Fibrous tissue on the tibia plateau of the kangaroo. A theory on the pressure absorption of joint surfacesкод для вставкиСкачать
THE ANATOMICAL RECORD 238:297-303 (1994) Fibrous Tissue on the Tibia Plateau of the Kangaroo A THEORY ON THE PRESSURE ABSORPTION OF JOINT SURFACES FRANZ K. FUSS Institute of Anatomy (1st Department) of the University of Vienna, A-1090 Vienna, Austria ABSTRACT The central part of the articular surface on the tibia plateau of Macropus agilis consists of fibrous cartilage of soft consistency and the fiber arrangement is macroscopically visible. The peripheral portions of the plateau are covered by hyaline cartilage but do not communicate with the hyaline articular surfaces of the femur, as they are covered by the menisci. The fibrous cartilage covering of the tibia plateau is a compliant or readily deformed pad that could serve the function of deforming enough under high joint loads to allow surrounding regions of the articular cartilage to share in carrying those loads, thereby magnifying the articular contact surface and decreasing the magnitude of the peak unit loads in the region of the fibrous tissue pad. This pressure-absorbing mechanism represents the evolutionary response to the higher articular stress resulting from kangaroo locomotion. o 1994 WiIey-Liss, Inc. Key words: Fibrous tissue, Joint surface, Tibia plateau, Kangaroo, Mammals, Pressure absorption, Joint mechanics The knee joint is a so-called “anatomically incongruent” joint which, in comparison to “congruent” joints, has relatively small articular contact surfaces (between the tibia plateau and femoral condyles in this case). The stress on the joint surface area is in inverse proportion to the size of the contact surfaces. The fibrocartilage in the discs and menisci is softer than the hyaline cartilage of the joint surfaces and hence seems most suited complementarily to enlarge the given contact area. The resulting load on the knee is not given alone by the sum of ground reaction and muscle forces, as is the case in other joints, but also by the forces simultaneously arising from the cruciate ligaments, which increase the total joint load (Paul, 1988). Due to the cruciates, the joint force vector or resultant falls onto the tibia plateau perpendicularly, and mainly into the above mentioned small contact areas. Joint loads depend on the manner and velocity of locomotion. There are two kinds of bipedal locomotion: (1)alternating ground contact by the feet as in walking and running (e.g., humans and ostrich), and (2) simultaneous ground contact of the feet as in hopping (e.g., kangaroo). The vertical fluctuations of the body’s center of mass are greater in hopping than in running, leading in the former case to higher ground reaction forces and increased joint loads. This form of locomotion might require morphologic changes of the joint to prevent excessive wear. Such a change, namely the existence of a patellar-shaped fibrocartilaginous pad instead of a n osseous patella (Parsons, 1990; Alexander and Dimery, 1985), has recently been discussed by Holladay et al. (1990). The phenomenon of a fibrocartilaginous patella can be explained by the theories on causal histogenesis by 0 1994 WILEY-LISS. INC Pauwels (1960) and Kummer (1980). According to Pauwels (1960)) there are two components of deformation which lead to differentiated developments of connective tissue: (1)shape change: tension (stretching, elongation) of the tissue due to pressure, pull or shear would provide the mechanical stimulus (shear stress and eventually compression stress) for collagen fiber production, and tendons or ligaments would develop; and (2) volume change: the compression of cells with increasing hydrostatic pressure would provide the mechanical stimulus (compression stress) to form cartilaginous tissue; hyaline cartilage would develop. When tissue is subjected to both shape and volume changes, fibrocartilage would develop. This is why menisci consist of fibrous cartilage: they are not only compressed but also subjected to pull and shear forces in the course of motion (Anderson et al., 1991). According to Kummer (1980), the tissue differentiation would strongly depend on the magnitude of the strain of the tissue: optimum strain (low shear stress) would lead to the differentiation of hyaline cartilage. The external compression load on the tissue would counteract the internal hydrostatic pressure due to the swelling of the chondrocytes. The tissue is thereby fulled through or “milled” (“Durchwalken,” Kummer, 1980). If the deformation is suboptimal (nearly no shear stress), the swelling of the chondrocytes prevails, Received July 28, 1992; accepted October 6, 1993. Address reprint requests to Franz K. Fuss, M.D., Ph.D., Institute of Anatomy, 1st Department, Wahringerstr. 