Alexander G Murray, Lorna A Munro, I Stuart Wallace, Edmund J Peeler and Mark A Thrush

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1 Scottish Marine and Freshwater Science Volume 2 No 3 BACTERIAL KIDNEY DISEASE: ASSESSMENT OF RISK TO ATLANTIC SALMON FARMS FROM INFECTION IN TROUT FARMS AND OTHER SOURCES Alexander G Murray, Lorna A Munro, I Stuart Wallace, Edmund J Peeler and Mark A Thrush March 2011

2 Scottish Marine and Freshwater Science Vol 2 No 3 BACTERIAL KIDNEY DISEASE: ASSESSMENT OF RISK TO ATLANTIC SALMON FARMS FROM INFECTION IN TROUT FARMS AND OTHER SOURCES Alexander G Murray, Lorna A Munro, I Stuart Wallace, Edmund J Peeler and Mark A Thrush The Scottish Government, Edinburgh 2011

3 Marine Scotland is the directorate of the Scottish Government responsible for the integrated management of Scotland s seas. Marine Scotland Science (formerly Fisheries Research Services) provides expert scientific and technical advice on marine and fisheries issues. Scottish Marine and Freshwater Science is a series of reports that publish results of research and monitoring carried out by Marine Scotland Science. These reports are not subject to formal external peer-review. Crown copyright 2011 ISBN: (web only) ISSN: The Scottish Government St Andrew s House Edinburgh EH1 3DG Produced for the Scottish Government by APS Group Scotland DPPAS11590 (04/11) Published by the Scottish Government, April 2011

4 BACTERIAL KIDNEY DISEASE: ASSESSMENT OF RISK TO ATLANTIC SALMON FARMS FROM INFECTION IN TROUT FARMS AND OTHER SOURCES Alexander G. Murray 1, Lorna A. Munro 1, I. Stuart Wallace 1, Edmund J. Peeler 2 and Mark A. Thrush 2 1 Marine Scotland Science Marine Laboratory, Aberdeen 2 Centre for Environment, Fisheries and Aquaculture Science, Weymouth 1 Objectives Bacterial kidney disease (BKD) is a disease of salmonid fish caused by the bacterium Renibacterium salmoninarum (OIE 2006). In Great Britain (GB) BKD occurs in both Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) farms and has been historically recorded in wild Atlantic salmon (Smith 1964; Bruno 1986). In 2004, the European Union granted GB additional guarantees for the control of BKD, subject to a control program for existing cases of infection (Munro 2007). The impacts of BKD on trout are considered less serious than impacts on salmon where higher levels of mortality occur mainly in valuable sea grown fish. It is therefore desirable to minimise the exposure of farmed salmon to R. salmoninarum, but control of infection in trout may be less cost effective. It may be possible to manage infection on salmon and trout independently, but the practicality of this depends on the infection risk that farmed trout pose to farmed salmon. The objective of this exercise is to assess the factors affecting the exposure of farmed salmon to R. salmoninarum. It is only worth controlling infection on trout farms with the objective of protecting salmon IF transmission from farmed trout is a significant risk in absolute terms AND it is significant relative to risk from other sources. That is, assuming control of R. salmoninarum in trout is not considered worthwhile to protect trout as an end in itself. This risk analysis identifies routes whereby farmed salmon could be exposed to R. salmoninarum infection. These risk routes may apply to freshwater or marine sites. We use case histories and analysis of potential contact patterns (networks, shared drainage basins, survival in water or transmission by wild/escaped fish) to derive the relative importance of different routes of pathogen introduction into freshwater salmon sites such as: 1

5 Wild or escaped fish populations Farmed rainbow trout Introduction of ova Import of fry or parr to freshwater site(s) The importance of routes of introduction of pathogens into marine salmon sites are also investigated: Movement of infected smolts from freshwater Migrating wild salmon Import of smolts to marine sites Movement of equipment, e.g. well boats, across the North Sea 2 Introduction The objective of the risk analysis is to inform policy on the control of BKD in GB. Policies for management include restriction on movement from infected sites, which frequently leads to eradication by clearance and fallowing of all R. salmoninarum infected stocks at hatcheries. The additional guarantees allow eradication to be carried out at the cage level, but farm or larger units may be more epidemiologically appropriate. The opposite extreme would be deregulation of BKD throughout the entire aquaculture industry. This would be considered more satisfactory by the trout industry than the salmon industry. Between these extremes lies a status quo policy of enforcing movement restrictions to isolate infected sites, allowing restocking but no movement of live fish off such infected sites. If interaction of infection between trout and salmon is not significantly contributing to risk then compartmentalisation of the industries, with separate regulation on salmon and trout may be practicable as the sub-populations are clearly defined and can potentially be isolated from each other (Zepeda et al. 2008). 2

6 Figure 1. Alternative pathways by which the hazard (R. salmoninarum) might be introduced to salmon farms. Red lines directly or indirectly from trout farms, blue lines independent of trout farms. In this study the hazard is the transmission of R. salmoninarum infection to farmed salmon. Three risk pathways are considered (Figure 1): A. infection could be introduced by the activity of the salmon industry itself, such as imports of ova or movements of well boats; B. introduction from a wild fish reservoir; C. introduction from trout farms, directly or through wild and escaped fish vectors. To protect salmon farms from BKD all these risks must be kept low, however, if the risk from trout is not significant in both absolute and relative terms (relative to the other two pathways) then reduction of the risk from trout would not significantly protect salmon. In the following text we review risk analysis and other modelling methods used to identify routes that represent risk of transmission. We follow this with an analysis of case histories of BKD and R. salmoninarum infection in Scotland. From this, and other sources, we summarise the key risk factors that may lead to the transfer of infection and then develop systematic descriptions of risk pathways for both freshwater and marine salmon farms. 3

7 3 Literature Review 3.1 Biophysical Properties of R. salmoninarum Laboratory experiments have demonstrated that R. salmoninarum can survive in sediment / faecal material for up to 21 days (Austin and Rayment 1985), however, the bacterium was not detected in the water overlying the sediment. Whilst R. salmoninarum can survive in filtered-sterilised river water for up to 28 days however, in unsterile river water the R. salmoninarum count declines dramatically after 48 hours (Austin and Rayment 1985). As such R. salmoninarum is probably unable to compete with the normal water-borne micro-organisms. 3.2 Epidemiology Transmission Renibacterium salmoninarum has been found within fertilised eggs (Paterson et al. 1981) and vertical transmission of R. salmoninarum via eggs has been demonstrated in a number of studies (Fryer and Sanders 1981; Evelyn et al. 1986). Lee and Evelyn (1989) found that smolts reared from the eggs of naturally infected broodstock were R. salmoninarum positive by fluorescent antibody technique, whilst smolts from R. salmoninarum free broodstock tested negative. Pascho et al. (1991) demonstrated that segregating broodstock on the basis of maternal R. salmoninarum infection levels can affect survival, prevalence and levels of R. salmoninarum in the progeny of Chinook salmon (Oncorhynchus tshawytscha) during rearing. Observations of BKD in hatchery reared brown trout (Salmo trutta) released into rivers with infected brook trout (Salvelinus fontinalis) (Mitchum and Sherman 1981), demonstrated that horizontal transmission can take place. Experimentally it has been shown that oral intubation with R. salmoninarum infected organic matter can lead to infection (Balfry et al. 1996) Environmental Reservoir There is no evidence that R. salmoninarum is a normal component of the aquatic microflora. In one study of 56 fish farms, water and sediment were examined for the presence of the bacterium but it was not detected (Austin and Rayment 1985). 4

