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First report of multiple anthelmintic resistance in nematodes of sheep in Colombia

Abstracts

This study aimed to report the presence of parasites resistant to the most used anthelmintic drugs in sheep in Colombia. Four farms (denominated farm 1, 2, 3 and 4) were selected where the animals were not treated with anthelmintics for two months before the trial. Animals with faecal egg count (FEC) above 150 and of different ages were allocated into six groups, each consisting of at least 5 animals. The drugs and dosages used were: ivermectin 1% (0.2 mg/kg), albendazole 25% (5 mg/kg), fenbendazole 10% (5 mg/kg), levamisole 10% (5 mg/kg), and moxidectin 1% (0.2 mg/kg). Anthelmintic efficacy was determined by the FEC reduction test (FECRT) with a second sampling 14 days post-treatment. The efficacy of albendazole and fenbendazole at farm 1 was above 95%, which was different from the others farms. The FECRT indicated the presence of multidrug resistance in the other farms where no tested drugs showed activity higher than 79% (albendazole: 0 to 55%, fenbendazole: 51.4 to 76.6%, ivermectin: 67.3 to 93.1%, levamisole: 0 to 78.1%, and moxidectin: 49.2 to 64.1%).Haemonchus contortus was the predominant (96%) species, followed by a small presence of Trichostrongylus sp. (3%) andCooperia sp. (1%). Therefore, we report for the first time the existence of multiple anthelmintic resistance in gastrointestinal nematodes of sheep in Colombia.

drug resistance; EPG; FECRT; helminth


Este estudo teve o objetivo de relatar a presença de parasitos resistentes aos fármacos anti-helmínticos mais usados em ovinos na Colômbia. Quatro fazendas (denominadas fazendas 1, 2, 3 e 4) foram selecionadas, onde os animais não foram tratados com anti-helmínticos por dois meses antes do experimento. Animais com contagem de ovos por grama de fezes (OPG) acima de 150 e de diferentes idades foram divididos em seis grupos, sendo que cada composto teve pelo menos cinco animais. Os fármacos e dosagens utilizadas foram: ivermectina 1% (0,2 mg/kg); albendazol 25% (5 mg/kg); fembendazol de 10% (5 mg/kg); levamisol 10% (5 mg/kg) e moxidectina 1% (0,2 mg/kg). A eficácia anti-helmíntica foi determinada pelo teste de redução na contagem de ovos nas fezes (TRCOF), com uma segunda amostragem 14 dias após o tratamento. A eficácia do albendazol e fembendazol na fazenda 1 foi acima de 95%, o que foi diferente das outras fazendas. O TRCOF indicou a presença de resistência a múltiplas drogas nas outras fazendas onde os fármacos testados não mostraram atividade superior a 79% (albendazol: 0%-55%, fenbendazole: 51,4-76,6%, ivermectina: 67,3-93,1%, levamisol: 0-78,1% e moxidectina: 49,2-64,1%). Haemonchus contortus foi a espécie predo minante (96%), seguido por uma pequena presença deTrichostrongylus sp. (3%) e Cooperia sp. (1%). Portanto, nós relatamos pela primeira vez a existência de resistência anti-helmíntica múltipla em nematóides gastrintestinais de ovinos na Colômbia.

resistência anti-helmíntica; OPG; TRCOF; helmintos


INTRODUCTION

Colombia is considered a livestock country and currently a great interest in sheep farming is occurring (Ospina et al. 2011Ospina Ó,Grajales H and Manrique C. 2011. Gestión del conocimiento: mayor producción y competitividad: Perspectivas para los sistemas de producción ovino-caprinos. Rev Med Vet 22: 95-113.). The production is mainly focused on meat with a marginal milk industry (González et al. 2011). The population of sheep was estimated at 3.4 million, located mainly in the states of Boyacá, Magdalena, Córdoba, Cundinamarca and Cesar (FAOSTAT 2008Faostat - Food and Agriculture Organization of the United Nations. 2008. Roma: FAO. [Cited 2013 jul. 5]. Viewed in: http://faostat.fao.org/.
http://faostat.fao.org/...
). There are many factors favorable to this activity, including the great adaptability of the animals to different climates and environments, and the ease of management (Benavides-Ortiz et al. 2010Benavides-Ortiz E, Guerra Múrcia N,Valdivia Trujillo V, Gutiérrez Camacho D, López Rozo M and Serrano Contreras AM. 2010. Reporte de caso: pulicosis por Ctenocephalides felis felis en ovinos y caprinos en la sabana de Bogotá, Colombia. Rev Med Vet 19:123-135. ).

