enteric redmouth disease
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IdentityTop of page
Preferred Scientific Name
- enteric redmouth disease
International Common Names
- English: bacterial septicaemia; enteric red mouth disease; enteric redmouth disease of salmonids; ERM disease; red mouth disease; red throat; redmouth; redmouth disease; redthroat; Yersinia ruckeri infections; yersiniosis
OverviewTop of page
Enteric redmouth (ERM) is an acute or chronic infection of fish caused by Yersinia ruckeri, a Gram-negative, enteric bacterium. It is present in a carrier state in many species of fish and remains undetected until stress, particularly associated with intensive culture and poor water quality, may result in heavy losses requiring immediate intervention.
Yersinia ruckeri was first isolated in the Hagerman Valley, Idaho, USA, in the early 1950s and was described fully by Ross et al. (1966) and Rucker (1966). The early terminology used to describe the disease, such as redmouth, redthroat or bacterial septicaemia, was derived from the gross clinical signs, which in many cases were caused by mixed infections of Gram-negative organisms. In other cases, where Y. ruckeri was isolated and almost certainly the causative agent, they were absent. Standardization as ‘enteric redmouth’ was made by the Fish Health Section of the American Fisheries Society in 1975 and this, with ‘yersiniosis’, remains the commonest name.
The placement of the causative agent in the genus Yersinia (Ewing et al., 1978) has also proved problematic, but this remains the accepted identifier. Since its isolation in the Hagerman Valley, ERM has either spread or been recognized in most areas of Europe and the USA where freshwater fish are cultured intensively. It may be controlled to acceptable levels by good husbandry, particularly high water quality, and it responds well to antibiotics and vaccines. Even so, it presents a constant threat, requiring management procedures and treatments which erode the profitability of the farms on which it is endemic. Losses of 10-15% over a growth cycle are not uncommon and individual outbreaks may result in much higher mortalities. In small scale, artificial challenge trials, where no intervention takes place, over 90% mortality may occur.
In spite of significant progress in certain areas, many questions concerning Y. ruckeri remain unanswered. Its taxonomic position is unclear and requires further study, probably at the molecular level. The serology is vastly complex, and consensus between different countries regarding nomenclature should be achieved. Furthermore, the methodologies on which serotyping is based need to be standardized, such that results from different laboratories may be reliably compared.
More is now known of the pathogenesis of Y. ruckeri with identification of a major temperature regulated protease (Yrp1) and catecholaate siderophore iron uptake system. A model for investigating in vivo-expressed genes has been reported and further advances are now expected in this area of understanding. A type III secretion system similar to that found in Y. enetercolitica has also been discovered, though no role for it in pathogenicity has yet been identified. Clearly with the advent of these new techniques and findings, further understanding of the processes involved in disease progression will rapidly follow.
Perhaps most importantly, the complacency resulting from the generally successful commercial vaccines must be overcome, as their mode of action and the specific antigens involved in protection are unknown. Whilst the Yrp1 protease appears to be protective, this does not seem to explain the general efficacy of commercial bacterins. Further work needs to be undertaken to determine the mechanisms of protection and cross-protection against this pathogen in salmonids and, in particular, the nature of the antigens involved. Without this vital knowledge, aquaculturists may find themselves helpless if vaccines begin to fail.
[Based upon material originally published in Woo PTK, Bruno DW, eds., 1999. Fish diseases and disorders, Vol. 3 Viral, bacterial and fungal infections. Wallingford, UK: CABI Publishing.]
Hosts/Species AffectedTop of page
The initial isolation and description of ERM was from farmed rainbow trout, Oncorhynchus mykiss (Ross et al., 1966; Rucker, 1966), but has since been isolated from many species of fish, marine and freshwater, and from other animals. Environmental samples from river water, from sewage and from dairy situations have also been found to be positive (Pritchard et al., 1995). The majority of clinical disease conditions occur in intensively cultured salmonids and it is considered primarily a disease of salmonids (Busch, 1982), but a number of other families of fish have also been found to be infected (Berc et al., 1999; Carlson et al., 2002; Danley et al., 1999; Popovic et al., 2001; Valtonen et al., 1992; Xu et al., 1991). In those species where isolations have been made without the presence of clinical signs, it is probable that such species would succumb to infection if sufficient husbandry stress were applied.
Farmed species and young age were shown to be primary risk factors in ERM outbreaks in Canada (Good et al., 2001). Brook trout (Salvelinus fontinalis) proved to be more susceptible than other species, and detection of the pathogen in the genus Salvelinus was generally more likely than in other genera included in the study (Good et al., 2001). There was a significant increase in likelihood of detection in the 1-5 month age group compared with 6-19 month or in broodstock (>20 month) (Good et al., 2001).
DistributionTop of page
Following the first recognition of Y. ruckeri in Idaho, other workers began to identify the pathogen elsewhere. McDaniel (1971) recorded its presence in sites covering most of the Rocky Mountain area of the western USA, including Alaska; Wobeser (1973) showed its presence in Canada. Much of this early apparent spread was probably genuine and resulted from the dissemination of fish throughout this area, in the absence of strict controls and monitoring schemes. Its introduction to Europe in 1983 and its subsequent spread probably occurred in the same way, and it is now known to be present over large areas of the USA and Europe (Denmark, France, Germany, Italy, Norway, Hungary, Poland, Croatia and UK). It is also present in Australia (Bullock et al., 1978; Green and Austin, 1982), South Africa (Bragg and Henton, 1986) and Chile, all of which received imported salmonid eggs and fry. However, there is some variation in the strains and serotypes within the genus associated with geographical areas and it cannot be ruled out that it is of a more widespread occurrence in a natural manner than was at first thought.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Mediterranean and Black Sea||Present||Karatas et al., 2004|
|Iran||Present||Soltani et al., 1999|
|Turkey||Present||Karatas et al., 2004|
|South Africa||Present||Bragg and Henton , 1986|
|Canada||Present||Wobeser , 1973|
|USA||Present||Present based on regional distribution.|
|-Alaska||Present||McDaniel , 1971|
|-Arkansas||Present||Danley et al., 1999|
|-Colorado||Present||McDaniel , 1971|
|-Idaho||Present||Ross and et al. , 1966; Rucker , 1966|
|-Montana||Present||McDaniel , 1971|
|-Utah||Present||McDaniel , 1971|
|-Wyoming||Present||McDaniel , 1971|
|Chile||Present||Enríquez and Zamora, 1987; Horne and Barnes , 1999|
|Peru||Present||Bravo and Kojagura, 2004|
|Croatia||Present||Oraic et al., 2002|
|Czechoslovakia (former)||Present||Vladik and Prouza, 1990|
|Denmark||Present||Horne and Barnes , 1999; Dalsgaard and Madsen, 2000|
|Finland||Present||Valtonen et al., 1992|
|France||Present||Horne and Barnes , 1999|
|Germany||Present||Horne and Barnes , 1999|
|Hungary||Present||Csaba et al., 1991|
|Italy||Present||Horne and Barnes , 1999; Lucangeli et al., 2000|
|Norway||Present||Horne and Barnes , 1999|
|Poland||Present||Popovic et al., 2001; Kozinska and Pekala, 2004|
|Portugal||Present||Sousa et al., 1996; Sousa et al., 2001|
|Spain||Present||Romalde and et al. , 1993; Rodríguez et al., 1999; Romalde et al., 2003|
|UK||Present||Horne and Barnes , 1999|
|Yugoslavia (former)||Present||Jeremic et al., 1997|
|Australia||Present||Bullock and et al. , 1978; Green and Austin , 1983|
PathologyTop of page
Internally, there is congestion of the blood-vessels throughout the peritoneum, and petechial haemorrhages, affecting liver, pancreas, swim-bladder, lateral muscles and adipose tissues associated with the pyloric caecae (Wobeser, 1973). The kidney and spleen may be swollen and there may be fluid in both the stomach and the intestine, where it has a yellowish, opaque, mucoid appearance (Busch, 1982). Light microscopy shows bacteria in virtually all tissues, particularly the kidney, heart, liver and gills. There may be severe necrosis of the haemopoietic tissues of the kidney.
