Eprinomectin and levamisole action on gastrointestinal nematodes in a Mexican dairy goat production system

Main Article Content

Laura González-Reyes
Yesmín María Domínguez-Hernández
Cintli Martínez Ortiz de Montellano

Abstract

The effectiveness of eprinomectin and levamisole was evaluated in a dairy goat herd in El Bajío with a history of multi-resistance to fenbendazole (0 %) and ivermectin (70 %) using the Fecal Egg Count Reduction Test. Larval cultures were used to assess the epidemiology of the disease. Thirty goats with ≥ 150 eggs per gram (EPG) and no anthelmintic treatment for ≥ 60 days were selected. The modified McMaster technique (sensitivity: 50 EPG) was used to quantify the parasite burden. Three groups (n = 10) were weighed and treated: eprinomectin (0.5 mg/kg, topical), levamisole (12 mg/kg, subcutaneous), and an untreated control. The effectiveness of eprinomectin was 65 %, while that of levamisole was 100 %. Trichostrongylus spp. (90–100 %) and Oesophagostomum sp. (10 %) were identified. The reduced effectiveness of eprinomectin may be linked to ivermectin resistance. Multidrug resistance in small ruminants highlights the urgent need for targeted selective treatments and integrated parasite management to preserve effective anthelmintics.

Keywords:
Anthelmintic efficacy, Gastrointestinal nematodes, Eprinomectin, Levamisole, Dairy goat production systems, Parasite control in goats

Article Details

Author Biography

Cintli Martínez Ortiz de Montellano, Universidad Nacional Autónoma de México. Facultad de Medicina Veterinaria y Zootecnia. Departamento de Parasitología. Ciudad de México, México.

MVZ, MC (Salud Animal), PhD (Patología, Nutrición, Parasitología), Certificada por CONCERVET (Parasitología)

References

Piña-Martínez R, Martínez-Ortiz-de-Montellano C, Márquez-Mota CC, Dantán-González E. Integrative view of diseases in ruminants: towards a holistic model. 2025(Feb);20(1):0015. doi.org/10.1079/cabireviews.2025.0015.

Miller JE, Kaplan RM, Pugh DG. Internal parasites. In: DG Pugh, AN Baird, editors. Sheep and Goat Medicine. 2nd edition. St. Louis, Missouri, US: Elsevier; 2002. pp. 106–125. DOI: https://doi.org/10.1016/B978-1-4377-2353-3.10006-X

Bowman DD. Georgi. Parasitología para veterinarios. 11th edition. Barcelona, SP: Elsevier Health Sciences; 2022.

Torres-Acosta JFJ, Mendoza-de-Gives P, Aguilar-Caballero AJ, Cuéllar-Ordaz JA. Anthelmintic resistance in sheep farms: update of the situation in the American continent. Veterinary Parasitology. 2012;189(1),89–96. doi.org/10.1016/j.vetpar.2012.03.037. DOI: https://doi.org/10.1016/j.vetpar.2012.03.037

Zajac AM, Garza J. Biology, epidemiology, and control of gastrointestinal nematodes of small ruminants. Veterinary Clinics of North America: Food Animal Practice. 2020;36(1):73–87. DOI: https://doi.org/10.1016/j.cvfa.2019.12.005

Kaplan RM. Biology, epidemiology, diagnosis, and management of anthelmintic resistance in gastrointestinal nematodes of livestock. Veterinary Clinics of North America: Food Animal Practice. 2020;36(1):17–30. doi.org/10.1016/j.cvfa.2019.12.001. DOI: https://doi.org/10.1016/j.cvfa.2019.12.001

Shoop WL, Egerton JR, Eary CH, Haines HW, Michael BF, Mrozik H, et al. Eprinomectin: a novel avermectin for use as a topical endectocide for cattle. International Journal for Parasitology. 1996(Nov);26(11):1237–1242. doi.org/10.1016/s0020-7519(96)00122-1. DOI: https://doi.org/10.1016/S0020-7519(96)00123-3

Lespine A, Sutra JF, Dupuy J, Alvinerie M. Eprinomectin in goat: assessment of subcutaneous administration. Parasitology Research. 2003(Jan);89(2):120–122. doi.org/10.1007/s00436-002-0727-z. DOI: https://doi.org/10.1007/s00436-002-0727-z

Modi CM, Modi SK, Patel HB. The pharmacokinetics of eprinomectin in sheep following subcutaneous administration. Veterinarski Arhiv. 2014;84(4):347–354.

