Abstract

For the past several years a debilitating condition termed "submarine syndrome" has afflicted Japanese farm-raised koi. This syndrome is characterized by difficulty maintaining neutral buoyancy whereby koi have a normal "positional" attitude, but are consistently negatively buoyant and exhibit abnormal behaviors, such as "porpoising." It affects primarily 1 to 2 year-old koi that are maintained at higher water temperatures and increased feed intake to maximize their growth-rate. Mortality is low and morbidity is high with symptoms persisting into later life. Clinical and pathologic evaluations were undertaken on 16 affected, 1 to 2 year-old koi in order to elucidate the pathogenesis of the syndrome. Serum chemistries and CBCs of the koi were unremarkable. However, using radiography and computed tomography, 13 of 16 fish had swimbladder abnormalities characterized by compartmentalization and variations in size and shape. At necropsy, 7 of 9 koi had cranial and/or caudal airsacs with irregularly thickened walls, multilobulation and varying degrees of inflation and deflation. Histologically, 9 of 9 koi had a granulomatous pneumocystitis characterized by infiltrates of macrophages, lymphocytes and multinucleated giant cells that in two fish involved the rete mirabile. Many macrophages contained variable amounts of heterogeneous, intracytoplasmic granular material, including pigment and membrane-bound particles. Gram-negative, non-acid-fast, rod-shaped bacteria were present within granulomas in 1 of 9 fish. A regionally extensive granulomatous polyserositis involving the ovary, kidney, and coelomic peritoneum accompanied the pneumocystitis of most fish. Additionally, many fish had a lymphohistiocytic epicarditis, endocarditis, meningitis, and/or encephalomyelitis, as well as lymphohistiocytic and heterophilic branchitis associated with occasional monogenean trematodes and protozoal cysts. Bacterial cultures of swimbladder mucosal swabs yielded Aeromonas veronii biovar sobria from 7 of 9 fish. No viruses were isolated from goldfish (Carassius auratus) cell lines inoculated with swimbladder tissue. Transmission electron microscopy of selected swimbladder sections failed to reveal any organisms. Based on our findings, koi "submarine syndrome" is associated with gross morphologic, radiographic and histopathologic lesions of the swimbladder. Reduced compliance of the swimbladder wall due to inflammation, as well as perfusion/diffusion mismatching across the rete mirabile, are suspected as being responsible for the malformations and variability of airsac inflation. Our findings of chronic inflammation in multiple organs, including swimbladder, bacterial granulomas and positive bacterial cultures suggest that a chronic bacterial infection with Aeromonas veronii biovar sobria plays an important role in the disease. Although no viral, protozoal, metazoan or fungal organisms were identified, they could not be definitively ruled-out as contributing etiologies. Additionally, the association of clinical signs with increased feed intake and elevated water temperature suggests a nutritional and/or environmental component to the syndrome. Further investigation is required to adequately define the multiple contributing factors to this complex disease.

Acknowledgements

The authors would like to thank Michael Dykstra, Jim Guy, Diane Deresienski, David Brazik and Maureen Trogdon for their contributions to this project.