ABSTRACT
The mechanical and neurological properties of ligaments are reviewed and updated with recent development from the perspective which evaluates their role as a source of neuromusculoskeletal disorders resulting from exposure to occupational activities. Creep, tension-relaxation, hysteresis, sensitivity to strain rate and strain/load frequency were shown to result not only in mechanical functional degradation but also in the development of sensory-motor disorders with short- and long-term implication on function and disability. The recently exposed relationships between collagen fibers, applied mechanical stimuli, tissue microdamage, acute and chronic inflammation and neuromuscular disorders is delineated with special reference to occupational stressors.
Author Keywords: Ligaments; Muscles; Reflexes; Risk factors; Ergonomics
ARTICLE OUTLINE
1. Introduction
2. Ligament structure
3. Mechanical properties
4. Recovery of creep and tension-relaxation with rest
5. Responses to increased physical activity and inactivity
6. Ligament inflammation
7. Ligaments as sensory organs
8. Ligamento-muscular reflex
9. Neuromuscular disorders
10. Conclusion
Acknowledgements
References
Vitae
1. INTRODUCTION
There are several ligaments in every joint in the human skeleton and they are considered as the primary restraints of the bones constituting the joint. Ligaments are also sensory organs and have significant input to sensation and reflexive/ synergistic activation of muscles. The muscles associated with any given joint, therefore, also have a significant role as restraints. In some joints, such as the intervertebral joints of the spine, the role of the muscles as restraints is amplified. The role of ligaments as joint restraints is rather complex when considering the multitude of physical activities performed by individuals in routine daily functions, work and sports, the complexity of the anatomy of the different joints and the wide range of magnitude of the external loads. The functional complexity of ligaments is amplified when considering their inherent viscoelastic properties such as creep, tension-relaxation, hysteresis and time or frequency dependent length-tension behavior. As joints go through their range of motion, with or without external load, the ligaments ensure that the bones associated with the joint travel in their prescribed anatomical tracks, keep full contact of the articular surface, prevent separation of the bones from each other by increasing their tension, as may be necessary, and ensuring stable motion. Joint stability, therefore, is the general role of ligaments without which the joint may subluxate, cause damage to the capsule, cartilage, tendons, nearby nerves and blood vessels, discs (if considering spinal joints) and to the ligaments themselves. Such injury may debilitate the individual by preventing or limiting his/her use of the joint and the loss of function. Unstable joints are also known to drastically modify the intra-articular pressure and the muscular activity about the joint, resulting in early onset of osteoarthritis, pain, disability and eventually the need for joint replacement surgery. Dysfunctional or ruptured ligaments, therefore, result in a complex syndrome, various sensory-motor disorders and other long-term consequences which impact the individuals well-being, employer, skilled work force pool and national medical expenses.
2. LIGAMENT STRUCTURE
Ligaments consist of closely packed, parallel collagen fibers which appear to have various degrees of undulation (or helical) form along the axis of each fiber at a resting length. There are also short cross fibrils which connect the axial fibers to each other. The helical shape of various wave size of each fiber or group of fibers (bundles) gives rise to a process called “recruitment”. As axial stretching of a ligament is applied, fibers or bundles with a small helical wave appearance straighten first and begin to offer resistance (increased stiffness) to stretch. As the ligament is further elongated, fibers or fiber bundles of progressively larger helical wave straighten and contribute to the overall stiffness. Once all the fibers are straightened a sharp increase in stiffness is observed. Overall, the recruitment process gives rise to a non-linear length-tension relationship of a ligament shown in Fig. 1 (see also next section).
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The geometric shape of a ligament and its insertion into the bones associated with their joint give rise to another “recruitment” process. The medial collateral ligament of the elbow, for example, is a thin fan-shaped structure where the collagen fibers radiate from a relatively small, focal area in the distal humerus, but terminate on a large segment of the ulna. This type of geometric arrangement recruits different bundles of the ligament at different elbow angles. At full extension the anterior fibers are stretched and offer resistance, whereas with flexion, the anterior fibers gradually relax as more posteriorly situated fibers straighten and stretch.
The intraspinous ligament, for example, has a membrane-like arrangement with the fiber direction set diagonally to the axis of the spine, such as to provide the optimal forces during a relevant component of the range of motion of the intervertebral joint in flexion.
Even the simplest, rope-shaped ligaments, such as the anterior cruciate ligament undergoes a type of regional recruitment; the rotation (screw home) mechanism during knee extension causes the ligament to twist in addition to its axial stretch, recruiting different fiber bundles.
Overall, the mostly collagen (75%), elastin and other substances structure of ligaments is custom tailored by long evolutionary processes to provide various degrees of stiffness at various loads and at various ranges of motion of a joint, while optimally fitting the anatomy inside (inter-capsular) or outside (extra-capsular) a given joint. The various degrees of helical shape of the different fibers allows generation of a wide range of tensile forces by the fiber recruitment process, whereas the overall geometry of the ligament allows selective recruitment of bundles such as to extend function over a wide range of motion. The large content of water (70%) and the cross weave of the long fibers by short fibers provides the necessary lubrication for bundles to slide relative to each other, yet to remain bundled together and generate stiffness in the transverse directions.
3. MECHANICAL PROPERTIES
Ligaments are functional (effective) under tension, or when stretched and completely non-functional in compression or when shortened below their resting length. The general response of ligaments to stretch or tension is rather complex and non-linear, and subjected to several phenomena which are time-dependent, such as creep, tension-relaxation, strain rate and hysteresis. Ligament length-tension (or strain-stress) behavior is also temperature-dependent, exhibiting reduced capability to sustain load as temperature increases, while at the same length [82].
The general length-tension (or strain-stress) behavior of a ligament is non-linear as shown in the schematic diagram of Fig. 1.
