Resistência anti-helmíntica em nematódeos gastrintestinais de bovinos no Brasil e Argentina - situação atual e perspectivas globais

Borges, Fernando de Almeida; Amarante, Alessandro Francisco Talamini do; Lopes, Welber Daniel Zaneti; Canton, Candela; Alvarez, Luis; Lifschitz, Adrian

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Brasil

Revista Brasileira de Parasitologia Veterinária

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Brasil

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Sumário

Review Article • Rev. Bras. Parasitol. Vet. 33 (3) • 2024 • https://doi.org/10.1590/S1984-29612024041 copiar

Resistência anti-helmíntica em nematódeos gastrintestinais de bovinos no Brasil e Argentina - situação atual e perspectivas globais

Autoria SCIMAGO INSTITUTIONS RANKINGS

Resumo

Esta revisão tem como objetivo delinear o estado atual da resistência anti-helmíntica (RAH) em nematódeos gastrintestinais (NGIs), em bovinos na Argentina e no Brasil, enfatizando o impacto econômico na saúde e no bem-estar animal. A análise explora fatores associados à RAH e propõe uma solução potencial: o uso de combinações de medicamentos. Ambos os países enfrentam um cenário grave de AHR, progredindo por meio de fases incipientes, estabelecidas e avançadas, levando a casos extremos de mortalidade animal, devido a estratégias de controle ineficazes. Os gêneros Cooperia e Haemonchus apresentam mais relatos de resistência, enquanto Oesophagostomum radiatum também pode causar problemas significativos. Embora os benzimidazóis orais e o levamisol permaneçam eficazes na maioria dos rebanhos, a moxidectina está entrando em uma fase avançada de resistência, e as avermectinas são cada vez mais consideradas ineficazes. A revisão explora o impacto do clima, pastoreio misto, movimentação dos animais, práticas de criação e a relação entre o controle dos ectoparasitas e o surgimento de helmintos resistentes. Notavelmente, o uso estratégico de combinações de medicamentos pode ser uma abordagem valiosa para o controle de NGIs resistentes em bovinos, destacando-se o seu potencial significativo na mitigação dos desafios colocados pela RAH naqueles países.

Palavras-chave:
Cooperia; Haemonchus; manejo na pecuária; combinação de drogas; saúde de bovinos

