Rheumatology 2007;46:246–249 doi:10.

1093/rheumatology/kel263
Advance Access publication 5 August 2006

Lack of bone stiffness/strength contribution to

osteoarthritis—evidence for primary role of cartilage damage
B. M. Rothschild1–4 and R. K. Panza3,*

Objectives. This study was performed to assess osseous contributions to osteoarthritis, obviating the analysis challenges
presented by confounding factors in humans and rarity of osteoarthritis in free-ranging mammals.
Methods. Frequency of osteoarthritis in 21 bird species was examined and contrasted with measures of afflicted element bone
stiffness and strength and compression/tension-resistant characteristics.
Results. Osteoarthritis was present in the ankle of 0–16% of bird species analysed, independent of bone laminarity, cortical
thickness, circularity, polarization, cross-sectional diameter, length and pneumatization.
Conclusions. No correlation of frequency of osteoarthritis with parameters of bone strength and biomechanical parameters was
found, suggesting that bone is only secondarily affected in osteoarthritis and that cartilage is the initial target of the disease.
KEY WORDS: Osteoarthritis, Animal model.

Introduction de Margerie [26] suggested as a stiffness/strength (torsion-

Osteoarthritis is the most common form of arthritis in humans
[1–3]. While there have been significant advances in the under-
standing of its biochemistry [4–6], application of these perspec-
tives has not yet been demonstrated to significantly affect disease
progression. Biomechanical factors are thought to have a primary
role in the development of osteoarthritis [7–9], but which ones?
Abnormalities are found in both cartilage and bone [6, 9]. One of
the basic questions has been which tissue is primarily affected [10,
11]. Does bone damage with stiffening predispose to cartilage
damage or is it the alterations in cartilage that produces the
subchondral sclerosis [12–14]? The question has been difficult to
answer because of the complexity of confounding factors in
humans, rarity in free-ranging mammals and artificiality of
captive-mammal studies [10, 11, 15–18]. However, birds offer a
unique opportunity to address some of these questions. The bird
hock or ankle joint is homologous with the human knee, both
morphologically and functionally [19–26]. The similarity of the
bird ankle (distal tibiotarsus) and human knee (distal femur) is so
great that the one has often been mistaken (by non-ornithologists)
for the other. Osteoarthritis is common in bird hock (analogous in
morphology to the human knee) joints with significant variation
in species susceptibility (and thus lifestyle) [19], and the frequency
of osteoarthritis is independent of weight [20].
Currey [21] and Meers [22] examined general correlation
between long-bone cross-sectional structure and biomechanical
environment, while Cubo and Casinos [23, 24], Skedros et al. [25]
and de Margerie et al. [26] specifically studied those relationships
in birds. The latter group was one of the first to examine
biomechanical significance of bone histology. They and de
Ricqles et al. [27] noted that highly vascularized, fast-growing
fibrolamellar cortex characterized the long bones of medium and
larger adult birds. The three groups defined laminar bone on
the basis of vessels paralleling the periosteal surface, a feature
resisting) feature.
Torsion resistance decreases as cross-sectional circularity is
replaced by shapes less resistant to bending (e.g. ellipse), in
contrast to compressive or tensile loading, in which cross-sectional
area is the defining factor [28]. Torsion resistance also increases as
a function of diaphyseal diameter and cortical thinness [28, 29]
within elastic instability (buckling) limitations [21, 28]. The latter
occur with very long bones or very thin cortices.
Oblique orientation of collagen fibres is another mechanism
of torsion resistance. Collagen fibre orientation is recognizable
microscopically because of their greater anisotrophy [26], resulting
in greater transmission of polarized light [30].
Distinguishing between tension and compression resistance
has been suggested on a histological basis, with longitudinally
oriented collagen fibres in the former and transversely aligned
fibres in the latter [31, 32]. Lee [33] and McMahon et al. [34]
suggested that longitudinally oriented fibres might also act to
‘withstand possible reversal of bending loads’ [35].
Methods
Birds species, selected to provide a range of sizes (200 g to 10 kg)
and morphotypes (e.g. hawks, partridges, ducks and swans), were
analysed for contribution of stiffness and strength, as measured
by torsion resistance, to occurrence of osteoarthritis. The distal
tibiotarsi (hocks) of adult birds of selected species (Table 1) were
examined from the following collections: Academy of Natural
Sciences of Philadelphia (ANSP), Pennsylvania; American
Museum of Natural History (AMNH), New York City, NY;
Carnegie Museum (CM), Pittsburgh, PA; Cleveland Museum of
Natural History (CMNH), Ohio; Field Museum of Natural
History (FMNH), Chicago, IL; Los Angeles County Museum
(LACM), Los Angeles, CA; Michigan State Museum (MSU),

