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Anthelmintic efficacy and management practices in sheep farms from the state of Rio de Janeiro, Brazil
Veterinary Parasitology 170 (2010) 340–343
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Anthelmintic efficacy and management practices in sheep farms from the state of Rio de Janeiro, Brazil Daniela Guedes da Cruz a , Letícia Oliveira da Rocha a , Sabrina Santos Arruda a , Jorge Guilherme Bergottini Palieraqui a , Rudymilla Cunha Cordeiro a , Edizio Santos Junior b , Marcelo Beltrão Molento c , Clóvis de Paula Santos a,∗ a
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Parque California, 28013-600 Campos dos Goytacazes, RJ, Brazil b Laboratório de Zootecnia e Nutric¸ão Animal Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, 28013-600 Campos dos Goytacazes, RJ, Brazil c Laboratório de Doenc¸as Parasitárias, Departamento de Medicina Veterinária, Universidade Federal do Paraná, Curitiba, Paraná, Brazil
a r t i c l e
i n f o
Article history: Received 1 October 2009 Received in revised form 8 February 2010 Accepted 21 February 2010 Keywords: Anthelmintic resistance Sheep Ruminants Gastrointestinal nematodes
a b s t r a c t Anthelmintic resistance in parasites maybe a consequence of over-exposing populations of parasites to drugs or from the commerce/transit of animals harboring resistant parasites. Knowledge of the sensitivity of nematodes to anthelmintics is essential to establish an efficient integrated program of parasite control. In Brazil, producers rely on technology transfer from field professionals and non-technical labor for new management strategies of parasite control. The aim of this work was to determine the practices farmers used for anthelmintic management and to monitor drug efficacy on sheep farms from northern and northwestern regions of the state of Rio de Janeiro, Brazil. A questionnaire was sent to 34 farms, and anthelmintics were tested on ten of these farms. Sheep (n = 10/group) were weighed and treated with albendazole, closantel, doramectin, fenbendazole, ivermectin, levamisole, moxidectin, or nitroxynil with their recommended doses. Faeces were collected on the day of treatment and after 7–10 days. The faecal egg count reduction test was evaluated based on RESO 2.0. Among the farmers interviewed, 97% applied commercial anthelmintics to control parasites, 77% rotated anthelmintics annually, 72% used ivermectin as the principal anthelmintic, and 38% applied anthelmintics with a frequency of 30–60 days. On two farms, none of the anthelmintics was efficacious. Levamisole had the best overall efficacy (70%). Albendazole, ivermectin, and fenbendazole were efficacious (above 95%) on only two farms. The present work illustrates the alarming lack of efficacy of drugs even in an area new to sheep farming. It is important to establish alternative strategies of management in a broad program of parasite control for reducing the selection pressure on parasites by the commercially available anthelmintics. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Brazil is the eighth largest producer of sheep and goats in the world, with 25.8 million head. In 2004, the state
∗ Corresponding author. Tel.: +55 22 2739 7180; fax: +55 22 2739 7178. E-mail address: [email protected] (C. de Paula Santos). 0304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2010.02.030
of Rio de Janeiro contributed about 1% of the Brazilian production of sheep (IBGE, 2004). However, the importation of improved breeds, such as Boer, Dorper, Savannah, and Alpine, and the dissemination of the Santa Inês breed, developed in northeastern Brazil (Jardim, 1987), has increased the growth expectation of sheep for meat and milk production in Rio de Janeiro as well as states of the southeastern and central-western parts of the country.
