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1985

EDWARDSIELLA INFECTIONS OF

G. L. Bullock U.S. Fish and Wildlife Service

Roger L. Herman U.S. Fish and Wildlife Service

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Bullock, G. L. and Herman, Roger L., " INFECTIONS OF FISHES" (1985). US Fish & Wildlife Publications. 132. https://digitalcommons.unl.edu/usfwspubs/132

This Article is brought to you for free and open access by the US Fish & Wildlife Service at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in US Fish & Wildlife Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. EDWARDS/ELLA INFECTIONS OF FISHES

G. L. Bullock and Roger L. Herman

u.s. Fish and Wildlife Service National Fisheries Center-Leetown National Fish Health Research Laboratory Box 700, Kearneysville, West Virginia 25430

FISH DISEASE LEAFLET 71

UNITED STATES DEPARTMENT OF THE INTERIOR Fish and Wildlife Service Division of Fishery Research Washington, D.C. 20240

1985 Introduction ing or erratic pattern. Gross external lesions vary with species. Channel often develop small, cutane­ The genus Edwardsiella was suggested by Ewing et ous ulcerations; in advanced cases, however, larger al. (1965) to encompass a group of enteric depigmented areas mark the sites of deep muscle generally described under vernacular names such as (Meyer and Bullock 1973). The flounder paracolon. The type species is E. tarda, which is an Para/iehthys olivaeeus and the cichlid Ti/apia nUotiea opportunistic pathogen of many animals. Meyer and develop swollen abdomens due to ascites (Nakat­ Bullock (1973) reported E. tarda as a pathogen of sugawa 1983; Kubota et al. 1981), and the bream Evyn­ (Ieta/urus punetatus) and named the nis japonicus develops ulcers on the head (Kusuda et disease emphysematous putrefactive disease of catfish. al. 1977). Diseased common carp (Cyprinus carpio), However, the organism described by Hoshina (1962) Japanese , and striped bass (Morone saxatilis) show as the fish pathogen Parae%baetrum anguillimor­ hemorrhages on the body and fins (Miyazaki and tiferum is now recognized as beingE. tarda (Wakabay­ Egusa 1976b; Sae-Oui et al. 1984). In , lesions on ashi and Egusa 1973). internal organs may perforate the body wall, and in Hawke (1979) isolated several strains of a bacterium striped bass, epithelial hyperplasia sometimes gives the closely resembling E. tarda from diseased cultured fish a tattered appearance. channel catfish, but later research showed it to be a Internally, the most common gross lesion consists distinct new species named E. ieta/uri (Hawke et al. of light-colored nodules on the kidneys, spleen, or 1981). Accordingly, the name applied to E. ieta/urus liver. Histologically such lesions are focal necrotic infections in catfish is enteric septicemia. areas, often with abundant bacteria, both free and within macrophages. These lesions may be walled off by fibrocytes and epitheloid cells, or be invasive and spread into adjacent skeletal muscle. Two forms of the Etiology and Diagnosis disease have been described from Japanese eels (Miyazaki and Egusa 1976a, b): in the more common and E. icta/uri are both gram­ form the initial lesions occur in the kidneys (sup­ negative motile rods that are cytochrome oxidase purative interstitial nephritis) and in the second form negative and ferment glucose with production of acid the liver is the primary organ affected (suppurative and gas. The two species can be differentiated hepatitis). Histopathology of internal organs is gen­ biochemically in that E. tarda produces both indol and erally similar in Japanese eels, tilapia, and striped bass. hydrogen sulfide whereas E. ieta/uri produces neither. Tilapia sometimes also shows intestinal abscesses and