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An evaluation of the relative risks of infectious salmon anaemia transmission associated with different salmon harvesting methods in Scotland
Ocean & Coastal Management 46 (2003) 157–174
An evaluation of the relative risks of infectious salmon anaemia transmission associated with different salmon harvesting methods in Scotland Pauline D. Munroa,*, Alexander G. Murraya, David I. Frasera, Edmund J. Peelerb b
a Fisheries Research Services, P.O. Box 101, Victoria Road, Aberdeen AB11 9DB, UK CEFAS Weymouth Laboratory, The Nothe, Barrack Road, Weymouth, Dorset DT4 8UB, UK
Abstract In aquaculture, harvesting presents an unavoidable risk of disease transmission. The spread of the disease infectious salmon anaemia appears to have been associated with harvesting in both Scotland and Norway. An assessment is made of the relative risks of disease transmission associated with various different means of harvesting farmed salmon based on the assumption that best practice is followed for each harvest method. The assessment is qualitative, quantitative data being absent for most of the processes involved. Slaughter on the farm risks the spread of infection to adjacent farms, whereas, infection at a processing plant may be rebroadcast by well-boats. The risks associated with transporting live fish in cages and of storing live fish near centralised processing plants are discussed. Provided the vessel does not release contaminated water in the vicinity of salmon farms, transport of live fish directly to the processing plant for immediate slaughter by sea may be the safest means of collecting harvest. Crown Copyright r 2002 Published by Elsevier Science Ltd. All rights reserved.
1. Introduction Infectious salmon anaemia (ISA) was first recognised in Norwegian farmed Atlantic salmon (Salmo salar L.) in 1984 [1]. The causal agent was proven to be a virus [2], and subsequently shown to be an enveloped RNA virus of the Orthomyxoviridae family [3]. ISA outbreaks have been confirmed in Canada since *Corresponding author. Fax: +44-1224-295-511. E-mail address: [email protected] (P.D. Munro). 0964-5691/03/$ - see front matter Crown Copyright r 2002 Published by Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 4 - 5 6 9 1 ( 0 2 ) 0 0 1 2 5 - 4
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1996 [4,5], Scotland in 1998/9 [6], Chile [7] and the Faeroes since 1999 and since 2000 in the USA [8]. It is listed under ‘‘diseases notifiable to Office International des Epizooties (OIE)’’. Fish affected with ISA suffer anaemia and are often observed swimming near to the surface of the water swallowing air. A high level of mortality is common. For example, 80% mortality occurred in the first outbreak in Norway [9]. The last outbreak of ISA in the UK was in farmed salmon in Scotland 1998/9 [10]. ISA is classified as a List I disease under European Union legislation and the Scottish Executive is obliged to follow an eradication policy through the withdrawal of all fish on infected premises. ISA virus (ISAV) can be transmitted between farms by human activities and during the Scottish outbreak of 1998/9 cases of ISAV could usually be traced to a specific contact [10]. However, wild carrier fish are a potential source of infection [11,12] and it is theoretically possible, but extremely improbable, that birds may transmit the virus mechanically, or by regurgitation of an infected fish. The movement of live fish stocks between farms carries the highest risk per event. In the Scottish outbreak a large number of cases appeared to be associated with harvesting operations [11,13]. The risk involved the transport of live fish to holding cages adjacent to a processing plant, hereafter referred to as a harvest station, which became infected. Unloaded ships leaving this harvest station then rebroadcast the infection. Current technology enables a number of different methods to be used when harvesting farmed salmon. The method of choice will depend on several factors, including the remoteness of the location, the access to a processing plant and the size and number of fish to be harvested. In this risk assessment, various harvesting methods are compared for their associated risk of transmission of ISA based on an assumption that best practice is followed, i.e. risk reduction measures are employed, for all the harvest methods described. Recommendations are made to reduce the likelihood of ISA transmission associated with harvesting. These recommendations will also be effective in reducing transmission of other fish diseases.
2. Materials and methods 2.1. Risk assessment This paper will assess the risks of ISA being spread by eight harvest methods. An assessment of the consequences of ISA will not be considered. The harvest operations were ranked according to the probability of transmission of ISAV. For each harvest operation the risks of transmission to farms in the vicinity of the harvested farm, farms en route between the harvested farm and the processing plant, and in the vicinity of the processing plant are considered. The possibility of a harvesting station near the processing plant becoming a source of infection and re-broadcasting the infection is assessed. An outbreak of ISA at a harvest station is important since it may result in widespread transmission [13]. We also assess the risk of mechanical transmission between farms.
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The Joint Government/Industry Working Group on ISA, whose membership comprised representatives from the Scottish Executive Environment and Rural Affairs Department, Fisheries Research Services (FRS), the State Veterinary Service, the Scottish Environment Protection Agency and the Scottish trout and salmon farming industries, concluded that one of the major risks associated with harvesting was environmental contamination with blood and other processing waste. They recommended that blood water effluent from salmon processing plants should be disinfected before discharge and other processing waste should be ensiled [14]. For the purposes of this risk assessment, the assumption was made that risk reduction measures are employed where possible. For example, it was assumed that blood is contained during all harvesting methods that involve slaughter at sea and blood water from the processing plant is disinfected in all cases. It was also assumed that vessels used to transport live fish for harvest, such as well-boats, operate with the valves closed to prevent water exchange in the vicinity of fish farms other than the farm where the fish are uploaded. Currently, the FRS Fish Health Inspectorate monitors compliance with the recommendations of the Joint Government/Industry Working Group on ISA during routine inspections of fish farms throughout Scotland. Although every harvesting operation cannot be inspected, compliance to date has been high.
2.2. Harvesting methods The harvest methods assessed (Figs. 1a and b) were: Slaughter on site M1 Fish killed and bled into the wells of a well-boat then transported by sea direct to the processing plant. M2 Fish killed and bled into the wells of a well-boat then transported to a local pier for transfer into a tanker or harvest tubs for onward transport to the processing plant by road. M3 Fish killed and bled into harvest tubs onboard a boat then transported to a local pier where the tubs are transferred onto a vehicle for onward transport by road to the processing plant. M4 Fish killed and bled into harvest tubs onboard a harvesting barge, transferred to a boat and transported to a local pier before transfer onto a vehicle for onward transport by road to the processing plant. M5 Fish killed and bled into harvest tubs on a boat then transferred by sea to a processing plant. Slaughter at a killing station at or near a processing plant M6 Live fish transported by well-boat direct to a processing plant and killed and bled within the plant. M7 Live fish transported by well-boat to a harvest station (cages situated near a processing plant). M8 Live fish in cages towed to a harvest station near a processing plant.
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Fig. 1. (a) Harvest methods involving the transport of dead fish. (b) Harvest methods involving the transport of live fish.
3. Results 3.1. Hazard ID This paper refers to the risk of ISAV transmission from harvesting techniques, however, many of the conclusions will be applicable to other diseases.
3.2. Release assessment Harvesting methods may result in the release of ISAV through four main pathways: 1, escape of live fish; 2, loss of dead fish; 3, discharge of blood, effluent and ballast water and 4, mechanical transmission. The harvesting methods pertinent to each pathway are summarised in Table 1. Three categories of farms may be affected: A, farms neighbouring the farm where the salmon are harvested; B, farms en route to the harvesting station or processing plant and C, farms neighbouring the harvesting station or processing plant (Fig. 2). It was assumed that when fish were transferred from a boat to a lorry the transfer took place at a pier local to the farm. A detailed list of the risks posed by each method is given in Appendix A.
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Table 1 Summary of biological routes of transmission by harvest method Routes of transmission
Harvest methods
A. Transmission to neighbouring farms Escape of live fish Loss of dead fish Discharge of blood, effluent
M1–8 M1–5 M1–5
B. Transmission to farms en route to pier/harvest station/processing plant Escape of live fish Loss of dead fish Discharge of blood effluent or ballast water
M6–8 M1–5 M1–8
C. Transmission to farms neighbouring pier/harvest station/processing plant Escape of live fish Loss of dead fish Discharge of blood, effluent or ballast water
M6–8 M1–5 M1–7
D. Mechanical transmission Divers removing morts before harvest moving between farms Shared harvesting equipment Well-boats moving between farms Shared staff moving between farms
M1–8 M1–5 M1, 2, 6, 7, 8 M1–8
Fig. 2. Map illustrating: (A) farms neighbouring the salmon farm being harvested, (B) farms en route to the harvest station or processing plant and (C) farms neighbouring the harvesting station or processing plant.
