Abstract
The current study is to distinguish between osteochondrosis and osteochondritis, utilizing surface microscopy of individuals with documented pathology. Osteochondrosis is associated with smooth borders and gradient from edge to defect base, while osteochondritis and subchondral impaction fractures are associated with subsidence of the affected area of articular surface with irregular edges. The base of osteochondrosis is penetrated by multiple channels, smoothly perforate its surface, indistinguishable from unfused epiphyses, confirming their vascular nature. This study provides a technique for distinguishing osteochondrosis and osteochondritis and further documents of the value of epi-illumination microscopy in expanding our understanding of bone and joint disease.
Keywords: Subchondral impaction fractures, Bone modification, Vascular supply, Epiphyses, Epi-illumination microscopy
1. Introduction
1.1. Controversy
Osteochondrosis and osteochondritis, common causes of lameness, are terms often used interchangeably, but actually describe very different phenomena.1, 2, 3, 4, 5, 6 Osteochondrosis is the term applied to free cartilage bodies,7 related to specific joint defects.8 Ytrehus et al.9 (2004) and Olstad et al.10,11 suggested a role for vascular compromise during embryogenesis/development in osteochondrondrosis. This suggested role contrasts with König's12 application of the term osteochondritis dissecans to loose bodies resulting from subchondral knee fractures. Note use of the term “dissecans”, derives from the Latin term dissecare, which means “to separate”. The terminology becomes even more convoluted, as osteochondritis (at least of the knee) was once considered a form of avascular necrosis (AVN),13, 14, 15 with debate about the primary or secondary nature of the AVN.16 However, subsequent analysis has revealed that the pathology is actually that of subchondral fractures.2,5,6,16, 17, 18, 19, 20, 21, 22, 23 Subchondral fractures are found with repetitive impact injuries.3,23,24 This finding is in contrast to osteochondritis related to infection, a subject beyond the scope of the current analysis.25
1.2. Subchondral collapse
Collapse of subchondral bone is also a complication of AVN,15 but which is primary? AVN occurs in watershed regions where compromise of circulation restricts nutritional supply to the portion of bone served by that (those) vessel(s).26 The distribution of trauma-related (whether acute or repetitive) subchondral fractures is independent of vascular watersheds.6,27,28 Recognition that human knee “osteochondritis” distribution does not follow watershed vascular patterns led to revised perspectives.9,29 AVN is also a complication typically of corticosteroid use and decompression syndrome in humans.30,31 However, in the absence of those risk factors, AVN is not responsible for the damage in human knees.21
1.3. Vascular considerations
The character of the subchondral bone-cartilage interface has been subject of much discussion, with some authors describing macroscopic surface “porosity,”32 which is a claim that has subsequently disputed.33 Madry et al.15,p.420 noted it is the “cortical lamella directly underneath the radiologically discernible joint space” which is recognized macroscopically. Subchondral vasculature invades the calcified zone, but the tidemark is not penetrated.15,34,35 Moreover, Hoemann et al.36,p.2 stated epiphyseal bone expands “into the cartilage anlage until the interface forms a calcific layer that arrests vascular invasion”. Because osteochondrosis is perceived as failure of cartilage maturation, we hypothesize that vascular channels should be recognized, similar to those structures expected at the metaphyseal surface adjacent to unfused epiphyses.36
1.4. Goal of study
The current study was conducted: 1) to test the vascular channel hypothesis as to the characteristics of the surface of unfused epiphyses and to distinguish between the nature of osteochondrosis and osteochondritis/subchondral impaction fractures at a resolution several orders of magnitude greater than macroscopic or x-ray evaluation; and 2) to identify additional clues that would allow distinguishing between osteochondrosis and osteochondritis.
2. Material and methods
2.1. Sample selection for unfused epiphyses and tibial plateau collapse
All 23 individuals under age 17 with unfused distal tibial epiphyses, as well as adults with subchondral tibial plateau segmental collapse and other subchondral defects are selected for evaluation from the 2906 early 20th century individual human skeleton component of the Hamann-Todd (HT) Collection of the Cleveland Museum of Natural History (Cleveland, Ohio, USA).37 Individuals with tibial plateau fractures are identified from the HT database (L. Jellema, personal communication).