Wobeser (1973), Quentel and Aldrin (1986) and Lehman et al. (1987) observed acute anaemia, with an average haematocrit as low as 23% and total serum-protein values of 2.8 g 100 ml-1. Miller (1983) attributed this to the effects of endotoxin on coagulation ultimately producing thrombosis in the capillaries and generalized haemorrhaging.
DiagnosisTop of page
The early signs of yersiniosis in the acute phases of infection are typical of many other Gram-negative bacterial septicaemias, and anorexia, darkening of the skin and lethargy almost always precede the disease, except in small fry, where virtually asymptomatic deaths may occur (Kawula et al., 1996). The reddening of the throat and mouth, caused by subcutaneous haemorrhaging and from which the disease received its name, are commonly, but not invariably, present. If the disease progresses without treatment, erosion of the jaw and palate may occur. Haemorrhage occurs on the body surface, at the gill tips, at the base of the fins and around the lateral line. Rarely, these may progress to ulcers. The vent area may also become inflamed, both externally and internally, at the distal end of the intestine. Exophthalmia has been reported in some cases in the later stages of infection, with haemorrhaging of the ocular cavity and iris (Fuhrmann et al., 1983). This has been referred to as a separate condition in Australian trout (Llewellyn, 1980).
Provisional diagnosis of yersiniosis in fish is often made on the basis of experience at a particular site, combined with the clinical signs seen in the fish. However, as indicated above, these are typical of many other Gram-negative, septicaemial infections; even the frequently cited reddening of the mouth may be absent and, in any case, is seen in other types of infection. Additionally, small fish may die virtually asymptomatically.
Confirmation of yersiniosis is most easily made by culture from tissues, particularly the spleen, heart and kidney. Widely available media, such as tryptone soya agar (TSA), sometimes supplemented with 5% blood, are the most effective. The use of a preculture procedure, where the tissue suspected to be infected is incubated in liquid media (tryptone soya broth (TSB) or TSB + blood) at 18°C for up to 48 h may increase the number of positives obtained from a population (Daly and Stevenson, 1985). If required, confirmation can be obtained by non-lethal sampling (Noga et al., 1988). The regular cyclical shedding of Y. ruckeri which has been reported to occur from the intestinal tract of carrier fish, however, may hinder isolation (Busch and Lingg, 1975). Furthermore, the populations sampled should be designed to take into account the higher prevalence in age blocks between 1-5 months (Good et al., 2001).
Attempts have been made to produce diagnostic media to aid culture (Waltman and Shotts, 1984; Rodgers, 1991b), but, as with most diagnostic selective media, growth of the target organism may be reduced in addition to the desirable reduction in growth of other species. Additionally, the requirement of this medium that Tween 80 should be hydrolysed is not met by many isolates (Austin and Austin, 1993), complicating the concept of its use. More recently, differentiation based on virulence characteristics has been used successfully (Furones et al., 1993), but, in general, standard TSA is effective and preferred for isolation (Hastings and Bruno, 1985; Rodgers and Hudson, 1985).
Identification by the determination of attributes uses traditional methods, and laboratory minikits, such as API 20E, are also used successfully (Santos et al., 1993). However, additional tests may be required here if an exact definition of the species is required, since closely related species, such as H. alvei, would not be differentiated by this method.
The use of immunodiagnostic methods has matured to the point where these may also be described as traditional. Choice may be made between monoclonal and polyclonal reagents in the protocols of these methods, although, for commercial purposes, monospecific polyclonals are more robust and problemfree. Antigen detection, using specific antibodies in enzyme-linked immunosorbent assay (ELISA) formats, has been used in both research and commercially in plate and rapid, ‘on-stick’ formats. Antibody detection by latexagglutination tests has been used to determine subclinical infections, both experimentally (Johnson et al., 1974; Hansen and Lingg, 1976) and commercially (Romalde et al., 1995).
The most recent method of detection and identification, based on the development of specific molecular probes and polymerase chain reaction (PCR), is capable of detecting extremely low levels of Y. ruckeri (Argenton et al., 1996). However, this laboratory method is not used routinely and its sensitivity generally restricts its use to special, screening situations. Problems arise in validation of this technique and in judging the relevance of the positives obtained to farm husbandry situations (Hiney and Smith, 1998).
Refined methods of molecular diagnosis have been reported (Wilson and Carson, 2003). These can detect rRNA from <10 cfu cultured Y.ruckeri and have been adapted for high throughput screening. The relevance of these assays in clinical samples has not yet been demonstrated and they are likely to suffer from the same limitations as other PCR-based methodologies.
Safest diagnoses will always be made based on combinations of observed symptoms, histology, culture along with immunological and molecular methods.