8 3.2.3 Prevalence of R. salmoninarum Infection and BKD in Wild Fish Populations in the UK In a survey of wild fish from six rivers in England and Wales (Chambers et al. 2008) the prevalence of R. salmoninarum, detected by polymerase chain reaction (PCR), varied between rivers from 0% to 10%. The highest prevalence (8%) was found in grayling (Thymallus thymallus) and four of 84 salmon were PCR positive. Renibacterium salmoninarum was cultured from only two (one salmon and one grayling) of the 946 fish sampled (Chambers et al. 2008). The Fish Health Inspectorates in England and Wales and in Scotland have regularly sampled post-spawning salmon and sea trout (Salmo trutta) since 1982 and R. salmoninarum has never been cultured. Unpublished results from a large survey of infectious salmon anaemia virus (ISAV) in wild freshwater Atlantic salmon in the UK (Raynard et al. 2001) provided no evidence of clinical BKD. A survey of Scottish wild fish for R. salmoninarum was undertaken from 2005 to 2007 screening with quantitative real-time polymerase chain reaction (qpcr). Renibacterium salmoninarum was detected at low prevalence in escaped rainbow trout and at even lower prevalence in 3-spined-stickleback (Gasterosteus aculeatus) and minnow (Phoxinus phoxinus) in association with infected fish farms Wallace et al. (in prep) Farm Level Prevalence in the UK Austin and Rayment (1985) found R. salmoninarum in two of 13 farms (15%) surveyed (150 fish sample from each farm). Surveys conducted by the Fish Health Inspectorate (FHI) in 1993 and 1994 found that 28 of 288 farms (10%) tested were R. salmoninarum positive. Thirty fish per farm were examined, hence farms with low prevalences of infection may not have been detected (a 30 fish sample provides a 95% probability of detecting the presence of R. salmoninarum if the prevalence is greater than 10%). As a result, the true farm level prevalence was likely to have been higher than these estimates. More recently in a survey of 10 fish farms, 150 fish per farm were sampled and tested for R. salmoninarum by PCR (Chambers et al. 2008). None of the farms were found to be infected, however, since the farms were not selected randomly it is difficult to generalise from these results. Overall R. salmoninarum infection was not widely detected within the trout industry. 3.3 Risk Method The guidelines for Import Risk Analysis (IRA) published in the Aquatic Animal Health Code (OIE 2006) of the World Organisation for Animal Health (OIE) are based on the Covello-Merkhofer model (CM) (Covello and Merkhofer 1993). These guidelines have been generally preferred for aquatic animal risk analysis. There are four parts to the CM 5

9 risk analysis model. Hazard identification is the first step and considered separately from the risk assessment. Risk assessment is subdivided into stages: i) release assessment (pathways for the introduction of the hazard), ii) exposure assessment (pathways necessary for the hazard to occur following introduction), iii) consequence assessment (identification of the adverse human health, animal health, economic or environmental effects), and iv) risk estimation (integration of the release, exposure and consequence assessments). Risk management and risk communication combined with risk assessment and hazard identification are referred to as risk analysis. The CM model can be applied qualitatively or quantitatively. Both approaches are based on a reasoned, systematic and logical discussion of the relevant contributory factors and epidemiology of a hazard. Qualitative assessments of likelihood of its release and exposure and the magnitude of its consequences are expressed using non-numerical terms such as high, medium, low or negligible (Murray et al. 2004). In quantitative assessments, the likelihoods are expressed numerically and the uncertainty associated with an input, and its known variability, can be modelled by probability distributions. Monte Carlo simulation, using software programmes Palisade Inc.), is generally used in quantitative risk analyses to assimilate the probability components. Generally it is recommended that all risk analyses should first be attempted qualitatively (Vose 2001). Expending further resources on a quantitative assessment depends, firstly, on whether the qualitative results were adequate for decision making and, secondly, on whether resources and data are available for a quantitative analysis. The application of risk assessment in aquatic animal health management has been reviewed by Peeler et al. (2007). The main application has been in the field of IRA (e.g. Hervé-Claude et al. 2008). These IRA models can be successfully used to assess disease spread at other scales, for example between rivers (Høgåsen and Brun 2003; Peeler et al. 2004) and farms (Munro et al. 2003). The risk model described in the OIE code (OIE 2006) has been proven to be a flexible tool for assessing and ranking routes of disease spread. 3.4 Mathematical Models The factors behind transmission of disease can also be assessed using mathematical models. Models of the structure of transmission between sites have been used to identify relative roles of distance and shared ownership (as a substitute for contacts) in the spread of infectious salmon anaemia (ISA) in Norway (Scheel 2007) and transmission between sites and movements between fresh and marine environments in the spread of infectious pancreatic necrosis virus (IPNV) (Murray 2006; Ruane et al. 2009). In the case of IPNV, freshwater transmission plays a key role in overall risk of 6

10 infection, even in marine sites, and controls in freshwater are predicted to be more effective than controls in the marine environment. Movement between sites is non-uniform with some sites far more highly connected than others. Network modelling is being developed by Munro and Gregory (2009) and Green et al. (2009). Models of spread through the system result in highly skewed outbreaks with a large proportion of small, but some very large, epidemics (Thrush and Peeler 2006). 4 Scottish Data on BKD Outbreaks Bacterial kidney disease has been present in Scotland since the 1930s when outbreaks of Dee disease occurred in wild salmon on the river Dee, Aberdeenshire (Smith 1964). The first recorded outbreak in farmed fish in Scotland was in rainbow trout in 1976 (Bruno 1986). Since this time, however, BKD has not been reported in wild fish, although very recently the causative agent has been detected using the qpcr screening method. Outbreaks of BKD have occurred in Scotland in freshwater and marine trout farms and marine salmon farms. The characteristics of these outbreaks have varied considerably depending on the type of farm involved. In salmon farms and in tank-based trout farms the outbreaks tend to be relatively short-lived, while some cage-based trout farms have retained infection controls for many years (Bruno 1986). We analyse the epidemiological patterns in recent Scottish BKD cases which we categorise as being: 1. Persistent cases in freshwater trout farms; 2. Outbreaks in freshwater trout farms linked to a hatchery in 2005; 3. A site that may have been reinfected following fallowing; 4. Outbreaks in marine salmon on the west coast of Scotland in 2004 and 2007; 5. Latent infection in a freshwater salmon farm deduced from outbreak 4; 6. Outbreaks in marine salmon in Shetland in Persistent Infection in Freshwater Trout Farms Several trout farming sites in Scotland have been infected with R. salmoninarum for many years (Figure 2). Four of these sites have been continuously under Designated Area Order (DAO) restrictions since 1981 or These are freshwater cage farms where continuous stocking is practiced and therefore a fallowing period in production is not incorporated. Three of these sites have been studied in detail (Wallace et al. in prep). Infection was detected in established populations and in newly stocked cohorts 7