Year	Country	Diagnostic Method	Drugs	Species/Genus						Other relevant results	Reference
				C	H	N	Oe	Os	T
1990	BR	Necropsy	BZDs		X					T, Os and C were susceptible	Pinheiro & Echevarria (1990)Pinheiro AC, Echevarria FAM. Susceptibilidade de Haemonchus spp. em bovinos ao tratamento anti-helmíntico com albendazole e oxfendazole. Pesq Vet Bras 1990; 10(1-2): 19-21.
2001	BR	LDA	IVM	X							Paiva et al. (2001)Paiva F, Sato MO, Acuna AH, Jensen JR, Bressan MCRV. Resistência a ivermectina constatada em Haemonchus placei e Cooperia punctata em bovinos. Hora Vet 2001; 20: 29-32.
2001	AR	FECRT and necropsy	IVM, LA-IVM, DRM, MOX	X							Anziani et al. (2001)Anziani OS, Zimmermann G, Guglielmone AA, Vazquez R, Suarez V. Avermectin resistance in Cooperia pectinata in cattle in Argentina. Vet Rec 2001; 149(2): 58-59. http://doi.org/10.1136/vr.149.2.58. PMid:11488345. http://doi.org/10.1136/vr.149.2.58...
2001	AR	FECRT and necropsy	IVM, LA-IVM, DRM,	X						MOX and FBZ: efficacy >95%.	Fiel et al. (2001)Fiel CA, Saumell CA, Steffan PE, Rodriguez EM. Resistance of Cooperia to ivermectin treatments in grazing cattle of the Humid Pampa, Argentina. Vet Parasitol 2001; 97(3): 211-217. http://doi.org/10.1016/S0304-4017(01)00407-1. PMid:11390073. http://doi.org/10.1016/S0304-4017(01)004...
2003	AR	FECRT and necropsy	IVM and BZD	X	X			X			Mejía et al. (2003)Mejía ME, Fernández Igartúa BM, Schmidt EE, Cabaret J. Multispecies and multiple anthelmintic resistance on cattle nematodes in a farm in Argentina: the beginning of high resistance? Vet Res 2003; 34(4): 461-467. http://doi.org/10.1051/vetres:2003018. PMid:12911862. http://doi.org/10.1051/vetres:2003018...
2004	AR	FECRT	IVM and BZD	X	X					LEV: efficacy >95%	Anziani et al. (2004)Anziani OS, Suarez VH, Guglielmone AA, Warnke O, Grande H, Coles GC. Resistance to benzimidazole and macrocyclic lactone anthelmintics in cattle nematodes in Argentina. Vet Parasitol 2004; 122(4): 303-306. http://doi.org/10.1016/j.vetpar.2004.05.018. PMid:15262008. http://doi.org/10.1016/j.vetpar.2004.05....
2004	AR	FECRT	AVMs	X							Anziani & Fiel (2004)Anziani OS, Fiel CA. Estado actual de la resistência anti-helmíntica (nematodos gastrointestinaems) en bovinos de la Argentina. Vet Argent 2004; 21: 86-101.
2005	BR	FECRT	IVM and DRM		X					MOX and ABA: efficacy >99%	Rangel et al. (2005)Rangel VB, Leite RC, Oliveira PR, Santos EJ Jr. Resistência de Cooperia spp. e Haemonchus spp. às avermectinas em bovinos de corte. Arq Bras Med Vet Zootec 2005; 57(2): 186-190. http://doi.org/10.1590/S0102-09352005000200008. http://doi.org/10.1590/S0102-09352005000...
2006	BR	FECRT	IVM, ABA, DRM and MOX	X					X	H susceptible to ABA	Mello et al. (2006)Mello MHA, Depner R, Molento MB, Ferreira JJ. Resistência lateral às macrolactonas em nematodas de bovinos. Arch Vet Sci 2006; 11(1): 8-12. http://doi.org/10.5380/avs.v11i1.5628. http://doi.org/10.5380/avs.v11i1.5628...
2007	BR	FECRT	IVM, AS and LEV	X	X					25 farms. Percentage of farms with FECRT< 90%: IVM-92%, LEV-20%, AS-8%, MOX-0%	Soutello et al. (2007)Soutello RGV, Seno MC, Amarante AF. Anthelmintic resistance in cattle nematodes in northwestern São Paulo State, Brazil. Vet Parasitol 2007; 148(3-4): 360-364. http://doi.org/10.1016/j.vetpar.2007.06.023. PMid:17656022. http://doi.org/10.1016/j.vetpar.2007.06....