Additionally, the two species do not cross-react gill inflammation. Striped bass have epidermal hyper­ serologically. plasia and necroses (particularly in the cephalic canals Presumptive diagnosis of E. tarda or E. ieta/uri is of the lateral line system) in which masses of E. tarda based on clincal signs and on isolation and serological may occur. identification of the causative agents. A positive slide Large abscesses that develop in muscles of channel agglutination test with antiserum specific for E. tarda catfish and striped mullet (MugU eepha/us), and in in­ or E. ieta/uri provides a confirmatory diagnosis. ternal organs of Japanese eels emit a malodorous gas Rogers (1981) developed a fluorescent antibody test when punctured. and enzyme immunoassay that identify E. tarda and E. ieta/uri, both in culture and in infected tissues. Horiuchi et al. (1980) also demonstrated that an indi­ rect fluorescent antibody test in which tissue impres­ sions are used was effective in detecting and diagnos­ ing E. tarda in Japanese eels (Anguilla japoniea). Channel catfish infected with E. ieta/uri refuse feed, tend to hang at the surface, and swim with a spiral movement that includes erratic bursts. Gross external Pathology lesions include hemorrhages around the mouth, on the lateral and ventral portions of the body, and on the Edwardsiella tarda fins. Other signs include pale gills, exophthalmia, and small ulcerations on the body. Ulceration in the fon­ Fish infected with E. tarda sometimes become tanelle of the frontal bones gives the disease one of lethargic, "hang" at the surface, and swim in a spiral- its common names, "hole-in-the-head disease." Inter- 2 nally, petechiae occur or develop throughout the Table 1. Fish hosts of Edwardsiella tarda and Edwardsiella visceral mass and in the peritoneum and body ictal uri. musculature. Some fish develop ascites, and the liver, kidneys, and spleen are commonly enlarged (Plumb Edwardsiella tarda and Schwedler 1982; Rogers 1983). Danios (Dania devaria) infected with E. ieta/uri Atlantic salmon Sa/mo sa/ar swim erratically in a spinning pattern, but gross lesions Black skirted tetra Gymnocorymbus sp. have not been observed in this species. Brown bullhead lcta/urus nebu/osis Channel catfish leta/urus punctatus Histopathology has been described for both natural Chinook salmon Oncorhynchus tshawytscha and experimental infections of channel catfish ] apanese eel Anguilla japonica (Areechon and Plumb 1983; Jarboe et al. 1984; Blazer Emerald shiner Notropis atherinoides et al. 1985). Chronic natural infections are character­ Hirame flounder Paralichthys o/ivaceus ized by infiltrates of mononuclear cells that include Goldfish Carassius auratus Grass carp Ctenopharyngodon idella bacteria-laden macrophages, and diffuse necrosis and Largemouth bass Micropterus sa/moides inflammation occur in visceral organs. Inflammation Striped mullet Mugil cepha/us of the intestinal submucosa and mucosa is common. Striped bass Morone saxatilis Blazer et al. (1985) reported diffuse inflammation of Nile tilapia Tilapia nilotica the olfactory bulb and telencephalon, and considered Yellowtail Serio/a /a/andei the nares a possible route of infection. Jarboe et al. Edwardsiella icta/uri (1984) detected no lesions in the brain but did not ex­ amine the olfactory tract. Areechon and Plumb (1983) Brown bullhead leta/urus nebu/osis found necrotic lesions in the liver, spleen, kidneys, and Channel catfish lcta/urus punctatus pancreas of channel catfish that had been injected with Dania Danio devario Green knifefish Eigenmannia virescens E. ieta/uri; due to the acute course of the experimen­ Blue tilapia Tilapia aurea tal infection, the intestine did not become involved. White catfish leta/urus catus