D.G. da Cruz et al. / Veterinary Parasitology 170 (2010) 340–343
One of the most important diseases that limit the production of small ruminants in the tropics and sub-tropics is parasitism by gastrointestinal nematodes (FAO, 1998). In Brazil, the disease is recognized as a major problem in the production of small ruminants (Padilha and Gives, 1996; Ramos et al., 2002). The control of parasites in livestock relies almost exclusively on multiple and regular use of anthelmintics, with no standard monitoring of their efficacy. However, the prophylactic use of anthelmintics has led to the global emergence of drug resistance in helminths and particularly multiple anthelmintic resistances in nematodes of ruminants (Echevarria, 1996; Thomaz-Soccol et al., 2004; Ketzis et al., 2006; Jackson and Miller, 2006). The evolution of anthelmintic resistance is a complex process involving several factors, which are divided into intrinsic, relating to the parasites, and operative, relating to man’s actions. The inadequate management of anthelmintics and their indiscriminate use are among the main operative factors that lead to the occurrence of this phenomenon (FAO, 2003). Molento and Almeida (2004) have reported that sheep farmers in Brazil use anthelmintics as well as pasture rotation and winter grazing as their major strategies for parasite control, with anthelmintics being used from 2 up to 21 times a year in rapid rotation. Lawrence et al. (2006) have associated farm practices with the presence of resistance to half-doses of ivermectin based on faecal egg count reduction tests (FECRT) on sheep farms in New Zealand. The authors found that ivermectin resistance was increased on farms that used this product in ewes as a pre-lambing treatment for ≥3 of the previous 5 years. Another factor identified in association with ivermectin resistance was the importation of resistant parasites with purchased stock. From a questionnaire to sheep farmers in the Taihape area, New Zealand, Hughes et al. (2007) found a high association (p < 0.05) between the presence of ivermectin resistance and the practices of farm management. Resistance was evident to ivermectin on 47% of the farms, benzimidazoles on 54%, levamisole on 37%, and the combination of benzimidazole and levamisole on 5% of the farms. Thus, the knowledge on the sensitivity of nematodes to anthelmintics is one of the most fundamental components for establishing any integrated program of parasite control, along with a single set of on-farm management practices. Therefore, the objective of the present study was to collect reference data of anthelmintic management at the farm level and efficacy based on FECRT in sheep farms in the northern and northwestern regions of the state of Rio de Janeiro, Brazil. 2. Materials and methods 2.1. Farms The study was performed on 34 sheep farms located in the state of Rio de Janeiro in the municipal districts of Campos dos Goytacazes, Porciúncula, Cardoso Moreira, São Francisco de Itabapoana, Santo Antonio de Pádua, São João da Barra, Quissamã, Casimiro de Abreu, Duque de Caxias, and Petrópolis. The data on anthelmintic manage-
341
ment were collected using a questionnaire containing eight questions. Ten farms located in the municipal districts of Campos dos Goytacazes, Cardoso Moreira, Quissamã São Francisco de Itabapoana, Santo Antonio de Pádua, and São João da Barra were randomly selected for testing by FECRT. 2.2. Anthelmintic test The anthelmintic test used Saint Inês sheep, preferentially males, aged between 6 and 10 months. These animals were weighed and distributed into eight groups of 10 animals each and treated with the following anthelmintics: albendazole, closantel, doramectin, fenbendazole, ivermectin, levamisole, moxidectin, and nitroxynil at their recommended doses. 2.3. Anthelmintic efficacy The faeces were collected directly from the rectum of each animal on day zero and 7–10 days after anthelmintic treatment. Two grams of faeces were used for quantifying the number of eggs per gram of faeces (EPG) in a counting chamber (Mc Master), according to the modified technique of Gordon and Withlock (1939). A supersaturated salt solution was used as a flotation fluid (specific gravity: 1.200). The chamber Mac Master detects 50 or more EPG. The efficacy of the products was estimated by the modified test RESO 2.0 (Wursthorn and Martin, 1990). 3. Results and discussion Among the 34 producers interviewed, 97% drenched animals as the main method to control parasitic infections, 77% rotated anthelmintic group, 72% have used or now use ivermectin, and 38% drench animals with a frequency of 30–60 days (Table 1). Ivermectin is the best characterized endectocide of the avermectin group; it was synthesized and initially described in the early 1980 (Chabala et al., 1980). Ivermectin’s endo- and ectoparasitic properties, relative low cost, and high efficacy appeal to farmers and is still the compound most used (Table 1). Although the frequency of use of anthelmintics was relatively similar on the examined properties, with most of the producers drenching animals with short intervals (between 30 and 60 days), some producers treated their animals at an interval of 120 days (Table 1). The majority of producers affirmed that they applied the dose recommended by the manufacturers but admitted to rarely considering the weight of the animals for the calculation of the exact amount of the compound. Therefore, under- or over-dosing was detected, which could influence the development of drug resistance. The improved efficacy observed at property 8 maybe due to the long interval between treatments (240 days), mainly with levamisole and ivermectin. Recent studies based on questionnaires have provided important information about the management practices of anthelmintic use. Hughes et al. (2007) interviewed 84 farmers to ascertain whether particular management or drenching strategies were associated with the presence of resistance. Resistance was evident for ivermectin on 47%, benzimidazoles on 54%, levamisole on 37%, and benzim-