2007	AR	FECRT	IVM and BZD	X				X		25 farms. Percentage of farms with AHR: IVM-60%, FBZ-32%, LEV-0%.	Suarez & Cristel (2007)Suarez VH, Cristel SL. Anthelmintic resistance in cattle nematode in the western Pampeana Region of Argentina. Vet Parasitol 2007; 144(1-2): 111-117. http://doi.org/10.1016/j.vetpar.2006.09.016. PMid:17049746. http://doi.org/10.1016/j.vetpar.2006.09....
2008	BR	FECRT	IVM, AS and LEV	X	X					39 farms. Percentage of farms with AHR: IVM-82.1%, LEV-15.4% and AS-7.8%	Souza et al. (2008)Souza AP, Ramos CI, Bellato V, Sartor AP, Schelbauer CA. Resistência de helmintos gastrintestinais de bovinos a anti-helmínticos no Planalto Catarinense. Cienc Rural 2008; 38(5): 1363-1367. http://doi.org/10.1590/S0103-84782008000500026. http://doi.org/10.1590/S0103-84782008000...
2008	BR	Necropsy	IVM and DRM	X							Cardoso et al. (2008)Cardoso JMS, Martins IVF, Sant’anna FB, Correia TR, Tancredi IP, Coumendouros K, et al. Identification of ivermectin and doramectin-resistant Cooperia punctata (Linstow, 1907) in a dairy herd in the State of Rio de Janeiro, Brazil. Braz J Vet Res Anim Sci 2008; 45(Suppl.): 75-81. http://doi.org/10.11606/S1413-95962008000700010. http://doi.org/10.11606/S1413-9596200800...
2009	BR	Necropsy	MOX	X			X			H susceptible to MOX	Condi et al. (2009)Condi GK, Soutello RGV, Amarante AFT. Moxidectin-resistant nematodes in cattle in Brazil. Vet Parasitol 2009; 161(3-4): 213-217. http://doi.org/10.1016/j.vetpar.2009.01.031. PMid:19251366. http://doi.org/10.1016/j.vetpar.2009.01....
2009	BR	Necropsy	IVM and LA-IVM	X	X		X		X	High efficacy of Trichlorfon	Lopes et al. (2009)Lopes WDZ, Santos TR, Borges FA, Sakamoto CA, Soares VE, Costa GH, et al. Anthelmintic efficacy of oral trichlorfon solution against ivermectin resistant nematode strains in cattle. Vet Parasitol 2009; 166(1-2): 98-102. http://doi.org/10.1016/j.vetpar.2009.07.045. PMid:19709817. http://doi.org/10.1016/j.vetpar.2009.07....
2010	BR	FECRT	IVM, LA-IVM, ABA and DRM	X	X			X	X	Os was resistant only to IVM. MOX and SA: efficacy >95%	Cezar et al. (2010)Cezar AS, Vogel FSF, Sangioni LA, Antonello AM, Camillo G, Toscan G, et al. Ação anti-helmíntica de diferentes formulações de lactonas macrocíclicas em cepas resistentes de nematódeos de bovinos. Pesq Vet Bras 2010; 30(7): 523-528. http://doi.org/10.1590/S0100-736X2010000700002. http://doi.org/10.1590/S0100-736X2010000...
2010	BR	FECRT	IVM	X						MOX and SA: efficacy >95%	Soutello et al. (2010)Soutello RVG, Coelho WMD, Oliveira FP, Fonzar JF, Luquetti BC, Souza RFP, et al. Evaluation of reduction in egg shedding of gastrointestinal nematodes in cattle following administration of anthelmintics. Rev Bras Parasitol Vet 2010; 19(3): 183-185. http://doi.org/10.1590/S1984-29612010000300011. PMid:20943024. http://doi.org/10.1590/S1984-29612010000...
2010	AR	FECRT	IVM and MOX	X							Lifschitz et al. (2010)Lifschitz A, Suarez VH, Sallovitz J, Cristel SL, Imperiale F, Ahoussou S, et al. Cattle nematodes resistant to macrocyclic lactones: comparative effects of P-glycoprotein modulation on the efficacy and disposition kinetics of ivermectin and moxidectin. Exp Parasitol 2010; 125(2): 172-178. http://doi.org/10.1016/j.exppara.2010.01.009. PMid:20109455. http://doi.org/10.1016/j.exppara.2010.01...
2011	BR	FECRT	IVM, LA-IVM, AS, ABA and DRM	X	X					High frequency of treatments (8 treatments/2 years). Dairy cattle.	Costa et al. (2011)Costa MSVLF, Araújo RN, Costa AJLF, Simões RF, Lima WS. Anthelmintic resistance in a dairy cattle farm in the State of Minas Gerais. Rev Bras Parasitol Vet 2011; 20(2): 115-120. http://doi.org/10.1590/S1984-29612011000200005. PMid:21722485. http://doi.org/10.1590/S1984-29612011000...
