EQUINE VETERINARY JOURNAL Vol. I. No. 1. January 1975
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Structural and Mechanical Properties of Tendon related to Function J. H. EVANS J. C. BARBENEL Bioengineering Unit, University of Strathclvde, Glasgow
ONE of the commonest and most disastrous lesions of the horse is tearing or strain of the suspensory ligament or flexor tendon (Rooney, 1969) yet surprisingly little research has been conducted into tendon function and dysfunction. In mechanical terms, tendon serves principally as a force transmitter. This passive role has long been recognised, but in recent years other mechanical functions have been attributed to tendon. These include that of a dynamic amplifier during rapid muscle contraction (Hill, 1951), an elastic energy store (Dawson and Taylor, 1973) and more commonly that of a force attenuator during rapid and unexpected movement (Smith, 1954; Barnett, Davies and McConaill, 1961). The tensile mechanical characteristics of tendon are extensively documented although the data presented are by no means comprehensive. In general, the investigators have either used tendon as a relatively simple, collagen-rich tissue for basic studies or they have been principally concerned with the rupture characteristics of tendon in vitro. Relatively little is known of the physiological significance of the load/deformation characteristics of tendons. It is often assumed that they provide a relatively stiff elastic link between bone and muscle and yet it has been clearly demonstrated that tendons exhibit time-dependent and probably, irreversible characteristics. In the literature there occur rather vague references to fatiguing which are possibly explicable in terms of the viscoelastic characteristics of this tissue. The following paper explores the relation between structure, function and rupture of tendons in general and discusses those characteristics which are probably of clinical significance. Reference is made to human and other animal tendons which have received considerably more attention than their equine counterparts. This is considered admissible as there is a basic similarity in the structure and function of most tendons. Presented at the annual congress of the British Equine Veterinary Association, Edinburgh, 1972.
STRUCTURE Tendon comprises mainly collagen in the form of submicroscopic fibrils, arranged in what is essentially a unidirectional structure. The aggregations of collagen fibrils within tendon are very variable, but it is reasonable to consider the principal unit of tendon structure to be the coherent bundle of collagenous fibrils lying between the tendon cells. These fibres or “primary tendon bundles” as they are sometimes named (Elliott, 1965) can range in diameter up to 300 pm. The arrangement of tendon fibres into larger units is more easily studied than the arrangement at the fibrillar level, but is also more variable. Fibres are grouped into bundles or fasciculi but the dimensions and arrangement of these bundles vary considerably from tendon to tendon. Most tendons exhibit considerable lateral adhesion between the bundles, yet some can be unfolded into a ribbon. In contrast the relative independence of the fibre bundles in tail tendons is most striking. Fresh tendon appears like “watered silk” and it is just possible to see with the unaided eye alternate dark and light transverse bands which are approximately 70 pm wide. These bands disappear when tension is applied to tendon, but reappear on relaxation (Viidik, 1972). However Rigby, Hirai, Spikes and Eyring (1959) reported that this structural change is irreversible above 4 per cent strain. The surface waveform has been investigated by several workers with conflicting results. On theoretical considerations, Lerch (1950) concluded that the apparent wave is due to a three-dimensional twisting of collagen fibrils within the primary tendon bundle. This hypothesis is supported by Verzar (1957) and Cruise (1958), but opposed by Rigby, et al. (1959) and Kiihnke (1962). It seems that the disagreement stems in part from the fact that not all tendons have identical structure. There is evidence to suggest that the majority of mammalian tendons are structurally very similar with the principal exception of tail tendon. Recent studies by Diamant, Keller, Baer, Litt and Arridge (1972) suggest that the
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Fig. 1.
Scanning electron micrograph of replica (Silcoset
105, ICI) o f an unstrainedfibre bundle from rat tail tendon. Regular crimping produces what is essentially a planar zig-zag. x 500.
fibrillar structure of tail tendon is sensibly two dimensional in that the fibrils describe a planar wave. This conclusion was reached by Diamant, et a/. (1972) using almost precisely the same polarising microscopical technique that had enabled Verzdr and Huber (1958) to conclude that tail tendon had a regular helical structure. Single micrographs presented by both authors appear identical. However Diamant and colleagues improved on the basic technique by rotating the tendon specimens about their long axis under the microscope. This technique satisfactorily differentiated between two- and three-dimensional structures and decided in favour of a planar, zig-zag fibrillar arrangement and against the helical array previously suggested. Recent studies by the authors using scanning electron microscopy would suggest that the conclusions drawn by Diamant, et a/. (1972) are basically correct. Using both unfixed rat tail tendon and silicon elastomer (Silcoset 105, IC1) replicas of fresh, unstrained tendon, the course of the collagen fibrils is readily observable. The structure is clearly seen in the electron micrograph (fig. I ) of rat tail tendon. Viewed normal to the principal plane of fibrillar array, the structure does indeed appear as a saw-tooth with abrupt reorientation of the fibrils at the peaks of the wave form. The scanning electron micrograph reveals, however, that the structure is not truly planar and the structure resembles a helical array which has been partially collapsed into two dimensions (see fig. 1). Discounting the literature relating to tail tendon, the concensus of opinion is that the collagen in mammalian tendon is arrayed in a sensibly parallel manner, but that it follows a helical course along the length of the tendon. Dale, Baer, Keller and Kohn (1972) claim that the planar wave form is common to all tendons. The surface wave which has been observed and reported by many authors (Elliott, 1965 and Viidik, 1968 and 1972) is not an indication that the fibrils adopt a planar wave form. Scanning electron micrographs of free tendon surfaces which have been enzymatically cleaned by using a amylase in the manner proposed by Finlay, Hunter and Steven, 1971 or hyaluronidase can reveal details of the packing of fibrils in the surface layer. Although it is possible, using limited enzymatic
digestion, to reveal the fibrils whilst leaving them adherent to one another, the most striking evidence of fibrillar packing is obtained by extending such enzymolysis to the point where individual fibrils or fibrillar groups become separated. Figs. 2 and 3 are micrographs of human tendons which have been treated with hyaluronidase to the point where their surfaces are partially disrupted. The impression of helical coiling of the fibres is clear and the arrangement whereby they are packed to produce a planar surface wave is readily deduced. Stereographic analysis has confirmed the existence of a helical structure (Barbenel, Evans and Gibson, 1971) but the dimensions of the helices (fig. 2) are clearly abnormal as the fibrillar bundles released from the parent tendon have contracted and otherwise distorted. Internal surfaces produced both by fracture along natural cleavage planes or by the microtome reveal considerable structural detail. The fibrillar packing observed on a surface produced by fracture is principally that of a parallel helical array (fig. 4) where all fibrils have similar form and aggregate in a close packed but sensibly non-intertwining arrangement. I t is interesting to note that this structure is identical to the “plasticine” model which Lerch (1950) constructed based on his light microscope studies. Lerch (1950) also demonstrated that fibrils cannot lie entirely in parallel array since fissures produced in a thin tissue section reveal fibrils crossing in both directions. The scanning electron micrograph (fig. 5) shows the same phenomenon in a surface produced by the microtome blade. The predominance of fibrils crossing in the onedirection indicates
Fig. 2. Scanninkr electron micrograph of unsrrained human palmaris longus tendon treated with hyaluronidase. Surface waveform evident with adjacent coiling fibres released b.v enzymolisis. x 225.