Host and Geographic Range

Edwardsiella tarda has been isolated from many 1983). Fish that survive epizootics serve as carriers and, warm water fishes and some coldwater fishes, whereas because E. tarda is prevalent in the intestines of turkey E. ieta/uri has been isolated only from a few species vultures (Cathartes aura), birds may also be an impor­ of warm water fishes (Table I). Additionally, E. tarda tant reservoir of infection (Winsor et al. 1981). causes disease in such other animals as marine mam­ Catfish that survive epizootics of E. ieta/uri prob­ mals, pigs, turtles, alligators, ostriches, skunks, and ably serve as reservoirs of infection, since fish are the snakes. It has also occasionally infected humans (Clar­ only known host and the bacterium survives less than ridge et al. 1980; Nagel et al. 1982). In contrast, E. 8 days in pond water (Rogers 1983). ieta/uri is limited to fish, and survivors of epizootics probably become carriers. The geographic range of E. tarda is worldwide, Incubation Period whereas that of E. ieta/uri is still confined to the cat­ fish growing areas of the United States (Rogers 1983). Incubation time is temperature related; channel cat­ fish that were infected with E. tarda and held at 27 DC died within 10 days (Meyer and Bullock 1973). In Source and Reservoir of Infection studies at the National Fish Health Research Laboratory, striped bass held at 22 DC began dying Because E. tarda is ubiquitous, many animals can within 72 h after a 90-s bath exposure. serve as reservoirs of infection. Furthermore, the en­ Hawke (1979) reported that channel catfish injected vironment can be a source of infectivity because this with E. ieta/uri died within 96 h, and that fish exposed bacterium survives as long as 76 days in pond water to this bacterium in aquarium water died within 2 and mud (Ishihara and Kusuda 1982; Minagawa et al. weeks. 3

Control Blazer, V. S., E. B. Schotts, Jr., and W. D. Waltman. 1985. Pathology associated with Edwardsiella ictaluri in catfish Prevention (Ietalurus punctatus) and danio (Danio devario). J. Fish BioI. In press.

Because both E. tarda and E. ieta/uri are principal­ First report of Edwardsiella ictaluri in a species other than ly pathogens of warmwater fishes held in ponds, it is channel catfish. difficult to prevent disease outbreaks by following specific management procedures. At present, E. ie­ Clarridge, J. E., D. M. Musher, V. Fanstein, and R. J. ta/uri is more damaging than E. tarda as a cause of Wallace, Jr. 1980. Extraintestinal human infection caused mortality of cultured (J. A. Plumb, personal by Edwardsiella tarda. J. Clin. Microbiol. 11(5):511-514. communication). Outbreaks of E. ieta/uri infections Edwardsiella tarda is an uncommon enteric bacterium that occur at water temperatures of 24-28 °C, and are thus has been found generally in animal hosts and occasional­ restricted essentially to May-June and September­ ly in human feces. Three cases of extraintestinal infection October. Management procedures that reduce stress in man that were caused by E. tarda included a typhoid­ during these months may lessen the severity of like illness, with , and cellulitis from a wound received by an angler while fishing. The microbiol­ outbreaks. ogy of E. tarda and the previous reports of infections An experimental E. ieta/uri vaccine produced high caused by this organism are reviewed. titers in channel catfish (Rogers 1983). Commercial production of vaccines for both Edwardsiella Coles, B. M., R. K. Stroud, and S. Sheggeby. 1978. Isola­ pathogens is feasible. tion of Edwardsiella tarda from three Oregon sea mam­ mals. J. Wildl. Dis. 14(3):339-341.

Treatment Edwardsiella tarda was isolated from the peritoneal ex­ udate of a northern (Steller) sea lion (Eumetopias jubata) Outbreaks of E. tarda or E. ieta/uri can be con­ with peritonitis, and from the liver of a harbor porpoise trolled by feeding Terramycin at the rate of 2.5- (Phocena phocena), and a California sea lion (Zalophus californianus). These findings indicate that E. tarda is an 3.0 g/lOO lb of fish per day for 10 days. However, a opportunistic invader of sick or injured marine . strain of Terramycin-resistant E. tarda from channel catfish was reported by Hilton and Wilson (1980). Ad­ Ewing, W. H., A. C. McWhorter, M. R. Escobar, andA. H. ditionally, the potentiated sulfonamide Romet has Lubin. 1965. Edwardsiella, a new genus of Enterobac­ proved effective in controlling E. ieta/uri outbreaks, teriaceae based on a new species, E. tarda. Int. Bull. and the drug is in the process of registration with the Bacteriol. Nomencl. Taxon. 15(1):33-38. U.S. Food and Drug Administration for use on E. ic­ A full description of a new species and genus to be in­ ta/uri infections in catfishes. cluded in the family Enterobacteriaceae. The generic name Edwardsiella and the species name Edwardsiella tarda are suggested.