2011	AR	Necropsy	IVM	X		X			X		Fiel et al. (2011)Fiel C, Guzmán M, Steffan P, Prieto O, Bhushan C. Comparative efficacy of trichlorphon and trichlorphon/ivermectin combination treatment against anthelmintic-resistant cattle nematodes in Argentina. Parasitol Res 2011;109(Suppl. 1): 105-112. http://doi.org/10.1007/s00436-011-2407-3. PMid:21739380. http://doi.org/10.1007/s00436-011-2407-3...
2012	BR	FECRT	IVM and DRM	N.I.	N.I.	N.I.	N.I.	N.I.	N.I.	ABA and SA: efficacy >95%	Bruhn et al. (2013)Bruhn FRP, Lopes MA, Perazza CA, Demeu FA, Santos G, Franco A No, et al. Eficiência técnica e econômica da aplicação de diferentes anti-helmínticos em fêmeas da raça holandesa na fase de recria durante o outono-inverno de 2009. Acta Tecnol 2013; 7(2): 25-30. http://doi.org/10.35818/acta.v7i2.138. http://doi.org/10.35818/acta.v7i2.138...
2013	BR	FECRT	IVM, LA-IVM and LA-DRM	X	X						Borges et al. (2013)Borges FA, Almeida GD, Heckler RP, Lemes RT, Onizuka MKV, Borges DGL. Anthelmintic resistance impact on tropical beef cattle productivity: effect on weight gain of weaned calves. Trop Anim Health Prod 2013; 45(3): 723-727. http://doi.org/10.1007/s11250-012-0280-4. PMid:23076819. http://doi.org/10.1007/s11250-012-0280-4...
2013	BR	LMIT	IVM	X						8 farms. 100% of isolates were resistant.	Almeida et al. (2013)Almeida GD, Feliz DC, Heckler RP, Borges DG, Onizuka MKV, Tavares LER, et al. Ivermectin and moxidectin resistance characterization by larval migration inhibition test in field isolates of Cooperia spp. in beef cattle, Mato Grosso do Sul, Brazil. Vet Parasitol 2013; 191(1-2): 59-65. http://doi.org/10.1016/j.vetpar.2012.08.012. PMid:22963710. http://doi.org/10.1016/j.vetpar.2012.08....
2014	BR	Necropsy	LA-IVM	X	X		X			6 farms.	Felippelli et al. (2014)Felippelli G, Lopes WDZ, Cruz BC, Teixeira WFP, Maciel WG, Fávero FC, et al. Nematode resistance to ivermectin (630 and 700μg/kg) in cattle from the Southeast and South of Brazil. Parasitol Int 2014; 63(6): 835-840. http://doi.org/10.1016/j.parint.2014.08.001. PMid:25130588. http://doi.org/10.1016/j.parint.2014.08....
2014	BR	FECRT	IVM, MOX and AS	X	X		X		X	10 farms. Percentage of farms with AHR: IVM-100%, MOX-80%, LEV-10% and AS-10%. Mean efficacy of MOX>80%.	Neves et al. (2014)Neves JH, Carvalho N, Rinaldi L, Cringoli G, Amarante AFT. Diagnosis of anthelmintic resistance in cattle in Brazil: a comparison of different methodologies. Vet Parasitol 2014; 206(3-4): 216-226. http://doi.org/10.1016/j.vetpar.2014.10.015. PMid:25468021. http://doi.org/10.1016/j.vetpar.2014.10....
2014	BR	Necropsy	IVM	X	X		X				Lopes et al. (2014a)Lopes WDZ, Felippelli G, Teixeira WFP, Cruz BC, Maciel WG, Buzzulini C, et al. Resistência de Haemonchus placei, Cooperia punctata e Oesophagostomum radiatum à ivermectina pour-on a 500mcgkg-1 em rebanhos bovinos no Brasil. Cienc Rural 2014a; 44(5): 847-853. http://doi.org/10.1590/S0103-84782014000500014. http://doi.org/10.1590/S0103-84782014000...
2014	BR	Necropsy	LA-IVM	X	X					MOX: efficacy >95%	Lopes et al. (2014b)Lopes WDZ, Teixeira WFP, Felippelli G, Cruz BC, Maciel WG, Soares VE, et al. Assessing resistance of ivermectin and moxidectin against nematodes in cattle naturally infected using three different methodologies. Res Vet Sci 2014b; 96(1): 133-138. http://doi.org/10.1016/j.rvsc.2013.11.001. PMid:24290235. http://doi.org/10.1016/j.rvsc.2013.11.00...
