Sustainable worm control in ruminants in Europe: current perspectives

Abstract

Anthelmintic resistance is an escalating problem in Europe and the environmental consequences (soil and aquatic health) related to anthelmintic use are an increasing matter of concern. Several sustainable worm control (SWC) practices are available now. These include the increased use of diagnostics and decision support enabling a targeted use of anthelmintics. Complementary control measures, referred to as the “Basket of Options”, include plant-based control, grazing management, nematode-destroying fungi, and selective breeding and can also reduce the need for anthelmintic use. Their use is more complex than the simple use of anthelmintics and their uptake has remained relatively low. Equipped by recent studies on the barriers to and drivers of uptake of SWC practices, it is now time to develop a Community of Practice across Europe, involving all relevant stakeholders at local, national, and European levels to achieve SWC together. Cattle, sheep, goats, and their associated industries are a vital component in the development of rural areas and sustainable land use strategies in Europe. With 77 million bovines and 74 million sheep and goats in the EU (Eurostat, 2023), ruminant production is deeply linked to European culture. All European farmed ruminant populations with outdoor access are exposed to parasitic worm (helminth) infections and these remain an important constraint on ruminant productivity. They cost the sector an estimated over €1.8 billion a year, with 80% of this due to production losses and 20% due to treatment costs (Charlier et al., 2020). Worm infections are sensitive to weather conditions and the changing climate, can severely impact animal welfare, and lead to an increase in greenhouse gas emissions from parasitized livestock (Charlier et al., 2017; Houdijk et al., 2017). Reducing the burden of helminth infections in livestock is thus an actionable contribution to the United Nation’s sustainable development goals and the EU’s long-term strategy to reduce greenhouse gas emissions from the agricultural sector by 49% by 2050. Current worm control relies on the regular administration of anthelmintic drugs. However, in a recent meta-analysis of European data aggregated since 2010, the average prevalence of anthelmintic resistance (AR) to the 3 major anthelmintic drug classes ranged between 48% and 86% (Rose Vineer et al, 2020). Cases of cross-resistance and multidrug resistance are increasingly reported (Bordes at al., 2020). Thus, a report from the World Organisation for Animal Health (WOAH, formerly OIE) warns of the urgent need for responsible and prudent use of anthelmintics to limit the development of AR in grazing livestock (WOAH, 2021). In Europe, stakeholders, including the European Farmers and Agri-Cooperatives (Copa-Cogeca), the Federation of Veterinarians of Europe, and the animal health industry (AnimalhealthEurope) have recognized the need to take action to ensure the responsible use of anthelmintics in food-producing animals through the European Platform for Responsible Use of Medicines in Animals (EPRUMA, 2019). Research on sustainable worm control (SWC) practices has been occurring for a long time in Europe. Now, it is time to move from research to implementation. This article will lay down the vision to build a European Community of Practice (CoP), over the coming years, supported by the novel Horizon Europe Thematic Network “SPARC—Sustainable Parasite Control in ruminants”. There is a long tradition of research toward improved worm control in Europe thanks to EU funding (e.g., FP6, FP7, ERA-NETs, Horizon 2020, and Horizon Europe). One of the foundational projects was the EU-funded PARASOL consortium (running from 2006 to 2009), the first transnational project in Europe, and beyond, as the consortium also included partners from Africa. The project recognized that while concerns around the sustainability of helminth control in ruminant livestock had been building globally for well over a decade (Waller, 1993), the application of SWC was critically dependent on finding pragmatic methods for farms in Europe. PARASOL built on refugia-based approaches (Leathwick et al., 2006; Van Wyk et al., 2006) and further developed them through concepts of anthelmintic targeted treatments (TT) and targeted selective treatments, improved in vivo and in vitro tests for detection of AR, and worked on optimizing efficacy and bioavailability of anthelmintic compounds (Vercruysse et al., 2009). During the same period, the DELIVER project addressed the growing problem of liver fluke disease in Europe. The project improved knowledge on Fasciola hepatica epidemiology, the genetics of different isolates, and vaccine studies to design effective and sustainable control strategies. Control of both parasitic helminths (nematodes and liver fluke) was integrated into the GLOWORM (2012 to 2014) and PARAVAC (2011 to 2015) projects. GLOWORM developed high-throughput and multiplex diagnostic methods, models predicting parasite infections under climate change conditions, and sustainable control strategies (Rinaldi et al., 2015), whereas PARAVAC consolidated research on vaccines against helminth infections (Matthews et al., 2016). All the above networks allowed for the development of intense research interactions on worm control between European actors. These networks were further consolidated and extended via the creation of the Livestock Helminth Research Alliance in 2014 (Charlier et al., 2017) and the COST Action COMBAR (2017 to 2022; Charlier et al., 2022), resulting in a network of over 200 researchers from across Europe and from various specific disciplines working together to find solutions for the problem of AR. COMBAR was the first project placing emphasis on using more