List of Symptoms/SignsTop of page
|Finfish / Build up of bloody fluids - Body Cavity and Muscle||Aquatic:Fry||Sign|
|Finfish / Cessation of feeding - Behavioural Signs||Aquatic:Adult,Aquatic:Broodstock,Aquatic:Larval||Sign|
|Finfish / Darkened coloration - Skin and Fins||Aquatic:Adult,Aquatic:Broodstock,Aquatic:Larval||Sign|
|Finfish / 'Dropsy' - distended abdomen, 'pot belly' appearance - Body||Aquatic:Fry||Sign|
|Finfish / 'Dropsy' - distended abdomen, 'pot belly' appearance - Body||Aquatic:Fry||Sign|
|Finfish / Fish swimming near surface - Behavioural Signs||Aquatic:Fry||Sign|
|Finfish / Fish swimming near surface - Behavioural Signs||Aquatic:Fry||Sign|
|Finfish / Generalised lethargy - Behavioural Signs||Aquatic:Adult,Aquatic:Broodstock,Aquatic:Larval||Sign|
|Finfish / Haemorrhagic lesions - Skin and Fins||Aquatic:Adult,Aquatic:Broodstock,Aquatic:Larval||Sign|
|Finfish / Liver - white / grey patches (haemorrhage / necrosis / tissue damage) - Organs||Aquatic:Fry||Sign|
|Finfish / Liver - white / grey patches (haemorrhage / necrosis / tissue damage) - Organs||Aquatic:Fry||Sign|
|Finfish / Mortalities -Miscellaneous||Aquatic:Fry||Sign|
|Finfish / Paleness - Gills||Aquatic:Fry||Sign|
|Finfish / Paleness - Gills||Aquatic:Fry||Sign|
|Finfish / Periorbital oedema - Eyes||Aquatic:Adult||Sign|
|Finfish / Pop-eye - Eyes||Aquatic:Adult||Sign|
Disease CourseTop of page
Many potentially pathogenic Gram-negative organisms persist in small numbers in the intestine of apparently healthy fish and remain undetected in standard health checks. Viable bacteria detected in the lymphoid tissues of fish, however, indicate that the health of the fish has been compromised, even though no external indicators of poor condition may be noticeable. Yersinia ruckeri behaves in this manner and is sometimes described as establishing a ‘carrier state’ although, in the strictest definition of this phrase, this is arguable.
Throughout the farm cycle, periodic stress factors may move the balance of advantage towards the pathogen, as the performance of the immune system and other physiological factors are reduced to suboptimal levels. Fish carrying Y. ruckeri become sluggish in behaviour, reduce diet intake and may have a darkening of the skin. Factors known to promote subclinical and clinical infection by Y. ruckeri are, predictably, handling, grading and excessive stocking densities. When infection occurs in the absence of these factors, suspended organic matter in the water, coupled with high temperatures and consequentially low oxygen, along with exposure to low levels of chemicals in the water-supply, may promote clinical disease (Bullock and Snieszko, 1975; Knittel, 1981). In conditions where Y. ruckeri is endemic, therefore, the farm cycle is characterized by rapid changes in the external appearance of the stock and persistent low mortalities from ERM. Correction of the environmental factor(s) responsible may restore the fish to health, although an antibiotic may be needed to reduce the level of loss if condition has deteriorated too far. Acute infections, if not rapidly checked, can vary between 30 and 70% of the stock. As the fish become larger, chronic, slower infections are more characteristic, but these too may reach epizootic proportions if mishandled.
It is somewhat ironic that, in spite of numerous effective vaccination regimes, little is known of the virulence determinants associated with Y. ruckeri. Perhaps this may in part be explained by the complexity of the different serogroups and the fact that relatively few studies have compared virulent and avirulent isolates within single serogroups, concentrating predominantly on comparisons between serogroups. The lack of research in this area may also reflect the early successes with vaccination against this disease, reported as early as 1965 (Ross and Klontz, 1965). Nevertheless, the data available suggest that the virulence of Y. ruckeri, as with most pathogens, is multifactorial.
Iron uptake and in vivo induced genes
Further light has been shed on the virulence mechanisms of this group of pathogens using novel molecular techniques to investigate in vivo-induced genes (Fernandez et al., 2004). Using a promoterless reporter system Fernandez et al (2004) showed that a number of genes associated with the expression and activity of the catecholate siderophore Ruckerbactin were expressed during infection and critical for high virulence; isogenic mutants lacking rucC were less virulent the wild type. Various putative transport proteins were also expressed in vivo during infection in rainbow trout (Fernandez et al., 2004).
Yrp1 serralysin metalloprotease
The Yrp 1 protease of Y. ruckeri was identified and characterized by Secades and Guijarro (1999). The gene encoding Yrp1 forms part of an operon which is regulated by temperature and osmolarity (Fernandez et al., 2003). Expression of the protease is optimal at 18°C. Interestingly, inactivated Yrp1 was protective when delivered as an immunogen by intraperitoneal injection, suggesting a key role in pathogenesis and virulence (Fernandez et al., 2003).
Type III secretion system
Type III secretion systems (TTSS) are involved in subversion of host cellular systems for direct secretion of bacterial products into host cells. Systems such as these form important components of colonization strategies for human and mammalian pathogens such as Y. pestis, Y. entercolitica, Shigella flexneri and Salmonella enterica var typhimurium, with the plasmid-mediated Yop system of Yersinia pestis being the most thoroughly studied. Components of a TTSS system with some homology to the Y. enteroclitica system have been identified in Y. ruckeri (Gunasena et al., 2003). However, the role it plays in the pathology of ERM has not been explored.
In the human pathogenic Yersinia species, Y. pestis, Y. enterocolitica and Y. pseudotuberculosis, virulence is associated with a 40-50 MDa plasmid (Skurnik, 1985). Plasmid profiling of Y. ruckeri has identified a large plasmid of 70-88 kb carried in many isolates of serovar I (de Grandis and Stevenson, 1982; Toranzo et al., 1983, Stave et al., 1987). However, this plasmid was not homologous with virulence plasmids from other yersiniae (Stave et al., 1987), although strains of serovar I carrying the plasmid decreased the chemiluminescent response of striped bass macrophages (Stave et al., 1987).
Furones et al. (1990) compared virulent and avirulent isolates of Y. ruckeri from serovar I. They reported a strong correlation between the production of a heatsensitive factor (HSF), probably lipid in nature, and virulence. Indeed when trout were infected by bath or intraperitoneal injection, only HSF+ isolates resulted in mortality. However, mortalities during bath challenge were variable and the study concluded that other factors must also be involved.
Resistance to Non-Specific Immune Mechanisms
Strains of Y. pestis carrying the 40-50 MDa plasmid produce antiphagocytic factors, which reduce the oxidative microbicidal activity of mouse macrophages (Charnetzky and Shuford, 1985), as determined by chemiluminescent (CL) response. Stave et al. (1987) reported that serovar I isolates of Y. ruckeri harbouring a 70 MDa plasmid also depleted the CL response of striped bass, Morone saxatilis, macrophages, although the factors expressed by the plasmid were not determined. Furthermore, one of the serovar II isolates, which did not carry the plasmid, also showed a decreased CL response in striped bass macrophages. The decreased CL response may reflect the method used.
Chemiluminescent assays detect reactive oxygen species (ROS); it may be that the reduced CL response results from quenching of ROS by bacterial enzymes, such as superoxide dismutase (SOD) and catalase. Indeed, all serovar I isolates analysed contain at least one superoxide dismutase enzyme, depending on the growth conditions. These enzymes may in themselves be important virulence factors, increasing resistance to phagocytic killing. It remains to be determined whether they are plasmid- or chromosomally encoded.
In addition to resistance to macrophage bactericidal activity, virulent serovar I isolates of Y. ruckeri are reported to be resistant to killing by non-immune rainbow trout serum, while avirulent serovar I isolates are sensitive (Davies, 1991b). However, not all serum-resistant isolates are virulent, reaffirming the multifactorial nature of virulence.
