Impacts of Schmallenberg virus infection in early lambing sheep flocks following the second wave of virus circulation in South West England in 2012/2013: a mixed-methods descriptive study

Abstract Background The first cases of Schmallenberg virus (SBV) infection in the UK were confirmed in congenitally malformed lambs born in South East England in January 2012. Epidemiological studies confirmed that SBV infection could have severe negative impacts on animal welfare and productivity in affected flocks of sheep (Ovis aries), but there was a lack of specific research on the impacts of infection on recorded reproductive performance, animal welfare, financial performance, and farmers’ emotional well-being in some of the first affected early lambing flocks in South West England in 2012 / 2013. Objectives This mixed methods veterinary practice-based descriptive study aimed to describe the clinical signs observed by sheep farmers in the region experiencing outbreaks of disease due to SBV for the first time; to evaluate physical records (quantitative data) on reproductive performance in early lambing flocks prior to and during the affected 2012 / 2013 production year; and to gauge farmers’ perceptions (qualitative interview data and quantitative severity scores) of the impacts of SBV infection on animal welfare, financial performance, and their emotional well-being, and risks of future outbreaks of disease and preventive strategies including SBV vaccination. Evidentiary value This mixed-methods descriptive study reported farmers’ detailed experiences, and recorded and perceived impacts, of SBV infection in six pedigree and purebred flocks in South West England, lambing early between November 2012 and January 2013. Previous surveys were larger than the current study and assessed the impacts of SBV at farm rather than flock level and on a more diverse range of British sheep farms lambing over extended periods; impacts were compared between three categories of farms based on laboratory confirmation or farmers’ suspicions of infection i.e. ‘SBV confirmed’, ‘SBV suspected’ and ‘SBV not suspected’. This study was able to capture and compare the reproductive performance of these flocks in the SBV affected production year in 2012 / 2013 with up to three previous unaffected years; it found variable negative effects of SBV not only on ewe and lambs losses, stillbirths and abortions, levels of dystocia and need for variable levels of assistance to deliver lambs, but also on overall flock reproductive performance, barren rate, lambing percentage and lamb rearing percentage. The qualitative elements of the study enabled new insights into the variable effects of SBV infection in flocks on ewes and lambs and on farmers’ perceptions of the impacts on animal welfare, flock financial performance and their own emotional well-being. The findings suggest previous surveys may not have fully captured the impacts of SBV infection in high value pedigree and purebred early lambing flocks infected for the first time during the second wave of virus circulation and peak midge vector activity in the southwest region in summer and autumn 2012. The findings highlight the need for further research to explore factors influencing uptake of SBV vaccination by farmers to protect flocks against future waves of infection, and to develop more rational vaccination programmes based on ‘early warning’ surveillance systems. Methods Face-to-face semi-structured interviews were conducted in 2013. Qualitative interview data were thematically analysed to gain an understanding of the perspectives, perceptions and lived experiences of sheep farmers. Quantitative data in the form of (i) farmers’ self-appraised severity scores of the perceived impacts on flock welfare, financial performance and their emotional well-being; and (ii) flock records of pregnancy scanning results, lambing dates, and mortality records for ewes and lambs, were collected for the SBV affected 2012/2013 production year and for up to 3 previous years for comparison. Results Farmers perceived generally high but widely variable negative impacts of SBV infection on animal welfare (median score: 3.5/5, range: 2–5), financial performance (median score: 3.5/5, range: 2–5) and their own well-being (median score: 4/5, range: 2–5); variation between farmers in the severity of impacts appeared not to be directly related to recorded lamb losses (of all lambs born, an overall average of 21% (range: 13.7–42.6%) were stillborn or died within 7 days; 15% (range: 4.1–42.6%) were stillborn or died due to SBV), or to reductions in lamb rearing percentage (10–38% fewer lambs reared in the affected year compared to previous reproductive performance or an industry benchmark). The qualitative elements of the study enabled new insights into the variable effects of SBV