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Tierarztl Prax Ausg G Grosstiere Nutztiere 2023; 51(03): 153-159
DOI: 10.1055/a-2097-9361
Übersichtsartikel

Fünf nach zwölf – zur Resistenzlage gastrointestinaler Nematoden bei kleinen Wiederkäuern in Deutschland

Five past twelve – the resistance situation in small ruminant gastrointestinal nematodes in Germany
Katja Voigt
1   Klinik für Wiederkäuer mit Ambulanz und Bestandsbetreuung, Ludwig-Maximilians-Universität München
,
Maximilian Geiger
1   Klinik für Wiederkäuer mit Ambulanz und Bestandsbetreuung, Ludwig-Maximilians-Universität München
,
Miriam Jäger
2   Labor ParaDocs, Ismaning
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Zusammenfassung

Anthelminthikaresistenzen haben weltweit ein besorgniserregendes Ausmaß erreicht, das die Weidehaltung kleiner Wiederkäuer in einigen Regionen der Welt bereits ernsthaft gefährdet. Auch in Europa hat sich die Resistenzlage im letzten Jahrzehnt dramatisch verschlechtert. Der Artikel fasst den Stand der Wissenschaft zum Vorkommen von Anthelminthikaresistenzen bei kleinen Wiederkäuern mit Schwerpunkt auf Deutschland und seinen Nachbarländern zusammen, erläutert Mechanismen der Resistenzentstehung und -verbreitung und gibt Hinweise für einen verantwortungsvollen Umgang mit Anthelminthika in der tierärztlichen Praxis.

Abstract

Anthelmintic resistance has reached alarming levels worldwide and already seriously threatens pasture-based small ruminant production in certain geographic regions. The situation in Europe has also dramatically deteriorated in the last decade. This review provides an overview of the occurrence of anthelmintic resistance in small ruminants with a particular focus on Germany and its neighbouring countries. It also covers mechanisms leading to the development and spread of anthelmintic resistance, and recommendations for a responsible use of anthelmintics in veterinary practice.

Schlüsselwörter

Schaf - Ziege - Anthelminthika - Wirksamkeit

Key words

Sheep - goat - anthelmintics - effectiveness


Publikationsverlauf

Eingereicht: 30. Januar 2023

Angenommen: 23. März 2023

Artikel online veröffentlicht:
11. August 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • Literatur

