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Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor-induced strain.

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THE ANATOMICAL RECORD 242147-158 (1995)
Pattern of Collagen Fiber Orientation in the Ovine Calcaneal Shaft
and Its Relation to Locomotor-Induced Strain
Department of Anthropology (J.M.M.) and Hard Tissue Research Unit, Department of
Anthropology, (T.G.B.), Hunter College, City University of New York, New York;
Department of Anatomy and Developmental Biology, University College London,
London, U.K. (A.B.)
Background: Gebhardt (1905. Arch. Entwickl. Org., 20:187322) originated the hypothesis that the direction of collagen fibers in bone
is a structural response to the type of mechanical load to which the bone is
subjected. He proposed that collagen fibers aligned parallel to the loading
a x i s are best suited to withstand tensile strain, whereas fibers oriented
perpendicular to the loading axis are best able to resist compressive strain.
Research comparing load patterns with fiber alignment in bone have
tended to support Gebhardt’s hypothesis. The aim of the present study is to
further test this hypothesis by assessing the correspondence between the
distribution of strain and the distribution of collagen fiber orientation in a
bone that is subjected to compound loading (i.e., both tension and compression at different phases during the loading cycle). The ovine calcaneum was
selected to meet this criterion.
Methods: Calcaneum surface strain distributions were obtained from experimental results reported by Lanyon (1973. J. Biomech. 6:41-49). Histological sections of the calcaneal shaft were prepared and observed using
circularly polarized light (CPL)microscopy to determine the distribution of
collagen fiber alignment. The observed alignment pattern was then compared with the predicted pattern based on Gebhardt’s hypothesis.
Results: Contrary to previous studies, our findings show no clear correspondence between the strain type of greatest magnitude and the direction
of collagen fibers. Areas of bone characterized by high compression and
low tension showed predominantly longitudinal collagen alignment (contra
to Gebhardt).
Conclusions: It is argued that even small magnitudes of tension operating
on local areas of bone may be sufficient to induce collagen alignment favorable to this type of strain, even when greater magnitudes of compressive
strain are acting on the same bone volume. 0 1995 Wiley-Liss, Inc.
Key words: Collagen fiber alignment, Bone strain, Biomechanics, Calcaneum, Talocrural joint, Ouis aries, Circularly polarized light
Calcified tissue research has shown unequivocally
that mechanical function plays a crucial role in regulating the structure of bone. Studies of patients with
chronic limb paralysis, or with experimental animals
in which functional loading is arrested have allowed
investigators to distinguish between structural properties of bone that do not depend upon external loading
stimuli and structural features that are dependent
upon external function (i.e., structural responses to
strain). It has been shown in such cases that the normal size and shape of various processes and tuberosities, the girth, cortical thickness and cross-sectional
geometry, and the extent of longitudinal curvature of
the shaft of long bones all depend on the functional
loading environment for their development (Howell,
1917; Stinchfield et al., 1949; Lanyon, 1980).
Early recognition of these facts prompted Wolff
(1892) to postulate that the external conformation of
bone will develop so as to best withstand, and take
advantage of, the functional strains to which it is subjected. This principle was soon extended to include microscopic features of bone structure, and research into
Received March 21, 1994; accepted January 18, 1995.
Address reprint requests to James McMahon Hard Tissue Research
Unit, Department of Anthropology, Hunter College, C.U.N.Y., 695
Park Avenue, New York, NY 10021.
the mechanical properties of such features as bone density, distribution of mass, tissue type, and the alignment of various tissues has since been a major focus of
research (see Evans, 1970; Currey, 1984a).
Gebhardt (1905),in an early investigation of collagen
fiber alignment, proposed that the ability to resist different types of forces covaried with the direction of collagen fibers in bone. More specifically, collagen fibers
aligned parallel with the loading axis (i.e., longitudinal
in a long bone) are best able to withstand tensile stress,
whereas collagen fibers oriented perpendicular to the
loading axis (i.e., transverse in a long bone) are best able
to resist compressive stress.
The purpose of the present study is to test Gebhardt’s
hypothesis by assessing the degree of correspondence
between the distribution of principal strains and the
pattern of collagen fiber orientation over entire crosssectional areas of the ovine calcaneal midshaft. This
study differs from previous related work in that the
calcaneal diaphysis (unlike many other long bone diaphyses) is subjected to both tension and compression at
different phases during the loading cycle, and it was
therefore possible to examine the effects of this compound loading on the alignment of collagen fibers.
In lamellar bone, the arrangement of collagen fibers
and mineral crystallites is highly ordered. Fibers
within each lamella run parallel in their orientation
and follow a helical path with respect to the axis of the
canal. Hydroxyapatite crystallites are mostly aligned
in nearly the same direction as the collagen fibers
(Lees and Davidson, 1977; Ascenzi et al., 1983).
Von Ebner (1875) and more recently, Cooper et al.
(1966)have suggested that within osteons the direction
of fibers changes dramatically in successive lamellae.
Ascenzi and Bonucci (19681, however, contend that
there are three distinct types of osteons with respect to
fiber orientation. In the first type, all lamellae possess
fiber bundles with a predominantly transverse helical
course; in the second type, successive lamellae alternate between longitudinal and transverse helical orientation; and type three osteons have lamellae with
nearly all longitudinally aligned collagen fibers.
Gebhardt originally theorized that collagen fibers in
Haversian systems serve to absorb forces applied to
bone during functional loading and channel these
forces (stress) along the plane of expansive strain. With
this model it can be seen that compressive force acting
on the long axis of an osteon, which results in expansive strain in the transverse plane, is best regulated by
transversely oriented collagen fibers, and tensile force
acting along the same axis, which results in expansive
strain in the longitudinal axis, is best resisted by longitudinally directed fibers.