The initial segments of the curve demonstrate rather large strain for very small increase in load. Once all the waves in the collagen fibers of the ligament have been straightened out, and all of the fibers were recruited, additional increase in strain is accompanied with a fast increase in tension. The resting length of ligaments is a difficult issue to establish due to the complexity of measurements in vivo. Some interesting data, however, show that the anterior cruciate ligament in the knee has relatively no changes in length between 60° to full flexion, and a fast increase in strain when extending the knee from 60° to full extension [56]. In that study, the authors normalized the measurement to show negative strain in the flexed range, whereas the same data could be presented as zero strain. It is conceivable that the resting length is near or just above the origin of the length-tension curve.
When a constant load is applied to a ligament, it first elongates to a given length. If left at the same constant load, it will continue to elongate over time in an exponential fashion up to a finite maximum. This elongation over time is termed “creep”, and is expressed as the percent elongation relative to the length it arrived to immediately after the load was applied. Fig. 2, depicts the response of a ligament to a constant load over time, as well as the creep. The recovery of the creep with rest, after the load was removed is also shown [72].
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When ligaments are subjected to a stretch and hold over time (or constant elongation) the tension-relaxation phenomena is observed. The tension in the ligament increases immediately upon the elongation to a given value. As time elapses, the tension decreases exponentially to a finite minimum while the length does not change. Fig.3 depicts the tension-relaxation phenomena associated with the constant elongation paradigm, as well as its recovery following rest [29].
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The tension developed in a ligament also depends on the rate of elongation or strain rate [49]. In general, slow rates of elongation are associated with the development of relatively low tension, whereas higher rates of elongation result in the development of high tension. Fast stretch of ligaments, such as in high frequency repetitive motion or in sports activities are known to result in high incidents of ligamentous damage or rupture. Fig. 4 depicts the length-tension curve for a supraspinous ligament stretched at different rates [13]. From the figure, it is evident that the supraspinous ligament can develop up to 50% more tension at a given length if stretched at 200% / s, relative to 25% / s. Fast rates of stretch, therefore, may exceed the physiological loads that could be sustained by a ligament safely, yet it may still be well within the physiological length range.
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In occupational activities, minimizing the speed of motion for a given task can contribute toward safer working conditions, especially when such tasks are repetitive.
Another important behavioral property of ligaments is its inability to track the same length-tension curve when subjected to a single stretch-release or load-unload cycle, i.e. hysteresis. This phenomenon is also associated with repetitive motion when a series of stretch-release cycles are performed over time. When the ligament is stimulated repetitively with constant peak load, the hysteresis develops along the length axis, i.e. the ligament length limits increase with each cycle reflecting the hysteresis associated with the development of creep as shown in Fig. 5B.
Conversely, when cycles of constant peak stretch are applied, the peak tension decreases in sequential cycles, reflecting the on-going development of tension-relaxation. Fig. 5A depicts the hysteresis exhibited under constant elongation [8 and 67].
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The impact of hysteresis, therefore, is manifested by gradually decreasing tension in the ligament, development of joint laxity, reduced joint stability and increased risk of injury. Repetitive occupational tasks should be limited in duration and allow sufficient rest periods to facilitate recovery of normal ligament function.
Ligament behavior is also dependent on the frequency of load application and unloading, such as in repetitive occupational tasks. Cyclic loading of a ligament with the same peak load, but at a higher frequency, results in larger creep development and longer period of rest required for the full recovery of the creep [36]. The data in Fig. 6 show the peak displacement of the supraspinous ligament subjected to a peak load of 40 N, but at two different frequencies: 0.1 and 0.5 Hz. The data show that the initial displacement at 0.1 Hz is larger than the initial displacement at 0.5 Hz, but the creep developed at the end of 20 min is much larger for the loading frequency of 0.5 Hz. Similarly, the recovery of the creep takes much longer when loading at 0.5 Hz.
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Occupational tasks requiring repetitive motion at high frequency, therefore, induce larger creep in the ligaments of the workers, require longer rest time to recover, and probably induce larger risk for cumulative creep from one work session to the next, in the same day and from day-to-day. Larger creep results in increased laxity of the joint as the work goes on, and the associated risks as discussed above.
4. RECOVERY OF CREEP AND TENSION-RELAXATION WITH REST
The recovery of the creep developed in a ligament during a sustained loading is a relatively unexplored issue. Some early assessments in healthy humans and in vivo animal models show that creep developed over relatively short periods of 10-60 min of loading did not fully recover at the end of up to 2 h of rest [9, 12 and 40]. Crisco et al. [9] observed, however, that nearly full recovery was measured after 24 h rest. Recent evidence demonstrate that both creep and tension-relaxation induced in a 20-50 min of loading or stretching a ligament, respectively, demonstrated 40-60% recovery in the first hour of rest, whereas full recovery is a very slow process which may require 24-48 h [8,19, 29 and 66]. Fig. 2 and Fig. 3 provide experimental illustrations of the recovery of creep and tension-relaxation over 7-8 h of rest after the loading or stretch. It is evident, therefore, that loading or stretching a ligament over relatively short periods induces changes in its length-tension behavior that may last 20-40 times longer than the duration of the loading / stretching. This phenomenon has significant implications on the ability of a ligament to protect and stabilize joints in workers who are subjected to sequential periods of static or cyclic activities during a given day. As the work-rest periods go on, the ligament exhibit cumulative creep and reduction in its ability to protect the joint, causing the later wart of a work period (or day) to be more prone to injury. Since full recovery of the creep with rest also requires more than 24 h, there would be a cumulative creep from the previous work day at the beginning of a new work day. The phenomenon of inter- and intra-day cumulative creep is illustrated with experimental data from the supraspinous ligament in Fig. 6 and Fig. 7, and may provide valuable insights to the mechanical aspects of the development of cumulative trauma disorders.
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5. RESPONSES TO INCREASED PHYSICAL ACTIVITY AND INACTIVITY
Ligaments are adaptive to exercise or series of repetitive functions and to immobilization. Moderate exercise or occupational activities followed with sufficient rest and recovery results, over time, with increase in the strength of a ligament, as well as in its size and collagen content [20, 77, 78, 79, 80, 83, 89 and 861. These changes indicate enhanced collagen metabolism in response to the stimulus. Indeed, such stimulus was shown to increase the total number of collagen fibrils in the ligament, as well as in the fibril diameter [41, 42, 44, 45 and 89]. Overall, moderate repetitive stimulation of ligaments coupled with appropriate rest and recovery allows the tissue to hypertrophy, increase its strength and protect joint stability in persons exposed to more demanding physical activity [76].