Yersinia ruckeri has been reported to produce water-soluble antimicrobial activity capable of inhibiting Vibrio anguillarum, Aeromonas hydrophila and Aeromonas salmonicida (Michel and Faivre, 1987). This is not without precedent, as strains of Y. pestis produce a potent murein-hydrolysing bacteriocin, pesticin (Ferber and Brubaker, 1979). However, the activity produced by Y. ruckeri does not inhibit other strains of Y. ruckeri and, as such, does not fulfil the criteria of a bacteriocin (Michel and Faivre, 1987), although it is important to state that it is unclear which serotypes were used in this study. Whether or not the production of antimicrobial activity confers a genuine selective advantage on Y. ruckeri remains contentious, as mixed infections with both A. salmonicida and V. anguillarum could be obtained experimentally in rainbow trout (Michel and Faivre, 1987).
Survival Under Starvation Conditions
Survival under conditions of starvation is important to pathogenesis in two ways. Firstly, the organism is at an advantage if it can survive outside the host for extended periods to facilitate transmission. In this respect, Y. ruckeri is capable of surviving in unsupplemented fresh or brackish water (salinity 0-20 p.p.t.) for at least 4 months, while survival is greatly reduced in water of salinity 35 ppt. (Thorsen et al., 1992). Furthermore, Romalde et al. (1994) reported that Y. ruckeri was capable of survival for over 100 days in river water, lake water, estuarine water and sediments. While acridine orange direct counts remained constant, viable counts decreased over the experimental period, with culturable cells persisting for longer periods in sediments than in water (Romalde et al., 1994). In all cases, dormant bacteria could be revived by addition of fresh TSB to the microcosms and virulence was maintained throughout the dormant state. Although non-culturable cells showed marked changes in shape, size and metabolic rate, no changes were reported in membrane proteins or plasmid profiles, while minor changes were detected in LPS (Romalde et al., 1994). Long-term survival may be facilitated by replication of the genome before the onset of starvation is complete, with starved cells being able to carry up to six copies of the genome (Thorsen et al., 1992). The second important factor is the ability to acquire iron during the early stages of infection. Availability of iron in the host is largely restricted by its association with iron-binding proteins, such as haemoglobin and transferrin. The ability of a pathogen to acquire iron is therefore of utmost importance. It has been reported that Y. ruckeri has a siderophore-mediated iron-uptake system, along with several outer membrane proteins associated with iron-restricted growth conditions (Romalde et al., 1991a).
Other putative virulence-associated factors which have been studied in Y. ruckeri include cell-surface hydrophobicity and haemagglutination. Santos et al. (1990) reported no haemagglutinating activity against human or trout erythrocytes for all serovar I and II strains tested. This study also reported a lack of hydrophobicity and no adherence to epithelioma papillosum cyprini (EPC) cells for the same strains. However, adherence would appear to be dependent upon the cell line used in the study, with Y. ruckeri strains showing moderate adhesion and invasiveness in the chinook salmon embryo cell line CHSE-214 (Romalde and Toranzo, 1993). In addition, Romalde and Toranzo (1993) reported that extracellular products from Y. ruckeri were strongly toxic for fish, and displayed haemolytic activities for trout, salmon, sheep and human erythrocytes.
In conclusion, the pathogenicity of Y. ruckeri is poorly understood, predominantly as a result of the scarcity of good data. This lack of data may reflect the general view that yersiniosis represents ‘a problem solved’ through the early success of vaccination regimes. However, the limited data that are available suggest that pathogenesis is complex and multifactorial, and highlights the necessity for further study of this organism.
Although Y. ruckeri O-antigen has been used as a model antigen for the study of the kinetics of immune responses in rainbow trout (Anderson et al., 1979a,b,c) and carp (Lamers and Muiswinkel, 1984), little is known of the key antigenic components of Y. ruckeri to which the fish responds during infection or following vaccination.
The kinetics of the antibody response to O-antigen has been thoroughly documented in rainbow trout. Peak numbers of antibody-producing cells are detected in the spleen 14 days after antigen administration by flush. The titres of circulating antibody increase to a maximum after about 28 days, with the onset of detection coinciding with maximum numbers of antibody producing cells (Anderson et al., 1979c). Immunization of rainbow trout, using commercial Y. ruckeri bacterin, also demonstrated a significant secondary response to antigen injected intraperitoneally 146 days after first exposure (Cossarini- Dunier, 1986a). This demonstration of an anamnestic immune response to Y. ruckeri in rainbow trout is important. However, there is a lack of correlation between antibody titre and protection; Cipriano and Ruppenthal (1987) found that, although humoral agglutinins were detected in brook trout 24 h after passive immunization by intraperitoneal injection with immune sera, these antibodies conferred no resistance to disease. Furthermore, Lillehaug et al. (1996) demonstrated that protection in fry could not be achieved by passive transfer of antibodies maternally. Brood-stock females were vaccinated repeatedly by injection, and an increase in antibody titre, determined by ELISA and agglutination, was obtained against serovars I and II in the serum of vaccinated fish. Low levels were also detected in eggs and fry 1 week posthatching, although mortalities were not reduced in the offspring of vaccinated mothers compared with unvaccinated controls. This suggests that other immune mechanisms, such as a localized or cell-mediated response, must be involved in protection against yersiniosis.
Cell-mediated response to Y. ruckeri has been less thoroughly studied. Jones et al. (1993) reported that killed cells of serovar I and serovar II strains stimulated proliferation of naïve peripheral-blood leucocytes, and that the two strains were similarly mitogenic. However, the study concluded that this was irrespective of the immune status of the fish.
Antibodies produced by rainbow trout appear to be serotype-specific (Cipriano and Ruppenthal, 1987). Furthermore, antibodies against serovar I do not recognize LPS in immunoblot, while those raised against 0:2/serovar II do bind LPS (Stevenson et al., 1993). Additionally, a significantly higher dose of Oantigen from serovar I is required to elicit a response in rainbow trout than with O-antigen from serovar II (Anderson and Dixon, 1980).
In spite of the serological differences between Y. ruckeri serovars, there are numerous reports of cross protection. Indeed, Cipriano and Ruppenthal (1987) reported that, although immunization by intraperitoneal injection with bacterins against Y. ruckeri resulted in circulating antibody only to the specific serovar used in the bacterin, brook trout immunized in such a manner were protected during experimental challenge with both serovars I and II. Furthermore, a bacterin prepared from an avirulent serovar II isolate performed equally well compared with bacterins produced from virulent isolates (Cipriano and Ruppenthal, 1987). It is unlikely that this is a result of non-specific crossprotection, as Amend and Johnson (1984) reported that there was no antigenic competition between Y. ruckeri, A. salmonicida, V. anguillarum and Renibacterium salmoninarum when administered to rainbow trout. The antigens responsible for cross-protection have not yet been clearly identified; however, a recent review suggested that native flagellar antigens seem to be antigenically common among motile serogroups (Stevenson, 1997). In addition, Fernandez et al. (2003) reported high protective efficacy of heat inactivated Yrp1 protease from Y.ruckeri. However, most commercial vaccines are produced at temperatures where Yrp1 expression would be minimal to non-existent, and are formalin inactivated, so these observations do not explain the efficacy of commercial bacterins.