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3.3. Exposure assessment An outbreak of ISA will only occur if the ISAV which has been released into the aquatic environment comes into contact with and infects a susceptible host(s), and that infected individual(s) infects more than one other individual (basic rate of reproduction (R0 ) greater than one [15]). The escape of live salmon is considerably more likely to result in ISAV transmission to other fish farms compared with the loss of dead salmon. The behaviour of escaped salmon is likely to depend on their development stage. For example, grilse may head for fresh water. Escaped salmon may be attracted to fish farms in search of food. Although salmon clinically infected with ISAV may not travel far, sub-clinically infected individuals may survive a considerable length of time and travel some distance. The loss of an infected dead salmon will only result in ISA becoming established if a susceptible fish is exposed to a sufficient viral dose to cause infection. Hence, the loss of a few dead salmon when loading or unloading is unlikely to result in a disease outbreak. The release of blood, effluent or ballast water will only result in disease transmission if the viral load is sufficient to infect susceptible fish. Continual high volume effluent discharge from a processing plant poses an important risk; however, small spillages of blood or effluent from on farm killing, or when loading or unloading, may be less likely to cause ISAV transmission. The mechanical transmission of ISAV is possible since the virus will survive in seawater at pH 7.2 at 10 C for more than 24 h [16].
3.4. Ranking The ranking of the harvesting methods according to the likelihood of transmission to the three categories of farms is summarised in Table 2.
Table 2 Ranking of risk of ISAV transmission by harvesting method Probability of disease transmission
High
Low
Risk of ISAV transmission to Neighbouring farms
Farms en route to processing plant
Farms in vicinity of processing plant
M8 M2 M4 M3 M5 M1 M6,7
M8 M6, 7 (bad weather) M5 M6, 7 (good weather) M1 M2,3,4
M7 M8 M1 M5 M6 M2,3,4
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3.4.1. Transmission to neighbouring farms For methods M2–M4, the pier where fish are unloaded is considered local to the farm and the risks of transport to the pier are considered as risks to farms neighbouring the harvested farm. All harvest methods may result in the loss of live fish into the aquatic environment. If the fish are killed at the farm of origin (methods M1–M5) then it is possible that occasionally a fish will escape from the killing table. For methods M6–M8, a low possibility exists for fish to escape whilst being loaded into well-boats or tubs. A high risk of spreading infection in the vicinity of the farm is associated with towing cages, which has a high risk of allowing escapes from torn nets (method M8). Low risks are also associated with the possible accidental discharge of blood or effluent when fish are killed at the farm of origin (methods M1–M5) and again at transfer at a local pier (methods M2–M4). Overall, the transport of live fish directly to the processing plant by boat (methods M6 and M7) poses few risks to local farms. 3.4.2. Transmission to farms en route to the processing plant The escape of live fish en route to the processing plant or harvest station is only possible for methods M6–M8, and under normal circumstances the possibility is diminishingly small except for method M8, which carries a high risk of escape from torn nets. In practice, method M8 would only be applied within the vicinity of the processing plant, i.e. over short distances. In the case of mechanical failure of a wellboat the fish would have to be transferred to another vessel which would increase the risk of escape. Loss of dead fish en route to the processing plant (methods M1 and M5) is unlikely, although road accidents leading to the spillage of full harvest tubs have been known. There is a risk that lorries transporting dead fish from the pier to the processing plant may leak ISAV contaminated water. The probability that this will result in ISAV being introduced into the aquatic environment is considered remote, particularly if sealed harvest bins in good condition are used. Adverse weather conditions will increase the risk of transmission of disease to farms en route to the processing plant for methods M6 and M7 because the well-boat may have to shelter near the coast in relatively close proximity to fish farms. The longer the bad weather persists, the greater the likelihood that the valves will be opened for water exchange in order to keep the fish alive and, thus, the greater the risk of disease transmission to farms in the area. New well-boat designs with chilled, recirculated water facilities, which would eliminate the risk of release of contaminated water, are under trial elsewhere but this technology is not yet available in Scotland. Although improbable, in extremely severe weather conditions the entire cargo may be lost. 3.4.3. Transmission to farms near the processing plant and harvest station Live fish may also escape during unloading at the processing plant but the probability is low. Loss of live fish from the harvest station is more likely (methods M7 and M8), since fish may be kept there for some time and the cages may be damaged in bad weather or from attacks by seals or vandals.
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The frequency of well-boat movements and potential for fish from multiple sources to be transported to the harvest station cages increases the risk of ISAV transmission to farms near a harvesting station (methods M7 and M8). The stress of transport may increase susceptibility to infection and induce pathogen shedding in subclinically affected individuals or result in clinical disease. The risk of disease transmission to neighbouring farms will increase with the period fish spend in the harvest station cages. Cages are also held near the processing plant under method M8, but the fish in the cages are from only one source and are usually held for a relatively short period. The risk of infection of farms near a processing plant associated with methods M2–M4 is deemed to be very low since these methods involve road transport to the plant. 3.4.4. Risk of rebroadcast infection from the processing plant Processing plants may act as sources of infection, particularly when a harvest station is associated with the plant. Harvest stations are potential reservoirs of infection, since fish from different farms are in close proximity and the stress of transport will increase the risk of virus shedding. The fish may also be exposed to pathogens in the effluent discharged from a processing plant, even if the discharge is disinfected [9]. When fish are unloaded from well-boats at a processing plant or harvest station, ballast water is taken, which is then be discharged when a new harvest is loaded. If there is ISAV present in the environment it may be transported. A low risk of disease transmission is associated with each journey but the very large number of harvesting vessels visiting a busy processing plant means that is a potentially important source of transmission. These risks only apply to methods M7 and M8, and M1, M5 and M6 if a harvest station is located at the processing plant. Transmission of disease via harvest tubs is also possible. 3.4.5. Risk associated with contaminated equipment Divers may be used to remove morts before any of the harvesting methods are used. Poor disinfection of diving suits and equipment may result in transfer of ISAV to other farms visited by the diver. More equipment and personnel are involved in methods M1–M5, compared with M6–M8. Again, if the equipment and personnel move to another farm without strict attention to disinfection, ISAV may be transmitted. There are detailed guidelines for well-boat disinfection and inspection [17]. If these guidelines are not followed then the movement of well-boats between farms may result in disease transmission. Well-boats are relatively difficult to disinfect due to their size and limited accessibility or number of inspection hatches associated with the fish pumps. It is possible for dead fish to be left in the pumps. Harvest barges are also difficult to disinfect due to their size but, given the high number of well-boat movements between farms, the risk of disease transmission if a well-boat is not disinfected effectively is relatively high. The risks associated with mechanical transmission by different pieces of equipment used in harvesting fish are ranked in Table 3.
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Table 3 Ranking of equipment used in harvesting fish according to the risk of transmitting ISA Probability
Equipment
High Well-boat Harvest barge Grading equipment Killing tables Harvest tubs Site boat Personnel Vehicles Low
Disinfection reduces the risk associated with equipment but does not necessarily eliminate it. If the concentration of disinfectant used is incorrect or the contact time is insufficient some virus particles may not be inactivated. Similarly, virus particles may remain active if they are harboured in tissue or detritus and, therefore, not accessible to the disinfectant.
4. Discussion A range of different harvesting methods were assessed for the risk of transmission of disease to neighbouring farms, farms en route to the processing plant and farms in the vicinity of the processing plant. It was not possible to quantify the level of risk associated with each activity due to the limited amount of data available. Instead, the methods were compared against each other. Because risk factors depend upon the nature of the environment it is quite possible that the lowest risk will apply to different methods for different farms and that lowest risk can vary with time depending upon weather episodes, season or inter-annual climate variation. Overall, harvesting fish poses the greatest risk of ISA transmission to farms in the vicinity of the processing plant; the risk to farms in the vicinity of the harvested farm is lower, but still significant. The increased risk of ISA is lowest for farms en route to the processing plant. 4.1. Risk to farms in the vicinity of a harvested farm It has been shown in Norway that the risk of ISA increases for farms within 5 km of an infected farm, compared with more distant farms [9]. The risk has also been found to increase with the number of ISA-infected neighbouring farms [18]. If the farm is infected then harvesting methods where fish are killed on site (methods M1–M5) will result in an increased risk of transmission. Slaughter on site may result
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in blood spillage, escape of fish from the killing table and movement of contaminated equipment to other farms. These are significant risks that are not associated with the movement of live fish. The risks to local farms will be increased by spillage of blood or dead fish during the transfer at a local pier (methods M2–M4).