13, A-1090 Vienna, Austria. 298 F.K. FUSS resulting in cell hypertrophy with lacunar enlargement and cell column formation, and endochondral ossification would begin. If, however, the deformation exceeds the optimum (high shear stress), the collagenous fiber mass increases, namely a t the expense of the ground substance, thus leading to fibrous cartilage and finally to connective tissue (ligamentousltendinous tissue). The latter mechanism might be responsible for the existence of the patellar fibrocartilage pad in kangaroos. Holladay et al. (1990) also suspected a n increase of the forces on the quadriceps tendon of the kangaroo, which they attributed to the “unusual locomotion pattern of the species.” The present paper reports on a n even more unusual pressure-absorbing mechanism in the kangaroo knee and discusses how the manner of locomotion could influence its knee mechanics. RESULTS Macromorphology As opposed to the uniformly hyaline articular cartilage surfaces of the femur (Fig. l a ) , two macroscopically differentiated articular surface areas with distinct tissue properties are located on the tibia plateau of the kangaroo (Fig. l b d ) . The peripheral portions of the articular surfaces which are covered by the menisci consisted of hyaline cartilage only (Fig. lc,d). The central portions, which are peripherally covered by the menisci, consisted of soft fibrous tissue in which the superficial fibers radiated from the intercondylar eminence to the peripheral regions (Fig. lM).This tissue area represented approximately 45%of the medial and 50% of the lateral articular surfaces. The respective hyaline cartilage percentages were 55% and 50%. The respective menisci covered 50% of the medial and 60% of the lateral articular surfaces. As the menisci overlapped the collagenous fiber areas, the femoral MATERIALS AND METHODS condyles rested on at least 2.5-3 mm thick layer of soft Four knees of two agile wallabys (Macropus agilis) fibrous tissue (Fig. 2). None of the other examined were dissected and measured with the aid of a three- mammals exhibited such a conspicuous field of fibrous dimensional digitizer (HyperSpaceQ Modeler, Miraa tissue on their respective tibia plateaus. Imaging Inc.). The specimens had previously served comparative functional and evolutionary investigaComparative Morphology of the Tibia Plateau tions into the tetrapod knee joint (Fuss, 1992). The According to the anteroposterior curvatures of the joints originated from juvenile animals (with open epiphyses), which died after collisions with wire fences tibia condyles, tibia plateaus can be subdivided into (one male weighed 16.5 kg, one female weighed 12.5 three groups (Table 1; Fig. 4): (1) both condyles are strongly convex; (2) both condyles are either slightly kg) . convex, slightly concave, or one condyle is slightly conThe patellar-shaped pad, tissue from the articular surfaces of the femur and tibia, both menisci and the vex while the other is slightly concave; and (3) both femorofibular discus were analyzed histologically. The condyles are strongly concave. The curvature correspecimens had been fixed in formaldehyde, dehydrated lates with the meniscus cross-section, with the rotation in graded alcohols and embedded in paraffin. Continu- range of the tibia and with the size of the joint surface ous longitudinal serial sections were cut on a sliding contact area (Table 1; Fig. 4). microtome at 5 pm and stained with hematoxylinl Micromorphology eosin. These sections were used to determine the tissue Histologically, the central regions of the kangaroo’s types. The tissues were classified by purely morphologic features, including the uniformity of the articular tibia plateau consisted of fibrous tissue (Fig. 3a-e) surface or any macroscopically identifiable fiber pat- whilst the peripheral portions consisted of hyaline cartern of a tissue; the possibility of subdividing the tissue tilage (Fig. 3f). Near the intercondylar eminence and into fibrillar strands; microscopic fibrillation or mask- the transition to hyaline cartilage, there were mainly ing of fibers; whether the cells looked like chondrocytes chondrocytes, while fibrocytes prevailed in the interor fibrocytes; if there were single chondrocytes or cell mediate areas where chondrocytes were scarce (Fig. nests; and if the tissue had high or low cellular density. 