The generally successful vaccination of salmonids against yersiniosis using bacterins based on serovar I and the numerous studies reporting cross-protection have perhaps led to a degree of complacency and a general consideration that other serovars are unnecessary in commercial vaccines (McCarthy and Johnson, 1982). With regard to the latter, as reported above, experience in Norway has suggested otherwise (Erdal, 1989).
EpidemiologyTop of page
Transmission of the Disease
Early work and descriptions of the disease were made by those working in salmonid aquaculture, leading to the concept of yersiniosis as primarily a disease of salmonids. Confirmed clinical outbreaks were seen in both trout (rainbow, steelhead, cutthroat, brown and brook) and in salmon (coho, sockeye and Atlantic) (Busch, 1982). Early epizootics in these species have been described in detail by Ross et al. (1966), Rucker (1966) and Busch (1973). It has been recognized that the host range of Y. ruckeri is more diverse. Whether it is capable of a saprophytic existence as a part of the environmental flora outside a host is a matter of debate; Rucker (1966) suggested that this may be the case, but later authors, such as Klontz and Huddlestone (1976), argued against this. Their findings reflected those seen for many other Gram-negative coliforms, including E. coli and Aeromonas salmonicida, where the survival in clean water in a laboratory experiment may be a matter of hours, but may be prolonged for 2-3 months in sediments or where there is organic matter present (Romalde et al., 1994). This allows transmission from fish to fish under natural conditions without the need to propose that the organism has lived saprophytically outside an animal host.
Whilst birds have been implicated as vectors (Willumsen, 1989), the prime source of infection is generally considered to be the shedding of large numbers of bacteria from carrier or infected fish in the faeces. Such fish do not normally shed quantities capable of causing infection, unless stressed (Hunter et al., 1980). The level of carrier fish in a population depends on the criteria and methods used. Busch and Lingg (1975) demonstrated that, 45 days postinfection, 25% of a population of rainbow trout carried Y. ruckeri asymptomatically in the lower intestine. The preculture/culture method used in this case is sensitive and the data may reflect a situation in fish following the first serious epizootic in a population. However, where a detailed investigation is made, using culture, immunological and molecular methods together, in a population grown under normal farm conditions for several months, a much higher proportion of individuals is found to be positive and it is not improbable that all are actually carrying the pathogen. Once infected, therefore, a fish population can maintain the pathogen indefinitely.
Yersinia ruckeri has also been isolated from brood stock, which are frequently, if not always, infected, but transmission through eggs where disinfection has been properly carried out has not been reported (Dulin et al., 1976).
Conditions predisposing populations to clinical infection relate primarily to stress. Healthy laboratory populations can withstand exposure to high numbers of cells without succumbing to clinical disease (Ross et al., 1966). Infection may occur where fish are obese through poor feeding regimes, but poor water quality is the prime cause. Common causes are high ammonia, due to poor water flow or too high densities, low oxygen, due to poor flow and high temperatures, or the presence of a high level of suspended organic and siliceous matter (Bullock and Snieszko, 1975). When these conditions are marginal, handling stress may trigger infections where the fish would have remained healthy if left untouched. The expectation of trouble, therefore, is in summer conditions, where temperatures rise and water flows are reduced. The peak is considered to be 15-18°C, and monitoring oxygen and temperatures daily is an effective warning system where yersiniosis is endemic. Infections have not been reported below 10°C.
Impact SummaryTop of page
|Fisheries / aquaculture||Negative|
Impact: EconomicTop of page
The British Trout Association estimated losses of £1.3-1.5 million in 1998. However, vaccines against ERM are generally effective, so in regions where vaccination is routinely used, the impacts of ERM are limited. Elsewhere it can be managed to a degree through use of good biosecurity practices and antibiotic treatments.
Impact: EnvironmentalTop of page
Yersinia ruckeri is not widely reported to cause significant wild fish kills. Treatment of diseased farm stock with antibiotics clearly has serious environmental implications. Use of vaccines and best practice can eliminate this impact.
Zoonoses and Food SafetyTop of page
Yersinia ruckeri is not reported to be zoonotic and as any isolates are unable to initiate growth at 37°C (de Grandis et al., 1988) this would appear to be an unlikely scenario. There have not been any reports of food safety issues related to Y. ruckeri.
ReferencesTop of page
Amend DF, Johnson KA, 1984. Evidence for lack of antigenic competition among various combinations of Vibrio anguillarum, Yersinia ruckeri, Aeromonas salmonicida and Renibacterium salmoninarum bacterins when administered to salmonid fishes. Journal of Fish Diseases, 7(4):293-299; 13 ref.
Anderson DP, Dixon OW, 1980. Immunological memory in rainbow trout to a fish disease bacterin administered by flush exposure. In: Manning MJ, ed. Phylogeny of Immune Memory. Amsterdam: Elsevier, 103-109.
Anderson DP, Dixon OW, Roberson BS, 1979. Kinetics of the primary immune response in rainbow trout after flush exposure to Yersinia ruckeri O-antigen. Developmental and Comparative Immunology, 3(4):739-744.
Anderson DP, Robertson BS, Dixon OW, 1979. Cellular immune response in rainbow trout Salmo gairdneri Richardson to Yersinia ruckeri O-antigen monitored by the passive haemolytic plaque assay test. Journal of Fish Diseases, 2(3):169-178.
Argenton F, Mas Sde, Malocco C, Dalla Valle L, Giorgetti G, Colombo L, 1996. Use of random DNA amplification to generate specific molecular probes for hybridization tests and PCR-based diagnosis of Yersinia ruckeri. Diseases of Aquatic Organisms, 24(2):121-127; 22 ref.
Austin B, Austin D, 1993. Bacterial Fish Pathogens: Disease in Farmed and Wild Fish, 2nd edition. UK: Ellis Horwood, 208-226.
Bercovoer H, Mollaret HH, 1984. Genus XIV. Yersinia. In: Krieg NR, ed. Bergey's Manual of Systematic Bacteriology. Vol. 1. Williams and Wilkins Company, 498-506.
Betoulle S, Troutaud D, Khan N, Deschaux P, 1995. Antibody response, cortisol and prolactin levels in rainbow-trout. Comptes Rendus de l’Académie des Sciences Série III - Sciences de la Vie - Life Sciences, 318(6):677-681.
Bravo S, Kojagura V, 2004. First isolation of Yersinia ruckeri from rainbow trout in Peru. Bulletin of the European Association of Fish Pathologists, 24:104-108.
Bruno DW, Munro ALS, 1989. Immunity in Atlantic salmon, Salmo salar L., fry following vaccination against Yersinia ruckeri, and the influence of body weight and infectious pancreatic necrosis virus (IPNV) on the detection of carriers. Aquaculture, 81(3-4):205-211; 12 ref.
