This report details histopathological findings of atypical vacuolated hepatocytes in the white perch Morone americana. Vacuolated cell lesions have been reported from a number of species in association with degraded habitats, often in the presence of hepatic neoplasms. Extensive atypical vacuolated cell lesions assuming characteristic acinar or ductular configurations have been reported previously only from the winter flounder Pseudopleuronectes americanus. Light microscopic findings, utilizing a variety of histochemical stains, suggest the identical nature of this lesion to that of winter flounder. The discovery of this lesion in a free-swimming species, feeding throughout the water column, is in direct contrast to that of the bottom dwelling pleuronectid, feeding from and constantly in contact with potentially contaminated sediments. While the winter flounder has become the sentinel fish species for pollution monitoring on the northeast coast, increased surveillance of other species may prove atypical vacuolated cell lesions represent a common mechanism of chronic cellular injury in relation to impacted environments

Camus, A. C.

Wolke, Richard E.

English

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University of Rhode IslandDigitalCommons@URIFisheries, Animal and Veterinary Sciences FacultyPublications Fisheries, Animal and Veterinary Sciences1991Atypical hepatic vacuolated cell lesion in the whiteperch Morone americanaA. C. CamusUniversity of Rhode IslandRichard E. WolkeUniversity of Rhode Island, richard_wolke@uri.eduFollow this and additional works at: https://digitalcommons.uri.edu/favs_facpubsTerms of UseAll rights reserved under copyright.This Article is brought to you for free and open access by the Fisheries, Animal and Veterinary Sciences at DigitalCommons@URI. It has been acceptedfor inclusion in Fisheries, Animal and Veterinary Sciences Faculty Publications by an authorized administrator of DigitalCommons@URI. For moreinformation, please contact digitalcommons@etal.uri.edu.Citation/Publisher AttributionCamus, A. C., & Wolke, R. E. (1991). Atypical hepatic vacuolated cell lesion in the white perch Morone americana. Diseases of AquaticOrganisms, 11, 225-228. doi: 10.3354/dao011225Available at: http://dx.doi.org/10.3354/dao011225Vol. 11: 225-228, 1991 DISEASES OF AQUATIC ORGANISMS Dis. aquat. Org. Published October 17 NOTE Atypical hepatic vacuolated cell lesion in the white perch Morone americana A. C. Camus, R. E. Wolke Comparative Animal Pathology Lab. East Farm. Department of Fisheries, Animal and Veterinary Sciences. University of Rhode Island. Kingston. Rhode Island 02881-0804. USA ABSTRACT: This report details histopathological findings of atypical vacuolated hepatocytes in the white perch Morone americana. Vacuolated cell lesions have been reported from a number of species in association with degraded habitats, often in the presence of hepatic neoplasms. Extensive atypical vac- uolated cell lesions assuming characteristic acinar or ductular configurations have been reported previously only from the winter flounder Pseudopleuronectes americanus. Light micro- scopic findings, utilizing a variety of histochemical stains, suggest the identical nature of this lesion to that of winter flounder. The discovery of this lesion in a free-swimming species, feeding throughout the water colun~n,  is in direct contrast to that of the bottom dwelling pleuronectid, feeding from and constantly in contact with potentially contaminated sediments. While the winter flounder has become the sentinel fish species for pollution monitoring on the northeast coast, increased surveillance of other species may prove atypical vacuolated cell lesions represent a common mechanism of chronic cellular injury in relation to impacted environments. Vacuolated cell lesions, hepatic and biliary, have been reported from a number of species under natural and experimental conditions (Smith et al. 1979, Hen- dricks et  al. 1984, Cormier 1986, Grizzle & Thiyagara- jah 1988, Hinton et al. 1988). In Boston Harbor (USA) a unique lesion was reported in winter flounder Pseudo- pleuronectes americanus by Murchelano & Wolke (1985); extensive areas of hepatocytes appeared replaced by atypical vacuolated cells in distinct acinar and ductular configurations. Unlike