11 (sourced from farms approved as R. salmoninarum free under an official control and eradication programme (Munro 2007)) with these becoming infected within a time period of one week to four months. The prevalence of R. salmoninarum in these cohorts was initially low and increased over time in three illustrating a dynamic infection in at least some of these populations. This transmission occurred even although the increase in prevalence within the cages was slow and no classic clinical or gross pathological signs of BKD were observed in any of the fish sampled (although signs of other diseases such as salmonid alphavirus (SAV) were noted in a few fish). Therefore clinically infected sites would be likely to transmit infection quite effectively between individual cages within sites. It is likely that the source of infection to these naïve cohorts was by horizontal transmission from established stocks on site via fish-to-fish contact or by the movement of water, or from wild and escaped fish reservoirs. A low prevalence of R. salmoninarum was recorded from wild and escaped fish caught in the vicinity of one of these farms. Figure 2. Persistence of R. salmoninarum (in years) in different types of fish production, as measured between the initial imposition of DAO and time lifted (or until 1 st June 2008 if still in force at that time). Number in brackets = number of DAOs imposed. 4.2 An Epidemic Hatchery-Based Outbreak In 2005 BKD was recorded at a freshwater trout farm (site 2005/1) near Aviemore. The source of this infection was traced to the supplying hatchery (2005/3) (Figure 3) located 8

12 in central Scotland. Contact tracing showed several other sites had been infected (Bland 2007), two Scottish sites (including 2005/1) and one English site were confirmed and one Scottish site was under suspicion due to positive Enzyme-Linked Immuno- Sorbent Assay (ELISA) positive results, but was not confirmed as R. salmoninarum positive bacterial cultures were not obtained in support of this. The bacterium was also detected using qpcr in a pooled sample of two wild 3-spined-sticklebacks in the vicinity of this hatchery (2005/3). The supplying hatchery (2005/3) was cleared of R. salmoninarum on a tank-by-tank basis and this approach was effective because good biosecurity could be maintained at this indoor facility. As a result the DAO was revoked in November The spread of the epidemic reflected movements of fish through the network (Figure 3). The outbreak shows the capacity of highly connected nodes in a network to spread R. salmoninarum (or other pathogens) between individual sites and the importance of cross-border movement of fish which result in a border that is potentially highly porous to R. salmoninarum. Figure 3. Spread of R. salmoninarum via a Scottish hatchery (2005/3). Sites in black confirmed as R. salmoninarum positive; sites in grey = suspicion (ELISA not supported by culture); and sites in white = ELISA negative sites (Bland 2007). Four English sites other than site B received fish from supply hatchery 2005/3, but did not test positive. 9

13 4.3 Re-Infection of a Tank-Based Trout Site Three of the sites which were infected from the hatchery described above (Section 4.2) were fallowed to clear the infection. This was successful for site 2005/1 with the DAO being revoked and on 2005/5 (which was never confirmed positive). However, 2005/4 was unable to establish clearance in spite of being a pond rather than a cage-based site. One possible explanation for this is re-infection from an infected cage-based site in a loch situated approximately 13 km upstream. Infected wild and escaped fish have been found in the vicinity of this cage-based farm and there is a possibility that these could have carried infection into 2005/4. It is also possible that there was a biosecurity failure during the fallowing of this site which was carried out on a pond by pond (rather than farm-wide) basis and this is perhaps the more likely explanation. 4.4 West Coast Outbreaks in Atlantic Salmon Table 1. Marine salmon farms on the Scottish west coast from which BKD was reported Site Business DAO DAO revoked Mortality (kg) imposed MS1 X 16/02/ /02/2007 N/A MS2 X 16/02/ /02/2007 N/A MS3 Y 21/06/ /06/ ,298 MS4 Y 21/06/ /02/2006 *0 MS5 Y 28/06/ /05/ ,382 MS6 Y 28/06/ /02/ ,319 MS7 Y 28/06/ /08/ ,524 MS8 Y 12/07/ /02/ ,708 MS4 Y 21/06/ /02/ MS9 Y 05/02/ /07/ MS10 Y 21/02/ /02/2006 6,828 MS4 Y 18/05/ /01/ ,920 + MS11 Y 18/05/2007 Active 0 + MS12 Y 18/05/2007 Active 0 + * The DAO at MS4 was imposed in 2003, however, mortality did not occur until the next production cycle; + mortality to end of

14 Several discrete outbreaks of BKD have occurred with each affecting several salmon farms on the west coast of Scotland (Table 1). In 2002 only two sites owned by company X were affected. The second outbreak was larger affecting six sites all belonging to company Y in 2003 and a further two in 2005, with all DAOs revoked by mid A third (or forth depending on whether the company Y outbreaks are seen as one or two separate events) again affected company Y in 2007, with two DAOs which are still active. None of the sites in Table 1 were among the five salmon sites affected by BKD between 1976 and 1985 (Bruno 1986). It is significant that single companies are affected in each outbreak, usually company Y. The outbreaks showed a very significant link to the freshwater smolt producing site FS1 (Figure 7) and a smaller site located upstream in the same loch FS2 (not labelled), both through contact tracing and analysis of numbers of movements onto company Y sites. Sites receiving smolts from FS1 and FS2 had high odds ratios (OR) for BKD of 19:94 and 10:43, respectively as opposed to the overall total of 34:658. These give highly significant OR of having BKD for FS1 and FS2 of 3.9 (p = 2.9E-5) and 4.5 (p = ), respectively, relative to averaged odds. This is a statistical association an it is certainly possible that this association was itself coincidental with other factors associated with the marine salmon sites that happened to use the same sources of smolts. 11

15 Figure 4. Locations of west coast salmon sites affected by BKD restrictions Sites FS1 and FS2 were larger than the average smolt farm so there was an association of BKD outbreaks with the size of the smolt producer (0.11% per delivery dispatched, R 2 = 0.37 p = ). 12

16 All but two of the positive sites received fish from FS1 (Figure 7) in the year classes that suffered BKD-induced mortality or which had a DAO imposed because they tested positive for R. salmoninarum. This includes MS9 for a production cycle without any mortality attributed to BKD but with R. salmoninarum reported on site and MS4 in two production cycles where there was and was not mortality. The two exceptions were MS10 which received smolts from FS2, a site that is also significantly associated with BKD cases, and MS3 which does not link to either FS1 or FS2, however, it did receive smolts from FS1 in the previous production cycle. The affected sites were not randomly spatially distributed, forming two distinct clusters on the mainland and a couple of more isolated cases on the Islands to the west (MS8 and MS9) (Figure 4). The two clusters are separated by a considerable number of uninfected farms, so it is probable that they were independently infected. Transmission between sites at a local level within the clusters could have subsequently occurred; even within clusters a site within the Loch Sunart cluster tested negative. Three of the affected sites, MS3, MS4 and MS10 are situated in the uppermost part of Loch Linnhe and Loch Eil (Figure 4). They are close to a river discharge connected to FS1. It is possible therefore that R. salmoninarum was transported to these sites by movements of water from FS1, or by movement of wild or escaped fish. Farm MS3 itself had no smolt contacts with FS1 (or FS2) and its location at the head of the Loch Linnhe system suggests direct exposure via water or wild or escaped fish is possible. Two separate outbreaks occurred with an outbreak in the MS3 site in autumn 2003 and then in MS10 and MS4 (very limited mortality) in summer This latter mortality was only in larger fish (2-3 kg) and infection, in MS4 at least, was present back to summer 2003 so these sites could have been infected from the MS3 outbreak. This site could also be a source of infection to MS10 since there was a prolonged period of disease-free (or at least mortality-free) infection. However, these sites MS10 and MS4 are associated with smolt movements from FS1 or FS2 and they were fallowed in co-ordination with MS3, so persistent infection although possible is unlikely. Outbreaks occurred in salmon of a range of sizes (Figure 5), and in some cases mortality was reported soon after input to seawater. The first reported mortalities for site MS7 were of 0.56 kg, compared to 3.55 kg in MS3. However, infection may have been present well in advance of any mortality. The site MS4 was determined to be R. salmoninarum positive and a DAO imposed in summer 2003, but mortality was not reported until summer 2005, and then only briefly. In many cases mortality continued until fish were of harvest size (up to 5 kg). Mortality affected similar fish at the sites at MS5, MS6, MS7 and MS8 (Figure 5). Three of these were in Loch Sunart, but one site (MS8) was located at a considerable distance 13