Bullock GL, Anderson DP, 1984. Immunization against Yersinia ruckeri, cause of enteric redmouth disease [of salmonid fish]. Symposium on fish vaccination, Paris, 20-22 February 1984., 151-166; [Discussion pp. 228-229]; 48 ref.
Bullock GL, Snieszko SF, 1975. Hagerman Redmouth, a Disease of Salmonids Caused by a Member of the Enterobacteriaceae. Fish Disease Leaflet 42, United States Department of the Interior, Fish and Wildlife Service, 1-5.
Bullock GL, Stuckey HM, Shotts EBJr, 1978. Enteric redmouth bacterium: comparison of isolates from different geographic areas. Journal of Fish Diseases, 1(4):351-356.
Busch RA, 1974. The serological surveillance of salmonid populations for presumptive evidence of specific disease association. Dissertation Abstracts International, 34B(No.8):3579.
Busch RA, 1978. Protective vaccines for mass immunisation of trout. Salmonid, 1:10-22.
Busch RA, 1983. Enteric redmouth disease (Yersinia ruckeri). Les antigènes des micro-organismes pathogènes des poissons, symposium international. [Antigens of fish pathogens, international symposium] Talloires, France, 10-12 May 1982., 201-222; [Discussion p.223]; 57 ref.
Busch RA, Lingg AJ, 1975. Establishment of an asymptomatic carrier state infection of enteric redmouth disease in rainbow trout (Salmo gairdneri). Journal of the Fisheries Research Board of Canada, 32(12):2429-2432.
Carlson EA, Li Y, Zelikoff JT, 2002. Exposure of Japanese medaka (Oryzias latipes) to benzo[a]pyrene suppresses immune function and host resistance against bacterial challenge. Aquatic Toxicology, 56(4):289-301.
Charnetzky WT, Shuford WW, 1985. Survival and growth of Yersinia pestis within macrophages and an effect of the loss of the 47-megadalton plasmid on growth in macrophages. Infection and Immunity, 47:234-241.
Cipriano RC, Ruppenthal T, 1987. Immunization of salmonids against Yersinia ruckeri: significance of humoral immunity and cross protection between serotypes. Journal of Wildlife Diseases, 23(4):545-550; 32 ref.
Cipriano RC, Schill WB, Pyle SW, Horner R, 1986. An epizootic in chinook salmon (Oncorhynchus tshawytscha) caused by a sorbitol-positive serovar 2 strain of Yersinia ruckeri. Journal of Wildlife Diseases, 22(4):488-492; 26 ref.
Cossarini-Dunier M, 1986. Protection against enteric redmouth disease in rainbow trout, Salmo gairdneri Richardson, after vaccination with Yersinia ruckeri bacterin. Journal of Fish Diseases, 9(1):27-33; 16 ref.
Cossarini-Dunier M, 1986. Secondary response of rainbow trout (Salmo gairdneri Richardson) to DNP-haemocyanin and Yersinia ruckeri. Aquaculture, 52(2):81-86; 19 ref.
Csaba G, Szakolezai J, Toth L, 1991. Redmouth disease of trout in Hungary. Magyar Allatorvosok Lapja, 46:395-401.
Dales RP, Kalac Y, 1992. Phagocytic defence by the earthworm, Eisenia foetida, against certain pathogenic bacteria. Comparative Biochemistry and Physiology A - Comparative Physiology, 101:487-490.
Danley ML, Goodwin AE, Killian HS, 1999. Epizootics in farm-raised channel catfish, Ictalurus punctatus (Rafinesque), caused by the enteric redmouth bacterium Yersinia ruckeri. Journal of Fish Diseases, 22(6):451-456; 26 ref.
de Grandis SA, Stevenson RMW, 1982. Variation in plasmid profiles and growth characteristics of Yersinia ruckeri strains. FEMS Microbiology Letters, 15:199-202.
Dulin MP, Huddlestone TR, Larson R, Klontz G, 1976. Enteric Redmouth Disease. Bulletin 8, Forest Wildlife and Range Experimental Station, University of Idaho, 15 pp.
Ellis AE, 1988. Vaccination against enteric redmouth (ERM). Fish vaccination., 85-92; 29 ref.
Erdal JI, 1989. Vaccination against common infectious disease of fish. Norsk Veterinærtidsskrift, 101(6):489-495; 4 ref.
Farmer JJ, Davies BR, Hickman-Brenner FW, McWhorter A, Huntley-Carter GP, et al, 1985. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. Journal of Clinical Microbiology, 21:46-76.
Ferber DM, Brubaker RR, 1979. Mode of action of pesticin: N-acetylglucosaminidase activity. Journal of Bacteriology, 139:506-511.
Fernandez L, Lopez JR, Secades P, Menendez A, Marquez I, Guijarro JA, 2003. In vitro and in vivo studies of the Yrp1 protease from Yersinia ruckeri and its role in protective immunity against enteric red mouth disease of salmonids. Applied and Environmental Microbiology, 69(12):7328-7335.
Fernandez L, Marquez I, Guijarro JA, 2004. Identification of a specific in vivo-induced (ivi) genes in Yersinia ruckeri and analysis of ruckerbactin, a catecholate siderophore iron acquisition system. Applied and Environmental Microbiology, 70:5199-5207.
Fuhrmann H, Böhm KH, Schlotfeldt H-J, 1984. On the importance of enteric bacteria in the bacteriology of freshwater fish. Bulletin of the European Association of Fish Pathologists, 4(3):42-46; 13 ref.
Furones MD, Gilpin MJ, Alderman DJ, Munn CB, 1990. Virulence of Yersinia ruckeri serotype I strains is associated with a heat sensitive factor (HSF) in cell extracts. FEMS Microbiology Letters, 66(1-3):339-344; 12 ref.
Furones MD, Gilpin ML, Munn CB, 1993. Culture media for the differentiation of isolates of Yersinia ruckeri, based on detection of a virulence factor. Journal of Applied Bacteriology, 74(4):360-366; 30 ref.
Good CM, Thorburn MA, Stevenson RMW, 2001. Host factors associated with the detection of Aeromonas salmonicida and Yersinia ruckeri in Ontario, Canada government fish hatcheries. Preventive Veterinary Medicine, 49(3/4):165-173.
Grandis SAde, Krell PJ, Flett DE, Stevenson RMW, 1988. Deoxyribonucleic acid relatedness of serovars of Yersinia ruckeri, the enteric redmouth bacterium. International Journal of Systematic Bacteriology, 38(1):49-55; 25 ref.
Gunasena DK, Komrower JR, MacIntyre S, 2003. The fish pathogen Yersinia ruckeri possesses a TTS system. Advances in Experimental medicine and Biology, 529:105-107.
Hastings TS, Bruno DW, 1985. Enteric redmouth disease: survey in Scotland and evaluation of a new medium, Shotts-Waltman, for differentiating Yersinia ruckeri. Bulletin of the European Association of Fish Pathologists, 5(2):32-35; 5 ref.