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that the fissure had not necessarily formed parallel to the mean fibrillar direction. The true migration of fibrils across the fissure is seen to be small and would suggest that interweaving of fibrils in the parent tendon is a secondary effect. At this level the rope-like structure sometimes attributed to tendon (Elliott, 1965) cannot be substantiated, although the observed fibrillar migration within the primary tendon bundles probably affords considerable lateral cohesion. However binding between fibre may not be attributable to fibrillar migration as the surfaces of fibre bundles revealed by longitudinal fracture (fig. 4) show no evidence of ruptured or loose surface fibrils. MECHANICAL PROPERTIES The mechanical characteristics of the tendon have been established almost exclusively by uniaxial tensile tests where the direction of loading coincides with the long axis of the tendon. The load/deformation characteristics of tendon in uniaxial tension are non-linear. Wertheim (I 847) described the relation as “a hyperbola whose apex is at the origin of the co-ordinates stress and strain”. The stress-strain behaviour is more commonly reported as comprising an initial lax response with progressive stiffening leading to a quasi-linear relationship. However, at higher stresses the tissue “yields” and the entire stress-strain relation to failure is best described as sigmoidal (fig. 6). The basic form of the quasi-static stress-strain relation for tendon was established some forty years ago (Gratz and Blackberg, 1935). In the intervening
Fig. 3 . Scanning electron micrograph of unstrained human palmaris longus tendon treated with hyaluronidase. Parallel, coiling fibres completely separated by enzymolisis. x 225.
Fig. 4. Scanning electron micrograph of unstrained human palmaris longus tendon treated with hyaluronidase. Fibrillar components of fibre aggregated in sensibly parallel array over an entire wavelength. x 650.
period this form has been reiterated in many papers in which data have been derived from a range of mammalian tendons and the rather specialised “tail” tendons, principally from the rat. Unfortunately much of these data relate to ultimate properties with the concomitant large experimental error and in general there has been little regard for the time-dependent characteristics of this tissue. The majority of investigators fit into two camps-those mainly concerned with characteristics of functional significance and those who have chosen the tendon for more basic investigations because of its relatively simple structure. Resulting from research in this latter group the literature abounds with mechanical data on denatured and chemically modified tendon. These data have little significance in functional terms. There appears to be no published data on the flexibility of tendon nor on its transverse or torsional characteristics. The ultimate tensile strength of tendon was first reported in 1844 by Valentin, Otz and Henzi. Ever since this early work the emphasis has been on stress at rupture and relatively little data have been published on the associated deformation. This corpus of work has been very fully reviewed by Cronkite ( I 936), Stucke( I950), Rollhauser (1950) and more recently by Elliott (1965). There is a suggestion from this data pool that the tensile strength of fresh tendon is in the range 5-10 kg/mm2 (50-100 MPa). Paradoxically, although clinically observed tendon ruptures are not uncommon, there are no published data on experimentally produced lesions in vivo. The literature relates almost exclusively to the study of ultimate properties in vitro, although not necessarily excised from the cadaver (Barfred, 1973). The changes in mechanical properties occurring immediately post morteni have been assumed by most authors to be negligible. Tendon is metabolically inert, slow to repair, slow to degenerate and as Edwards (1946) describes “virtually dead, even during life”. Unfortunately many of the earlier workers were not aware of the significance of time rate and perhaps the first recognition of the rate dependence of rupture strength was given by Stucke (1950). He also commented that the strength of fresh tendocalcaneus (human) was dependent o n the previous history of the stress and strain, including the duration of stress and
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finding of Partington, et al. (1963) that tendon specimens treated with the enzyme hyaluronidase offer little resistance to extension. It has been demonstrated that tendon has a helical microstructure. When subjected to tensile force the collagen helices will tend to unwind. Preliminary experimentation demonstrates that this phenomenon of tension/torsion coupling occurs in the initial lax phase of uniaxial response. An axial force of 10 N (approximately I kg) applied to adult human palmaris longus is accompanied by a twisting moment of 5 mNm (approximately .05 kg cm). These results indicate that the twisting action of tendon is a secondary mechanical effect.
Fig. 5 . Scanning electron micrograph of unstrained human palmaris longus tendon. In the surface produced by a microtome a fissure reveals general fibril migration. x 250.
the rate of loading. The significance of rate of loading of tendon is clearly demonstrated in fig. 7. In uniaxial tension tendon appears initially to be highly compliant but on extension there is a transition to a stiffer region of response. This transition is usually abrupt and has been termed the “toe” or sometimes the “heel”. It has been reported by many authors (Rigby, et al., 1959; Stromberg and Wiederhielm, 1969 and Viidik, 1968 and 1972) that the transition in mechanical properties corresponds with the disappearance of the wave form on the surface of tendon. The transition occurs typically at about 3 per cent extension (Viidik, 1968) and on removal of force the wave form reappears. In the initial lax phase of response little time rate dependence has been demonstrated and Rigby, et al. (1959) report that repeated load cycles in this phase of response are reproducible. However, Partington and Wood (1963) also working with “tail” tendon, observed a progressive increase in extension with load cycling. Abrahams (1967) found equine tendon to be elastic in the lax phase although the stress-strain relations for repeated load cycles were not identical. Beyond the initial lax phase tendon becomes much more resistant to elongation and in this region the mechanical characteristics display significantly greater time dependence (Rigby, et al. 1959), Abrahams (1967) and Vogt, Arnold and Lippert (1973). Under constant load, tendon extends progressively with time (creep) and when held at constant elongation it exhibits stress relaxation. Abrahams (1967) and Vogt, et al. (1973) conclude that tendon is linearly viscoelastic above the toe region. Stromberg, et al. (1969) have suggested that the ground substance is responsible for the time-dependent behaviour of tendon by providing a viscous resistance to the relative movement of fibrils. Creep tests performed on primary tendon bundles from mouse tail (highly ordered structure) demonstrate relatively little deformation, even over a period of several hundred seconds. The authors suggested that the more pronounced creep obtained in tests on whole tendon was due to rearraneement of the disordered fibre network obtaining in thgunstressed state rather than being a property 0’; the collagen itself. This hypothesis agrees with the