17 from the others on Skye. Mortality in MS3 appears to have had a completely different outbreak occurring in large fish at the end of 2003; the timing of this means it could potentially be involved in the initiation of outbreaks listed above, but its location does not fit with such a hypothesis. Outbreaks in the MS10 and MS4 sites occurred later and only affected large fish so it is possible these were infected from a site in the event but went undetected until outbreaks occurred in larger fish. The outbreak in MS4 was minimal but this site was reported as infected and had a DAO served in 2003 as having BKD but with zero attributed mortality and therefore might represent the link between the 2003 and 2005 outbreaks. However, the site was restocked in February 2004 so the detection was in other fish and any link is unclear, but could indicate survival of R. salmoninarum through fallowing. The MS4 farm is an unusual case, positive in three consecutive production cycles. In the first a DAO was imposed, but no mortality occurred, limited mortality happened in the second production cycle, and the DAO was re-imposed for a third production cycle. This farm is located close to a processing plant, so might have been exposed repeatedly by discharges or other factors associated with processing if infected material was handled by the processing plant. Figure 5. Weight of individual fish affected by BKD induced mortality from west coast marine salmon sites. 14

18 MS3 MS4 Linnhe cluster MS10 MS5 MS6 Sunart cluster MS7 MS8 Skye MS Western Isles k 3k-30k 30k-300k Figure 6. Outbreaks of BKD on west coast salmon farms Circles are quarterly mortality levels; black triangles = DAOs imposed white triangles = DAOs lifted. The patterns within outbreaks varied; even with similar fish infected at similar times there were very different patterns. In MS7 large numbers of small fish died shortly after input so it is possible this high level early mortality spread infection to other sites, especially MS5 and MS6 with are geographically proximate. Mortality was detected in MS5 at the same time as MS7, but at a much lower level, so it is possible BKD had already spread to this neighbour. Alternatively, it could be the sites were infected from a shared freshwater smolt source, an explanation that fits particularly well with the MS8 outbreak. At this site although mortality was initially very low, occasional BKD related losses were reported back to the beginning of December of Differential levels of mortality from 0 to 133 tonnes were recorded between the sites (Table 1), temporal patterns were different even for fish that were infected at similar times (Figure 6). This suggests that one way of reducing risk may be reducing the consequence of infection, even in probability of infection were not reduced. More than 83% of mortality in the last 12 events occurred at three sites. If mortality were reduced on these strongly affected sites to the average level across the other nine events, then 15

19 mortality could be reduced by nearly 80%. It is also likely risk of transmission to other sites is less when clinical disease does not occur. Data from company Y was available to quantify mortalities ascribed to BKD for , and to trace sources of smolts for , data should become available to analyse more recent periods. The marine outbreaks were very strongly linked to the movement of infected salmon from the freshwater sites FS1 and FS2, with the exception of MS3 which is geographically close to FS1 so may be exposed by this route. This site shares its catchment with a trout farm (TF1, Figure 7) which is downstream, but could still be contacted by movements of migratory fish. The freshwater loch in which FS1 is situated contains a population of Arctic char (Salvelinus alpinus), which are a potential reservoir for R. salmoninarum (Section 7.5), but whose infection status in this case is unknown. 4.5 Latent Infection in FS1? The FS1 freshwater smolt production site was linked by live fish movements to many of the marine outbreaks on the west coast as described in the previous section. However, routine testing at the time did not detect R. salmoninarum and it has never been found at this site. A possible explanation could be that the standard screening methods employed are less sensitive than the qpcr test Bruno et al. (2007). In the study of Wallace et al. (in prep) a low prevalence of R. salmoninarum was found in three rainbow trout farms known to be infected so there is a possibility that infection on FS1 was simply not detected due to the reduced testing sensitivity. The hypothesis that infection was absent and the association of infection in marine sites with smolts from FS1 was coincidental is also possible. Infection could have been introduced to here from other salmon producing sites such as a source hatchery. If this was the case, we may expect R. salmoninarum to be more widespread within the salmon smolt producing industry and contact tracing of sibling groups of fish by FHI did not detect any spread among groups that were associated with suppliers of FS1. 16

20 Figure 7. Fish farm location map illustrating the spatial distribution of sites referred to in the text. Black circles are freshwater salmon farms; the white circle is a freshwater rainbow trout farm and black triangles are marine salmon farms. Unlabelled sites are not discussed in the text as there is no evidence of association with BKD. Pale blue lines represent fresh water; dark blue lines are fresh water systems with migratory salmonid populations and white represents marine water. An alternative salmon-farm source of R. salmoninarum is the marine salmon site at MS3. This site underwent mortality (Figure 8) among fish that had been on site for approximately 18 months when the DAO was imposed, within a week of four other DAOs (Table 1). Given these were nearly simultaneous DAOs, R. salmoninarum did not spread to these other sites after the DAO was imposed, and the DAO was imposed more than two months before BKD induced mortality was recorded on site. This makes MS3 unlikely to be a source of infection, especially as the statistically significant link is through FS1, not direct transfer from MS3. However, from the weekly mortality time series for MS3 (Figure 8) it can be seen that elevated mortality began to occur before the DAO was imposed. Therefore it is possible the disease was present well before it was officially reported. It is then possible that migratory salmonids carried infection from this site to FS1 from which the 2003 outbreak was then spread. Site MS3 has not been stocked since 2005 so it could not be associated with the 2007 outbreaks. 17

21 Other salmon sites in the Loch Linnhe system are also potential, but less likely, sources of infection. It appears MS4 was infected with the same movement of fish from FS1 that spread infection to MS5, MS6 MS7 and MS8. Therefore MS4 would not have been the source of this outbreak. MS10 was only infected much later in However, it is always possible that undetected infection was present earlier on these, or other, sites. Figure 8. Weekly mortality (number of fish) on MS3 over (not attributed to BKD = thin line, attributed to BKD = thick line). Note that, although mortality was only ascribed to BKD for the last few weeks of production, elevated mortality had occurred for months prior to this and began to rise even before a DAO was imposed. The FS1 site shares the loch with a population of wild Arctic char and Jónsdóttir et al. (1998) report these to be carriers of R. salmoninarum infection in Iceland. The infection status of char in the loch is unknown and therefore they certainly cannot be ruled out as a reservoir of infection for FS1. Finally there is a trout farm (TF1) close to FS1 (Figure 7). This farm is downstream of FS1 and R. salmoninarum has never been reported from the site. However, this does not rule out a low prevalence infection. Previous research has demonstrated the presence of R. salmoninarum in wild and escaped fish in the vicinity of another site in a different catchment, although that farm had a very low prevalence infection (Wallace et al. in prep). Therefore, it is at least possible that escaped fish, or migratory salmonids, could carry infection up stream to FS1. 18