Rostang A, Devos J, Chartier C. Review of the eprinomectin effective doses required for dairy goats: where do we go from here? Veterinary Parasitology. 2020;277:108992. doi.org/10.1016/j.vetpar.2019.108992. DOI: https://doi.org/10.1016/j.vetpar.2019.108992

Ménez C, Alberich M, Kansoh D, Blanchard A, Lespine A. Acquired tolerance to ivermectin and moxidectin after drug selection pressure in the nematode Caenorhabditis elegans. Antimicrobial Agents and Chemotherapy. 2016;60(8):4809–4819. doi.org/10.1128/AAC.00713-16. DOI: https://doi.org/10.1128/AAC.00713-16

Torres-Acosta JF, Villarroel-Álvarez MS, Rodríguez-Arévalo F, Gutiérrez-Segura I, Alonso-Díaz MA. Diagnosis of gastrointestinal nematodes resistant to bencimidazols and imidazothiazols in a goat herd in Yucatan, México. Revista Biomédica. 2003;14(2):75–81. DOI: https://doi.org/10.32776/revbiomed.v14i2.344

Torres-Acosta JF, Aguilar-Caballero AJ, le Bigot C, Hoste H, Canul-Ku HL, Santos-Ricalde R, et al. Comparing different formulae to test for gastrointestinal nematode resistance to benzimidazoles in smallholder goat farms in Mexico. Veterinary Parasitology. 2005;134(3–4):241–248. doi.org/10.1016/j.vetpar.2005.07.012. DOI: https://doi.org/10.1016/j.vetpar.2005.07.012

Aguilar XM, Arellano MEL, Prats VV, Hernández EL, de Gives PM. Resistencia antihelmíntica de nematodos gastroentéricos en ovinos a febendazol e ivermectina en la región noroeste del estado de Tlaxcala. Revista Mexicana de Ciencias Pecuarias. 2006;44(1):81–90.

Garduño RG, Hernández GT, Arellano MEL, de Gives PM. Resistencia antihelmíntica de nematodos parásitos en ovinos. Revista de Geografía Agrícola. 2012;(48–49):63–74. DOI: https://doi.org/10.5154/r.rga.2012.48-49.04

Medina P, Guevara F, La O M, Ojeda N, Reyes N. Resistencia antihelmíntica en ovinos: una revisión de informes del sureste de México y alternativas disponibles para el control de nematodos gastrointestinales. Pastos y Forrajes. 2014;37:257–263.

Muñoz-Vargas L, Zamora-Sanabria R, Hidalgo-Jara W. Animal welfare, stress and food safety. In: R García Pinillos, SM Huertas Canén, editors. One Welfare Animal Health and Welfare, Food Security and Sustainability. Wallingford, UK: CABI; 2023. pp. 62–88. DOI: https://doi.org/10.1079/9781789249507.0004

Organización Mundial de Sanidad Animal. Código Sanitario para los Animales Terrestres. WOAH; 2024. https://www.woah.org/es/lo-que-ofrecemos-normas/codigo-terrestre-acceso-en-linea/

Organización Mundial de Sanidad Animal. Uso responsable y prudente de los fármacos antihelmínticos para contribuir al control de la resistencia a antihelmínticos en las especies ganaderas herbívoras [PDF]. WOAH; 2022. https://www.woah.org/fileadmin/Home/esp/Health_standards/docs/pdf/Antihelminticos_2022.pdf

García Pinillos R, Huertas Canén SM. One Welfare Animal Health and Welfare, Food Security and Sustainability. Wallingford, UK: CABI; 2023. doi.org/ 10.1079/9781789249507.0000. DOI: https://doi.org/10.1079/9781789249507.0000

Karaer MC, Čebulj-Kadunc N, Snoj T. Stress in wildlife: comparison of the stress response among domestic, captive, and free-ranging animals. Frontiers in Veterinary Science. 2023;10:1167016. doi.org/ 10.3389/fvets.2023.1167016. DOI: https://doi.org/10.3389/fvets.2023.1167016

Instituto Nacional de Estadística y Geografía. Economía y Sectores Productivos. Ganadería. Aguascalientes, MX: 2020. https://www.inegi.org.mx/temas/ganaderia/

García E. Modificaciones al sistema de clasificación climática de Köppen. Mexico City, Mexico: Universidad Nacional Autónoma de México, Instituto de Geografía; 2004. 20 pp.

Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, et al. World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology. 1992;44:35–44. DOI: https://doi.org/10.1016/0304-4017(92)90141-U

Kaplan RM, Denwood MJ, Nielsen MK, Thamsborg SM, Torgerson PR, Gilleard JS, et al. World Association for the Advancement of Veterinary Parasitology (WAAVP) guideline for diagnosing anthelmintic resistance using the faecal egg count reduction test in ruminants, horses and swine. Veterinary Parasitology. 2023;318:109936. doi.org/10.1016/j.vetpar.2023.109936. DOI: https://doi.org/10.1016/j.vetpar.2023.109936

Bauer BU, Pomroy WE, Gueydon J, Gannac S, Scott I, Pfister K. Comparison of the FLOTAC technique with the McMaster method and the Baerman technique to determine counts of Dictyocaulus eckerti L1 and strongylid eggs in feces of red deer (Cervus elaphus). Parasitology Research. 2010;107(3):555–560. doi.org/10.1007/s00436-010-1918-4. DOI: https://doi.org/10.1007/s00436-010-1893-z

Corticelli B, Lai M. Ricerche sulla tecnica di coltura delle larve infestive degli strongili gastrointestinali del bovino. Acta Médica Veterinaria. 1963;9:347–357.

Van Wyk JA, Mayhew E. Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Onderstepoort Journal of Veterinary Research. 2013;80(1):1–14. doi.org/10.4102/ojvr.v80i1.539. DOI: https://doi.org/10.4102/ojvr.v80i1.539

Burke JM, Miller JE. Sustainable approaches to parasite control in ruminant livestock. Veterinary Clinics of North America: Food Animal Practice. 2020;36(1):89–107. doi.org/10.1016/j.cvfa.2019.11.007. DOI: https://doi.org/10.1016/j.cvfa.2019.11.007

Chartier C, Pors I, Sutra JF, Alvinerie M. Efficacy and pharmacokinetics of levamisole hydrochloride in goats with nematode infections. Veterinary Record. 2000;146(12):350–351. doi.org/10.1136/vr.146.12.350. DOI: https://doi.org/10.1136/vr.146.12.350

Murri S, Knubben-Schweizer G, Torgerson P, Hertzberg H. Frequency of eprinomectin resistance in gastrointestinal nematodes of goats in canton Berne, Switzerland. Veterinary Parasitology. 2014;203(1–2):114–119. doi.org/10.1016/j.vetpar.2014.02.052. DOI: https://doi.org/10.1016/j.vetpar.2014.02.052

Dey AR, Begum N, Anisuzzaman, Alim MA, Alam MZ. Multiple anthelmintic resistance in gastrointestinal nematodes of small ruminants in Bangladesh. Parasitology International. 2020;77:102105. doi.org/10.1016/j.parint.2020.102105. DOI: https://doi.org/10.1016/j.parint.2020.102105

Bordes L, Dumont N, Lespine A, Souil E, Sutra JF, Prévot F, et al. First report of multiple resistance to eprinomectin and benzimidazole in Haemonchus contortus on a dairy goat farm in France. Parasitology International. 2020;76:102063. doi.org/10.1016/j.parint.2020.102063. DOI: https://doi.org/10.1016/j.parint.2020.102063

Mickiewicz M, Czopowicz M, Kawecka-Grochocka E, Moroz A, Szaluś-Jordanow O, et al. The first report of multidrug resistance in gastrointestinal nematodes in goat population in Poland. BMC Veterinary Research. 2020;16(1):270. doi.org/10.1186/s12917-020-02501-5. DOI: https://doi.org/10.1186/s12917-020-02501-5

Chaparro JJ, Villar D, Zapata JD, López S, Howell SB, López A, et al. Multidrug resistant Haemonchus contortus in a sheep flock in Antioquia, Colombia. Veterinary Parasitology: Regional Studies and Reports. 2017;10:29–34. doi.org/10.1016/j.vprsr.2017.07.005. DOI: https://doi.org/10.1016/j.vprsr.2017.07.005

Arece-García J, López-Leyva Y, Olmedo-Juárez A, Ramírez-Vargas G, Reyes-Guerrero D, et al. First report of multiple anthelmintic resistance in goat farm in Cuba. Helminthologia. 2017;54(4):358–362. doi.org/10.1515/helm-2017-0037. DOI: https://doi.org/10.1515/helm-2017-0037