Ph.ysiological Loading of Tendon Clinical interpretation of the mechanical and structural properties of tendon is dependent on a knowledge of its “working range” as defined by the magnitude and duration of transmitted forces, and most important, their time rate of change. While numerous “estimates” have been made of the forces to which tendons are subject, little direct experimental evidence is available. The peak force transmitted by tendon during sensibly normal activities and its relation to measured rupture strength have been assessed by several authors (reviewed by Barfred, 1973). Similarly comparison between failure strength and the maximum isometric tetanic tension of muscle has been attempted by Walker, Harris and Benedict (1964) and Elliott (1965). Direct measurement ,oftendon force in the foreleg of the horse has been reported by Barnes and Pinder (1974). The common extensor tendon transmitted a peak force of 100 N (Thoroughbred mare, 450 kg, 1.5 m high) at walking pace and approximately twice this force at the trot. No direct comparison was made with measured rupture strength. In this thesis, Barfred (1973) concludes that tendon force magnitudes in normal if strenuous activity may approach the rupture strength as determined from post mortem material. However there are reported estimates of tendon force which greatly exceed the generally accepted value for rupture strength (Grafe, 1969) and this discrepancy has not yet been satisfactorily resolved. The errors in estimating internal body forces from kinematic data are large (Paul, 1967). Conversely tendon rupture strength determined by quasi-static testing in vitro does not constitute an accurate estimate of the ultimate properties of tendon in the rapidly moving body. In ascertaining the possible significance of tendon’s dynamic characteristics it is necessary to consider both the rate of loading and the magnitude range of force. For instance, it is imperative to know whether tendon behaves as a linear material or if the lax phase of response is functionally significant. Paradoxically, while several direct and indirect assessments during normal function of maximum force exist, little attention has been given to minimum forces. It cannot reasonably be assumed that this force tends to zero. Although graphical presentation of tendon force (Morrison, 1967; Barnes, et al., 1974) might suggest such a tendency, the techniques employed and the calculated error margins do not iustifv this conclusion. Ekott (1965j suggests that the normal range of tension transmitted in vivo might fall within the lax
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phase of response. This is highly improbable as the “toe” region corresponds to a tension of less than 10 per cent of the tissue’s rupture strength (Elliott, 1965). There is tenuous evidence to suggest that tendon may function in the nearly linear, stiffer region of response such that it does not normally experience forces less than those corresponding to the transition. Schatzker and Branemark (1968) whilst studying tendon blood supply in anaesthetised rabbits commented that surface waves appeared when tendon was transected. Despite the foregoing it is possible that the functional response of tendon is highly non-linear with the transition region embraced within the “working range” (Viidik, 1972; Gathercole and Keller, 1974). The time rate of loading of tendon can be derived from the foregoing data and as such it is subject to the same magnitude of error. In normal locomotion tendon force varies cyclicly with a frequency equal to or greater than the cadence. Indirect (Morrison, 1967) and direct (Barnes, et al., 1974) estimates of force show there to be peaks corresponding to limb acceleration and weight bearing. Although the mean rate of loading corresponding to these peaks is relatively low Barnes, et al. (1974) show that high frequency components of force exist which result in a
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loading rate of 800 Ns-’, even in level walking. These rates more than double at the trot. The Etiology of Tendon Rupture Clinically observed tendon lesions are sometimes caused by cutting and crushing action to the tendon body but there is also the not uncommon occurrence of pure tensile, subcutaneous rupture. In man the most prevalent etiologies are a sudden, voluntary action (45 per cent), an unexpected passive loading (15 per cent) and voluntary muscle action accompanied by a passive loading (6 per cent) (Barfred, 1973). Stromberg and Tufvesson ( 1969) conclude that avascular necrosis or other degenerative changes in the tendon may predispose to mechanical failure but Barfred (1973) maintains that these are not essential factors. Of the many other body factors that have been linked with subcutaneous tendon rupture three in particular have many adherents. They are previously inactive or exhausted musculature and abnormal angulation at the insertion. While it is agreed that training increases the work capacity of muscles and strengthens the associated tendons (Barfred, 1973; Viidik, 1968) there is debate as to the effect on tendon of “warming up” prior to some
strain rate
0.001 s-1
80
0
i t-
0
0.02
0-04
0-06
0-08
0 -1
strain
Fig. 6. Stress-strain characteristic of human palmaris longus tendon in tension. An initially lax response precedes a relatively s:iff, nearly linear region. Rupture usually occurs after yield and apparent plastic J ~ w. O This stress-strain characteristic is usually described as signioidal. (Strain is the incremental extension relative to the original length).
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concerted effort. The rate of muscle metabolism is enhanced and its temperature rises. Temperature rises also occur in tendon (Asmussen, 1968). These are unlikely to have a similar route as the tissue is almost metabolically inert. Heating is possibly due to hysteretic energy transfer as tendon is imperfectly elastic. Tendon becomes more compliant with increasing temperature but its rupture strength falls marginally (Asmussen, 1968). However in common with other soft connective tissues, rapidly repeated loading tends to stabilise the mechanical response of tendon. In the stabilised condition thus attained the tissue is more nearly elastic (Abrahams, 1967) and slightly stiffer. This connective tissue phenomenon sometimes referred to as preconditioning is sensibly reversible in vivo (Stark, 1971). At the other end of the scale overactivity will produce muscle exhaustion and perhaps uncoordinated muscle activity. Lindhard ( 1931) demonstrated that muscle stiffens as it becomes exhausted and thus the associated tendon is mechanically vulnerable. The combination of fully contracted exhausted muscle may pave the way to tendon damage as the possibility exists of large extensions and relatively stiff muscle response (Barfred, 1973). Abnormal changes in angulation at the tendon insertion
may result in an uneven local stress distribution which could precipitate failure. Such changes in angulation are likely to be accompanied by sudden and unexpected passive loading. Barfred (1973) proposes that training on rough surfaces may have a prophylactic effect. An interesting observation is that 53 per cent of human Achilles tendon ruptures occur some 3-4 cm from the calcaneus (Schonbauer, 1960). As this corresponds closely to the region where the components of the Achilles tendon twist, support is given to the hypothesis that local tendon damage may result from the rubbing of one tendon upon another. The most important external factor associated with subcutaneous tendon rupture is that of unexpected and rapid loading. Its effect may often be combined with that of abnormal angulation. The body responds both actively and passively to rapid loading of a limb extremity. Barfred (1973) proposes that the active response of muscle may be determined by short reflex arcs which block the normal proprioceptive pathways. Under rapid loading conditions tendon rupture strength increases marginally (Chvapil, Hruza and Roth, Z . , 1962) but more significantly it becomes stiffer (fig. 6). The combined effects of the response of the musculature and tendon to rapid loading, that is a relatively brittle tendon attached to a rapidly contracting muscle, may
30
2
z 20
cn cn
a L CI
v)
10
0 0
0.02
0.04
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strain Fig. 7. Strain-rate dependence of the stress-strain relation of tendon in tension. Higher strain-rates are rejected by apparently stiffer mechanical characteristics. Graph 3 corresponds to extremely slo w rates of extension, whereas graph 1 corresponds to the slower extension rates experienced in vivo.
