Resistência das lactonas macrocíclicas injetáveis em bovinos: uma revisão sistemática e meta-análise

Baiak, Barbara Haline Buss; Lehnen, Cheila Roberta; Rocha, Raquel Abdallah da

doi:10.1590/S1984-296120180093

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Original Article • Rev. Bras. Parasitol. Vet. 28 (1) • Jan-Mar 2019 • https://doi.org/10.1590/S1984-296120180093 copiar

Resistência das lactonas macrocíclicas injetáveis em bovinos: uma revisão sistemática e meta-análise

Autoria SCIMAGO INSTITUTIONS RANKINGS

Resumo

O objetivo deste trabalho foi identificar, avaliar criticamente e resumir os dados disponíveis da literatura primária sobre resistência anti-helmíntica a lactonas macrocíclicas injetáveis em bovinos. Uma meta-análise foi realizada para estimar o “Odds Ratio” e Intervalos de Confiança (95%). Dos 1504 resumos selecionados para elegibilidade, 80 foram considerados relevantes para a revisão completa da publicação. Treze publicações foram incluídas na síntese qualitativa, as quais foram avaliadas quanto ao viés sistemático. Apenas cinco estudos foram incluídos na análise quantitativa porque apresentaram um baixo risco de produzir resultados tendenciosos em todos os parâmetros. O gráfico de floresta indicou quatro estudos que apresentaram resistência anti-helmíntica (P <0,05), enquanto um não apresentou (P <0,05). A estimativa combinada mostrou uma maior probabilidade de publicações de estudos que relatam resistência anti-helmíntica no valor de 0,59 (95%: 0,8, 0,47) do que estudos relatando tratamento anti-helmíntico eficaz. Os dados apresentaram baixa heterogeneidade (I² = 25%). A resistência anti-helmíntica a lactonas macrocíclicas é uma realidade. Há a necessidade de melhorar a metodologia dos estudos, pois é um problema para os trabalhos que envolvem revisões sistemáticas e meta-análises (RS-MA).

Palavras-chave:
Anti-helmínticos; nematódeos; ivermectina; moxidectina

Acronym	Definition
Interventions	Under-dosing: This occurs when the cattle receive less than the optimal anthelmintic dosage. This may occur for various reasons, including inaccurate weight estimation, or incorrect method of administration
	Route of administration: Anthelmintic drugs can be administered orally, pour on or subcutaneously.
	Long-acting/persistent anthelmintic drugs: Anthelmintic drugs that have a persistent action, either because of their lipophilic nature, or because of their formulation.
	Timing of anthelmintic treatment: The timing of treatment relative to certain stages of production or management stages.
	Mixed-species grazing: Simultaneous grazing of cattle with other species.
	Rotational grazing: The practice of moving grazing livestock between pastures (often called paddocks) as needed or on a regular basis.
	Strategic treatment: Anthelmintic treatments of the group that are aimed at identified potential periods of risk based on fecal egg count monitoring or clinical signs.
	Pasture management: Grazing management strategies that reduce reliance on anthelmintics by decreasing the cattle's exposure to parasite burdens on pasture.
	Rotation of anthelmintics: Changing the drug class used on the farm every one to two years.
	Drench-and-shift: Treating the animals with anthelmintics, and then moving them immediately to pasture considered as free of, or with a low level of, contamination with gastro-intestinal nematodes, to reduce risk of re-infection.
	Drench gun calibration: Emptying of the drench gun into a graduated measure device and adjusting to ensure that the drench gun is delivering the correct amount of anthelmintic drug.

Acronym	Search string
Population	(“cattle” OR “calves”) (“beef” OR “dairy”)
Outcome	(anthelmintic OR “macrocyclic lactone*” OR ivermectin OR moxidectin OR doramectin OR abamectin) AND (gastrointestinal OR internal) AND (parasite OR nematode OR worms OR worming) AND (resistance OR resistant) AND (efficacy OR effectiveness) AND (faecal egg count reduction test OR FECRT) AND (route of administration” OR “injectable formulation”) AND (“natural infections”)