Conversely, immobilization or reduced physical activity is accompanied with degenerative changes in the ligaments structure and function consisting of decreased collagen fiber diameter, fibril density and fibril number and overall collagen mass and its metabolism [1, 4, 32 and 77].
Furthermore, the immobilization seems to have significant impact on the ligament-bone junction (or insertion to the bone). Immobilization results in increased osteoclastic activity, resorption of bone and disruption of the pattern of diffusion of the ligament fibers into the bone [85]. Overall, immobilization or decreased physical activity results not only in weaker and thinner ligaments, but also in weaker attachment to the bones of the respective joint, increasing the risk for potential injury if drastic increases in physical activity are implemented. This is important to note when workers return to activity after prolonged sickness, unemployment or holiday. Similarly, changing position from one job to another where different type of physical functions are performed requiring relatively dormant joints to be fully engaged may result in high exposure to injury. A gradual “work in” period in such circumstances may be a safe method to avoid exposure to injury.
6. LIGAMENT INFLAMMATION
Inflammatory response in ligaments is initiated whenever the tissue is subjected to stresses which exceed its routine limits at a given time. For example, a sub-injury/ failure load, well within the physiological limits of a ligament when applied to the ligament by an individual who does not do that type of physical activity routinely. The normal homeostatic metabolic, cellular, circulatory and mechanical limits are therefore exceeded by the load, triggering an inflammatory response.
Similarly static or repetitive loading of a ligament, within its physiological limits, when extended over a period of time result in creep which is an expression of a micro-damage within the collagen fibers structure of the tissue. The micro-damage triggers inflammatory responses as well [5, 14, 17 and 39].
Inflammatory signs consisting of swelling, redness, elevated temperature and pain demonstrate that a healing process is underway. The collagen fibers are undergoing changes in cellular, metabolic and vascular condition in order to improve the mechanical properties of the ligament such that it may be able to negotiate with the increased demand to physical activity. The inflammation also manages the breakdown and removal of damaged protein and the importation of new protein to repair and reconstruct the micro-damage and hypertrophy the tissue.
Acute inflammation, therefore, represents the healing or upgrading of the ligament’s properties and if left undisturbed by additional over-exposure to stress or intervention of anti-inflammatory drugs will allow recovery and upgrading of the ligament [34].
Another case where acute inflammation is present is when physical activities presenting sudden overload/ stretch cause a distinct damage to the tissue which is felt immediately. Such cases, as a sudden loss of balance, a fall, collision with another person, exposure to unexpected load, etc., may result in what is called a sprain injury or a partial rupture of the ligament. Acute inflammation set in within several hours and may last several weeks and up to 12 months. The healing process, however, does not result in full recovery of the functional properties of the tissue. Mostly, only up to 70% of the ligaments original structural and functional characteristics are attained by healing post injury [82].
The inflammation process described above is designated as acute inflammation which is distinctly different from a chronic inflammation.
Chronic inflammation is an extension of an acute inflammation when the tissue is not allowed to rest, recover and heal. Repetitive exposure to physical activity and reloading of the ligament over prolonged periods without sufficient rest and recovery represent cumulative micro-trauma. The resulting chronic inflammation is associated with atrophy and degeneration of the collagen matrix leaving a permanently damaged, weak and non-functional ligament [34]. The dangerous aspect of a chronic inflammation is the fact that it builds up silently over many weeks, months or years (dependent on a presently unknown dose-duration levels of the stressors) and appears one day as a permanent disability associated with pain, limited motion, weakness and other disorders [57]. Rest and recovery allow only partial resolution of the disability [82]. Full recovery was never reported.
7. LIGAMENTS AS SENSORY ORGANS
While ligaments are primarily known as mechanical apparatus responsible for joint stability, they have equally important sensory functions. Anatomical studies demonstrate that ligaments in the extremity joints and the spine are endowed with mechanoreceptors consisting of: Pancinian, Golgi, Ruffini and bare nerve endings [6,15,18,22, 23, 28, 43, 50, 51, 53, 54, 60, 61, 63, 68, 87, 88 and 90]. The presence of such afferents in the ligaments confirms that they contribute to proprioception and kinesthesia and may also have a distinct role in reflex activation or inhibition of muscular activities.
Studies of patients with ruptured ACL exhibit decreased ability to accurately position/reposition their limbs, indicating defective kinesthetic sensation [62]. Similarly, such patients also demonstrate defective reflexive responses to joint loading that may disturb stability indicating that a deficit in proprioception is present as well [3, 65 and 69]. Overall, the decrease or loss of function in a ligament due to rupture or damage does not only compromise its mechanical contributions to joint stability, but also sensory loss of kinesthetic perception and fast reflexive activation of muscles and the forces they generate in order to enforce joint stability.
8. LIGAMENTO-MUSCULAR REFLEX
It was suggested, as far back as the turn of the last century, that a reflex may exist from sensory receptors in the ligaments to muscles that may directly or indirectly modify the load imposed on the ligament [48]. Experiments performed in the 1950s resulted in conflicting data and no conclusion [2,11,46, 47, 73 and 74]. A clear demonstration of a reflex activation of muscles by stimulation of the anterior cruciate ligament (ACL) was finally provided in 1987 [65] and reconfirmed several times since then [3, 10, 55, 30 and 31]. It was further shown that such a ligamento-muscular reflex exists in most extremity joints [16, 21, 33, 58, 59, 68, 52 and 701 and in the spine [26, 27, 75 and 71].
Biomechanical data demonstrate that the muscular activity elicited by the reflex from the anterior cruciate ligament always acts to prevent the distraction of the joint [24, 25, 35, 37 and 38], as well as reduce the strain in the ACL [56], establishing the functional objective of such reflex, synergistic activity of muscles and ligaments to maintain joint stability.