Empirical support for Gebhardt’s hypothesis was
forthcoming in the mid-l960s, when Ascenzi and Bonucci (1964, 1967, 1968) reported on a series of experiments in which they measured the ultimate cornpressive and tensile strengths of single isolated osteons of
each of the three fiber orientation types. Table 1 lists
the ultimate compressive strengths of isolated (wet)
osteons taken from a 30-year-old human femur. These
data show that osteons with longitudinal fibers (“longitudinal osteons,” for short) fracture under conditions
TABLE 1. Ultimate compressive strength of single
isolated osteons (kglrnm’)’
Full calcification
16.70 1.19 n = 13
13.66 k 0.95 n = 12
11.20 ? 1.03 n = 7
Initial calcification
10.02 1.05n=8
7.99 5 1.37n=7
8.96 + 0.94n = 7
‘From Ascenzi and Bonucci, 1968.
of relatively low compressive loading (11.20 kgimm’)
compared to transverse osteons (16.70 kg/mm 1, with
alternate osteons intermediate between the two (13.66
kg/mm’). Conversely, as shown in Table 2, transverse
osteons subjected to tensile strain appear to fracture at
a much lower loading threshold (3.49 kg/mm2)than do
longitudinal osteons (11.07-12.64 kg/mm’), with alternate osteons intermediate but trending toward the
higher values (9.59 kg/mm2).
The degree of calcification also appears to have an
effect on the ability of osteons to withstand compressive and tensile strain (Evans and Vincentelli, 1974;
Riggs et al., 199313). This fact was not emphasized in
these studies, but perhaps for good reason. The lag between the onset and initial completion of osteonic calcification is relatively short (days). Thus even formative bone segments will consist predominantly of fully
calcified osteons.
Apart from these experimental studies, another approach to test Gebhardt’s hypothesis is to assess the
correspondence between strain type and collagen fiber
orientation over entire cross sections of bone. Two
types of data are thus required: (1)the distribution
pattern of transverse and longitudinal lamellae, and
(2) the distribution of compressive and tensile strain,
over corresponding cross-sectional areas of bone.
Fewer than a dozen such correlative studies have
appeared in the literature, the vast majority of which,
especially early on, have focused on the human femur.
This is not surprising since most investigators have
relied on published strain data for their assessments,
and the human femur is one of the most thoroughly
studied of all human long bones.
A typical example of this type of study is provided by
Portigliatti Barbos et al. (1984), who documented the
distribution of transverse and longitudinal lamellae in
transverse femoral sections (nearly the entire diaphysis of the human femur was represented). These authors found that “. . . the orientation of transverse
lamellae undergoes a rotation from the medial toward
the posterior wall in going from the proximal to the
distal end of the shaft” (p. 313). In order to assess the
correspondence between fiber orientation and functional strain, they reviewed the available literature on
patterns of strain operating on the human femur. They
conclude: “The recent literature reports data that consistently suggest a distribution of bending forces in the
femur that could account for the rotational distribution
of the transverse and longitudinal osteonic and interstitial lamellae along the femoral shaft . . .” (p. 314).
Boyde and Riggs (1990)recently conducted a similar
study on the equine radius. The radius is the major
load bearing long bone of the horse forelimb. Its in vivo
strain pattern is highly predictable due to the marked
TABLE 2. Ultimate tensile strength of single isolated
osteons (kg/mm2)
Full calcification
3.49 0.79n= 4l
9.59 I+_ 1.55n= g2
12.64 _t 1.51n=12’
11.07 rt 0.68n= 4l
Initial calcification
3.05 k 0.94 n = 3l
9.06 * 1.48 n = 9’
10.95 _t 1.88 n
9.41 2 1.71 n
‘From Simkin and Robin, 1974.
2From Ascenzi and Bonucci. 1968.
longitudinal concave curvature of its caudal aspect.
This pattern-tensile strain on the cranial, medial,
and lateral sides, and compressive strain posteriorlyhas been confirmed experimentally using electric
strain gauge technology (e.g., Rubin and Lanyon,
1982). The correspondence between published strain
data and the distribution of transverse and longitudinal lamellae over cross sections of the horse radius is
unambiguous: “A striking pattern for the distribution
of TS [transverse spiral] and LS [longitudinal spiral]
collagen is apparent. The bulk of the cranial, medial
and lateral cortices has a very high proportion of LS
collagen-the caudal cortex contains predominantly
TS collagen” (Boyde and Riggs, 1990, p. 37).
Results of these and other correlative studies (e.g.,
Portigliatti Barbos et al., 1983, 1984, 1987, 1995;
Boyde et al., 1984; Ascenzi et al., 1987a, b; Carando et
al., 1989; Boyde and Riggs, 1990; Riggs et al., 1993a;
Bromage, 1992) demonstrate support, at least in part,
for Gebhardt’s hypothesis of the relationship between
functional loading and preferential collagen alignment.
bers appear bright. The advantage of using circularily
polarized light, as compared to linearly polarized light,
is that sections can be viewed in all 360” rotational
positions without affecting the pattern or magnitude of
bright- and darkfields, which is thus a more accurate
representation of the orientations of collagen arrays
(Boyde et al., 1984).
More recently, Boyde and Riggs (1990) elaborated
this method to include both simple qualitative and
quantitative imaging techniques. Qualitative observations are easily made as a result of displaying whole
ground sections of even very large bones by placing the
section between two large circular polars. One can then
readily comprehend the macroscopic patterns of preferentially oriented collagen. Quantitative procedures
for producing a digitized, pseudo-color coded image of
the signal intensity returned from whole ground sections examined by a macro lens between crossed circular polars has been described in detail by Boyde and
Riggs (1990).
Preparation of Materials
Five ovine calcanei were prepared for analysis in the
present study (Table 3). The diaphysis was removed
from each calcaneum with a high-speed diamond saw.