2.2. Sample selection for osteochondrosis
Phalanges with proximal articular surface defects, previously identified as caused by osteochondrosis,38 are selected from the Dinosaur Provincial Park hadrosaur collection of the Royal Tyrrell Museum of Palaeontology (TMP) (Drumheller, Alberta, Canada). The paleontological collections of the Carnegie Museum of Natural History (Pittsburgh, Pennsylvania, USA) and the Peabody Museum of Natural History at Yale University (New Haven, Connecticut, USA) are surveyed for phalangeal impact fractures.
2.3. Rationale and validation for trans-phylogenetic sample selection
As osteochondrosis and impact fractures are not catalogued in the HT collection and given the documented validity of trans-phylogenetic (e.g., mammal and reptiles, including dinosaurs) comparisons for diseases which affect bone,39, 40, 41 previously documented osteochondrosis cases38 in the TMP collection are chosen to provide an epidemiologically-derived sample. Utilization of a trans-phylogenetic source (i.e., dinosaurs) is valid, because of documentation that the character and skeletal distribution of affliction by a given disease are between human and veterinary collections (was trans-phylogenetically reliable) and, indeed, through geologic time in the fossil record.40,42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60
2.4. Criteria for recognition of pathology
Subchondral fractures are macroscopically recognized on the basis of focal irregular or linear depressions in articular surfaces. Focal defects are distinguished from erosions because of absence of new bone formation or presence of exposed unremodeled, underlying trabeculae (in the absence of taphonomic alterations).61 Impact fractures are recognized on the basis of tibial plateau collapse.23,24,62 Osteochondrosis is recognized on the basis of regular, smooth-bordered articular surface defects in absence of new bone formation.38,63, 64, 65
2.5. Examination technique
Epi-illumination microscopy is pursued on the surface of unfused distal tibial epiphyses, human tibial plateaus (both normal or containing subchondral defects), and dinosaur phalangeal defects using a white light-emitting diode (LED) (Dino-lite digital microscope (AM7915MZT, Dunwell Tech, Inc, 19803 Hamilton Ave. #200, Torrance, CA 90502) with polarizing optics to characterize the nature of macroscopically recognized cortical discontinuities.
3. Theory/calculation
Osteochondrosis and osteochondritis are very different phenomena which can be distinguished macroscopically on the basis of the characteristics of the edges of the lesions and microscopically (surface magnification) on the basis of presence or absence of vascular channels.
Beyond clarification of the differences between the phenomena, this study provides greater clarity in recognition of tibial plateau fractures.
4. Results
4.1. Defect border characteristics
Defects are identified in: 1) 20 hadrosaur phalanges; 2) impact fractures in Diplodicus (sauropod) and Othnielosaurus (ornithischian dinosaur); and 3) osteochondritis-related surface defects in 10 humans. Use of epi-illumination microscopy reveals sharply defined borders in both osteochondrosis and osteochondritis. However, what distinguishes between osteochondrosis and osteochondritis is the nature of that border. Osteochondrosis in all so afflicted individuals is associated with a smooth gradient from the edge to the defect base (Fig. 1, Fig. 2), while lesions of osteochondritis and subchondral impaction fractures in all afflicted individuals is associated with “step off” subsidence of the affected area of articular surface (Fig. 3, Fig. 4). The border of osteochondrosis is smoothly elliptical in shape (Fig. 1, Fig. 2), while the edges of osteochondritis defects are irregular (Fig. 3, Fig. 4, Fig. 5).
Fig. 1.
Enface view of hadrosaur TMP 67/9/61 articular surface of proximal phalanx. Osteochondrosis is associated with a smooth gradient from the edge to the defect base. The borders of osteochondrosis are smoothly elliptical in shape. A. 20x. B. 200x.
Fig. 2.
Enface view of HT 1204 osteochondrosis associated with the tibial plateau. A. Global view of tibial plateau. B. 200x. Multiple channels perforate exposed surface.
Fig. 3.
Enface view of HT 1149 tibial plateau. A. 20x. B. 50x. C. 200x. “Step off” subsidence of the affected area of articular surface in osteochondritis/subchondral fracture. The edges within the defect are irregular, and the base (visible articular surface) is indistinguishable from the appearance of unaffected adjacent bone.
Fig. 4.
HT 1198 tibial plateau fracture. A. Enface view. B. 200x. Note area of exposure of underlying trabeculae. C. Medial view.
Fig. 5.
Enface view of distal surface of proximal Diplodicus CM 42699 phalanx. A. Global view. B. 200× magnified view. Note crack and irregular surface from impact fracture, but no vascular perforations.