Recently, new evidence support that the ligamento-muscular reflex may also have inhibitory effects on muscles associated with that joint [69 and 81]. Indeed, such inhibition may prevent extremely large forces from developing in muscles that increase the stress in the ligaments. A typical case is demonstrated by inhibition of large quadriceps forces during extension in the range of motion of 60° to full knee flexion [7]. It is well established that quadriceps force in that range of motion contributes toward distraction of the knee [24], as well as increasing the strain in the ACL [56]. The reflex inhibition, therefore, also serves to protect the ligament.
Ligamento-muscular reflexes, therefore, may be inhibitory or excitatory, as may be fit to preserve joint stability; inhibiting muscles that destabilize the joint or increased antagonist co-activation to stabilize the joint.
Indirect control of joint stability, via the ligamento-muscular reflex, by activating muscles that do not cross the joint is observed in the ankle joint. Stimulation of the medial collateral ligament of the ankle results in activation of the intrinsic muscles of the foot. The force generated by these muscles increases the arch of the foot and thereby corrects or prevents eversion and the associated joint instability [70].
Another special case is the ligaments associated with the shoulder. The capsule surrounding the joint exhibits thickening bands on its superior, anterior and posterior region, as well as in its inferior region which constitutes relatively weak ligaments. In some cases the thickening is hardly noticeable, confirming the relatively minor mechanical role of these ligaments. The four bands, however, are well endowed with the four types of mechanoreceptors, indicating an increased importance of their sensory role in perception of joint position and in ligamento-muscular reflex activation [22 and 68]. Similarly, there are several articular nerves supplying the afferents in these ligaments and a complex, vivid reflexive activation of the muscles associated with the rotator cuff [21, 33 and 681. The muscles, therefore seem to be a major component in maintaining the stability of the shoulder.
The reflex from the ligaments, therefore, can provide muscular assistance for the preservation of joint stability directly (by muscles crossing the joint) or indirectly (by muscles not crossing the joint) using muscular activation or inhibition.
9. NEUROMUSCULAR DISORDERS
Considering the ligaments’ mechanical properties (length-tension, creep, tension-relaxation, hysteresis, etc.), together with its sensory-motor functions (kinesthesia, proprioception and reflex activation/inhibition of muscles) and biological behavior (hypertrophy, degeneration, inflammation and healing) can motivate one to form several hypothesis regarding its role in triggering neuromusculoskeletal disorders.
Workers engaged in daily performance of static or repetitive activities over periods of weeks or months will exhibit first hypertrophy of the ligaments, but still subjected to creep, tension-relaxation and hysteresis. The ligament becomes lax over a day’s work and cannot exert sufficient tension to maintain the motion of the bones on track and maintain even pressure distribution on the cartilage surface, while supporting the same external loads. Such degradation of function can cause increased exposure to injury as the work day progresses, while at the same time causing gradual degeneration of the articular surfaces of the joint, leading to osteoarthritis.
The development of cumulative creep in the ligament may build up at some point to trigger sufficient micro-damage in the collagen fibers with the acute inflammation becoming chronic and consequently degeneration of the ligament and permanent disability [34 and 571.
While the two disorders presented above are widely recognized due to long experience in the orthopaedic and rehabilitation clinics, the interaction of the mechanical and sensory (reflexive) properties of ligaments and the potential disorders that can result is still unexplored. As ligaments develop creep, tension-relaxation and hysteresis, the length or tension sensory thresholds of the various afferents are shifted significantly in the range of motion and with the loads experienced by the ligament through the same motion [13 and 67]. The direct results of such sensory thresholds shift is degradation in kinesthetic and proprioceptive perception that lead to inaccuracies of movement and dysfunctional reflexive activation of muscles.
Solomonow et al. [72] described a neuromuscular disorder, consisting of five distinct components, associated with static loads applied to lumbar ligaments. The first component consists of a gradually decreasing reflexive muscular activity which is directly related to the creep developed in the ligaments, eliciting a shift in the sensory trigger thresholds of the reflex.
The second component consists of spasms observed during the static loading (lumbar flexion) period, elicited by the micro-damage in the collagen fibers and relayed reflexively by pain receptors.
The third component was observed in the first hour of rest after the static loading. This was expressed as a transient hyper-excitability of reflexive muscular activity. The hyperexcitability was attributed to the attempt of the musculature to protect the severely stretched ligament from any further development of micro-damage until substantial recovery of creep took place.
The fourth component consisted of a relatively prolonged reflex muscular hyperexcitabiltiy that gradually increased from the second to the sixth hour of rest after static loading of the lumbar ligaments. The amplitude of this “morning after” hyperexcitability was much stronger than the initial hyperexitability by two- to three-fold and seemed to last over 24 h. This component was correlated to the development of inflammation in the supraspinous ligament [66], which dictated the time constants of the development and decay of the hyperexcitability.
The fifth component of the disorder is the slow exponential recovery-of the reflexive EMG to its normal (initial) level as rest time progresses.
Similar responses were observed by Claude et al. [8] when cyclic loading of lumbar viscoelastic tissues were performed.
Fig. 8 shows recording of reflexive EMG from the multifidus muscles while the lumbar spine and the supraspinous ligaments are subjected to cyclic anterior flexion for 20 min followed by 7h of rest. The development of creep and its recovery and the corresponding spasms and two hyperexcitabilities are noticeable in the different phases.
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Fig. 9 shows the pooled, processed data of Fig. 8, together with a few other in vivo specimen subjected to the same cyclic anterior flexion of the lumbar spine. Note the creep and its recovery with rest as well as the five components of the neuromuscular disorder.
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Fig. 10 shows a schematic of the five components of the neuromuscular disorder associated with creep during the loading period and the following rest.
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The mechanical properties of the viscoelastic tissue of ligaments (and other such tissues as discs, facet capsule, doroslumbar fascia, etc.) could give rise to or be the source of a neuromuscular disorder. Prolonged exposure of a joint to static posture allows the development of creep (in a constant load condition) or tension-relaxation (in a constant displacement condition). Data obtained from normal, healthy young subjects shows that spasms develop in the musculature during the static activity and significant modification of muscular activity, primarily hyperactivity, is observed after the loading period [7 and 64]. The above results obtained from the ACL in the knee and from the lumbar spine reinforces the assertion made earlier concerning the similar behavior of the ligamento-muscular reflex in most, if not all, the major joints.