Specimens were then cleaned in a 1%Tergazyme (Alconox, New York City) solution a t 40”C, with occasional ultrasonication. A series of plane parallel
100-km sections was made with a water-cooled, slowspeed diamond saw transverse (perpendicular) to the
longitudinal axes of the shafts. Sections were retreated
with 1%Tergazyme and ultrasonicated for further
cleaning. Each section was then treated with chlorofordmethanol (1:l ratio), rinsed in methanol, and
mounted in DPX. Sections were then observed and phoThe calcaneum was selected for study here because it tomicrographed in CPL.
shares several properties with long bones-its function
is primarily mechanical, it acts as a lever, and it has a
shaft and medullary cavity-and results are therefore
comparable with those of previous studies involving
long bones. Yet, unlike previously studied long bones,
Photomicrographs of the ovine calcaneal sections all
elements of the calcaneum experience compound load- revealed a consistent pattern of bright and dark distriing (i.e., both principal tension and compression) dur- bution under circularly polarized light. Unlike the reing normal locomotion. For example, in the sheep, the sults obtained for the human femoral shaft, in which
caudal aspect of the calcaneal shaft undergoes both the pattern rotates from medial to posterior moving
compressive and tensile strain a t different phases of distally, the pattern of bright and dark lamellae in the
the locomotor cycle. This allows study of microstruc- sheep calcaneum remains constant along the length of
tural responses to more complex loading situations the shaft.
The following patterns in the distribution of Erigkit
than have previously been reported. The sheep calcaneum was chosen for study because reliable strain data and dark lamellae of a typical section were observed
for this bone is available in the literature (Lanyon, (see Fig. 1). First, a progressive increase in the density
of bright (transverse) lamellae was observed proceed1973).
ing from the exterior surface to the interior of the secAssessing Distribution of Collagen Fiber Alignment in Bone tion, culminating with endosteal and trabecular tissue
Boyde et al. (1984) used circularly polarized light that was nearly all transverse. This pattern has also
(CPL) microscopy to detect the pattern of collagen fiber been observed in shafts of the human femur (Portigliorientation in bone sections. This technique involves atti Barbos et al., 1984; Ascenzi et al., 1987a) and tibia
the use of two polarizing filters and two quarter wave (Portigliatti Barbos et al., 19951, and the horse radius
plates, each set a t a specified orientation. Thin sections (Riggs et al., 1993a).
There were two notable exceptions t o this pattern:
of lamellar bone observed between crossed circular polars appear either bright or dark depending on the ori- (1) in some sections, areas of outer circumferential
entation of their collagen fiber: lamellae composed of lamellae appeared bright, and (2) the occurrence of a
longitudinally aligned collagen fibers appear dark, few bright lamellae (bright “rings”) around each of othwhereas lamellae composed of transversely aligned fi- erwise dark osteons was observed in both the caudal
TABLE 3. Specimen data for calcanei of Ovis aries used in this study
Specimen #
Fig. 1, Photomicrograph of the diaphysis of a left subadult sheep calcaneum (OVA6 in Table 3) under
circularly polarized light (CPL), showing the pattern of collagen fiber orientation. The cranial aspect is
at the top and the medial aspect is to the left. Cranial (A),lateral (B),medial (0,and caudal (D) aspects
are shown to the right at higher resolution. The scale bars shown on the main figure and insert D
represent 1 mm (A-C scale to D).
and, especially, cranial aspects of nearly all specimens.
In some sections, particularly in the cranial cortex of
OVA4, the greater density of these bright-ringed osteons resulted in a relatively higher concentration of
bright lamellae (see Riggs et al., 1993a).
Second, bright (transverse) lamellae were observed
predominantly in the medial and (to a lesser extent in
some sections) lateral aspects of the shaft, as exemplified by OVA6 (see Fig. 1).However, there are several
important differences between the bright lamellae in
the medial and lateral segments: (1) in OVAl and
OVA2, bright lamellae of the medial aspect extends
over the entire cortical thickness (with the exception in
some instances of the external circumferential lamellae), whereas the bright lamellae in the lateral aspect
are concentrated along the endosteal surface of the cortex, and ( 2 )bright lamellae in the medial aspect consist
mostly of interstitial and compacted coarse cancellous
bone with some bright secondary osteons, whereas
bright lamellae of the lateral aspect consist almost exclusively of secondary osteons (with the exception that
in several sections of OVA2 resorption of the medial
side has left only bright cancellous bone).
Finally, the cranial and caudal aspects of the shaft
were composed predominantly of dark lamellae. Along
with the bright “rings,” the only other source of bright
lamellae in the cranial and caudal aspects of the shaft
is from interstitial tissue.
Previously Published Strain Data
Data used in this study to reconstruct the strain cycles experienced by the sheep calcaneal shaft during
normal locomotion comes from two sources. Badoux
(1987) has proposed a biomechanical model for the
equine talocrural joint that, with modifications, can be
applied to the sheep talocrural joint and used to predict
the distribution of strain along the ovine calcaneal
shaft. Lanyon (1973) has published in vivo strain data
recorded from rosette strain gauges adherent to the
sheep calcaneal shaft during locomotor activity.
Lanyon (1973)implanted rosette foil strain gauges in
various positions on the calcaneum of live sheep (For a
discussion of the in vivo strain gauge technique, see
Cochran, 1972, and Caler et al., 1981). In each case, at
least one of the gauge elements was aligned parallel to
the long axis of the shaft. The changing direction and
Craniolateral &
Event #
3 1
Fig. 2. Cycle of strain on caudolateral (top), craniolateral, and lateral (bottom) aspects of the sheep
calcaneum during normal locomotion (after Lanyon, 1973). The horizontal lines running through each of
the two graphs indicate the point of zero strain: tension ( + ) is above the line; compression (-1 is below
it. The horizontal axis represents time, and the numbers signify important locomotor events: (1) midpoint
of swing phase, (2) midpoint of weight-bearingphase, and (3)just after hindlimb lift, before swing phase.
magnitude of principal compressive and tensile strain
were then recorded during walking a t various speeds.