4.2. Risks to farms en route to a processing plant Overall the risk to farms en route to a processing plant is small assuming risk mitigating factors are employed, except where fish are transported in cages. When fish are transported by other means, a significant risk only occurs in bad weather when well-boats carrying live fish may have to take shelter on route to the processing plant and open the valves to ensure the fish are kept alive.
4.3. Risks to farms in the vicinity of a processing plant It has been found in Norway that farms within 5 km of a processing plant had an increased risk of ISA, compared with farms more distant; even when the effluent from the processing plant was disinfected [9]. Similarly, the number of processing plants near a farm was positively associated with the risk of ISA [18]. The risk of disease transmission to farms in the vicinity of the processing plant is from effluent discharge, or disease in the fish kept at the harvest station. By comparison, the disease risk directly resulting from the harvesting methods, i.e. risks associated with unloading, is very low. The Norwegian studies [9,18] indicated that ISAV can survive outside the host for a considerable length of time and be transmitted considerable distances in seawater. This suggests that untreated blood and effluent from on site killing and processing plants pose a real risk of disease transmission. Fish kept at a harvest station are highly likely to become infected in the event of an ISA outbreak since they originate from a number of sources, they are stressed and thus predisposed to infection and more likely to shed ISAV. They are also likely to be infected from contaminated effluent from the neighbouring processing plant. Harvesting stations, therefore, pose a very serious threat to neighbouring farms. If ISAV becomes established at a harvesting station, well-boat movements could spread the virus to many farms, as occurred in Scotland in 1998 [13]. Although the risk per journey is probably small, the large number of vessels leaving a processing plant and the wide area that they cover makes this a serious risk for ISA spread. At the time of the ISA outbreak in Scotland, the effluent from a processing plant situated near the harvest station, from which many well-boat movements occurred, was not disinfected prior to discharge. ISAV could have been spread by well-boats taking up water contaminated by effluent directly from the plant. In addition, infection could have been maintained in fish exposed to contaminated effluent in the holding cages at the harvest station resulting in additional shedding of ISAV. Disinfection of the processing plant effluent would have reduced both these risks and could potentially have prevented the spread of ISA to other farms.
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4.4. Mechanical transmission Studies from Norway and Canada which have investigated risk factors for ISA [9,18,19] confirm that mechanical transmission is an important source of spread. Shared personnel [18], the movement of boats between farms [19] and divers were shown to be risk factors. Well-boats delivering fish to a processing plant with a harvest station were implicated in the last outbreak of ISA in Scotland [13].
5. Conclusions The most serious risks of ISA transmission associated with harvesting are associated with holding live fish in cages, known as harvest stations, adjacent to processing plants and the discharge of untreated effluent from processing plants. It is recommended that holding live fish in harvest stations near the processing plant is phased out. Meanwhile, fish in such holding cages should be regularly monitored for clinical signs of disease to ensure rapid detection and the residence time in the cages should be kept as short as possible. Effluent from processing plants should be treated to inactivate ISAV and other pathogens. This measure has been effective in reducing the number of ISA outbreaks in Norway. In general, if well-boats operate with their values closed to prevent water exchange in the vicinity of fish farms and the recommended disinfection and ballast discharge procedures are followed, large shipments of live fish in well-boats directly to a processing plant is a safe method of harvesting. It is suggested that the operation of well-boats is investigated. It is important to establish how frequently they operate with the values open and whether disinfection and ballast discharge recommendations are followed. A maximum journey time may be required to be specified to ensure that the boats operate with the values closed. The harvesting method which is most likely to spread ISA is method M8, towing cages of live fish to a harvesting station at processing plant. Cages are only likely to be towed to a harvest station if the distance between the farm and the harvest station is relatively short. It is recommended that this harvesting method be discontinued. There is a real risk of mechanical spread of ISAV between farms. Efforts should be made to make farmers aware of the biosecurity measures that are required to minimise the risk of ISAV spread. A list of mitigating factors for the transmission of ISA by harvesting methods is presented in Appendix B. A more accurate assessment of the risks associated with harvesting can be achieved by taking a more quantitative approach (see Appendix C). The numbers of farms in each of the three categories considered could be calculated. Generally, the risk of transmission will be positively associated with the number of movements of harvested fish. Occasional large shipments probably pose less risk than more frequent shipments of smaller volume. Data could be obtained on the volumes of fish moved by different methods. Absolute risks for each harvesting method cannot realistically be estimated; however, scoring the risks would enable an overall ranking to be obtained. The following areas need to be investigated in order to generate the
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data needed for a better evaluation of the risk of ISAV transmission: dose required to cause infection, the epidemiological importance of the carrier state, the viral load in the tissues of an infected individual, survival of ISAV outside of the host under various conditions. A more complete list of data required for quantitative risk analysis is presented in Appendix C. The release assessment for ISAV will be largely applicable for other salmon pathogens. The exposure assessment depends to a greater extent on the characteristics of the pathogen, i.e. survival in the aquatic environment, required infective dose, etc. For example, infectious pancreatic necrosis (IPN) virus is more robust and has more known carrier species than ISAV, as a result IPN is more likely to be spread through the environment and the relative role of the factors discussed here is less than for ISA. Overall, however, the recommendations made in this report will also be effective at reducing the transmission of other fish pathogens. Appendix A. Risk factors The risk factors associated with each of the harvesting methods described above are listed below. They are not ranked in any order. Method M1: dead fish in well-boat direct to processing plant * * * * *
* * * *
Blood spillage at point of slaughter Fish escapes from killing table Possible blood loss if valves are opened accidentally or otherwise Adverse weather conditions could lead to catastrophic loss if shipwreck occurs Mechanical failure of well-boat engine could lead to increased risk associated with transfer of fish at sea or catastrophic loss Blood spillage at pier while pumping fish into processing plant Dead fish may be left in pumps Inadequate disinfection of blood residue in wells before disposal Inadequate disinfection of well-boats between operations on different sites. Method M2: dead fish in well-boat to local pier
* * * * *
* *
* * *
Blood spillage at point of slaughter Fish escapes from killing table Possible blood loss if valves are opened accidentally or otherwise Adverse weather conditions could lead to catastrophic loss if shipwreck occurs Mechanical failure of well-boat engine could lead to increased risk associated with transfer of fish at sea or catastrophic loss Blood spillage at pier while transferring fish to tanker/harvest tubs Loss of harvest tubs during transport by road, which could be a disease risk for watercourses Tanker/harvest tubs must be disinfected after use Cross contamination of clean and dirty tubs Inadequate disinfection of vehicles used to transport harvest tubs.
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Method M3: dead fish in harvest tubs to local pier * * * * * * * * * * *
Blood spillage at point of slaughter Fish escapes from killing table Accidental loss from tub due to tipping Bad weather increases risk of loss Tubs must not be cracked or overfilled Lower capacity than well-boat leads to more frequent trips Harvest tubs must be disinfected properly Tubs could fall during transfer at the pier or during transport by road Blood leakage during road transport Tub liners pose disposal problem Frequent movements by road. Method M4: harvest tubs on barge transferred by sea to local pier
* *
As Method M3 but increased number of tub transfers increases risk Barge difficult to disinfect, should be site specific or limited to a management area at least. Method M5: harvest tubs direct to processing plant by sea
* * * * * * * * *
Blood spillage at point of slaughter Fish escapes from killing table Tendency to overfill tubs, resulting in spillage of blood and effluent Increased risk of fish loss if harvest tub falls Bad weather increases risk of loss Tubs must not be cracked or overfilled Lower capacity than well-boat leads to more frequent trips Harvest tubs must be disinfected properly Tubs could fall during transfer at the pier. Method M6: live fish in well-boat direct to processing plant
* * *
*
* *
*
Fish escapes during uplift from cages Bad weather could cause catastrophic loss or disposal problem if fish die on route Potential for disease transmission if valves are opened accidentally or otherwise, increases with distance from processing plant and in adverse weather conditions Mechanical failure of well-boat engine could lead to increased risk associated with transfer of fish at sea or catastrophic loss Risk of fish escape during transfer to killing station Transfer water must be returned to site of origin or disinfected before discharge, if free of blood, effluent or fish material. Pumps and wells must be inspected for the presence of fish/organic material and disinfected.