22 In conclusion, we do not know if FS1 was ever infected with R. salmoninarum and BKD has never been reported from here. Plausible routes of infection can be derived for all the risk pathways shown in Figure Outbreak in Shetland 2008 In 2008 an outbreak of BKD occurred in farmed Atlantic salmon in Shetland. This consisted of an outbreak at a salmon farm (SS4) in north east Shetland and subsequent detection of R. salmoninarum on several other sites from throughout the islands. All six sites affected were owned by the same company (Z), although ownership of sites did change. The affected farms were in different regions of Shetland, and sites belonging to other companies in these regions were not affected. The affected fish from the different sites all came from different sources of smolts from throughout Scotland. The outbreak affected fish that had been on site for a considerable period of time and were due for harvest. The pattern of this outbreak resembled the epidemiology of MS3. There is a very powerful association between Scottish sites belonging to the company and their becoming infected with R. salmoninarum sometimes leading to BKD. With a total of 31 of the 107 sites in Shetland belonging to company Z then the probability that all the four confirmed infected sites were not associated with company Z is p = or p = if SS1 is included as an infected site. Table 2. The detection of R. salmoninarum at salmon farms in Shetland Farm Result Date imposed Restriction Smolt source Management Area SS1 N/A 05/04/08 DAO 4a SS2 1/1 28/06/06 TDN 4a SS3 1/6 26/06/07 TDN Highlands 3a SS4 6/7 30/01/08 DAO Dumfries 2c SS5 4/38 27/05/08 DAO (17/07/08) Argyll 3a SS6 2/6 2/32 04/06/08 12/06/08 fallowed Jura 3a There is no significant difference between Management Areas (MAs) in Shetland with numbers of positives proportional to the number of company Z sites in the particular region. With no geographical association, so no evidence for hydrodynamic or other environmental contact on the one hand, and a lack of common smolt origin on the other, 19

23 the association provides very strong evidence of intra-company anthropogenic spread of infection. Association might be via a processing plant, although other companies used this and none of their farms underwent outbreaks of BKD. The use of the processing plant might be confounded with other unmeasured company-based management practices (e.g. shared personnel, equipment etc.). A total of 31 sites from company Z used this processing plant, 24 sites from eight other companies used this plant and had no positive sites. This is statistically consistent with contact with the processing plant being the sole risk factor for infection as 4/31 and 0/24 are within the 90% confidence ranges of 4/55 overall prevalence of infected sites using the processing plant and even more consistent if one of the company Z sites was an index case infected from another source. It seems therefore that activities within the company lead to the spread of R. salmoninarum over a large area of Shetland and to many sites (but only within company Z). One initially infected site can thus spread infection to the other sites as a result of company activity, possibly via a processing plant. As a postscript, a further clinical BKD case was identified in January 2009 at a site belonging to company Z as a result of surveillance following an ISA outbreak in MA 3a (D. Bruno pers. comm.). Again, no BKD was evident among fish farm sites belonging to other companies in the area. In this same investigation it became apparent that another company was using busstop deliveries whereby well boats picked up half a load at one site, before moving to another site to complete the load. We do not know if company Z engaged in this practice, but if it did it could explain spread with-in the company between sites that were some distance apart. Bus stop deliveries are more likely to occur within a company than simple access to a processing plant, which is shared by several companies. 4.7 West Coast Outbreaks in Trout and Salmon in 2009 More recently, BKD was diagnosed in marine farmed rainbow trout and Atlantic salmon from an area of the west coast. These species were cultured in separate cage farms that are geographically close to each other. This highlights possible epidemiological links between the two industries and between fresh and marine trout farms and these are discussed in the following section. 20

24 4.7.1 Marine Rainbow Trout Initial Outbreak and Diagnostic Testing Figure 9. Schematic area map: white circles = R. salmoninarum negative farms; black circles = R. salmoninarum positive farms; crosshatch = tidal excursions around positive trout farms; stippled = tidal excursion around positive Atlantic salmon farm (tidal excursions overlap). 21

25 Tonnes lost per month In April 2009 the FHI were notified of high mortalities (Figure 10) at two marine cage rainbow trout farms, MT3 and MT4 situated in a sea loch on the west coast (Figure 9). There are five cage farms in this loch all growing rainbow trout with four stocked at the time (farm MT2 was fallow). All are operated by the same company and are in close geographical proximity within a single tidal excursion of each other. Mortality of marine-farmed trout in 2009 was more than twice that in 2008 (427 tonnes as opposed to 197 tonnes) according to the Scottish Environment Protection Agency (SEPA) database (the average biomass in the water was similar in both years: 1291 and 1495 tonnes). This elevated mortality in 2008 seems to be accounted for by the elevated mortality in site MT3 and MT4 in March to July of 2008, a time that coincides with the confirmation of BKD. The SEPA data does not include cause of death. Elevated mortality also occurred in MT1, SEPA does not treat MT1 and MT2 as separate sites, but MT2 was not populated at the time of this peak J F M A M J J A S O N D J F M A M J J A S O N D Date total trout MT1&2 MT3 MT4 other 1 other 2 other 3 other 4 other 5 Figure 10. Mortality of marine trout from SEPA monthly mortality records. Losses shown for total trout, sites MT1 and MT2 combined (not separated in SEPA records), MT3 and MT4 and for five other sites not in the region. In response to this notification diagnostic testing was undertaken in early May on 10 fish from each of these farms. Both farms were confirmed R. salmoninarum positive by ELISA and qpcr and BKD pathology was observed in all 20 fish. Movement controls in the form of Confirmed Detection Notices (CDN) were applied to these sites and the other 22

26 two farms (numbers MT1 and MT5) were subject to statutory 150 fish ELISA tests in mid May as they were within a tidal excursion of the positive farms (Figure 9). From this testing, R. salmoninarum was confirmed at farm MT1 from ELISA, qpcr and histology but was not detected at farm MT5. A CDN was then applied at MT1 with MT5 having no movement controls. Connectivity between the Farms Farms MT3 and MT4 had initial mortality in April 2009, R. salmoninarum was confirmed and BKD pathology observed in May and in addition, MT1 was confirmed. All four farms are operated by the same company and are served from the same shore base, sharing personnel and boats. Fish were moved from MT4 to MT3 in October 2008 and then from MT3 to MT4 in February Fish were also moved from MT3 to MT1 in February These practices highlight possible pathways for the spread of R. salmoninarum between the farms. Interestingly, infection was not detected at MT5 (another of the companies farms) and this site is served by a different shore base. Previous work on the spread of R. salmoninarum in marine Atlantic salmon in Shetland (Section 4.6) and fresh water rainbow trout (Section 4.2; Bland 2007) supports this type of intra company spread with the most likely transmission pathways being movements of fish and boats rather than hydrographically. As such the observed infection pattern within the loch is well explained by these routes and may also account for MT5 testing negative. Possible Infection Sources On-Farm Reservoirs In the past, R. salmoninarum has been detected at two of these farms (MT1 in & 2008 and MT5 in 2002) and these infrequent and sporadic positive tests would make it unlikely that R. salmoninarum persists as on-site reservoirs in the long term. In addition, these farms are fallowed on a regular basis, although not synchronously, at approximately every two years thus removing the most likely reservoir (fish) from the system. As such the likelihood that R. salmoninarum survives between production cycles at the individual farms is low. Wild and Escaped Fish Wild and escaped fish are attracted to aquaculture facilities (Carss 1990; Dempster et al. 2009) and this highlights a potential for infection to be transferred between farmed, wild and escaped fish. Wild fish have been shown to move between fish farms (Uglem et al. 2009) illustrating the potential for infection to be spread to new localities. 23