Figure 2 shows several cycles of strain (corresponding
with locomotor cycles) for three strain gauges adherent
to the lateral, craniolateral, and caudolateral aspects of
the shaft (the medial surface was not measured). Each
is aligned parallel to the long axis of the shaft.
These data show that the lateral and craniolateral
(dorsal) aspects underwent a cycle of relatively high
compression followed by low tension and that the occurrence of maximum compressive strain coincided
with full weight bearing of the hindlimb (event 2 of
Fig. 2). During this phase of the cycle, the craniolateral
aspect of the shaft reached a greater magnitude of compression than did the lateral aspect (not shown in Fig.
2). The strain cycle on the caudolateral (plantar) side
was somewhat different. Here, the shaft underwent a
cycle of tension and compression of nearly equal magnitude. Moreover, the pattern of correspondence to locomotion is nearly opposite to that of the other two
surfaces measured. Whereas the lateral and craniolatera1 surfaces tended toward maximum compression
during maximum weight-bearing, the caudolateral
surface experienced maximum tension. Once the hindlimb passed the point of maximum weight-bearing, the
lateral and craniolateral regions met with decreased
compression (and moved toward tension), whereas the
caudolateral aspect decreased in tension (and moved
toward compression). Once the hindlimb was lifted
(event 3 of Fig. 2), the lateral and craniolateral sides
experienced relatively small magnitudes of tension,
whereas the caudolateral aspect underwent maximum
compression. Subsequently, all regions of the shaft
tested met with neutral strain during the swing phase
before the cycle was repeated.
Lanyon’s (1973) own interpretation of his strain data
is somewhat different from that proposed here. He did
not view the calcaneum as a lever with alternating
bending cycles. He surmised that “If the calcaneum
acted as a lever, then pull by the gastrocnemius muscle
. . . would have bent the bone, causing compression on
one side [cranial] and tension on the other [caudal].”
But he insisted, “This did not happen, indeed in the
plantar [caudal] region there was either little strain
change, or a degree of compression, during the dominant compression period (Lanyon 1973, p.47). In his
experiments, there were only two test limbs for which
strain data on the craniolateral and caudolateral surfaces of the calcaneum were measured parallel to the
long axis of the shaft (denoted as S34 and S35).
Lanyon’s (1973) interpretation is based primarily on
one of these (S35) in which peak compression on the
craniolateral side during maximum weight bearing is
separated from peak tension on the caudolateral side
by -.06 seconds. On S34, these opposing peaks occur
virtually simultaneously.
Data presented in Table 4 are derived from the original strain cycle graphs in Figure 4 of Lanyon (1973)
for S34 and S35. These data support the interpretation
proposed here that the sheep calcaneum undergoes alternating bending forces during each locomotor cycle.
First, bending in a cranial direction causes compression cranially and tension caudally (0-.36 seconds in
S34), then, slight bending in a caudal direction results
in slight tension cranially and compression caudally
(.36-.5 seconds in ,534). Although the timing of opposing peak strains and instant of crossover are not precisely simultaneous for the cranial and caudal aspects
of 5335, a similar trend is evident.
This interpretation is consistent with the biomechanical model proposed for the equine talocrural joint
by Badoux (1987) and reproduced (with modifications
reflecting ovine anatomy) in Figure 3. When the hindlimb comes into substrate contact, the resultant forces
TABLE 4. Comparison of strain values for various gauge elements read at .l-sec
intervals through a typical loading cycle’
Specimen S34
(gauge 1)
(gauge 2 )
+ 83.50
+ 225.45
+ 117.00
- 43.60
+ 58.50
Specimen S35
(gauge 1)
(gauge 2)
+ 190.90
+ 24.90
+ 43.20
‘Source: Lanyon (1973),Fig. 4.
F1 and F2-from the loads applied by the superficial
digital flexor (SDF) and gastrocnemius tendons (GAS),
respectively-cause the calcaneal shaft to bend, resulting in compressive strain cranially and tensile strain
caudally (see Fig. 3a). That the shaft is subjected to
bending in the craniocaudal (parasagittal) plane is further indicated by its cross-sectional geometry in which
the maximum diameter from centroid is also along the
craniocaudal plane. Once the point of maximum weight
bearing has been attained, there follows a gradual decrease in the amount of weight supported by the hindlimb, resulting in a progressive decrease of compression cranially and of tension caudally. This condition is
further advanced by the fact that, in the sheep, the
gastrocnemius muscle actively contracts only during
the phase leading up t o maximum weight-bearing
(Lanyon, 1973j. Subsequently, the plantar ligament,
which functions to stabilize the calcaneum against the
metatarsus, can more easily neutralize the bending effects of the superficial digital flexor tendon. Moreover,
as the angle at the talocrural joint widens during the
phase leading up to hindlimb lift, the bending force of
the superficial digital flexor diminishes, as more of its
applied load is directed axially along the calcaneum
(see Fig. 3b).
The tensile strain recorded on the craniolateral and
lateral surfaces of the calcaneum during maximum
plantar flexion a t hindlimb lift can be explained biomechanically by observing how the angle between the
calcaneum and the gastrocnemius tendon changes during plantar flexion. The gastrocnemius muscle originates from the distal femur and inserts on the cranial
side of the proximal end of the calcaneum via the tendo
calcaneum. In a dorsiflexed position (see Fig. 3a), the
gastrocnemius tendon pulls on the calcaneal tuber at
an oblique angle (resulting in cranially oriented bending of the shaft and compression on the cranial side).
