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 veterinary practice-based 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 (10–37% 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

Size of supernumerary teats in sheep correlates with complexity of the anatomy and microenvironment.

Supernumerary nipples or teats (polythelia) are congenital accessory structures that may develop at any location along the milk line and have been implicated in the pathogenesis of mastitis. We describe the anatomy and histology of 27 spontaneously occurring supernumerary teats from 16 sheep, delineating two groups of teats - simple and anatomically complex - according to the complexity of the anatomy and microenvironment. Anatomically complex supernumerary teats exhibited significantly increased length and barrel diameter compared with simple supernumerary teats. A teat canal and/or teat cistern was present in anatomically complex teats, with smooth muscle fibres forming a variably well-organised encircling teat sphincter. Complex supernumerary teats also exhibited immune cell infiltrates similar to those of normal teats, including lymphoid follicle-like structures at the folds of the teat cistern-teat canal junction, and macrophages that infiltrated the peri-cisternal glandular tissue. One complex supernumerary teat exhibited teat end hyperkeratosis. These anatomical and histological features allow inference that supernumerary teats may be susceptible to bacterial ingress through the teat canal and we hypothesise that this may be more likely in those teats with less well-organised encircling smooth muscle. The teat cistern of anatomically complex teats may also constitute a focus of milk accumulation and thus a possible nidus for bacterial infection, potentially predisposing to mastitis. We suggest that size of the supernumerary teat, and relationship to the main teats, particularly in the case of 'cluster teats', should be considerations if surgical removal is contemplated.British Veterinary Association Animal Welfare Foundation (BVA AWF) Norman Hayward Fun

Overview of the practices of on-farm emergency slaughter of cattle in the Nordic countries

On farm mortality is an increasing problem in cattle production systems in the Nordic countries. It represents an economic loss to the farmer and raises questions of sustainability, food waste and animal welfare. On-farm emergency slaughter (OFES) represents, in some situations, an opportunity for a farmer to salvage some of the economic value from an animal that cannot be transported to a slaughterhouse. The basis of the regulation of OFES in the Nordic countries originates largely from legislation from the European Union. However, this review has found that the availability and practice of OFES in the Nordic countries differs considerably. For example, in Norway 4.2% of all cattle slaughter is OFES, whilst in Iceland OFES has never been recorded. National food safety authorities have issued differing regulations and guidelines regarding the suitability of sick and injured animals for OFES. This review shows there is a paucity of data regarding the incidence and reasons for the use of OFES of cattle in the Nordic countries and points out the need for more investigation into this area to improve veterinary education, consumer protection and animal welfare

Antimicrobial resistance in ovine bacteria: a sheep in wolf’s clothing?

Background: To monitor the prevalence of antimicrobial resistance (AMR), methods for interpretation of susceptibility phenotypes of bacteria are needed. Reference limits to declare resistance are generally based on or dominated by data from human bacterial isolates and may not reflect clinical relevance or wild type (WT) populations in livestock or other hosts. Methods: We compared the observed prevalence of AMR using standard and bespoke interpretations based on clinical breakpoints or epidemiological cut-offs (ECOFF) using gram positive (Staphylococcus aureus) and gram negative (Escherichia coli) bacteria from sheep as exemplars. Isolates were obtained from a cross-sectional study in three lowland sheep flocks in Scotland, and from a longitudinal study in one flock in Norway. S. aureus (n = 101) was predominantly isolated from milk or mammary glands whilst E. coli (n = 103) was mostly isolated from faecal samples. Disc diffusion testing was used to determine inhibition zone diameters, which were interpreted using either clinical breakpoints or ECOFF, which distinguish the bacterial wild type population from bacteria with acquired or mutational resistance to the compound of interest (non-wild type). Standard ECOFF values were considered as well as sheep-specific values calculated from the data using Normalized Resistance Interpretation (NRI) methodology. Results: The prevalence of AMR as measured based on clinical breakpoints was low, e.g. 4.0% for penicillin resistance in S. aureus. Estimation of AMR prevalence based on standard ECOFFs was hampered by lack of relevant reference values. In addition, standard ECOFFS, which are predominantly based on human data, bisected the normal distribution of inhibition zone diameters for several compounds in our analysis of sheep isolates. This contravenes recommendations for ECOFF setting based on NRI methodology and may lead to high apparent AMR prevalence. Using bespoke ECOFF values based on NRI, S. aureus showed non-wild type for less than 4% of isolates across 13 compounds, and ca. 13% non-wild type for amoxicillin and ampicillin, while E. coli showed non-wild type for less than 3% of isolates across 12 compounds, and ca. 13% non-wild type for tetracyclines and sulfamethoxazole-trimethoprim. Conclusion: The apparent prevalence of AMR in bacteria isolated from sheep is highly dependent on interpretation criteria. The sheep industry may want to establish bespoke cut-off values for AMR monitoring to avoid the use of cut-offs developed for other host species. The latter could lead to high apparent prevalence of resistance, including to critically important antimicrobial classes such as 4th generation cephalosporins and carbapenems, suggesting an AMR problem that may not actually exist

