Efficacy of the main anthelmintics used in the control of bovine flukes in warm and humid climate in Mexico
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Abstract
Fasciola hepatica and paramphistomids are common endoparasites in cattle. Chemical control is the main method to avoid the effects of both trematodes on herd health. This study aimed to evaluate the efficacy of the most commonly used anthelmintics against trematodes (paramphistomids and F. hepatica) in cattle raised in a warm climate in Mexico. Fecal samples were obtained from 393 cows that were naturally infected with F. hepatica and paramphistomids. The fecal egg count was determined using the sedimentation technique, recording the eggs per gram of feces (EPG). Only trematode-positive cows were used to assess anthelmintics such as nitroxynil (NITROX), triclabendazole (TCBZ), fenbendazole (FBZ), rafoxanide (RAFOX), albendazole (ABZ) and oxyclozanide (OCZ). Efficacy was determined following the WAAVP guidelines; samples were taken 15 days post-treatment to perform the fecal egg count reduction test (FECRT). According to FECRT, the efficacy of anthelmintics was 0–83.3% against paramphistomids and 51.8%–100% against F. hepatica. The most effective anthelmintics against F. hepatica were NITROX (89–100%) and RAFOX (93–100%). Triclabendazole in all its combinations (TCBZ + FBZ and ABZ) had lower efficacy in controlling paramphistomids (0–39%), but high efficacy against F. hepatica (59-73%). Most anthelmintics were effective against F. hepatica; however, control alternatives for paramphistomids require further investigation.
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References
Abdel Fatah, O. R., Arafa, W. M., Wahba, A. A. & El Dakhly, K. M. (2022). Tegumental alterations and resistance of Fasciola gigantica adult worms exposed to flukicides in Egypt. Beni-Suef University Journal of Basic and Applied Sciences, 11, 106. https://doi.org/10.1186/s43088-022-00287-z
Arias, M. S., Sanchís, J., Francisco, I., Francisco, R., Piñeiro, P., Cazapal-Monteiro, C., Cortiñas, F. J., Suárez, J. L., Sánchez-Andrade, R. & Paz-Silva, A. (2013). The efficacy of four anthelmintics against Calicophoron daubneyi in naturally infected dairy cattle. Veterinary Parasitology, 197(1–2), 126–129. https://doi.org/10.1016/j.vetpar.2013.06.011
Castro-Trejo, L., Garcja-Vasquez, Z. & Casildo-Nieto, J. (1990). The Susceptibility of Lymnaeid Snails to Paramphistomum cervi Infections in Mexico. Veterinary Parasitology, 35(1-2), 157-161. https://doi.org/10.1016/0304-4017(90)90125-U
Červená, B., Anettová, L., Nosková, E., Pafčo, B., Pšenková, I., Javorská, K., Příhodová, P., Ježková, J., Václavek, P., Malát, K. & Modrý, D. (2022). The winner takes it all: dominance of Calicophoron daubneyi (Digenea: Paramphistomidae) among flukes in Central European beef cattle. Parasitology, 149(5), 612-621. https://doi.org/10.1017/S0031182021002158
Dobson, R. J., Hosking, B. C., Jacobson, C. L., Cotter, J. L., Besier, R. B., Stein, P. A. & Reid, S. A. (2012). Preserving new anthelmintics: A simple method for estimating faecal egg count reduction test (FECRT) confidence limits when efficacy and/or nematode aggregation is high. Veterinary Parasitology, 186(1–2), 79–92. https://doi.org/10.1016/j.vetpar.2011.11.049
Elelu, N. & Eisler, M. C. (2018). A review of bovine fasciolosis and other trematode infections in Nigeria. Journal of Helminthology, 92(2), 128–141. https://doi.org/10.1017/S0022149X17000402
Fairweather, I. (2011). Reducing the future threat from (liver) fluke: Realistic prospect or quixotic fantasy? Veterinary Parasitology, 180(1–2), 133–143. https://doi.org/10.1016/j.vetpar.2011.05.034
