. 1, Fig. 3) [40]. However, the majority of the loss in force occurs early [40] with less loss occurring at higher repetition number (Fig. 1) [115] perhaps due to the decline
Muscle length
It is quite clear that muscles are more susceptible to injury at long muscle lengths [67] or on the descending limb of the length tension relationship [66]. For example, if humans are exposed to protocols that stretch the elbow extensor muscles at short muscle lengths or long muscle lengths, the greatest injury occurs from stretches at long muscle lengths [69]. The length of the stretch also influences the amount of damage that is produced with larger excursions producing more injury [14], [51].
Velocity and acceleration
Wrist movements with high-accelerations (i.e. increasing velocity) have an increased risk for cumulative trauma disorder [82]. In the work-place with uncontrolled movements under load, high acceleration or high velocity movements would require high deceleration forces (high peak strain forces). The muscles resist the load by lengthening in order to slow and stop the movement of the limb. Under controlled velocity conditions in animal muscles, an absence of influence of velocity of the stretches
Fiber type and size
It has been noted that fast (type II) muscle fibers are selectively damaged by acute bouts of repeated strains in rabbits [50]. We have found similar results for the medial gastrocnemius muscle of rats [97]. Since in animals fast myofibers are larger in cross-sectional area than slow myofibers, larger muscle fibers may be more prone to strain injury. Using very large numbers of strains in rats, we found that the small fiber fast (type II) fibers were the last to be injured (Willems and Stauber,
Location of fibers
Few studies have looked at the distribution of injured fibers within a muscle. In our studies, it would appear that there are regions more susceptible to injury and that under certain conditions, the fibers on the outer edge of the muscle on the opposite side to the tendon plate become injured first. In humans, a higher proportion of type II fibers were observed at the boundary of a fascicle than internally [86]. Little is known about the regional differences in injured fibers except that the
Sex
No difference between men and women in muscle response to repeated strains has been reported [77], but there was a difference in the post-injury degree of soreness with women reporting less soreness than men [101]. Since soreness results from post-injury inflammation, estrogen could alter the degree of inflammatory response to injury. Likewise in rats, force deficits produced by repeated strains were not different between males and females [111], [117], but in females less post-exercise
Age
In humans and mice, advanced age results in weakness as measured by maximal isometric force production, but the peak stretch force is maintained [41], [73]. Since peak stretch force is most important in producing muscle injury, strain-induced injury would be expected not to differ with advancing age. In old female rats, the magnitude of the force deficits of plantar flexor muscles in vivo following a series of 30 stretches was similar to that of young rats [115]. Similar force deficits were
Inflammation
A series of 30 strains can result in a 50% reduction in muscle force (Fig. 1) but, depending on the conditions, not all injuries are accompanied by inflammation [97]. Inflammation and histopathologic changes in skeletal muscle appear to require membrane damage and the entry of extracellular calcium into the muscle cell (Fig. 4).
Additional issues: health status
Other factors may also influence muscle pain and weakness resulting from occupational tasks. For instance, certain medications such as the lipophilic statins [102] can produce muscle pain and loss of strength. Any disease such as hypertension [39] that reduces the capillary density of skeletal muscles could also pose additional risks. Similarly, exercise intolerance has been reported for hypothyroid patients [61]. Therefore, exposure to environmental agents such as dioxin and polychlorinated
Muscle repair
It is well known that skeletal muscles can recover fully from a single bout of repeated strains [23], [28], [33], [33], [56], [109] even if cellular death occurred [93]. Muscle contains its own stem cell, the satellite cell, which can proliferate and participate in the regeneration of entire fibers [16], even if severely damaged by crush injury. The process requires many days but the muscles return to normal function and are often more resistant to injury (i.e. a training effect) [81], [100].