Rehbein S, Kellermann M, Wehner TA. Pharmacokinetics and anthelmintic efficacy of topical eprinomectin in goats prevented from grooming. Parasitology Research. 2014;113(11):4039–4044. doi.org/10.1007/s00436-014-4072-9. DOI: https://doi.org/10.1007/s00436-014-4072-9

Hamel D, Visser M, Kellermann M, Kvaternick V, Rehbein S. Anthelmintic efficacy and pharmacokinetics of pour-on eprinomectin (1 mg/kg bodyweight) against gastrointestinal and pulmonary nematode infections in goats. Small Ruminant Research. 2015;127:74–79. doi.org/10.1016/j.smallrumres.2015.04.003. DOI: https://doi.org/10.1016/j.smallrumres.2015.04.003

Alvinerie M, Lacoste E, Sutra JF, Chartier C. Some pharmacokinetic parameters of eprinomectin in goats following pour-on administration. Veterinary Research Communications. 1999;23:449–455. DOI: https://doi.org/10.1023/A:1006373609314

De Souza Chagas AC, da Silva Vieira L, Rodrigues Aragão W, do Carmo Navarro AM, Vasques Villela LC. Anthelmintic action of eprinomectin in lactating Anglo-Nubian goats in Brazil. Parasitology Research. 2007;100(2):391–394. doi.org/10.1007/s00436-006-0316-7. DOI: https://doi.org/10.1007/s00436-006-0316-7

Hinney B, Wiedermann S, Kaiser W, Krücken J, Joachim A. Eprinomectin and moxidectin resistance of trichostrongyloids on a goat farm in Austria. Pathogens. 2022;11(5):498. doi.org/10.3390/pathogens11050498. DOI: https://doi.org/10.3390/pathogens11050498

Nielsen P, Rasmussen F. Pharmacokinetics of levamisole in goats and pigs. In: Y Ruckebusch, PL Toutain, GD Koritz, editors. Veterinary Pharmacology and Toxicology. Dordrecht: Springer Netherlands; 1983. pp. 241–244. DOI: https://doi.org/10.1007/978-94-009-6604-8_24

Dalvi RR. Pharmacology and toxicology of levamisole in domestic animals: a review. International Journal of Animal Sciences. 1990;5(1):15–19.

Oliveira CC, Costa DFL, Limeira CH, Nogueira DB, Nascimento BHR, Vaz AFM. Anthelmintic intoxication in goats and sheep: a systematic review. Research in Veterinary Science. 2022;152:657–662. doi.org/10.1016/j.rvsc.2022.09.038. DOI: https://doi.org/10.1016/j.rvsc.2022.09.038

Food Animal Residue Avoidance and Databank. 2025. https://www.farad.org

Olivas-Salazar R, Estrada-Angulo A, Mellado M, Aguilar-Caballero AJ, Castro-Pérez BI, et al. Prevalence of gastrointestinal nematode infections in goat flocks on semi-arid rangelands of northeastern Mexico. Tropical Animal Health and Production. 2018;50:807–813. DOI: https://doi.org/10.1007/s11250-017-1499-x

Olivas-Salazar R, Aguilar-Caballero AJ, Estrada-Angulo A, Mellado M, Castro-Pérez BI, et al. Factors associated to gastrointestinal nematodes infections in dairy goats grazing on semi-arid rangelands of northeastern Mexico. Tropical and Subtropical Agroecosystems. 2019;22(3):585–594. DOI: https://doi.org/10.56369/tsaes.2804

Zajac AM, Gipson TA. Multiple anthelmintic resistance in goat herd. Veterinary Parasitology. 2000;87:163–172. doi.org/10.1016/s0304-4017(99)00174-0. PMID: 10622608. DOI: https://doi.org/10.1016/S0304-4017(99)00174-0

Almeida FA, García KC, Torgerson PR, Amarante AF. Multiple resistance to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International. 2010;59(4):622–625. doi.org/10.1016/j.parint.2010.09.006. DOI: https://doi.org/10.1016/j.parint.2010.09.006

Martínez-Ortiz-de-Montellano C, Torres-Acosta JFDJ, Ojeda-Robertos NF, González-Reyes L, Maldonado-Marín SA. Manejo integrado de parásitos en pequeños rumiantes. Bioagrociencias. 2022;15(2):4463. doi.org/10.56369/BAC.4463 DOI: https://doi.org/10.56369/BAC.4463