economic and social sciences in the development of SWC strategies, recognizing the central importance of producer behavior (McArthur and Reinemeyer, 2014). It also called for the development of multi-actor approaches involving veterinarians, farmers, pharmaceutical industry, and research bodies to create awareness and cocreate solution paths in mitigating the escalating spread of AR (Höglund et al., 2021). Therefore, SPARC was developed as a natural evolution and culmination of the previous 2 decades’ work to make a pan-European multi-actor movement on sustainable parasite control a reality. SPARC aims to establish a collaborative network across Europe, with its vast diversity in ruminant livestock production systems (See Text Box), involving various stakeholders to enhance the sustainability, efficiency, and resilience of ruminant livestock farms. The project focuses on curbing the escalating threat of AR and aims to achieve 3 primary objectives: enhancing animal health and welfare, improving economic performance, and promoting environmental sustainability within the sector (Figure 1). In SPARC, SWC strategies will be translated and promoted into user-friendly advice/guidelines through multiple approaches across Europe. Regional and production type-specific adaptation of these approaches will be applied. To achieve its goals, SPARC will engage in horizontal knowledge exchange, drawing insights from farmers, veterinarians, advisors, and industry partners to identify and disseminate cost-effective, practical, stakeholder-driven solutions for sustainable ruminant production (Figure 2). Summary of workflow and interaction of the SPARC project work packages The project will establish national and regional stakeholder networks across participating countries, leveraging existing networks of partner institutions, and recruiting additional participants to form a CoP. The CoP will revolve around 3 central actor groups: farmers, veterinarians, and farm advisors. These groups collaborate with partners and associated organizations, including governmental agencies, universities, research institutes, technical and pharmaceutical companies, and farmer organizations. This CoP will identify and disseminate best practices for SWC. Stakeholder needs are being assessed through focus groups and selected control strategies are being implemented in pilot farms in 17 countries. The impact of the control strategies on animal productivity, welfare, economic returns, and anthelmintic efficacy will be monitored. Simultaneously, SPARC is developing a knowledge exchange platform (KEP) populated with insights gathered from the focus groups, the pilot farms, and other activities from associated organizations. The knowledge will then be disseminated through regional CoP subnetworks using multimedia info-packs in different languages with a specific emphasis on overcoming external obstacles encountered during the trial implementation. “United in diversity,” the motto of the EU reflects the diversity in the cultures, traditions, and languages across the European continent. This diversity is equally a characteristic of the European livestock systems and hence the SWC strategies that are practical, feasible, and fit with longstanding traditions. Below we want to show this diversity through a few examples that underline the situation and SWC activities in different countries. Ireland is a predominantly grass-based livestock system, with a temperate, high-rainfall climate, and largely seasonal breeding, particularly in the prominent dairy industry. The extensive reliance on grazing translates to livestock farming that is heavily impacted by helminth infections. Additionally, resistance in both sheep and cattle roundworms and liver fluke is increasingly concerning for the livestock industry. Partly due to this resistance risk, Ireland is currently in a transition period where antiparasitic medicines will require a veterinary prescription, having previously been exempt. This has resulted in a focus on best practice messaging and prudent use of anthelmintics from advisory bodies such as Teagasc and Animal Health Ireland, who facilitate a working group of parasite experts; as well as the establishment of an industry Antiparasitic Resistance Stakeholder Group. Examples of promoted measures include a Targeted Advisory Service on Animal Health focusing on parasite control (Meunier, 2023) and the ongoing development of best practice guidelines. Despite these recent initiatives, like elsewhere, changing behavior to sustainable measures can be slow. Excluding small farms, more than half of Irish farmer households have off-farm employment, 30% of farmers are of pensionable age and an average of one-third of sheep and cattle-rearing farms are economically vulnerable (Teagasc, 2023). Therefore, interventions that are time and cost-effective, with minimal management, are required if a majority of farmers are to adopt these behaviors. Poland is the 5th largest (cattle) milk producer of the EU and 12th largest globally. However, despite the large cattle population, data on the prevalence of AR in this species are unavailable. Knowledge about resistance to anthelmintics among veterinarians, farm advisors, and farmers is low. The method of anthelmintic prevention in cattle herds depends largely on the knowledge and experience of the veterinarian and the financial resources of the owner. The length of the milk withdrawal period is crucial in deciding on the use of anthelmintics, which is why in recent years, drugs with 0 d or a short milk withdrawal period have been more practice is to animals with anthelmintics a the and of the grazing and on SWC practices are Knowledge on the prevalence of AR and SWC practices in small is than for cattle et al., 2021). 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