other reported vac- uolated hepatocyte lesions, hepatocellular steatosis and clear cell foci, affected hepatocytes of winter floun- der contain a condensed apical nucleus and a single large clear vacuole devoid of lipid, glycogen or mucopolysaccharides. The lesion also lacks the floccu- lent, eosinophilic material generally associated with cystic parenchyma1 degeneration or the locular appear- ance of spongiosis hepatis. Additionally, while exten- sive areas of hepatocytes may be  replaced by hyper- trophic vacuolated cells, often surrounded by connec- O Inter-Research/Printed in Germany tive tissue, the lesion is restricted to the hepatic cords and normal architecture is generally preserved. Since 1985, several authors have reported this lesion in winter flounder from various sites along the New England seaboard, typically in association with con- taminated sediments adjacent to population centers (Zdanowicz et al. 1986, Gardner et al. 1989). Similar lesions have been noted in rock sole Lepidopsetta bilineata, starry flounder Platichthys stellatus and white croaker Genyonemus lineatus on the west coast (M. S. Meyers, National Marine Fisheries Service, Seat- tle, WA, pers. comm.). Recently, a n  atypical vacuolated hepatocyte lesion resembling that of winter flounder was found in one of a group of 5 white perch collected from a Rhode Island coastal salt pond open indirectly to Narragansett Bay. White perch, unlike winter flounder, are found in these shallow ponds throughout the year. While capable of tolerating full seawater, they prefer the brackish waters of the ponds, where they wander and feed in small schools. In winter they congregate in deeper waters to hibernate, running up into fresh or slightly brackish water to spawn April through June.  White perch are highly predaceous, feeding on the spawn and fry of numerous fish and  crustaceans (Bigelow & Schroeder 1953). Materials and methods. Five post-spawning female white perch Morone americana were taken by fyke net in July of 1990 in a population survey of coastal salt ponds of Rhode Island, USA. Fish were euthanized in tricaine methanesulfonate (MS-222), weighed, meas- ured and necropsied immediately. Collected tissues were identified, fixed in 10 % neutral buffered forma- lin, embedded in paraffin and sectioned at  6 pm for light microscopic examination. Staining procedures, a s  outlined by Luna (1968), included hematoxylin and esoin (H & E), periodic acid Schiff (PAS), Perls' method 226 Dls. aquat. Org. 11: 225-228, 1941 for iron, >lasson's trichrome (hlT), Ziehl-Neelsen acid fast stain (ZN) ,  and alcian blue (AB). Formalin fixed tissue was embedded in gelatin, seclioned frozen and stained for lipids with oil red 0 (ORO) and sudan black B (SB). Results and discussion. Fish appeared to be  in good flesh, ranging in weight from 154 to 506 g and in length from 26 to 32 cm. Little abdominal fat was present. but was not considered unusual for post-spawning indi- viduals. Livers were of firm consistency and uniform light mahogany coloration. Gross observation revealed the presence of multiple 1 mm white foci scattered throughout the hepatic and  splenic parenchymas of all fish examined. Microscopically, these were identified as the metacercariae of digenetic trematodes. Metacer- cariae were encircled by a thln fibrous capsule, but did not appear to elicit a significant inflammatory response. Under light microscopy, prespawning individuals r e v ~ a l  arge polygona! hepatocytes arrazged in irrzgu- lar cords. The pattern is typical tubulosinusoidal, lack- ing distinct lobulation, as described in rainbow trout by Hampton e t  al. (1985). Nuclei are spherical and gener- ally centrally located with dispersed chromatin and single prominent nu.cleoli. Most hepatocytes contain one to several inclusions within their pale, finely granular cytoplasm. Small inclusions are (PAS) positive for glycogen, while larger inclusions, often perinuclear, are (SB) and (ORO) positil-C: for lipids. In contrast, hepatocytes of post-spawning indi\.iduals appeared small, darker staining and dcpleted of cytoplasmic inclusions. Shrunken hepatocytes result In an  appear- ance of dilated sinusoids. Atypical vacuolated hepatocytes, possessing a single large clear vacuole, occurred singly or in characteristic