During plantar flexion (see Fig. 3b), this angle is increased until the tendon is pulling nearly parallel to
the calcaneal axis (resulting in tension on the cranial
It is much more difficult to account for the compressive strain recorded on the caudolateral side during
this phase. Lanyon (1973)postulated that pull from the
superficial digital flexor tendon could cause overall
compression of the shaft. But this seems unlikely, since
it could occur only if both the distal (plantar) and proximal portions of the SDF pulled downward from the tip
of the calcaneum, a condition requiring an exceedingly
small talocrural angle, in contrast to the large talocru-
ral angle observed during caudolateral compression.
More likely is Lanyon’s (1973) second suggestion, that
plantar flexion results in stretching the plantar ligament: “This effect, from fibres inserting above the
gauge site, could explain the continued compression [of
the caudolateral aspect] during the time when the heel
was lifting from the ground” (p. 47).
The four principal underlying assumptions upon
which our interpretations are based are made explicit
here. All deal with the degree of confidence with which
the strain histories of the calcanei used in our histological analysis can be inferred. Since collagen fiber
orientation data were derived from calcaneal specimens different from those used to generate strain cycle
data, it is first assumed (assumption 1)that the strain
cycles experienced by the sheep calcanei in Lanyon’s
(1973) experiments are the same as those experienced
by the calcanei used in our CPL microscopic analysis.
But even if both structural and functional analyses
were performed on the same specimens, three further
suppositions are required: assumption 2, Lanyon’s in
vivo strain gauge data for sheep locomotion are accurate; assumption 3, the strain cycles recorded are representative of the total loading repertoire influencing
microstructural response in the sheep calcaneum; and
assumption 4, strain gauge data read on a limited surface area of bone can be extrapolated to include bone
deep t o the surface.
Assumption 1 : lntraspecific invariability of strain cycle
Lanyon (1973) found little interindividual variation
in strain cycles among the seven sheep that were studied. Of the four specimens (S34, S35, S47, and S48) to
which gauges were attached to the cranial aspect and
aligned parallel to the long axis of their calcanei, all
showed the same wave form and relative compression
to tension magnitudes (although the absolute magnitudes of each varied somewhat). As previously discussed, the wave forms indicated by gauges adherent to
the caudolateral aspects of specimens S34 and S35
were slightly different, but their relative compression
and tension magnitudes and correspondence with
strain cycles on the cranial side were similar.
Although not explicitly stated by Lanyon, it is clear
from his diagrams (e.g., Fig. 2 in Lanyon, 1973) that
specimens of Ovis aries (domestic sheep) were used as
experimental subjects. There are many breeds, but this
f- Cranial
Caudal +
Plantar flexion
Fig. 3.Ovine talocrural joint in (a)dorsiflexion and (b) plantar flexion (see text for details).
species exhibits remarkable morphological homogeneity (prompting Hafez et al., 1962, to argue for a single
origin of domestic sheep). Prummel and Frisch (1986),
in a morphological comparison of domestic sheep and
goats, have drawn attention to numerous invariabilities in the postcranium (including the calcaneum) of
European domestic breeds. Indeed, our own dissections
of several domestic ewe hindlimbs revealed a configuration of skeletal, muscular, tendinous, and ligamentous relationships identical to that shown in Lanyon’s
(1973) diagram (his Fig. 1)of an ovine talocrural joint.
This evidence favors the supposition of high interindividual invariability of calcaneal strain cycles among
members of Ovis aries.
Assumption 2: Accuracy of strain gauge data
Although encouraged by the consistency of his strain
gauge results, Lanyon (1973) cautioned that the accuracy with which the gauge technique can effectively
measure in vivo bone strain has never been adequately
determined. There are, in fact, several characteristics
of the strain cycle that require confirmation. Of particular importance to our own analysis are the peak compressive and tensile strain magnitudes attained during
loading. Cochran (1972) obtained consistent results
when he compared strain magnitudes from gauges that
had been implanted in vivo on dog tibiae with in vitro
gauge measurements on the same bones removed postmortem and applied with a known load. Lanyon (1973)
employed a different postmortem calibration technique
on three of the gauges used in his study. He attempted
to leave the gauges attached only to a small pieces of
the original bone that he then applied to tensiontesting machine. The three gauges tested (S34 and S35
not among them) demonstrated ‘l. . . a linear response
t o applied strain over the range encountered in vivo,
and a faithful indication of strain direction . . .” (p. 46).
The peak in vivo microstrain’ ranges (200-300 compression, and 60-75 tension, Fig. 4 in Lanyon, 1973)
recorded for the axially aligned gauges applied to the
caudolateral and craniolateral aspects of the sheep calcanei (S34 and S35) are low when compared to maximum strain magnitudes recorded on the caudal and
cranial aspects of other long bones (at similar stride
durations), e.g., - 1205 and 760 for sheep radii (Lanyon
and Baggott, 1976), -947 and 1122 for tibiae (Lanyon
and Bourn, 1979). But given that the calcaneal shaft
has no longitudinal curvature and is primarily designed to resist cranial bending in the parasagittal
plane (having a high craniocaudal t o mediolateral dimension), it is perhaps not surprising to find such low
deformation values in the craniocaudal plane.
Another important characteristic of the strain cycle
is the wave form. Interpretation of the wave forms reported for gauges S34 and S35 has already been given.
That the wave shapes produced by the two caudolateral
gauges of these specimens are different suggests either
that strain is variable a t this position or, more likely,
that either or both of them are inaccurate. However,
the overall pattern observed in both is consistent: as
the craniolateral gauge records increases toward maximum compression, the direction of strain indicated by
the caudolateral gauge is toward maximum tension.
