Lorna Ann Munro

Epidemiological investigation into the re-emergence and control of an outbreak of infectious salmon anaemia in the Shetland Islands, Scotland.

Infectious salmon anaemia (ISA) is an orthomyxoviral disease, primarily affecting marine-phase farmed Atlantic salmon, which can result in high levels of mortality. ISA first emerged in Norway in the 1980s and subsequently has occurred in Canada, the USA, the Faeroe Islands and Chile. An outbreak occurred in Scotland in 1998-1999, but was eradicated at a cost of over pounds sterling 20M. The epidemiology of a new outbreak of ISA in the Scottish Shetland Islands during 2008-2009 is described. Six sites have been confirmed ISA-positive. Spread of the virus via transport of fish between marine sites, harvest vessels, smolts and wild fish appears to have been of little or no importance, with spread primarily associated with marine water currents. The use of management areas by Marine Scotland to control the event appears to have been effective in restricting spread to a small area. This localised outbreak contrasts with the 1998-1999 outbreak that spread over a wide geographic area with transported fish and harvest vessels. The development and application of industry codes of good practice, good husbandry and biosecurity practices, limited marine site-to-site movement of live fish and improved disinfection of vessels and processing plant waste that occurred subsequent to the 1998-1999 outbreak may explain the localised spread of infection in 2008-2009. Depopulation of confirmed sites has been achieved within 7 wk (mean = 3.7 wk); however, it is likely that subclinical infection persisted undetected for months on at least 1 site. The origin of the 2008-2009 outbreak remains unknown. Potential sources include evolution from a local reservoir of infection or importation. Synchronous fallowing of management areas, with good husbandry and biosecurity, reduces the risk of ISA recurring. Movement of fish between sites in different management areas represents the greatest risk of regional-scale spread, should this occur.

Small- and large-scale network structure of live fish movements in Scotland.

Networks are increasingly being used as an epidemiological tool for studying the potential for disease transmission through animal movements in farming industries. We analysed the network of live fish movements for commercial salmonids in Scotland in 2003. This network was found to have a mixture of features both aiding and hindering disease transmission, hindered by being fragmented, with comparatively low mean number of connections (2.83), and low correlation between inward and outward connections (0.12), with moderate variance in these numbers (coefficients of dispersion of 0.99 and 3.12 for in and out, respectively); but aided by low levels of clustering (0.060) and some non-random mixing (coefficient of assortativity of 0.16). Estimated inter-site basic reproduction number R(0) did not exceed 2.4 at high transmission rate. The network was strongly organised into communities, resulting in a high modularity index (0.82). Arc (directed connection) removal indicated that effective surveillance of a small number of connections may facilitate a large reduction in the potential for disease spread within the industry. Useful criteria for identification of these important arcs included degree- and betweenness-based measures that could in future prove useful for prioritising surveillance.

Application of network analysis to farmed salmonid movement data from Scotland

The movement of live animals plays an important role in the spread of diseases. In the farming industry, this role is evident in both terrestrial systems, for example, the 2001 UK foot and mouth (FMD) outbreak (Kao 2002; Mansley, Dunlop, Whiteside & Smith 2003), and aquatic systems, for example, the 1998 UK infectious salmon anaemia (ISA) outbreak (Murray, Smith & Stagg 2002). Diseases of aquatic animals can also be spread by a variety of routes other than direct movement of live fish, for example, with the movement of water (Gustafson, Ellis, Beattie, Chang, Dickey, Robinson, Marenghi, Moffett & Page 2007) or by the movement of wellboats (Murray et al. 2002). However, the focus of this study is spread of disease by live fish movements, which is likely to be the most effective means of spreading disease within aquaculture, especially over longer distances (Murray & Peeler 2005). In the UK aquaculture industry, there are substantial movements of live fish from hatcheries to on-growing sites and ultimately onwards to processing plants, broodstock sites or fisheries. This study presents research on live salmonid movements within Scotland, where Marine Scotland, Marine Laboratory, Aberdeen is the official authority, regulation of the industry in the UK being devolved. To date, fish movement data have been used to model pathogen spread with the aim of informing contingency plans (Sharkey, Fernandez, Morgan, Peeler, Thrush, Turnbull & Bowers 2006; Thrush & Peeler 2006). The study described here represents the first attempt to apply social network analysis to the structure of live fish movements within Scotland. Social network analysis is well established in the social and physical sciences (Liljeros, Edling, Amaral, Stanley & Aberg 2001; Albert & Barabási 2002) and has been applied to animal health issues following the 2001 foot and mouth outbreak (Christley, Robinson, Lysons & French 2005; Kiss, Green & Kao 2006). The aim of this type of analysis is to identify sites with high vulnerability to infection and therefore enhance the management and risk-based surveillance (Stärk, Regula, Hernandez, Knopf, Fuchs, Morris & Davies 2006) of aquatic diseases. The contact models developed also offer an opportunity to calculate network-based measures for incorporation in epidemiological models. In this study, a database of movement records from Scottish registered fish farm sites from 2003 was created and analysis conducted on a component of both Atlantic salmon, Salmo salar L. and rainbow trout, Oncorhynchus mykiss (Walbaum), industries in Scotland. At Marine Scotland, the Fish Health Inspectorate (FHI) holds paper records of all live fish movements that take place on and off all registered sites in Scotland. Each record contains date of movement, species, number or weight, development stage (e.g. fry), source and destination, supplier, method of transportation and name of carrier. A database was created in Microsoft Access from the paper records of movements occurring between 1 January 2003 and 31 December 2003. A Journal of Fish Diseases 2009, 32, 641–644 doi:10.1111/j.1365-2761.2009.01076.x

