The impact of farm gate biosecurity on the transmission of FMD in UK in 2001

Transcription

1 Appendix 3 The impact of farm gate biosecurity on the transmission of FMD in UK in 2001 Introduction: Nick Honhold FAO Ankara, Birlik Mah. 2 Cad No. 11, Cankaya, Ankara, Turkey Nick.Honhold@fao.org Culling and vaccination of susceptible animals are well established methods for the control of spread of FMD. In recent years, the concept of biosecurity as a part of disease control has also been emphasised. However, there is no accepted definition of the term biosecurity. FAO (2005) has a broad but general definition of biosecurity that focuses on policy and regulatory frameworks and includes animal and plant health and the preservation of the environment and biodiversity. Wikipedia (2006), the online encyclopaedia, lists several definitions dating from The USDA focuses on the prevention of bioterrorism in the information in their recently produced biosecurity advisory leaflet (USDA 2006), although other USDA sites for avian influenza focus more on the prevention of fomite and personnel transmission of viruses to farms (Aphis 2004a, 2004b). An on-line newsletter for farmers in Massachusetts USA from 2001 defines biosecurity as the practical steps taken to reduce the risk of spreading infectious and contagious disease. (Massachusetts Department of Food and Agriculture, 2001). The New Zealand government has a broader definition of biosecurity, including controls on imports, surveillance and disease control measures of all kinds under their definition of the subject (Biosecurity New Zealand, 2006). Defra in the UK focus mostly on the prevention of fomite and personnel spread of disease in their biosecurity advice to farmers, although they also mention the potential spread by purchasing animals (Defra, 2006). One can therefore pretty much decide to focus on biosecurity at any level from cleansing and disinfection at the farm gate to controls on the international trade in live animals and animal products, or any combination of the stages between these two. In the context of livestock disease, biosecurity can be broken down into three main components: Prevent entry / spread Risk assessment of trade commodities International border controls National/zonal internal movement controls Compartmentalisation Farm gate controls (includes dairies, feed mills etc) Find the disease quickly Surveillance Reporting Investigation of possible sources and spread Veterinary risk assessment of in contact premises Extinguish it quickly Culling of susceptible stock on infected premises Culling of susceptible stock on premises vet assessed as at high risk Vaccination However, it is a given fact that in a disease outbreak, measures will be in place to control movements of live animals and animal products. Equally, disease surveillance and reporting will be strengthened to shorten report times and resources will be made available to cull infected and high risk in contact susceptible livestock as rapidly as possible. The remaining element of biosecurity is the prevention of spread by people and fomites by measures taken at the farm gate. For the purposes of this paper, the definition of biosecurity is limited to the pre-emptive measures taken to prevent the spread of a pathogen from an infected premises to an uninfected premises via fomites including vehicles and personnel on premises that are not known to be infected i.e. it is pre-emptive and pro-active biosecurity rather than reactive. 26

2 Just how important is it to have good farm gate biosecurity and what does good mean? Although fomite spread is accepted to occur and to be important, this is based on field evidence in which all other possible routes are excluded i.e. that it must have occurred. There has been experimental work that has shown the potential for fomite spread of porcine respiratory and reproductive syndrome (Amass et al., Dee et al., Dee et al, Otake et al, 2002), both via immediate contact and via a sequence of events, but only one equivalent study exists for FMDV (Amass et al, 2002). But there are only a few papers and whilst showing fomite spread can occur, the work does not quantify how much spread could be prevented by biosecurity. In the epidemic, the overall risk of infection of contiguous premises (CPs) i.e. premises with shared boundaries with an infected premise (IP) was 17% (House Of Commons Select Committee On Environment, Food And Rural Affairs, 2002). However, this