27 i. Wild Fish: Wild marine fish are not classed as susceptible to BKD (OIE 2006) and there have been few reports of R. salmoninarum positive tests from marine nonsalmonids (Dutil and Lallier 1984; Kent et al. 1998). As a result, the likelihood of these being reservoirs for infection to the marine trout farms is negligible. Wild salmonids are susceptible (OIE 2006) and there are reports of R. salmoninarum positive results (Smith 1964; Chambers et al. 2008) and these species occur in many of the local fresh waters. Atlantic salmon and sea trout are present in the river that discharges to the sea loch close to MT1 and tends to eddy in the immediate area so there is a possibility that salmonids could be moving in proximity to some of the marine farms. There are also reports of R. salmoninarum positive diagnostic tests in wild fresh water non-salmonids (Chambers et al. 2008; Wallace et al. (in prep)). However, the infection status of wild fish in the local environment is not known so their potential as reservoirs can not be determined. ii. Fish Escaped from Fresh Water: There have been a number of reported escapes and escape investigations in this area. In July 2007 escaped rainbow trout were caught by anglers in the river and fresh water loch and were also observed congregating above the dam at the loch outflow. An investigation was undertaken and although the source of these fish is unknown it is likely from the freshwater farms FT1 and FT2 in the loch due to the proximate location (Figure 9). Whatever the fish source, these farms have a long history of R. salmoninarum so are a potential risk to other farms in the area. Fishery FT3 discharges via two burns to the river and the outlets from the ponds are not screened illustrating another potential freshwater escape route. As such there is a potential for infected fish reared in fresh water to spread infection to other fresh water sites and to marine farms. iii. Fish Escaped from Marine Water: Escapes from the marine farms have been reported and investigated in 2005, 2006, 2007 and Large rainbow trout have been caught by anglers in the sea loch, the river and have been recorded ascending the fish ladder into the fresh water loch. Due to the large size of these fish they must have originated from the marine farm(s) and in some instances have moved into fresh water. If they are infected these escaped marine trout have the potential to spread R. salmoninarum to fresh water farms, wild salmonids and in addition, to re-introduce infection to marine farms following the fallowing periods. Fresh Water Trout Farms The main fresh water catchment that drains into this sea loch has two fresh water rainbow trout cage farms FT1 and FT2 (Figure 9). These have a history of 24

28 R. salmoninarum and BKD and long-term movement controls. In addition, there is a put and take trout fishery (FT3) situated on the river near the discharge to the sea and BKD has been reported from here in the past. The study of previous outbreaks (Sections 4.2, 4.3, 4.4, 4.5 and 4.6) have not identified hydrographic spread as a main risk pathway for R. salmoninarum however, the potential for spread from fresh to marine waters by this route can not be ruled out. Stock Inputs Many of the trout stocked to the marine farms originated from fresh water farm TF1 (Section 4.5; Figure 7). This farm has never tested positive for R. salmoninarum however, it is in the same catchment as the fresh water smolt farm FS1 (Figure 7) and this site has previously been linked with two outbreaks in marine Atlantic salmon farms in the Linnhe system in and 2007 (Section 4.4). This may represent a tentative theoretical link to the outbreak in the marine trout farms although there is no direct evidence to support this Marine Atlantic Salmon Initial Outbreak and Diagnostic Testing In May 2009 the FHI were notified of the presence of BKD on two marine Atlantic salmon farms, AS1 and AS2 and these farms are located close to the marine trout farms (Figure 9). Diagnostic testing was undertaken and R. salmoninarum was confirmed at AS1 with AS2 returning negative results. Both farms are operated by the same company using the same shore base, boats and personnel. As a result of the confirmation, statutory testing was implemented in June at two other marine Atlantic salmon farms AS3 and AS4 (also operated by the company) which are located within a tidal excursion of the confirmed site (AS1). The results of this testing for both farms was negative. Possible Infection Sources Marine Trout Farms The tidal excursions from the marine trout farms and the infected Atlantic salmon farm overlap illustrating a close geographical proximity (Figure 9). Due to this close distance there is a possibility for the occurrence of hydrographic spread from the marine trout farms to the salmon farm via the discharge from the sea loch. However, the sea loch catalogue (Edwards and Sharples 1986) states the flushing time for the loch as just over 13 days so despite the proximity the water is not particularly mobile in this vicinity. As previously stated (Sections 4.2, 4.3, 4.4, 4.5 and 4.6) intra-company rather than 25

29 hydrographic spread is the more likely transmission route. This is supported by many years of surveillance testing in fresh water where a few farms become and remain positive with little spread to neighbouring facilities. However, due to this close proximity and the timing of the outbreak at the marine salmon farm a mere few weeks after the marine trout farms were confirmed does point to a connection as opposed to mere chance. Wild and Escaped Fish It is possible that infected escaped rainbow trout could have been the source of R. salmoninarum to the marine Atlantic salmon. Previously R. salmoninarum has been detected in escaped rainbow trout by Wallace et al. (in prep) illustrating the potential to spread infection to other localities depending on the post escape movement patterns. In this region escaped fish have been caught by anglers in marine and fresh waters and have also been taken in coastal bag nets in the Linnhe system. Regardless of the initial fish location this illustrates dispersal away from the point of escape and the potential to transmit infection to new localities. The potential for wild fish to transmit infection to marine farmed fish has been discussed in the marine rainbow trout section and also applies here to the farmed Atlantic salmon. Links to Previous Marine Outbreaks Two previous marine outbreaks of BKD have occurred in the Linnhe and Sunart systems (Section 4.4; Figure 4). These are geographically close to the area where the marine trout and salmon outbreaks occurred and the Linnhe system is in the same MA (15b) so is linked by tidal excursions (Figure 11). It is possible that other farms situated between these two areas could link them in a kind of hedge hopping pattern and spread infection via this route. However, as yet there have been no other positive farms in the MA and the Linnhe and Sunart farms have not had any positive R. salmoninarum tests since The likelihood of R. salmoninarum surviving in a reservoir in the general area for this length of time and being able to infect the farm is unlikely. There are, at the time of writing, 16 Atlantic salmon farms in MA 15b and the majority are operated by the same company, some using shared shore bases. In view of this and the previously identified intra company spread as being an important transmission route there is a potential for infection to be introduced to these other farms from the confirmed site. 26

30 Figure 11. Location of the local MAs illustrating connectivity within the region Summary The initial infection source for the outbreaks in this area is unknown. However, in view of the proximity and timings of the respective marine trout and Atlantic salmon outbreaks the more likely route of transmission would be from marine trout to marine salmon by one or more of the pathways outlined in this section. There is a long history of R. salmoninarum in the farms situated in the fresh water catchment and escaped rainbow trout are present. In view of this, the most likely source of the marine infection would perhaps be from the fresh water catchment. Intra company spread is the most likely route of transmission between the marine rainbow trout farms via movements of 27