Overview and Evaluation of Existing Guidelines for Rational Antimicrobial Use in Small-Animal Veterinary Practice in Europe

Antimicrobial stewardship guidelines (ASGs) represent an important tool to help veterinarians optimize their antimicrobial use with the objective of decreasing antimicrobial resistance. The aim of this study was to map and qualitatively assess the ASGs for antimicrobial use in cats and dogs in Europe. Country representatives of the European Network for Optimization of Veterinary Antimicrobial Treatment (ENOVAT) were asked to identify ASGs published in their countries. All collated ASGs updated since January 2010 containing recommendations on antimicrobial therapy for at least three conditions affecting different organ systems in cats and dogs underwent detailed review including AGREE II analysis. Out of forty countries investigated, fifteen ASGs from eleven countries met the inclusion criteria. Several critical principles of antimicrobial use were identified, providing a framework that should assist development of stewardship guidance. The AGREE II analysis highlighted several methodological limitations of the currently available ASGs. This study sheds light on the lack of national ASGs for dogs and cats in multiple European countries and should encourage national bodies to prioritize guideline development in small animals. A greater awareness of the need to use a structured approach to guideline development could improve the quality of ASGs in the future.publishedVersio

Increasing importance of anthelmintic resistance in European livestock: creation and meta-analysis of an open database

peer reviewedHelminth infections are ubiquitous in grazing ruminant production systems, and are responsible for significant costs and production losses. Anthelmintic Resistance (AR) in parasites is now widespread throughout Europe, although there are still gaps in our knowledge in some regions and countries. AR is a major threat to the sustainability of modern ruminant livestock production, resulting in reduced productivity, compromised animal health and welfare, and increased greenhouse gas emissions through increased parasitism and farm inputs. A better understanding of the extent of AR in Europe is needed to develop and advocate more sustainable parasite control approaches. A database of European published and unpublished AR research on gastrointestinal nematodes (GIN) and liver fluke (Fasciola hepatica) was collated by members of the European COST Action “COMBAR” (Combatting Anthelmintic Resistance in Ruminants), and combined with data from a previous systematic review of AR in GIN. A total of 197 publications on AR in GIN were available for analysis, representing 535 studies in 22 countries and spanning the period 1980–2020. Reports of AR were present throughout the European continent and some reports indicated high within-country prevalence. Heuristic sample size-weighted estimates of European AR prevalence over the whole study period, stratified by anthelmintic class, varied between 0 and 48%. Estimated regional (country) prevalence was highly heterogeneous, ranging between 0% and 100% depending on livestock sector and anthelmintic class, and generally increased with increasing research effort in a country. In the few countries with adequate longitudinal data, there was a tendency towards increasing AR over time for all anthelmintic classes in GIN: aggregated results in sheep and goats since 2010 reveal an average prevalence of resistance to benzimidazoles (BZ) of 86%, macrocyclic lactones except moxidectin (ML) 52%, levamisole (LEV) 48%, and moxidectin (MOX) 21%. All major GIN genera survived treatment in various studies. In cattle, prevalence of AR varied between anthelmintic classes from 0–100% (BZ and ML), 0–17% (LEV) and 0–73% (MOX), and both Cooperia and Ostertagia survived treatment. Suspected AR in F. hepatica was reported in 21 studies spanning 6 countries. For GIN and particularly F. hepatica, there was a bias towards preferential sampling of individual farms with suspected AR, and research effort was biased towards Western Europe and particularly the United Kingdom. Ongoing capture of future results in the live database, efforts to avoid bias in farm recruitment, more accurate tests for AR, and stronger appreciation of the importance of AR among the agricultural industry and policy makers, will support more sophisticated analyses of factors contributing to AR and effective strategies to slow its spread

