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**Fish Disease Leaflet 82****Enteric Redmouth Disease of Salmonids**G. L. Bullock and R. C. Cipriano
 U.S. Fish and Wildlife Service, National Fisheries Research Center-Leetown, National Fish Health Research Laboratory,  Box 700, Kearneysville, West Virginia.   25430

UNITED STATES DEPARTMENT OF THE INTERIOR, Fish and Wildlife Service.  1990

*(Revision of Fish Disease Leaflet 57 (1979), same title, by G. L.Bullock and S. F. Snieszko and Fish Disease Leaflet 67 (1984) by G. L.Bullock.)*
- **Introduction**  **Clinical Signs****Etiology**
- **Diagnosis and Detection**  **Source and Reservior of Infection****Mode of Transmission**
- **Incubation Period**  **Host and Geographic Range****Methods of Control**
- ***Prevention***  ***Treatment***
- **Bibliography**     **Introduction**  Enteric redmouth disease (ERM) is a systemic bacterial infection offishes, but is known principally for its occurrence in rainbow trout,*Oncorhynchus**mykiss*. It was first reported in the 1950'sin Idaho rainbow trout and described by Rucker (1966). In recognition ofthat first description, the causal organism was named *Yersinia**ruckeri* by Ewing et al. (1978).**Clinical Signs**
In early acute epizootics, typically affected rainbow trout arelethargic and anorexic and have subcutaneous hemorrhages in and aroundthe mouth, oral cavity, and isthmus, and at the base of fins. Gillfilaments may be hemorrhagic. Petechial hemorrhages may occur on thesurface of the liver, pancreas, pyloric caeca, and swim bladder, and inthe lateral musculature. The spleen is enlarged and friable, gonads arehemorrhagic, and the lower intestine is inflamed and filled with athick, yellowish fluid. Exophthalmus occurs, commonly accompanied byhemorrhages around the ocular cavity and iris. The affected eyescommonly rupture. If fish survive, they darken and seek shelter, orwithdraw from other fish (Busch 1983; Rucker 1966). In atypicalinfections that sometimes occur, no hemorrhages develop on the mouth andgill cover; fish merely become dark and swim near the surface (Frerichset al. 1985). Histological examination of tissues from infected troutshows an acute bacteremia and attendant inflammatory response invirtually all tissues. Bacteria are especially conspicuous in vasculartissue and in areas of petechial hemorrhage (Rucker 1966). Bacterialcolonization occurs in the capillaries of well vascularized tissue andis followed by dilation of small blood vessels; petechial hemorrhages;erythrocyte congestion; and edema of the kidneys, liver, spleen, heart,and gills. Focal necrosis may occur in the liver, and markedaccumulations of mononuclear cells in periportal areas. Hemorrhagesdevelop in outer portions of the digestive tract, and the lining ormucosa becomes edematous and necrotic and sometimes sloughs into thelumen (Busch 1983).

Enteric redmouth disease commonly causes sustained, lowlevelmortality, eventually resulting in high losses. Largescale, acuteepizootics sometimes occur if chronically infected fish are stressed.
**Etiology**
Serotypic differences of *Y*. *ruckeri* wereoriginally associated with the ability of isolates to ferment sorbitol.For several years after the original isolation of *Y*. *ruckeri*from salmonids in the Hagerman Valley, Idaho, all isolates wereserologically similar and did not ferment sorbitol (Ross et al. 1966;Busch 1983). These were called Type I. Even today, most*Y*. *ruckeri* that do not ferment sorbitol form a singleand distinct serotype (Pyle et al. 1985, 1987).