However, there are also many barriers for sheep production. Gastrointestinal parasitism is one of the most important negative economic factors of the small ruminant industry of Colombia (Pulido-Medellín et al. 2014Pulido-Medellín MO, García-Corredor D, Díaz-Anaya A andAndrade-Becerra R. 2014. Pesquisa de parásitos gastrointestinales en pequeñas explotaciones ovinas del municipio de Toca, Colombia. Rev Salud Ani 36(1): 65-69.). In Colombia there are only a few studies relating small ruminants and parasite infections. Herrera et al. (2013)Herrera L,Ríos LA and Salas RZ. 2013. Frecuencia de la infección por nemátodos gastrointestinales en ovinos y caprinos de cinco municipios de Antioquia. Rev MVZ 18(3): 3851-3860. have reported that Haemonchus contortus is the most prevalent nematode, followed by Trichostrongylus spp.,Cooperia spp., Strongyloides spp. andOesophagostomun spp.. These infections have been described as being responsible for decreasing weight gain, delaying puberty, causing anemia and even death (Ensuncho-Hoyos et al. 2014Ensuncho-Hoyos C, Castellano-Coronado A, Maza-Ángulo L,Bustamante-Yánez M andVergara-Garay O. 2014. Prevalencia y grado de infección de nematodos gastrointestinales en ovinos de pelo en pastoreo de cuatro municipios de Córdoba, Colombia. Rev Cient FCV-LUZ 27(5): 414-420.).

Parasite control is usually carried out with the use of anthelmintics, often indiscriminately and without any epidemiological knowledge (Lara 2013Lara DM. 2013. Resistencia a los antihelmínticos: origen, desarrollo y control. Rev Cien Tec Agropec 4(1): 55-71.). The use of such suppressive regime added to inaccurate management strategies, contributes to the selection and establishment of parasites that are resistant to the anthelmintics (Almeida et al. 2010Almeida FA,Garcia Kcod, Torgerson PR and Amarante Aft. 2010. Multiple resistance to anthelmintics by Haemonchus contortus and Trichos trongylus colubriformis in sheep in Brazil. Parasitol Int 59(4): 622-625. ). As parasite resistance is an inherited trait, after every generation there may be an increase in individual parasites that would be able to survive drug treatment (Molento 2004Molento MB. 2004. Resistência de helmintos em ovinos e caprinos. Rev Bras Parasitol Vet 13: 82-87.). Parasite resistance is an alarming scenario in small ruminants worldwide, but there are no data on the magnitude of parasite resistance in sheep in Colombia. Therefore, the aim of this study was to report the lack of efficacy of the most used anthelmintics against gastrointestinal nematodes of sheep in Colombia.

MATERIALS AND METHODS

The experiment was performed from January to July of 2011 on four selected sheep Farms, two located in the state of Cundinamarca and two in the state of Valle del Cauca. The drug test protocol was based on Coles et al. (1992)Coles GC,Bauer C, Borgsteede Fhm, Geerts S, Klei TR, Taylor MA and Waller PJ. 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44:35-44. . The animals used in this experiment were of mix ages, breeds and were not treated to a minimum of 60 days prior to the study. Initial faecal samples were taken from all animals, to perform parasite egg counts per gram (EPG) according to Gordon and Whitlock (1939)Gordon Hmland Whitlock HV. 1939. A new technique for counting nematode eggs in sheep faeces. J Counc Sci Indian Res 12(1): 50-52..