1
Arthritis Center of Northeast Ohio, 5500 Market, Youngstown, OH 44512, 2Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44512,
3
Carnegie Museum of Natural History, 4400 Forbes Ave, Pittsburgh, PA 15213 and 4Dyche Hall, University of Kansas Museum of Natural History,
Lawrence, KS 66044, USA.

Submitted 31 January 2006; revised version accepted 27 June 2006.

Correspondence to: Bruce M. Rothschild, Arthritis Center of Northeast Ohio, 5500 Market Street, Youngstown, OH 44512, USA.
E-mail: bmr@neoucom.edu
*The corresponding author verifies that the co-author has contributed to the work but that the author is non-contactable.
246
ß The Author 2006. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org
 Bone not primary in osteoarthritis 247

TABLE 1. Frequency of osteoarthritis as a function of measures of tibiotarsal resistancea

Cross
Examined Cortical Polarized Polarized section
Species (wingspan) Common name (afflicted) Laminarity thicknessb Circularity fibrolamellar endosteal (mm2) L/Dc
Accipiter nisus (28–38 cm) Eurasian sparrowhawk 31 (16.1%) 0.125 0.273 0.862 78 104 2.4 22.3
Uria aalge (40–43 cm) Common mure 63 (11.1%) 0 0.449 0.781 69 179 7.0 23.1
Scolopax rusticola (33–35 cm) Eurasian woodcock 27 (11.1%) 0.375 0.296 0.921 86 204 3.3 21.9
Perdix perdix (30 cm) Gray partridge 31 (9.6%) 0.500 0.358 0.945 100 184 4.7 21.3
Falco tinnunculus (31–35 cm) Common kestrel 58 (8.6%) 0.400 0.276 0.879 96 217 3.1 20.3
Tyto alba (33–35 cm) Common barn owl 82 (8.5%) 0.250 0.247 0.907 68 203 6.0 21.7
Fulica atra (43 cm) Common coot 34 (5.9%) 0 0.404 0.855 62 107 6.3 27.6
Asio otus (35–37 cm) Northern long- eared owl 39 (5.1%) 0.571 0.227 0.856 94 198 3.9 22.3
Macronectes giganteus (86–99 cm) Southern giant petrel 22 (4.5%) 0 0.403 0.851 69 187 29.9 23.3
Phalacrocorax carbo (80–100 cm) Great comorant 26 (3.8%) 0.375 0.286 0.800 82 201 15.6 17.3
Alca tarda (186–204 cm) Razorbill 26 (3.8%) 0 0.459 0.896 55 110 3.8 25.3
Podiceps cristatus (46–51 cm) Great crested grebe 39 (2.6%) 0 0.501 0.751 75 123 9.4 24.0
Buteo buteo (51–57 cm) Eurasian buzzard 52 (1.9%) 0.167 0.296 0.886 97 223 8.0 19.4
Anas clypeata (44–52 cm) Northern shoveler 107 (0%) 0 0.379 0.936 75 195 3.9 23.3
Anas platyrhynchos (50–65 cm) Mallard duck 120 (0%) 0.500 0.372 0.890 98 226 7.8 22.2
Aythya fuligula (40–47 cm) Tufted duck 82 (0%) 0 0.570 0.886 57 167 4.9 25.3
Cygnus olor (125–155 cm) Mute swan 105 (0%) 0.449 0.904 186 53.1 20.7
Larus fuscus (137 cm) Lesser black-backed gull 50 (0%) 0 0.419 0.886 73 8.6 25.6
Procellaria Aeqquinoctialis (130–140 cm) White-chinned petrel 31 (0%) 0 0.345 0.887 59 131 9.7 21.5
Diomedia melanophris (83–93 cm) Black-browed albatross 22 (0%) 0.125 0.312 0.868 60 191 19.2 22.5
a
Derived from reference [35].
b
As percentage of diameter.
c
Ratio of tibiotarsal length to mid-diaphyseal diameter.

