Iranian Journal of Fisheries Sciences 16(4)1135-1156 2017

Enteric redmouth disease: Past, present and future: A review

Zorriehzahra M.J.1; Adel M.1*; Torabi Delshad S.2

Received: October 2015 Accepted: December 2016

Abstract Enteric red mouth disease (also known as ) is one of the most significant bacterial infections in coldwater farms that cause significant mortalities and economical losses in the salmonids fish farms, especially in (Oncorhynchus mykiss). ERM is caused by the gram negative pathogen ruckeri that has five O-serotypes (O1, O2, O5, O6 and O7), five outer membrane protein types (OMP types 1–5) and two biotypes 1 and 2. The disease has a wide geographical distribution in various fresh or sea water fish. More than twenty species mainly of Salmonide origin have been affected and this number is likely to rise in the future following the introduction of new species and the increase of aquaculture trade. The disease can affect fish of all age classes but is most acute in small fish up to fingerling size. Affected fish may reveal different clinical symptoms depending on species, age and temperature. The most characteristic and common clinical signs of the disease include lethargic behavior and inactivity, swimming near the surface, anorexia, and darkening of the skin. The reddening of the throat and mouth, caused by subcutaneous haemorrhaging and exophthalmos are commonly present. Different diagnostic methods have been used for Y. ruckeri, including culturing, serological,

Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 biochemical tests, histopathological studies and molecular techniques. This review summarizes the past, present and future state of yersiniosis with emphasis on status of this disese in Iran. Also, some criteria in diagnosis, control and prevention of ERM were discussed.

Keywords: Enteric redmouth disease, Yersinia ruckeri, Diagnosis, Control and preventation

1- Iranian Fisheries Sciences Research Institute (IFSRI), Agricultural Research Education and Extension Organization (AREEO), P.O. Box: 13185-116, Tehran, Iran. 2- Department of Aquatic Animal Health and Diseases, School of Veterinary Medicine, Shiraz University, P.O. Box 1585-71345, Shiraz, Iran. *Corresponded author’s Email:[email protected]

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Introduction salmonid fish species, reared in both Enteric redmouth disease (ERM) or fresh and marine waters, especially Yersiniosis is a systemic bacterial rainbow trout (Austin and Austin, 2003; infection and one of the most Fadaeifard et al., 2011). significant diseases in farmed fish, especially salmonids (Gregory et al., Aetiology 2010). Yersiniosis is caused by Gram- Morphological and genomic negative bacteria that belonged to a characteristics member of the family Y. ruckeri is a gram-negative rod with with the name of rounded ends of 0.5-0.8 × 1.0-3.0 μm in Yersinia ruckeri (Argenton et al., 1996; size (Gregory et al., 2010). This Soltani et al., 2014). The pathogen was bacterium does not form endospores, a first isolated from rainbow trout capsule is not present, but often has Oncorhynchus mykiss, in the Hagerman flagella and Y. ruckeri strains show Valley of Idaho, USA, in the 1950s variable motility (Bastardo et al., 2011). (Rucker, 1966). At present, Yersiniosis It was demonstrated that Y. ruckeri has been isolated from different isolates had a G + C ratio of 47.5- continent including the USA (Arias et 48.5% (Ewing et al., 1978). al., 2007; Bastardo et al., 2011; Haig et Several studies showed that Y. ruckeri al., 2011), Europe (Austin et al., 2003; is a highly clonal and biochemically Fouz et al., 2006; Tobback et al., 2007; homogeneous species (Wheeler et al., Wheeler et al., 2009; Welch et al., 2009). At present, five O-serotypes 2011; Chettri et al., 2013), Australia (O1, O2, O5, O6 and O7), five outer (Carson and Wilson, 2002; Keeling et membrane protein types (OMP types 1– al., 2012(, Africa (Hussein et al., 1997; 5) and two biotypes of Y. ruckeri are Eissa et al., 2008) and Asia recognized. Romalde et al. (1993) Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 (Zorriehzahra et al., 2002; Akhlaghi proposed that serovar O1 can be and Sharifi, 2008; Adel et al., 2013; subdivided into two subgroups O1a Soltani et al., 2014; Fadaeifard et al., (previously serovar I) and O1b (serovar 2014). Yersiniosis is the second III) and serovar O2 (serovar II) into bacterial disease in coldwater fish farms three subgroups O2a, O2b and O2c. in Iran and 15 epidemic outbreaks of Biotype 1 strains are positive for this bacterial disease were reported in motility and lipase activity, whereas the country’s provinces especially from biotype 2 strains are negative for both Mazandaran, Tehran, Lorestan and tests (Strom-Bestor et al., 2010; Kumar Chaharmal Bakhtiari provinces during et al., 2015). 2012-2013 (Zorriehzahra et al., 2012; Results showed that, most epizootics Soltani et al., 2014). The bacterium and mortality of Yersiniosis are caused responsible for economic losses is by biotype 1 strains (Garcia et al., numerous in salmonid and non- 1998; Arias et al., 2007). In addition, Y.

