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An Outbreak of Disease Caused by Francisella Sp. in Nile Tilapia Oreochromis Niloticus at a Recirculation Fish Farm in the UK

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An Outbreak of Disease Caused by Francisella Sp. in Nile Tilapia Oreochromis Niloticus at a Recirculation Fish Farm in the UK Vol. 91: 161–165, 2010 DISEASES OF AQUATIC ORGANISMS Published September 2 doi: 10.3354/dao02260 Dis Aquat Org OPENPEN ACCESSCCESS NOTE An outbreak of disease caused by Francisella sp. in Nile tilapia Oreochromis niloticus at a recirculation fish farm in the UK Keith R. Jeffery*, David Stone, Stephen W. Feist, David W. Verner-Jeffreys Centre for Environment, Fisheries and Aquaculture Science (Cefas), Barrack Road, Weymouth, Dorset DT4 8UB, UK ABSTRACT: This study details the first diagnosis of Francisella sp. in tilapia in the United Kingdom. Losses of tilapia fry at a recirculation fish farm in England were investigated, giving a presumptive positive diagnosis of infection with Francisella sp. by histopathological examination. Most fish sam- pled showed moderate to marked pathology of the major organs, with lesions being present in most tissues. The most obvious host response was granuloma formulation. A subsequent follow-up visit provided further evidence for the presence of a Francisella species. PCR amplicons were obtained using Francisella spp.-specific primers that shared 100% sequence identity with the 16S rRNA gene of the type strain of the species F. asiatica previously described as the cause of disease in tilapia in Southeast Asia and Central America. This outbreak and the subsequent investigation emphasise the importance of strict biosecurity at fish farms and the care that needs to be taken when using a new supplier of fish. KEY WORDS: Francisellosis · Tilapia · Granulomas · Recirculation Resale or republication not permitted without written consent of the publisher INTRODUCTION diseases, and vulnerability can increase with stock densities. The tilapia farming industry in England and Wales In SE Asia and Central America, for example, tilapia has seen a significant expansion in recent years. There have been affected by a granulomatous disease caused are now at least 12 recirculation systems in operation, by an intracellular bacterial pathogen (Chen et al. ranging in size from those producing just 5 tonnes of 1994). Studies have confirmed, using molecular tech- fish to those capable of producing several hundred niques, that this is caused by a Francisella sp. (Hsieh et tonnes of fish. Fully enclosed recirculation aquaculture al. 2006, Mauel et al. 2007, Ottem et al. 2009, Mikalsen has many advantages in terms of green credentials & Colquhoun in press). Bacteria from the genus Fran- such as being able to farm close to markets, control of cisella are characterised as strictly aerobic, facultatively effluent and the elimination of predators, pests and intracellular, non-motile, Gram-negative cocco bacilli. escapees. It also gives control over the elements and At least 2 closely related but distinguishable species allows optimal temperature control. Biosecurity and of Francisella cause disease in fish. F. noatensis comb. the introduction of pathogens are then under the con- nov., sp. nov. (Mikalsen & Colquhoun in press) (syn = trol of the farm manager. However, this type of site has F. philomiragia subsp. noatensis [Mikalsen 2007] and often experienced technical problems (Little et al. F. piscicida [Ottem et al. 2007]), is the cause of disease 2008). Tilapia have long been considered a species that in farmed and wild cod Gadus morhua in northern is ideal for use in aquaculture due to its hardy nature, Europe (Ottem et al. 2009) and Atlantic salmon in fast growth, tolerance of suboptimal water quality and Chile (Birkbeck et al. 2007). The second group, F. disease resistance (Little et al. 2008). However, as with noatensis subsp. orientalis subsp. nov. (Ottem et al. all species of farmed fish, tilapia are still affected by 2009) (syn = F. asiatica sp. nov. [Mikalsen & Colquhon *Email: [email protected] © Inter-Research 2010 · www.int-res.com 162 Dis Aquat Org 91: 161–165, 2010 in press]) is the cause of disease in farmed tilapia in processed in paraffin wax using standard protocols. Asia and South America (Hsieh et al. 2006, Mauel et al. Sections were cut and mounted onto glass slides before 2007), three-lined grunt Parapristipoma trilineatum in staining with haematoxylin and eosin (H&E). Sections Japan (Kamaishi et al. 2005) and a range of cichlid spe- were analysed by light microscopy (Eclipse E800, cies (Hsieh et al. 2007). Nikon) and digital images were captured using the Lucia™ Screen Measurement System (Nikon). Live fish were also selected and boxed and taken back to MATERIALS AND METHODS the Cefas laboratory for parasitological examination. At a second visit, 7 wk later, the number of unhealthy The UK Centre for Environment, Fisheries and fish in the system had declined. However, additional Aquaculture Science (Cefas) Fish Health Inspectorate samples were taken from the remaining affected fish; investigated a fish farm that was experiencing low swabs were taken from spleen, kidney and liver and in- level chronic losses of imported tilapia Oreochromis oculated onto cysteine heart agar (CHA) plates. Liver niloticus fry between 0.5 and 5 g in weight. Cumula- and spleen swabs were also taken onto Selective kid- tive losses of fry were approximately 20% of each ney disease media plates (SKDM). Further samples of batch brought onto site. The fry were being ongrown heart, liver and spleen were again taken for histology between 24 to 27°C (23.9°C at time of visit) and moved and were fixed in NBF. In addition, 10 whole fry (~0.5 g) up through the system from shallow tanks into deeper that had recently been imported and stocked into a dis- tanks and then into suspended net hapas within race- infected tank were preserved in NBF. ways before they were ready for resale. The farm’s pri- For molecular analyses, 10 samples (Sample nos. 11 mary function was ongrowing thousands of imported to 20) of combined spleen liver and heart tissue, as well fry before supply to the main grow-out sites. The fry as whole newly imported fry, were taken and immedi- had been imported and sourced from several different ately stored in absolute ethanol until analysis. Tissues sites over the year preceding the mortalities. There were removed from the ethanol, weighed and homo- was no in-house fry production, although some future genised in transport medium using a FastprepTM tissue brood-fish were held. No other species of fish were disruptor (MP Biomedicals) to give 10% w/v. Total held on site. nucleic acid was extracted from a 50 µl aliquot of the The site operated a recirculation system using large homogenate using the Virus Mini Kit (Qiagen) and the bead filters with a backwash system. Replacement EZ-1 BioRobot (Qiagen) eluting the nucleic acid in a water was supplied at approximately 2% per day. volume of 60 µl. Water quality parameters recorded over the previous Two separate PCR reactions were performed using months were within acceptable ranges for this type of Francisella-specific primers based on those of Barns et operation (e.g. total ammonia readings were <1 mg l–1, al. (2005). Mixed bases were introduced to increase the nitrite was <10 mg l–1 at a pH of 6.4). Oxygen levels range of Francisella species that could be detected were not documented, but flow rates and aeration in (Table 1). the tanks were observed to be high. PCR was performed in a 50 µl reaction volume of 1× Sick and moribund fish were collected, and a range Go Taq PCR buffer containing 2.5 mM MgCl2, 200 mM of samples were taken for the disease investigation. dNTPs, 100 pmol of the forward primer, 50 pmol each Pools of spleen, kidney and brain tissue (~1 g total) of the reverse primers, 2.5 units of Go Taq DNA poly- from each of 5 fish were placed into viral transport merase (Promega) and 2.5 µl of the nucleic acid medium, chilled and returned to the laboratory for extract. The reaction mix was overlaid with mineral oil standard cell culture techniques. Cell lines used in- and subjected to 40 temperature cycles of 1 min at cluded fathead minnow (FHM), chinook salmon em- 95°C, 1 min at 60°C and 1 min at 72°C, followed by a bryo (CHSE), striped snakehead (SSN), blue gill fry final extension step of 10 min at 72°C. Amplified prod- caudal trunk (BF) and epithelial papilloma of carp ucts were resolved on a 2% (w/v) agarose/TAE (EPC); these were inoculated and incubated at both (40 mM Tris-acetate, pH 7.2, 1 mM EDTA) gel contain- 20 and 25°C. ing 1.0 mg/ml ethidium bromide, and visualised under Swabs were taken from kidney and spleen of sick UV irradiation. fish and inoculated onto tryptone soya agar (TSA) and PCR products were purified using the Freeze ‘n river Anacker Ordal modified agar (RIVAOA) plates. Squeeze DNA purification system (Anachem), and For the purposes of pathology and ultra-structural both DNA strands were sequenced using the primers examination, tissues from kidney, spleen, gill, liver, used in the initial amplification and the ABI PRISM™ intestine, heart, eye, skin and muscle were removed dye terminator cycle sequencing system (Applied and fixed by placing in 10% neutral buffered formalin Biosystems). Sequencing was analysed using Sequen- (NBF). Whole fish were also fixed. The samples were cher software (Gene Codes). Jeffery et al.: Francisella in Nile tilapia in the UK 163 Table 1. Degenerative primers used to amplify Francisella 16S gene sequences. gills and some petechial haemorrhag- +: positive sense; –: negative sense ing on and around the pectoral fins. Internally the fish had empty intestines Primer Sequence Orientation and very large gall bladders. Seven of 10 fish had enlarged granular spleens Fr153ForU GCC CAY YWG WGG GGG ATA CC + Fr1281RevU1 GGA CTA MGA STR SCT TTM TGR GA – (Fig. 1) and a small minority had en- Fr1281RevU2 GGA CTA MGA STR SCT TTM TGR GT – larged kidneys.
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