342
D.G. da Cruz et al. / Veterinary Parasitology 170 (2010) 340–343
Table 1 Percentile data for control and anthelmintic management in sheep farms from northern and northwestern regions of the state of Rio de Janeiro from interviews of 34 producers. Question
%
Drench animals
97
Frequency of anthelmintic use 30–60 days 90–120 days More than 120 days Not determined
38 29 9 24
Criterion of anthelmintic use EPG FAMACHA Expected period Clinical signs None
26 3 50 18 3
Dose according to weight and drug labeling Anthelmintic rotation Pasture rotation Knowledge of strategic controla Knowledge of integrated controlb
100 77 50 38 35
Obs: 72% of the producers that use anthelmintics specified that they now use or previously used Ivermectin. a Strategic control is the term used in Brazil for “Drenchplan” or “Wormkill” programs in Australia (Waller, 1986; Echevarria et al., 1988; Vieira et al., 1997). b According to Waller (1999).
idazole/levamizole on 5% of farms. Positive associations (p < 0.05) were determined for resistance to macrocyclic lactones when weaning more than half of the lambs onto paddocks not grazed by lambing ewes since June, not always returning lambs to the same paddock after drenching, and using visual signs to assess ‘worminess’. Measuring drench efficacy between January and March rather than later in the year, and the presence of resistance to benzimidazole or levamisole were associated with a higher apparent prevalence of resistance to macrocyclic lactones (p < 0.05). The prevalence of resistance was lower on farms where management practices, particularly those involving lambs, maintained refugia of unselected nematodes. Cernanská et al. (2008) also obtained information through a questionnaire on practices of worm control and management of sheep on 49 sheep farms. Mean drenching rates for lambs and yearlings/adults were 1.76 and 1.70, respectively. Weights of the heaviest animals were used
to determine anthelmintic doses only on 16.7% of farms. Coprological examinations were performed once a year on 47.9% of farms. The most frequently used drugs during the period from 1999 to 2004 were albendazole and ivermectin. Note that ivermectin as the drug of choice and the failure to weigh animals for determining dose are common to the work presented here. The percentage of efficacy depended on the anthelmintic agent and ranged from: albendazole (0–100%), closantel (0–100%), doramectin (35–100%), fenbendazole (0–100%), ivermectin (0–100%), levamisole (86–100%), moxidectin (71–100%) and nitroxynil (76–100%) (Table 2). Of the farms assessed, only properties numbers 1 and 6 showed anthelmintic inefficiency for all compounds tested. On the other hand, five drugs were effective at property number 8. At properties 9 and 10, only levamisole was effective. The drug that showed the best efficacy was levamisole, being effective in 70% of the properties assessed, followed by moxidectin with an efficacy of 66%. The anthelmintics with the lowest rates of effectiveness were: nitroxynil (33%), doramectin (30%), closantel, fenbendazole, ivermectin (20%), and albendazole (11%) (Table 2). The overall efficacy obtained in the present work corroborates published data. Melo et al. (2003), working with ivermectin and levamisole in the state of Ceará, Brazil, found a 0–100% and an 18–100% effectiveness, respectively. Furthermore, Cunha Filho and Yamamura (1999) showed that in the region of Tamarana, state of Paraná, Brazil, albendazole showed ineffective anthelmintic action with a 0% reduction in EPG while moxidectin had 100% reduction. Similar results were found in The Netherlands where doramectin, albendazole, moxidectin, and levamisole had an efficacy of 15, 87, 99, and 100%, respectively (Borgsteede et al., 2007). Property 1, where no products reduced egg counts, and properties 9 and 10, where only levamisole was effective, had short frequencies of drug treatment (30–60 days). Furthermore, a variety of generic brands of drugs were used without any criteria for drug rotation. Although properties 1 and 9 were the most organized, with good infrastructure, a reasonable set of strategies for sanitation, and adequate nutrition, as endorsed by one veterinarian and one animal scientist, the use of anthelmintics for prophylaxis has encouraged the development of resistance due to
Table 2 Percentile of efficacya of eight anthelmintics on sheep farms from northern and northwestern regions of the state of Rio de Janeiro. Farm
1 2 3 4 5 6 7 8 9 10
Anthelmintics Nitroxynil
Doramectin
Levamisole
Ivermectin
Albendazole
NE 76 100 100 89 87 88 100 90 77
88 100 86 63 100 36 100 75 88 50
86 91 96 100 100 91 100 100 100 100
88 95 17 0 71 58 100 50 55 64
79 90 95 0 NE 0 86 94 85 82
Obs: 10 sheep/each anthelmintic. NE, not evaluated. a Indices lower than 95% are indicative of inefficacy.