Iranian Journal of Fisheries Sciences 16(4) 2017 1137

ruckeri strains can be grouped into Taxonomic characterization and clonal types on the basis of biotype, phylogenetic analysis serotype and outer membrane protein The taxonomic position of Y. ruckeri (OMP) type into 6 major clonal groups. has been subject to debate since its first Clonal group 5 isolates (include the classification in the genus Yersinia by Hagerman type strain) are the most Ewing et al. (1978). This study prevalent cause of Yersiniosis in demonstrated that Y. ruckeri isolates mainland Europe and the US, while had a G+C ratio of 47.5 - 48.5%, and on clonal group 2 isolates are responsible this basis it would be included in the for ERM in the UK (Davies, 1991; genus Yersinia. Other researchers found Fouz et al., 2006). that the biochemical characteristics of It was confirmed that, clonal groups Y. ruckeri have more similarities with 2 and 5 are predominantly associated Serratia and Salmonella (Llewellyn, with rainbow trout. Strains of serotypes 1980). This bacterium with 47.5–48% O1a (classic serovar I) and O2b (classic G + C (Fouz et al., 2006) differs clearly serovar II) cause most epizootic from Serratia species (52–60% G+C) outbreaks, and serotype O1a (heat- and is closer to other Yersiniae (46– stable O1 antigen) is predominant in 50% G+C). cultured salmonids (Arias et al., 2007). Kotetishvili et al. (2005) used Annotated whole genome sequences of multilocus sequence typing (MLST), two strains of Y. ruckeri are currently and considered that Y. ruckeri was the available: the motile CSF007-82 strain, most genetically distant species within isolated from diseased rainbow trout the genus Yersinia, and that the and the motile O1b 37551 strain, taxonomic status possibly needs to be isolated from vaccinated Atlantic reassessed (Wheeler et al., 2009). From (Salmo salar) (Navas et al., the results of many studies and the Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 2014; Nelson et al., 2015). In previous similarities with many other members studies, several virulence mechanisms of the Enterobacteriaceae, Y. ruckeri of Y. ruckeri including: extra-cellular could possibly belong to its own products (such as the iron-regulated separate genus. DNA studies based on Serratia-like haemolysin YhlA, guanine plus cytosine percentage azocasein protease, 47 kDa content of total DNA initially resulted metalloprotease Yrp1), yrpA and yrpB in classification of this organismas as a (Secades and Guijarro, 1999) and a heat new species of Yersinia (Kotetishvili et sensitive factor (HSF) have been al., 2005). Several studies identified (Navais et al., 2014). demonstrating heterogeneity in biochemical (Daly et al., 1986) and antigenic characteristics resulted in Y. ruckeri isolates being classified (Davies 1138 Zorriehzahra et al., Enteric redmouth disease: Past, present and future: A review