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Method M7: live fish in well-boat to cages at processing plant *
* * *
As method M6 except increased risk of waterborne pathogen transfer to farms in the region of the processing plant Risk of stress-induced disease Fish from multiple origins increases likelihood of disease Fish could act as reservoir for pathogens in processing plant effluent or escapes, which may for a focal point for widespread infection. Method M8: live fish towed in cages to processing plant
* *
*
*
Risk of fish escapes increases in adverse weather conditions Fish escapes possible if net snags on sea bed or in general movement or slaughter operations. Fish could act as reservoir for pathogens in processing plant effluent or escapes, which may for a focal point for widespread infection Risk of stress-induced disease.
Appendix B. Mitigating factors The risks associated with any harvesting method can be reduced by implementing risk reduction measures. Examples of risk reduction measures for each of the harvest methods are described below. Method M1: dead fish in well-boat direct to processing plant * *
* * * * * * * * * *
High sides on killing table and nets on deck to reduce potential for escapes Tarpaulin under killing table to contain blood spillage, check to ensure fish cannot escape from the vessel when tarpaulin is in place. Disinfectant on board to treat blood spillages and disinfect equipment Harvest in good weather conditions Ensure sufficient time for the movement Ensure valves are kept closed on route to processing plant Carry out regular maintenance to reduce risk of breakdown Disinfect residual blood in wells Disinfected wells between trips Conduct regular pipe inspections Tarpaulin underneath transfer pipe to catch fish or blood if the pipe bursts Inspection hatches to fish pumps to ensure all fish removed. Method M2: dead fish in well-boat to local pier
* *
As method M1 but in addition tanker or harvest tubs must be properly disinfected Disinfectant required at transfer point to treat blood spillages
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Dedicated tanker required, not visiting fish farms Any residual discharges should be properly treated Use only experienced staff particularly fork lift operator. Method M3: dead fish in harvest tubs to local pier
* * * * * * * * * * *
High sides on killing table and nets on deck to reduce potential for escapes Tarpaulin under killing table to contain blood spillage Disinfectant on board to treat blood spillages and disinfect equipment Harvest in good weather conditions Check harvest tubs for cracks regularly, replace damaged tubs Use sealed harvest tub liners and do not overfill tubs Use tubs with close-fitting lids and securing straps and should not be overfilled Blood and effluent should be held in separate tubs and treated prior to disposal Use dedicated vehicles or disinfected vehicles, including wheels, between trips Vehicle should carry disinfectant to treat spillages Vehicles should travel safely using an agreed route. Method M4: harvest tubs on barge transferred by sea to local pier
*
*
As method M3 but, in addition, harvest barge should be dedicated to one site or one management area Disinfectant should be available on board the harvest barge to deal with blood spillages. Method M5: harvest tubs direct to processing plant by sea
*
As method M3. Method M6: live fish in well-boat direct to processing plant
* * * * *
* * * *
Harvest in good weather conditions Carry out regular maintenance to reduce risk of breakdown Ensure valves remain closed on route to processing plant Do not over stock wells Ensure distance to processing plant does not exceed capacity to keep fish alive without opening valves, ensure adequate time for movement. Only transfer healthy fish Route well-boat to avoid fish farms. Have oxygen supply available to extend holding period if necessary Residual discharges from the vessel should be properly disinfected. Method M7: live fish in well-boat to cages at processing plant
*
As method M6 but, in addition, minimise residence time in cages at harvesting station
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Carry out regular net inspections to prevent escapes Only transport apparently healthy fish Remove damaged/dead fishes immediately. Method M8: live fish towed in cages to processing plant
* * * * * * *
Only ever tow cages in good weather conditions Tow cages slowly with the tide Carry out regular net inspections Clean and disinfect nets afterwards Use experienced personnel only who know the sea bed in the area Tow only healthy fish Remove damaged/dead fish immediately.
Appendix C. Data required for quantitative evaluation of risks We have only attempted to provide a qualitative assessment of the relative risks. To analyse risks in a quantitative manner would require far more data than is available. Some data is available from Norway on the processes that favour transmission of ISAV and data from Scotland was used to assess the role of wellboats in transfer of the pathogen [13]. However, practices are being constantly evolved and hopefully improved, so historical risks may not be a guide to the current situation. Risks must be assessed for discharge of waste, escaped fish, management failures and the extent of shipping associated with harvesting operation. Dead fish and waste risks * * *
*
Viral Titre and Survival Times in discharges of blood, tissue and dead fish Probabilities of release of blood, tissue or dead fish during harvest Probabilities of release of blood, tissue or dead fish during loading/unloading operations at the farm, at the pier or processing plant, or during emergency unloading operation at sea and depending upon whether tubs or well-boats are used to transport the fish Numbers of farms within areas into which blood, tissue or dead fish will disperse in a given period, or within 1, 2 and 5 km radii if detailed analysis of local currents is impractical. Escaped fish risks
* *
* * *
Period of persistence of virus in escaped fish so they act as source of virus Behaviour of escaped fish, do they remain near site of escape, disperse out to sea or move to the vicinity of other fish farms Probability and numbers of escapes during harvesting operations Probability and numbers of escapes during loading/unloading of live fish Probability and numbers of escapes during towing of cages.
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Poor management risks *
*
* * * *
* * *
Probability of virus survival in inadequately disinfected tubs or holds or on shared equipment Probability that disinfection or inspection processes for equipment or ships are inadequate Extent to which equipment is shared between farms or site dedicated Probability valves are opened during transport Probability of breakdown of ships or road vehicles Frequency with which farms are inspected for pathogens and in particular any fish held near processing plants are inspected Frequency with which dead fish are removed from cages Degree of stress or overcrowding in cages Adequacy of disinfection of slaughter and processing effluent Shipping data
* * *
*
Source, destination and routes of movements of ships with respect to farms Numbers of harvest visits required by a site Frequency with which ships seek shelter on route and locations where shelter is available, with the numbers of farms in the vicinity of these locations Weather conditions along the route.
References [1] Thorud K, Djupvik H. Infectious salmon anaemia in Atlantic salmon (Salmo salar L.). Bulletin of the European Association of Fish Pathologists 1988;8:109–11. [2] Dannevig BH, Falk K, Namork E. Isolation of the causal virus of infectious salmon anaemia (ISA) in a long-term cell line from Atlantic salmon head kidney. Journal of General Virology 1995;76:1353–9. [3] Falk K, Namork E, Mjaaland S, Rimstad E, Dannevig BH. Characterisation of infectious salmon anaemia virus, an orthomyxo-like virus isolated from Atlantic slamon (Salmo salar L.). Journal of Virology 1997;71:9016–23. [4] Lovely JE, Dannevig BH, Falk K, Hutchin L, MacKinnon AM, Melville KJ, Rimstad E, Griffiths SG. First identification of infectious salmon anaemia virus in North America with haemorrhagic kidney syndrome. Diseases of Aquatic Organisms, 1999;35:145–8. [5] Mullins JE, Groman D, Wadowska D. Infectious salmon anaemia in salt water Atlantic salmon (Salmo salar L.) in New Brunswick, Canada. Bulletin of the European Association of Fish Pathologists 1998;18:110–4. [6] Rodger HA, Turnbull T, Muir T, Millar S, Richards RH. Infectious salmon anaemia in the United Kingdom. Bulletin of the European Association of Fish Pathologists 1998;18:115–6. [7] Kibenge FSB, G!arate ON, Johnson G, Arriagada R, Kibenge MJT, Wadowska D. Isolation and identification of infectious salmon anaemia virus (ISAV) from Coho salmon in Chile. Diseases of Aquatic Organisms 2001;45:9–18. [8] Bouchard DA, Brockway K, Giray C, Keleher W, Merrill PL. First report of infectious salmon anaemia (ISA) in the United States. Bulletin of the European Association of Fish Pathologists 2001;21:86–8. [9] Jarp J, Karlsen E. Infectious salmon anaemia (ISA) risk factors in sea-cultured Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 1997;28:79–86.
