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      Increasing importance of anthelmintic resistance in European livestock: creation and meta-analysis of an open database Translated title: Importance croissante de la résistance aux anthelminthiques chez les ruminants européens : création et méta-analyse d’une base de données ouverte

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      EDP Sciences

      Anthelmintic resistance, Ruminants, Europe, Gastrointestinal nematodes, Liver fluke, Prevalence, Maps, Database

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          Helminth 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 A database of European published and unpublished AR research on gastrointestinal nematodes (GIN) and liver fluke ( Fasciola hepatica) was collated by members of the European COST Action “COMBAR” (Combatting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.

          Translated abstract

          Les helminthes sont omniprésents dans les systèmes de production de ruminants au pâturage et sont responsables de coûts et de pertes de production importants. La résistance aux anthelminthiques (RA) des parasites est maintenant répandue dans toute l’Europe, bien qu’il existe encore des lacunes dans nos connaissances dans certaines régions et certains pays. La RA est une menace majeure pour la pérennité de la production moderne de ruminants, en diminuant la productivité, en compromettant la santé et le bien-être des animaux, et en augmentant les émissions de gaz à effet de serre au travers d’une augmentation du parasitisme et des intrants agricoles. Une meilleure compréhension de l’étendue de la RA en Europe est nécessaire pour développer et préconiser des approches de lutte antiparasitaire plus durables. Une base de données intégrant des informations publiées et non publiées en Europe concernant la RA des nématodes gastro-intestinaux (NGI) et de la douve du foie ( Fasciola hepatica) a été compilée par les membres de l’action européenne COST « COMBAR » (« Combattre la résistance aux anthelminthiques chez les ruminants ») et combinée avec les données d’une précédente étude systématique concernant la RA des NGI. Au total, 197 publications sur la RA des NGI étaient disponibles pour analyse, représentant 535 études dans 22 pays et couvrant la période 1980–2020. Des signalements de RA étaient présents sur tout le continent européen et certains rapports indiquaient une forte prévalence nationale. Les estimations heuristiques pondérées par la taille de l’échantillon de la prévalence de la RA en Europe sur toute la période d’étude, stratifiées par classe d’anthelminthiques, variaient de 0 à 48 %. La prévalence régionale (nationale) estimée était très hétérogène, variant entre 0 % et 100 % selon le secteur de l’élevage et la classe d’anthelminthique, et augmentait généralement avec les efforts de recherche dans le pays. Dans les quelques pays disposant de données longitudinales adéquates, il y avait une tendance à l’augmentation de la RA au fil du temps pour toutes les classes d’anthelminthiques des NGI : les résultats agrégés chez les ovins et caprins depuis 2010 révèlent une prévalence moyenne de résistance aux benzimidazoles (BZ) de 86 %, aux lactones macrocycliques sauf moxidectine (ML) de 52 %, au lévamisole (LEV) de 48 % et à la moxidectine (MOX) de 21 %. Tous les genres principaux de NGI ont survécu au traitement dans diverses études. Chez les bovins, la prévalence de la RA variait selon les classes d’anthelminthiques de 0 à 100 % (BZ et ML), 0 à 17 % (LEV) et 0 à 73 % (MOX), et Cooperia et Ostertagia ont survécu aux traitements. Une RA suspectée chez F. hepatica a été signalée dans 21 études portant sur 6 pays. Pour les NGI, et encore plus pour F. hepatica, il y avait un biais d’échantillonnage en faveur des exploitations individuelles suspectées de RA, et l’effort de recherche était biaisé vers l’Europe occidentale et en particulier le Royaume-Uni. La capture continue des résultats futurs dans la base de données, en direct, les efforts pour éviter les biais dans le recrutement des exploitations, des tests plus précis pour la RA et une meilleure appréciation de l’importance de la RA parmi l’industrie agricole et les décideurs politiques, soutiendront des analyses plus sophistiquées des facteurs contribuant à la RA, et des stratégies efficaces pour ralentir sa propagation.

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          Most cited references 49

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              An inconvenient truth: global worming and anthelmintic resistance.

              Over the past 10-15 years, we have witnessed a rapid increase in both the prevalence and magnitude of anthelmintic resistance, and this increase appears to be a worldwide phenomenon. Reports of anthelmintic resistance to multiple drugs in individual parasite species, and in multiple parasite species across virtually all livestock hosts, are increasingly common. In addition, since the introduction of ivermectin in 1981, no novel anthelmintic classes were developed and introduced for use in livestock until recently with the launch of monepantel in New Zealand. Thus, livestock producers are often left with few options for effective treatment against many important parasite species. While new anthelmintic classes with novel mechanisms of action could potentially solve this problem, new drugs are extremely expensive to develop, and can be expected to be more expensive than older drugs. Thus, it seems clear that the "Global Worming" approach that has taken hold over the past 40-50 years must change, and livestock producers must develop a new vision for parasite control and sustainability of production. Furthermore, parasitologists must improve methods for study design and data analysis that are used for diagnosing anthelmintic resistance, especially for the fecal egg count reduction test (FECRT). Currently, standards for diagnosis of anthelmintic resistance using FECRT exist only for sheep. Lack of standards in horses and cattle and arbitrarily defined cutoffs for defining resistance, combined with inadequate analysis of the data, mean that errors in assigning resistance status are common. Similarly, the lack of standards makes it difficult to compare data among different studies. This problem needs to be addressed, because as new drugs are introduced now and in the future, the lack of alternative treatments will make early and accurate diagnosis of anthelmintic resistance increasingly important. Copyright © 2011 Elsevier B.V. All rights reserved.

