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Fibrous tissue on the tibia plateau of the kangaroo. A theory on the pressure absorption of joint surfaces

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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.,
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Windle, B.C.A., and F.G. Parsons 1898 On the anatomy of Macropus
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