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Piscirickettsiosis and Piscirickettsia Salmonis in Fish: a Review

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Piscirickettsiosis and Piscirickettsia Salmonis in Fish: a Review Journal of Fish Diseases 2014, 37, 163–188 doi:10.1111/jfd.12211 Review Piscirickettsiosis and Piscirickettsia salmonis in fish: a review M Rozas1,2 and R Enrıquez3 1 Faculty of Veterinary Sciences, Graduate School, Universidad Austral de Chile, Valdivia, Chile 2 Laboratory of Fish Pathology, Pathovet Ltd., Puerto Montt, Chile 3 Laboratory of Aquatic Pathology and Biotechnology, Faculty of Veterinary Sciences, Animal Pathology Institute, Universidad Austral de Chile, Valdivia, Chile prevention of and treatment for piscirickettsiosis Abstract are discussed. The bacterium Piscirickettsia salmonis is the aetio- Keywords: control, epidemiology, pathogenesis, logical agent of piscirickettsiosis a severe disease pathology, Piscirickettsia salmonis, piscirickettsiosis, that has caused major economic losses in the transmission. aquaculture industry since its appearance in 1989. Recent reports of P. salmonis or P. salmonis-like organisms in new fish hosts and geographical regions have increased interest in the bacterium. Introduction Because this gram-negative bacterium is still poorly understood, many relevant aspects of its Piscirickettsia salmonis was the first rickettsia-like life cycle, virulence and pathogenesis must be bacterium to be known as a fish pathogen (Fryer investigated before prophylactic procedures can be et al. 1992). Since the first reports of pisciricketts- properly designed. The development of effective iosis in Chile at the end of the 1980s, Piscirickett- control strategies for the disease has been limited sia-like bacteria have been frequently recognized due to a lack of knowledge about the biology, in various fish species farmed in fresh water and intracellular growth, transmission and virulence of sea water and have significantly affected the pro- the organism. Piscirickettsiosis has been difficult ductivity of aquaculture worldwide (Mauel & to control; the failure of antibiotic treatment is Miller 2002). The first record of a fish rickettsia- common, and currently used vaccines show vari- like organism (RLO) was described in fahaka puf- able long-term efficacy. This review summarizes ferfish, Tetraodon fahaka (Hasselquist 1762), that the biology and characteristics of the bacterium, originated from the Nile River in Egypt (Moham- including its virulence; the infective strategy of ed 1939). P. salmonis for survival and evasion of the host A similar rickettsial septicaemia, ‘parenthesis immune response; the host immune response to disease’, has been recognized since 1970 in salmon invasion by this pathogen; and newly described held in sea water in British Columbia, Canada features of the pathology, pathogenesis, epidemiol- (Evelyn 1992). This septicaemia was first observed ogy and transmission. Current approaches to the in 1970 and 1978 in pink salmon, Oncorhynchus gorbuscha (Walbaum 1792), that were being cul- tured in seawater tanks for experimental purposes Correspondence M Rozas Graduate School, Faculty of Veteri- nary Sciences, Universidad Austral de Chile, Isla Teja, Valdivia and was later observed in 1983 and 1984 in 5090000, Chile (e-mail: [email protected]) farmed coho, Oncorhynchus kisutch (Walbaum Ó 2013 John Wiley & Sons Ltd 163 Journal of Fish Diseases 2014, 37, 163–188 M Rozas & R Enrıquez Piscirickettsiosis review 1792), and chinook salmon, Oncorhynchus for the organism was P. salmonis (Olsen et al. tshawytscha (Walbaum 1792) (Evelyn 1992). Sub- 1997). The main histopathological finding was sequently, a similar rickettsial septicaemia was hepatic necrosis and the presence of an RLO. The described in 1991 in Atlantic salmon, Salmo salar disease was frequently recorded after algal blooms, (Linnaeus 1758), farmed in sea water in British and the smolt pens tended to be overstocked with Columbia (Brocklebank et al. 1992). Gross fish in poor condition (Olsen et al. 1997). Since pathology was consistent with the features of then, the impact of infection caused by P. salmo- piscirickettsiosis described in Chile and was similar nis on the Norwegian industry has been low, per- to pathological lesions previously noted in 1980 haps because the better quality of smolt, better in coho and chinook salmon (Evelyn 1992). Later, culture conditions and natural environmental con- a Piscirickettsia-like organism (PLO) was isolated ditions are not favourable for the bacterium or its from farmed Atlantic salmon from the eastern possible vector (Olsen et al. 1997). coast of Canada (Jones et al. 1998; Cusack, In Chile, the first outbreaks of piscirickettsiosis Groman & Jones 2002). appeared by the end of 1989, although it has been In addition, RLOs have also been recognized in suggested that the disease has been present