A survey of wild marine fish identifies a potential origin of an outbreak of viral haemorrhagic septicaemia in wrasse, Labridae, used as cleaner fish on marine Atlantic salmon, Salmo salar L., farms

Viral haemorrhagic septicaemia virus (VHSV) was isolated from five species of wrasse (Labridae) used as biological controls for parasitic sea lice predominantly, Lepeophtheirus salmonis (Krøyer, 1837), on marine Atlantic salmon, Salmo salar L., farms in Shetland. As part of the epidemiological investigation, 1400 wild marine fish were caught and screened in pools of 10 for VHSV using virus isolation. Eleven pools (8%) were confirmed VHSV positive from: grey gurnard, Eutrigla gurnardus L.; Atlantic herring, Clupea harengus L.; Norway pout, Trisopterus esmarkii (Nilsson); plaice, Pleuronectes platessa L.; sprat, Sprattus sprattus L. and whiting, Merlangius merlangus L. The isolation of VHSV from grey gurnard is the first documented report in this species. Nucleic acid sequencing of the partial nucleocapsid (N) and glycoprotein (G) genes was carried out for viral characterization. Sequence analysis confirmed that all wild isolates were genotype III the same as the wrasse and there was a close genetic similarity between the isolates from wild fish and wrasse on the farms. Infection from these local wild marine fish is the most likely source of VHSV isolated from wrasse on the fish farms.

Modelling management strategies for a disease including undetected sub-clinical infection: Bacterial kidney disease in Scottish salmon and trout farms

Abstract Disease is a major constraint on animal production and welfare in agriculture and aquaculture. Movement of animals between farms is one of the most significant routes of disease transmission and is particularly hard to control for pathogens with subclinical infection. Renibacterium salmoninarum causes bacterial kidney disease (BKD) in salmonid fish, but infection is often sub-clinical and may go undetected with major potential implications for disease control programmes. A Susceptible-Infected model of R. salmoninarum in Scottish aquaculture has been developed that subdivides the infected phase between known and undetected sub-clinically infected farms and diseased farms whose status is assumed to be known. Farms officially known to be infected are subject to movement controls restricting spread of infection. Model results are sensitive to prevalence of undetected infection, which is unknown. However, the modelling suggests that controls that reduce BKD prevalence include improve biosecurity on farms, including those not known to be infected, and improved detection of infection. Culling appears of little value for BKD control. BKD prevalence for rainbow trout farms is less sensitive to controls than it is for Atlantic salmon farms and so different management strategies may be required for the sectors.

The potential for targeted surveillance of live fish movements in Scotland

The network structure of the movements of live fish in the Scottish aquaculture industry has recently been demonstrated for 2003. In this paper, we enlarge this analysis to a longer 3-year period from 2002 to 2004, the new data allowing complete coverage of at least one production cycle. The resulting network contains slightly more sites than that for a single year and is denser with more arcs (directed site-to-site connections) present, but otherwise features recognizable in the 1-year network are still recognizable in the 3-year network. Arc-removal algorithms (a proxy for targeted surveillance) were identified that could successfully reduce the portion of the network reachable from a node (a proxy for potential epidemic size) by approximately one-third by removing as few as four arcs. This results from the high centrality of particular nodes and arcs. A strong community structure was identified in the network, corresponding with species farmed, but only weakly geographical, with a high proportion of arcs occurring between management areas and catchments.

Seasonality and heterogeneity of live fish movements in Scottish fish farms

Movement of live animals is a key contributor to disease spread. Farmed Atlantic salmon Salmo salar, rainbow trout Onchorynchus mykiss and brown/sea trout Salmo trutta are initially raised in freshwater (FW) farms; all the salmon and some of the trout are subsequently moved to seawater (SW) farms. Frequently, fish are moved between farms during their FW stage and sometimes during their SW stage. Seasonality and differences in contact patterns across production phases have been shown to influence the course of an epidemic in livestock; however, these parameters have not been included in previous network models studying disease transmission in salmonids. In Scotland, farmers are required to register fish movements onto and off their farms; these records were used in the present study to investigate seasonality and heterogeneity of movements for each production phase separately for farmed salmon, rainbow trout and brown/sea trout. Salmon FW-FW and FW-SW movements showed a higher degree of heterogeneity in number of contacts and different seasonal patterns compared with SW-SW movements. FW-FW movements peaked from May to July and FW-SW movements peaked from March to April and from October to November. Salmon SW-SW movements occurred more consistently over the year and showed fewer connections and number of repeated connections between farms. Therefore, the salmon SW-SW network might be treated as homogeneous regarding the number of connections between farms and without seasonality. However, seasonality and production phase should be included in simulation models concerning FW-FW and FW-SW movements specifically. The number of rainbow trout FW-FW and brown/sea trout FW-FW movements were different from random. However, movements from other production phases were too low to discern a seasonal pattern or differences in contact pattern.

An approach to evaluating the reliability of diagnostic tests on pooled groups of infected individuals

An experimental design and statistical analysis providing information on the reliability of pooled test procedures is described. It involves estimating the relationship between the probability of a positive pooled test result (dependent variable) and the expected number of infected individuals in a pool (explanatory variable). The intercept is an estimate of the proportion of false positives (1-pooled specificity) and pooled sensitivities can be estimated for indicative prevalences of infected individuals. Simulations for a theoretical infection are used to investigate the advantages and limitations of the approach. The approach is used to evaluate the reliability of a virus isolation and qRT-PCR test procedure detecting Salmonid alphavirus the pathogenic agent necessary for the development of Pancreas Disease in Atlantic salmon (Salmo salar).