Study (author and year)	Country	Risk and protective factors reported	Anthelmintic drug	Outcome measurement	Type of GIN recovered	Route of administration
Alonso-Diaz et al. (2015) Alonso-Díaz MA, Arnaud-Ochoa RA, Becerra-Nava R, Torres-Acosta JFJ, Rodríguez-Vivas RI, Quiroz-Romero RH. Frequency of cattle farms with ivermectin resistant gastrointestinal nematodes in Veracruz, Mexico. Vet Parasitol 2015; 212(3-4): 439-443. http://dx.doi.org/10.1016/j.vetpar.2015.07.023. PMid:26238656. http://dx.doi.org/10.1016/j.vetpar.2015...	Mexico	Climate; farm type; last dewormed	Ivermectin	FECRT	Cooperia sp.; Haemonchus sp.; Strongyloides sp.; and Oesophagostomum sp.	Injectable 0.2 mg/Kg
Arantes et al. (1995) Arantes GJ, Silva CR, Costa JO, Marra DB. Atividade anti-helmíntica da ivermectina a 1% (solução injetável), no tratamento de bezerros naturalmente infectados com nematóides gastrintestinais. Rev Bras Parasitol Vet 1995; 4(2): 113-116.	Brazil	Not specified	Ivermectin	FECRT	Haemonchus placei;Trichostrongylus axei; T. colubriformis; Bunostomum phlebotomum; Cooperia punctata; Oesophagostomum radiatum	Injectable 0.2 mg/Kg
Canul-Ku et al. (2012) Canul-Ku HL, Rodríguez-Vivas RI, Torres-Acosta JFJ, Aguilar-Caballero AJ, Pérez-Cogollo LC, Ojeda-Chi MM. Prevalence of cattle herds with ivermectin resistant nematodes in the hot sub-humid tropics of Mexico. Vet Parasitol 2012; 183(3-4): 292-298. http://dx.doi.org/10.1016/j.vetpar.2011.07.029. PMid:21831526. http://dx.doi.org/10.1016/j.vetpar.2011...	Mexico	Climate; location; average temperature; farm type; frequency of treatment	Ivermectin	FECRT	Haemonchus sp.; Ostertagia sp.; Trichostrongylus sp.; Cooperia sp.	Injectable 0.2 mg/Kg
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://dx.doi.org/10.1016/j.vetpar.2009.01.031. PMid:19251366. http://dx.doi.org/10.1016/j.vetpar.2009...	Brazil	Farm type; mixed-species grazing; frequency of treatment; rotation of anthelmintic drug	Moxidectin	FECRT	Cooperia sp.; Oesophagostumum sp.; Trichuris sp.	Injectable 0.2mg/Kg
El-Abdellati et al. (2010) El-Abdellati A, Charlier J, Geldhof P, Levecke B, Demeler J, von Samson-Himmelstjerna G, et al. The use of a simplified faecal egg count reduction test for assessing anthelmintic efficacy on Belgian and German cattle farms. Vet Parasitol 2010; 169(3-4): 352-357. http://dx.doi.org/10.1016/j.vetpar.2010.01.015. PMid:20149547. http://dx.doi.org/10.1016/j.vetpar.2010...	Belgium and Germany	Frequency of treatment; season grazing	Macrocyclic Lactone	FECRT	Cooperia oncophora	Injectable Not specified
Geurden et al. (2004) Geurden T, Claerebout E, Deroover E, Vercruysse J. Evaluation of the chemoprophylactic efficacy of 10% long acting injectable moxidectin against gastrointestinal nematode infections in calves in Belgium. Vet Parasitol 2004; 120(4): 331-338. http://dx.doi.org/10.1016/j.vetpar.2004.01.016. PMid:15063943. http://dx.doi.org/10.1016/j.vetpar.2004...	Belgium	season grazing	Moxidectin	FECRT	Ostertagia sp.; Cooperia sp.; Trichostrongylus sp.; Oesophagostomum sp.	Injectable 1mg/Kg