31 fish and boats. Wild and escaped fish may be the source of infection to the marine Atlantic salmon. Possibilities for the further spread of infection within marine rainbow trout and Atlantic salmon farms in the area have been outlined and this situation is being closely monitored. 5 Scottish BKD Surveillance: Routine and Contact Tracing Since 2004 routine surveillance (30 fish samples) for R. salmoninarum has been undertaken in Scottish salmonid farms. These samples are screened using ELISA in pools of five fish. As a result of this surveillance R. salmoninarum has been detected in seven trout farms, a trout fishery and at seven salmon sites leading to DAOs being imposed. During the same period DAOs were revoked from seven trout farms and nine salmon farms, so the total number of sites under restriction has been reduced by one. Many of the outbreaks have been described earlier in the report and some detection resulted from contact tracing rather than routine surveillance. For example the outbreak described in Section 4.2 was detected at site 2005/1 by routine sampling but traced back to the hatchery at 2005/3 and from there to 2005/2. Outbreaks, as described, show more association with movements of fish than with their spatial location. Several sites show very persistent infection, resulting from cage-to-cage horizontal transmission. The FHI have also undertaken routine surveillance of wild fish for R. salmoninarum. Historically this has been achieved using culture on Mueller Hinton Agar plus Cysteine and Antibiotics (MHCA) plates and since 2005 also using qpcr. Despite many hundreds of fish being tested there have been no R. salmoninarum positives from this survey. An epidemiological wild fish study was carried out during with testing focused mainly around a fish farm that had long term movement controls for BKD. Over 2700 wild and escaped fish were tested for R. salmoninarum using qpcr. Six pools were R. salmoninarum positive, illustrating low infection prevalence. 6 BKD in England and Wales When additional guarantees for BKD were granted to the UK in 2004, three rainbow trout farm sites in England and Wales were known to be R. salmoninarum positive. A programme of testing began in 2005 and as a result R. salmoninarum was detected on 10 sites in nine catchments (Figure 12). Clinical disease was not evident on any of these sites and testing indicated a low prevalence of infection. Live fish movements connected many of the infected sites. The spatial distribution of infected farms did not 28

32 indicate spread of R. salmoninarum within the same catchment through water currents or wild vectors. Some sites in England and Wales have had long standing R. salmoninarum infections without resulting spread of the pathogen to sites downstream. Figure 12. Distribution of R. salmoninarum negative (black) and positive (white) salmonid fish farm sites among 198 river catchments in England and Wales since

33 7 Routes of Transmission 7.1 Transmission with Anthropogenic Fish Movements The spread of disease such as BKD requires contact processes between infected and uninfected farms. These contacts may be local processes through the water (Gustafson et al. 2007), or over longer distances via anthropogenic processes such as transport of fish between locations (Thrush and Peeler 2006) or movements of well boats (Murray et al. 2002). From the case studies presented, anthropogenic links clearly account for most spread of R. salmoninarum and therefore networks of movements are critical to BKD risks. These movements form a network whose structure determines the spread of disease. Such networks have been drawn up for both the salmon and trout industries in Scotland for 2003 data (Munro and Gregory 2009) and both Scottish and English networks are used here to analyse the interaction of salmon and trout production. Even when interaction is not directly between farms, R. salmoninarum may be transmitted through the environment by water movements or movement of wild and escaped fish and so disease may spread between farms that share watercourses. Movement networks can be used to assess the potential for increased risk for salmon should R. salmoninarum infection become widespread in trout. Three specific questions are addressed in this section: 1. Can Scottish and English production (combined salmon and trout) be managed separately? 2. Are salmon and trout networks separate? and 3. Even if salmon and trout networks are separate, how much contact do they have through shared drainage basins? Can English and Scottish Production be Separated? A network has been drawn up for movements to and from English trout and salmon production sites and Scottish sites (Figure 13). From this it is clear that some Scottish sites are tightly bound into the English network, with many contacts and therefore England and Scotland do not form separate compartments (Zepeda et al. 2008). Some of these sites are also important components in the Scottish movement network (not shown). This means that there are extensive movements across the border so the Scotland/England border is not a barrier to disease transmission and controls must be GB wide. 30

34 Figure 13. The English fish movement network for 2004 (grey circles), showing Scottish farms (black circles) that have links to that network. Circle size is proportional to the number of contacts. There are also other contact networks across this border. For example, when a viral haemorrhagic septicaemia (VHS) outbreak occurred in England, Scottish FHIs traced an extensive network of movements of lorries transporting both fish and fish products between farms and processing plants in northern England and southern Scotland. Smaller numbers of imports of live fish originate in Ireland or elsewhere in the EU (Smith 2007). The maximum input was parr and smolts in 2000, but this had fallen to in 2006; the import of ova is discussed in Section Are Salmon and Trout Networks Separate? A plot has been derived for the fish movement network in Scotland (Munro and Gregory 2009) in which nodes are divided into salmon, trout and those with both species (Figure 14). This network shows that there are very few links between trout and salmon farms. In addition the trout farms have few links to the mixed species nodes. The trout farms 31

35 are themselves broken into separate sections that do not interact (at least not within Scotland). Therefore pure trout farms do not connect with salmon farms to any significant extent. Figure 14. Salmon (pink), trout (black) and mixed (light blue) species movement networks for Scotland Node sizes are proportional to numbers of connections. Salmon farms interact widely and the network links most salmon farms together into a single huge network thus forming an epidemiological compartment (Zepeda et al. 2008). This means disease may have the potential to become widespread with movements in this network, although this may be less severe than it appears because of unidirectional movements. There are a number of mixed species elements within this cluster in the network and these may be related to sea reared trout farming but appear to be isolated from the main trout farming network. 32

36 Figure 15. The trout farm network and its connections to the salmon farm network. Connections to the salmon farming network are indicated by thick arrows connecting to picture of a fish (via a mixed species farm). Note that the main trout cluster and an isolated pair of trout farms have no connections to the salmon network and two minor clusters have only one connection each to the network. Also shown are Scottish sites with persistent R. salmoninarum infection (white) and Scottish sites involved in hatchery based outbreak (black). If trout farms are plotted separately (Figure 15) it can be seen that most form a single network which is entirely separate from the salmon network, while two smaller subcomponents are connected into the salmon network, but only by single routes of contact each (Munro and Gregory 2009). Therefore the trout movement network is to a very large degree separate from the salmon network and they may be treated as separate compartments. It can be demonstrated that BKD outbreaks in Scottish trout have followed the structure predicted by the network. Persistent infection (white symbols) does not spread from the infected sites which are dead-end nodes (Section 4.1). Sites that were positive (black symbols) in the hatchery based BKD outbreak (Section 4.2) 33

37 reflect movements in the network from this hatchery (S323); it is fortunate infection did not spread to S292 or the outbreak could have been considerably larger. This match between the network and observed outbreaks indicates that it is reasonable to assume that the lack of links between trout and salmon industries does represent a substantial barrier to disease transmission, and hence contributes greatly to risk reduction. In conclusion, broadly, pure trout farms are isolated from salmon farms in the network. There are some mixed species elements, most of which are within the salmon rather than the trout cluster. These mixed species farms are isolated from the main trout farming network and for the most part do not form a conduit by which disease in pure trout farms can be introduced into the salmon network Contacts between Salmon and Trout Farms in Shared Drainage Basins It has been established that there is little overlap between salmon and trout networks at the site level. The next step is to determine the level of contact between these industries when they are located in the same drainage basin. The location of trout and salmon farms in Scotland was mapped using geographic information systems GIS software (ESRI (UK) Ltd.). This illustrates that the majority of trout farms are in the south and east, while the majority of salmon farms are in the west or the Northern Isles (Figure 16). However, there is some overlap with trout and salmon farms sharing a number of small areas and some of these are illustrated on Figure 16. In Shetland there are a few trout farms and over 60 salmon farms. As discussed earlier, BKD has recently been detected in some Shetland salmon farms (Figure 16, area I) and the source of this is unknown. However, a group of mixed salmon and trout farms in the Western Isles (area II) has not been associated with BKD, possibly because these farms use their own trout broodstock to a large extent. On the west coast (area III) BKD has affected a group of marine salmon farms associated with freshwater site FS1 (which is possibly associated with trout farm TF1, although neither FS1 or TF1 (Figure 9) have tested positive for R. salmoninarum). There was a positive marine salmon site in the Western Isles however, this is associated with a movement from the area III cluster and is not associated with area II (Section 4.4). Further south (area IV) farms in Loch Awe and Loch Earn (which are in separate drainage basins) have been persistently infected (Section 4.1). Loch Awe drains into the west coast waters and might expose marine salmon or trout (which are found closer to the discharge) farms in these areas, however, there is no evidence for the transmission of infection. There is another shared drainage basin in southern Scotland (area V) consisting of two salmon and several trout farms. Although this represents a potential contact point between the industries, the salmon farms are on protected borehole water supplies greatly reducing this risk and infection has not been detected in any of these farms. 34