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ment simple bien que I’arrangement helicoidal particulier de ses fibres collagenes lui confkre des proprittks mecaniques particulitres. Secondary Functions of Tendon Le comportement fonctionnel du tendon et sa rkponse Several functions have been attributed to tendon in addition to its major role as a force transmitter. These aux differents types de sollicitations mecaniques, sont hypothetical functions hinge on tendon’s ability to ma1 connus. Notamment le taux de deformation et la store energy elastically. Whilst not perfectly elastic, force minimal supportte durant la locomotion normale mechanically stabilised and relatively highly stressed attendent encore d’Ctre definis. La plupart des valeurs publites concernant les forces tendon will give up a large proportion of its stored maximales transmises par les tendons ne coincident pas energy. The ability of tendon to store energy is related to the avec les forces mesurtes, de facon statique suffisantes average force of extension and the amount by which it pour en provoquer la rupture. Certaines estimations extends. In man the tendons of the leg are short. sont supirieures aux forces de rupture et montrent The total energy stored in human Achilles tendon is quelles erreurs peuvent Ctre introduites par une mesure decidedly less than 10 per cent of the energy involved in i ndirecte. Les methodes de merwre directe, dont il est maintenant performing one step. Dawson, et a/. (1973) deduced from treadmill experiments that the Achilles tendon of etabli qu’elles peuvent &trepratiquees devraient produire the red kangaroo acts as an energy store effectively des informations plus prkcises. Evidemment les autres fonctions mecaniques que l’on reducing the energetic cost of high speed locomotion. However this tendon in the red kangaroo (40 kg) measures attribue aux tendons sont probalement d’une importance some 35 cm in length. secondaire. On doit encore connaitre plus du comThe suspensory ligament in the horse with its ana- portement du muscle pour verifier ces hypothbes. tomical uniqueness may also serve as an elastic energy Compte tenu de nos connaissances Ctriquees quant au store (Hildebrand, 1960). fonctionnement tendineux normal il semble heureux que The ability to attenuate the forces produced by rapid les techniques de traitement et de reparation soient en and unexpected movement (Smith, 1954; Barnett, et a f . , rapide progression. 1961) is also dependent on tendon’s extensibility. Thus, although in the Achilles tendon of man this ZUSAMM ENFASSUNG function is doubtful (except in the case of contracted Sehnengewebe erfullt seine primare Aufgabe als and exhausted muscle) it may have relevance to the Kraftiibertrager sehr wirkungsvoll. Das Versagen dieses horse and other animals. passiven Gewebes fiihrt zu ausgepragten Storungen. Als ein Bindegewebe ist seine Struktur verhaltnismassig einSUMMARY fach und die eigenartige, schneckenartig gewundene Tendon normally fulfils its primary role as a flexible Anordnung der kollagenen Fasern erzeugt ausgepragte, force transmitting element very effectively and yet nicht-lineare und auch zeitabhangige mechanische Eigenfailure of this passive tissue leads to great disability. schaften. Die funktionelle Signifikanz irgendeiner mechAs a connective tissue its structure is relatively simple anischen Antwort kann nicht beantwortet werden, bevor and the peculiar helical arrangement of collagen fibres das physiologische Belastungsmuster bekannt ist. Vor confers highly non-linear as well as time-dependent allem mussen vorerst noch die Deformationsrate und die mechanical properties. Functional significance cannot minimale Kraft, die auf Sehnen bei der normalen Fortbe attributed to any facet of mechanical response until bewegung einwirkt, abgeklart werden. the physiological pattern of loading is established. Die meisten veroffentlichten Werte von MaximalIn particular the rate of deformation and the minimum kraften, die von Sehnengewebe iibertragen werden force experienced by tendon in normal locomotion have konnen, sind kleiner als die gemessene, praktisch yet to be elicited. statische Reissfestigkeit. Die Tatsache, dass gewisse Most published values of maximum forces transmitted Schatzungen diese Endgrosse iibertreffen, illustriert die by tendon fall short of the measured quasi-static rupture Fehlermoglichkeiten aller indirekten Schatzungen. Distrength. The fact that some estimates exceed this rekte und praktikable Messverfahren werden wohl ultimate force illustrates the errors incurred in indirect wertvolle Informationen liefern, wenn sie an Sehnen assessment. Direct measurement techniques, which angewendet werden, die spontan reissen konnen. have now been demonstrated to be practicable, should Die anderen mechanischen Funktionen von Sehnen yield valuable information when applied to tendons sind nur von sekundarer Bedeutung. Wir haben noch susceptible to spontaneous rupture. vie1 zu lernen, was die Muskelreaktion auf schnelle Other proposed mechanical functions of tendon are Belastung und Streckung anbetrifft, bevor entsprechende clearly of secondary importance. Much has yet to Hypothesen iiberpriift werden konnen. be learned of the response of muscle to rapid loading Bei unseren geringen Kenntnissen der normalen and extension before these hypotheses can be tested Sehnenfunktion konnen wir uns gliicklich schatzen, dass fully. die Behandlungsmethoden geschadigter Sehnen rasche With our scant knowledge of normal tendon function Fortschritte machen. it is indeed fortunate that the techniques of repair and treatment of damaged tendon are rapidly advancing. REFERENCES predispose to rupture.
RESUME Le role primordial du tendon est de transmettre une force variable; en consequence une defaillance de ce tissu “passif” entraine une certaine impotence. En tant que tissu conjonctif la structure du tendon est relative-
Abraham, M. (1967). Mechanical behaviour of tendon in vitro. Med. and biol. Engng. 5, 433. Asmussen, E. (1968). The neuromuscular system and exercise. In Exercise Physiology, H. B. Falls, London. Barbenel, J. C., Evans, J. H. and Gibson, T. (1971). Quantitative relationships between structure and mechanical properties of tendon. Digest 9th I.C.M.B.E., Melbourne, 150.
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Barfred, T. (1973). Achilles tendon rupture. Acta. orthop. scand. Siippl. 152. Barnes, G. R. G. and Pinder, D. N. (1974). In vivo tendon tension and bone strain measurement and correlation. J. Biornech. 7 ( I ) , 35. Barnett, F. H., Davies, D. V. and McConaill, M. A. (1961). Synovial joints: their structure and mechanics. London, Longmans. Chvapil, M., Hruza, Z. and Roth, Z. (1962). Physical and physical-chemical heterogeneity of collagen fibres from rat tail tendon. Gerontologia 6, 102. Cronkite, A. E. (1936). The tensile strength of human tendons. Anat. Rec. 64, 173. Cruise, A. J. (1958). The structural periodicity of microscopic collagen fibres. I n : Recent advances in gelatin and glue research, ed. G. Stainsby, p. 45, London, Pergamon. Dale, W. C., Baer, E., Keller, A. and Kohn, R. R. (1972). On the ultrastructure of mammalian tendon. Sep. Experientia 28, 1293. Dawson, T. J . and Taylor, C. R. (1973). Energetic cost of locomotion in kangaroos. Nature 246, Nov. 30, 3 13. Diamant, J., Keller, A., Baer, E., Litt, M. and Arridge, R. G. C. ( 1972). Collagen; ultrastructure and its relation to mechanical properties as a function of ageing. Proc. Roy. SOC., London B 180, 293. Edwards, D. A. W. (1946). The blood supply and lymphatic drainage of tendons. J . Anat. 80, 147. Elliott, D. H. (1965). Structure and function of mammalian tendon. B i d . Rev. 40, 392. Finlay, J. B., Hunter, J. A. A. and Steven, F. S. (1971). Preparation of human skin for high resolution scanning electron microscopy using phosphate buffered crude bacterial a amylase. J. Microscopy 93 (3), 241. Gathercole, L. J. and Keller, A. (1974). Supermolecular structural hierarchies in collagenous fibres. In: Structure of fibrous biopolymers, Butterworth (in press). Grafe, H. (1969). Aspekte zur Aetiologie der subcutanen Achillessehnenruptur. Zbl. Chir. 94, 1073. Gratz, C. M. and Blackberg, S. N. (1935). Engineering methods in medical research. Mech. Engng. 57, 217. Hildebrand, M. (1960). The suspensory ligament as an energy store. Sci. Am. 202, 148. Hill, A. V. (1951). The mechanics of voluntary muscle. Lancet 261, 947. Kunhke, E. (1962). The fine structure of collagen fibrils as the basis for functioning of tendon tissue. In Collagen, ed. N. Ramanthan, p. 479. New York, Interscience. Lerch, H. (1950). Uber den Aufbau des Sehnengewebes. Gegenbaiirs morph. Jb. 90, 192. Lindhard, J. (1931). Der Skeletmuskel und seine Funktion. Erg. Physiol. Berlin 33, 337. Morrison, J. B. (1967). The forces transmitted by the human knee ioint during- activity. Ph.D. thesis, University of Strat h d yde.