This “mirror image” wave form is typical for gauges
‘Strain is the ratio of the change of length of a material after loading to the original length before loading. One unit of microstrain is
equal to
units of strain. All measures of strain are given in
microstrain units.
TABLE 5. Correspondence of predicted and observed collagen fiber orientation
Calcaneal aspect
Recorded strain
High compression,
low tension
High compression,
low tension
Not measured
Equal compression
and tension
Predicted collagen
Mostly transverse
Observed collagen orientation
Mostly longitudinal
Observed CPL image
Dark (some bright)
Mostly transverse
Transverse and longitudinal
Bright and dark
Mostly transverse
Mostly longitudinal
Bright (some dark)
Dark (some bright)
Mixed longitudinal
and transverse
attached to opposite sides of long bones loaded in bending (e.g., Lanyon and Baggott, 1976, Lanyon and
Bourn, 1979). The alternating bending strain cycles
(described previously) characteristic of the calcaneal
shaft have not received independent confirmation.
flexion of one or both hindlimbs. However, if collagen
fiber ultrastructure responds to the same strain properties as do other structural features (e.g., redistribution of mass), then strain intermittency, as well as
magnitude, is an essential condition for structural response. Low stretching involves dynamic rather than
intermittent strain. This contrasts sharply with sexual
mounting, which is accompanied by pelvic and hindlimb oscillations. Dominant rams may engage in
mounting activity for extensive periods of time, especially during the beginning of estrous in females (Hulet, 1966).The degree of talocrural plantar flexion during sexual mounting by the male has not been
measured, but in such activity the hindlimbs function
to balance the bulk of the ram’s weight, thus actually
limiting the extent of plantar flexion. Conversely, during male-male head butting, the hindlimbs act to
thrust the body forward and slightly upward resulting
in pronounced talocrural plantar flexion and, presumably, high magnitudes of stress on the calcaneum. This
could help explain the predominantly dark (“tension
resistant”) lamellae found in the cranial segments of
the sheep calcaneum, but this explanation, as with the
behavior, refers only to males. Of these behaviors only
pseudosexual mounting is performed by females, but
such occurrences are rarely observed (Hafez et al.,
1962). It is therefore difficult to account for the dark
(longitudinal) lamellae found on the cranial aspect of
OVA4, a confirmed female.
Assumption 3: Experimentally measured strain represents
natural strain repertoire
To assess the correspondence properly between
strain distribution and pattern of collagen fiber orientation, a complete history of the total strain regimen
influencing collagen alignment must be attained. Incomplete strain information could lead to inaccurate
assessments. For example, the discordance between
predicted and observed collagen fiber orientation for
the craniolateral and lateral aspects of the calcaneal
shaft, as presented in Table 5, could be due to a flaw in
Gebhardt’s (1905)original hypothesis, or alternatively,
to incomplete data on the pattern of applied strain.
Lanyon (1973) recorded calcaneal strain data for locomoting sheep at four different speeds: slow walk, medium walk, fast walMslow trot, and medium trot. His
results show that peak strain magnitudes increase
slightly at each faster pace, but that the wave form
generally remains unchanged. However, members of
the genus Ovis (including domestic sheep) exhibit
many more locomotor and positional behaviors than
simply walking and trotting at variable speeds. Are
there any other kinesiological activities that have an
effect on microstructural response to functional loading? If so, and the cranial and lateral aspects of the Assumption 4: Correspondence of deep strain with
ovine test calcaneum had actually experienced high surface strain
tension during some locomotor behavior not included
However accurate, an electrical resistance strain
in Lanyon’s (1973) study, then the predicted collagen gauge measures strain only on the limited surface of
orientation might more closely match that observed.
bone directly covered by the gauge apparatus. AccordLanyon’s (1973) strain data show that the instances ing to Huiskes (1982) and Huiskes and Chao (19831,
at which the craniolateral and lateral sides of the cal- surface strains recorded using strain gauges are concaneum undergo tension correspond to maximum sistent with those predicted by finite element analysis,
talocrural flexion (both at the beginning and a t the end a computer model used to approximate the distribution
of the weight-bearing phase). Therefore, any positional of stresses and strains in structures of complex shape
behavior in sheep in which the hindlimb is loaded dur- and material characteristics, such as bone. The finite
ing maximal plantar flexion would tend to induce element method predicts that, in the case of long bones,
great tensile strain on the cranial and lateral sides. At the direction of principal strain will be similar on the
least three such motor activities have been described bone surface and deep to the surface. This finding also
for the male domestic sheep; these include low stretch- gains support from data obtained using the photoelasing, sexual mounting, and butting (Hafez et al., 1962; tic method2 of stress analysis (see Bianchi et al., 1983)
Banks, 1964; Grubb, 1974), all of which occur during
the breeding season (generally during the autumn and
‘Certain plastic materials become birefringent when loaded and
early winter months in temperate climates) and relate
observed in polarized light. By constructing and loading a plastic
to agonistic or sexual activities. Low stretching by the model
of a bone, it is possible to see lines (or fringes) of differing
ram occurs during positional behavior associated with optical intensity which reveal the trajectories of stress that occurred
pre-mating displays and involves talocrural plantar in the element during loading.
TABLE 6. Correspondence of predicted and observed collagen fiber orientation, assuming Lanyon’s “dorsal”
and lateral gauges were both cranially placed, and his “plantar” gauges were laterally placed
Calcaneal aspect
Lateral (Lanyon’s
Recorded strain
High compression,
low tension
Equal compression
and tension
Not measured
Not measured
Predicted collagen
Mostly transverse
Observed collagen orientation
Mostly longitudinal
Observed CPL image
Dark (some bright)
Equal transverse
and longitudinal
Transverse and longitudinal
Bright and dark
Bright (some dark)
Dark (some bright)
for various bone elements, including the calcaneal
shaft (Preuschoft, 1970).