figure does not differentiate between the routes of infection. In general, the risk of infection can divided into two main routes, direct and indirect. Direct spread is when susceptible animals become infected from contact with infected animals by close contact including short distance aerosol spread. Indirect spread is when the infectious agent is transferred from an infected animal to an a susceptible animal via an object that acts as a mechanical vector i.e. fomites including vehicles personnel. There are other forms of spread, such as long distance wind borne spread and spread via biological vectors, but these played no significant role in the 2001 FMD outbreak in the UK. Donaldson et al (2001) showed that for the virus type responsible, spread over more than a few 10s of metres required there to be substantial numbers of infected animals shedding virus at the same time. FMD has no significant biological vectors in the UK. The risk of infection can be summed up: Overall risk of infection = Direct risk + Indirect risk Direct risk is not typically susceptible to farm gate biosecurity measures, but indirect risk is. But how much spread of FMD in 2001 was due direct and how much due to indirect risk? How much impact can be expected from strengthened farm gate biosecurity? Methods: Figure 1 a shows the locations of the major clusters of infected premises (IPs) in Cumbria in Detailed records of livestock locations on infected premises (IPs) and all contiguous premises (CPs) were available for Cumbria from 01-May-01 to 30-Sep-01. This allowed the measurement of distances between stock on IPs and on CPs from field boundary to field boundary to assess the closest distance between stock in the infectious period. If this was 50m or less, stock on the CP were automatically culled. If it was over 50m, stock could not be culled unless there was known evidence of other contact with any other IP through indirect routes i.e. fomites or personnel. Details of the methods used are given in Honhold et al. (2004b). The majority of the IPs in this period were in the area know as the south Penrith spur. 27

3 Fig 1. Maps showing the location of (a) the main clusters of IPs in Cumbria and (b) the location of IPs in GB and the three major clusters of IPs in England in 2001 a) Major clusters of IPs in Cumbria in 2001 b) Location of IPs in GB during 2001 showing the location of the three main clusters analysed Adapted from Taylor et al., 2004 From Honhold et al., 2004a One key concept used in the analysis is that of the temporal risk window. This is the period during which if a CP became an infected premises, it could be considered as possibly having been infected from the neighbouring IP. It was calculated using the estimated first lesion date on the IP and the known period of virus shedding before this date combined with the known range of incubation periods for the virus. An IP was assumed to cease to be a source of virus (at least by the direct infection route) on the day that slaughter of susceptible stock was completed. This concept is described in more detail in Taylor et al (2004) and is shown diagrammatically in figure 2. This window was calculated for each IP and was used to determine whether a CP later found to be an IP might have been infected from a previous neighbouring IP. This was then combined with known distance between stock and the numbers of CPs that became an IP during the risk window to give an infection rate between IP and CPs for increasing distances between stock. This gives an indication of the route of infection (direct vs. indirect). 28

4 Fig 2: Diagrammatic representation of the calculation of the risk window for infection to have spread from an IP to other premises virus shedding Da y FL SL SL min.in maximum incubation period c. temporal risk window of IP IP is considered a possible source of infection for any cases with first lesion dates in this window Key: FL marks the day of first lesions; SL marks the day of completion of slaughter; min.inc. is the minimum incubation period. The figure exemplifies an IP with first lesions occurring on the first day of a month, and slaughtered 3 days later on the fourth day of the month, which therefore gives a risk window from the second to the 18 th day of the month inclusive (17 days). (From Taylor et al., 2004) This data has been combined with data from other sources (House Of Commons Select Committee On Environment, Food And Rural Affairs, Taylor et