Fang, W., Yang, J., Wang, H. Y., Chen, S. R., Li, K. R., Liu, Y. H., Duan, Y. & Li, T. M. (2022). Exploration of animal models to study the life cycle of Fasciola hepatica. Parasitology, 149(10), 1349–1355. https://doi.org/10.1017/S0031182022000609
Fenemore, C., Floyd, T. & Mitchell, S. (2021). Rumen Fluke in Great Britain. Journal of Comparative Pathology, 184, 31–36. https://doi.org/10.1016/j.jcpa.2021.01.012
Forstmaier, T., Knubben-Schweizer, G., Strube, C., Zablotski, Y. & Wenzel, C. (2021). Rumen (Calicophoron/paramphistomum spp.) and liver flukes (Fasciola hepatica) in cattle—prevalence, distribution, and impact of management factors in Germany. Animals, 11(9), 2727. https://doi.org/10.3390/ani11092727
González-Warleta, M., Lladosa, S., Castro-Hermida, J. A., Martínez-Ibeas, A. M., Conesa, D., Muñoz, F., López-Quílez, A., Manga-González, Y. & Mezo, M. (2013). Bovine paramphistomosis in Galicia (Spain): Prevalence, intensity, aetiology and geospatial distribution of the infection. Veterinary Parasitology, 191(3–4), 252–263. https://doi.org/10.1016/j.vetpar.2012.09.006
Hernández-Guzmán, K., Molina-Mendoza, P., Olivares-Pérez, J., Alcalá-Canto, Y., Olmedo-Juárez, A., Córdova-Izquierdo, A. & Villa-Mancera, A. (2021). Prevalence and seasonal variation of Fasciola hepatica in slaughtered cattle: the role of climate and environmental factors in Mexico. Journal of Helminthology, 95(e46), 1–8. https://doi.org/10.1017/S0022149X21000444
Hernández-Hernández, J. C., González-Garduño, R., Ortiz-Pérez, D. O., Villa-Mancera, A., Arias-Vázquez, M. S. & Paz-Silva, A. (2023). Prevalence of flukes (Fasciola hepatica and paramphistomids) in cattle in south-eastern Mexico. Helminthologia, 60(2), 141–151. https://doi.org/10.2478/helm-2023-0017
Hoyle, R. C., Rose Vineer, H., Duncan, J. S., Williams, D. J. L. & Hodgkinson, J. E. (2022). A survey of sheep and/or cattle farmers in the UK shows confusion over the diagnosis and control of rumen fluke and liver fluke. Veterinary Parasitology, 312, 109812. https://doi.org/10.1016/j.vetpar.2022.109812
Huson, K. M., Oliver, N. A. M. & Robinson, M. W. (2017). Paramphistomosis of Ruminants: An Emerging Parasitic Disease in Europe. Trends in Parasitology, 33(11), 836–844. https://doi.org/10.1016/j.pt.2017.07.002
Ico-Gómez, R., González-Garduño, R., Ortiz-Pérez, D., Mosqueda-Gualito, J. J., Flores-Santiago, E. D. J., Sosa-Pérez, G. & Salazar-Tapia, A. A. (2021). Assessment of anthelmintic effectiveness to control Fasciola hepatica and paramphistome mixed infection in cattle in the humid tropics of Mexico. Parasitology, 148(12), 1458-1466.https://doi.org/10.1017/S0031182021001153
Jiménez-Penago, G., González-Garduño, R., Torres-Hernández, G., Torres-Chablé, O. M., Ramírez-Bribiesca, E. & & David Hernández-Sánchez. (2023). Fasciola hepatica and Rumen Flukes-In Vitro Evaluation of Main Commercial Anthelmintics. Acta Scientiae Veterinariae, 51,1912. https://doi.org/10.22456/1679-9216.130294
Jones, R. A., Brophy, P. M., Mitchell, E. S. & Williams, H. W. (2017). Rumen fluke (Calicophoron daubneyi) on Welsh farms: Prevalence, risk factors and observations on co-infection with Fasciola hepatica. Parasitology, 144(2), 237–247. https://doi.org/10.1017/S0031182016001797
Kahl, A., von Samson-Himmelstjerna, G., Helm, C., Hodgkinson, J., Williams, D., Weiher, W., Terhalle, W., Steuber, S., Ganter, M. & Krücken, J. (2023). Efficacy of flukicides against Fasciola hepatica and first report of triclabendazole resistance on German sheep farms. International Journal for Parasitology: Drugs and Drug Resistance, 23, 94–105. https://doi.org/10.1016/j.ijpddr.2023.11.001