and Frerichs, 1989) into five serovars is most acute in small fish up to (Wheeler et al., 2009). fingerling size (Tobback, 2009; Şeker et Molecular analysis based on nucleic al., 2011). Pre-acute to acute infection acid hybridization and sequence usually occurs in the spring and in the analysis of 16S rDNA of the Y. ruckeri beginning of summer, during periods of genome has been conducted to rising water temperatures (Eissa et al., determine the phylogeny of this 2008; Şeker et al., 2011). Acute to sub- organism (Ibrahim et al., 1993). Based acute infections usually appear in on DNA hybridization and G 1+C yearling fish in the fall and early winter ratios, Y. ruckeri was found to be only with declining water temperatures 30% related to other Yersiniae and (Eissa et al., 2008). The acute Serratia, however, 16S rDNA epizootics can result in severe similarities between Y.ruckeri and other mortalities (30-70%) depending on the Yersiniae was as high as 98.3% size of fish, stress condition, water (Ibrahim et al., 1993). Dot-blot DNA temperature and individual hybridization assays also demonstrated susceptibility and are also assiocaited a high level of genetic relatedness with strain virulence (Furones et al., among Y. ruckeri serovars (Kotetishvili 1993; Noga, 2010). et al., 2005). Like other bacterial septicaemia there are no specific early signs of Hosts and geographical distribution disease for ERM except in small fry, Yersiniosis is one of the most common where mortality may be seen without diseases in salmonids, especially in clinical signs (Altinok et al., 2001). juvenile rainbow trout, but it was also Observable signs (Fig. 1) of the disease reported from seawater in several other include lethargic behavior and fish species, and in both farmed and inactivity (Tobback et al., 2007; Austin Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 wild fish. Some of the host species of and Austin, 2012), swimming near the Yersinia ruckeri are shown in Table 1. surface (Keeling et al., 2012), anorexia Y. ruckeri is highly contagious and has (Carson and Wilson, 2002), darkening been reported in several fish species in of the skin (Woo and Bruno, 2011). North and South America, Australia, Prolapse and hemorrhages in the anus New Zealand, Africa, Europe and Asia has been observed in many cases and especially in Iran and Turkey (Tobback could be counted as a specific sign for et al., 2007; Keeling et al., 2012; ERM (Seker et al., 2011). Fish infected Soltani et al., 2014). with Y. ruckeri are often jadish and found in areas of low flow. Clinical signs Redmouth disease takes place as acute to chronic forms (Woo and Bruno, 2011; Kumar et al., 2015). Yersiniosis Iranian Journal of Fisheries Sciences 16(4) 2017 1139

Table 1: Some of the host species of Yersinia ruckeri. Common name Scientific name Reference Rainbow trout Oncorhynchus mykiss (Chettri et al., 2013; Fadaeifard et al., 2014; Soltani et al., 2014, etc.) Arctic charr Salvelinus alpines (Tinsley, 2010) Atlantic salmon Salmo salar (Rintamäki et al., 1986; Valtonen et al., 1992; Bastardo et al., 2011) Cod Gadus morhua (Tinsley, 2010) Coalfish Pollachius virens (Michel et al., 1986) Sturgeon Acipenser sturio Vuillaume et al., 1987 Amur Sturgeon Acipenser schrencki (Shaowu et al., 2013) Sole Soleidae sp. (Michel et al., 1986) Nile tilapia Oreochromis niloticus (Eissa et al., 2008) Brown trout Salmo trutta Mc Daniel, 1971) Gudgeon Gobio gobio (McDaniel, 1971) Turbot Scophthalmus maximus (Michel et al., 1986) Goldfish Carassius auratus (McArdle and Dooley-Martyn, 1985) Common carp Cyprinus carpio (Fuhrmann et al., 1983; Berc et al., 1999) Indian major carp Cirrhinus mrigala (Manna et al., 2003) Eel Anguilla Anguilla (Fuhrmann et al., 1983) Pike Esox lucius (McDaniel, 1971) African catfish Clarias gariepinus (Abd-El Latief, 2001) Minnows Pimephales promelas (Michel et al., 1986) Channel catfish Ictalurus punctatus (Danley et al., 1999) Sea bass Dicentrarchus labrax (Savas and Ture, 2007) Char Salvelinus leucomaenis (Sakai et al., 2012) Whitespotted char Salvelinus leucomaenis (Sakai et al., 2012)

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Figure 1: Hemorrhage and red spots in mouth cavity (A), darkening and exophtalmia (B), hemorrhage and abdominal distention (C, d) of naturally Yersinia ruckeri infected rainbow trout (Zorriehzahra et al., 2002; Adel et al., 2015).

