Abstract
There is an increasing interest in the study of gas bubble disease and barotrauma in marine mammals. In the past, it was thought that cetaceans and pinnipeds were resistant to barotrauma because of these animals' unique physiological adaptations that allow them to feed at great depths. However, recently, histological studies have reported lesions associated with gas bubbles in vessels and parenchyma of vital organs in stranded, dead marine mammals.1,2,3,5,6,7 Biomedical imaging techniques such as magnetic resonance imaging (MRI) represent valuable diagnostic tools to better understand gas bubble disease in live marine mammals.4
Here we present in vivo evidence of gas bubbles in the cerebellum and progression of the disease in a male, yearling California sea lion (Zalophus californianus) stranded along the California coast in fall 2009 and admitted for rehabilitation at The Marine Mammal Center, Sausalito, CA. On admission the animal presented with cerebellar ataxia, as well as visual deficits. Radiographs indicated complete, proximal fractures of left ribs three, four and five, pneumothorax, and multiple gas filled areas that were restricted to the cerebellum. These latest findings were confirmed with MRI of the brain. Cerebrospinal fluid (CSF) analyses were within normal ranges for healthy animals. Hematology and serum chemistry values were clinically unremarkable, suggesting the absence of ongoing inflammatory diseases. The animal received supportive care, and was treated with metronidazole and trimethoprim/sulfadiazine until the results from CSF tap and MRI were known. Two months after admission, volume computed tomography (VCT) and a second MRI were performed. The VCT and MRI images revealed that the areas once filled with gas were filled with fluid. The sea lion was released on December 4th, 2009 with a satellite-linked transmitter which recorded location and depth. The sea lion travelled up to 40 km from the release site and dove to depths over 100 m, confirming its ability to dive and forage. The animal re-stranded a month from release, weak and malnourished, with evidence of swelling and minor purulent-bloody discharge from the nostrils. Blood analysis revealed low white blood cell count and serum chemistry consistent with malnutrition. The animal died on January 3rd, 2010. Post mortem MRI confirmed the persistence of fluid filled regions in the cerebellum. The necropsy revealed bacterial pleuritis presumably contracted while in the wild and unrelated to the cerebellar pneumatosis.
This report suggests that barotrauma and gas-bubble disease do occur in California sea lions and can be easily detected with MRI and VCT. We speculate that the source of gas originated from the pneumothorax and that the gas was confined to the cerebellum because of preferential blood flow to the cerebellum during deep dives as part of the "dive reflex" that provides perfusion of vital organs, including the caudal fossa structures of the brain.
References
1. Fernàndez J, Edwards F, Rodriguez F, Espinosa de los Monteros A, Herràez P, Castro P, Jaber JR, Martìn V, Arbelo M. 2005. Gas and fat embolic syndrome involving a mass stranding of Beaked Whales (Family Ziphiidae) exposed to anthropogenic sonar signals. Veterinary Pathology 42:446-457.
2. Houser DS, Dankiewicz-Talmadge LA, Stockard TK, Ponganis PJ. 2009. Investigation of the potential for vascular bubble formation in a repetitively diving dolphin. The Journal of Experimental Biology 213:52-62.
3. Jepson PD, Arbelo M, Deaville R, Patterson IAP, Castro P, Baker JR, Degollada E, Ross HM, Herráez P, Pocknell AM, Rodríguez F, Howie FE, Espinosa A, Reid RJ, Jaber JR, Martin V, Cunningham AA, Fernández A. 2003. Gas-bubble lesions in stranded cetaceans. Was sonar responsible for a spate of whale deaths after an Atlantic military exercise? Nature 425:575-576.
4. Jepson PD, Deaville R, Patterson IAP, Pocknell AM, Ross HM, Baker JR, Howie FE, Reid RJ, Colloff A, Cunningham AA. 2005. Acute and chronic gas bubble lesions in cetaceans stranded in the United Kingdom. Veterinary Pathology 42:291-305.
5. Montie EW, Pussini N, Schneider G, Battey TWK, Dennison S, Barakos J, Gulland F. 2009. Neuroanatomy and volumes of brain structures of a live California sea lion (Zalophus californianus) from magnetic resonance images. The Anatomical Record 292:1523-1547.
6. Moore MJ, Bogomolni AL, Dennison SE, Early G, Garner MM, Hayward BA, Lentell BJ, Rotstein DS. 2009. Gas bubbles in seals, dolphins, and porpoises entangled and drowned at depth in gillnets. Veterinary Pathology 46:536-547.
7. Moore MJ, Early GA. 2004. Cumulative sperm whale bone damage and the bends. Science 306:24.