  • 1 Vercruysse J, Charlier J, van Dijk J. et al. Control of helminth ruminant infections by 2030. Parasitology 2018; 145: 1655-1664
    CrossrefPubMedSuche in Google Scholar
  • 2 Richter A, Steuber S Antiparasitica. In: Frey H-H, Löscher W, Hrsg. Lehrbuch der Pharmakologie und Toxikologie für die Veterinärmedizin, 3. Aufl. Stuttgart: Enke; 2010: 469-526
    PubMed
  • 3 Vetidata. Im Intenet: https://www.vetidata.de Stand: 28.01.2023
    PubMed
  • 4 Kaminsky R, Gauvry N, Schorderet Weber S. et al. Identification of the amino-acetonitrile derivative monepantel (AAD 1566) as a new anthelmintic drug development candidate. Parasitol Res 2008; 103: 931-939
    CrossrefPubMedSuche in Google Scholar
  • 5 Emmerich IU, Ganter M, Wittek T. Dosierungsvorschläge für Arzneimittel bei kleinen Wiederkäuern und Neuweltkameliden. 2. Aufl. Stuttgart: Schattauer; 2016
    Suche in Google Scholar
  • 6 Hennessy DR, Sangster NC, Steel JW. et al. Comparative pharmacokinetic behaviour of albendazole in sheep and goats. Int J Parasitol 1993; 23: 321-325
    CrossrefPubMedSuche in Google Scholar
  • 7 Hennessy DR, Sangster NC, Steel JW. et al. Comparative pharmacokinetic disposition of closantel in sheep and goats. J Vet Pharmacol Therap 1993; 16: 254-260
    CrossrefPubMedSuche in Google Scholar
  • 8 Escudero E, Carceles CM, Diaz MS. et al. Pharmacokinetics of moxidectin and doramectin in goats. Res Vet Sci 1999; 67: 175-179
    CrossrefPubMedSuche in Google Scholar
  • 9 Gokbulut C, Yalinkilinc HS, Aksit D. et al. Comparative pharmacokinetics of levamisole-oxyclozanide combination in sheep and goats following per os administration. Can J Vet Res 2014; 78: 316-320
    PubMedSuche in Google Scholar
  • 10 Lecová L, Stuchlíková L, Prchal L. et al. Monepantel: the most studied new anthelmintic drug of recent years. Parasitology 2014; 141: 1686-1698
    CrossrefPubMedSuche in Google Scholar
  • 11 Myers MJ, Howard KD, Kawalek JC. Pharmacokinetic comparison of six anthelmintics in sheep, goats, and cattle. J Vet Pharmacol Therap 2021; 44: 58-67
    CrossrefPubMedSuche in Google Scholar
  • 12 Kaplan RM. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 2004; 20: 477-481
    CrossrefPubMedSuche in Google Scholar
  • 13 Scott I, Pomroy WE, Kenyon PR. et al. Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis . Vet Parasitol 2013; 198: 166-171
    CrossrefPubMedSuche in Google Scholar
  • 14 van Wyk JA, Hoste H, Kaplan RM. et al. Targeted selective treatment for worm management – how do we sell rational programs to farmers?. Vet Parasitol 2006; 139: 336-346
    CrossrefPubMedSuche in Google Scholar
  • 15 Rose H, Rinaldi L, Bosco A. et al. Widespread anthelmintic resistance in European farmed ruminants: a systematic review. Vet Rec 2015; 176: 546
    CrossrefPubMedSuche in Google Scholar
  • 16 Rose Vineer H, Morgan ER, Hertzberg H. et al. Increasing importance of anthelmintic resistance in European livestock: creation and meta-analysis of an open database. Parasite 2020; 27: 69
    CrossrefPubMedSuche in Google Scholar
  • 17 Mavrot F, Hertzberg H, Torgerson P. Effect of gastro-intestinal nematode infection on sheep performance: a systematic review and meta-analysis. Parasit Vectors 2015; 8: 557
    CrossrefPubMedSuche in Google Scholar
  • 18 Deplazes P, Joachim A, Mathis A, Strube C, Taubert A, von Samson-Himmelstjerna G, Zahner H. Parasitologie für die Tiermedizin. 4. Aufl. Stuttgart: Thieme; 2021
    Suche in Google Scholar
  • 19 Kaplan RM, Vidyashankar AN. An inconvenient truth: Global worming and anthelmintic resistance. Vet Parasitol 2012; 186: 70-78
    CrossrefPubMedSuche in Google Scholar
  • 20 Bauer C. Multispecific resistance of trichostrongyles to benzimidazoles in a goat herd in Germany. Dtsch Tierarztl Wochenschr 2001; 108: 49-50
