Abstract

Comprehensive necropsy evaluation of marine mammals is an essential part of any captive animal health program. Additionally, necropsy of free-ranging animals, for both disease surveillance and as part of long-term studies of specific trends or health problems, has become a necessary and broadly accepted endeavor. Of all organ systems, the central nervous system (CNS) is generally the least comprehensively or consistently evaluated in any species. In marine mammals, failing to evaluate the CNS is no less problematic, and perhaps an even greater omission, since our knowledge of pathology and disease is relatively limited. Two case reports of recent interesting and unusual CNS lesions presented here underscore the need to evaluate the CNS during the necropsy of marine mammals.

Case 1

Tissues from a 198-kilogram, juvenile, female, free-ranging, Atlantic bottlenose dolphin (Tursiops truncatus) were presented for histologic evaluation. This individual died within 24 hours of being transported to a rehabilitation facility. The gross necropsy report indicated this individual had sustained a large, deep-penetrating though healing, shark bite wound immediately subjacent to the dorsal fin. Histologically, the meninges adjacent to a dorsal nerve root of cervical spinal cord (C1) had moderate accumulations of neutrophils and lymphocytes, few macrophages and multinucleated giant cells, and admixed 5-20-µm diameter, non-parallel walled, aseptate, acute-angle branching fungal hyphae consistent with a zygomycete. Frequent meningeal vessels contained lumenal fungal hyphae, and/or fibrin thrombi, and several vessels had multifocal to diffuse mural necrosis. A vessel in the nerve root was similarly affected. The remaining meninges had multifocal moderate accumulations of lymphocytes and lesser neutrophils, with occasional prominent perivascular cuffing. Dorsal horn grey matter bilaterally had several vessels cuffed by small numbers of lymphocytes with mild gliosis in the surrounding neuropil, and one vessel contained few lumenal fungal hyphae.

Most likely, spinal meningitis was a direct consequence of the deep shark bite wound. Hematogenous or local extension from a deep cellulitis/myositis could also have led to the spinal meningitis. If spread did occur along the meninges and/or via CSF to reach the reviewed C1 spinal cord, certainly the brain could have been similarly affected. Unfortunately, brain was not available for histologic evaluation. No spinal cord was available for fungal culture, and identifying the fungus beyond histologic designation, as zygomycete was not possible.

Case 2

A 205-kilogram, adult, reproductively active, female, captive, Atlantic bottlenose dolphin was presented after sudden death. This animal had a chronic history of malaise, intermittent anorexia, dullness, and depression. It had been treated over the two months prior to death with antibiotics due to intermittent signs of colitis, and low-dose steroids to increase appetite (alternating megesterol acetate and dexamethasone). Continued clinical improvement prompted the discontinuation of medications several days prior to death. At necropsy, moderate quantities of blood exuded from the central canal upon severing the brainstem/cervical spinal cord at the atlanto-occipital joint. The panchymeninges overlying the right occipital lobe had a 5-cm diameter, irregular area of mild hemorrhage. Deep in the subjacent cerebral parenchyma and extending to the lateral ventricle was a 3x4x5-cm cavitation filled with clotted blood. The surrounding neuropil was malacic and delimited by a faint 2-mm-wide pale green region. Both lateral ventricles contained large blood clots, which followed the ventricular contours. Histologically, the affected region had extensive hemorrhage and necrosis, and adjacent white matter often had swollen axons and/or dilated axon sheaths. Rare arterioles, both adjacent to, and distant from, the lesion had a slightly hyaline appearance; however, amyloid was not found in any cerebral vessel.

Additional histologic lesions included diffuse hepatocellular hydropic degeneration (steroid hepatopathy) with bile stasis, adrenal cortical atrophy, and two small foci of necrosuppurative bronchointerstitial pneumonia with intralesional fungi consistent with Aspergillus sp.

Obviously, rapid clinical course and death in this individual was due to cerebral hemorrhage. Interestingly, the location was similar to that previously described in a bottlenose dolphin.¹ In human classification of intracerebral hemorrhage, this case would be a lobar hemorrhage, that is, it occurred in a cerebral hemisphere. Lobar hemorrhages can occur with hypertension, vasculitis, amyloid vasculopathy, hemorrhagic diathesis, neoplasia, or as an idiopathic/spontaneous occurrence without identified underlying conditions. In domestic animals, cerebral hemorrhage is rare. Some specific conditions such as mulberry heart disease in swine, thiamine deficiency in cats and dogs, and cerebral amyloid vasculopathy in dogs are recognized as causes of cerebral hemorrhage, yet these conditions also have additional lesions, either in the brain, or in other organ systems. In this case, no evidence of traumatic injury, such as subdural hemorrhage or subcutaneous bruising, was observed. No amyloid was found in cerebral vessels, and no intracranial neoplasms were identified. With the history of long-term corticosteroid administration, generalized vascular fragility, hypertension, and possibly even derangement of the clotting cascade due to liver disease (steroid hepatopathy) could all have been contemplated as potential causes or contributing factors. Focal vascular anomaly or weakness (aneurysm or otherwise) or vasculitis was equally plausible as a potential pathogenesis; however, none of the above could be conclusively ruled in or out.

Discussion

In the past 12 months, the University of Illinois Zoological Pathology Program (ZPP) reviewed case material on 61 marine mammals (50 necropsy, 11 biopsy) including 23 cetaceans and 38 pinnipeds. Twenty-four (48 percent) necropsy cases had either limited (single tissue, as in Case 2) or no CNS tissue submitted. Ten necropsy cases (20 percent) had lesions in the central nervous system (CNS), and in 9 cases (18 percent), the lesion was either contributory to demise or the sole cause of death. In many cases, including case 2 presented here, had the CNS not been evaluated, no cause of death would have been established.

The evaluation of the central nervous system as part of a comprehensive necropsy examination of marine mammals is essential. The reasons for not evaluating the CNS are varied, ranging from logistical difficulties such as lack of proper tools, technique, or appropriate-sized containers for fixation, to sensitive issues such as not "mutilating" the remains of a beloved animal to scientific issues such as not altering samples intended for museum specimens or morphometric studies. It is imperative that we overcome such difficulties. A skilled veterinarian or properly trained technician can easily and quickly harvest the brain during a postmortem exam without significantly impinging on emotional issues and without infringing on other postmortem scientific studies. Ascertaining diseases of the central nervous system in marine mammals goes beyond an academic quest for knowledge. Diagnostic pathology findings may guide treatment regimes for similarly affected surviving individuals. Establishing a sound cause of death may also be beneficial to institutions in the course of regulatory review of facilities and management. Finally, cumulative information regarding causes of morbidity and mortality in marine mammals serves to enhance captive management, and similar benefits may be attained for free-ranging animals. That this body of data be as complete as possible seems self-evident.

Acknowledgements

The author thanks the excellent technical assistance of Jane Chladny and the University of Illinois Veterinary Diagnostic Laboratory histology lab.

References

1.  Hall NR, RD Schimpff, JC Woodard, CC Carleton, RT Goldston. 1977. Intracerebral hemorrhage in a bottle-nosed dolphin (Tursiops truncatus). Journal of Wildlife Diseases 13(4): 341-345.