Groups with a minimum of five animals were treated with Ivermectin (IVM) 1% 0.2 mg/kg (Next Mk(r), Technochemistry, Cali, Colombia), Albendazole (ABZ) 25% 5 mg/kg (Insubenzol(r), Insuvin, Bogota, Colombia), Fenbendazole (FBZ) 10% 5 mg/kg (Panacur(r), MSD Salud Animal, Bogota, Colombia), Levamisole (LEV) 10% 5 mg/kg (Levamisol(r), Vicar Pharmaceutical, Bogota, Colombia), Moxidectin (MOX) 1% 0,2 mg/kg (Cydectin(r), Wyeth Inc., Fort Dodge, Bogota, Colombia) and a Control group that received no treatment. The animals were distributed so that the mean EPG was similar between the groups. The animals were weighed before treatment to adjust the correct dose according to the manufacturer recommendations. Although the ideal number of animals would be 6 per group, typical farms in Colombia do not have large numbers of animals and we had to find naturally infected animals with acceptable EPG.

Faecal samples were collected from each animal directly from the rectum, on days: -3, 0 and 14 after treatment. Samples were placed in individually sealed containers and sent to the Laboratory of Parasitology at the La Salle University, located in Bogota for EPG counts. A stool culture was performed using the method described by van Wyk et al. (2004)Van Wyk JA,Cabaret J and Michael LM. 2004. Morphological identification of nematode larvae of small ruminants and cattle simplified. Vet Parasitol 119(4): 277-306., identifying 100 larvae per farm. Farmers from each property completed a questionnaire related to treatment with antiparasitic products in order to better describe the situation of parasite control. All procedures were carried out according to the international practices for animal use and care under the control of an internal committee of the University of La Salle, Bogota, Colombia.

Drug efficacy was determined by the faecal egg count reduction test (FECRT) and the percentage reduction was calculated according to Coles et al. (1992). The efficacy of the anthelmintics was analyzed using the RESO 2.01 Analysis Software (Wursthorn and Martin 1990 Wursthorn L and Martin P. 1990. Reso: faecal egg count reduction test (FECRT) Analysis Program. 2.01. Parkville:CSIRO Animal Health Research Laboratory.). Data was analyzed considering resistance when the effectiveness of the anthelmintic was lower than 95% and when the confidence interval was below 90% (Coles et al. 2006).

RESULTS AND DISCUSSION

The results for the efficacy test in each farm are shown on Table I. The FECRT showed that the response to ABZ and FBZ in farm 1 was different from the others. According to the RESO software, a suspect of resistance was diagnosed for ABZ and FBZ in farm 1 because the treatment revealed an egg count reduction just above 95% (95.5 and 96.5%, respectively) with a confidence interval below 90% (89.6 and 89%, respectively).

Table I
Mean of eggs per gram in pretreatment (Mepgpre) and post-treatment (Mepgpos), percentage of faecal egg count reduction (FECR), and lower 95% confidence interval (CI95%Low) after anthelmintic treatments in sheep in Colombia.

At the other farms, no tested drug showed activity higher than 95% (ABZ: 55 to -15.1%; FBZ: 76.6 to 51.4%; IVM: 93.1 to 67.3%; LEV: 78.1 to -8.1%; and MOX: 49.2%, confirming anthelmintic resistance to all tested products.

In most parts of Latin American countries there are very few restrictions or even none for buying veterinary medicines and farmers are able to purchase them without prescriptions (Molento 2007, Molento et al. 2011). In Colombia this is not different, where the prophylactic use of triclabendazole to control sheep nematodes led to the emergence of Fasciola hepatica resistance detected by the FECRT (Flanagan et al. 2011Flanagan A,Edgar Hwj, Gordon A, Hanna Reb, Brennan GP and Fairweather I. 2011. Comparison of two assays, a faecal egg count reduction test (FECRT) and a coproantigen reduction test (CRT), for the diagnosis of resistance to triclabendazole in Fasciola hepatica in sheep. Vet Parasitol 176(2): 170-176.).