Closantel 0 0 84 100 93 75 72 100 83 75
Moxidectin
Fenbendazole
86 100 100 100 100 84 100 100 71 NE
73 70 0 90 100 89 39 100 74 54
D.G. da Cruz et al. / Veterinary Parasitology 170 (2010) 340–343
the extermination of populations of nematodes in refugia. It was interesting to observe that levamisole, even after 38 years on the market, still remained the most effective anthelmintic. 4. Conclusion Data from the questionnaire and anthelmintic tests are important for obtaining records of management practices relating to the anthelmintics used on sheep farms in the northern and northeastern regions of the state of Rio de Janeiro. The results demonstrate the need to implement urgent actions for the dissemination of appropriate strategies for controlling parasites. Acknowledgment The authors thank Dr. Renato Augusto DaMatta for reviewing the manuscript. References Borgsteede, F.H.M., Dercksen, D.D., Huijbers, R., 2007. Doramectin and albendazole resistance in sheep in The Netherlands. Vet. Parasitol. 144, 180–183. Cernanská, D., Várady, M., Cudeková, P., Corba, J., 2008. Worm control practices on sheep farms in the Slovak Republic. Vet. Parasitol. 154, 270–276. Chabala, J., Mrozik, H., Tolman, R., Eskola, P., Lusi, A., Peterson, L., Woods, M., Campbell, W., 1980. Ivermectin, a new broad-spectrum antiparasitic agent. J. Med. Chem. 23, 1134–1136. Cunha Filho, L.F.C., Yamamura, M.H., 1999. Resistência a anti-helmínticos em ovinos da região de Tamarana, Paraná, Brasil. Cient. Ciênc. Biol. Saúde. 1, 31–39. Echevarria, F.A.M., 1996. Resistência anti-helmíntica. In: Padilha, T. (Ed.), Controle de nematóides gastrintestinais em ruminantes. EmbrapaCNPGL, Coronel Pacheco, pp. 53–76. Echevarria, F.A. M., Pinheiro, A.C., Correa, M.B.C., 1988. Alternativas para controle da verminose ovina no Rio Grande do Sul. Bagé, EmbrapaCPPSUL, (comunicado técnico, 8). 6p. FAO, 1998. Biological Control of Gastro-intestinal Nematodes of Ruminants using Predacious Fungi, FAO Animal Production and Health Papers. FAO, Rome, 94 pp. FAO, 2003. Resistencia a los Antiparasitarios: Estado actual con énfasis en América Latina, FAO Animal Production and Health Papers 141. FAO, Rome, 53 pp.