2014	AR	FECRT	IVM and MOX	X						LEV+RBZ: efficacy = 99%	Fazzio et al. (2014)Fazzio LE, Sánchez RO, Streitenberger N, Galvan WR, Giudici CJ, Gimeno EJ. The effect of anthelmintic resistance on the productivity in feedlot cattle. Vet Parasitol 2014; 206(3-4): 240-245. http://doi.org/10.1016/j.vetpar.2014.10.010. PMid:25468022. http://doi.org/10.1016/j.vetpar.2014.10....
2015	BR	Necropsy	IVM, LA-IVM and LA-DRM	X	X		X				Borges et al. (2015)Borges FA, Borges DGL, Heckler RP, Neves JPL, Lopes FG, Onizuka MKV. Multispecies resistance of cattle gastrointestinal nematodes to long-acting avermectin formulations in Mato Grosso do Sul. Vet Parasitol 2015; 212(3-4): 299-302. http://doi.org/10.1016/j.vetpar.2015.06.015. PMid:26129974. http://doi.org/10.1016/j.vetpar.2015.06....
2015	BR	FECRT	LA-IVM	X	X		X		X		Holsback et al. (2015)Holsback L, Silva MA, Patelli THC, Jesus AP, Sanches JR. Resistance of Haemonchus, Cooperia, Trichostrongylus, and Oesophagostomum to ivermectin in dairy cattle in Paraná. Semina: Ciênc Agrár 2015;36(3 Suppl. 1): 2031-2036. http://doi.org/10.5433/1679-0359.2015v36n3Supl1p2031. http://doi.org/10.5433/1679-0359.2015v36...
2016	BR	FECRT	IVM, DRM, EPR, FBZ, CLO, NIT, DIS, LEV, AS and MOX	X	X				X	11 farms. Combinations MOX+LEV, DRM+FBZ and LEV+CLO: efficacy>95%.	Ramos et al. (2016)Ramos F, Portella LP, Rodrigues FS, Reginato CZ, Pötter L, Cezar AS. Anthelmintic resistance in gastrointestinal nematodes of beef cattle in the state of Rio Grande do Sul, Brazil. Int J Parasitol Drugs Drug Resist 2016; 6(1): 93-101. http://doi.org/10.1016/j.ijpddr.2016.02.002. PMid:27054068. http://doi.org/10.1016/j.ijpddr.2016.02....
2016	BR	FECRT	DRM, MOX and LEV	X	X						Heckler et al. (2016)Heckler RP, Borges DGL, Vieira MC, Conde MH, Green M, Amorim ML, et al. New approach for the strategic control of gastrointestinal nematodes in grazed beef cattle during the growing phase in central Brazil. Vet Parasitol 2016; 221: 123-129. http://doi.org/10.1016/j.vetpar.2016.03.010. PMid:27084483. http://doi.org/10.1016/j.vetpar.2016.03....
2017	AR	FECRT	IVM	X	X						Canton et al. (2017)Canton C, Ceballos L, Fiel C, Moreno L, Domingo Yagüez P, Bernat G, et al. Resistant nematodes in cattle: pharmaco-therapeutic assessment of the ivermectin-ricobendazole combination. Vet Parasitol 2017; 234: 40-48. http://doi.org/10.1016/j.vetpar.2016.12.021. PMid:28115181. http://doi.org/10.1016/j.vetpar.2016.12....
2017	AR	FECRT	IVM	X	X			X		62 farms. Percentage of farms with AHR (genus): IVM-93.5% (C and H), RBZ-27.9% (C and Os), FBZ-7.4 (H), LEV-0%.	Cristel et al. (2017)Cristel S, Fiel C, Anziani O, Descarga C, Cetrá B, Romero J, et al. Anthelmintic resistance in grazing beef cattle in central and northeastern areas of Argentina: an update. Vet Parasitol Reg Stud Rep 2017; 9: 25-28. http://doi.org/10.1016/j.vprsr.2017.04.003. PMid:31014837. http://doi.org/10.1016/j.vprsr.2017.04.0...
2018	AR	FECRT	IVM	X							Canton et al. (2018)Canton C, Ceballos L, Domínguez MP, Moreno L, Fiel C, Bernat G, et al. Pharmaco-parasitological evaluation of the ricobendazole plus levamisole nematodicidal combination in cattle. J Vet Pharmacol Ther 2018; 41(1): 83-91. http://doi.org/10.1111/jvp.12438. PMid:28695609. http://doi.org/10.1111/jvp.12438...