Annotated Bibliography Hawke, J. P. 1979. A bacterium associated with disease of pond cultured channel catfish, Ietalurns punctatus. J. Fish. Amandi, A., S. F. Hiu, J. S. Rohovec, and J. L. Fryer. 1982. Res. Board Can. 36(12):1508-1512. Isolation and characterization of Edwardsiella tarda from fall chinook salmon (Oncorhynchus tshawytscha). Appl. Original description of Edwardsiella ictaluri. The Environ. Microbiol. 43(6): 1380-1384. characteristics of this bacterium were compared with those of E. tarda; although the organism was described as a First description of Edwardsiella tarda infection in salmon. species of Edwardsiella, the species name was not officially The E. tarda isolate was also pathogenic for steelhead and assigned until 1981. rainbow trout. Hawke, J. P., A. C. McWhorter, A. G. Steigerwalt, and Areechon, N., and J. A. Plumb. 1983. Pathogenesis of Ed­ D. J. Brenner. 1981. Edwardsiella ietaluri sp. nov., the wardsiella ictaluri in channel catfish, Ietalurus punctatus. causative agent of enteric septicemia of catfish. Int. J. Syst. J. World Maricult. Soc. 14:249-260. Bacteriol. 31(4):396-400.

A description of hematological and histopathological On the basis of biochemical and serological tests, the changes after intraperitoneal injection of Edwardsiella authors described a new species of Edwardsiella and pro­ ictaluri. posed ictaluri as the specific epithet. 4

Herman, R. L., and G. L. Bullock. 1985. Pathology caused Kubota, S. S., N. Kaige, T. Miyazaki, and T. Miyashita. by Edwardsiella tarda in striped bass. Trans. Am. Fish. 1981. Histopathological studies on Edwardsiellosis of Soc. In press. tilapia-1. Natural infection. Bull. Fac. Fish. Mie Univ. 9:155-165. This is the first report of Edwardsiella tarda from striped bass. Pathogenicity was proved by contact infection. Nile tilapia with gross signs including pale body color Characteristic histopathology consisted of epithelial ascites, prolapsed anus, and cloudy eyes were found to hyperplasia and necrosis associated with the lateral line have abscesses primarily in the liver, spleen, and kidney. canals, and formation in the anterior kidney and These lesions progressed to granuloma formations. other internal organs. Kusuda, R., T. Itami, M. Munekiyo, and H. Nakajima. Hilton, L. R., and J. L. Wilson. 1980. Terramycin-resistant 1977. Characteristics of a Edwardsiella sp. from ar Edwardsiella tarda in channel catfish. Prog. Fish-Cult. epizootic of cultured crimson sea breams. Bull. Jpn. Soc. 42(3):159. Sci. Fish. 43(2):129-134.