A pilot survey of farm animal welfare in Serbia, a country preparing for EU accession

publishedVersio

Highs and lows of lambing time: Sheep farmers? perceptions of the first outbreak of schmallenberg disease in south west England on their well-being

The outbreak of a previously unknown and new disease in the United Kingdom, known as ‘Schmallenberg disease’, a disease associated with abortions, stillbirths and fetal deformities in naïve ewes, was reported for the first time in South West England during the 2012/13 early lambing season. Epidemiological studies confirmed that the Schmallenberg virus (SBV) had a severe negative impact upon animal welfare and the productivity of affected flocks. By contrast, there was a specific lack of research on the impact of SBV on sheep farmer well-being. This study aimed to improve our understanding of sheep farmers’ experiences of Schmallenberg disease, and the impact of the first outbreak on sheep farmer well-being during the 2012/13 early lambing season in South West England. Face-to-face, semi-structured interviews with six farmers with small flocks of pedigree and purebred sheep in South West England were conducted in 2013. The data were analysed via thematic analysis. The main themes regarding the impact of disease on farmer well-being included: (i) emotional highs and lows are part of a normal lambing season; (ii) negative emotions and memories associated with the Schmallenberg disease outbreak; and (iii) resilience and coping with the unexpected disease outbreak. These novel data present preliminary findings from a small number of sheep farmers, and indicate that for some farmers, an unexpected outbreak of a new and emerging disease for the first time during lambing, and dealing with high levels of dystocia, deformities and deaths in their animals, had a negative impact on their emotional well-being during the peak period of the sheep production cycle.publishedVersio

Highs and Lows of Lambing Time: Sheep Farmers’ Perceptions of the First Outbreak of Schmallenberg Disease in South West England on Their Well-Being

The outbreak of a previously unknown and new disease in the United Kingdom, known as ‘Schmallenberg disease’, a disease associated with abortions, stillbirths and fetal deformities in naïve ewes, was reported for the first time in South West England during the 2012/13 early lambing season. Epidemiological studies confirmed that the Schmallenberg virus (SBV) had a severe negative impact upon animal welfare and the productivity of affected flocks. By contrast, there was a specific lack of research on the impact of SBV on sheep farmer well-being. This study aimed to improve our understanding of sheep farmers’ experiences of Schmallenberg disease, and the impact of the first outbreak on sheep farmer well-being during the 2012/13 early lambing season in South West England. Face-to-face, semi-structured interviews with six farmers with small flocks of pedigree and purebred sheep in South West England were conducted in 2013. The data were analysed via thematic analysis. The main themes regarding the impact of disease on farmer well-being included: (i) emotional highs and lows are part of a normal lambing season; (ii) negative emotions and memories associated with the Schmallenberg disease outbreak; and (iii) resilience and coping with the unexpected disease outbreak. These novel data present preliminary findings from a small number of sheep farmers, and indicate that for some farmers, an unexpected outbreak of a new and emerging disease for the first time during lambing, and dealing with high levels of dystocia, deformities and deaths in their animals, had a negative impact on their emotional well-being during the peak period of the sheep production cycle