38 In total there are 27 Scottish catchments (consisting of main river and small coastal catchments) containing both farmed salmon and trout (the 2003 data has been used to be consistent with the contact network analysis). This list includes 17 catchments with single mixed species farms so where the risk is intra-site as opposed to inter-site interactions. In addition, some of these facilities are operated by fishery trusts or fishery boards so represent wild origin fish hence these will not be dealt with in this section. Of the 10 remaining catchments, some of which have multiple salmon farms located within, there were 14 salmon farms which share a water course with trout farms. Five of these salmon farms are separated from the nearest trout farm by 5 km or less, these are 0.106, 0.342, 0.84, 4.1 and 5.0 km from a trout farm. In 2003 there were 176 smolt production sites (Smith 2007), so it seems therefore that the great majority of Scottish freshwater salmon production occurs at sites that do not share catchments with pure trout farms. 35

39 Figure 16. Contact mapping 2003 illustrating all fish farms in the analysis: freshwater trout (red); salmon (blue); and mixed (yellow) farms. The symbol size is proportional to the number of contacts. Arrows mark the spread associated with a hatchery outbreak (Section 4.2). Inset map I. is the Shetland outbreak, Section 4.6, circles mark: II. an area of mixed salmon and trout farming not associated with BKD; III. the main west coast outbreaks and FS1, Sections 4.4 and 4.5; IV. an area of persistent BKD infection in rainbow trout, Section 4.1 and V. a drainage basin shared by salmon and trout and to date not associated with BKD. 36

40 In England and Wales there is a greater overlap with 22 of 26 salmon farms sharing catchments with trout farms (Figure 17). Seven of these farms, all from catchments containing trout, have exported salmon to Scotland. In addition two of these farms have also exported trout. Most of the non-mixed species sites have significant separation distances, with only one trout farm within 5 km of a salmon farm. Although trout farms are clearly separated from salmon farms in the network of fish movements there is some overlap at the drainage basin level. The potential for transmission in such circumstances is discussed in Section 7.4. Figure 17. English and Welsh salmon production sites. Colour of drainage basins is proportional to the number of trout farms in those basins. Sites from which fish have been exported to Scotland are shown as white. 37

41 7.2 Vertical Transmission of R. salmoninarum As discussed under epidemiology (Section 3.2), R. salmoninarum is a truly vertically transmitted pathogen (Paterson et al. 1981; Evelyn et al. 1986). This means that R. salmoninarum could be introduced with imported ova. Some 700,000 to 30M salmon ova are imported each year (Figure 18). The numbers of these imports are increasing with some coming from countries such as Iceland, Norway and the USA where BKD is present. Bacterial kidney disease was reported from salmon broodstock in Norway in 2008; illustrating the possibility of vertical transmission within the salmon industry. Although imports will be certified as R. salmoninarum free any failure in this process could represent a risk for the import of infection. Trout ova are also imported highlighting another route for introducing R. salmoninarum into the UK, however, this would be into the trout farming industry. Increased prevalence in the trout industry may increase the risk to the salmon industry, but only if the trout industry does represent a risk to salmon. Figure 18. Numbers and sources of imported salmon ova from outside the UK into Scotland (Smith 2007). If ova had been the source of infection in FS1 (Section 4.5) other sites would also have been expected to be infected as, even if the ova went to one hatchery, the parr would have been distributed to multiple smolt producing sites. As such the outbreak would be 38

42 expected to have been more widespread. However, if import did occur to freshwater there would be a risk of widespread secondary infection (Ruane et al. 2009). 7.3 Other Anthropogenic Networks Movement of contaminated equipment poses a risk of importing or moving pathogens. The well boat network was shown to play a key role in transmitting ISA during the 1998/9 epidemic (Murray et al. 2002) and fish transport lorries were identified as a potential risk factor for spreading VHS across the England-Scotland border during the 2005 outbreak. Empty fish transporters have been identified as a risk factor for import of pathogens (Peeler and Thrush 2009). The Shetland outbreak was confined to company Z and spatially scattered in a pattern that indicated anthropogenic spread. It did not, however, appear related to fish movements and therefore represents another anthropogenic network with well boats (possibly servicing a processing plant) possibly playing a role. Within the marine trout industry in Loch Etive, sites that shared facilities became infected, while a site that did not share facilities avoided infection, although it was also further away from the cluster of infection. Well boat traffic appears to be increasing, including international movements, and this could increase direct risks to salmon, thereby cutting relative risk from trout. 7.4 Hydrodynamic Transmission of R. salmoninarum In order for the geographical proximity of infected farms to represent a risk to uninfected farms it is necessary that the pathogen is transmitted between these farms. This could be via movements of wild or escaped fish (see later) but it may also occur through water movements. Therefore in this section we assess the potential for water-borne transmission of R. salmoninarum. 39

43 Figure 19. Exposed R. salmoninarum decays rapidly in the water, but bound to particles it is transported longer distances. However, if the particles are large these will sink and transport will again be limited. Current direction = blue arrow, Velocity = 0, 1, 2, 4, 8 or 16 cm/s. Horizontal transmission of R. salmoninarum has been demonstrated in seawater via contact with skin (Hoffman et al. 1984), eyes (Hendricks and Leek 1975; Hoffman et al. 1984) or consumption of faecal material (Balfry et al. 1996). This means hydrodynamic transmission is possible and this is likely to have occurred between separate cages in freshwater trout farms (Wallace et al. in prep), although vectors such as wild and escaped fish may also have played a role. Decay rates of exposed R. salmoninarum are rapid, with Balfry et al. (1996) finding that after 8 hours some 40 60% of R. salmoninarum had decayed in seawater (filtered and raw respectively). This is equivalent to a decay of 6-11% h -1, similar to ISAV and one which limits the potential for hydrodynamic dispersal (Murray et al. 2005). However, when bound to particles, decay is much slower, if 1-10% of R. salmoninarum are assumed to survive for a week when bound to particles this gives decay of 1-3% h -1, equivalent to IPNV and provides much greater potential for hydrodynamic transport (Murray et al. 2005). However, faeces have been calculated to have a settling velocity of ms -1 and using this estimate Gowen and Bradbury (1987) calculated that faeces may be distributed 200 m from a typical salmon farm. Maximum potential for hydrodynamic distribution depends on the faecal material breaking up into fine slowly sinking particles. When decay rates from the ranges cited above (6.4% and 1% h -1 ) are applied to the model of Murray et al. (2005) then the results are very different (Figure 19). Exposed 40

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