Llorens et al. (2014) Llorens IYG, Ponce JDM, Suárez JCM, Carrazana BM, Méndez DG. Eficacia antihelmíntica del Labiomec® (Ivermectina 1%) en rebaños bovinos de Camagüey. Rev Salud Anim 2014; 36(1): 58-61.	Cuba	Last dewormed	Ivermectin	FECRT	Haemonchus sp.; Trichostrongylus sp.; Bunustomun sp.;.	Injectable 0.2 mg/Kg
Mena et al. (2008) Mena LAE, Arellano MEL, Gives PMG, Hernández EL, Prats VV, Ycuspinera GV. Primer informe en México sobre la presencia de resistencia a ivermectina en bovinos infectados naturalmente com nematodos gastrointestinales. Vet Mex 2008; 39(4): 423-428.	Mexico	Mixed-species grazing; last dewormed	Ivermectin	FECRT	Cooperia sp.; Oesophagostomum sp.; Haemonchus sp.	Injectable 0.2 mg/Kg
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://dx.doi.org/10.1590/S0102-09352005000200008. http://dx.doi.org/10.1590/S0102-0935200...	Brazil	Farm type; climate; location; last dewormed; frequency of treatment; species grazing	Moxidectin;ivermectin and doramectin	FECRT	Cooperia sp. and Haemonchus sp.	Injectable 0.2 mg/Kg
Ranjan et al. (1992) Ranjan S, Trudeau C, Prichard RK, von Kutzleben R, Carrier D. Efficacy of moxidectin against naturally acquired nematode infections in cattle. Vet Parasitol 1992; 41(3-4): 227-231. http://dx.doi.org/10.1016/0304-4017(92)90082-K. PMid:1502785. http://dx.doi.org/10.1016/0304-4017(92)...	Canada	Farm type	Moxidectin	FECRT	Ostertagia sp.; Trichostrongylus sp.; Cooperia sp. and Nematodirus sp.	Injectable 0.2 mg/Kg
Sievers & Fuentealba (2003) Sievers G, Fuentealba C. Comparación de la efectividad antihelmíntica de seis productos comerciales que contienen lactonas macrocíclicas frente a nematodos gastrointestinales del bovino. Arch Med Vet 2003; 35(1): 81-88. http://dx.doi.org/10.4067/S0301-732X2003000100008. http://dx.doi.org/10.4067/S0301-732X200...	Chile	Farm type and location	Ivermectin; doramectin and moxidectin	FECRT	Cooperia sp.; Ostertagia sp.; and Trichostrongylus sp.	Injectable 0.2 mg/Kg
Sievers & Alocilla (2007) Sievers G, Alocilla A. Determinación de resistencia antihelmíntica frente a ivermectina de nematodos del bovino en dos predios del sur de Chile. Arch Med Vet 2007; 39(1): 67-69. http://dx.doi.org/10.4067/S0301-732X2007000100010. http://dx.doi.org/10.4067/S0301-732X200...	Chile	Farm location and frequency of treatment	Ivermectin	FECRT	Ostertagia sp.; Cooperia sp. and Trichostrongylus sp.	Injectable 0.2 mg/Kg
Stafford & Coles (1999) Stafford K, Coles GC. Nematode control practices and anthelmintic resistance in dairy calves in the south west of England. Vet Rec 1999; 144(24): 659-661. http://dx.doi.org/10.1136/vr.144.24.659. PMid:10404603. http://dx.doi.org/10.1136/vr.144.24.659...	United Kingdom	Frequency of treatment and pasture rotation	Ivermectin	FECRT	Cooperia sp.	Injectable 0.2 mg/Kg