Correspondence between Strain Data and Collagen Fiber
Orientation and Interpretation of Results
Potential Effects of Tissue Type on Collagen
Fiber Alignment
As noted, most correlation studies involve two components: distribution of strain and pattern of collagen
fiber orientation. Bromage (n.d.) introduced a third
variable, namely, tissue type, which is the product of a
number of factors, including origin, location, and rate
of osteogenesis. He argued that the direction of collagen fibers in bone is subject to developmental constraints and may therefore be influenced by remodeling processes. For example, results obtained by
Bromage (n.d.) for the macaque mandibular corpus
showed that bone of periosteal origin was composed
predominantly of longitudinal lamellae, whereas
lamellae of endosteal origin was primarily transverse.
This led him to suggest that tissue of endosteal origin
(under certain conditions) may be physically and developmentally constrained by the remodeling process
to lay down collagen fibers with a predominantly transverse orientation. Thus the observation made in this
and other correlation studies that there is a progressive
increase in the amount of transverse lamellae toward
the endosteal surface of the bone does not necessarily
require a functional explanation (e.g., Carando et al.,
Moreover, it would mean that both tissue type and
bone growth history need to be considered in any evaluation of the relationship between functional strain
and collagen alignment. The predominantly bright
(transverse) area of bone in the caudomedial cortex of
the sheep calcaneal shaft, for instance, may be due not
to strain stimulus but t o a concentration of compacted
coarse cancellous bone (of endosteal origin) relocated to
this position by the craniolateral drift apparent in the
diaphysis of this bone. Riggs et al. (1993a) found that
primary lamellar bone in the horse radius was composed predominantly of longitudinal collagen fibers, independent of the strain regime. Even if collagen orientation in primary cortical bone in the sheep calcaneum
is influenced by functional strain, such an effect must
have occurred during collagen deposition, on either a
periosteal or endosteal surface. Thus collagen alignment of primary cortical bone would reflect structural
response to past, rather than present, functional
Secondarily remodeled structures, however, have the
potential to respond intracortically to current loading
regimes (Lanyon et al., 1982). Yet, Bromage (n.d.) further cautioned that even secondarily remodeled osteons may in some instances be influenced by various
growth factors and the tissue type within which they
develop. The effects that developmental constraints
have on the microstructural remodeling of localized regions of bone are largely unknown, and clearly much
work is needed in this area.
Correspondence between Strain and Collagen Fiber
Orientation in Secondary Osteons
If only secondarily remodeled structures are considered, it can be seen that only the medial and lateral
aspects of the sheep calcaneum contain a significant
proportion of bright secondary osteons, whereas these
lamellae are primarily dark in all other areas of the
diaphysis. Table 5 summarizes the correspondence between the distribution of collagen fiber orientation and
strain in four sectors of the ovine calcaneal shaft. It can
be seen that in contrast to previous studies of long
bones, there is no simple correspondence between the
predicted (based on Gebhardt’s hypothesis) and the observed collagen fiber orientation.
For instance, although the strain signatures for the
craniolateral and lateral segments of the shaft are (apparently) virtually identical (see Fig. 2), CPL results
demonstrate a greater concentration of bright (transverse) lamellae on the lateral side. One way in which
this particular inconsistency can be eliminated is by
postulating that Lanyon’s (1973) dorsal (craniolateral)
and lateral strain gauges were actually both positioned
craniolaterally and that his “plantar” (caudal) gauges
were positioned laterally. This speculation is prompted
by the fact that in all of the sheep calcanei observed in
dissections, the plantar ligament completely covered
(was attached to) the caudal side of the bone and, in
fact, extended considerably up on the lateral side. Since
Lanyon (1973, p. 47) described the position of his “plantar” strain gauges as “adjacent to the [fibers of the1
plantar ligament,” it is not unreasonable to assume
that they were actually laterally, rather than caudally,
positioned. Table 6 shows a revised comparison of predicted and observed collagen orientation based on this
interpretation. However, although this eliminates certain inconsistencies (e.g., the difficulty in accounting
for the occurrence of compressive strain on the caudal
surface, and the greater than predicted amount of longitudinal lamellae on the lateral side) it raises new
ones: how to explain compression operating on the lateral aspect during a phase of tension directed cranially.
Considering only the craniolateral aspect, it can be
seen with reference to both Tables 5 and 6 that the
predicted and observed collagen fiber orientations are
inconsistent. Gebhardt’s (1905) hypothesis predicts
that the high degree of compression recorded by Lanyon (1973) on the cranial surface should result in the
formation of bright (transverse) lamellae, rather than
the dark (longitudinal) lamellae actually observed.
Proposed Modification of Gebhardt’s Hypothesis
The fact that bone, as a tissue, generally appears to
be less resistant to tensile strain than compressive
strain (Evans, 1957; Currey, 1959, 1984a,b; Yamada,
1970; also see Tables 1 and 2) may provide at least a
partial (albeit tentative) explanation for the inconsistencies between the predicted and observed results,
summarized in Tables 5 and 6. Since the ultimate
strength (and by implication, the yield point) is lower
under tension than it is under compression, the occurrence of even a small magnitude of tensile strain acting
on a localized bone volume may be sufficient to stimulate (by as yet unknown processes) the formation of
longitudinal collagen fibers (which are purportedly
better suited to resist tension), even when the same
bone region is undergoing greater compressive strain
during another phase of the locomotor cycle.
This “tension-resistance priority’’ (TRP) hypothesis
gains some support from several studies involving compound strain. Bromage (n.d.) found that collagen fibers
along the inferior border of the macaque mandibular
corpus were aligned predominantly in a longitudinal
(tension-resistant) direction even though this region is
subject to both tension and compression during different phases of the various masticatory cycles. Hobby et
aI. (in prep.) found that sectors of the macaque femoral
diaphysis that appear to have been loaded in both compression and tension are also composed of longitudinal
collagen fibers.