acinar (Fig. 1)  or ductular (Fig. 2) patterns. No histo- logical alterations were noted in hepatocytes adjacent to the vacuolated foci, nor were there any associated inflammatory changes. Nuclei were compact, uniform- ly basophilic and displaced apically. Occasionally, small PAS positive inclusions were present, but invari- ably displaced peripherally by  the large central vac- uole. The extensive areas of vacuolated cells were often invested in a fine sheath of connective tissue (MT). Vacuoles were consistently negative for glyco- gen (PAS), mucopolysaccharides (AB) and lipids (SB, CRC) as in winter flounder. In addition to the vacuolated cell lesion, histo- pathological changes in the affected liver included multiple foci of necrosis, focal hepatitis, pericholangitis and vasculitis. Vacuolated cells appeared random in distribution, demonstrating no spatial relationships to any of the aforementioned lesions or metacercanae. Pericholangi.al fibrosis was common. A single focus of bile duct hyperplasia also contained vacuolated cells Fig. 1. Morone americana. Acinus of vacuolated hepatocytes demonstrating large c ~ n t r a l  vacuoles and apicslly displaced nuclei. Note investing sheath of collagcnous fibers. H & E;  X 1000 Camus S \Volkc ..\typical ht-patlc crll l e s~on  in white perch 227 Fig. 2. Morone amedcana. Vacuolated cells occurring singly and in a large ductular configurat~on H & E; X 500 within its connective tissue matrix, light microscopi- cally indistinguishable from those found in the hepatic parenchyma. Pigmented macrophage aggregates were numerous, strongly (ZN) and (PAS) positive, but only weakly Pei-l's positive for ferric iron. Irregular focl of coagulat~ve necrosis contained amorphous hyalin material and s~ng le  pigment laden macrophages with staining properties identical to those of nearby aggregates. Tissue coarse eosinophilic granulocytes were also common. Number, extent and severity of pathological lesions appeared to increase dramatically with fish size, even within this small sample group. The vacuolated cell lesion was present in the second largest fish, a 480 g specimen. The ultrastructural characteristics of this lesion in winter flounder have recently been reviewed (Bodam- mer & Murchelano 1990). The large vacuole has been determined to represent the dilated cisternae of a mod- ified endoplasmic reticulum system. These cells show additional signs of chronic cellular injury, including numerous autophagic vacuoles and condensed mito- chondna. At present, the cellular origin of this lesion and its progression remains unclear Based on cellular orientation and junctional complexes, it appears to involve both bile preductular cells (Moore et al. 1990) and hepatocytes (Bodammer & Murchelano 1990). Likewise, the relationship of this lesion to hepatic neo- plasia is also uncertain. Flounder possessing atypical vacuolated cell lesions demonstrate a high incidence of hepatic neoplasia (Murchelano & Wolke 1985, 1991). Statistical evidence supports a correlation between hepatic neoplasia in flatfish and polynuclear aromatic hydrocarbons (Malins et al. 1984, Gardner et al. 1989). While serial sections of the vacuolated cell llver did not demonstrate neoplasms, it did possess a variety of lesions associated with polluted environments (Meyers et al. 1987, Murchelano & Wolke 1991). Demonstration of an  atypical vacuolated hepatocyte lesion in the white perch suggests a common mechan- ism of cellular injury, not unique to the winter flounder or solely bottom dwelling species. While experimental evidence is lacking, the striking cellular alterations are presumed to be  the result of environmental toxins. The nature of the vacuolar contents in both species is unclear, but histochemical staining has shown them to be distinct from the more well described lipid and polysaccharide inclusions seen in other fish. Electron microscopy, in winter flounder, has identified the vac- uoles as dilated cisternae of endoplasmic reticulum, often containing membranous inclusions considered autophagic in nature, a significant sign of sublethal cell injury (Bodammer & Murchelano 1990). Clearly, elec- tron microscopy is needed to further characterize this lesion in the white perch. Increased monitoring of non- Dis. aquat. Org. 11 225-228, 1991 traditional species  as sentinels may  prove this lesion Hinton, D. E., Couch. J. A., Teh, S. J.,  Courtney, L. A. (1988). . - . . more  widespread than  originally reported. It is hoped  Cytological changes during progression of neoplasia in that  discovery of this lesion in the whlte perch will selected fish species. Aquat. Toxlcol. 