Hiney MP, Smith PR, 1998. DNA based diagnostics in aquaculture: can we overcome the problems of interpretation in the field? In: Barnes AC, Davidson GA, Hiney MP, McIntosh D, eds. Methodology in Fish Diseases Research. Aberdeen: Fisheries Research Services, 143-159.
Horne MT, Barnes AC, 1999. Enteric redmouth disease (Yersinia ruckeri). Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections., 455-477; 7 pp of ref.
Hunter VA, Knittel MD, Fryer JL, 1980. Stress-induced transmission of Yersinia ruckeri infection from carriers to recipient steelhead trout Salmo gairdneri Richardson. Journal of Fish Diseases, 3(6):467-472.
Ibrahim A, Goebel BM, Liesack W, Griffiths M, Stackebrandt E, 1993. The phylogeny of the genus Yersinia based on 16s rDNA sequences. FEMS Microbiology Letters, 114:173-178.
Jeremic S, Veljovic LJ, Andelic D, 1997. Biochemical and serological characteristics of Yersinia ruckeri which causse typical and atypical infections in California trout (Oncorhynchus mykiss). Acta Veterinaria, Beograd, 47:345-351.
Johnson GR, Wobeser G, Rouse BT, 1974. Indirect fluorescent antibody technique for detection of RM bacterium of rainbow trout (Salmo gairdneri). Journal of the Fisheries Research Board of Canada, 31(12):1957-1959.
Jones SRM, Stevenson RMW, Paterson WD, 1993. Proliferation of rainbow trout (Oncorhynchus mykiss) lymphocytes in response to the bacterial pathogen, Yersinia ruckeri. Bulletin of the Aquaculture Association of Canada, No. 4:93-95; 7 ref.
Karatas S, Candan A, Demircan D, 2004. Enteric Redmouth Disease in cultured rainbow trout (oncorhynchus mykiss) on the Black Sea coast of Turkey. Bamidgeh, 56:226-231.
Kawula TH, Lelivelt MJ, Orndorff PE, 1996. Using a new inbred fish model and cultured fish tissue cells to study Aeromonas hydrophila and Yersinia ruckeri pathogenesis. Microbial Pathogenesis, 20(2):119-125; 12 ref.
Klontz GW, Huddlestone TR, 1976. Control of Enteric Redmouth Disease: a Twelve Month Activity Report on Contract 10690004 DEMO-1014. Moscow, Idaho.
Kozinska A, Pekala A, 2004. Prevelance of Yersinia rucckeri in salmonid fish in Poland and the phenotype characteristics of isolates. Medycyna Weterynaryjna, 60:880-882.
Lamers CHJ, Muiswinkel WB, 1984. Primary and secondary immune responses in carp (Cyprinus carpio) after administration of Y. ruckeri O-antigen. In: Fish Diseases, Proceedings of 4th COPRAQ. Madrid: ATP, 119-127.
Lehman J, Sturenberg FJ, Mock D, 1987. The changes in haemogram of rainbow trout (Salmo gairdneri, Richardson) to an artificial and natural challenge with Yersinia ruckeri. Journal of Applied Ichthyology, 3:174-183.
Lillehaug A, Sevatdal S, Endal T, 1996. Passive transfer of specific maternal immunity does not protect Atlantic salmon (Salmo salar L.) fry against yersiniosis. Fish & Shellfish Immunology, 6(7):521-535; 37 ref.
Liltved H, Hektoen H, Efraimsen H, 1995. Inactivation of bacterial and viral fish pathogens by ozonation or UV irradiation in water of different salinity. Aquacultural Engineering, 14(2):107-122; 28 ref.
Liltved H, Landfald B, 1996. Influence of liquid holding recovery and photoreactivation on survival of ultraviolet-irradiated fish pathogenic bacteria. Water Research (Oxford), 30(5):1109-1114; 29 ref.
Llewellyn LC, 1980. A bacterium with similarities to the redmouth bacterium and Serratia liquefaciens (Grimes and Hennerty) causing mortalities in hatchery reared salmonids in Australia. Journal of Fish Diseases, 3(1):29-39.
Lucangeli C, Morabito S, Caprioli A, Achene L, Busani L, Mazzolini E, Fabris A, Macrì A, 2000. Molecular fingerprinting of strains of Yersinia ruckeri serovar O1 and Photobacterium damsela subsp. piscicida isolated in Italy. Veterinary Microbiology, 76(3):273-281.
Martinsen B, Oppegaard H, WichstrOm R, Myhr E, 1992. Temperature-dependent in vitro antimicrobial activity of four 4-quinolones and oxytetracycline against bacteria pathogenic to fish. Antimicrobial Agents and Chemotherapy, 36(8):1738-1743; 32 ref.
McArdle JF, Dooley-Martyn C, 1985. Isolation of Yersinia ruckeri type I (Hagerman strain) from goldfish Carassium auratus. (L). Bulletin of the European Association of Fish Pathologists, 5(1):10-11; 7 ref.
McDaniel DW, 1971. Hagerman redmouth. American Fisheries US Trout News, 15:14-28.
Michel C, Faivre B, Kinkelin Pde, 1986. A clinical case of enteric redmouth in minnows (Pimephales promelas) imported in Europe as bait-fish. Bulletin of the European Association of Fish Pathologists, 6(4):97-99; 8 ref.
Miller T, 1983. Blood coagulation in ERM infected trout: role of bacterial endotoxin. In: Proceedings of the 8th Annual FHS/AFS Workshop, Kearneysville, West Virginia, USA, 48.
Mitchum DL, 1981. Concurrent infections: ERM and furunculosis found in emerald shiners. FHS/AFS Fish Health Newsletter, 9:2.
Noga EJ, Levine JF, Townsend K, Bullis RA, Carlson CP, Corbett WT, 1988. Kidney biopsy: a nonlethal method for diagnosing Yersinia ruckeri infection (enteric redmouth disease) in rainbow trout (Salmo gairdneri). American Journal of Veterinary Research, 49(3):363-365; 11 ref.
O’Leary PJ, 1977. Enteric redmouth of salmonids: a biochemical and serological comparison of selected isolates. MSc thesis. Corvallis: Oregon State University.
Popovic NT, Hacmanjek M, Teskeredzic E, 2001. Health status of rudd (Scardinius erythrophthalmus hesperidicus H.) in Lake Vrana on the Island of Cres, Croatia. Journal of Applied Ichthyology, 17(1):43-45.
Pritchard TJ, Beliveau CM, Flanders KJ, Donnelly CW, 1995. Environmental surveillance of dairy processing plants for the presence of Yersinia species. Journal of Food Protection, 58:395-397.
Quentel C, Aldrin JF, 1986. Blood changes following intraperitoneal inoculation of Yersinia ruckeri in catheterized rainbow trout, Salmo gairdneri. Aquaculture, 53(3/4):169-185; 29 ref.