10. CONCLUSION
It is evident that ligaments evolved to become the optimal biological passive tissue to provide the function of joint stability. Ligaments are also adaptive to the extent that increase and decrease in physical activity is accompanied with hypertrophy and atrophy, respectively. Their normal function, however, is dependent on a dose-duration-rest formula which is not known at the present. Sufficient rest between periods of physical activity seems to be of paramount importance for long-term healthy, normal function, and such data are just becoming available.
Due to the mechanical properties of viscoelastic tissue, two classes of disorders originate from ligaments; mechanical and neuromusculoskeletal. Mechanical deficits such as joint laxity, instability, osteoarthritis, sprain, rupture, etc., are the direct result of creep, tension-relaxation, hysteresis and time/frequency dependence of the length-tension of ligaments.
The same mechanical factors are also manifested with complex sensory-motor disorders (or syndrome) associated with changes in kinesthetic and proprioceptive perception, reflex activation of muscles and overall performance. Inflammatory responses of viscoelastic tissues, a result of mechanical stimuli seems to be a significant factor in the development of cumulative trauma disorders in workers maintaining jobs that require daily performance of static and repetitive motion.
ACKNOWLEDGEMENTS
This work was supported by the National Institute of Occupational Safety and Health with Grants OH-04079 and OH-07622, and by the Occupational Medicine Research Center Grant, HEF (2000-5)-7 from the Louisiana Board of Regents.
REFERENCES
1. D. Amiel, W.H. Akeson and F.L. Harwood, Stress deprivation effect on metabol-is turnover of the medial collateral ligament collagen: A comparison between nine- and 12-week immobilization. Clin. Orthop. 172 (1983), pp. 265-270. Abstract-MEDLINE I Abstract-EMBASE
2. S. Andersson and B. Stener, Experimental evaluation of the hypothesis of ligamento-muscular protective reflexes, II. A study in cats using medial collateral ligament of the knee joint. Acta Physiol. Scand. 166 Suppl. (1959), pp. 27-49. Abstract-MEDLINE
3. D.J. Beard, P.J. Kyberd, J.J. O’Connor, C.M. Fergusson and C.A.F. Dodd, Reflex hamstring contraction in anterior cruciate ligament deficiency. J. Orthop. Res. 12 (1994), pp. 219-228. Abstract-MEDLINE I Abstract-EMBASE I Abstract-Compendex Full Text via CrossRef
4. J.M. Binkley and M. Peat, The effect of immobilization on the ultra structure and mechanical properties of the medial collateral ligament of rats. Clin. Orthop. 203 (1986), pp. 301-308. Abstract-MEDLINE I Abstract-EMBASE
5. W. Bryant, Wound healing. Clin. Symp. 29 (1977), pp. 1-36.
6. P. Burgess and F. Clark, Characteristics of knee joint receptors in the cat. J. Physiol. 203 (1969), pp. 317-335. Abstract-MEDLINE
7. D. Chu, R. LeBlanc, P. D’Ambrosia, R. D’Ambrosia, R.V. Baratta and M. Solomonow, Neuromuscular disorder in response to anterior cruciate ligament creep. Clin. Biomechanics 19 (2003), pp. 222-230. SummaryPlus I Full Text + Links I PDF (192 K)
8. L. Claude, M. Solomonow, B. Zhou, R.V. Baratta and M. Zhu, Neuromuscular dysfunction elicited by cyclic lumbar flexion. Muscle and Nerve 27 (2003), pp. 348-358. Abstract-Elsevier BIOBASE I AbstractMEDLINE I Abstract-EMBASE I Full Text via CrossRef
9. J. Crisco, S. Chelikani and R. Brown, Effects of exercise on ligamentous stiffness in the wrist. J. Hand Surg. 22A (1997), pp. 44-48. Abstract-MEDLINE I AbstractEMBASE
10. P. Dyhre-Poulsen and M. Krogsgard, Muscular reflexes elicited by electrical stimulation of the anterior cruciate ligament in humans. J. Appl. Physiol. 89 (2000), pp. 2191-2195. Abstract-MEDLINE I AbstractElsevier BIOBASE I Abstract-EMBASE
11. J. Ekholm, G. Eklund and S. Skoglung, On the reflex effects from the knee joint of the cat. Acta Physiol. Scand. 50 (1960), pp. 167-174. Abstract-MEDLINE
12. L. Ekstrom, A. Kaigle, E. Hult et al., Intervertebral disc response to cyclic loading: An animal model. Proc. Inst. Mech. Engr. 209 (1996), pp. 249-258. Abstract-MEDLINE I Abstract-Compendex I Abstract-INSPEC
13. E. Eversull, M. Solomonow, B. Zhou, R.V. Baratta and M. Zhu, Neuromuscular neutral zones sensitivity to lumbar displacement rate. Clin. Biomechanics 16 (2001), pp. 102-113.
14. C. Frank, D. Amiel, S. Woo and W. Akeson, Normal ligament properties and ligament healing. Clin. Orthopaedics. 1% (1985), pp. 15-25. Abstract-MEDLINE I Abstract-EMBASE
15. M. Freeman and B. Wvke, The innervation of the knee joint: An anatomical and histological study in the cat. J. Anat. 101 (1%7), pp. 505-532. Abstract-MEDLLNE
16. M. Freeman and B. Vvke, Articular reflexes at the ankle joint: an electromvographic study of normal and abnormal influences of ankle-joint mechanoreceptors upon reflex activity in the leg muscles. Br. J. Surg. 54 (1967), pp. 990-1001. AbstractMEDLINE
17. J. Gamble, The Musculoskeletal System; Physiological Basics. , Raven Press, NY (1988).
18. E. Gardner, The distribution and termination of nerves in the knee joint of the cat. J. Comp. Neurol. 80 (1944), pp. 11-32. Full Text via CrossRef
19. U. Gedalia, M. Solomonow, B. Zhou, R.V. Baratta, Y. Lu and M. Harris, Biomechanics of increased exposure to lumbar injury by cyclic loading: II. Recovery of reflexive muscular activity with rest. Spine 24 (1999), pp. 2461-2467. Abstract-MEDLINE I AbstractEMBASE I Full Text via CrossRef
20. M. Gomez, The effect of tension on normal and healing medial collateral ligament. Thesis, University of California, San Diego, 1988.