1140 Zorriehzahra et al., Enteric redmouth disease: Past, present and future: A review

Also, fish with chronic Yersiniosis may Tissue tropism display dark pigmentation (Fig. 1) or Similar to other septicemic bacterial depigmentation in the skin (Tobback et diseases, Y. ruckeri causes generalised al., 2007). haemorrhaging over the external and The reddening of the throat and internal organs. Tissues tropism of mouth cavity resulted from yersinosis has seen in hematopoietic subcutaneous haemorrhaging and from organs including anterior and posterior which it has led to its present name kidney, liver and spleen. But in the (Carson and Wilson, 2002; Woo and chronic or acute forms of Yersiniosis, Bruno, 2011). Haemorrhages are found histopathological changes were on the external surface, at the base of observed in other organs such as the fins, at the gill tips, and around the stomach, intestine, pyloric cecae, lateral line (Bastardo et al., 2011; pancreas, swim blader, body muscles Huang et al., 2013). The involved fins and etc. (Zorriehzahra et al., 2009; in the haemorrhagic congestion Fadaeifard et al., 2014). comprise the pectoral and pelvic, anal caudal fins (Carson and Wilson, 2002; Transmission routes Seker et al., 2011). Shaowu et al. Transmission is primarily horizontal (2013) observed that the disease in from fish to fish by direct contact with Amur sturgeon (Acipenser schrencki) infected fish or carriers. The role of fish showed obvious hemorrhages carrier fish is important during Y. around the mouth, at the lower jaw, the ruckeri infections. Diffirent studies base of the pectoral fins, the abdomen, showed that wild animals, such as birds, and the urogenital pore as the main wild fish, invertebrates and even external signs. humans could act as vectors for Y. In atypical infections of ruckeri (Tinsley, 2010). Hunter et al. Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 hemorrhages are observed on the mouth (1980) discussed the importance of and gill operculum (Bullock and stress inducted transmission of Y. Cipriano, 1990; Woo and Bruno, 2011); ruckeri from asymptomatic carriers to fish sometimes show abnormal healthy fish. It was found that the behavior and may become dark and organism was shed in the faeces over swim near the surface (Bullock and 36-40 day cycles. The organism may Cipriano, 1990) thus lack of classic remain for up to 2 months in pond mud ‘redmouth’ does not deny infection (Tinsley, 2010). Y. ruckeri has been with Y. ruckeri (Tobback et al., 2007). recovered from the aquatic There are frank patches of environment, including water, faeces haemorrhagic congestion on the iris of and sewage sludge and from human bile the eye, is a feature for the epithet (Farmer et al., 1985; Coquet et al., salmonid blood spot disease (Carson 2002). Results showed while and Wilson, 2002; Keeling et al., 2012). asymptomatic fish can remain carriers Iranian Journal of Fisheries Sciences 16(4) 2017 1141

for an indefinite period of time, major diameter were observed. Also, Y. stressors, such as an increase in ruckeri grows readily on MacConkey temperature, can trigger an increase of agar and Xylose Lysine Desoxycholate pathogen shedding and increase the (XLD) agar. In addition, this bacterium probability of horizontal transmission to can tolerate bile salts, the selective healthy fish (Hunter et al., 1980). component in a number of media used Vertical transmission has not been for the isolation of enteropathogenic demonstrated (Tinsley, 2010), and Enterobacteriaceae. probably does not occur. Although, Y. The Shotts-Waltman medium is a ruckeri from chinook salmon semi-selective indicator medium for Y. (Oncorhynchus tshawytscha) eggs was ruckeri, with inhibitory properties reported, highlighting that vertical equivalent to MacConkey agar (Shotts, transmission could be a possibility; 1991). The indicator is based on the further evidence of this issue has not ability of Y. ruckeri to hydrolyse Tween yet been provided (Tinsley, 2010). 80, and inability to produce acid from Although, the presence of Y. ruckeri sucrose (Shotts, 1991). In secondary DNA in ovarian fluids and unfertilized infection with other bacteria, samples eggs of Chinook salmon should also be cultured on plates of (Oncorhynchus tshawytscha) indicates XLD agar (Oxoid CM469) or that vertical transmission of the Y. preferably Ribose Ornithine ruckeri from females to their progeny is Desoxycholate agar (ROD), a possible (Richard et al., 2014). moderately selective indicator medium for Y. ruckeri (Tinsley, 2010). Also, Diagnostic methods ROD can be useful for the detection of Different diagnostic methods have been Y. ruckeri in faeces of carrier fish and used for Y. ruckeri, including culturing, can detect both biotypes 1 and 2 Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 serological, biochemical tests, (Tinsley, 2010). The density of Y. histopathology studies and molecular ruckeri in faecal samples tends to be techniques (Altinok et al., 2001; low in carriers and, typically, few Kubilay and Timur, 2001; Bastardo et colonies of Y. ruckeri will be evident on al., 2012; Kumar et al., 2015). culture plates. Yersinia Selective Agar is a Media culture isolation selective and differential medium Y. ruckeri can be grown on simple supporting good growth of Y. ruckeri culture media such as blood agar and and some Yersinia spp such as Y. Tryptone Soya Agar (TSA) that is are enterocolitica (Fig. 2). commonly media for identification of bacteria (Fig. 2). After incubation for 48 h at 25°C, off-white, opaque colonies of approximately 2-3 mm in 1142 Zorriehzahra et al., Enteric redmouth disease: Past, present and future: A review