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[10] Stagg RM, Bruno DW, Cunningham CO, Raynard RS, Munro PD, Murray AG, Allan CET, Smail DA, McVicar AH, Hastings TS. Epizootiological investigations into an outbreak of Infectious Salmon Anaemia (ISA) in Scotland. Fisheries Research Services, Aberdeen, 2001. [11] Nylund A, Jakobsen P. Sea trout as a carrier for infectious salmon anaemia (ISA). Journal of Fish Biology 1995;47:174–6. [12] Raynard RS, Murray AG, Gregory A. Infectious salmon anaemia virus in wild fish in Scotland. Diseases of Aquatic Organisms 2001;46:93–100. [13] Murray AG, Smith RJ, Stagg RM. Shipping and the spread of infectious salmon anemia in Scottish aquaculture. Emerging Infectious Diseases 2002, in press. [14] Anon. Final Report of the Joint Government/Industry Working Group on Infectious Salmon Anaemia (ISA). Fisheries Research Services, Aberdeen, 2000a. [15] Anderson R, Nokes DJ. Mathematical models of transmission and control. In: Detels R, Holland WW, McEwen J, Omenn GS, editors. Oxford textbook of public health., Vol. 1. Oxford: Oxford University Press, 1997. p. 689–719. [16] Munro P, Allan C. Infectious salmon anaemia. Bulletin of the European Association of Fish Pathologists 1999;19:286–8. [17] Anon. A Code of Practice to Avoid, Minimise the Impact of Infectious Salmon Anaemia (ISA). The Crown Estate, Edinburgh, 2000b. [18] Vagsholm I, Djupvik HO, Willumsen FV, Tveit AM, Tangen K. Infectious salmon anaemia (ISA) epidemiology in Norway. Preventive Veterinary Medicine, 1994;19:277. [19] Hammell KL, Dohoo IR. The epidemiology of hemorrhagic kidney syndrome—infectious salmon anaemia in Atlantic salmon in Atlantic Canada. Paper presented at the Society for Veterinary Epidemiology and Preventive Veterinary Medicine, Bristol, 1999.
An evaluation of the relative risks of infectious salmon anaemia transmission associated with different salmon harvesting methods in Scotland Pauline D. Munroa,*, Alexander G. Murraya, David I. Frasera, Edmund J. Peelerb b
a Fisheries Research Services, P.O. Box 101, Victoria Road, Aberdeen AB11 9DB, UK CEFAS Weymouth Laboratory, The Nothe, Barrack Road, Weymouth, Dorset DT4 8UB, UK
Abstract In aquaculture, harvesting presents an unavoidable risk of disease transmission. The spread of the disease infectious salmon anaemia appears to have been associated with harvesting in both Scotland and Norway. An assessment is made of the relative risks of disease transmission associated with various different means of harvesting farmed salmon based on the assumption that best practice is followed for each harvest method. The assessment is qualitative, quantitative data being absent for most of the processes involved. Slaughter on the farm risks the spread of infection to adjacent farms, whereas, infection at a processing plant may be rebroadcast by well-boats. The risks associated with transporting live fish in cages and of storing live fish near centralised processing plants are discussed. Provided the vessel does not release contaminated water in the vicinity of salmon farms, transport of live fish directly to the processing plant for immediate slaughter by sea may be the safest means of collecting harvest. Crown Copyright r 2002 Published by Elsevier Science Ltd. All rights reserved.
1. Introduction Infectious salmon anaemia (ISA) was first recognised in Norwegian farmed Atlantic salmon (Salmo salar L.) in 1984 [1]. The causal agent was proven to be a virus [2], and subsequently shown to be an enveloped RNA virus of the Orthomyxoviridae family [3]. ISA outbreaks have been confirmed in Canada since *Corresponding author. Fax: +44-1224-295-511. E-mail address: [email protected] (P.D. Munro). 0964-5691/03/$ - see front matter Crown Copyright r 2002 Published by Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 4 - 5 6 9 1 ( 0 2 ) 0 0 1 2 5 - 4
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1996 [4,5], Scotland in 1998/9 [6], Chile [7] and the Faeroes since 1999 and since 2000 in the USA [8]. It is listed under ‘‘diseases notifiable to Office International des Epizooties (OIE)’’. Fish affected with ISA suffer anaemia and are often observed swimming near to the surface of the water swallowing air. A high level of mortality is common. For example, 80% mortality occurred in the first outbreak in Norway [9]. The last outbreak of ISA in the UK was in farmed salmon in Scotland 1998/9 [10]. ISA is classified as a List I disease under European Union legislation and the Scottish Executive is obliged to follow an eradication policy through the withdrawal of all fish on infected premises. ISA virus (ISAV) can be transmitted between farms by human activities and during the Scottish outbreak of 1998/9 cases of ISAV could usually be traced to a specific contact [10]. However, wild carrier fish are a potential source of infection [11,12] and it is theoretically possible, but extremely improbable, that birds may transmit the virus mechanically, or by regurgitation of an infected fish. The movement of live fish stocks between farms carries the highest risk per event. In the Scottish outbreak a large number of cases appeared to be associated with harvesting operations [11,13]. The risk involved the transport of live fish to holding cages adjacent to a processing plant, hereafter referred to as a harvest station, which became infected. Unloaded ships leaving this harvest station then rebroadcast the infection. Current technology enables a number of different methods to be used when harvesting farmed salmon. The method of choice will depend on several factors, including the remoteness of the location, the access to a processing plant and the size and number of fish to be harvested. In this risk assessment, various harvesting methods are compared for their associated risk of transmission of ISA based on an assumption that best practice is followed, i.e. risk reduction measures are employed, for all the harvest methods described. Recommendations are made to reduce the likelihood of ISA transmission associated with harvesting. These recommendations will also be effective in reducing transmission of other fish diseases.
2. Materials and methods 2.1. Risk assessment This paper will assess the risks of ISA being spread by eight harvest methods. An assessment of the consequences of ISA will not be considered. The harvest operations were ranked according to the probability of transmission of ISAV. For each harvest operation the risks of transmission to farms in the vicinity of the harvested farm, farms en route between the harvested farm and the processing plant, and in the vicinity of the processing plant are considered. The possibility of a harvesting station near the processing plant becoming a source of infection and re-broadcasting the infection is assessed. An outbreak of ISA at a harvest station is important since it may result in widespread transmission [13]. We also assess the risk of mechanical transmission between farms.
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The Joint Government/Industry Working Group on ISA, whose membership comprised representatives from the Scottish Executive Environment and Rural Affairs Department, Fisheries Research Services (FRS), the State Veterinary Service, the Scottish Environment Protection Agency and the Scottish trout and salmon farming industries, concluded that one of the major risks associated with harvesting was environmental contamination with blood and other processing waste. They recommended that blood water effluent from salmon processing plants should be disinfected before discharge and other processing waste should be ensiled [14]. For the purposes of this risk assessment, the assumption was made that risk reduction measures are employed where possible. For example, it was assumed that blood is contained during all harvesting methods that involve slaughter at sea and blood water from the processing plant is disinfected in all cases. It was also assumed that vessels used to transport live fish for harvest, such as well-boats, operate with the valves closed to prevent water exchange in the vicinity of fish farms other than the farm where the fish are uploaded. Currently, the FRS Fish Health Inspectorate monitors compliance with the recommendations of the Joint Government/Industry Working Group on ISA during routine inspections of fish farms throughout Scotland. Although every harvesting operation cannot be inspected, compliance to date has been high.
2.2. Harvesting methods The harvest methods assessed (Figs. 1a and b) were: Slaughter on site M1 Fish killed and bled into the wells of a well-boat then transported by sea direct to the processing plant. M2 Fish killed and bled into the wells of a well-boat then transported to a local pier for transfer into a tanker or harvest tubs for onward transport to the processing plant by road. M3 Fish killed and bled into harvest tubs onboard a boat then transported to a local pier where the tubs are transferred onto a vehicle for onward transport by road to the processing plant. M4 Fish killed and bled into harvest tubs onboard a harvesting barge, transferred to a boat and transported to a local pier before transfer onto a vehicle for onward transport by road to the processing plant. M5 Fish killed and bled into harvest tubs on a boat then transferred by sea to a processing plant. Slaughter at a killing station at or near a processing plant M6 Live fish transported by well-boat direct to a processing plant and killed and bled within the plant. M7 Live fish transported by well-boat to a harvest station (cages situated near a processing plant). M8 Live fish in cages towed to a harvest station near a processing plant.