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Gordon, N.M., Withlock, H.V., 1939. A new technique for counting nematode eggs in sheep faeces. J. Comm. Cient. Ind. Res. Org. 12, 50–52. Hughes, P.L., Dowling, A.F., Callinan, A.P.L., 2007. Resistance to macrocyclic lactone anthelmintics and associated risk factors on sheep farms in the lower North Island of New Zealand. N. Z. Vet. J. 55, 177–183. IBGE, 2004. Produc¸ão da Pecuária Mundial, vol. 32, 21 pp. Jackson, F., Miller, J., 2006. Alternative approaches to control-Quo vadit? Vet. Parasitol. 139, 371–384. Jardim, W.R., 1987. Os ovinos, 4th ed. Livraria Nobel, São Paulo, 193 pp. Ketzis, J.K., Vercruysse, J., Stromberg, B.E., Larsen, M., Athanasiadou, S., Houdijk, J.G., 2006. Evaluation of efficacy expectations for novel and non-chemical helminth control strategies in ruminants. Vet. Parasitol. 139, 321–335. Lawrence, K.E., Rhodes, A.P., Jackson, R., Leathwick, D.M., Heuer, C., Pomroy, W.E., West, D.M., Waghorn, T.S., Moffat, J.R., 2006. Farm management practices associated with macrocyclic lactone resistance on sheep farms in New Zealand. N. Z. Vet. J. 54 (6), 283–288. Melo, A.C.F.L., Reis, I.F., Bevilaqua, C.M.L., Vieira, L.S., Echevarria, F.A.M., Melo, L.M., 2003. Nematódeos resistentes a anti-helmíntico em rebanhos de ovinos e caprinos do estado do Ceará, Brasil. Ciênc. Rural. 33, 339–344. Molento, M.B., Almeida, L., 2004. Práticas de controle parasitário adotadas por criadores de ovinos e caprinos no Brasil. In: XIII Congresso Brasileiro de Parasitologia Veterinária, Anais. Ouro Preto, MG (CDRom). Padilha, T., Gives, P.M., 1996. Controle microbiano das formas de vida livre dos nematódeos trichostrongilídeos: Uma alternativa para higienizac¸ão das pastagens. In: Padilha, T. (Ed.), Controle dos nematóides em ruminantes. Embrapa-CNPGL, Coronel Pacheco, pp. 216–235. Ramos, C.I., Bellato, V., Ávila, V.S., Coutinho, G.C., Souza, A.S., 2002. Resistência de parasitos gastrintestinais de ovinos a alguns antihelmínticos no Estado de Santa Catarina, Brasil. Ciênc. Rural. 32, 473–477. Thomaz-Soccol, V., Souza, F.P., Sotomaior, C., Castro, E.A., Milczewski, V., Mocelin, G., Pessoa e Silva, M.C., 2004. Resistance of gastrointestinal nematodes to anthelmintics in sheep (Ovis aries). Brazil Arch. Biol. Technol. 47, 41–47. Vieira, L.S., Cavalcante, A.C.R., Ximenes, L.J.F., 1997. Epidemiologia e Controle das principais parasitoses de caprinos nas regiões semi-áridas do nordeste. Embrapa-CNPC, Sobral, Ceará, 50 pp. Waller, P.J., 1986. Anthelmintic resistance in nematode parasites of sheep. Agric. Zool. Rev. 1, 333–373. Waller, P.J., 1999. International approaches to the concept of integrated control of nematode parasites of livestock. Int. J. Parasitol. 29, 155–164. Wursthorn, L., Martin, P., 1990. Reso 2. 0: calculation for fecal egg count reduction test (FECRT) analysis program. Animal Health Research Laboratory, Parkville, CSIRO.