Figure 2: Pure culture of Yersinia ruckeri on Yersinia selective agar (CIN Agar Base/Schiemann Medium Base) (A) and Tryptic Soy Agar (B) after incubation at 25°C for 48 hours (Zorriehzahra et al., 2013).

Yersinia Selective Agar was first Gills: described by Schiemann (1979) as an In gill tissue often hypotrophy and alternative to MacConkey Agar and hyperplasia of the epithelial cells on the other commonly used media for filaments and lamellae were observed isolation of Y. ruckeri, a causative agent along with lamellae destruction that of Yersiniosis. leads to fusion and clubbing (Fig. 3). Furthermore, capillary dilatation of the Histopathology assay lamellae and diffused haemorrhages in The histopathology assay could be a both the lamellae and filaments could supportive diagnosis method regarding be observed (Adel et al., 2014). the lack of pathognomonic lesions in Kidney: Yersiniosis. According to obtained Obvious changes could be found in the

Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 findings in recent years, the most posterior kidney. Pathological sections important histopathological changes in were revealing large amounts of varied tissues could be distinguished as congestion with blood suggesting loss follows: of haemopoeitic tissue. Noticeable Skin: changes in kidney tubule structure in Skin of infected rainbow trout shows an sample later into the infection are due increase in mucus cells that has a to slight interstitial haemopoeitic relation with marked epidermal hyperplasia. So, glomerular nephritis, hyperplasia. Also, thinning of the melanin deposits and destruction of the stratum spongiosum and red muscle renal tubules could occur. Also, severe degradation was observed (Tobback et necrosis may be seen in the al., 2009). haemopoietic tissues of anterior and posterior parts of the kidney (Tobback et al., 2009; Woo and Bruno, 2011).

Iranian Journal of Fishereis Sciences 16(4) 2017 1143

Figure 3: Hyperplasia (A) necrosis and lifting of the pilar cell (B) in gill tissue of rainbow trout infected by yersiniosis (Adel et al., 2014, H&E. X40).

Furthermore, pyknotic cells in the culturing, serological tests and lumen and glomerulus are observed, molecular biological techniques suggesting that the cells are going (Tobback, 2009). Some methods may through apoptosis. Basophilic immature be used in detecting Y. ruckeri such as kidney tubules are often visible, enzyme-linked immunosorbent assay highlighting signs of regeneration. (ELISA), agglutination test and Melano-macrophages cells in the immunofluorescence antibody kidney often increase throughout the technique (IFAT), based on serological course of the infection (Mahjoor and characteristics (Tobback, 2009; Woo Akhlaghi, 2012). and Bruno, 2011). Liver: Since leukocyte phagocytosis, Liver sections often displayed marked antibody production and lymphocyte areas of necrosis with diffused areas proliferation are activated in fish lipidosis of hepatocytes. So, hyperplasia infected by Y. ruckeri (Tobback et al., Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 of necrotic foci and blood congestion 2007), ELISA can be important to should be anticipated (Tinsley, 2010). detect and determine amount of specific Heart: antibodies in fish. Antigen detection has Pathological observations in rainbow been utilised either in studies or trout heart originated from infection commercially in plate using specific procedure. So, hyperplasia of the antibodies in ELISA formats (Romalde epicardium and myocardial necrosis are et al., 1995). observed in acute infectious cases (Avci Enzyme linked immunosorbent et al., 2005). assays (ELISA) have been improved to detect antibodies against Y. ruckeri in Enzyme-Linked Immunosorbent assays rainbow trout. The tests have proved to (ELISA) be more sensitive than the agglutination Different diagnostic methods have been test (Olesen, 1991; Furones et al., 1993; developed for Y. ruckeri, including Tobback et al., 2007).