3 M ) . A few chondrocytes and nests of chondrocytes The above mentioned previous investigation into the were found in the vicinity of the intercondylar emitetrapod knee supplied us with further mammals for nence (Fig. 3a). Towards the hyaline cartilage region, comparative purposes. They include Tachyglossus ac- the chondrocytes formed cell nests and the collagenous uleatus (short beaked spiny anteater), Ornithorhyn- fibers were masked (Fig. 3f). The deeper layer of the chus anatinus (platypus), Erinaceus europaeus (hedge- fibrous region had a lower cellular density and conhog), Oryctolagus cuniculus domesticus (rabbit), Sus sisted of typical-appearing fibrocartilage-containing scrofa domestica (domestic pig), Phacochoerus aethiopi- cell nests (in rows) and proximodistally oriented fiber cus (warthog), Hippopotamus amphibius, Bos taurus tracts (Fig. 3e). The menisci and the femorofibular disc of Macropus (cow), Ovis ammon musimon (wild mountain sheep), Aepyceros melampus (impala), Neotragus moschatus consisted of cellularly dense fibrocartilage with chon(suni), Camelus dromedarius (camel), Equus caballus dro- and fibrocytes, but without cell nests (Fig. 3f). The (domestic horse), Equus quagga ( E . burchelli; zebra), fiber tracts were irregular (Fig. 3f). The fibrocartilagLoxodonta africana (african elephant), Canis familiaris inous patellar pad exhibited low cellular density and a (domestic dog), Panthera leo (lion), Phoca vitulia (seal), pattern of alternating horizontal and longitudinal fiPteropus rufus (flying fox), Papio ursinus (baboon), and ber tracts (Fig. 3g). The articular surfaces of the other mammals which Homo sapiens. The joint surfaces of the tibia were analyzed histologically in the following species: Sus were also subjected to histologic analyses consisted enscrofa domestica, Canis familiaris, Equus caballus, tirely of hyaline articular cartilage, a s were those areas which were covered by fibrous tissue in kangaroos. Phoca uitulina, and Homo sapiens. 299 PRESSURE ABSORPTION IN T H E KANGAROO KNEE Fig. 1. Knee joint of Mucropus ugilis. a: Distal end of the femur with hyaline cartilage covering. b-d: Tibia plateau with (b) and without (c,d) menisci. The fibrous cartilage areas are clearly visible (shaded in d). Abbreviations: rn = medial; 1 = lateral; f = fernorofibular disc; a = anterior or cranial cruciate ligament; p = posterior or caudal cruciate ligament. The soft fibrous tissue on the tibia plateau of the kangaroo could well be a n articular stress absorber designed to help to spread out the maximum loads on the knee over a larger part of the total joint surface. DISCUSSION A special pressure absorber could be necessary in the knee when above-average articular stresses occur. The following summarizes literature statements which sug- 300 F.K. FUSS ........... ........... ............ ........... ............ ............ ........... ............ ............ ........... ........... fibrous cartilage Fig. 2. Schematic section through the Macropus knee joint, showing the distribution of the tissue types. TABLE 1. Comparative morphology of the tibia plateau (c.f. Fig. 4)’ curvature contact area menisci rotation species Group 1 strongly convex small thick > 50” artiodactyls except hippo, horse, dog, lion, (seal) Group 2 slightly convex or slightly concave intermediate intermediate O‘-50” monotremes, kangaroo, hedgehog, rabbit, baboon, man Group 3 strongly concave large thin 0” hippo, elefant, (flying fox) ’Species in parentheses do not use their hindlimbs for terrestrial locomotion. gest that above-average articular stresses do arise in the kangaroo knee. The joint force in the knee depends on the ground reaction force (GRF). Human walking (approximately 4 k m h ) results in a ground reaction force of approximately 110-120% of the individual’s body weight (bw; Cochran, 1982). In the case of a hopping (6.5 k d h ) Benett’s wallaby (10.5 kg bw), the measured GRF amounted to 312% bw, i.e., 156% per leg (Alexander and Vernon, 1975). The maximum hopping speed of large kangaroos, however, lies between 50 and 65 k d h (Dawson and Taylor, 1973) and far exceeds that of humans. Humans and kangaroos have a similar ratio of Froude numbers (velocity squared per gravitational acceleration per hip height) to relative stride length (stride length per hip height: Alexander, 1977, 1991). The fact that the human hip height is greater than that of kangaroos implies that kangaroos have a smaller absolute stride length and thus a higher stride frequency when progressing at the same velocity. This implies more frequent stresses per time unit of each kangaroo knee. At a hopping velocity approaching 40 k d h , the body’s center of mass vertical fluctuations are greater than those in running, which results in greater and more frequent stresses of the knee. As opposed to humans, kangaroos can sustain speeds of 40 k d h for several kilometers (Dawson and Taylor, 1973). With increasing speed, not only the the articular stresses but also the body’s oxygen consumption increases, hence high speed periods as well a s the duration of high articular stresses are temporally limited, thus preventing a n overstress of the locomotor system. This is otherwise in the case of kangaroos. According to Dawson and Taylor (19731, the oxygen consumption actually decreases by 7% with a n increase in velocity from 7.5 to 21.5 k d h . From 18 kmlh upwards, hopping appears to be more energy-saving than running by a four-legged animal of the same body weight (Dawson and Taylor, 1973). The low use of energy in hopping might be related to the higher “survival chances” of kangaroos, a s quadrupedal herbivores became extinct in Australia (Dawson and Taylor, 1973). The cause of this minimized oxygen consumption a t medium velocity could lie in the energy storage capacity of the long tendons of the rear limbs (Dawson and Taylor, 1973). The stretched spring tendons recoil during take-off and P R E S S U R E ABSORPTION I N T H E KANGAROO K N E E Fig. 3. Tissue types (Mucropus). a 4 Tibia (a: near intercondylar eminence; b: superficial layer of fibrous tissue area; c, d central layer; e: deep layer [note the chondrocyte rows]; f: transition to the hyaline cartilage); g: Meniscus; h Patellar pad. 301 302 F.K. FUSS Fig. 4. Schematic representation of the different tibia plateaus in mammals (a: group 1; b group 2; c: group 3; c.f. text and Table 1). Fig. 5. Schematic representation of the relation of contact area (arrows) to tissue softness. could make use of the stored elastic energy (Alexander and Vernon, 1975). The duration of maximal joint load is not unlimited; it will only be allowed for as long as 0,-reserves are sufficient. As the 0,-consumption in kangaroos first decreases with increasing speed, the animals lack this “overload protection at medium speeds, allowing them to maintain higher load levels over longer distances and hence longer time periods than the average of other species. A decrease of the average load per unit area by softer fibrous tissue on the articular, surface appears advantageous. The cause of different curvatures of tibia plateaus is found in the rotation range rather than in average joint load. Two of the examined species do not use their hind extremities for terrestrial locomotion but nevertheless exhibit extreme curvatures: Pteropus, with extremely concave articular surfaces and Phoca, with convex ones. The thickness of the menisci does not, in these two species, correspond to the group average; in the case of Phoca they are thinner than in other species exhibiting strongly convex curvatures; in Pteropus there are none. This may well correlate to the inferior average load per unit area exerted on the respective joints of these two species. The Pteropus knee cannot perform rotations whilst that of Phoca exclusively rotates (although extension/flexion is possible in the seal’s knee, its practical function seems doubtful as the shank is fixed to the pelvis by the hamstring muscles). The contact surfaces of an “incongruent” joint depend on the material properties of the tissue. If the material is very stiff, i.e., if it has a high Young’s mod- ulus of elasticity (E), the contact surface would be very small. The smaller E is, the more compressible the material and the larger the joint contact surfaces will be (Fig. 5). This would reduce the unit loads on the tissue and its stresses. In the case of a constant joint load, the unit loads on the joint surface can be decreased by lowering E. Thus, a soft, compressible and fibrous articular surface will serve to decrease peak articular unit loads. That the tibia plateau is not generally covered with fibrous tissue could be due to the fact that the articular cartilage was deformed in its optimum (Kummer, 1980, c.f. Introduction) in the other mammals which were examined, while the deformation in kangaroos could obviously exceed this optimum amount if the tibia plateau were covered with hyaline cartilage. Although this theory of causal histogenesis (Pauwels, 1960; Kummer, 1980) is antiquated, it is useful for the finding of a sensible explanation of the phenomenon that fibrous tissue can be found in kangaroo knees. The mechanism, in which a tissue adapts to the generally prevailing mechanic situation and finds its balance in a specific differentiation type, can be termed tissue “modeling” (Frost, 1990) or “mechanostat” (Frost, 1987). This mechanism must, however, be termed a long-term evolutionary mechanostat, as an unphysiological joint overstress or shear stress, due to cruciate ligament rupture, leads to joint degeneration