2020	BR	FECRT	MLs and AS	X	X					LEV: efficacy>95%	Pivoto et al. (2020a)Pivoto FL, Cezar AS, Vogel FSF, Marques CB, Alves MEM, Becker CC, et al. Economic losses caused by the use of low-efficacy anthelmintic drugs in growing heifers. Trop Anim Health Prod 2020a; 52(3): 1365-1374. http://doi.org/10.1007/s11250-019-02144-1. PMid:31758387. http://doi.org/10.1007/s11250-019-02144-...
2020	BR	FECRT	LMs	X	X					A case of clinical helminthosis culminating in the death of steers. LEV and AS: efficacy>95%	Pivoto et al. (2020b)Pivoto FL, Cezar AS, Vogel FSF, Leal MLR. Effects of long-term indiscriminate use of macrocyclic lactones in cattle: parasite resistance, clinical helminthosis, and production losses. Vet Parasitol Reg Stud Rep 2020b; 20: 100381. http://doi.org/10.1016/j.vprsr.2020.100381. PMid:32448543. http://doi.org/10.1016/j.vprsr.2020.1003...
2020	BR	FECRT	IVM	X	X					BZDs: efficacy>95%	Neves et al. (2020)Neves JH, Carvalho N, Amarante AFT. Gastrointestinal nematode infections do not hinder the development of Simmental × Nellore crossbred calves raised with a nutritionally enhanced diet. Rev Bras Parasitol Vet 2020; 29(1): e015819. http://doi.org/10.1590/s1984-29612020006. PMid:32236331. http://doi.org/10.1590/s1984-29612020006...
2021	BR	FECRT								FBZ: efficacy=100%	Nakatani et al. (2021)Nakatani MTM, Conde MH, Freitas MG, Fávero FC, Paula LC, Cabrera MS, et al. Economic viability analysis of an oral anthelmintic treatment for cattle in feedlot. J Agric Stud 2021; 9(2): 188-204. http://doi.org/10.5296/jas.v9i2.18032. http://doi.org/10.5296/jas.v9i2.18032...
2021	BR	FECRT	IVM	X	X					BZDs: efficacy>95%	Neves et al. (2021)Neves JH, Carvalho N, Santos NC, Ratti J Jr, Martins CL, Amarante AFT. Effect of antihelminths with contrasting efficacy against gastrointestinal nematodes on the live-weight gain of young Nellore cattle. Vet Parasitol Reg Stud Rep 2021; 25: 100597. http://doi.org/10.1016/j.vprsr.2021.100597. PMid:34474790. http://doi.org/10.1016/j.vprsr.2021.1005...
2021	BR	FECRT	IVM, BZD, CLO	N.I.						20 farms. Percentage of farms with AHR: IVM-95%, AS-95%, CLO-75% and LEV-20%.	Melo et al. (2021)Melo LRB, Sousa LC, Menezes Oliveira CS, Alvares FBV, Ferreira LC, Bezerra RA, et al. Resistance of bovine gastrointestinal nematodes to four classes of anthelmintics in the semiarid region of Paraíba state, Brazil. Rev Bras Parasitol Vet 2021; 30(3): e010921. http://doi.org/10.1590/s1984-29612021077. PMid:34550213. http://doi.org/10.1590/s1984-29612021077...
2022	BR	FECRT	LA-IVM	X	X					A case of clinical helminthosis culminating in the death of cattle.	Lima et al. (2022)Lima SC, Borges DGL, Pupin RC, Guizelini CC, Paula JPL, Borges FA, et al. Mortality caused by gastrointestinal nematodes in beef cattle submitted to an inadequate sanitary protocol. Pesq Vet Bras 2022; 42: e07030. http://doi.org/10.1590/1678-5150-pvb-7030. http://doi.org/10.1590/1678-5150-pvb-703...
2022	BR	FECRT	IVM, LA-IVM, MOX	X	X						Borges et al. (2022)Borges DGL, Conde MH, Cunha CCT, Freitas MG, Moro E, Borges FA. Moxidectin: a viable alternative for the control of ivermectin-resistant gastrointestinal nematodes in beef cattle. Acta Vet 2022; 72(1): 16-29. http://doi.org/10.2478/acve-2022-0002. http://doi.org/10.2478/acve-2022-0002...

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[1] *Corresponding author: Fernando de Almeida Borges. E-mail: fernando.borges@ufms.br