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Fig. 1. (a) Harvest methods involving the transport of dead fish. (b) Harvest methods involving the transport of live fish.
3. Results 3.1. Hazard ID This paper refers to the risk of ISAV transmission from harvesting techniques, however, many of the conclusions will be applicable to other diseases.
3.2. Release assessment Harvesting methods may result in the release of ISAV through four main pathways: 1, escape of live fish; 2, loss of dead fish; 3, discharge of blood, effluent and ballast water and 4, mechanical transmission. The harvesting methods pertinent to each pathway are summarised in Table 1. Three categories of farms may be affected: A, farms neighbouring the farm where the salmon are harvested; B, farms en route to the harvesting station or processing plant and C, farms neighbouring the harvesting station or processing plant (Fig. 2). It was assumed that when fish were transferred from a boat to a lorry the transfer took place at a pier local to the farm. A detailed list of the risks posed by each method is given in Appendix A.
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Table 1 Summary of biological routes of transmission by harvest method Routes of transmission
Harvest methods
A. Transmission to neighbouring farms Escape of live fish Loss of dead fish Discharge of blood, effluent
M1–8 M1–5 M1–5
B. Transmission to farms en route to pier/harvest station/processing plant Escape of live fish Loss of dead fish Discharge of blood effluent or ballast water
M6–8 M1–5 M1–8
C. Transmission to farms neighbouring pier/harvest station/processing plant Escape of live fish Loss of dead fish Discharge of blood, effluent or ballast water
M6–8 M1–5 M1–7
D. Mechanical transmission Divers removing morts before harvest moving between farms Shared harvesting equipment Well-boats moving between farms Shared staff moving between farms
M1–8 M1–5 M1, 2, 6, 7, 8 M1–8
Fig. 2. Map illustrating: (A) farms neighbouring the salmon farm being harvested, (B) farms en route to the harvest station or processing plant and (C) farms neighbouring the harvesting station or processing plant.
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3.3. Exposure assessment An outbreak of ISA will only occur if the ISAV which has been released into the aquatic environment comes into contact with and infects a susceptible host(s), and that infected individual(s) infects more than one other individual (basic rate of reproduction (R0 ) greater than one [15]). The escape of live salmon is considerably more likely to result in ISAV transmission to other fish farms compared with the loss of dead salmon. The behaviour of escaped salmon is likely to depend on their development stage. For example, grilse may head for fresh water. Escaped salmon may be attracted to fish farms in search of food. Although salmon clinically infected with ISAV may not travel far, sub-clinically infected individuals may survive a considerable length of time and travel some distance. The loss of an infected dead salmon will only result in ISA becoming established if a susceptible fish is exposed to a sufficient viral dose to cause infection. Hence, the loss of a few dead salmon when loading or unloading is unlikely to result in a disease outbreak. The release of blood, effluent or ballast water will only result in disease transmission if the viral load is sufficient to infect susceptible fish. Continual high volume effluent discharge from a processing plant poses an important risk; however, small spillages of blood or effluent from on farm killing, or when loading or unloading, may be less likely to cause ISAV transmission. The mechanical transmission of ISAV is possible since the virus will survive in seawater at pH 7.2 at 10 C for more than 24 h [16].
3.4. Ranking The ranking of the harvesting methods according to the likelihood of transmission to the three categories of farms is summarised in Table 2.
Table 2 Ranking of risk of ISAV transmission by harvesting method Probability of disease transmission
High
Low
Risk of ISAV transmission to Neighbouring farms
Farms en route to processing plant
Farms in vicinity of processing plant
M8 M2 M4 M3 M5 M1 M6,7
M8 M6, 7 (bad weather) M5 M6, 7 (good weather) M1 M2,3,4
M7 M8 M1 M5 M6 M2,3,4
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3.4.1. Transmission to neighbouring farms For methods M2–M4, the pier where fish are unloaded is considered local to the farm and the risks of transport to the pier are considered as risks to farms neighbouring the harvested farm. All harvest methods may result in the loss of live fish into the aquatic environment. If the fish are killed at the farm of origin (methods M1–M5) then it is possible that occasionally a fish will escape from the killing table. For methods M6–M8, a low possibility exists for fish to escape whilst being loaded into well-boats or tubs. A high risk of spreading infection in the vicinity of the farm is associated with towing cages, which has a high risk of allowing escapes from torn nets (method M8). Low risks are also associated with the possible accidental discharge of blood or effluent when fish are killed at the farm of origin (methods M1–M5) and again at transfer at a local pier (methods M2–M4). Overall, the transport of live fish directly to the processing plant by boat (methods M6 and M7) poses few risks to local farms. 3.4.2. Transmission to farms en route to the processing plant The escape of live fish en route to the processing plant or harvest station is only possible for methods M6–M8, and under normal circumstances the possibility is diminishingly small except for method M8, which carries a high risk of escape from torn nets. In practice, method M8 would only be applied within the vicinity of the processing plant, i.e. over short distances. In the case of mechanical failure of a wellboat the fish would have to be transferred to another vessel which would increase the risk of escape. Loss of dead fish en route to the processing plant (methods M1 and M5) is unlikely, although road accidents leading to the spillage of full harvest tubs have been known. There is a risk that lorries transporting dead fish from the pier to the processing plant may leak ISAV contaminated water. The probability that this will result in ISAV being introduced into the aquatic environment is considered remote, particularly if sealed harvest bins in good condition are used. Adverse weather conditions will increase the risk of transmission of disease to farms en route to the processing plant for methods M6 and M7 because the well-boat may have to shelter near the coast in relatively close proximity to fish farms. The longer the bad weather persists, the greater the likelihood that the valves will be opened for water exchange in order to keep the fish alive and, thus, the greater the risk of disease transmission to farms in the area. New well-boat designs with chilled, recirculated water facilities, which would eliminate the risk of release of contaminated water, are under trial elsewhere but this technology is not yet available in Scotland. Although improbable, in extremely severe weather conditions the entire cargo may be lost. 3.4.3. Transmission to farms near the processing plant and harvest station Live fish may also escape during unloading at the processing plant but the probability is low. Loss of live fish from the harvest station is more likely (methods M7 and M8), since fish may be kept there for some time and the cages may be damaged in bad weather or from attacks by seals or vandals.
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The frequency of well-boat movements and potential for fish from multiple sources to be transported to the harvest station cages increases the risk of ISAV transmission to farms near a harvesting station (methods M7 and M8). The stress of transport may increase susceptibility to infection and induce pathogen shedding in subclinically affected individuals or result in clinical disease. The risk of disease transmission to neighbouring farms will increase with the period fish spend in the harvest station cages. Cages are also held near the processing plant under method M8, but the fish in the cages are from only one source and are usually held for a relatively short period. The risk of infection of farms near a processing plant associated with methods M2–M4 is deemed to be very low since these methods involve road transport to the plant. 3.4.4. Risk of rebroadcast infection from the processing plant Processing plants may act as sources of infection, particularly when a harvest station is associated with the plant. Harvest stations are potential reservoirs of infection, since fish from different farms are in close proximity and the stress of transport will increase the risk of virus shedding. The fish may also be exposed to pathogens in the effluent discharged from a processing plant, even if the discharge is disinfected [9]. When fish are unloaded from well-boats at a processing plant or harvest station, ballast water is taken, which is then be discharged when a new harvest is loaded. If there is ISAV present in the environment it may be transported. A low risk of disease transmission is associated with each journey but the very large number of harvesting vessels visiting a busy processing plant means that is a potentially important source of transmission. These risks only apply to methods M7 and M8, and M1, M5 and M6 if a harvest station is located at the processing plant. Transmission of disease via harvest tubs is also possible. 3.4.5. Risk associated with contaminated equipment Divers may be used to remove morts before any of the harvesting methods are used. Poor disinfection of diving suits and equipment may result in transfer of ISAV to other farms visited by the diver. More equipment and personnel are involved in methods M1–M5, compared with M6–M8. Again, if the equipment and personnel move to another farm without strict attention to disinfection, ISAV may be transmitted. There are detailed guidelines for well-boat disinfection and inspection [17]. If these guidelines are not followed then the movement of well-boats between farms may result in disease transmission. Well-boats are relatively difficult to disinfect due to their size and limited accessibility or number of inspection hatches associated with the fish pumps. It is possible for dead fish to be left in the pumps. Harvest barges are also difficult to disinfect due to their size but, given the high number of well-boat movements between farms, the risk of disease transmission if a well-boat is not disinfected effectively is relatively high. The risks associated with mechanical transmission by different pieces of equipment used in harvesting fish are ranked in Table 3.