Study (author and year)	Random sequence generation	Random allocation concealment	Blinding of outcome assessment	Incomplete outcome data	Selective outcome reporting
Alonso-Diaz et al. (2015) Alonso-Díaz MA, Arnaud-Ochoa RA, Becerra-Nava R, Torres-Acosta JFJ, Rodríguez-Vivas RI, Quiroz-Romero RH. Frequency of cattle farms with ivermectin resistant gastrointestinal nematodes in Veracruz, Mexico. Vet Parasitol 2015; 212(3-4): 439-443. http://dx.doi.org/10.1016/j.vetpar.2015.07.023. PMid:26238656. http://dx.doi.org/10.1016/j.vetpar.2015...	Unclear	Unclear	High	Low	Low
Arantes et al. (1995) Arantes GJ, Silva CR, Costa JO, Marra DB. Atividade anti-helmíntica da ivermectina a 1% (solução injetável), no tratamento de bezerros naturalmente infectados com nematóides gastrintestinais. Rev Bras Parasitol Vet 1995; 4(2): 113-116.	Low	Unclear	Low	Low	Low
Canul-Ku et al. (2012) Canul-Ku HL, Rodríguez-Vivas RI, Torres-Acosta JFJ, Aguilar-Caballero AJ, Pérez-Cogollo LC, Ojeda-Chi MM. Prevalence of cattle herds with ivermectin resistant nematodes in the hot sub-humid tropics of Mexico. Vet Parasitol 2012; 183(3-4): 292-298. http://dx.doi.org/10.1016/j.vetpar.2011.07.029. PMid:21831526. http://dx.doi.org/10.1016/j.vetpar.2011...	Low	Low	Low	Low	Low
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://dx.doi.org/10.1016/j.vetpar.2009.01.031. PMid:19251366. http://dx.doi.org/10.1016/j.vetpar.2009...	Low	Low	Low	Low	Low
El-Abdellati et al. (2010) El-Abdellati A, Charlier J, Geldhof P, Levecke B, Demeler J, von Samson-Himmelstjerna G, et al. The use of a simplified faecal egg count reduction test for assessing anthelmintic efficacy on Belgian and German cattle farms. Vet Parasitol 2010; 169(3-4): 352-357. http://dx.doi.org/10.1016/j.vetpar.2010.01.015. PMid:20149547. http://dx.doi.org/10.1016/j.vetpar.2010...	Low	Low	Unclear	High	Low
Geurden et al. (2004) Geurden T, Claerebout E, Deroover E, Vercruysse J. Evaluation of the chemoprophylactic efficacy of 10% long acting injectable moxidectin against gastrointestinal nematode infections in calves in Belgium. Vet Parasitol 2004; 120(4): 331-338. http://dx.doi.org/10.1016/j.vetpar.2004.01.016. PMid:15063943. http://dx.doi.org/10.1016/j.vetpar.2004...	Low	Low	Low	Low	Low
Llorens et al. (2014) Llorens IYG, Ponce JDM, Suárez JCM, Carrazana BM, Méndez DG. Eficacia antihelmíntica del Labiomec® (Ivermectina 1%) en rebaños bovinos de Camagüey. Rev Salud Anim 2014; 36(1): 58-61.	Unclear	Unclear	High	Low	Low
Mena et al. (2008) Mena LAE, Arellano MEL, Gives PMG, Hernández EL, Prats VV, Ycuspinera GV. Primer informe en México sobre la presencia de resistencia a ivermectina en bovinos infectados naturalmente com nematodos gastrointestinales. Vet Mex 2008; 39(4): 423-428.	Unclear	Low	High	Low	Low
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://dx.doi.org/10.1590/S0102-09352005000200008. http://dx.doi.org/10.1590/S0102-0935200...	Unclear	Unclear	Unclear	Low	Low
Ranjan et al. (1992) Ranjan S, Trudeau C, Prichard RK, von Kutzleben R, Carrier D. Efficacy of moxidectin against naturally acquired nematode infections in cattle. Vet Parasitol 1992; 41(3-4): 227-231. http://dx.doi.org/10.1016/0304-4017(92)90082-K. PMid:1502785. http://dx.doi.org/10.1016/0304-4017(92)...	Low	Low	Low	Low	Low
Sievers & Fuentealba (2003) Sievers G, Fuentealba C. Comparación de la efectividad antihelmíntica de seis productos comerciales que contienen lactonas macrocíclicas frente a nematodos gastrointestinales del bovino. Arch Med Vet 2003; 35(1): 81-88. http://dx.doi.org/10.4067/S0301-732X2003000100008. http://dx.doi.org/10.4067/S0301-732X200...	Low	Low	Low	Low	Low
Sievers & Alocilla (2007) Sievers G, Alocilla A. Determinación de resistencia antihelmíntica frente a ivermectina de nematodos del bovino en dos predios del sur de Chile. Arch Med Vet 2007; 39(1): 67-69. http://dx.doi.org/10.4067/S0301-732X2007000100010. http://dx.doi.org/10.4067/S0301-732X200...	Low	High	Low	Low	Low
Stafford & Coles (1999) Stafford K, Coles GC. Nematode control practices and anthelmintic resistance in dairy calves in the south west of England. Vet Rec 1999; 144(24): 659-661. http://dx.doi.org/10.1136/vr.144.24.659. PMid:10404603. http://dx.doi.org/10.1136/vr.144.24.659...	Unclear	Unclear	High	Low	Low

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[1] * Corresponding author: Raquel Abdallah da Rocha. Departamento de Zootecnia, Universidade Estadual de Ponta Grossa – UEPG, Av. Carlos Cavalcante, 4748, Uvaranas, CEP 84030-900, Ponta Grossa, PR, Brasil. e-mail: raroliveira@uepg.br