in the individual. Overstressed articular cartilage does not turn into fibrocartilage but nevertheless does degenerate with an increase of collagenous fibrils, i.e., its fiber content increases (Kummer, 1980). The “biomechani- PRESSURE ABSORPTION IN THE KANGAROO KNEE cal” embryology of Blechschmidt (1960) can explain the differentiation of hyaline cartilage and fibrous tissue in the embryo, namely, long before normal mechanical loads are borne on those tissues. Ligaments and tendons arise in the growing retention fields due to simultaneous pull and transverse compression of the mesenchyme by adjacent growth dynamics. The same applies to the hyaline cartilage developing in the distusion fields under compression (Blechschmidt, 1960). All these structures possibly develop similarly and their tissues may differentiate under similar stresses to which they are exposed in adult life. It is surprising that the fibrous articular surface of the tibia has never been discussed in publications dealing with the kangaroo knee (Windle and Parsons, 1898; Parsons, 1900; Haines, 1942; Holladay et al., 1990). The general opinion that all articular surfaces consist of only hyaline cartilage (except for clavicula and mandibula; Barnett et al., 1961; Williams and Warwick, 1980) must be revised. In summary, the fibrous cartilage covering of the tibia plateau can be regarded as a compliant or readily deformed pad that could serve the function of deforming enough under high joint loads to allow surrounding regions of the articular cartilage to share in carrying those loads, thereby magnifying the articular contact surface and decreasing the magnitude of the peak unit loads in the region of the fibrous tissue pad. ACKNOWLEDGMENTS My special thanks go to Dr. Brian Freeman from the University of New South Wales, Kensington, N.S.W., Australia, for the supply of the wallaby and monotreme knees. I a m also grateful to two anonymous reviewers for providing very valuable comments. This work was supported by the “Fonds zur Forderung der wissenschaftlichen Forschung” (P7914-MED). LITERATURE CITED Alexander, R.McN. 1977 Terrestial locomotion. In: Mechanics and Energetics of Animal Locomotion. R.McN. Alexander, and G. Goldspink, eds. Chapmann & Hall, London, pp. 168-203. 303 Alexander, R.McN. 1991 How dinosaurs ran. Sci. Am., 264t62-68. Alexander, R.McN., and N.J. Dimery 1985 The significance of sesamoids and retro-articular processes for the mechanics of joints. J . Zool. Lond., 205t357-371. Alexander, R.McN., and A. Vernon 1975 The mechanics of hopping by kangaroos (Macropodidae). J . Zool. Lond., 11 7t265-303. Anderson, D.R., S.L.-Y. Woo, M.K. Kwan, and D.H. Gershuni 1991 Viscoelastic shear properties of the equine medial meniscus. J . Orthop. Res., 9:550-558. Barnett, C.H., D.V. Davies, and M.A. MacConaill 1961 Synovial Joints. Longmans, London. Blechschmidt, E. 1960 The Stages of Human Development Before Birth. Kager, London. Cochran, G.V.B. 1982 A Primer of Orthopaedic Biomechanics. Churchill Livingstone, New York. Dawson, T.J., and C.R. Taylor 1973 Energetic cost of locomotion in kangaroos. Nature, 246:313-314. Frost, H.M. 1987 Bone “mass” and the “mechanostat”: A proposal. Anat. Rec., 219:l-9. Frost, H.M. 1990 Skeletal structural adaptations to mechanical usage (SATMU): 1-4. Anat. Rec., 226t403-439. Fuss, F.K. 1992 Comparative functional morphology of intra-articular knee ligaments and the evolution of the cruciate ligaments. 9th European Anatomical Congress, Krakbw, 14.-18. 9. 1992, Abstract, p. 81. Haines, R.W. (1942) The tetrapod knee joint. J. Anat., 76t270-301. Holladay, S.D., B.J. Smith, J.E. Smallwood, and L.C. Hudson 1990 Absence of a n osseous patella and other observations in Macropodidae stifle. Anat. Rec., 225t112-114. Kummer, B. 1980 Kausale Histogenese der Gewebe des Bewegungsapparates und funktionelle Anpassung. In: BenninghoffGoerttler: Lehrbuch der Anatomie des Menschen. H. Ferner and J. Staubesand, eds. Urban & Schwarzenberg, Munchen, Vol. 1, pp. 242-256. Parsons, F.G. 1990 The joints of mammals compared with those of man. Part 11-joints of the hind limb. J . Anat., 34:301-323. Paul, J.P. 1988 Mechanics of the knee joint and certain joint replacements. In: Total Knee Replacement, Proceedings of the International Symposium on Total Knee Replacement. 1987, Nagoya, Springer, Tokyo pp. 25-35. Pauwels, F. 1960 Eine neue Theorie uber den EinfluB mechanischer Reize auf die Differenzierung der Stutzgewebe. ‘Zeitschr. Anat. Entwicklgesch., 121~478-515. Williams, P.L., and R. Warwick 1980 Gray’s Anatomy 36th Ed., Churchill Livingstone, Edinburgh. Windle, B.C.A., and F.G. Parsons 1898 On the anatomy of Macropus rufus. J . Anat., 32t119-134.