21. C. Guanche, T. Knatt, M. Solomonow, Y. Lu and R.V. Baratta, The synergistic action of the capsule and shoulder muscles. Am. J. Sports Med. 23 (1995), pp. 301-306. AbstractMEDLINE I Abstract-EMBASE
22. C. Guanche, J. Noble, M. Solomonow and C. Wink, Periarticular neural elements in the shoulder. Orthopaedics 22 (1999), pp. 615-617. Abstract-MEDLINE I AbstractEMBASE
23. Z. Halata, T. Retting and W. Schulze, The ultra-structure of sensory nerve endings in the human knee joint capsule. Anat. Embryol. 172 (1985), pp. 65-275.
24. S. Hirokawa, M. Solomonow, Y. Lu, Z.P. Lou and R. D’Ambrosia, Anterior posterior and rotational displacement of the tibia elicited by quadriceps contraction. Am. J. Sports Med. 20 (1992), pp. 299-306. AbstractEMBASE I Abstract-MEDLINE
25. S. Hirokawa, M. Solomonow, Y. Lu, Z. Lou and R. D’Ambrosia, Muscular co-contraction and control of knee stability. J. EMC Kinesiol. 1 (1991), pp. 199-208. Abstract
26. A. Indahl, A. Kaigle, O. Reikeras and S. Holh, EMG response of porcine multifidus musculature after nerve stimulation. Spine 20 (1995), pp. 2652-2658. Abstract-MEDLL-E I Abstract-EMBASE
27. A. Indahl, A. Kaigle, 0. Reikeras and S. Holm, Interaction between porcine lumbar intervertebral disc, zvgapophysial joints and paraspinal muscles. Spine 22 (1997), pp. 2834-2840. Abstract-. EDLINE AbstractEMBASE I Full Text via CrossRef
28. H. Jackson, R. Winkelman and VV. Bickel, Nerve endings in the human lumbar spinal column and related structures. J. Bone Joint Surg. 48A (1966), pp. 1272-1281. AbstractMEDLINE
29. M. Jackson, M. Solomonow, B. Zhou, R.V. Baratta and M. Harris, Multifidus EMG and tension-relaxation recovery after prolonged static lumbar flexion. Spine 26 (2001), pp. 715-723. Abstract-EMBASE I AbstractMEDLINE I Full Text via CrossRef
30. H. Johansson, P. Sjolander, P. Sojka and I. Wadell, Reflex actions on the gammamuscle-spindle systems of muscles acting at the knee joint elicited by stretch of the posterior cruciate ligament. Neuro. Orthop. 8 (1989), pp. 9-21. Abstract-EMBASE
31. A. Kim, A. Rosen, V. Brander and T. Buchanan, Selective muscle activity following electrical stimulation of the collateral ligaments in human knees. Arch Phys. Med. Rehab. 76 (1995), pp. 750-757. Abstract I PDF (1169 K)
32. L. Klein, J.S. Player and K.G. Heiple, Isotopic evidence for resorption of soft tissues and bone in immobilized dogs. J. Bone Joint Surg. 64A (1982), pp. 225-230. AbstractMEDLINE I Abstract-EMBASE
33. T. Knatt, C. Guanche, M. Solomonow, Y. Lu, R.V. Baratta and B. Zhou, The Glenohumeral-biceps reflex in the feline. Clin. Orthop. Rel. Res. 314 (1995), pp. 247-252. Abstract-MEDLINE I Abstract-EMBASE
34. W. Leadbetter, An Introduction to sports induced soft tissue inflammation. In: W. Leadbetter, J. Buckwalter and S. Gordon, Editors, Sports Induced Inflammation, AAOS, Park Ridge, IL (1990).
35. J. Louie and C. Mote, Contribution of the musculature to rotary laxity and torsional stiffness at the knee. J. Biomech. 20 (1987), pp. 281-300. Abstract
36. D. Lu, M. Solomonow, B. Zhou, R.V. Baratta, L. Li, Frequency dependent changes in neuromuscular responses to cyclic lumbar flexion. J. Biomechanics (in press).
37. K. Markolf, A. Graff-Radford and H. Amstutz, In vivo knee stability. J. Bone Joint Surg. [Am] 60 (1978), pp. 664-674. AbstractMEDLINE I Abstract-EMBASE
38. K. Markolf, J. Mensch and H. Amstutz, Stiffness and laxity of the knee: Contribution of the supporting structures. J. Bone Joint Surg. 58 (1976), pp. 583-594. AbstractEMBASE I Abstract-MEDLINE
39. A. Martinez-Hernandez, Repair, degeneration and fibrosis. In: E. Farber and J. Farber, Editors, Pathology, JB Lippincott, Philadelphia (1988).
40. S. McGill and S. Brown, Creep response of the lumbar spine to prolonged full flexion. Clin. Biomechanics 7 (1992), pp. 43-46. Abstract
41. H. Michna, Morphometric analysis of loading-induced changes in collagen-fibril populations in young tendons. Cell Tiss. Res. 236 (1984), pp. 465-470. Abstract-MEDLINE I Abstract-EMBASE
42. E. Mosler, W. Folkhard and E. Knorzer Stress-induced molecular rearrangement in tendon collagen. J. Mol. Biol. 182 (1985), pp. 589-596. Abstract
43. V. Mountcastle, Medical Physiology. , Mosby-Year Book, St Louis (1974).
44. T. Nemetschek, K. Jelinek, E. Knorzer et al., Transformation of the structure of collagen: A time- resolved analysis of mechanochemical processes using synchrotron radiation. J. Mol. Biol. 167 (1983), pp. 461-479. Abstract-EMBASE I Abstract-MEDLINE
45. B.W. Oakes, A.W. Parker and J. Norman, Changes in collagen fiber populations in young rat cruciate ligaments in response to an intensive one month’s exercise program. In: P. Russo and G. Gass, Editors, Human Adaption, Cumberland College of Health Sciences, Williamsberg, KT (1981), pp. 223-230.