Description of a Terramycin- resistant Edwardsiella tarda A disease outbreak among cultured sea bream was caused isolated from an epizootic among channel catfish. by a variant of Edwardsiella tarda. The bacterium differed from typical E. tarda strains in being nonmotile and a Horiuchi, M., T. Sato, H. Takagi, and K. Tozuka. 1980. fermenter of arabinose and sorbitol. Studies on rapid diagnosis system of main bacterial diseases of pond-cultured eels in Japan-II. Application Kusuda, R., T. Toyoshima, Y. Iwamura, and H. Sako. 1976. results of direct immunofluorescence for diagnosis of Ed­ Edwardsiella tarda from an epizootic of mullets (MugU wardsiellosis in field cases. Fish Pathol. 15(2):63-67. cephalus) in Okitsu Bay. Bull. Jpn. Soc. Sci. Fish. 42(3):271-275. The direct fluorescent antibody test was found to be reli­ able in diagnosing Edwardsiella tarda infection from An epizootic among striped mullet was found to be caused kidney or liver smears. by Edwardsiella tarda. Affected fish swam erratically in a whirling pattern, and bore large malodorous body Hoshina, T. 1962. On a new bacterium, Paracolobactrum abscesses. anguillimortiferum n. sp. Bull. Jpn. Soc. Sci. Fish. 28(1):162-164. Meyer, F. P., and G. L. Bullock. 1973. Edwardsiella tardo a new pathogen of channel catfish (letalurus punctatus) Appl. Microbiol. 25(1):155-156. The original description of Edwardsiella tarda in Japan. First description of Edwardsiella tarda in catfish. Ishihara, S., and R. Kusuda. 1981. Experimental infection of elvers and anguillettes with Edwardsiella tarda bacteria. Minagawa, T., T. Nakai, and K. Muroga. 1983. Edwardsiella Bull. Jpn. Soc. Sci. Fish. 47(8):999-1002. tarda in eel culture environment. Fish Pathol. 17(4):243-250. Elvers and anguillettes (larger eels) were challenged with Edwardsiella tarda by 1- or 3-h bath exposures, or by ad­ Field surveys on the presence and abundance of Edward­ dition of bacteria to feed. Both routes of infection pro­ siella tarda in water and mud of eel culture ponds were duced mortality in elvers but not in larger eels. made during each of the four seasons of the year in 1981-1982. The incidences of E. tarda in water and mud Ishihara, S., R. Kusuda. 1982. Growth and survival of samples from 30 ponds were 900/0 and 91 % in summer, Edwardsiella tarda bacteria in environmental water. Bull. 97% and 100% in autumn, 48% and 25% in winter, and Jpn. Soc. Sci. Fish. 48(4):483-488. 73% and 75% in spring. The density of organisms was also highest during the two warmer seasons. Edwardsiella tarda survived for up to 76 days in pond water. This long survival time may aid in transmission of Miyashita, T. 1984. Pseudomonas f/uorescens and Edward­ E. tarda. siella tarda isolated from diseased tilapia. Fish Pathol. 19(1):45-50. Jarboe, H. H., P. R. Bowser, and H. R. Robinette. 1984. Pathology associated with a natural Edwardsiella ictaluri Cultured tilapia suffered chronic mortality from Psuedo­ infection in channel catfish (letalurus punctatus Rafin­ monas f/uorescens and Edwardsiella tarda. Infections esque). J. Wildl. Dis. 20(4):352-354. caused by P. f/uorescens were characterized by hemor­ rhage, particularly in the ovary, and those caused by the A clinical description that includes behavior, gross signs, E. tarda showed discrete colonies in the spleen. histopathology, and hematocrit values. Lesions differed from those described in other reports, and it is suggested Miyazaki, T., and S. Egusa. 19760. Histopathological stud­ that the route of infection may alter clinical signs. ies of Edwardsiellosis of the Japanese eel (Anguilla 5

japonica)-1. Suppurative interstitial nephritis form. Fish Plumb, J. A., and T. E. Schwedler. 1982. Enteric septicemia pathol. 11(1):33-44. of catfish (ESC): a new bacterial problem surfaces. Aquaculture 18(4):26-27. The nephritic infection is characterized by abscesses in the kidney. Advanced lesions may penetrate the musculature Description of Edwardsiella ictaluri infection of channel and perforate the skin. catfish, including clinical signs, pathology, severity, and chemotherapy. Miyazaki, T., and S. Egusa. 1976b. Histopathological stud­ ies of Edwardsiellosis of the Japanese eel (Anguilla Rogers, W. A. 1981. Serological detection of two species of japonica)-II. Suppurative hepatitis form. Fish Pathol. Edwardsiella infecting catfish. Pages 169-172 in D. P. 11(2):67-76. Anderson and W. Hennessen, eds. Proceedings of the In­ ternational Symposium on Fish Biologics: Serodiagnostics Description of hepatic abscesses that predominate in this and Vaccines, Kearneysville, West Virginia, 26-30 April form of Edwardsiella infection. 1981.