Findings from other studies, however, contradict the
TRP hypothesis. Portigliatti Barbos et al. (1995) have
reported that the anteromedial surface of the distal
portion of the human tibia1 shaft, which was made up
primarily of transverse lamellae, is subject “mainly” to
compression (which implies at least a small magnitude
in the direction of tensile strain). Bromage (n.d.) has
also reported findings of this type with respect to several localized areas of the macaque mandible. Indeed,
our own results demonstrate the occurrence of both
tensile strain and a high proportion of bright (compressive resistant) lamellae on the lateral side of the ovine
calcaneum (this holds true for both Tables 5 and 6 results). Thus by proposing that collagen fibers will align
preferentially to resist tensile strain, when both tension and compression are alternately acting on bone
tissue, we can account for some but not all of the observed inconsistencies in Gebhardt’s hypothesis.
The particular ultrastructural response (i.e., the direction in which collagen fibers are laid down) to varying magnitudes of tensile strain, acting as part of a
compound loading regimen, may be dependent on other
mechanical and physiological properties of bone in a
localized area. This “holistic response” is consistent
with recent findings that indicate that both macrostructural and microstructural features of bone function together to maintain a constant strain environment in the face of changing load regimes, both
throughout ontogeny (Biewener et al., 1986) and phylogeny (Rubin and Lanyon, 1985). Viewed in this way,
the longitudinal alignment of collagen fibers observed
in the craniolateral aspect of the ovine calcaneum may
function to preserve Young’s modulus of elasticity in a
direction optimally suited to the local loading environment. In other words, collagen orientation (and other
microstructural features) in bone may be developmentally constrained to contribute to the maintenance of
local strain regimes in combination with macrostructural properties. More work on the role of bone growth
and development, and on the interactions among the
mechanical properties of various bone structures (both
at the micro and macro level) is needed before Gebhardt’s (1905) hypothesis can be adequately modified
and placed within the wider context of the relationship
between bone structure and function.
Following is a summary of the conclusions reached in
this study.
1. Collagen fiber alignment in the diaphysis of the
sheep calcaneum is characterized by the following
properties. There is a progressive increase in the density of bright (transverse) lamellae proceeding from the
exterior surface to the interior of each section, with the
exception that some outer circumferential lamellae are
bright. Bright lamellar “rings” around the perimeter of
otherwise dark osteons were a common occurrence.
There was little interindividual variation in the regional pattern of bright and dark secondary osteons
among the cross-sectional specimens observed. The
general pattern (as shown in Table 5) was characterized by the presence of mostly longitudinal (dark) osteons in the craniolateral and caudolateral aspects of
the shaft, mostly transverse (bright) osteons on the medial side, and a combination of transverse and longitudinal osteons laterally.
2. Reinterpretation of Lanyon’s (1973) published
strain data for the ovine calcaneum, recorded in vivo
during normal locomotion, indicates that this bone acts
as a lever with alternating bending cycles.
3. Correlative studies of the type presented here rely
on a number of assumptions that are rarely, if ever,
stated or explored. Many of these involve the assumed
accuracy with which we know (or think we know) the
strain histories of the skeletal elements on which collagen fiber orientation analysis is undertaken. The following questions need to be addressed in correlative
studies: What is the effect of interindividual variation
of strain pattern on the external validity of the study
results? How can we determine the accuracy of strain
measurement or inference techniques? Is experimentally measured strain representative of the naturally
experienced strain (should the ethological literature
pertaining to mechanical movement be consulted)?
4.Both tissue type and bone growth history need to
be considered in any evaluation of the relationship between functional strain and collagen alignment: (1) tissue type (which reflects the mechanisms of bone remodeling) is a potential variable affecting the
orientation of collagen fibers, and (2) since bone tissue
is deposited only on surfaces, collagen fibers of primary
bone deep to the surface may have been laid down under different strain conditions from that experienced on
the existing surface of the bone. Thus not only must
one consider the remodeling history but also the strain
history acting on the bone.
5. If our assumptions and interpretations are correct,
then at least some of our results are inconsistent with
Gebhardt’s (1905) original hypothesis. For example,
the craniolateral side of the sheep calcaneum, which
clearly exhibits much greater magnitudes of compression than tension, should, according to Gebhardt, exhibit collagen fibers aligned predominantly transversely (bright under CPL). Yet this sector of the
calcaneum consistently exhibits predominantly longitudinal (dark under CPL) collagen fibers.
6.The results reported here indicate that Gebhardt’s
hypothesis (1905) may require modification. Two hypotheses are proposed to account for the observed inconsistencies between reported and predicted results.
The “tension-resistance priority” hypothesis states
that the occurrence of even a small magnitude of tensile strain acting on a localized bone volume may be
sufficient to stimulate the formation of longitudinal
collagen fibers, even when the same bone region is undergoing greater compressive strain during another
phase of the locomotor cycle. The “holistic response”
hypothesis holds that collagen fiber orientation functions to contribute to the overall maintenance of
Young’s modulus in combination with other microstructural and macrostructural properties. These hypotheses are tentative and require further systematic
This research was supported, in part, by the Horserace Betting Levy Board (A.B.), and by a PSC-CUNY
Faculty Award of the City University of New York
(T.G.B.). Research facilities used in this study are courtesy of an NSF grant to the New York Consortium in
Evolutionary Primatology (NYCEP). The authors wish
to thank Professor F.S. Szalay for contributing the dry
bone specimens. The original manuscript was improved by the helpful comments of three anonymous
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fiber, orientation, ovina, patterns, strait, induced, relations, locomotor, shaft, collagen, calcaneal
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