4.2. Fractures and taphonomy
Taphonomic loss of medial metaphyseal surface in one individual clearly documents that the surface subsidence is due to a fracture (Fig. 4). The base (visible articular surface) of subchondral impaction fractures/osteochondritis is indistinguishable from the appearance of unaffected adjacent bone (Fig. 3, Fig. 4). There is no significant alteration of the articulating surface of the affected bone fragment, unless taphonomically-exposed (e.g., by drawer damage breaking off the most external portion of subchondral bone) (Fig. 6).
Fig. 6.
Enface view of HT 2141 tibial plateau. A. 50x. B. 200x. Taphonomically-exposed subchondral trabeculae.
4.3. Characteristics of lesion base
The base of osteochondrosis has a very different appearance (Fig. 1, Fig. 2). It is penetrated by multiple channels, which smoothly perforate its surface. No new bone formation is recognized. Compare these findings to the appearance of distal tibial epiphyses (Fig. 7) in 23 individuals ranging in age from 6 months to 13 years, with tibial lengths ranging from 57 to 261 mm.
Fig. 7.
Enface view of HT 2370 distal tibial epiphysis at 200× magnification. Multiple channels perforate exposed surface.
4.4. Epiphyses
The appearance of epiphyses at 200× magnification is independent of age or growth (measured by length). The microscopic appearance of epiphyseal surfaces remains consistent and indistinguishable from the noted appearance in the base of osteochondrosis defects.
The caveat to microscopic recognition of osteochondrosis is the appearance of juvenile dinosaur bone. Smaller, less advanced dinosaurs (e.g., Othnielosaurus) are characterized by indeterminate growth, in contrast to determinate growth in larger more advanced species (e.g., Diplodicus).44 The reptilian equivalent of the mammalian epiphysis shares similar vascular penetration pattern (Fig. 8), which is a pattern that appears to be lost, or at least greatly diminished, in older individuals.
Fig. 8.
Enface view of proximal surface of Othneilosaurus phalanx YPM VP 001882. A 20x. B. affected area at 50 x. C. Affected area at 200x. D. Normal subchondral bone in juvenile dinosaur. Note vascular channels in contrast to B and C with subsided bone has lost vascular connections.
5. Discussion
Osteochondrosis and osteochondritis have characteristics which facilitate distinguishing between them macroscopically. Osteochondrosis is characterized as being elliptical with smooth borders, while the borders in osteochondritis are rough and irregular. It is the magnified view, however, that distinguishes between them and their pathophysiology clearly. Microscopic examination revealed that the base of osteochondrosis lesions has an appearance unique for articular surfaces. Because osteochondrosis is the result of failure of articular cartilage to calcify, the subchondral bone at that location focally retains its vascular continuity to overlying cartilage, which is normally lost with calcific maturation of overlying cartilage. This trait is indistinguishable from the appearance of epiphyseal bone-cartilage boundaries as manifest by epiphyseal junctions. Holmdahl and Ingelmark's66,p.157 perspective that “canal-like contacts between the articular cartilages and the medullary cavities of epiphyses” explains the “pores” seen on examination of both unfused epiphyses and the base of osteochondrosis lesions.
The articular surface of osteochondritis/subchondral fractures is indistinguishable from the appearance of normal bone. Part of the confusion in the literature may relate to a failure to recognize that the osteochondral junction is not the same as the tidemark separating calcified from non-calcified articular cartilage.15 Therefore, perforations in the osteochondral junction do not relate to the surface changes in bone in which soft tissues are no longer present.15,66, 67, 68 Vascular supply penetrates epiphyseal plates, which do not possess tidemarks related to joint cartilage.69 Thus, juvenile dinosaurs appear to preserve the penetrating vascular pattern that appears specific for osteochondrosis in mammals. However, the nature of the defect edge still appears to distinguish osteochondrosis from osteochondritis in those juvenile individuals with indeterminate growth. Interestingly, the subsided fracture (osteochondritic) region has lost its surface canals, which is a subject for future consideration.
6. Conclusions
Osteochondrosis and osteochondritis are very different phenomena which can be distinguished macroscopically on the basis of the characteristics of the edges of the lesions and microscopically (surface magnification) on the basis of presence or absence of vascular channels.
This study further provides documentation of the value of epi-illumination microscopy in expanding our understanding of bone and joint disease. Future study of effect of disease on the surface of subchondral bone will be of interest.
Declaration of competing interest
There are no conflicts of interest.
Acknowledgements
Appreciation is expressed to Amy Henrici, Lyman Jellema, Darren Tanke and Gregory Watkins-Colwell for facilitating access to the collections they curate.
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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