al., 2004) to estimate what proportion of CPs were infected through the indirect and direct routes. An additional calculation has been made using data from Taylor et al. (2004) to give an overall estimate of what proportion of IPs in Cumbria were infected via the direct and indirect routes. The largest cluster in GB during 2001was in Cumbria (892 IPs). This is shown in Fig 1b along with the two other largest clusters in England. Data from Cumbria has been analysed in order to determine the proportion of IPs that had a possible source IP within 1.5km, which will include most CPs. Details of this analysis are given in Taylor et al., Combining this with the data from Honhold et al (2004b) allows an estimation of the overall proportion of IPs infected via the direct and indirect routes. The relationships between the progress of the epidemic and the application of control measures have been analysed for the three English clusters. Details of this analysis are given in Honhold et al 2004a. The progress of the epidemic in the Cumbria cluster was assessed using the estimated dissemination rate (EDR) which is calculated as shown below. Estimated Dissemination Rate (EDR) Number of IPs by date of first lesion in a 7 day period Number of IPs by date of first lesion in previous 7 days Speed slaughter is known to be important in controlling disease and this was assessed using the time from date of estimated first lesion to end of slaughter. An average value was calculated for all IPs with a first lesion date in a given seven day period; this was designated as first lesion to slaughter (FLtoS). First lesion to slaughter (FLtoS) Sum of days from first lesion to slaughter Number of premises with first lesion These values have been calculated for each outbreak and plotted on a weekly basis for the Cumbrian outbreak. The results from the two sets of analysis have been combined to calculate the potential contribution of biosecurity to the control of disease over a range of values of EDR and the proportion of disease that is spread by the indirect route as compared to the direct route. Results: Between 01-May-01 and 30-Sep-01, there were 192 IPs in Cumbria, mostly in the south Penrith spur. These led to the assessment of 586 stocked contiguous parcels of land. 275 were subject to a complete depopulation of susceptible livestock. The remaining 311 on which all or some susceptible stock remained have been used in the subsequent analysis of the risk of disease transmission during the temporal risk window. The results are shown in Table 1. 29

5 There is no distance related trend in the percentage of CPs that became IPs within the temporal risk window, with the proportion being approximately the same for distances <50m and >500m. Overall, the percentage that became IPs during the temporal risk window was 11.9%. Table 1 No of assessments in Cumbria between 01-May-06 and 30-Sep-06 where stock were spared and number that became an IP within the temporal risk window, by separation distance between contiguous stock Minimum distance between stock on IP and CP (m) No. of assessments No. becoming IP in temporal risk window % becoming IP in temporal risk window < % % % > % TOTAL % The overall risk of a CP becoming an IP during the epidemic was reported to be 17%, a figure confirmed by Taylor et al. (2004). If the risk via the indirect route was 12%, then the risk via the direct route will have been 5% i.e. around two thirds of the risk to CPs was indirect. Taylor et al (2004), using a distance between premises of 1.5km or less as a surrogate for contiguity, found that the risk of becoming an IP due to being within that proximity of a possible source of disease was around 55% in the south Penrith spur. This implies that 45% of all IPs had no possible source within 1.5km, i.e. that they must have been infected by the indirect route. The two sets of results refer to the same set of IPs and can be combined to give an overall figure for the proportion of IPs infected via the indirect route of 84%, or around 4 out of 5 IPs. In North Cumbria (where there was little or no CP culling), 40% of IPs had no possible source within 1.5km. This gives and overall figure of 82% of IPs having been infected through the gate i.e. very similar to the figure for north Cumbria. If indirect infection through the gate is the commonest route of spread, even for CPs, how effective does farm gate biosecurity need to be for an outbreak to be controlled? This will depend