EQUINE VETERl NA RY JOURNAL Partington, F. R. and Wood, G. C . (1963). The role of noncollagen components in the mechanical behaviour of tendon fibres. Biochim. Biophys. Acra 69, 485. Paul, J. P. (1967). Forces transmitted by joints i n the human body. Proc. Symposium “Lubrication and wear in living and artificial human joints”. Proc. Inst. Mech. Eng. V181, 33, 8. Rigby, B. J., Hirai, N., Spikes, J. D. and Eyring, H. (1959). The mechanical properties of rat tail tendon. J . Ran. Physiol. 43, 265. Rollhauser, H . (1950). Konstruktions-und Altersunterschiede in Festigkeit Kollagener Fibrillen. Gegenbaurs morph Jb. 90, 157. Rooney, J. R. (1969). Biomechanics of lameness in horses. Williams and Wikins, Baltimore. Schatzker, J. and Branemark, P.-I. (1968) lntravital observations on the microvascular anatomy and microcirculation of the tendon. Acta. orthop. scand. Siippl. 126. Schonbauer, H. R. ( 1960). Subcutane Achillessehnenrisse. Chir. Prax. Wien. 4, 77. Smith, J. W. (1954). The elastic properties of the anterior cruciate ligament of the rabbit. J . Anaf. 88, 369. Stark, H. L. (1971). The surgical limits of extension and compression of the human skin. Ph.D. thesis, University of Strathclyde. Stromberg, B. and Tufvesson, G . (1969). Lesions of the superficial flexor tendon in racehorses. Clin. Orthop. 62, 113. Stucke, K. (1950). Uber das elastische Verhalten der Achillessehne im Belastingsversuch. Arch. Klin. Chir. 265, 579. Stromberg, D. D. and Wiederhielm, C. A. (1969). Viscoelastic description of collagenous tissue in simple elongation. J. appl. Physiol. 26 No. 6, 857. Valentine, G . G., Otz, Henzi (1844). Quoted by M. G. Wertheim (1847). Annls. Chin!. Phys. 21, 385. Verzar, F. (1957). The ageing of connective tissue. Gerontologia (Basel) 1, 363. Verzar, F. and Huber, K. (1958). Die Struktur der Sehnenfaser. Acta Anat. 33, 215. Viidik, A. (1968). Function and structure of collagenous tissues. Thesis, Gothenburg. Viidik, A. (1972). Simultaneous mechanical and light microscopic studies of collagen fibres. Z. Anat. EntwCesch. 136, 204. Vogt, C-H., Arnold, G. and Lippert, H. (1973). Relaxationseigenschaften menschlicher Sehnen. Eiirop. J. Appl. Physiol. 32, 87. Walker, L. B., Harris, E. H. and Benedict, J. V. (1964). Stressstrain relationships in human cadaveric plantaris tendon; a preliminary study. Med. Electron. and b i d . Engng. 2, 31. Wertheim. M. G . (1847). Mtmoir sur I’tlasticite et la cohesion des principaux tissues du corps humain. Annls Chin?. Phys. 21, 385.
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Structural and Mechanical Properties of Tendon related to Function J. H. EVANS J. C. BARBENEL Bioengineering Unit, University of Strathclvde, Glasgow
ONE of the commonest and most disastrous lesions of the horse is tearing or strain of the suspensory ligament or flexor tendon (Rooney, 1969) yet surprisingly little research has been conducted into tendon function and dysfunction. In mechanical terms, tendon serves principally as a force transmitter. This passive role has long been recognised, but in recent years other mechanical functions have been attributed to tendon. These include that of a dynamic amplifier during rapid muscle contraction (Hill, 1951), an elastic energy store (Dawson and Taylor, 1973) and more commonly that of a force attenuator during rapid and unexpected movement (Smith, 1954; Barnett, Davies and McConaill, 1961). The tensile mechanical characteristics of tendon are extensively documented although the data presented are by no means comprehensive. In general, the investigators have either used tendon as a relatively simple, collagen-rich tissue for basic studies or they have been principally concerned with the rupture characteristics of tendon in vitro. Relatively little is known of the physiological significance of the load/deformation characteristics of tendons. It is often assumed that they provide a relatively stiff elastic link between bone and muscle and yet it has been clearly demonstrated that tendons exhibit time-dependent and probably, irreversible characteristics. In the literature there occur rather vague references to fatiguing which are possibly explicable in terms of the viscoelastic characteristics of this tissue. The following paper explores the relation between structure, function and rupture of tendons in general and discusses those characteristics which are probably of clinical significance. Reference is made to human and other animal tendons which have received considerably more attention than their equine counterparts. This is considered admissible as there is a basic similarity in the structure and function of most tendons. Presented at the annual congress of the British Equine Veterinary Association, Edinburgh, 1972.
STRUCTURE Tendon comprises mainly collagen in the form of submicroscopic fibrils, arranged in what is essentially a unidirectional structure. The aggregations of collagen fibrils within tendon are very variable, but it is reasonable to consider the principal unit of tendon structure to be the coherent bundle of collagenous fibrils lying between the tendon cells. These fibres or “primary tendon bundles” as they are sometimes named (Elliott, 1965) can range in diameter up to 300 pm. The arrangement of tendon fibres into larger units is more easily studied than the arrangement at the fibrillar level, but is also more variable. Fibres are grouped into bundles or fasciculi but the dimensions and arrangement of these bundles vary considerably from tendon to tendon. Most tendons exhibit considerable lateral adhesion between the bundles, yet some can be unfolded into a ribbon. In contrast the relative independence of the fibre bundles in tail tendons is most striking. Fresh tendon appears like “watered silk” and it is just possible to see with the unaided eye alternate dark and light transverse bands which are approximately 70 pm wide. These bands disappear when tension is applied to tendon, but reappear on relaxation (Viidik, 1972). However Rigby, Hirai, Spikes and Eyring (1959) reported that this structural change is irreversible above 4 per cent strain. The surface waveform has been investigated by several workers with conflicting results. On theoretical considerations, Lerch (1950) concluded that the apparent wave is due to a three-dimensional twisting of collagen fibrils within the primary tendon bundle. This hypothesis is supported by Verzar (1957) and Cruise (1958), but opposed by Rigby, et al. (1959) and Kiihnke (1962). It seems that the disagreement stems in part from the fact that not all tendons have identical structure. There is evidence to suggest that the majority of mammalian tendons are structurally very similar with the principal exception of tail tendon. Recent studies by Diamant, Keller, Baer, Litt and Arridge (1972) suggest that the
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Fig. 1.
Scanning electron micrograph of replica (Silcoset
105, ICI) o f an unstrainedfibre bundle from rat tail tendon. Regular crimping produces what is essentially a planar zig-zag. x 500.
fibrillar structure of tail tendon is sensibly two dimensional in that the fibrils describe a planar wave. This conclusion was reached by Diamant, et a/. (1972) using almost precisely the same polarising microscopical technique that had enabled Verzdr and Huber (1958) to conclude that tail tendon had a regular helical structure. Single micrographs presented by both authors appear identical. However Diamant and colleagues improved on the basic technique by rotating the tendon specimens about their long axis under the microscope. This technique satisfactorily differentiated between two- and three-dimensional structures and decided in favour of a planar, zig-zag fibrillar arrangement and against the helical array previously suggested. Recent studies by the authors using scanning electron microscopy would suggest that the conclusions drawn by Diamant, et a/. (1972) are basically correct. Using both unfixed rat tail tendon and silicon elastomer (Silcoset 105, IC1) replicas of fresh, unstrained tendon, the course of the collagen fibrils is readily observable. The structure is clearly seen in the electron micrograph (fig. I ) of rat tail tendon. Viewed normal to the principal plane of fibrillar array, the structure does indeed appear as a saw-tooth with abrupt reorientation of the fibrils at the peaks of the wave form. The scanning electron micrograph reveals, however, that the structure is not truly planar and the structure resembles a helical array which has been partially collapsed into two dimensions (see fig. 1). Discounting the literature relating to tail tendon, the concensus of opinion is that the collagen in mammalian tendon is arrayed in a sensibly parallel manner, but that it follows a helical course along the length of the tendon. Dale, Baer, Keller and Kohn (1972) claim that the planar wave form is common to all tendons. The surface wave which has been observed and reported by many authors (Elliott, 1965 and Viidik, 1968 and 1972) is not an indication that the fibrils adopt a planar wave form. Scanning electron micrographs of free tendon surfaces which have been enzymatically cleaned by using a amylase in the manner proposed by Finlay, Hunter and Steven, 1971 or hyaluronidase can reveal details of the packing of fibrils in the surface layer. Although it is possible, using limited enzymatic
digestion, to reveal the fibrils whilst leaving them adherent to one another, the most striking evidence of fibrillar packing is obtained by extending such enzymolysis to the point where individual fibrils or fibrillar groups become separated. Figs. 2 and 3 are micrographs of human tendons which have been treated with hyaluronidase to the point where their surfaces are partially disrupted. The impression of helical coiling of the fibres is clear and the arrangement whereby they are packed to produce a planar surface wave is readily deduced. Stereographic analysis has confirmed the existence of a helical structure (Barbenel, Evans and Gibson, 1971) but the dimensions of the helices (fig. 2) are clearly abnormal as the fibrillar bundles released from the parent tendon have contracted and otherwise distorted. Internal surfaces produced both by fracture along natural cleavage planes or by the microtome reveal considerable structural detail. The fibrillar packing observed on a surface produced by fracture is principally that of a parallel helical array (fig. 4) where all fibrils have similar form and aggregate in a close packed but sensibly non-intertwining arrangement. I t is interesting to note that this structure is identical to the “plasticine” model which Lerch (1950) constructed based on his light microscope studies. Lerch (1950) also demonstrated that fibrils cannot lie entirely in parallel array since fissures produced in a thin tissue section reveal fibrils crossing in both directions. The scanning electron micrograph (fig. 5) shows the same phenomenon in a surface produced by the microtome blade. The predominance of fibrils crossing in the onedirection indicates
Fig. 2. Scanninkr electron micrograph of unsrrained human palmaris longus tendon treated with hyaluronidase. Surface waveform evident with adjacent coiling fibres released b.v enzymolisis. x 225.