1144 Zorriehzahra et al., Enteric redmouth disease: Past, present and future: A review

In a study, the quick diagnosis of Molecular assays clinical cases of ERM using a Nowadays, Polymerase Chain Reaction monoclonal antibody-based ELISA (PCR) has been able to represent a indicated value of a novel approach widely-used alternative to traditional using a dipstick-ELISA which was a identification methods (Eissa et al., method easily adaptable for field use. 2008). Many of them are based on the However, it was investigated the amplification of 16S ribosomal RNA technique was used for the confirmation (16S rRNA) genes (Fig. 5), to find out of clinical cases of ERM and didn’t various bacterial fish pathogens have usage for finding sub-clinically (Bastardo et al., 2012; Fadaeifard et al., infected or carrier fish. Probably 2014). This PCR assay is able to because of this lack of sensitivity, the demonstrate low amounts of Y. ruckeri ELISA method has not been greatly and provides the possibility to find used in the diagnostic field (Furones et asymptomatic carrier fish, this matter is al., 1993). highly important in order to inhibit the transmission and release of ERM into Immunofluorescence antibody test the environment (Tobback et al., 2007). (IFAT) It has been recommended that Immunofluorescence antibody test is an isolation in pure culture, afterwards important method for screening of Y. identification, by amplification and ruckeri (Kubilay and Timur, 2001). In sequencing of the 16S rRNA gene using this method by preparing the universal bacterial primers 27F and histopathological sections from the 1492R as the gold standard provide a kidney or other tissues such as spleen, very strong diagnostic method (Woo liver, and staining with specialized and Bruno, 2011). Also 16S rDNA PCR Immunofluorescence technique assay has been employed to identify or Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 indicates the localized bacteria in confirm the presence of Y. ruckeri in kidney and haematopoietic tissues (Fig. several studies (Akhlaghi and Sharifi, 4). The binding of antibodies to target 2008; Bastardo et al., 2012). tissues, cells or organisms can be Altinok et al. (2001) evaluated a visualized if those antibodies are PCR method for detecting Y. ruckeri, in directly coupled to a fluorochrome or the blood of rainbow trout. In this indirectly bound by a fluorescent study, the authors demonstrated that a reagent. Fluorochromes emit visible non-lethal blood sample can be used light (of an ‘emission’ wavelength) with PCR to find Y. ruckeri. Şeker et al. when exposed to light of a different (2011) extracted DNA from blood wavelength, usually in the ultraviolet samples and carried out PCR range (Kubilay and Timur, 2001). amplification based upon a pair of Y. ruckeri specific primers, as well.

Iranian Journal of Fishereis Sciences 16(4) 2017 1145

Figure 4: IFAT assay to diagnosis of Yersinia ruckeri isolated from rainbow trout (x 40, Zorriehzahra et al., 2013).

Figure 5: Electerophoretic analysis (2% agarose gel) of DNA amplified fragments from 8 isolates in this experiment. M: marker (100 bp), Lane 1: negative control, Lane 2: the isolated bacteria (409 bp), Lane 3: positive control, (Adel et al., 2013).