in Atlantic salmon farmed in Ireland and Scotland, coho salmon since 1983 (Bravo & Campos United Kingdom. In Ireland, an RLO was 1989). Originally, piscirickettsiosis was described observed in connection with low-mortality disease as affecting coho salmon (Bravo & Campos 1989; in Atlantic salmon post-smolts farmed along the Cvitanich, Garate & Smith 1990, 1991; Fryer western coast in 1991 (Rodger & Drinan 1993). et al. 1990; Sch€afer et al. 1990; Branson & Nieto No pathogen was isolated, but microorganisms Dıaz-Munoz~ 1991), causing up to 90% of mortal- similar to P. salmonis were observed in different ities on certain farms (Cvitanich et al. 1990). Eco- tissues by microscopy. Between 1995 and 1996, nomic estimates conducted in 1989 determined four new outbreaks of the disease were described, losses of approximately US $10 million, represent- and an RLO was isolated using the CHSE-214 ing the mortality of approximately 1.5 million (chinook salmon embryo) cell line and confirmed coho salmon (Cvitanich et al. 1990). Subse- using anti-P. salmonis antibodies (Rodger & quently, piscirickettsiosis was also detected in Drinan 1993). Finally, the association between Atlantic salmon and rainbow trout, Oncorhynchus the isolated agent and the disease was confirmed mykiss (Walbaum 1792) (Cvitanich et al. 1991; by experimental inoculation. In the same way, an Cvitanich, Garate & Smith 1995). The disease RLO was isolated from seawater-farmed Atlantic has been mainly described in sea water and brack- salmon with high mortality in Scotland (Grant ish waters (Bravo & Campos 1989; Cvitanich et al. 1996). The main histopathological lesion et al. 1990, 1991, 1995; Fryer et al. 1990; Sch€afer was encephalitis associated with vasculitis, and a et al. 1990; Branson & Nieto Dıaz-Munoz~ 1991) great number of coccoid and basophilic microor- and, very occasionally, in fresh water (Bravo 1994; ganisms, approximately 1 lm in diameter, were Gaggero, Castro & Sandino 1995). found. The agent was isolated from brain tissue In 2006, before the infectious salmon anaemia using the CHSE-214 cell line without antibiotics (ISA) crisis in Chile, the Technological Institute and showed a cytopathic effect (CPE) at 9 days of Salmon (INTESAL) estimated that the direct post-inoculation at 15 °C; Koch’s postulates were economic losses caused by piscirickettsiosis during fulfilled. Further outbreaks of disease associated the ongrowing phase in sea water were approxi- with P. salmonis in farmed Atlantic salmon have mately US $100 million and that losses of the been described in Scotland (Birrell, Mitchell & potential concept of harvest were worth approxi- Bruno 2003; Reid, Griffen & Birkbeck 2004), mately US $400 million (Cabezas 2006). These although the incidence and impact of pisciricketts- figures represented approximately 25% of total iosis in Scotland are very low. economic revenues from salmon exports during Between 1988 and 1992, an RLO was isolated the same year. After the ISA crisis, piscirickettsio- from 51 Atlantic salmon farms along the western sis lost its key role in the health scene; today, coast of Norway (Olsen et al. 1997). In total, however, together with the productive reactivation 71% of these outbreaks occurred during the fall of the Chilean salmon industry, the disease has re- of 1988. Because of morphological and serological emerged as the main health challenge in the sec- similarities to the type strain, the suggested name tor, thereby repositioning issues that are not yet Ó 2013 John Wiley & Sons Ltd 164 Journal of Fish Diseases 2014, 37, 163–188 M Rozas & R Enrıquez Piscirickettsiosis review solved and are associated with diagnosis, treat- P. salmonis that was closely related to the salmo- ment, prevention and control (Ibieta et al. 2011). nid pathogens (McCarthy et al. 2005). Two ITS Currently, piscirickettsiosis is one of the most regions were observed in the seabass PLO, one of important threats to the sustainability of the Chil- which contained tRNA genes. ean salmon industry (Ibieta et al. 2011). Piscirick- An RLO was observed in farmed Atlantic sal- ettsiosis has evolved over time; each new outbreak mon located in south-east Tasmania, Australia is increasingly insidious and refractory to treat- (Corbeil, Hyatt & Crane 2005). Whereas 16S ments, and each has shown increased bacterial vir- rDNA sequence and phylogenetic analyses demon- ulence, clinical and pathological severity and strated that the Tasmanian RLO is related to exo- variable presentation under similar conditions of tic P. salmonis isolates, and particularly to the species, age and management measures (Leal & Chilean isolate EM-90, the Tasmanian RLO Woywood 2007; Marshall et al. 2007). In general, exhibits an ITS sequence divergence from other the salmon industry has focused its control strat- P. salmonis isolates. This divergence is principally egy for the
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