                Author and article information

                EDP Sciences
                04 December 2020
                : 27
                : ( publisher-idID: parasite/2020/01 )
                [1 ] Department of Infection Biology and Microbiomes, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool Neston, Cheshire CH64 7TE UK
                [2 ] Institute for Global Food Security, Queen’s University Belfast, Biological Sciences 19 Chlorine Gardens Belfast BT9 5DL UK
                [3 ] Institute of Parasitology, University of Zurich 8057 Zurich Switzerland
                [4 ] Disease Control, Moredun Research Institute, Pentlands Science Park, Bush Loan Penicuik, Edinburgh EH26 0PZ UK
                [5 ] University of Naples Federico II, Unit of Parasitology and Parasitic Diseases, Department of Veterinary Medicine and Animal Production, CREMOPAR Via Delpino, 1 80137 Napoli Italy
                [6 ] Kreavet Hendrik Mertensstraat 17 9150 Kruibeke Belgium
                [7 ] BIOEPAR, INRAE, Oniris 44307 Nantes France
                [8 ] Laboratory for Parasitology, Faculty of Veterinary Medicine, Ghent University B9820 Merelbeke Belgium
                [9 ] School of Veterinary Medicine, University College Dublin Dublin D04 W6F6 Ireland
                [10 ] Avia-GIS Risschotlei 33 2980 Zoersel Belgium
                [11 ] Institute of Parasitology, Department of Pathobiology, Vetmeduni Vienna Veterinärplatz 1 1210 Vienna Austria
                [12 ] Swedish University of Agricultural Sciences, Department of Veterinary Public Health, Section for Parasitology P.O. Box 7036 Uppsala Sweden
                [13 ] Clinic for Reproduction and Large Animals, Veterinary faculty, University of Ljubljana Gerbičeva 60 1000 Ljubljana Slovenia
                [14 ] Department of Botany and Zoology, Faculty of Science, Masaryk University Brno 611 37 Czech Republic
                [15 ] Animal Bioscience Department, Teagasc Grange, Dunsany, Co. Meath C15 PW93 Ireland
                [16 ] Instituto de Ganaderia de Montana, CSIC Universidad de León 24346 Grulleros León Spain
                [17 ] CISAS – Centre for Research and Development in Agrifood Systems and Sustainability, Escola Superior Agrária, Instituto Politécnico de Viana do Castelo, Rua Escola Industrial e Comercial de Nun’Àlvares 4900-347 Viana do Castelo Portugal
                [18 ] EpiUnit – Instituto de Saúde Pública da Universidade do Porto Rua das Taipas, nº 135 4050-091 Porto Portugal
                [19 ] Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Garscube Estate Glasgow G61 1QH UK
                [20 ] Division of Veterinary Epidemiology and Economics, Institute of Veterinary Medicine, Warsaw University of Life Sciences Nowoursynowska 159c 02-776 Warsaw Poland
                [21 ] Faculdade de Medicina Veterinária – Universidade Lusófona de Humanidades e Tecnologias Av. Campo Grande 376 1749-024 Lisbon Portugal
                [22 ] Institute for Production Animal Clinical Science, Faculty of Veterinary Medicine, Norwegian University of Life Sciences Sandnes 4325 Norway
                [23 ] Department of Biomolecular Health Sciences, Division Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University Yalelaan 1 3584 CL Utrecht The Netherlands
                [24 ] Institute for Microbiology and Parasitology, Veterinary Faculty, University of Ljubljana Gerbičeva 60 1000 Ljubljana Slovenia
                [25 ] Department of Veterinary Medicine, Faculty of Agriculture, University of Novi Sad 21101 Novi Sad Republic of Serbia
                [26 ] Veterinary Research Institute, Section for Parasitology, HAO-DEMETER, Thermi 57001 Thessaloniki Greece
                [27 ] Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca 400372 Romania
                [28 ] Section for Parasitology and Aquatic Pathobiology, Department of Veterinary and Animal Sciences, University of Copenhagen DK-1870 Frederiksberg C Denmark
                [29 ] Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague Kamycka 129 165 00 Prague Suchdol Czech Republic
                [30 ] Institute of Parasitology of the Slovak Academy of Sciences Kosice 040 01 Slovakia
                [31 ] Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin Robert-von-Ostertag-Str. 7–13 14163 Berlin Germany
                Author notes
                parasite200140 10.1051/parasite/2020062
                © H. Rose Vineer et al., published by EDP Sciences, 2020

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 6, Tables: 2, Equations: 4, References: 54, Pages: 16
                Research Article
                Special Issue – Combatting Anthelmintic resistance in ruminants. Invited Editors: Johannes Charlier, Hervé Hoste, and Smaragda Sotiraki


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