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Anthelmintic efficacy and management practices in sheep farms from the state of Rio de Janeiro, Brazil Daniela Guedes da Cruz a , Letícia Oliveira da Rocha a , Sabrina Santos Arruda a , Jorge Guilherme Bergottini Palieraqui a , Rudymilla Cunha Cordeiro a , Edizio Santos Junior b , Marcelo Beltrão Molento c , Clóvis de Paula Santos a,∗ a
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Parque California, 28013-600 Campos dos Goytacazes, RJ, Brazil b Laboratório de Zootecnia e Nutric¸ão Animal Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, 28013-600 Campos dos Goytacazes, RJ, Brazil c Laboratório de Doenc¸as Parasitárias, Departamento de Medicina Veterinária, Universidade Federal do Paraná, Curitiba, Paraná, Brazil
a r t i c l e
i n f o
Article history: Received 1 October 2009 Received in revised form 8 February 2010 Accepted 21 February 2010 Keywords: Anthelmintic resistance Sheep Ruminants Gastrointestinal nematodes
a b s t r a c t Anthelmintic resistance in parasites maybe a consequence of over-exposing populations of parasites to drugs or from the commerce/transit of animals harboring resistant parasites. Knowledge of the sensitivity of nematodes to anthelmintics is essential to establish an efficient integrated program of parasite control. In Brazil, producers rely on technology transfer from field professionals and non-technical labor for new management strategies of parasite control. The aim of this work was to determine the practices farmers used for anthelmintic management and to monitor drug efficacy on sheep farms from northern and northwestern regions of the state of Rio de Janeiro, Brazil. A questionnaire was sent to 34 farms, and anthelmintics were tested on ten of these farms. Sheep (n = 10/group) were weighed and treated with albendazole, closantel, doramectin, fenbendazole, ivermectin, levamisole, moxidectin, or nitroxynil with their recommended doses. Faeces were collected on the day of treatment and after 7–10 days. The faecal egg count reduction test was evaluated based on RESO 2.0. Among the farmers interviewed, 97% applied commercial anthelmintics to control parasites, 77% rotated anthelmintics annually, 72% used ivermectin as the principal anthelmintic, and 38% applied anthelmintics with a frequency of 30–60 days. On two farms, none of the anthelmintics was efficacious. Levamisole had the best overall efficacy (70%). Albendazole, ivermectin, and fenbendazole were efficacious (above 95%) on only two farms. The present work illustrates the alarming lack of efficacy of drugs even in an area new to sheep farming. It is important to establish alternative strategies of management in a broad program of parasite control for reducing the selection pressure on parasites by the commercially available anthelmintics. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Brazil is the eighth largest producer of sheep and goats in the world, with 25.8 million head. In 2004, the state
∗ Corresponding author. Tel.: +55 22 2739 7180; fax: +55 22 2739 7178. E-mail address: [email protected] (C. de Paula Santos). 0304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2010.02.030
of Rio de Janeiro contributed about 1% of the Brazilian production of sheep (IBGE, 2004). However, the importation of improved breeds, such as Boer, Dorper, Savannah, and Alpine, and the dissemination of the Santa Inês breed, developed in northeastern Brazil (Jardim, 1987), has increased the growth expectation of sheep for meat and milk production in Rio de Janeiro as well as states of the southeastern and central-western parts of the country.
D.G. da Cruz et al. / Veterinary Parasitology 170 (2010) 340–343
One of the most important diseases that limit the production of small ruminants in the tropics and sub-tropics is parasitism by gastrointestinal nematodes (FAO, 1998). In Brazil, the disease is recognized as a major problem in the production of small ruminants (Padilha and Gives, 1996; Ramos et al., 2002). The control of parasites in livestock relies almost exclusively on multiple and regular use of anthelmintics, with no standard monitoring of their efficacy. However, the prophylactic use of anthelmintics has led to the global emergence of drug resistance in helminths and particularly multiple anthelmintic resistances in nematodes of ruminants (Echevarria, 1996; Thomaz-Soccol et al., 2004; Ketzis et al., 2006; Jackson and Miller, 2006). The evolution of anthelmintic resistance is a complex process involving several factors, which are divided into intrinsic, relating to the parasites, and operative, relating to man’s actions. The inadequate management of anthelmintics and their indiscriminate use are among the main operative factors that lead to the occurrence of this phenomenon (FAO, 2003). Molento and Almeida (2004) have reported that sheep farmers in Brazil use anthelmintics as well as pasture rotation and winter grazing as their major strategies for parasite control, with anthelmintics being used from 2 up to 21 times a year in rapid rotation. Lawrence et al. (2006) have associated farm practices with the presence of resistance to half-doses of ivermectin based on faecal egg count reduction tests (FECRT) on sheep farms in New Zealand. The authors found that ivermectin resistance was increased