    PubMedSuche in Google Scholar
  • 21 Moritz E. Ein Beitrag zum Befall mit Endoparasiten und zum Nachweis von Benzimidazolresistenzen bei Magen-Darm-Strongyliden der Schafe in Niedersachsen [Dissertation]. Hannover: Tierärztliche Hochschule Hannover; 2005
    Suche in Google Scholar
  • 22 Perbix C. Die Resistenzlage von Magen-Darm-Strongyliden gegenüber Moxidectin in deutschen Schafherden [Dissertation]. Hannover: Tierärztliche Hochschule Hannover; 2008
    Suche in Google Scholar
  • 23 Scheuerle MC, Mahling M, Pfister K. Anthelminthic resistance of Haemonchus contortus in small ruminants in Switzerland and Southern Germany. Wien Klin Wochenschr 2009; 121: 46-49
    CrossrefPubMedSuche in Google Scholar
  • 24 Voigt K, Scheuerle M, Hamel D. Triple anthelmintic resistance in Trichostrongylus spp. in a German sheep flock. Small Rum Res 2012; 106: 30-32
    CrossrefPubMedSuche in Google Scholar
  • 25 Düvel S. Untersuchungen zum Vorkommen von Endoparasiten und zur Verbreitung anthelminthikaresistenter Strongylidenpopulationen in deutschen Ziegenherden [Dissertation]. Gießen: Justus-Liebig-Universität. 2016
    PubMedSuche in Google Scholar
  • 26 Springer A, Kloene P, Strube C. Benzimidazole resistant Haemonchus contortus in a wildlife park. Schweiz Arch Tierheilkd 2022; 164: 51-59
    CrossrefPubMedSuche in Google Scholar
  • 27 Kaplan RM. Biology, epidemiology, diagnosis, and management of anthelmintic resistance in gastrointestinal nematodes of livestock. Vet Clin Food Anim 2020; 36: 17-30
    CrossrefPubMedSuche in Google Scholar
  • 28 Charlier J, Bartley DJ, Sotiraki S. et al. Chapter Three – Anthelmintic resistance in ruminants: challenges and solutions. Adv Parasitol 2022; 115: 171-227
    CrossrefPubMedSuche in Google Scholar
  • 29 Coles GC, Bauer C, Borgsteede FHM. et al. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol. 1992; 44: 35-44
    CrossrefPubMedSuche in Google Scholar
  • 30 Coles GC, Jackson F, Pomroy WE. et al. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 2006; 136: 167-185
    CrossrefPubMedSuche in Google Scholar
  • 31 Morgan ER, Lanusse C, Rinaldi L. et al. Confounding factors affecting faecal egg count reduction as a measure of anthelmintic efficacy. Parasite 2022; 29: 20
    CrossrefPubMedSuche in Google Scholar
  • 32 Voigt K, Geiger M, Jäger MC. et al. Effectiveness of anthelmintic treatments in small ruminants in Germany. Animals 2022; 12: 1501
    CrossrefPubMedSuche in Google Scholar
  • 33 Hinney B, Schoiswohl J, Melville L. et al. High frequency of benzimidazole resistance alleles in trichostrongyloids from Austrian sheep flocks in an alpine transhumance management system. BMC Vet Res 2020; 16: 132
    CrossrefPubMedSuche in Google Scholar
  • 34 Untersweg F, Ferner V, Wiedermann S. et al. Multispecific resistance of sheep trichostrongylids in Austria. Parasite 2021; 28: 50
    CrossrefPubMedSuche in Google Scholar
  • 35 van den Brom R, Moll L, Kappert C. et al. Haemonchus contortus resistance to monepantel in sheep. Vet Parasitol 2015; 209: 278-280
    CrossrefPubMedSuche in Google Scholar
  • 36 Ploeger HW, Everts RR. Alarming levels of anthelmintic resistance against gastrointestinal nematodes in sheep in the Netherlands. Vet Parasitol 2018; 262: 11-15
    CrossrefPubMedSuche in Google Scholar
  • 37 Claerebout E, De Wilde N, Van Mael E. et al. Anthelmintic resistance and common worm control practices in sheep farms in Flanders, Belgium. Vet Parasitol Reg Stud Reports 2020; 20: 100393
    CrossrefPubMedSuche in Google Scholar
  • 38 Bordes L, Dumont N, Lespine A. et al. First report of multiple resistance to eprinomectin and benzimidazole in Haemonchus contortus on a dairy goat farm in France. Parasitol Int 2020; 76: 102063
    CrossrefPubMedSuche in Google Scholar