infection in flocks on ewes and lambs and on farmers’ perceptions of the impacts on animal welfare, flock financial performance and their own emotional well-being. The semi-structure interviews captured narrative descriptions of the distressing clinical signs seen in ewes and lambs, the variable levels of dystocia, and the lived experiences of farmers caring for affected sheep including the increased workload during the lambing period, greater feelings of tiredness and anxiety than in ‘normal’ lambing periods, depression, and also more positive emotions of resilience and ability to cope with an unexpected and novel disease outbreak. Three of the six farmers subsequently vaccinated with SBV vaccine to protect their early lambing flocks before the next early breeding season. Of the three farmers who decided not to vaccinate: one delayed the start of the subsequent breeding season; the second felt uncertain about using the rapidly developed and authorised vaccine so close to the start of the breeding season but was reassured by veterinary advice that the risk of a further disease outbreak in the subsequent breeding season was low as flock SBV seroprevalence was high (~90% of ewe were seropositive) following the first outbreak; and the third experienced the lowest sheep losses of the six farmers in the first outbreak and perceived the severity of the impacts to be at the lowest level, but felt uncertain about the risks of repeat infections and future disease outbreaks. Conclusion Severity of farmer perceived impacts of SBV infection was generally high; farmers’ detailed descriptions of their experiences during the outbreak, and perceptions of the impacts on ewe and lamb welfare, financial performance and their emotional well-being, captured during semi-structured interviews, are reported for the first time. Variation in severity of impacts appeared not to be directly related to the number and proportion of lambs stillborn or that died in the first week of life and the overall reduction in percentage of lambs reared for sale. Qualitative interview data taken together with quantitative data on recorded flock performance suggested multiple factors and variable effects of SBV in flocks were likely to have contributed to, and variably influenced, the severity of impacts perceived by farmers. Uncertainty about the safety, efficacy and use of the vaccine so close to the next early breeding season when it was first authorised in May 2013, and the risks of repeat SBV infections and future disease outbreaks for farmers who decided not to vaccinate their flocks may have added to the impact on farmers’ emotional well-being. Reductions in lamb rearing percentage appeared to be higher in flocks that artificially inseminated ewes in synchronised oestrus in July 2012 than in those that mated ewes naturally in spontaneous oestrus in June 2012. These findings are important and suggest that recorded lamb losses and reduction in rearing percentage should not be used as proxy measures of the severity of impacts of SBV infection on farmers and sheep flocks. Further outbreaks have occurred in the UK in 2016/2017 and 2021/2022 and it is expected this pattern of virus circulation and disease re-emergence will be repeated every 3–6 years. Flocks remain at-risk of future SBV infection and, in high risk flocks, of severe impacts on animal health and welfare, flock financial performance and farmers’ emotional well-being. Further research is needed to explore farmers’ future risk perceptions, uncertainty and decision-making around preventive vaccination, and to explore the potential for more rational vaccination programmes based on active arbovirus (SBV and Bluetongue virus [BTV]) surveillance systems. Application These findings will be of interest to all stakeholders in the sheep industry e.g. farmers, veterinarians, advisers, researchers, welfare organisations, pharmaceutical companies, the UK Government, industry levy boards and other research funding bodies. The study offers new insights into the impacts of SBV infection in sheep flocks, particularly in production systems dependent upon early breeding (so called ‘out of season breeding’) overlapping with periods of peak midge activity and circulation of SBV in which risks of high impacts appear to be greater. Other studies are needed to investigate further possible associations between variability in reproductive outcomes and factors such as breed (not reported here) and timing and method of breeding (natural mating or artificial insemination; at a spontaneous or synchronised oestrus). Research is needed to better understand farmers’ decision-making around SBV vaccination and to investigate the potential for more rational vaccination programmes based on early warning systems, such as national or Europe-wide arbovirus surveillance systems.