Mushiake, K., K. Muroga, and T. Nakai. 1984. Increased An enzyme immunoassay test for identification of Ed­ susceptibility of Japanese eel Anguillajaponica to Edward­ wardsiella tarda and E. ictaluri compared favorably with siella tarda and Pseudomonas anguilliseptica following ex­ the fluorescent antibody procedure. When clinical spec­ posure to copper. Bull. Jpn. Soc. Sci. Fish. imens were used, both procedures provided identification 50(11): 1797-1801. of either pathogen within 20 min. Exposure of eels for 24 to 48 h to 100-340 ppm copper Rogers, W. A. 1983. Edwardsiellosis in fishes. Pages 153-159 increased susceptibility to Edwardsiella tarda. The authors in D. P. Anderson, M. Dorson, and Ph. Dubourget, eds. speculated that susceptibility was a result of a stress Antigens of fish pathogens. Les Antigenes des micro­ response. organismes pathogenes des poissons. Fondation Marcel Merieux, Lyon, France. Nagel, P., A. Serritella, and T. J. Layden. 1982. Edward­ siella tarda associated with a pet turtle. A general review of Edwardsiella tarda and E. ictaluri. Gastroenterol. Annu. 82:1436-1437.

Describes a patient who developed gastroenteritis that was Sae-Oui, D., K. Muroga, and T. Nakai. 1984. A case of induced by Edwardsiella tarda, seemingly from exposure Edwardsiella tarda infection in cultured colored carp to a diseased turtle. Cyprinus carpio. Fish Pathol. 19(3):197-199.

Nakatsugawa, T. 1983. Edwardsiella tarda isolated from Description of the first recorded Edwardsiella tarda in­ cultured young flounder. Fish Pathol. 18(2):99-101. fection in carp. The epizootic killed 60 colored (koi) carp. Affected fish showed hemorrhage and erythema on the First isolation of Edwardsiella tarda from a Hirame body. flounder. Diseased fish showed accumulations of ascitic fluid. The isolate killed yellowtails into which it was Ullah, Md. A., and T. Arai. 1983. Pathological activities injected. of the naturally occurring strains of Edwardsiella tarda. Fish Pathol. 18(2):65-70. Owens, D. R., S. L. Nelson, and J. B. Addison. 1974. Isola­ tion of Edwardsiella tarda from swine. Appl. Microbiol. Authors demonstrated that Edwardsiella tarda strains pro­ 27(4):703-706. duced hemolysins and dermotoxins, and suggested that these toxins may be virulence factors. Edwardsiella tarda was isolated from the intestinal tract of a 2- month-old pig. This is the first reported isolation of E. tarda from swine in the United States. Swine have Wakabayashi, H., and S. Egusa. 1973. Edwardsiella tarda been reported as potential carriers of E. tarda, but path­ (Paracolobactrum anguillimortijerum) associated with ogenicity of the organism for swine has not been pond-cultured eel disease. Bull. Jpn. Soc. Sci. Fish. determined. 39(9):931-936.

Plumb, J. A., and D. J. Sanchez. 1983. Susceptibility of five Description of morphological and biochemical species of fish to Edwardsiella ictaluri. J. Fish Dis. characteristics of 22 strains of Edwardsiella tarda isolated 6(3):261-266. from diseased eels.

Injection of 1.5 X 103 to 1.5 X 108 Edwardsiella ictaluri Winsor, D. K., A. P. Bloebaum, and J. J. Mathewson. 1981. cells killed all channel catfish within 10 days; however, Gram-negative, aerobic, enteric pathogens among in­ among tilapia, golden shiner (Notemigonus crysoleucus), testinal micro flora of wild turkey vultures (Cathartes aura) bighead carp (Aristichthys nobilis), and largemouth bass in west central Texas. Appl. Environ. Microbiol. (Micropterus salmoides) 70070 were refractive. 42(6): 1123-1124. 6

The prevalence of Edwardsiella tarda and other enteric skin, visceral, and dressed-fish samples, respectively. It bacteria in the intestines of turkey vultures suggested that was also isolated from 30% of imported dressed fish, from they may be reservoirs of the pathogens. 75% of the water samples and 64% of the mud samples from catfish ponds and from 100% of the frogs, turtles Wyatt, L. E., R. Nickelson II, and C. Vanderzant. 1979. and crayfish from catfish ponds. The incidence of Edward~ Edwardsiella tarda in freshwater catfish and their environ­ siella increased during summer, as water temperatures in­ ment. Appl. Environ. Microbiol. 38(4):710-714. creased. The significance of the incidence of Edwardsiel/a in catfish, catfish disease, and public health could not be Edwardsiella tarda was isolated from 47, 88, and 791170 of substantiated.

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