3.1 77-1 12 Luna, L. G. (1968). Manual of histologic staining methods of cont inue to promote its evolution as a biomarker  of the Armed Forces Institute of Pathology, 3rd edn. environmental  degradat ion.  McGraw-Hill Book Co., New York Acknotvlegements. Contribution number 2621 of the College of Resource Development, University of Rhode Island, with support of the Rhode Island Agricultural Experiment Station. Malins, D. C., McCain, B. B.. Brown, D. W.. Chan, S.-L., Meyers, M. S., Landahl, J. T., Prohaska, P. G., Friedman, A. J . ,  Rhodes, L. D., Burrows, D. G. ,  Gronlund, W. D., Hodgins, H 0 (1984). Chemical pollutants in sediments and diseases of bottom-dwelling fish in Puget Sound, Washington. Envir. Sci. Technol. 18: 705-713 Meyers, M. S., Rhodes, L. D., McCain, B. B. (1987). Pathologic LITERATURE CITED anatomy and patterns of occurrence of hepatic neoplams, putative preneoplastic lesions, and other idiopathic hepa- Bigelow, H. B . ,  Schroeder, W. C. (1953). Fishes of the Gulf of tic conditions in English sole (Parophrys vetulus) from Maine. Fishery Bulletin of the Fish and Wildlife Service, Vol. Puget Sound, Washington. J. natn. Cancer Inst. 78: 53. U. S. Govt. Printing Office, Washington, p. 405-406 333-363 Bodammer, J. E., Murchelano, R. A. (1990). Cytological study Moore, M. J., Smolowitz, R., Stegeman, J. J. (1990). Cellular of vacuoiated cells and other aberrant hepatocytes in alterations preceding neoplasia in Pseudopleuronectes winter flounder from Boston Harbor. Cancer Res. 50: amencanus from Boston Harbor. Mar. envir Res. 28: 6744-6756 425-429 Cormier, S. M. (1986). Fine structure of hepatocytes and Murcheidno, R. A., Woike, R. E. (1985). Epizootic carcinoma in hepatocellular carcinoma of the Atlantic tomcod, Micro- winter flounder, Pseudopleuronectes americanus. Science gadus tomcod (Walbaum). J. Fish. Dis. 9: 179-194 228: 587-589 Gardner, G. R., Pruell, R. J., Folmar, L. C. (1989). Acomparisonof Murchelano, R. A., Wolke, R. E. (1991). Neoplasms and non- both neoplastic and non-neoplastic disorders in winter neoplastic liver lesions in winter flounder, Pseudo- flounder (Pseudopleuronectesamencanus) from eight areas pleuronectes arnericanus, from Boston Harbor, in New England. Mar. environ. res. 28: 393-397 Massachusetts. Envir. Hlth Perspectives 90: 17-26 Grizzle, J .  M.,  Thiyagarajah, A. (1988). Diethylnitrosamine- Smith, C. E ,  Peck, T. H., Klauda, R. J., McLaren, J. B. (1979). induced hepatic neoplasms in the fish fivulus ocellatus Hepatomas in Atlantic tomcod Microgadus tomcod (Wal- rnarmoratus. Dis. aquat. Org. 5: 39-50 baurn) collected in the Hudson River estuary in New York. Hampton, J. A., McCuskey, P. A., McCuskey, R. S., Hinton, J. Fish Dis. 2: 313-319 D. E. (1985). Functional units in rainbow trout (Salmo Zdanowicz, V. S., Gadbois, D. F., Newman, M. W. (1986). gairdner~] liver: I. Arrangement and histochemical proper- Levels of organic and inorganic contaminants in sediments ties of hepatocytes. Anat. Rec. 213: 168-175 and fish tissues and prevalences of pathological disorders Hendricks, J. D . ,  Meyers, T. R . ,  Shelton, D. W. (1984). His- in winter flounder from estuaries of the northeast United tological progression of hepatic neoplasia in rainbow trout States, 1984. Institute of Electrical and Electronics (Salmo gairdneri). In: Hoover, K. L. (ed.), Use of small fish Engineers Oceans, 1986 Conference Proceedings. Institute in carcinogenicity testing. National Cancer Institute Mono- of Electrical and Electronics Engineers, Washington. p. graph No. 65. Bethesda. p. 321-326 578-585 Responsible Subject Edrtor: G. Peters, Hamburg, Germany Revised version accepted: June 4, 1991 

Atypical hepatic vacuolated cell lesion in the white perch \u3cem\u3eMorone americana\u3c/em\u3e

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Atypical hepatic vacuolated cell lesion in the white perch \u3cem\u3eMorone americana\u3c/em\u3e

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