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Table 3 Ranking of equipment used in harvesting fish according to the risk of transmitting ISA Probability
Equipment
High Well-boat Harvest barge Grading equipment Killing tables Harvest tubs Site boat Personnel Vehicles Low
Disinfection reduces the risk associated with equipment but does not necessarily eliminate it. If the concentration of disinfectant used is incorrect or the contact time is insufficient some virus particles may not be inactivated. Similarly, virus particles may remain active if they are harboured in tissue or detritus and, therefore, not accessible to the disinfectant.
4. Discussion A range of different harvesting methods were assessed for the risk of transmission of disease to neighbouring farms, farms en route to the processing plant and farms in the vicinity of the processing plant. It was not possible to quantify the level of risk associated with each activity due to the limited amount of data available. Instead, the methods were compared against each other. Because risk factors depend upon the nature of the environment it is quite possible that the lowest risk will apply to different methods for different farms and that lowest risk can vary with time depending upon weather episodes, season or inter-annual climate variation. Overall, harvesting fish poses the greatest risk of ISA transmission to farms in the vicinity of the processing plant; the risk to farms in the vicinity of the harvested farm is lower, but still significant. The increased risk of ISA is lowest for farms en route to the processing plant. 4.1. Risk to farms in the vicinity of a harvested farm It has been shown in Norway that the risk of ISA increases for farms within 5 km of an infected farm, compared with more distant farms [9]. The risk has also been found to increase with the number of ISA-infected neighbouring farms [18]. If the farm is infected then harvesting methods where fish are killed on site (methods M1–M5) will result in an increased risk of transmission. Slaughter on site may result
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in blood spillage, escape of fish from the killing table and movement of contaminated equipment to other farms. These are significant risks that are not associated with the movement of live fish. The risks to local farms will be increased by spillage of blood or dead fish during the transfer at a local pier (methods M2–M4).
4.2. Risks to farms en route to a processing plant Overall the risk to farms en route to a processing plant is small assuming risk mitigating factors are employed, except where fish are transported in cages. When fish are transported by other means, a significant risk only occurs in bad weather when well-boats carrying live fish may have to take shelter on route to the processing plant and open the valves to ensure the fish are kept alive.
4.3. Risks to farms in the vicinity of a processing plant It has been found in Norway that farms within 5 km of a processing plant had an increased risk of ISA, compared with farms more distant; even when the effluent from the processing plant was disinfected [9]. Similarly, the number of processing plants near a farm was positively associated with the risk of ISA [18]. The risk of disease transmission to farms in the vicinity of the processing plant is from effluent discharge, or disease in the fish kept at the harvest station. By comparison, the disease risk directly resulting from the harvesting methods, i.e. risks associated with unloading, is very low. The Norwegian studies [9,18] indicated that ISAV can survive outside the host for a considerable length of time and be transmitted considerable distances in seawater. This suggests that untreated blood and effluent from on site killing and processing plants pose a real risk of disease transmission. Fish kept at a harvest station are highly likely to become infected in the event of an ISA outbreak since they originate from a number of sources, they are stressed and thus predisposed to infection and more likely to shed ISAV. They are also likely to be infected from contaminated effluent from the neighbouring processing plant. Harvesting stations, therefore, pose a very serious threat to neighbouring farms. If ISAV becomes established at a harvesting station, well-boat movements could spread the virus to many farms, as occurred in Scotland in 1998 [13]. Although the risk per journey is probably small, the large number of vessels leaving a processing plant and the wide area that they cover makes this a serious risk for ISA spread. At the time of the ISA outbreak in Scotland, the effluent from a processing plant situated near the harvest station, from which many well-boat movements occurred, was not disinfected prior to discharge. ISAV could have been spread by well-boats taking up water contaminated by effluent directly from the plant. In addition, infection could have been maintained in fish exposed to contaminated effluent in the holding cages at the harvest station resulting in additional shedding of ISAV. Disinfection of the processing plant effluent would have reduced both these risks and could potentially have prevented the spread of ISA to other farms.
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4.4. Mechanical transmission Studies from Norway and Canada which have investigated risk factors for ISA [9,18,19] confirm that mechanical transmission is an important source of spread. Shared personnel [18], the movement of boats between farms [19] and divers were shown to be risk factors. Well-boats delivering fish to a processing plant with a harvest station were implicated in the last outbreak of ISA in Scotland [13].
5. Conclusions The most serious risks of ISA transmission associated with harvesting are associated with holding live fish in cages, known as harvest stations, adjacent to processing plants and the discharge of untreated effluent from processing plants. It is recommended that holding live fish in harvest stations near the processing plant is phased out. Meanwhile, fish in such holding cages should be regularly monitored for clinical signs of disease to ensure rapid detection and the residence time in the cages should be kept as short as possible. Effluent from processing plants should be treated to inactivate ISAV and other pathogens. This measure has been effective in reducing the number of ISA outbreaks in Norway. In general, if well-boats operate with their values closed to prevent water exchange in the vicinity of fish farms and the recommended disinfection and ballast discharge procedures are followed, large shipments of live fish in well-boats directly to a processing plant is a safe method of harvesting. It is suggested that the operation of well-boats is investigated. It is important to establish how frequently they operate with the values open and whether disinfection and ballast discharge recommendations are followed. A maximum journey time may be required to be specified to ensure that the boats operate with the values closed. The harvesting method which is most likely to spread ISA is method M8, towing cages of live fish to a harvesting station at processing plant. Cages are only likely to be towed to a harvest station if the distance between the farm and the harvest station is relatively short. It is recommended that this harvesting method be discontinued. There is a real risk of mechanical spread of ISAV between farms. Efforts should be made to make farmers aware of the biosecurity measures that are required to minimise the risk of ISAV spread. A list of mitigating factors for the transmission of ISA by harvesting methods is presented in Appendix B. A more accurate assessment of the risks associated with harvesting can be achieved by taking a more quantitative approach (see Appendix C). The numbers of farms in each of the three categories considered could be calculated. Generally, the risk of transmission will be positively associated with the number of movements of harvested fish. Occasional large shipments probably pose less risk than more frequent shipments of smaller volume. Data could be obtained on the volumes of fish moved by different methods. Absolute risks for each harvesting method cannot realistically be estimated; however, scoring the risks would enable an overall ranking to be obtained. The following areas need to be investigated in order to generate the
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data needed for a better evaluation of the risk of ISAV transmission: dose required to cause infection, the epidemiological importance of the carrier state, the viral load in the tissues of an infected individual, survival of ISAV outside of the host under various conditions. A more complete list of data required for quantitative risk analysis is presented in Appendix C. The release assessment for ISAV will be largely applicable for other salmon pathogens. The exposure assessment depends to a greater extent on the characteristics of the pathogen, i.e. survival in the aquatic environment, required infective dose, etc. For example, infectious pancreatic necrosis (IPN) virus is more robust and has more known carrier species than ISAV, as a result IPN is more likely to be spread through the environment and the relative role of the factors discussed here is less than for ISA. Overall, however, the recommendations made in this report will also be effective at reducing the transmission of other fish pathogens. Appendix A. Risk factors The risk factors associated with each of the harvesting methods described above are listed below. They are not ranked in any order. Method M1: dead fish in well-boat direct to processing plant * * * * *
* * * *
Blood spillage at point of slaughter Fish escapes from killing table Possible blood loss if valves are opened accidentally or otherwise Adverse weather conditions could lead to catastrophic loss if shipwreck occurs Mechanical failure of well-boat engine could lead to increased risk associated with transfer of fish at sea or catastrophic loss Blood spillage at pier while pumping fish into processing plant Dead fish may be left in pumps Inadequate disinfection of blood residue in wells before disposal Inadequate disinfection of well-boats between operations on different sites. Method M2: dead fish in well-boat to local pier
* * * * *
* *
* * *
Blood spillage at point of slaughter Fish escapes from killing table Possible blood loss if valves are opened accidentally or otherwise Adverse weather conditions could lead to catastrophic loss if shipwreck occurs Mechanical failure of well-boat engine could lead to increased risk associated with transfer of fish at sea or catastrophic loss Blood spillage at pier while transferring fish to tanker/harvest tubs Loss of harvest tubs during transport by road, which could be a disease risk for watercourses Tanker/harvest tubs must be disinfected after use Cross contamination of clean and dirty tubs Inadequate disinfection of vehicles used to transport harvest tubs.