on farms that used this product in ewes as a pre-lambing treatment for ≥3 of the previous 5 years. Another factor identified in association with ivermectin resistance was the importation of resistant parasites with purchased stock. From a questionnaire to sheep farmers in the Taihape area, New Zealand, Hughes et al. (2007) found a high association (p < 0.05) between the presence of ivermectin resistance and the practices of farm management. Resistance was evident to ivermectin on 47% of the farms, benzimidazoles on 54%, levamisole on 37%, and the combination of benzimidazole and levamisole on 5% of the farms. Thus, the knowledge on the sensitivity of nematodes to anthelmintics is one of the most fundamental components for establishing any integrated program of parasite control, along with a single set of on-farm management practices. Therefore, the objective of the present study was to collect reference data of anthelmintic management at the farm level and efficacy based on FECRT in sheep farms in the northern and northwestern regions of the state of Rio de Janeiro, Brazil. 2. Materials and methods 2.1. Farms The study was performed on 34 sheep farms located in the state of Rio de Janeiro in the municipal districts of Campos dos Goytacazes, Porciúncula, Cardoso Moreira, São Francisco de Itabapoana, Santo Antonio de Pádua, São João da Barra, Quissamã, Casimiro de Abreu, Duque de Caxias, and Petrópolis. The data on anthelmintic manage-
341
ment were collected using a questionnaire containing eight questions. Ten farms located in the municipal districts of Campos dos Goytacazes, Cardoso Moreira, Quissamã São Francisco de Itabapoana, Santo Antonio de Pádua, and São João da Barra were randomly selected for testing by FECRT. 2.2. Anthelmintic test The anthelmintic test used Saint Inês sheep, preferentially males, aged between 6 and 10 months. These animals were weighed and distributed into eight groups of 10 animals each and treated with the following anthelmintics: albendazole, closantel, doramectin, fenbendazole, ivermectin, levamisole, moxidectin, and nitroxynil at their recommended doses. 2.3. Anthelmintic efficacy The faeces were collected directly from the rectum of each animal on day zero and 7–10 days after anthelmintic treatment. Two grams of faeces were used for quantifying the number of eggs per gram of faeces (EPG) in a counting chamber (Mc Master), according to the modified technique of Gordon and Withlock (1939). A supersaturated salt solution was used as a flotation fluid (specific gravity: 1.200). The chamber Mac Master detects 50 or more EPG. The efficacy of the products was estimated by the modified test RESO 2.0 (Wursthorn and Martin, 1990). 3. Results and discussion Among the 34 producers interviewed, 97% drenched animals as the main method to control parasitic infections, 77% rotated anthelmintic group, 72% have used or now use ivermectin, and 38% drench animals with a frequency of 30–60 days (Table 1). Ivermectin is the best characterized endectocide of the avermectin group; it was synthesized and initially described in the early 1980 (Chabala et al., 1980). Ivermectin’s endo- and ectoparasitic properties, relative low cost, and high efficacy appeal to farmers and is still the compound most used (Table 1). Although the frequency of use of anthelmintics was relatively similar on the examined properties, with most of the producers drenching animals with short intervals (between 30 and 60 days), some producers treated their animals at an interval of 120 days (Table 1). The majority of producers affirmed that they applied the dose recommended by the manufacturers but admitted to rarely considering the weight of the animals for the calculation of the exact amount of the compound. Therefore, under- or over-dosing was detected, which could influence the development of drug resistance. The improved efficacy observed at property 8 maybe due to the long interval between treatments (240 days), mainly with levamisole and ivermectin. Recent studies based on questionnaires have provided important information about the management practices of anthelmintic use. Hughes et al. (2007) interviewed 84 farmers to ascertain whether particular management or drenching strategies were associated with the presence of resistance. Resistance was evident for ivermectin on 47%, benzimidazoles on 54%, levamisole on 37%, and benzim-
342
D.G. da Cruz et al. / Veterinary Parasitology 170 (2010) 340–343
Table 1 Percentile data for control and anthelmintic management in sheep farms from northern and northwestern regions of the state of Rio de Janeiro from interviews of 34 producers. Question
%
Drench animals
97
Frequency of anthelmintic use 30–60 days 90–120 days More than 120 days Not determined
38 29 9 24
Criterion of anthelmintic use EPG FAMACHA Expected period Clinical signs None
26 3 50 18 3
Dose according to weight and drug labeling Anthelmintic rotation Pasture rotation Knowledge of strategic controla Knowledge of integrated controlb
100 77 50 38 35
Obs: 72% of the producers that use anthelmintics specified that they now use or previously used Ivermectin. a Strategic control is the term used in Brazil for “Drenchplan” or “Wormkill” programs in Australia (Waller, 1986; Echevarria et al., 1988; Vieira et al., 1997). b According to Waller (1999).