Kamaludeen, J., Graham-Brown, J., Stephens, N., Miller, J., Howell, A., Beesley, N. J., Hodgkinson, J., Learmount, J. & Williams, D. (2019). Lack of efficacy of triclabendazole against Fasciola hepatica is present on sheep farms in three regions of England, and Wales. Veterinary Record, 184(16), 502-502. https://doi.org/10.1136/vr.105209
Khedri, J., Radfar, M. H., Borji, H. & Mirzaei, M. (2015). Prevalence and Intensity of Paramphistomum Spp. In Cattle from South-Eastern Iran. Iranian Journal of Parasitology, 10(2), 268–272. PMCID: PMC4522303
Kouadio, J. N., Giovanoli Evack, J., Achi, L. Y., Balmer, O., Utzinger, J., N’Goran, E. K., Bonfoh, B., Hattendorf, J. & Zinsstag, J. (2021). Efficacy of triclabendazole and albendazole against Fasciola spp. infection in cattle in Côte d’Ivoire: a randomised blinded trial. Acta Tropica, 222, 106039. https://doi.org/10.1016/j.actatropica.2021.106039
Lovarelli, D., Bacenetti, J. & Guarino, M. (2020). A review on dairy cattle farming: Is precision livestock farming the compromise for an environmental, economic and social sustainable production? Journal of Cleaner Production, 262, 121409. https://doi.org/10.1016/j.jclepro.2020.121409
Mas-Coma, S., Buchon, P., Funatsu, I. R., Angles, R., Artigas, P., Valero, M. A. & Bargues, M. D. (2020). Sheep and Cattle Reservoirs in the Highest Human Fascioliasis Hyperendemic Area: Experimental Transmission Capacity, Field Epidemiology, and Control Within a One Health Initiative in Bolivia. Frontiers in Veterinary Science, 7. https://doi.org/10.3389/fvets.2020.583204
Moazeni, M. & Ahmadi, A. (2016). Controversial aspects of the life cycle of Fasciola hepatica. Experimental Parasitology, 169, 81–89. https://doi.org/10.1016/j.exppara.2016.07.010
Mostafa, W., Abdel-Rady, A., El-Dakroury, M. F. & Felefel, W. (2023). Field trials to evaluate five fasciolicides against natural liver fluke infection in cattle and sheep in Egypt. International Journal of Veterinary Science, 12(1), 76-81. https://doi.org/10.47278/journal.ijvs/2022.160
Novobilský, A. & Höglund, J. (2015). First report of closantel treatment failure against Fasciola hepatica in cattle. International Journal for Parasitology: Drugs and Drug Resistance, 5(3), 172–177. https://doi.org/10.1016/j.ijpddr.2015.07.003
Nzalawahe, J., Hannah, R., Kassuku, A. A., Stothard, J. R., Coles, G. & Eisler, M. C. (2018). Evaluating the effectiveness of trematocides against Fasciola gigantica and amphistomes infections in cattle, using faecal egg count reduction tests in Iringa Rural and Arumeru Districts, Tanzania. Parasites and Vectors, 11, 384. https://doi.org/10.1186/s13071-018-2965-7
Olsen, A., Frankena, K., Bødker, R., Toft, N., Thamsborg, S. M., Enemark, H. L. & Halasa, T. (2015). Prevalence, risk factors and spatial analysis of liver fluke infections in Danish cattle herds. Parasites and Vectors, 8, 160. https://doi.org/10.1186/s13071-015-0773-x
Omran, E. & Ahmad, N. (2015). Effect of nitroxynil (fasciolid) on adult Fasciola gigantica and Fasciola hepatica in infected cows. Parasitologists United Journal, 8(2), 107. https://doi.org/10.4103/1687-7942.175008
Ortiz, P., Scarcella, S., Cerna, C., Rosales, C., Cabrera, M., Guzmán, M., Lamenza, P. & Solana, H. (2013). Resistance of Fasciola hepatica against Triclabendazole in cattle in Cajamarca (Peru): A clinical trial and an in vivo efficacy test in sheep. Veterinary Parasitology, 195(1–2), 118–121. https://doi.org/10.1016/j.vetpar.2013.01.001
Paraud, C., Gaudin, C., Pors, I. & Chartier, C. (2009). Efficacy of oxyclozanide against the rumen fluke Calicophoron daubneyi in experimentally infected goats. Veterinary Journal, 180(2), 265–267. https://doi.org/10.1016/j.tvjl.2008.01.002