Parasite resistance was determined in all tested farms in Colombia reflecting the same situation found in Uruguay (Bonino and Mederos 2003Bonino J andMederos A. 2003. Resistencia antihelmíntica en ovinos. Rev Plan Agropec1: 42-44. ), Argentina (Caracostantogolo et al. 2006Caracostantogolo J, Castaño R,Cutullé C, Cetrá B, Lamberti R and Olaechea F. 2006. Evaluación de la resistencia a los antihelmínticos en rumiantes en Argentina . In: Eddi C and Vargas Terán M (Eds), Resistencia a los Antiparasitarios Internos en Argentina.FAO Producción y Sanidad Animal, Roma, Italia, p.7-34.), Peru (Tang-Ploog 2005Tang-Ploog JF. 2005. Evaluación nematicida y de tolerancia de una formulación al 1% de ivermectina (Bovimec(c)) en ovinos. Agrovetmarket[online]. 2005[cited 2013 Jul 30]. Avaliable from:http://www.vetermex.com/Pdfs/Trabajos_investigacion/ Bovimec_LA.
http://www.vetermex.com/Pdfs/Trabajos_in...
), Venezuela (Muñoz et al. 2008) and Brazil (Almeida et al. 2010, Cezar et al. 2010Cezar AS,Toscan G, Camillo G, Sangioni LA, Ribas HO and Vogel Fsf. 2010. Multiple resistance of gastrointestinal nematodes to nine different drugs in a sheep flock in southern Brazil. Vet Parasitol 173(1):157-160., Cruz et al. 2010Cruz DG,Rocha LO, Arruda SS, Palieraqui Jgb, Cordeiro RC, Santos Junior E, Molento MB and Santos CP. 2010. Anthelmintic efficacy and management practices in sheep farms from the state of Rio de Janeiro, Brazil. Vet Parasitol 170(3): 340-343.). Veríssimo et al. (2012) determined resistance to both ABZ and IVM in 89.3% of the flocks, and to ABZ and MOX in 82.8% of the 30 sheep flocks studied in São Paulo, Brazil. Sczesny-Moraes et al. (2010)Sczesny-Moraes EA, Bianchin I,Silva Kfd, Catto JB, Honer MR and Paiva F. 2010. Resistência anti-helmíntica de nematóides gastrintestinais em ovinos, Mato Grosso do Sul.Pesq Vet Bras 30(3): 229-236. reported resistance to ABZ, closantel (CLO), IVM, LEV, MOX and trichlorfon (TRI) in 11 farms out of 16 in Mato Grosso do Sul, Brazil. Multidrug resistance to ABZ, CLO, IVM and LEV was found in 50% of the 32 sheep farms in Argentina (Caracostantogolo et al. 2006).

Haemonchus contortus was found in 100% of the stool culture before the treatment and was still predominant (96%) after anthelmintic use, followed by a small incidence of Trichostrongylus axei (3%) andCooperia sp. (1%).

The fact that H. contortus was the only nematode found in the pre-treatment stool culture may be due to its high prevalence throughout South America (Suárez and Busetti 2009, Almeida et al. 2010) including Colombia (Pulido-Medellín et al. 2014). Herrera et al. (2013) analyzed 95 stool samples of small ruminants from five municipalities in the state of Antioquia, Colombia, where 66.3% (63/95) were positive to H. contortus. Martinez (2011)Martinez O. 2011. Estudio de prevalencia de parásitos gastrointestinales en ovinos del municipio de Oicata-Boyaca, Tunja. Universidad Nacional Abierta y a Distancia (UNAD), 64 p., in a survey conducted in Oicata, state of Boyaca, examined 100 samples of sheep from five different farms and in 53% (53/100) of them, the presence of H. contortus was detected. In a study conducted in the state of Cordoba, Colombia, 97.7% (170/174) of the stool samples from sheep were contaminated by gastrointestinal Strongylidae. In 40.83% (71/174) of the coprocultures, the authors observed the presence of the infective stage larvae of Haemonchus sp. (Ensuncho-Hoyos et al. 2014).