Chronic exposure to repeated muscle strains
Unlike the well documented muscle responses to chronic nerve stimulation [18], [42], [72], less is known about muscle responses to chronic strains. However, it appears that a continuum exists where load, repetition number and rest interval interact differently to produce both positive (muscle hypertrophy) [15], [119] or negative (muscle fibrosis) [92], [94], [96] outcomes. Such a continuum exists for other components of the musculoskeletal system such as bone where repeated microtrauma can make
Prevention
Unlike manual lifting [112], [113], there is no reported guide (equation) to serve to reduce injury from hand and upper extremity intensive tasks. The lack of a guide is due in part to the lack of knowledge of the cellular mechanisms of strain-induced muscle injury that would provide a rational basis for injury prevention [52]. However, from the limited information available, rest times may be the most important factor for reducing risk of strain injury, as well as for diminishing negative
Over-load and over-activity
Models of chronic overload [95] and over-activity [35], [58] have been reported in animals. It appears that they can follow the same pathway from muscle cell injury to the appearance of inflammation, perhaps even leading to fibrosis as seen in the diaphragm of rats and humans with COPD [76]. In fact, the extensor carpi radialis brevis from humans with long standing lateral epicondylitis [55] resembles much of the histopathogic changes seen in our overloaded and chronic strained rat muscles.
Summary
An acute bout of repeated strains can overcome a muscle’s ability to resist mechanical deformation and produce a strength loss that requires days to recover accompanied by inflammation and pain. The major factors that produce the loss of strength are within the muscle cell. The force generating structures (sarcomeres) are pulled apart by the externally applied force so that myofilament overlap does not occur without this overlap no force can be developed by that sarcomere. The other less
Recommendations for prevention
Performing different jobs on consecutive days requiring different muscle groups would allow muscles a day or more to recover. Since peak stretch force and repetition number are key factors in producing strain injury, decreased loads and velocity of movements should decrease the braking forces required to decelerate loaded limbs reducing muscle strains. Decreased velocity would also decrease the repetition number. Finally, education about the importance of rest would be beneficial.
Acknowledgements
The author thanks Drs. Cutlip, Smith, and Willems for their participation in this research, Francoise Stauber, Paul Harton and Roger Miller for technical assistance and John Firth and Erin Barill for working with the human volunteers. This work was supported in part by a Cooperative Agreement Number R01 OH002918 from the Centers for Disease Control and Prevention. Its contents are solely the responsibility of the author and do not represent the official view of the National Institute of
William T. Stauber was born in East Orange, New Jersey, William Stauber received degrees from Ithaca College (BS, Physical Therapy) and Rutgers University (MS, PhD, Physiology) with Dr. John Bird. He was a Muscular Dystrophy Association and a NIH Postdoctoral Fellow in Physiology and Biophysics with Dr. Byron Schottelius at the University of Iowa before moving to Morgantown in 1979 as an Assistant Professor. Dr. Stauber currently holds joint appointments as Professor in Neurology and the
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William T. Stauber was born in East Orange, New Jersey, William Stauber received degrees from Ithaca College (BS, Physical Therapy) and Rutgers University (MS, PhD, Physiology) with Dr. John Bird. He was a Muscular Dystrophy Association and a NIH Postdoctoral Fellow in Physiology and Biophysics with Dr. Byron Schottelius at the University of Iowa before moving to Morgantown in 1979 as an Assistant Professor. Dr. Stauber currently holds joint appointments as Professor in Neurology and the Division of Physical Therapy at West Virginia University.
Dr. Stauber is an internationally recognized scientist in the area of muscle adaptation to muscle damage and disease with over 85 peer-reviewed manuscripts, nine book chapters, and 65 abstracts. He participates in continuing education programs in physical therapy and was honored for his lifetime research contributions to physical therapy by being invited to give the Steven Rose Memorial Lecture at Washington University, St. Louis, Missouri, in 1999. In April 2002, Dr. Stauber became a recipient of the Benedum Distinguished Scholar Award.
Dr. Stauber is a Fellow of the American College of Sports Medicine and an honorary Fellow of the International College of Cranio-Mandibular Orthopedics. He has received research awards from North American Life and NASA and served on special emphasis panels for the NIH and on panels to review NASA’s research on muscle atrophy and its prevention by exercise and myostimulation. He has been funded by NIH and NASA and is the Principal Investigator on a NIOSH grant, currently in its 10th year.