46. I. Palmer, On the injuries of the ligaments of the knee joint. Acta Chir. Scand. Suppl. 53 (1938).
47. I. Palmer, Pathophysiology of the medial ligament of the knee joint. Acta Chir. Scand. 115 (1958), pp. 312-318. AbstractMEDLINE
48. E. Payr, Der heutige Stand der Gelenkchirugie. Arch Min. Chir. 148 (1900), pp. 404-451.
49. R.H. Peterson, The effect of strain rate on biomechanical property of the medical collateral ligament. Thesis, San Diego, University of California, 1986.
50. S. Petrie, J. Collins, M. Solomonow, C. Wink, R. Chuinard and R. D’Ambrosia, Mechanoreceptors in the human elbow ligaments. J. Hand Surg. 23A (1998), pp. 512-518. Abstract-MEDLINE I Abstract-EMBASE
51. S. Petrie, J. Collins, M. Solomonow, C. Wink and R. Chuinard, Mechanoreceptors in the palmar wrist ligaments. J. Bone Joint Surg. 79B (1997), pp. 494-496. AbstractMEDLINE I Abstract-EMBASE I Full Text via CrossRef
52. D. Phillips, S. Petrie, M. Solomonow, B.H. Zhou, C. Guanche and R. D’Ambrosia, Ligamento-muscular protective reflex in the elbow. J. Hand Surg. 22A (1997), pp. 473-478. Abstract-EMBASE I Abstract-MEDLINE
53. P. Polacek, Receptors in the joints: their structure, variability and classification. Acta Fac. Med. 2 (1966), pp. 1-107.
54. U. Proske, H. Schaible and R. Schmidt, Joint receptors and kinesthesia. Exp. Brain Res. 72 (1988), pp. 219-224. Abstract-MEDLINE I Abstract-EMBASE
55. J. Raunest, M. Sager and E. Biirgener, Proprioceptive mechanisms in the cruciate ligaments: an electromyographic study on reflex activity in the thigh muscles. J. Trauma: Injury, Infect. Crit. Care 41 (1996), pp. 4881493. Abstract-MEDLINE I Full Text via CrossRef
56. P. Renstrom, S.W. Arms, T.S. Stanwyck, R.J. Johnson and M.M. Pope, Strain within the ACL during hamstring and quadriceps activity. Am. J. Sports Med. 14 (1986), pp. 83-87. Abstract-EMBASE I Abstract-MEDLINE
57. M. Safran, Elbow injuries in athletes: a review. Clin. Orthop. 310 (1985), pp. 257-277.
58. H. Schaible and R. Schmidt, Response of fine medial articular nerve afferents to passive movements to the knee joint. J. Neurophysiol. 49 (1983), pp. 1118-1126. Abstract-EMBASE I Abstract-MEDLINE
59. H. Schaible, R. Schmidt and W. Willis, Response of spinal cord neurons to stimulation of articular afferent fibers in the cat. J. Physiol. 372 (1986), pp. 575-593. AbstractMEDLINE I Abstract-EMBASE
60. R.A. Schulz, D.C. Miller, C.S. Keer and L. Micheli, Mechanoreceptors in the human cruciate ligaments. J. Bone Joint Surg. [Am] 66 (1984), pp. 1072-1076.
61. P. Sjolander, A sensory role for the cruciate ligaments. Dissertation, Umea University, Umea, Sweden, 1989.
62. H. Skinner and R. Barrack, Joint position sense in the normal and pathologic knee joint. J. EMG Kinesiol. 1 (1991), pp. 180-190. Abstract
63. S. Skoglund, Anatomical and physiological studies of the knee joint innervation in the cat. Acta Physiol. Scand. (Suppl.) 36124 (1956), pp. 1-101. Abstract-MEDLINE
64. M. Solomonow, R.V. Baratta, A. Banks, C. Freudenberger and B. Zhou, Flexion-retaxation response to static lumbar flexion in males and females. Clin. Biomech. 18 (2003), pp. 273-279. SummaryPlus I Full Text + Links I PDF (227 K)
65. M. Solomonow, R.V. Baratta, B.H. Zhou, H. Shoki, W. Bose, C. Beck and R. D’Ambrosia, The synergistic action of the ACL and thigh muscles in maintaining joint stability. Am. J. Sports Med. 15 (1987), pp. 20-213.
66. M. Solomonow, R.V. Baratta, B. Zhou, E. Burger, A. Zieske, A. Gedalia, Muscular dysfunction elicited by creep of lumbar viscoelastic tissues. J. EMG Kinesiol. 13 (2003) 381-396.
67. M. Solomonow, E. Eversull, B. Zhou, R.V Baratta and M. Zhu, Neuromuscular neutral zones associated with viscoelastic hysteresis during cyclic lumbar flexion. Spine 26 (2001), pp. E314-E324. AbstractMEDLINE I Full Text via CrossRef
68. M. Solomonow, C. Guanche, C. Wind, T. Knatt, R. Baratta and Y Lu, Mechanoreceptors and reflex arc in the feline shoulder. J. Shoulder Elbow Surg. 5 (19%), pp. 139-146. Abstract I PDF (1578 K)
69. M. Solomonow and M. Krogsgaard, Sensor-motor control of knee stability: a review. Scand. J. Med. Sci. Sports 11 (2001), pp. 64-80. Abstract-MEDLINE
70. M. Solomonow and J. Lewis, Reflexive control of ankle stability. J. EMG Kinesiol. 12 (2002), pp. 193-198. SummaryPlus I Full Text + Links I PDF (143 K)
71. M. Solomonow, B. Zhou, M. Harris, Y. Lu and R.V. Baratta, The ligamento-muscular stabilizing system of the spine. Spine 23 (1998), pp. 2552-2562. Abstract-EMBASE I Abstract-MEDLINE I Full Text via CrossRef
72. M. Solomonow, S. Hatipkarasulu, B. Zhou, R.V. Baratta, F. Aghazadeh, Biomechanics and EMG of a common idiopathic low back disorder. Spine 28 (2003) 1235-1248.