on the EDR and the proportion of spread via the indirect route. Table 2 shows the range of EDR and FLtoS for the Cumbrian, SouthWest and Settle outbreaks in Table 2 Statistics of EDR and days from first lesion to slaughter for three clusters in GB in 2001 Parameter Cluster n Minimum Median Maximum EDR Cumbria South-West Settle FLtoS Cumbria South-West Settle The initial level of EDR was around 3 with an FLtoS of almost 8 days in both the Cumbrian and SouthWest clusters. Both of these clusters commenced in the early part of the epidemic (late February 2001); whilst there was some farm gate biosecurity at this stage, it was minimal and there were significant delays in slaughtering livestock on IPs. The Settle cluster commenced later in the epidemic (May 2001) when biosecurity was better and policies had been modified to allow faster culling on IPs, so the maximum EDR and FLtoS were lower than in the other two clusters. A typical EDR at the start of an outbreak with relatively weak control measures was therefore around 3 and around 2 for a situation where procedures had been modified to give greater effectiveness. 30

6 Fig 3 shows the changes in EDR and FLtoS on a weekly basis for the duration of the outbreak in Cumbria. Fig 3: Progress of the epidemic and speed of slaughter in Cumbria in Enhanced biosecurity 3 6 EDR 2 4 FLtoS (days) Feb Mar Apr May Jun Jul Aug Sep Sep-01 Date EDR FLtoS In the early first phase, both EDR and FLtoS were initially high, but fell more or less consistently over the first 4-5 weeks. In the second phase of the Cumbrian outbreak, both EDR and FLtoS were relatively stable at around 1 and 3 respectively, but never consistently so. Indeed, FLtoS rose later in the epidemic to around 4, only falling again in the last weeks of the epidemic. Enhanced biosecurity measures were introduced on 07-Aug-06 over most of the epidemic area and amended on 26-Aug-06 to include the full area of active disease. It was in this third phase that the epidemic finally declined and was extinguished. The last case from which virus was isolated was reported on 14-Sep-06. This epidemic shows that even after control measures such as speed of culling and culling of dangerous contacts are tightened to their practical maximum, a lack of effective biosecurity still allows disease to persist, albeit at a lower level. Given the values of EDR and FLtoS seen in the three large clusters in England, how effective does biosecurity need to be to control an epidemic? Table 3 shows the impact of different levels of effectiveness of biosecurity for differing levels of EDR and proportions of IPs due to indirect spread. The table shows the expected impact for four levels of biosecurity, with 30%, 50%, 70% and 90% of possible indirect transmission events being prevented respectively. The cells highlighted in green show where the EDR might be reduced to 0.75 and those in yellow to between 0.76 and 1 by a given effectiveness of biosecurity. Given that a margin of safety is required, it is preferable to aim for an expected EDR that is not only slightly below 1. Table 3 shows that when the EDR is high, biosecurity alone cannot be adequate to halt the epidemic except at very, perhaps unfeasibly, high levels of efficacy. But at the lower EDRs, of the type seen during the latter stages of the epidemic in Cumbria, a 70% level of efficacy of biosecurity will stop sufficient indirect spread to bring the EDR reliably below 1. Discussion: The analysis in Cumbria showed that around 5% of CPs became IP due to direct spread from a neighbouring IP. Thrusfield et al (2004) found a similar finding, with 5-10% of CP premises becoming IPs dues to the proximity of livestock i.e. by direct transmission. The value of 5% was for probable transmission being via this route and 10% for probable and possible together. 31