Rintamäki P, Valtonen ET, Frerichs GN, 1986. Occurrence of Yersinia ruckeri infection in farmed whitefish, Coregonus peled Gmelin and Coregonus muksun Pallas, and Atlantic salmon, Salmo salar L., in northern Finland. Journal of Fish Diseases, 9(2):137-140; 9 ref.
Rodgers CJ, Hudson EB, 1985. A comparison of two methods for isolation of Yersinia ruckeri from rainbow trout (Salmo gairdneri). Bulletin of the European Association of Fish Pathologists, 5(4):92-93; 3 ref.
Rodríguez LA, Castillo A, Gallardo CS, Nieto TP, 1999. Outbreaks of Yersinia ruckeri in rainbow trout in north west of Spain. Bulletin of the European Association of Fish Pathologists, 19(3):130-132; 19 ref.
Romalde JL, Barja JL, Magarinos B, Toranzo AE, 1994. Starvation-survival processes of the bacterial fish pathogen Yersinia ruckeri. Systematic and Applied Microbiology, 17:161-168.
Romalde JL, Iteman I, Carniel E, 1991. Use of pulsed field gel electrophoresis to size the chromosome of the bacterial fish pathogen Yersinia ruckeri.. FEMS Microbiology Letters, 84(2):217-226; 31 ref.
Romalde JL, Magarinos B, Barja JL, Toranzo AE, 1993. Antigenic and molecular characterisation of Yersinia ruckeri. Systematic and Applied Microbiology, 16:411-419.
Romalde JL, Magarinos B, Fouz B, Bandín I, Núnez S, Toranzo AE, 1995. Evaluation of BIONOR mono-kits for rapid detection of bacterial fish pathogens. Diseases of Aquatic Organisms, 21(1):25-34; 32 ref.
Ross AJ, Klontz GW, 1965. Oral immunisation of rainbow trout (Salmo gairdneri) against an etiological agent of ‘redmouth disease’. Journal of Fisheries Research Board of Canada, 22:713-719.
Ross AJ, Rucker RR, Ewing W, 1966. Description of a bacterium associated with redmouth disease of rainbow trout (Salmo gairdneri). Canadian Journal of Microbiology, 12:763-770.
Rucker AJ, 1966. Redmouth disease of rainbow trout (Salmo gairdneri). Bulletin de l’Office International des Epizooties, 65:825-830.
Santos Y, Bandin I, Nieto TP, Bruno DW, Ellis AE, Toranzo AE, 1990. Comparison of the cell surface hydrophobicity of bacterial fish pathogens by different procedures. Pathology in marine science. Proceedings of the Third International Colloquium on Pathology in Marine Aquaculture, held in Gloucester Point, Virginia, October 2-6, 1988., 101-115; 23 ref.
Santos Y, Romalde JL, Bandín I, Magarinos S, Núnez S, Barja JL, Toranzo AE, 1993. Usefulness of the API-20E system for the identification of bacterial fish pathogens. Aquaculture, 116(2/3):111-120; 18 ref.
Secades P, Guijarro JA, 1999. Purification and characterization of an extracellular protease from the fish pathogen Yersinia ruckeri and effect of culture conditions on production. Applied and Environmental Microbiology, 65(9):3969-3975.
Siwicki AK, Dunier M, 1993. Quantification of antibody secreting cells to Yersinia ruckeri by ELISPOT assay after in vivo and in vitro immunization of rainbow trout (Oncorhynchus mykiss). Veterinary Immunology and Immunopathology, 37(1):73-80; 9 ref.
Skurnik M, 1985. Expression of antigens encoded by the virulence plasmid of Yersinia enterocolitica under different growth conditions. Infection and Immunity, 47:183-190.
Sousa JA, Magarinos B, Eiras JC, Toranzo AE, Romalde JL, 2001. Molecular characterization of Portuguese strains of Yersinia ruckeri isolated from fish culture systems. Journal of Fish Diseases, 24(3):151-159.
Sousa JA, Romalde JL, Ledo A, Eiras JC, Barja JL, Toranzo AE, 1996. Health status of two salmonid aquaculture facilities in North Portugal: characterization of the bacterial and viral pathogens causing notifiable diseases. Journal of Fish Diseases, 19(1):83-89; 28 ref.
Stevenson R, Flett D, Raymon BT, 1993. Enteric redmouth (ERM) and other enterobacterial infections. In: Inglis V, Roberts RI, Bromage NR, eds. Bacterial Diseases of Fish. Edinburgh: Blackwell Scientific Publications, 80-106.
Stevenson RMW, 1997. Immunization with bacterial antigens: yersiniosis. Developments in Biological Standardization, 90:117-124; 41 ref.
Tebbit GL, Erikson JD, Vandewater RB, 1981. Development and use of Yersinia ruckeri vaccines to control enteric redmouth disease. In: International Symposium on Fish Biologics: Serodiagnostics and Fish Vaccines, Leetown, West Virginia. Developments in Biological Standardisation, Vol. 49, 395-401.
Thorsen BK, Enger O, Norland S, Hoff KA, 1992. Long-term starvation survival of Yersinia ruckeri at different salinities studied by microscopical and flow cytometric methods. Applied and Environmental Microbiology, 58(5):1624-1628; 37 ref.
Torroba M, Anderson DP, Dixon OW, Casares F, Varas A, Alonso L, Delmoral MG, Zapata AG, 1993. In vitro antigen trapping by gill cells of rainbow trout - an immunohistochemical study. Histology and Histopathology, 8(2):363-367.
Vladik P, Prouza A, 1990. The finding of Yersinia ruckeri in rainbow trout in Czechoslovakia. Verinarni Medicina, 35:437-442.
Vuillaume A, Brun R, Chene P, Sochon E, Lesel R, 1987. First isolation of Yersinia ruckeri from sturgeon, Acipenser baeri Brandt, in South West of France. Bulletin of the European Association of Fish Pathologists, 7(1):18-19; 6 ref.
Waltman WD, Shotts EB, 1984. A medium for the isolation and differentiation of Yersinia ruckeri. Canadian Journal of Fisheries and Aquatic Sciences, 41:804-806.
Willumsen B, 1989. Birds and wild fish as potential vectors of Yersinia ruckeri.. Fish Diseases, 12(3):275-277; 7 ref.
Wilson T, Carson J, 2003. Development of sensitive, high-throughput one-tube RT PCR enzyme hybridisation assay to detect selected bacterial fish pathogens. Diseases of Aquatic Organisms, 54(2):127-134.
Wobeser G, 1973. An outbreak of redmouth disease in rainbow trout (Salmo gairdneri) in Saskatchewan. Journal of the Fisheries Research Board of Canada, 30(No.4):571-575; [2 plates].
Xu BH, Chen YS, Wu YS, 1991. An outbreak of a new epizootic in silver carp and bighead carp - Yersinia ruckeri, a new pathogen of silver carp and bighead. Chinese Science Bulletin, 36:1825-1828.
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