  • 39 Geurden T, Hoste H, Jacquiet P. et al. Anthelmintic resistance and multidrug resistance in sheep gastro-intestinal nematodes in France, Greece and Italy. Vet Parasitol 2014; 201: 59-66
    CrossrefPubMedSuche in Google Scholar
  • 40 Paraud C, Marcotty T, Lespine A. et al. Cross-resistance to moxidectin and ivermectin on a meat sheep farm in France. Vet Parasitol 2016; 226: 88-92
    CrossrefPubMedSuche in Google Scholar
  • 41 Schnyder M, Torgerson PR, Schönmann M. et al. Multiple anthelmintic resistance in Haemonchus contortus isolated from South African Boer goats in Switzerland. Vet Parasitol 2005; 128: 285-290
    CrossrefPubMedSuche in Google Scholar
  • 42 Murri S, Knubben-Schweizer G, Torgerson P. et al. Frequency of eprinomectin resistance in gastrointestinal nematodes of goats in canton Berne, Switzerland. Vet Parasitol 2014; 203: 114-119
    CrossrefPubMedSuche in Google Scholar
  • 43 Vadlejch J, Kyriánová IA, Várady M. et al. Resistance of strongylid nematodes to anthelmintic drugs and driving factors at Czech goat farms. BMC Vet Res 2021; 17: 106
    CrossrefPubMedSuche in Google Scholar
  • 44 Mickiewicz M, Czopowicz M, Kawecka-Grochocka E. et al. The first report of multidrug resistance in gastrointestinal nematodes in goat population in Poland. BMC Vet Res 2020; 16: 270
    CrossrefPubMedSuche in Google Scholar
  • 45 Mickiewicz M, Czopowicz M, Moroz A. et al. Prevalence of anthelmintic resistance of gastrointestinal nematodes in Polish goat herds assessed by the larval development test. BMC Vet Res 2021; 17: 19
    CrossrefPubMedSuche in Google Scholar
  • 46 Holm SA, Sörensen CR, Thamsborg SM. et al. Gastrointestinal nematodes and anthelmintic resistance in Danish goat herds. Parasite 2014; 21: 37
    CrossrefPubMedSuche in Google Scholar
  • 47 Peña- Espinoza M, Thamsborg SM, Demeler J. et al. Field efficacy of four anthelmintics and confirmation of drug-resistant nematodes by controlled efficacy test and pyrosequencing on a sheep and goat farm in Denmark. Vet Parasitol 2014; 206: 208-215
    CrossrefPubMedSuche in Google Scholar
  • 48 Martínez-Valladares M, Martínez-Pérez JM, Robles-Pérez D. et al. The present status of anthelmintic resistance in gastrointestinal nematode infections of sheep in the northwest of Spain by in vivo and in vitro techniques. Vet Parasitol 2013; 191: 177-181
    CrossrefPubMedSuche in Google Scholar
  • 49 Keegan JD, Keane OM, Good B. et al. A nationwide survey of anthelmintic treatment failure on sheep farms in Ireland. Irish Vet J 2017; 70: 7
    CrossrefPubMedSuche in Google Scholar
  • 50 Bull K, Glover MJ, Rose Vineer H. et al. Increasing resistance to multiple anthelmintic classes in gastrointestinal nematodes on sheep farms in southwest England. Vet Rec 2022; 190: e1531
    CrossrefPubMedSuche in Google Scholar
  • 51 Höglund J, Baltrušis P, Enweji N. et al. Signs of multiple anthelmintic resistance in sheep gastrointestinal nematodes in Sweden. Vet Parasitol Reg Stud Reports 2022; 36: 100789
    CrossrefPubMedSuche in Google Scholar
  • 52 Hamer K, Bartley D, Jennings A. et al. Lack of efficacy of monepantel against trichostrongyle nematodes in a UK sheep flock. Vet Parasitol 2018; 257: 48-53
    CrossrefPubMedSuche in Google Scholar
  • 53 Höglund J, Enweji N, Gustafsson K. First case of monepantel resistant nematodes of sheep in Sweden. Vet Parasitol Reg Stud Reports 2020; 22: 100479
    CrossrefPubMedSuche in Google Scholar
  • 54 Messer PW, Petrov DA. Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol Evol 2013; 28: 659-669
    CrossrefPubMedSuche in Google Scholar
  • 55 Redman E, Whitelaw F, Tait A. et al. The emergence of resistance to the benzimidazole anthelmintics in parasitic nematodes of livestock Is characterised by multiple independent hard and soft selective sweeps. PLoS Negl Trop Dis 2015; 9: e0003494