East Lansing, MI; Service et Museé cantonal d’Archéologie,
Laboratoire d’Archéozoologie (SAN-FA), Neuchâfel,
Switzerland; Natural History of Berne (NHMBE), Switzerland;
Royal Ontario Museum (ROM), Toronto, Canada; Science
Museum of Minnesota (SMM), Minneapolis, MN; United
States National Museum (USNM), Washington, DC; University
of California at Berkeley (MVZ); University of Manitoba (UM),
Winnipeg, Canada; University of Michigan (UMMZ), Ann
Arbor, MI; University of Winnipeg (UW), Winnipeg, Canada,
and Yale Peabody Museum (YPM), New Haven, CT.
Macroscopic closure (fusion) of peripheral epiphyses was accepted
as evidence of maturity. All tibiotarsi were surveyed for visible
evidence of articular and periarticular joint pathology.
Osteoarthritis was identified on the basis of synovial-lined joint
spur (osteophyte) formation [17, 18, 36–46]. While the utility of
clinical findings has been documented for diagnosis, the diarthro-
dial joint osteophyte is the structural finding documented to be
specific to the diagnosis of osteoarthritis [36–38]. Separate
examination by both authors of a subset of 300 individuals
revealed consensual agreement for two individuals and only one
discrepancy, and that individual was considered equivocal.
Severity of osteoarthritis is indicated by joint space loss, not by
osteophytes size [17, 18, 36–46]. In the absence of soft tissues,
affected joints were examined for eburnation (the only and most
severe marker of osteoarthritis severity and the pentultimate).
Given termination of skeletal growth in birds on achievement of
adulthood and minimal intraspecific skeletal measurement varia-
tion [21, 29], the skeletal pararmeters of individuals from the
delineated species (Table 1) were defined as per de Margerie et al.
[35] and Cubo and Casinos [23, 24]. Polarizing microscopy was
utilized to analyse histological details. Laminarity was defined on
the basis of extent of mid-diaphyseal cross section in which vessels
were oriented parallel to surface along entire circumference, with
values of 0 for total absence of any lamellar component and 1
when all cortical bone was lamellar. Circularity was defined on the
basis of directly measuring the area of the mid-diaphyseal cross
section and the penultimate cross sectional diameter. The cross-
sectional area was multiplied by 4 and divided by . The square
root of the result of that calculation was divided by the
penultimate diameter to provide the circularity index, with 1
representing a perfect circle. The ratio of internal cortical diameter
(bone marrow occupied or pneumatic space) to external cortical
diameter defined the cortical index. Subtracting this index from 1
provides the percentage of bone volume contributed by the cortex,
as indicated in Table 1. Fibrolamellar collagen fibre orientation
was revealed by polarizing light graded 0 to 2508 at the midpoint
of the cortex and in the peri-medullary portion. Collagen fibre
orientation was not recorded if more than 50% of cortex manifest
Haversian remodelling. Pneumatization (air containing character
of some bird bones, perceived as a modification of weight
reduction for flight) was recorded on the basis of presence or
absence of hollow bone status.
Regression analyses were performed to determine significance
of variation between frequency of observed osteoarthritis and
laminarity, cortical thickness, circularity, polarization, cross-
sectional diameter, length and pneumatization.
Results
Osteoarthritis in the form of osteophytes was found in 0–16.1% of
tibia examined, limited in distribution to the hock joint, which is
morphologically and functionally analogous/homologous to the
human knee [19–26]. Eburnation was not found. Birds are listed in
Table 1 according to diminishing frequency of osteoarthritis
(bilaterally expressed in 90%, independent of species).
Relationship of frequency of tibiotarsal osteoarthritis to
laminarity, cortical thickness, circularity, polarization, mid-
diaphyseal cross-sectional diameter and length is also delineated
in Table 1. Following the diminishing frequency of osteoarthritis
among the groups in the table, it is clear that there is no
relationship to bird size (as manifest by wingspan) or morphotype
(as illustrated by common name). Measures of resistance to
torsion, including circularity, diaphyseal diameter, cortical thin-
ness and collagen fibre orientation were independent of rate of
occurrence of osteoarthritis (Table 1).
Measures of tensile loading (e.g. cross-sectional area) were
also independent of rate of occurrence of osteoarthritis (Table 1).
No correlation with any of these values was noted.
248 B. M. Rothschild and R. K. Panza
Discussion
Birds provide a unique model for study of osteoarthritis. Other
pathologies are so infrequent (broilers excepted) that confounding