However, the quantitative PCR (qPCR) levels of pathogen load prior to Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 method is speedily replacing other significant losses (Taylor et al., 2009). molecular techniques for detecting the Thus, real-time qPCR methods would nucleic acids of pathogens (Purcell et be used for the detection of several fish al., 2011). This method is abe to detect pathogens such as Y. ruckeri (Glenn et and quantify DNA targets by scanning al., 2011; Bastardo et al., 2012). PCR product accumulation in the Several researchers have developed, a beginning of exponential phase of real-time primer/probe set for detecting amplification, shown by increased and quantifying the amount of Y. fluorescence (Bastardo et al., 2012). ruckeri DNA found in various samples QPCR assays can be used to detect the of fish exposed to Y. ruckeri (Glenn et pathogen within fish tissues, which can al., 2011; Zorriehzahra et al., 2013). be useful to investigate a continuous Intraspecific genetic diversity among carrier state or the beginning of an Chilean Y. ruckeri strains can be epizootic by comparison with threshold indicated using genotyping analyses by

1146 Zorriehzahra et al., Enteric redmouth disease: Past, present and future: A review

enterobacterial repetitive intergenic variable dosage, failure to complete the consensus (ERIC-) and repetitive recommended course or by repeated extragenic palindromic (REP-) PCR short term treatment,will probably lead methods (Bastardo et al., 2011). Huang to selection for drug resistance et al. (2013) in another study, (Rodgers, 2001). characterized Y. ruckeri originated from rainbow trout by biochemical profiling, Vaccination 16S rDNA sequencing, repetitive Vaccines against ERM are one of the sequence-based PCRs, including (GTG) success scenarios of disease control in 5 -PCR, BOX-PCR, ERIC-PCR and aquaculture, with the first commercial REP-PCR. product released in 1976 and are composed of formalin-killed whole Treatment, control and prevention bacterial cells. Soltani et al. (2013) methods expressed to establish a new native Antimicrobial compounds vaccine against Y. ruckeri that could The use of antimicrobial compounds protect sensitive rainbow trout in Iran. has been implemented in the treatment The level of mortality in immunized of Y. ruckeri infections in fish since groups was in the range of 10-20% several years ago (Gudding and Van within 10 weeks after vaccination, in Muiswinkel, 2013). Rucker (1966) contrast to those of control group was described treatment with in range 56.7-73.3% (p<0.05). sulphamethazine for 5 days, followed Tinsley et al. (2011) and Deshmukh by three days of chloramphenicol or et al. (2012) developed a bivalent oxytetracycline administration. Indeed, vaccine using formalin inactivated sulphonamide therapy has been of great biotypes 1 and biotype 2 Y. ruckeri value in the treatment of both strains that provides good protection Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 experimental and natural cases (Bullock against the biotype 2 strains in rainbow et al., 1983). Furthermore, Rodgers and trout. New vaccines have been Austin (1983) used oxolinic acid for developed that are based on the Y. prophylaxis and treatment of ruckeri Yrp1 protease, aroA gene, Yersiniosis in rainbow trout. Although extracellular product and Y. ruckeri is susceptible to various lipopolysaccharide and these provide antibiotics, there is acquired resistance good protection against Y. ruckeri of Y.ruckeri strains to many biotype 1 strains which are antimicrobial compounds. Post (1987) administered by several routes such as reported the absolute resistance of some immersion, injection and oral isolates of Y.ruckeri in the USA to (Deshmukh et al., 2014; Ispir and therapeutic levels of both Dorucu, 2014). Nowadays, some non- sulphamerazine and oxytetracycline. By motile strains seem to be unaffected by exposing bacteria to inadequate or commercial vaccines (Kim and Austin, Iranian Journal of Fisheries Sciences 16(4) 2017 1147