Rangel-Ruiz, L. J., Albores-Brahms, S. T. & Gamboa-Aguilar, J. (2003). Seasonal trends of Paramphistomum cervi in Tabasco, Mexico. Veterinary Parasitology, 116(3), 217–222. https://doi.org/10.1016/j.vetpar.2003.07.002
Rapic, D., Dzakula, N., Sakar, D. & Richards, R. (1988). Comparative efficacy of triclabendazole, nitroxynil and rafoxanide against immature and mature Fasciola hepatica in naturally infected cattle. Veterinary Record, 122(3), 59–62. https://doi.org/10.1136/vr.122.3.59
Rashid, M., Rashid, M. I., Akbar, H., Ahmad, L., Hassan, M. A., Ashraf, K., Saeed, K. & Gharbi, M. (2019). A systematic review on modelling approaches for economic losses studies caused by parasites and their associated diseases in cattle. Parasitology, 146(2), 129–141. https://doi.org/10.1017/S0031182018001282
Rodríguez-Vivas, R. I., Grisi, L., De León, A. A. P., Villela, H. S., De Jesús Torres-Acostaa, J. F., Sánchez, H. F., Salas, D. R., Cruz, R. R., Saldierna, F. & Carrasco, D. G. (2017). Potential economic impact assessment for cattle parasites in Mexico. Review. Revista Mexicana De Ciencias Pecuarias, 8(1), 61–74. https://doi.org/10.22319/rmcp.v8i1.4305
Romero, J., Villaguala, C., Quiroz, F., Landaeta-Aqueveque, C., Alfaro, G. & Pérez Fernández, R. (2019). Flukicide efficacy against Fasciola hepatica of Triclabendazole and Nitroxynil in cattle of the central valley of Chile. Revista Brasileira de Parasitologia Veterinaria, 28(1), 164–167. https://doi.org/10.1590/s1984-296120180089
Sabourin, E., Alda, P., Vázquez, A., Hurtrez-Boussès, S. & Vittecoq, M. (2018). Impact of Human Activities on Fasciolosis Transmission. Trends in Parasitology, 34(10), 891–903. https://doi.org/10.1016/j.pt.2018.08.004
SAS. (2017). SAS/STAT User´s Guide (S. Inst., Ed.; Release 6.).
Shokier, K. M., Aboelhadid, S. M. & Waleed, M. A. (2013). Efficacy of five anthelmintics against a natural Fasciola species infection in cattle. Beni-Suef University Journal of Basic and Applied Sciences, 2(1), 41–45. https://doi.org/10.1016/j.bjbas.2013.09.006
SIAP. (2021). Servicio de Información Agroalimentaria y Pesquera. Información Estadística. http://nube.siap.gob.mx/cierre_pecuario/
Soca-Pérez, M., Giupponi-Cardoso, P., López-Vigoa, O., Sanavria, A. & Labrada-Vázquez, A. (2016). Prevalence of Fasciola hepatica in grazing cows during the dry season. Pastos y Forrajes, 39(4), 263–267.
Thanasuwan, S., Piratae, S. & Tankrathok, A. (2021). Prevalence of gastrointestinal parasites in cattle in Kalasin Province, Thailand. Veterinary World, 14(8), 2091–2096. https://doi.org/10.14202/vetworld.2021.2091-2096
Ticona, D., Chávez, A., Casas, G., Chavera, A. & Li, O. (2010). Prevalencia de Fasciola hepatica en bovinos y ovinos de Vilcashuamán, Ayacucho. Revista de Investigaciones Veterinarias del Perú, 21(2), 168–174.
Titi, A., Mekroud, A., El Hadi Chibat, M., Boucheikhchoukh, M., Zein-Eddine, R., Djuikwo-Teukeng, F. F., Vignoles, P., Rondelaud, D. & Dreyfuss, G. (2014). Ruminal paramphistomosis in cattle from northeastern Algeria: Prevalence, parasite burdens and species identification. Parasite, 21, 50. https://doi.org/10.1051/parasite/2014041
Villa-Mancera, A. & Reynoso-Palomar, A. (2019). High prevalence, potential economic impact, and risk factors of Fasciola hepatica in dairy herds in tropical, dry and temperate climate regions in Mexico. Acta Tropica, 193, 169–175. https://doi.org/10.1016/j.actatropica.2019.03.005
Zárate-Rendón, D. A., Briones-Montero, A., Huaraca-Oré, N. A., Veirano, G. S., Levecke, B. & Geldhof, P. (2023). Comparison of the therapeutic efficacy of five anthelmintics against natural Fasciola hepatica infections in dairy cattle from the Mantaro Valley, Peru. Veterinary Parasitology: Regional Studies and Reports, 38, 1008027. https://doi.org/10.1016/j.vprsr.2022.100827