idazole/levamizole on 5% of farms. Positive associations (p < 0.05) were determined for resistance to macrocyclic lactones when weaning more than half of the lambs onto paddocks not grazed by lambing ewes since June, not always returning lambs to the same paddock after drenching, and using visual signs to assess ‘worminess’. Measuring drench efficacy between January and March rather than later in the year, and the presence of resistance to benzimidazole or levamisole were associated with a higher apparent prevalence of resistance to macrocyclic lactones (p < 0.05). The prevalence of resistance was lower on farms where management practices, particularly those involving lambs, maintained refugia of unselected nematodes. Cernanská et al. (2008) also obtained information through a questionnaire on practices of worm control and management of sheep on 49 sheep farms. Mean drenching rates for lambs and yearlings/adults were 1.76 and 1.70, respectively. Weights of the heaviest animals were used
to determine anthelmintic doses only on 16.7% of farms. Coprological examinations were performed once a year on 47.9% of farms. The most frequently used drugs during the period from 1999 to 2004 were albendazole and ivermectin. Note that ivermectin as the drug of choice and the failure to weigh animals for determining dose are common to the work presented here. The percentage of efficacy depended on the anthelmintic agent and ranged from: albendazole (0–100%), closantel (0–100%), doramectin (35–100%), fenbendazole (0–100%), ivermectin (0–100%), levamisole (86–100%), moxidectin (71–100%) and nitroxynil (76–100%) (Table 2). Of the farms assessed, only properties numbers 1 and 6 showed anthelmintic inefficiency for all compounds tested. On the other hand, five drugs were effective at property number 8. At properties 9 and 10, only levamisole was effective. The drug that showed the best efficacy was levamisole, being effective in 70% of the properties assessed, followed by moxidectin with an efficacy of 66%. The anthelmintics with the lowest rates of effectiveness were: nitroxynil (33%), doramectin (30%), closantel, fenbendazole, ivermectin (20%), and albendazole (11%) (Table 2). The overall efficacy obtained in the present work corroborates published data. Melo et al. (2003), working with ivermectin and levamisole in the state of Ceará, Brazil, found a 0–100% and an 18–100% effectiveness, respectively. Furthermore, Cunha Filho and Yamamura (1999) showed that in the region of Tamarana, state of Paraná, Brazil, albendazole showed ineffective anthelmintic action with a 0% reduction in EPG while moxidectin had 100% reduction. Similar results were found in The Netherlands where doramectin, albendazole, moxidectin, and levamisole had an efficacy of 15, 87, 99, and 100%, respectively (Borgsteede et al., 2007). Property 1, where no products reduced egg counts, and properties 9 and 10, where only levamisole was effective, had short frequencies of drug treatment (30–60 days). Furthermore, a variety of generic brands of drugs were used without any criteria for drug rotation. Although properties 1 and 9 were the most organized, with good infrastructure, a reasonable set of strategies for sanitation, and adequate nutrition, as endorsed by one veterinarian and one animal scientist, the use of anthelmintics for prophylaxis has encouraged the development of resistance due to
Table 2 Percentile of efficacya of eight anthelmintics on sheep farms from northern and northwestern regions of the state of Rio de Janeiro. Farm
1 2 3 4 5 6 7 8 9 10
Anthelmintics Nitroxynil
Doramectin
Levamisole
Ivermectin
Albendazole
NE 76 100 100 89 87 88 100 90 77
88 100 86 63 100 36 100 75 88 50
86 91 96 100 100 91 100 100 100 100
88 95 17 0 71 58 100 50 55 64
79 90 95 0 NE 0 86 94 85 82
Obs: 10 sheep/each anthelmintic. NE, not evaluated. a Indices lower than 95% are indicative of inefficacy.
Closantel 0 0 84 100 93 75 72 100 83 75
Moxidectin
Fenbendazole
86 100 100 100 100 84 100 100 71 NE
73 70 0 90 100 89 39 100 74 54
D.G. da Cruz et al. / Veterinary Parasitology 170 (2010) 340–343
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