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Method M3: dead fish in harvest tubs to local pier * * * * * * * * * * *
Blood spillage at point of slaughter Fish escapes from killing table Accidental loss from tub due to tipping Bad weather increases risk of loss Tubs must not be cracked or overfilled Lower capacity than well-boat leads to more frequent trips Harvest tubs must be disinfected properly Tubs could fall during transfer at the pier or during transport by road Blood leakage during road transport Tub liners pose disposal problem Frequent movements by road. Method M4: harvest tubs on barge transferred by sea to local pier
* *
As Method M3 but increased number of tub transfers increases risk Barge difficult to disinfect, should be site specific or limited to a management area at least. Method M5: harvest tubs direct to processing plant by sea
* * * * * * * * *
Blood spillage at point of slaughter Fish escapes from killing table Tendency to overfill tubs, resulting in spillage of blood and effluent Increased risk of fish loss if harvest tub falls Bad weather increases risk of loss Tubs must not be cracked or overfilled Lower capacity than well-boat leads to more frequent trips Harvest tubs must be disinfected properly Tubs could fall during transfer at the pier. Method M6: live fish in well-boat direct to processing plant
* * *
*
* *
*
Fish escapes during uplift from cages Bad weather could cause catastrophic loss or disposal problem if fish die on route Potential for disease transmission if valves are opened accidentally or otherwise, increases with distance from processing plant and in adverse weather conditions Mechanical failure of well-boat engine could lead to increased risk associated with transfer of fish at sea or catastrophic loss Risk of fish escape during transfer to killing station Transfer water must be returned to site of origin or disinfected before discharge, if free of blood, effluent or fish material. Pumps and wells must be inspected for the presence of fish/organic material and disinfected.
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Method M7: live fish in well-boat to cages at processing plant *
* * *
As method M6 except increased risk of waterborne pathogen transfer to farms in the region of the processing plant Risk of stress-induced disease Fish from multiple origins increases likelihood of disease Fish could act as reservoir for pathogens in processing plant effluent or escapes, which may for a focal point for widespread infection. Method M8: live fish towed in cages to processing plant
* *
*
*
Risk of fish escapes increases in adverse weather conditions Fish escapes possible if net snags on sea bed or in general movement or slaughter operations. Fish could act as reservoir for pathogens in processing plant effluent or escapes, which may for a focal point for widespread infection Risk of stress-induced disease.
Appendix B. Mitigating factors The risks associated with any harvesting method can be reduced by implementing risk reduction measures. Examples of risk reduction measures for each of the harvest methods are described below. Method M1: dead fish in well-boat direct to processing plant * *
* * * * * * * * * *
High sides on killing table and nets on deck to reduce potential for escapes Tarpaulin under killing table to contain blood spillage, check to ensure fish cannot escape from the vessel when tarpaulin is in place. Disinfectant on board to treat blood spillages and disinfect equipment Harvest in good weather conditions Ensure sufficient time for the movement Ensure valves are kept closed on route to processing plant Carry out regular maintenance to reduce risk of breakdown Disinfect residual blood in wells Disinfected wells between trips Conduct regular pipe inspections Tarpaulin underneath transfer pipe to catch fish or blood if the pipe bursts Inspection hatches to fish pumps to ensure all fish removed. Method M2: dead fish in well-boat to local pier
* *
As method M1 but in addition tanker or harvest tubs must be properly disinfected Disinfectant required at transfer point to treat blood spillages
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Dedicated tanker required, not visiting fish farms Any residual discharges should be properly treated Use only experienced staff particularly fork lift operator. Method M3: dead fish in harvest tubs to local pier
* * * * * * * * * * *
High sides on killing table and nets on deck to reduce potential for escapes Tarpaulin under killing table to contain blood spillage Disinfectant on board to treat blood spillages and disinfect equipment Harvest in good weather conditions Check harvest tubs for cracks regularly, replace damaged tubs Use sealed harvest tub liners and do not overfill tubs Use tubs with close-fitting lids and securing straps and should not be overfilled Blood and effluent should be held in separate tubs and treated prior to disposal Use dedicated vehicles or disinfected vehicles, including wheels, between trips Vehicle should carry disinfectant to treat spillages Vehicles should travel safely using an agreed route. Method M4: harvest tubs on barge transferred by sea to local pier
*
*
As method M3 but, in addition, harvest barge should be dedicated to one site or one management area Disinfectant should be available on board the harvest barge to deal with blood spillages. Method M5: harvest tubs direct to processing plant by sea
*
As method M3. Method M6: live fish in well-boat direct to processing plant
* * * * *
* * * *
Harvest in good weather conditions Carry out regular maintenance to reduce risk of breakdown Ensure valves remain closed on route to processing plant Do not over stock wells Ensure distance to processing plant does not exceed capacity to keep fish alive without opening valves, ensure adequate time for movement. Only transfer healthy fish Route well-boat to avoid fish farms. Have oxygen supply available to extend holding period if necessary Residual discharges from the vessel should be properly disinfected. Method M7: live fish in well-boat to cages at processing plant
*
As method M6 but, in addition, minimise residence time in cages at harvesting station
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Carry out regular net inspections to prevent escapes Only transport apparently healthy fish Remove damaged/dead fishes immediately. Method M8: live fish towed in cages to processing plant
* * * * * * *
Only ever tow cages in good weather conditions Tow cages slowly with the tide Carry out regular net inspections Clean and disinfect nets afterwards Use experienced personnel only who know the sea bed in the area Tow only healthy fish Remove damaged/dead fish immediately.
Appendix C. Data required for quantitative evaluation of risks We have only attempted to provide a qualitative assessment of the relative risks. To analyse risks in a quantitative manner would require far more data than is available. Some data is available from Norway on the processes that favour transmission of ISAV and data from Scotland was used to assess the role of wellboats in transfer of the pathogen [13]. However, practices are being constantly evolved and hopefully improved, so historical risks may not be a guide to the current situation. Risks must be assessed for discharge of waste, escaped fish, management failures and the extent of shipping associated with harvesting operation. Dead fish and waste risks * * *
*
Viral Titre and Survival Times in discharges of blood, tissue and dead fish Probabilities of release of blood, tissue or dead fish during harvest Probabilities of release of blood, tissue or dead fish during loading/unloading operations at the farm, at the pier or processing plant, or during emergency unloading operation at sea and depending upon whether tubs or well-boats are used to transport the fish Numbers of farms within areas into which blood, tissue or dead fish will disperse in a given period, or within 1, 2 and 5 km radii if detailed analysis of local currents is impractical. Escaped fish risks
* *
* * *
Period of persistence of virus in escaped fish so they act as source of virus Behaviour of escaped fish, do they remain near site of escape, disperse out to sea or move to the vicinity of other fish farms Probability and numbers of escapes during harvesting operations Probability and numbers of escapes during loading/unloading of live fish Probability and numbers of escapes during towing of cages.
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Poor management risks *
*
* * * *
* * *
Probability of virus survival in inadequately disinfected tubs or holds or on shared equipment Probability that disinfection or inspection processes for equipment or ships are inadequate Extent to which equipment is shared between farms or site dedicated Probability valves are opened during transport Probability of breakdown of ships or road vehicles Frequency with which farms are inspected for pathogens and in particular any fish held near processing plants are inspected Frequency with which dead fish are removed from cages Degree of stress or overcrowding in cages Adequacy of disinfection of slaughter and processing effluent Shipping data
* * *
*
Source, destination and routes of movements of ships with respect to farms Numbers of harvest visits required by a site Frequency with which ships seek shelter on route and locations where shelter is available, with the numbers of farms in the vicinity of these locations Weather conditions along the route.
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