Asilomar and the alligator TMJ

Last Thursday and Friday a subset of the UCD anatomic pathology resident crew attended the CL Davis Foundation West Coast Veterinary Pathology annual conference at Asilomar, on the coast in Pacific Grove, CA.

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Asilomar State Park Conference Grounds

Together with the attending UCD vet students, we made up more than half of the body of presenters. My case presentation concerned an alligator with a laundry list of ailments, but the slide I submitted for review was a transverse section of the articular process of the quadrate bone of the skull. This process is a condyle that articulates with the articular bone of the caudal mandible to form the 'jaw joint' of the crocodilians.

While you might be stellar and recall the list of criteria that makes a creature cool enough to belong to the elite club of Mammalia, it's easy to forget that a key defining feature is the temporomandibular joint (TMJ). Known largely to the lay person as a frequent site of cranial pain, this joint is formed by the articulation of the mandibular fossa in the temporal bone and the condylar process of the mandible. Between these bones is the articular disk, which makes this joint so unique. The structure of this joint allows for both hinge and lateral motion of the joint, and enables the mammal, be it a human or a cow, to both prehend and grind his/her feed.

In contrast to we fur-bearers, our distant reptilian cousins lack an articular disk, but have an array of nifty jaw gadgetry themselves. They run the gamut from the squamates (snakes), who can ‘unhinge’ their jaw and thus swallow food several times the diameter of their head, to the crocodilians, whose craniokinesis is limited to a strict simple hinge jaw joint. Of course, for them it makes sense- why waste an iota of energy on lateral sway when you can combine the efforts of every associated cranial myofiber to snap your prehistoric maw shut?  Of course, from our anthropocentric view, their TMJ counterpart is also curiously upside down…

 These images are from the amazing Holliday lab at Missouri, where they have constructed a 3D virtual alligator skull. Note that in direct opposition to the mammalian system, it is the mandibular articular bone which receives the condylar process of the quadrate bone of the caudal skull. In effect, the crocodilian skull is lifted, while the mandible remains relatively static. Thus it is both the power of the reptilian masseters and the potential energy of the elevated massive skull that combine in a very powerful SNAP.

But, I digress. Back to our patient…a middle-aged male captive alligator who died following several months of decline. At post mortem it was noted that his jaw had limited range of motion. On close examination and histopathology, there is a severe degenerative arthropathy characterized by extensive cartilage loss with replacement by fibrocartilage and fibrous connective tissue. To illustrate, look at the normal articular surface from a growing mammalian femur, below. Consistent with the life stage, the cartilage is hypercellular, but note the smooth surface, even thickness, and general organization. Beautiful, really.

Dartmouth Anatomy Lab

Now note our patient below. See that the articular cartilage on the left is replaced by fibrous connective tissue with a jagged surface, and in some areas the surface is thin, with minimal protection of the underlying bone. In other areas (top of lower image), fibrous connective tissue invades the subchondral bone. Nasty, really.

So, what does this have to do with anything? He’s a captive animal, so food apprehension shouldn’t be a problem…but did I mention that part of his presenting complaint involves something of a social coup? Our patient was once the top beast of the social hierarchy of his group, and in the months prior to his death, he increasingly became the brunt of attacks by his previously subservient brethren.

 

In many species, including our own, non-violent demonstrations of prowess provide an invaluable role in asserting dominance without the need for injury to either party. Think fluffed kittens and large antler racks on dominant bucks. The same holds true for crocodilians, which utilize a mouth gape display, as seen below, to cow their inferiors.

The keepers of this particular alligator noted that he had not gaped in the months prior to his death, despite frequent attacks by his fellows. Of course, we can’t rule out that he had other reasons to be seen as weak by his cohort. During the months of his decline, he developed infected wounds, and eventually a fungal pneumonia. The photomicrograph below depicts fungi within a pulmonary granuloma, with hyphae anchored in the parenchyma and flowering out into the air capillary. Like tourists at the beach. Nasty, really.

 And among other changes, he also had extensive renal necrosis and numerous urate tophi. The tophi are mineralizations likely secondary to acute antemortem dehydration. The necrosis is a possible sequel of synergistic effects of antimicrobial/antifungal therapy and dehydration. See one tophus below.

 It is not clear whether the degenerative changes in the jaw joint played a role in the decline of this animal. However, this case highlights the importance of a thorough post-mortem examination and knowing your comparative anatomy and the relative importance of lesions to a particular animal’s life history.

Interesting case! More later…