The resistance to H. contortus to all drug classes have being reported worldwide (Cudekova et al. 2010Cudekova P,Varady M, Dolinska M and Konigova A. 2010. Phenotypic and genotypic characterisation of benzimidazole susceptible and resistant isolates of Haemonchus contortus. Vet Parasitol172: 155-159.,Fauvin et al. 2010Fauvin A,Charvet C, Issouf M, Cortet J, Cabaret J and Neveu C. 2010. cDNA-AFLP analysis in levamisole-resistant Haemonchus contortus reveals alternative splicing in a nicotinic acetylcholine receptor subunit. Mol and BiochemParasitol 170(2): 105-107., Beech et al. 2010Beech R,Levitt N, Cambos M, Zhou S and Forrester SG. 2010. Association of ion-channel genotype and macrocyclic lactone sensitivity traits in Haemonchus contortus. Mol Biochem Parasitol 171(2): 74-80. ). To face this problem, effective new tools need to be developed and implemented for a sustainable control of parasites (Macedo et al. 2012Macedo IT,Bevilaqua CM, Oliveira L, Camurça-Vasconcelos AL, Morais SM, Machad LK and Ribeiro Wlc. 2012. In vitro activity of Lantana camara, Alpinia zerumbet, Mentha villosa and Tagetes minuta decoctions on Haemonchus contortus eggs and larvae. Vet Parasitol 190(3-4): 504-509.). Colombian research centers are studying new alternative methods, such as nematophagous fungi and herbal medicine (Pino-Benítez and Stashenko 2006Pino-Benítez N and Stashenko E. 2006. Contribución al estudio de la flora medicinal en el departamento del Chocó, Colombia. Fitoterapia 6(1):125.,Orozco et al. 2009Orozco M,Álvarez V, Jiménez A and Acuña Ó. 2009. In vitro assessment of nematophagus fungi for biological control of gastrointestinal nematodes of ruminants. Rev MVZ 14(3): 1820-1830.).

To date, no registered cases of multiple anthelmintic resistance to gastrointestinal nematodes have been reported in sheep in Colombia. Thus, it was very important to study the drug efficacy situation. In the studied regions of the country, there is a predominance of small farms with low levels of investment, which makes the obtained epidemiological information of paramount importance for the local farmers and breeders. We have demonstrated for the first time the existence of multidrug resistant parasites. New studies need to be conducted to further look into other regions of the country and using other compounds.

On the questionnaire, the farmers replied that the anthelmintic use was performed at every 30-day interval in two farms and in between two and three month-intervals. On three farms, the animals were weighted without the use of a scale before the treatment, and only one farmer used the FAMACHA method for partial selective treatment. Only one farmer had some knowledge about parasitic diseases and the drug resistance issue. About the choice of anthelmintic drugs, farmers reported that the choice was based just on the availability of products. Sheep producers should not neglect the present management data because a failure in health management could affect the production of meat and wool (Manfredi et al. 2010Manfredi MT,Di Cerbo AR, Zanzani S and Stradiotto K. 2010. Breeding management in goat farms of Lombardy, northern Italy: Risk factors connected to gastrointestinal parasites. Small Ruminant Res 88(2): 113-118.). We consider that the strategies for parasite control used by the farmers were responsible for drug failure, as the farmers reported the use of the suppressive strategy for parasite control as a standard sanitary protocol.

The use of questionnaires is an important tool to check how the parasite control is made and to better understand the local epidemiological situation (Nielsen et al. 2006Nielsen MK,Monrad J and Olsen SN. 2006. Prescription-only anthelmintics-a questionnaire survey of strategies for surveillance and control of equine strongyles in Denmark. Vet Parasitol135(1): 47-55.). This practice is used by research groups in an attempt to obtain more accurate worm control data (Čerňanská et al. 2008). In our case, it was determined that in general farmers do not know proper methods of parasite control, nor applied different techniques of sanitary management. In an interview conducted in Rio de Janeiro, Brazil, with 34 sheep producers, although a better technical knowledge about parasitic resistance and its implications was observed, the results were not satisfactory (Cruz et al. 2010). Only by understanding all the epidemiological factors involved in a parasite infection will a correct diagnosis be able to be made and the appropriate set of management strategies be used (Aagard-Hansen et al. 2010).

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  • Sczesny-Moraes EA, Bianchin I,Silva Kfd, Catto JB, Honer MR and Paiva F. 2010. Resistência anti-helmíntica de nematóides gastrintestinais em ovinos, Mato Grosso do Sul.Pesq Vet Bras 30(3): 229-236.
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Publication Dates

  • Publication in this collection
    05 Feb 2016
  • Date of issue
    Mar 2016

History

  • Received
    22 July 2014
  • Accepted
    28 May 2015
Academia Brasileira de Ciências Rua Anfilófio de Carvalho, 29, 3º andar, 20030-060 Rio de Janeiro RJ Brasil, Tel: +55 21 3907-8100 - Rio de Janeiro - RJ - Brazil
E-mail: aabc@abc.org.br