disease (e.g. infection and neoplasia) influences are almost non-
existent [47]. The analogous and homologous character of the bird
hock or ankle joint to the human knee, both morphologically
and functionally [19–26], makes it the ideal joint for study of
osteoarthritis. The tremendous variation (0–16% of various bird
species in this study) in species susceptibility to osteoarthritis [19]
and the great number of bird species available for study provides a
unique opportunity to better study and understand osteoarthritis.
The range of bird sizes from 200 g to 10 kg allowed that frequency
of osteoarthritis is actually independent of weight [20]. The lack of
correlation of frequency of osteoarthritis with weight, even within
the same genera (e.g. hawks), suggests that impact force is not
a prime factor in osteoarthritis development, at least in birds.
Lack of correlation among phylogenetic families suggests that
habitat effects are also limited in birds. One could speculate that
perceived relationships in humans [7, 8, 11] are actually the result
of a confounding factor, ligamentous laxity and hence joint
instability [20]. There was no evidence of tibiotarsal pneumatiza-
tion in any of the species studied [35, 48]. The lack of correlation
with tibiotarsal pneumatization additionally addresses the weight
question, as pneumatization is considered a modification for
weight reduction for flight. Presence or absence of this modifica-
tion did not impact frequency of osteoarthritis, again suggesting
that weight is not the issue.
The current analysis addresses another highly characteristic
variable in birds, morphotypes. Hawks, partridges, ducks and
swans, to name only a few, have very different body types [23–26].
Such variation is reflected in leg morphology, and is thus
amenable to analysis of its relationship to occurrence of
osteoarthritis. As analysis of gross structure characteristics has
not identified a significant factor contributing to osteoarthritis
[20], it seemed reasonable to examine the contribution of histo-
logical variation in pertinent skeletal elements among the bird
species. That analysis examined factors that define bone resilience
and thus potential resistance or predisposition to osteoarthritis.
It is clear that measures of torsion resistance to compression
(e.g. circularity, cortical thinness, diaphyseal diameter and
collagen fibre orientation) and tensile loading (e.g. cross-sectional
area) [28–30] do not correlate with frequency of osteoarthritis.
Indeed, the effectiveness of longitudinally oriented fibers in
withstanding bending loads [33–35] does not seem an important
factor in development of osteoarthritis. Lack of correlation of
frequency of osteoarthritis with cortical laminarity, thickness,
diameter, length or obliquity of collagen fibres (as measured by
polarizing anisotropy) all independently support the conclusion
that bone stiffness and strength are not defining parameters for
development of osteoarthritis [21, 23–26, 28, 29, 33–35, 48]. Those
studies analysed bone characteristics. The current study appears
to be the first to actually apply this approach to examining bone
strength and resilience as risk factors for development of
osteoarthritis. Lack of relationship of anisotropy to frequency
of osteoarthritis further suggests [31, 32] that resistance to
tension or compressive forces is also not a major factor in
development of osteoarthritis. This is parsimonious with the
observations of Mkukuma et al. [14], who found that the
character of mineral unit-cell dimensions and crystallite sizes
was not a factor in osteoarthritis.
These analyses suggest that bone is only secondarily affected
and that the primary target organ of osteoarthritis is cartilage.
Bone influences may relate more to joint stability [11]. Among the
factors impacting the cartilage is the effect of torque related to
rotational deformity of joints (rather than of the component
bones) [49]. Clearly, bone parameters pertinent to development of
osteoarthritis have yet to be documented in birds, and further
studies are indicated.
Key messages
Rheumatology
 Bone is only secondarily affected in
osteoarthritis.
 Birds represent a valuable new model for
osteoarthritis.
Acknowledgements
Appreciation is expressed to Drs. Laura Abraczinskas, Christine
Blake, Carla Cicero, Christopher Conroy, Alfredo Coppa, James
Dean, Kimball Garrett, Marcel Guentert, Janet Hinshaw, Robert
Hobson, Georges Lenglet Brad Livezey, Mike MacKinnon,
Timothy Matson, Werner Mueller, Glen Murphy, Dick
Oehlenschlager, Storrs Olson, Richard Plum, Rivka Rabinowitz,
Nate H Rice, Dave Steadman, Paul Sweet, Wim Van Neer, Greg
Watkins-Colwell, Tom Weber, Wim Wendelen, David Willard
and Kristof Zyskowski for facilitating access to the collections
they curate.
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