2006; Fouz et al., 2006). Thus, novel pathogens. The findings of Adel (2014) ways based on subunits or DNA demonstrated that the use of M. piperita vaccines might be an additional extract, particularly at the rate of 3% approach to eliminate or minimize this can increase the survival rate of diasease. Recently, attention to the use rainbow trout when exposed to Y. of live attenuated vaccines against ruckeri. Some researchers have bacterial pathogens in fish has examined antibacterial activity of increased, because they can provide Zataria multiflora, Nigella sativa, effective protection. Totally, they Scutellaria multicaulis, Punica reduce a greater cell-mediated response granatum, Olea europaea, Echinacea than bacterins, although the higher purpurea (Alishahi, 2012) Lavandula immunity caused by attenuated bacteria officinalis, Melissa officinalis, Ocimum in comparison with that provided by basilicum, Origanum vulgare, killed organisms is likely due to the Rosmarinus officinalis and Salvia induced expression of stress proteins officinalis on Y. ruckeri in in vitro (Temprano, 2005). condition (Bulfon, 2014). Application of certain probiotics to Immunostimulants reared trout enhanced their survival Recently, interest in the use of natural when exposed to Y. ruckeri. immunostimulants in the protection of Administration of feeds supplemented fish against bacterial fish pathogens has with Bacillus subtilis and B. increased. In addition, resistance to licheniformis (4 x 104 spores g-1 feed) bacterial pathogens can be improved by raised resistance in rainbow trout administration of immunostimulants to against withering caused by Y. ruckeri increase the effectiveness of vaccines. (Raida, 2003). Similarly, feed β-hydroxy-β-methylbutyrate (HMB) is supplemented with Carnobacterium Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 a breakdown product of the amino acid maltaromaticum or C. divergens dosed leucine which is an essential building at>107 cells g-1 feed also induced unit of proteins in all tissues and protection against challenge with Y. provided a positive immunostimulatory ruckeri because these cultures improved effect after in vivo immunization of cellular and humoral immune defences rainbow trout with anti-Y. ruckeri (Kim and Austin, 2006). When rainbow vaccine (Raida, 2003). trout fed with 108 cells Enterobacter Immunostimulating effects against Y. cloacae and Bacillus mojavensis g-1 ruckeri were also observed in rainbow feed for 60 days, it led to a significant trout using levamisole bathing (Ispir enhanced survival of the fish after bath and Yonar, 2007). Nowadays, herbal challenge with Y. ruckeri (Capkin and plants as immunostimulant agents are Altinok, 2009). Moreover, Abbas used in many countries such as Iran, (2010) showed that biotype 2 infections India, China, etc. against fish of Y. ruckeri could be inhibited by 1148 Zorriehzahra et al., Enteric redmouth disease: Past, present and future: A review

cellular components of certain probiotic consists of appropriate water quality, bacteria. high quality feeding, quarantine requirements, reduction of stress and Future prospects fish density, use of effective vaccine, Despite passing almost 50 years after probiotics, prebiotics and the first report of the ERM disease immunostimulants that should be (Rucker, 1966), some important issues considered as practical important still remain unresolved or not fully parameters in the control and understood, particularly those prevention of Yersiniosis in the fish concerned with the mechanisms of hatchery and rearing farms. transmission, disease spreading and the More attention should also be role of asymptomatic carrier fish. addressed in the future to interactions Furthermore, in some cases of Y. and exchanges of pathogens, between ruckeri occurrence, the possibility of farmed and wild populations, to assess vertical transmission has been the risk of transmission of infection suggested; nevertheless it has not yet from one environment to another. been definitively demonstrated whether Despite all attempts that can be it is a real vertical transmission or, performed and the more restrictive rather, a phenomenon of egg shell measures taken, it is estimated that the contamination which is more probably optimal solution can be acquired only what will happen. If so, it would be just when an effective and commercial a matter of finding an effective vaccine will be available. So, more disinfection procedure, which can studies are needed on the molecular inhibit the transmission of the disease epidemiological sights to produce from affected broodfish to their effective protection against ERM. offspring and produced eggs (green Moreover, using suitable health Downloaded from jifro.ir at 20:32 +0330 on Saturday September 25th 2021 eggs and eyed eggs). management strategy, besides Otherwise, in the presence of a true development of educational programs vertical transmission, the only choice to should be considered to share prevent infection in the larval and information and awareness of fish juvenile stages will be based farmers to new developmental exclusively on the identification and equipment and achievements. elimination of subclinical infected broodfish, as well as the need for Acknowledgements disinfection of water coming into the Many thanks are due to our colleagues hatchery and cultured fish farms. in IFSRI for their collaboration in data Generally, good health management collection for this article. strategy could play the most important role in control and prevention. Furthermore, good farm management Iranian Journal of Fisheries Sciences 16(4) 2017 1149

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