73. B. Stener, Experimental evaluation of the hypothesis of ligamento-muscular protective reflexes: I. A method for adequate stimulation of receptors in the medial collateral ligament of the knee joint of the cat. Acta Physiol. Scand. 48 Suppl. 166 (1959), pp. 5-26. Abstract-MEDLINE
74. B. Stener and 1. Petersen, Electromyogaraphic investigation of reflex effects upon stretching the partially ruptured medial collateral ligament of the knee. Acta Chir. Scand. 124 (1962), pp. 396-414.
75. M. Stubbs, M. Harris, M. Solomonow, B. Zhou, Y. Lu and R.V. Baratta, Ligamentomuscular protective reflex in the lumbar spine of the feline. J. Electromyogr. Kinesiol. 8 (1998), pp. 197-204. SummaryPlus I Full Text + Links I PDF (238 K)
76. H. Suominen, A. Kiiskinen and E. Heikkinen, Effects of physical training on metabolism of connective tissues in young mice. Acta Physiol. Scand. 108 (1980), pp. 17-22. Abstract-MEDLINE I AbstractEMBASE
77. C.M. Tipton, S.L. James and W. Mergner, Influence of exercise on strength of medial collateral knee ligaments of dogs. Am. J. Physiol. 218 (1970), pp. 894-902. AbstractMEDLINE
78. A. Viidik, Simultaneous mechanical and light microscopic studies of collagen fibers. Z. Anat. Entwicklungsgesch. 136 (1972), pp. 204-212. Abstract-MEDLINE I Full Text via CrossRef
79. A. Viidik, The effect of training on the tensile strength of isolated rabbit tendons. Scand. J. Plast. Reconstr. Surg. 1 (1967), pp. 141-147. Abstract-MEDLINE
80. A. Viidik and R. Ekholm, Light and electron microscopic studies of collagen fibers under strain. Anat. Entwickl. 127 (1968), pp. 154-164. Full Text via CrossRef
81. M. Voigt, J. Jakobsen and T. Sinkjaer, Non-noxious stimulation of the glenohumeral joint capsule elicits strong inhibition of active shoulder muscles in conscious human subjects. Neurosci. Lett. 254 (1998), pp. 105-108. SummaryPlus I Full Text + Links I PDF (54 K)
82. S. Woo and J. Buckwalter, Injury and Repair of Musculoskeletal Soft Tissue, AAOS, Park Ridge, IL (1988).
83. S.L.Y. Woo, M.A. Gomez, D. Amiel and W. Akeson, The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. J. Biomech. Eng. 103 (1981), pp. 51-56. Abstract-MLDLINE I Abstract-INSPEC 1 Abstract-Compendex I Abstract-EMBASE
85. S.L.Y. Woo, M.A. Gomez and T.J. Sites, The biomechanical and morphological changes in the medial collateral ligament of the rabbit after immobilization and remobilization. J. Bone Joint Surg. 69A (1987), pp. 1200-1211. Abstract-EMBASE I AbstractMEDLINE
86. S.L.Y. Woo, M.A. Ritter, D. Amiel and W. Akeson, The biomechanical and biochemical properties of swine tendons: Long term effects of exercise on the digital extensors. Connect Tiss. Res. 7 (1980), pp. 177-183. Abstract-MEDLINE I Abstract-EMBASE
87. B. Wyke, The neurology of joints: A review of general principles. Clin. Rheum. Dis. 7 (1981), pp. 223-229.
88. H. Yahia and N. Newman, Innervation of spinal ligaments of patients with herniated disc. Pathol. Res. Pract. 187 (1991), pp. 936-938.
89. R.F. Zernicke, D.L. Butler, E.S. Grood et al., Strain topography of human tendon and fascia. J. Biomech. Eng. 106 (1984), pp. 177-180. Abstract-INSPEC I AbstractMEDLINE I Abstract-Compendex
90. M. Zimney and C. Wink, Mechanoreceptors in the tissues of the knee. J. EMG Kinesiol. 1 (1991), pp. 148-157.
Corresponding author.
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VITAE
Moshe Solomonow, Ph.D., M.D. (Hon) is a Professor and Director of Bioengineering and of The Occupational Medicine Research Center at Louisiana State University Health Sciences Center in New Orleans, Louisiana. He received the B.Sc.,and M.Sc. in Engineering and the Ph.D. in Engineering and Neuroscience from the University of California, Los Angeles.
He is the Founding Editor of The Journal of Electromyography and Kinesiology, and serves on the Editorial Board of several bioengineering and medical journals. Dr. Solomonow is a consultant to the National Science Foundation, National Institute of Health, Center for Disease Control, The Veterans Administration and scientific agencies of several European and Asiatic governments and Canada. He was a council member of the International Society of Electrophysiological Kinesiology, the International Society of Functional Electrical Stimulation, and the IEEE-Biomedical Engineering Society. He published over 120 refereed journal papers on motor control, electromyography, muscle, ligament and joint biomechanics, electrical muscle stimulation, prosthetics and orthotic systems for paraplegic locomotion, and supervised more than 150 engineering, physical therapy, medical students and orthopaedic residents, as well as postgraduate students and fellows from several countries.
Dr. Solomonow organized the EMG Tutorial Workshop in the ISB Congress, the Canadian Society of Biomechanics, The Human Factors and Ergonomics Society, and The Society for Clinical Movement Analysis, was on the organizing committee of numerous conferences and gave keynote and symposia lectures in many others. He received the Crump Award For Excellence in Bioengineering Research (UCLA), the Distinctive Contribution Award.
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