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that the fissure had not necessarily formed parallel to the mean fibrillar direction. The true migration of fibrils across the fissure is seen to be small and would suggest that interweaving of fibrils in the parent tendon is a secondary effect. At this level the rope-like structure sometimes attributed to tendon (Elliott, 1965) cannot be substantiated, although the observed fibrillar migration within the primary tendon bundles probably affords considerable lateral cohesion. However binding between fibre may not be attributable to fibrillar migration as the surfaces of fibre bundles revealed by longitudinal fracture (fig. 4) show no evidence of ruptured or loose surface fibrils. MECHANICAL PROPERTIES The mechanical characteristics of the tendon have been established almost exclusively by uniaxial tensile tests where the direction of loading coincides with the long axis of the tendon. The load/deformation characteristics of tendon in uniaxial tension are non-linear. Wertheim (I 847) described the relation as “a hyperbola whose apex is at the origin of the co-ordinates stress and strain”. The stress-strain behaviour is more commonly reported as comprising an initial lax response with progressive stiffening leading to a quasi-linear relationship. However, at higher stresses the tissue “yields” and the entire stress-strain relation to failure is best described as sigmoidal (fig. 6). The basic form of the quasi-static stress-strain relation for tendon was established some forty years ago (Gratz and Blackberg, 1935). In the intervening
Fig. 3 . Scanning electron micrograph of unstrained human palmaris longus tendon treated with hyaluronidase. Parallel, coiling fibres completely separated by enzymolisis. x 225.
Fig. 4. Scanning electron micrograph of unstrained human palmaris longus tendon treated with hyaluronidase. Fibrillar components of fibre aggregated in sensibly parallel array over an entire wavelength. x 650.
period this form has been reiterated in many papers in which data have been derived from a range of mammalian tendons and the rather specialised “tail” tendons, principally from the rat. Unfortunately much of these data relate to ultimate properties with the concomitant large experimental error and in general there has been little regard for the time-dependent characteristics of this tissue. The majority of investigators fit into two camps-those mainly concerned with characteristics of functional significance and those who have chosen the tendon for more basic investigations because of its relatively simple structure. Resulting from research in this latter group the literature abounds with mechanical data on denatured and chemically modified tendon. These data have little significance in functional terms. There appears to be no published data on the flexibility of tendon nor on its transverse or torsional characteristics. The ultimate tensile strength of tendon was first reported in 1844 by Valentin, Otz and Henzi. Ever since this early work the emphasis has been on stress at rupture and relatively little data have been published on the associated deformation. This corpus of work has been very fully reviewed by Cronkite ( I 936), Stucke( I950), Rollhauser (1950) and more recently by Elliott (1965). There is a suggestion from this data pool that the tensile strength of fresh tendon is in the range 5-10 kg/mm2 (50-100 MPa). Paradoxically, although clinically observed tendon ruptures are not uncommon, there are no published data on experimentally produced lesions in vivo. The literature relates almost exclusively to the study of ultimate properties in vitro, although not necessarily excised from the cadaver (Barfred, 1973). The changes in mechanical properties occurring immediately post morteni have been assumed by most authors to be negligible. Tendon is metabolically inert, slow to repair, slow to degenerate and as Edwards (1946) describes “virtually dead, even during life”. Unfortunately many of the earlier workers were not aware of the significance of time rate and perhaps the first recognition of the rate dependence of rupture strength was given by Stucke (1950). He also commented that the strength of fresh tendocalcaneus (human) was dependent o n the previous history of the stress and strain, including the duration of stress and
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finding of Partington, et al. (1963) that tendon specimens treated with the enzyme hyaluronidase offer little resistance to extension. It has been demonstrated that tendon has a helical microstructure. When subjected to tensile force the collagen helices will tend to unwind. Preliminary experimentation demonstrates that this phenomenon of tension/torsion coupling occurs in the initial lax phase of uniaxial response. An axial force of 10 N (approximately I kg) applied to adult human palmaris longus is accompanied by a twisting moment of 5 mNm (approximately .05 kg cm). These results indicate that the twisting action of tendon is a secondary mechanical effect.
Fig. 5 . Scanning electron micrograph of unstrained human palmaris longus tendon. In the surface produced by a microtome a fissure reveals general fibril migration. x 250.