    CrossrefPubMedSuche in Google Scholar
  • 56 Le Jambre LF, Gill JH, Lenane IJ. et al. Inheritance of avermectin resistance in Haemonchus contortus . Int J Parasitol 2000; 30: 105-111
    CrossrefPubMedSuche in Google Scholar
  • 57 Martin PJ, McKenzie JA. Levamisole resistance in Trichostrongylus colubriformis: A sex-linked recessive character. Int J Parasitol 1990; 20: 867-872
    CrossrefPubMedSuche in Google Scholar
  • 58 Wolstenholme AJ, Fairweather I, Prichard R. et al. Drug resistance in veterinary helminths. Trends Parasitol 2004; 20: 469-476
    CrossrefPubMedSuche in Google Scholar
  • 59 Falzon LC, O’Neill TJ, Menzies PI. et al. A systematic review and meta-analysis of factors associated with anthelmintic resistance in sheep. Prev Vet Med 2014; 117: 388-402
    CrossrefPubMedSuche in Google Scholar
  • 60 Leathwick DM, Luo D. Managing anthelmintic resistance—Variability in the dose of drug reaching the target worms influences selection for resistance?. Vet Parasitol 2017; 243: 29-35
    CrossrefPubMedSuche in Google Scholar
  • 61 Niciura SCM, Cruvinel GG, Moraes CV. et al. In vivo selection for Haemonchus contortus resistance to monepantel. J Helminthol 2020; 94: e46
    CrossrefPubMedSuche in Google Scholar
  • 62 Stubbings L, Bartley D, Busin V et al. Sustainable control of parasites in sheep, SCOPS Technical Manual 2020. Im Internet: https://www.scops.org.uk/advisers-technical-info/(Stand 28.1.2023) doi:10.17605/OSF.IO/SQA4E
    PubMed
  • 63 van Wyk JA. Refugia – overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort J Vet Res 2001; 68: 55-67
    PubMedSuche in Google Scholar
  • 64 Besier RB. Refugia-based strategies for sustainable worm control: factors affecting the acceptability to sheep and goat owners. Vet Parasitol 2012; 186: 2-9
    CrossrefPubMedSuche in Google Scholar
  • 65 Kenyon F, McBean D, Greer AW. et al. A comparative study of the effects of four treatment regimes on ivermectin efficacy, body weight and pasture contamination in lambs naturally infected with gastrointestinal nematodes in Scotland. Int J Parasitol Drugs Drug Resist 2013; 3: 77-84
    CrossrefPubMedSuche in Google Scholar
  • 66 Bath GF, van Wyk JA. The Five Point Check© for targeted selective treatment of internal parasites in small ruminants. Small Rum Res 2009; 86: 6-13
    CrossrefPubMedSuche in Google Scholar
  • 67 Waghorn TS, Leathwick DM, Miller CM. et al. Brave or gullible: testing the concept that leaving susceptible parasites in refugia will slow the development of anthelmintic resistance. NZ Vet J 2008; 56: 158-163
    CrossrefPubMedSuche in Google Scholar
  • 68 Charlier J, Morgan ER, Rinaldi L. et al. Practices to optimise gastrointestinal nematode control on sheep, goat and cattle farms in Europe using targeted (selective) treatments. Vet Rec 2014; 250-255
    CrossrefPubMedSuche in Google Scholar
  • 69 van Wyk JA, Bath GF. The FAMACHA© system for managing haemonchosis in sheep and goats by clinically identifying individual animals for treatment. Vet Res 2002; 33: 509-529
    CrossrefPubMedSuche in Google Scholar
  • 70 Kenyon F, Greer AW, Coles GC. et al. The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Vet Parasitol 2009; 164: 3-11
    CrossrefPubMedSuche in Google Scholar
  • 71 Voigt K, Jaggy S, Scheuerle M. et al. Application of a clinical score for targeted selective treatment failed to identify goats with high strongylid egg excretion. Berl Munch Tierarztl Wochenschr 2019; 132: 166-177
    CrossrefPubMedSuche in Google Scholar
  • 72 Gilleard JS, Kotze AC, Leathwick D. et al. A journey through 50 years of research relevant to the control of gastrointestinal nematodes in ruminant livestock and thoughts on future directions. Int J Parasitol 2021; 51: 1133-1151
    CrossrefPubMedSuche in Google Scholar