7 The combination of the two sets of analysis from Cumbria (Taylor et al., Honhold et al., 2004b) that indicates that 80% of the IPs in the Cumbrian epidemic were infected via the indirect route i.e. through the farm gate, gives an insight into the importance of farm gate biosecurity in controlling an epidemic of FMD. Farm gate biosecurity has always been emphasised during FMD outbreaks, but the reality is that, unless it is policed, it is frequently lax, particularly when there is an urgency about the activities involved, such as silage making. Equally, with some movements on and off farms (such as milk tanker collections) taking place around the clock and without supervision by the farmer, applying farm gate biosecurity becomes a difficult task. How can anyone adequately cleanse and disinfect a milk tanker at the farm lane end in the dark? Even properly cleaning and disinfecting a lorry in daylight with a pressure washer and disinfectant takes a relatively long time and is hard to do completely. Fortunately, farm gate biosecurity does not have to be perfect, just good enough. How good is good enough varies with the EDR without effective biosecurity and how much spread is indirect. Nor are the effectiveness required of biosecurity and the effectiveness of other control measures independent of each other. If there is no spread, direct or indirect, then speed of slaughter doesn t matter. Table 3 The impact of different levels of effectiveness of biosecurity for differing levels of EDR and proportions of IPs due to indirect spread EDR without effective biosecurity % Spread indirect EDR Direct EDR Indirect Total EDR at different biosecurity effectiveness 30% 50% 70% 90% 3 80% % % % % % % % % % % % % % % % % % % % % % % % EDR between 0.76 and 1. EDR 0.75 But in many cases, speed of slaughter affects the amount of spread (viral load and time for spread to occur). It also affects how rigorous biosecurity needs to be, again because of viral load increasing over time. So, the two are interrelated: biosecurity buys time for slaughter to be completed and speed of slaughter buys biosecurity. In general, biosecurity should be such that it prevents around 70% of transmission events occurring. The present author also advocates that any 32

8 biosecurity system should have in place at least two processes on any potential fomite route that are capable of preventing spread if properly implemented. Two biosecurity processes that are each 50% effective will produce an overall effect of over 70%. This approach acknowledges that failures will occur in any biosecurity process. If two such processes are in place, a failure in one will, in most cases, be compensated for by the second being effective. The EDR at the start of early clusters (i.e. before animal movement controls had taken effect) was around 3. After movement controls had taken effect, but with substantial delays in slaughter, this fell to around 2. Once FLtoS was at or below 3.5 days, average EDR fell to below 1, but there was still variation around this average, leading to spread to new sparks of infection. Preventing this spread was only possible when biosecurity was enhanced. In practice it was not possible under the conditions prevailing in GB in 2001 to obtain consistently the speed of slaughter, accuracy of DC assessment or efficacy of biosecurity to control the epidemic on their own. The epidemic was only eradicated when all three were at a sufficiently high level that a failure of one process was compensated by the others. Control of FMD by stamping out is the ability to get several processes right over a sufficient period of time. Biosecurity is one of these processes. However, the figures given in this paper for efficacy of biosecurity and its impact are not meant to be taken as authoritative. They are the product of simple modelling and like all models, are only an approximation. We currently have little understanding of contact networks between farms. There have been a few studies published to date (e.g. Nielen et al., Sanson et al., 1993). More are now being conducted and it is hoped that this will lead to a greater understanding of how virus may spread via fomites and so help to improve biosecurity protocols to achieve high levels of efficacy. There are no data on how extensive biosecurity needs to be, the area that should be included in enhanced biosecurity measures. Taylor et al. (2004) reported that 14% of IPs in Cumbria had no source IP within 3km, suggesting that longer distance transmission is significant. But enhanced biosecurity within 3km of a known IP might be expected to decrease this figure. Whether this would be sufficient to prevent these sparks into uninfected areas is not known. However, biosecurity is cheap relative to the cost of controlling disease through culling of infected premises and the associated veterinary assessed dangerous contacts. In this situation, it would be justifiable under a precautionary principal, to extend enhanced biosecurity beyond the 3km protection zones and perhaps up to the boundary of the surveillance zone. The outbreak of FMD in Cumbria