the rate of loading. The significance of rate of loading of tendon is clearly demonstrated in fig. 7. In uniaxial tension tendon appears initially to be highly compliant but on extension there is a transition to a stiffer region of response. This transition is usually abrupt and has been termed the “toe” or sometimes the “heel”. It has been reported by many authors (Rigby, et al., 1959; Stromberg and Wiederhielm, 1969 and Viidik, 1968 and 1972) that the transition in mechanical properties corresponds with the disappearance of the wave form on the surface of tendon. The transition occurs typically at about 3 per cent extension (Viidik, 1968) and on removal of force the wave form reappears. In the initial lax phase of response little time rate dependence has been demonstrated and Rigby, et al. (1959) report that repeated load cycles in this phase of response are reproducible. However, Partington and Wood (1963) also working with “tail” tendon, observed a progressive increase in extension with load cycling. Abrahams (1967) found equine tendon to be elastic in the lax phase although the stress-strain relations for repeated load cycles were not identical. Beyond the initial lax phase tendon becomes much more resistant to elongation and in this region the mechanical characteristics display significantly greater time dependence (Rigby, et al. 1959), Abrahams (1967) and Vogt, Arnold and Lippert (1973). Under constant load, tendon extends progressively with time (creep) and when held at constant elongation it exhibits stress relaxation. Abrahams (1967) and Vogt, et al. (1973) conclude that tendon is linearly viscoelastic above the toe region. Stromberg, et al. (1969) have suggested that the ground substance is responsible for the time-dependent behaviour of tendon by providing a viscous resistance to the relative movement of fibrils. Creep tests performed on primary tendon bundles from mouse tail (highly ordered structure) demonstrate relatively little deformation, even over a period of several hundred seconds. The authors suggested that the more pronounced creep obtained in tests on whole tendon was due to rearraneement of the disordered fibre network obtaining in thgunstressed state rather than being a property 0’; the collagen itself. This hypothesis agrees with the
Ph.ysiological Loading of Tendon Clinical interpretation of the mechanical and structural properties of tendon is dependent on a knowledge of its “working range” as defined by the magnitude and duration of transmitted forces, and most important, their time rate of change. While numerous “estimates” have been made of the forces to which tendons are subject, little direct experimental evidence is available. The peak force transmitted by tendon during sensibly normal activities and its relation to measured rupture strength have been assessed by several authors (reviewed by Barfred, 1973). Similarly comparison between failure strength and the maximum isometric tetanic tension of muscle has been attempted by Walker, Harris and Benedict (1964) and Elliott (1965). Direct measurement ,oftendon force in the foreleg of the horse has been reported by Barnes and Pinder (1974). The common extensor tendon transmitted a peak force of 100 N (Thoroughbred mare, 450 kg, 1.5 m high) at walking pace and approximately twice this force at the trot. No direct comparison was made with measured rupture strength. In this thesis, Barfred (1973) concludes that tendon force magnitudes in normal if strenuous activity may approach the rupture strength as determined from post mortem material. However there are reported estimates of tendon force which greatly exceed the generally accepted value for rupture strength (Grafe, 1969) and this discrepancy has not yet been satisfactorily resolved. The errors in estimating internal body forces from kinematic data are large (Paul, 1967). Conversely tendon rupture strength determined by quasi-static testing in vitro does not constitute an accurate estimate of the ultimate properties of tendon in the rapidly moving body. In ascertaining the possible significance of tendon’s dynamic characteristics it is necessary to consider both the rate of loading and the magnitude range of force. For instance, it is imperative to know whether tendon behaves as a linear material or if the lax phase of response is functionally significant. Paradoxically, while several direct and indirect assessments during normal function of maximum force exist, little attention has been given to minimum forces. It cannot reasonably be assumed that this force tends to zero. Although graphical presentation of tendon force (Morrison, 1967; Barnes, et al., 1974) might suggest such a tendency, the techniques employed and the calculated error margins do not iustifv this conclusion. Ekott (1965j suggests that the normal range of tension transmitted in vivo might fall within the lax
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phase of response. This is highly improbable as the “toe” region corresponds to a tension of less than 10 per cent of the tissue’s rupture strength (Elliott, 1965). There is tenuous evidence to suggest that tendon may function in the nearly linear, stiffer region of response such that it does not normally experience forces less than those corresponding to the transition. Schatzker and Branemark (1968) whilst studying tendon blood supply in anaesthetised rabbits commented that surface waves appeared when tendon was transected. Despite the foregoing it is possible that the functional response of tendon is highly non-linear with the transition region embraced within the “working range” (Viidik, 1972; Gathercole and Keller, 1974). The time rate of loading of tendon can be derived from the foregoing data and as such it is subject to the same magnitude of error. In normal locomotion tendon force varies cyclicly with a frequency equal to or greater than the cadence. Indirect (Morrison, 1967) and direct (Barnes, et al., 1974) estimates of force show there to be peaks corresponding to limb acceleration and weight bearing. Although the mean rate of loading corresponding to these peaks is relatively low Barnes, et al. (1974) show that high frequency components of force exist which result in a
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loading rate of 800 Ns-’, even in level walking. These rates more than double at the trot. The Etiology of Tendon Rupture Clinically observed tendon lesions are sometimes caused by cutting and crushing action to the tendon body but there is also the not uncommon occurrence of pure tensile, subcutaneous rupture. In man the most prevalent etiologies are a sudden, voluntary action (45 per cent), an unexpected passive loading (15 per cent) and voluntary muscle action accompanied by a passive loading (6 per cent) (Barfred, 1973). Stromberg and Tufvesson ( 1969) conclude that avascular necrosis or other degenerative changes in the tendon may predispose to mechanical failure but Barfred (1973) maintains that these are not essential factors. Of the many other body factors that have been linked with subcutaneous tendon rupture three in particular have many adherents. They are previously inactive or exhausted musculature and abnormal angulation at the insertion. While it is agreed that training increases the work capacity of muscles and strengthens the associated tendons (Barfred, 1973; Viidik, 1968) there is debate as to the effect on tendon of “warming up” prior to some
strain rate
0.001 s-1
80
0
i t-
0
0.02
0-04
0-06
0-08
0 -1
strain
Fig. 6. Stress-strain characteristic of human palmaris longus tendon in tension. An initially lax response precedes a relatively s:iff, nearly linear region. Rupture usually occurs after yield and apparent plastic J ~ w. O This stress-strain characteristic is usually described as signioidal. (Strain is the incremental extension relative to the original length).
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concerted effort. The rate of muscle metabolism is enhanced and its temperature rises. Temperature rises also occur in tendon (Asmussen, 1968). These are unlikely to have a similar route as the tissue is almost metabolically inert. Heating is possibly due to hysteretic energy transfer as tendon is imperfectly elastic. Tendon becomes more compliant with increasing temperature but its rupture strength falls marginally (Asmussen, 1968). However in common with other soft connective tissues, rapidly repeated loading tends to stabilise the mechanical response of tendon. In the stabilised condition thus attained the tissue is more nearly elastic (Abrahams, 1967) and slightly stiffer. This connective tissue phenomenon sometimes referred to as preconditioning is sensibly reversible in vivo (Stark, 1971). At the other end of the scale overactivity will produce muscle exhaustion and perhaps uncoordinated muscle activity. Lindhard ( 1931) demonstrated that muscle stiffens as it becomes exhausted and thus the associated tendon is mechanically vulnerable. The combination of fully contracted exhausted muscle may pave the way to tendon damage as the possibility exists of large extensions and relatively stiff muscle response (Barfred, 1973). Abnormal changes in angulation at the tendon insertion
may result in an uneven local stress distribution which could precipitate failure. Such changes in angulation are likely to be accompanied by sudden and unexpected passive loading. Barfred (1973) proposes that training on rough surfaces may have a prophylactic effect. An interesting observation is that 53 per cent of human Achilles tendon ruptures occur some 3-4 cm from the calcaneus (Schonbauer, 1960). As this corresponds closely to the region where the components of the Achilles tendon twist, support is given to the hypothesis that local tendon damage may result from the rubbing of one tendon upon another. The most important external factor associated with subcutaneous tendon rupture is that of unexpected and rapid loading. Its effect may often be combined with that of abnormal angulation. The body responds both actively and passively to rapid loading of a limb extremity. Barfred (1973) proposes that the active response of muscle may be determined by short reflex arcs which block the normal proprioceptive pathways. Under rapid loading conditions tendon rupture strength increases marginally (Chvapil, Hruza and Roth, Z . , 1962) but more significantly it becomes stiffer (fig. 6). The combined effects of the response of the musculature and tendon to rapid loading, that is a relatively brittle tendon attached to a rapidly contracting muscle, may
30
2
z 20
cn cn
a L CI
v)
10
0 0
0.02
0.04
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strain Fig. 7. Strain-rate dependence of the stress-strain relation of tendon in tension. Higher strain-rates are rejected by apparently stiffer mechanical characteristics. Graph 3 corresponds to extremely slo w rates of extension, whereas graph 1 corresponds to the slower extension rates experienced in vivo.