O'Leary (1977) described another serotype of *Y*. *ruckeri*,isolated from Pacific salmon (*Oncorhynchus* spp.), that fermentedsorbitol. This was called Type II. Later research has shown thatcollections of *Y*. *ruckeri* that ferment sorbitol can bedifferentiated into as many as five distinct serotypes (Pyle et al.1985, 1987; Stevenson and Airdrie 1984). Only Types I and II are nowknown to cause ERM epizootics.
**Diagnosis and Detection**
Presumptive diagnosis of ERM can be based on clinical signs andon the inoculation of infected tissue on the differential medium ofShotts and Waltman (1983). The direct or indirect fluorescent antibodytest, and monoclonalbased, enzymelinked immunosorbent assay (Austin etal. 1986), may be used for serotypes I and II; however, as previouslymentioned, three additional serotypes have been described and if theseserological tests are negative, ERM cannot be ruled out. Antisera forthese additional serotypes are not generally available. Serologicalidentification of Type I and Type II is based on agglutination orfluorescent antibody tests. Confirmatory diagnosis of ERM requiresisolation and identification of the causative agent. Identification isbased on the isolation of a gramnegative, motile, rodshaped bacteriumwith distinctive properties: it is cytochrome oxidase negative; producesacid but usually no gas in glucose; produces an alkaline slant and acidbutt in triple sugar iron agar; and reacts positively with ornithine andlysine decarboxylase. The isolate should also be negative with esculinand salicin to separate it from certain isolates of *Serratia**liquifaciens*that do not ferment sucrose.
**Source and Reservoir of Infection**
Although *Y*. *ruckeri* was first isolated in Idaho byR. Rucker in the 1950's, it has now been established that the bacteriumwas also present in West Virginia and Australia in the 1950's (Bullocket al. 1977); consequently, the true source of the organism is unknown.Busch and Lingg (1975) showed that 25% of the rainbow trout surviving anexperimental ERM challenge became asymptomatic carriers in which thebacterium was localized in the lower intestine. Such trout serve asreservoirs of infection.
**Mode of Transmission**
Natural infections spread from fish to fish by direct contactwith infected fish or carriers. Rucker (1966) transmitted the disease byexposing healthy rainbow trout to waterborne bacteria shed by infectedtrout. Bullock et al. (1976) similarly infected Atlantic salmon (*Salmo**salar*). Vertical transmission has not been demonstrated (Dulinet al. 1976), and probably does not occur. Stressors have been shown toplay a significant role in triggering ERM outbreaks (Hunter et al.1980).
**Incubation Period**
Experimental evidence suggests that incubation time is 5 to 10days at 1315°C. In natural outbreaks, the incubation period isundoubtedly affected by environmental factors such as temperature, pH,and dissolved oxygen.
**Host and Geographic Range**
Since ERM was first reported, knowledge of the host andgeographic ranges has increased. The spread of ERM from Idaho wasoriginally associated with the transportation of carriers, and within 20years the disease had been spread to virtually all troutproducingregions of the United States and Canada. The disease has now beenreported in most European countries where trout are cultured. To datethere are no reports of ERM outbreaks in Japan, Australia, or NewZealand. The host range has also expanded to include Atlantic salmon andPacific salmon, and nonsalmonids such as emerald shiners,*Notropis atherinoides* (Mitchum 1981); fathead minnows,*Pimephales promelas* (Michel et al. 1986); goldfish, *Carassius**auratus*** (McArdle and DooleyMartyn 1985); and farmedwhitefish, *Coregonus* spp. (Rintamaki et al. 1986). Additionally,ERM infections have occurred in several farmed marine species such asturbot, *Scophthalmus maximus*; seabass, *Dicentrarchus labrax*;and seabream, *Sparus auratus* (Vigneulle 1984).
**Methods of Control*****Prevention***
Enteric redmouth disease is the first fish disease for which apractical, commercially available bacterin was developed. The firstsuccessful experimental bacterin, reported by Klontz (1963), wasintended for oral delivery. It was improved by later investigators (Rossand Klontz 1965; Anderson and Ross 1972). Anderson and Nelson (1974)then showed that injection of a bacterin was superior to oraladministration. However, injection is not practical for immunizing largenumbers of small fish.

Croy and Amend (1978) showed that fish could be immunized byimmersion in a hyperosmotic solution of sodium chloride, followed byimmersion in the bacterin. The first commercial ERM bacterin, licensedin 1976, was delivered by this procedure. Continued developments in thedelivery system showed that either simple immersion or spray applicationof bacterin resulted in protection. Cipriano and Ruppenthal (1987) foundthat brook trout (*Salvelinus**fontinalis*) immunized with *Y*. *ruckeri* ofserotypes I or II were protected against experimental challengeregardless of the serotype used for immunization. The use of commercialERM bacterin has resulted in decreased losses from the disease,decreased need for antibacterial therapy, and-surprisingly-an increasedgrowth rate in immunized fish (Amend and Eshenour 1980; Tebbitt et al.1981).

A considerable body of information is now available on theimmune response of trout to *Y*. *ruckeri* and ERM vaccines.Blazer and Wolke (1984) found that rainbow trout fed a commercial dietshowed a reduced immune response to *Y*. *ruckeri* antigensin comparison with trout fed a complete test diet. They postulated thatascorbic acid or vitamin E enhanced the immune response. Exposure oftrout to endrin adversely affected the immune response (Bennett andWolke 1987). Although humoral *Y*.*ruckeri* antibodies were not correlated with protection(Cossarini-Duner 1986; Cipriano and Ruppenthal 1987), these antibodieswere correlated with an increased rate of phagocytic ingestion of *Y*.*ruckeri* (Griffin 1983).  When salmonids are immunized by a bathprocedure, the gill pavement cells seem to play a major role in antigenuptake (Zapata et al. 1987); low (1:1000) vaccine dilution and anexposure time as long as 6 h provided the best protection (Tatner andHorne 1985). Recently Horne and Robertson (1987) developed a model thatenables the value of ERM vaccination to be determined under fieldconditions.

Tests conducted in vitro by Ross and Smith (1972) showed that 25ppm iodine of the iodophors Betadine or Wescodyne destroyed cells afteronly a 15s exposure. The authors suggested that a 5min exposure ofsalmonid eggs to 25 ppm iodine would be effective in killing ERM cells.
***Treatment***
Several antibacterials, including oxytetracycline, erythromycin,quinolones (Ceschia et al. 1987), and the potentiated sulfonamide Romet(Bullock et al. 1983), have been reported to be effective in controllingERM. Although the antibacterial tiamulin reportedly controlled ERM(Bosse and Post), it failed to control experimental*Y*. *ruckeri* infection in rainbow trout (Bullock andHerman 1988). To date no antibacterial is registered with the Food andDrug Administration for control of ERM in cultured food fish.
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Amend, D. F., K. A. Johnson, T. R. Croy, and D. H. McCarthy.1983. Some factors affecting the potency of *Yersinia**ruckeri*bacterins. J. Fish Dis. 6:337344.

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Bennett, R., and R. E. Wolke. 1987. The effect of sublethalendrin exposure on rainbow trout, *Salmo**gairdneri*Richardson. I. Evaluation of serum cortisol concentrations and immuneresponsiveness. J. Fish Biol. 31:375386.

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