is regarded as having been severe, to have spread rapidly initially and to have had a prolonged tail. The present paper suggests that controlling such an outbreak in a shorter period needs a combination of a shortened time from first lesion to slaughter and biosecurity that is capable of preventing 70% of fomite transmission. Acknowledgements: The Veterinary Record gave permission for reproduction of results and figures from papers published in that journal. DEFRA funded some of the original analysis. The contributions of other authors of the papers cited from the field analysis of the 2001 outbreak cannot be overstated. References: Amass S.F., Stevenson G.W., Anderson C., Grote L.A., Dowell C., Vyverberg B.D., Kanitz C. & Ragland D. (2000) Investigation of people as mechanical vectors for porcine reproductive and respiratory syndrome virus. Swine Health & Production, 8, Amass S.F., Pacheco J.M., Mason P.E., Schneider J.L., Alvarez R.M., Clark L.K. & Ragland D. (2003) Procedures for preventing the transmission of foot-and-mouth disease virus to pigs and sheep by personnel in contact with infected pigs. Veterinary Record 153, APHIS (2004a) Practice backyard security. [Accessed 17-Sep-06] APHIS (2004b) Biosecurity for the birds. [Accessed 17-Sep-06]. Biosecurity New Zealand (2006) What is biosecurity? [Accessed 17-Sep-06] 33

9 Dee S., Deen J., Rossow K., Wiese C., Otake S., Joo H.S. & Pijoan C. (2002) Mechanical transmission of porcine reproductive and respiratory syndrome virus throughout a coordinated sequence of events during cold weather. Canadian Journal of Veterinary Research, 66, Dee S., Deen J., Rossow K., Weise C., Eliason R., Otake S., Joo H.S. & Pijoan C. (2003) Mechanical transmission of porcine reproductive and respiratory syndrome virus throughout a coordinated sequence of events during warm weather. Canadian Journal of Veterinary Research, 67, Defra (2006) Disease control: Biosecurity [Accessed 17-Sep-06] Donaldson,A. I.,Alexandersen, S., Sørensen, J.H.& Mikkelsen, T. (2001) Relative risks of the uncontrollable (airborne) spread of FMD by different species. Veterinary Record 148, FAO (2005) Biosecurity for agriculture and food production [Accessed 17-Sep-06] Honhold, N.,Taylor, N. M.,Mansley, L. M. & Paterson,A.D. (2004a) Relationship of speed of slaughter on infected premises and intensity of culling of other premises to the rate of spread of the foot-and-mouth disease epidemic in Great Britain, Veterinary Record 155, Honhold, N., Taylor, N. M.,Wingfield, A., Einshoj, P., Middlemiss, C., Eppink, L., Wroth, R. & Mansley, L. M. (2004b) Evaluation of the application of veterinary judgement in the preemptive cull of contiguous premises during the foot-and-mouth disease epidemic in Cumbria in Veterinary Record 155, House Of Commons Select Committee On Environment, Food And Rural Affairs (2002) First Report: The Impact of Foot-and-Mouth Disease. London, The Stationery Office. Massachusetts Department of Food and Agriculture (2001) Farm and Market Report: Farm Biosecurity and Why It s Important. [Accessed 17-Sep-06] Nielen M., Jalvingh A.W., Horst H.S., Dijkhuizen A.A., Maurice H., Schut B.H., van Wuijckhuise L.A. & de Jong M.F. (1996) Quantification of contacts between Dutch farms to assess the potential risk of foot-and-mouth disease spread. Preventive Veterinary Medicine, 28, Otake S, Dee S.A., Rossow K.D., Deen J., Joo H.S., Molitor T.W. & Pijoan C. (2002) Transmission of porcine reproductive and respiratory syndrome virus by fomites (boots and coveralls). Journal of Swine Health & Production, 10, Sanson R.L, Struthers G., King P., Weston J.F. & Morris R.S. (1993). The potential extent of transmission of foot-and-mouth disease: A study of the movement of animals and materials in Southland, New Zealand. New Zealand Veterinary Journal, 41, Taylor, N.M., Honhold, N., Paterson, A.D. & Mansley, L. M. (2004) Risk of foot-and-mouth disease associated with proximity in space and time to infected premises and the implications for control policy during the 2001 epidemic in Cumbria. Veterinary Record 154, Thrusfield M, Mansley L, Dunlop P, Taylor J, Pawson A, & Stringer L (2005) The foot-andmouth disease epidemic in Dumfries and Galloway, : Characteristics and control. The Veterinary Record,156, USDA (2006) Pre-Harvest Security Guidelines and Checklist [Accessed 17-Sep-06] Wikipedia contributors (2006) 'Biosecurity', Wikipedia, The Free Encyclopedia, 1 September 2006, 16:36 UTC, [Accessed 26-Sep-06] 34