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ment simple bien que I’arrangement helicoidal particulier de ses fibres collagenes lui confkre des proprittks mecaniques particulitres. Secondary Functions of Tendon Le comportement fonctionnel du tendon et sa rkponse Several functions have been attributed to tendon in addition to its major role as a force transmitter. These aux differents types de sollicitations mecaniques, sont hypothetical functions hinge on tendon’s ability to ma1 connus. Notamment le taux de deformation et la store energy elastically. Whilst not perfectly elastic, force minimal supportte durant la locomotion normale mechanically stabilised and relatively highly stressed attendent encore d’Ctre definis. La plupart des valeurs publites concernant les forces tendon will give up a large proportion of its stored maximales transmises par les tendons ne coincident pas energy. The ability of tendon to store energy is related to the avec les forces mesurtes, de facon statique suffisantes average force of extension and the amount by which it pour en provoquer la rupture. Certaines estimations extends. In man the tendons of the leg are short. sont supirieures aux forces de rupture et montrent The total energy stored in human Achilles tendon is quelles erreurs peuvent Ctre introduites par une mesure decidedly less than 10 per cent of the energy involved in i ndirecte. Les methodes de merwre directe, dont il est maintenant performing one step. Dawson, et a/. (1973) deduced from treadmill experiments that the Achilles tendon of etabli qu’elles peuvent &trepratiquees devraient produire the red kangaroo acts as an energy store effectively des informations plus prkcises. Evidemment les autres fonctions mecaniques que l’on reducing the energetic cost of high speed locomotion. However this tendon in the red kangaroo (40 kg) measures attribue aux tendons sont probalement d’une importance some 35 cm in length. secondaire. On doit encore connaitre plus du comThe suspensory ligament in the horse with its ana- portement du muscle pour verifier ces hypothbes. tomical uniqueness may also serve as an elastic energy Compte tenu de nos connaissances Ctriquees quant au store (Hildebrand, 1960). fonctionnement tendineux normal il semble heureux que The ability to attenuate the forces produced by rapid les techniques de traitement et de reparation soient en and unexpected movement (Smith, 1954; Barnett, et a f . , rapide progression. 1961) is also dependent on tendon’s extensibility. Thus, although in the Achilles tendon of man this ZUSAMM ENFASSUNG function is doubtful (except in the case of contracted Sehnengewebe erfullt seine primare Aufgabe als and exhausted muscle) it may have relevance to the Kraftiibertrager sehr wirkungsvoll. Das Versagen dieses horse and other animals. passiven Gewebes fiihrt zu ausgepragten Storungen. Als ein Bindegewebe ist seine Struktur verhaltnismassig einSUMMARY fach und die eigenartige, schneckenartig gewundene Tendon normally fulfils its primary role as a flexible Anordnung der kollagenen Fasern erzeugt ausgepragte, force transmitting element very effectively and yet nicht-lineare und auch zeitabhangige mechanische Eigenfailure of this passive tissue leads to great disability. schaften. Die funktionelle Signifikanz irgendeiner mechAs a connective tissue its structure is relatively simple anischen Antwort kann nicht beantwortet werden, bevor and the peculiar helical arrangement of collagen fibres das physiologische Belastungsmuster bekannt ist. Vor confers highly non-linear as well as time-dependent allem mussen vorerst noch die Deformationsrate und die mechanical properties. Functional significance cannot minimale Kraft, die auf Sehnen bei der normalen Fortbe attributed to any facet of mechanical response until bewegung einwirkt, abgeklart werden. the physiological pattern of loading is established. Die meisten veroffentlichten Werte von MaximalIn particular the rate of deformation and the minimum kraften, die von Sehnengewebe iibertragen werden force experienced by tendon in normal locomotion have konnen, sind kleiner als die gemessene, praktisch yet to be elicited. statische Reissfestigkeit. Die Tatsache, dass gewisse Most published values of maximum forces transmitted Schatzungen diese Endgrosse iibertreffen, illustriert die by tendon fall short of the measured quasi-static rupture Fehlermoglichkeiten aller indirekten Schatzungen. Distrength. The fact that some estimates exceed this rekte und praktikable Messverfahren werden wohl ultimate force illustrates the errors incurred in indirect wertvolle Informationen liefern, wenn sie an Sehnen assessment. Direct measurement techniques, which angewendet werden, die spontan reissen konnen. have now been demonstrated to be practicable, should Die anderen mechanischen Funktionen von Sehnen yield valuable information when applied to tendons sind nur von sekundarer Bedeutung. Wir haben noch susceptible to spontaneous rupture. vie1 zu lernen, was die Muskelreaktion auf schnelle Other proposed mechanical functions of tendon are Belastung und Streckung anbetrifft, bevor entsprechende clearly of secondary importance. Much has yet to Hypothesen iiberpriift werden konnen. be learned of the response of muscle to rapid loading Bei unseren geringen Kenntnissen der normalen and extension before these hypotheses can be tested Sehnenfunktion konnen wir uns gliicklich schatzen, dass fully. die Behandlungsmethoden geschadigter Sehnen rasche With our scant knowledge of normal tendon function Fortschritte machen. it is indeed fortunate that the techniques of repair and treatment of damaged tendon are rapidly advancing. REFERENCES predispose to rupture.
RESUME Le role primordial du tendon est de transmettre une force variable; en consequence une defaillance de ce tissu “passif” entraine une certaine impotence. En tant que tissu conjonctif la structure du tendon est relative-
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Barfred, T. (1973). Achilles tendon rupture. Acta. orthop. scand. Siippl. 152. Barnes, G. R. G. and Pinder, D. N. (1974). In vivo tendon tension and bone strain measurement and correlation. J. Biornech. 7 ( I ) , 35. Barnett, F. H., Davies, D. V. and McConaill, M. A. (1961). Synovial joints: their structure and mechanics. London, Longmans. Chvapil, M., Hruza, Z. and Roth, Z. (1962). Physical and physical-chemical heterogeneity of collagen fibres from rat tail tendon. Gerontologia 6, 102. Cronkite, A. E. (1936). The tensile strength of human tendons. Anat. Rec. 64, 173. Cruise, A. J. (1958). The structural periodicity of microscopic collagen fibres. I n : Recent advances in gelatin and glue research, ed. G. Stainsby, p. 45, London, Pergamon. Dale, W. C., Baer, E., Keller, A. and Kohn, R. R. (1972). On the ultrastructure of mammalian tendon. Sep. Experientia 28, 1293. Dawson, T. J . and Taylor, C. R. (1973). Energetic cost of locomotion in kangaroos. Nature 246, Nov. 30, 3 13. Diamant, J., Keller, A., Baer, E., Litt, M. and Arridge, R. G. C. ( 1972). Collagen; ultrastructure and its relation to mechanical properties as a function of ageing. Proc. Roy. SOC., London B 180, 293. Edwards, D. A. W. (1946). The blood supply and lymphatic drainage of tendons. J . Anat. 80, 147. Elliott, D. H. (1965). Structure and function of mammalian tendon. B i d . Rev. 40, 392. Finlay, J. B., Hunter, J. A. A. and Steven, F. S. (1971). Preparation of human skin for high resolution scanning electron microscopy using phosphate buffered crude bacterial a amylase. J. Microscopy 93 (3), 241. Gathercole, L. J. and Keller, A. (1974). Supermolecular structural hierarchies in collagenous fibres. In: Structure of fibrous biopolymers, Butterworth (in press). Grafe, H. (1969). Aspekte zur Aetiologie der subcutanen Achillessehnenruptur. Zbl. Chir. 94, 1073. Gratz, C. M. and Blackberg, S. N. (1935). Engineering methods in medical research. Mech. Engng. 57, 217. Hildebrand, M. (1960). The suspensory ligament as an energy store. Sci. Am. 202, 148. Hill, A. V. (1951). The mechanics of voluntary muscle. Lancet 261, 947. Kunhke, E. (1962). The fine structure of collagen fibrils as the basis for functioning of tendon tissue. In Collagen, ed. N. Ramanthan, p. 479. New York, Interscience. Lerch, H. (1950). Uber den Aufbau des Sehnengewebes. Gegenbaiirs morph. Jb. 90, 192. Lindhard, J. (1931). Der Skeletmuskel und seine Funktion. Erg. Physiol. Berlin 33, 337. Morrison, J. B. (1967). The forces transmitted by the human knee ioint during- activity. Ph.D. thesis, University of Strat h d yde.
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