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Rheumatology Advance Access originally published online on August 5, 2006
Rheumatology 2007 46(2):246-249; doi:10.1093/rheumatology/kel263
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© 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

Lack of bone stiffness/strength contribution to osteoarthritis—evidence for primary role of cartilage damage

B. M. Rothschild1–4 and R. K. Panza3,*

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

Correspondence to: Bruce M. Rothschild, Arthritis Center of Northeast Ohio, 5500 Market Street, Youngstown, OH 44512, USA. E-mail: bmr{at}neoucom.edu


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
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
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Acknowledgements
 References
 
Osteoarthritis is the most common form of arthritis in humans [1–3]. While there have been significant advances in the understanding of its biochemistry [4–6], application of these perspectives 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 de Margerie [26] suggested as a stiffness/strength (torsion-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
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Acknowledgements
 References
 
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), 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.


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

 
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 diarthrodial 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 variation [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 {pi}. 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 250° 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
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Acknowledgements
 References
 
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 thinness 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.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Acknowledgements
 References
 
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 pneumatization 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 modification 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 histological 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.

Formula


   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
References
 
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.


   Notes
 
*The corresponding author verifies that the co-author has contributed to the work but that the author is non-contactable. Back


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 

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