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Revista Brasileira de Parasitologia Veterinária

On-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.22 no.2 Jaboticabal Apr./June 2013

https://doi.org/10.1590/S1984-29612013000200047 

Full Article

Susceptibility of Rhipicephalus(Boophilus) microplus (Acari: Ixodidae) to pyrethroids and their associations in Pernambuco, Brazil

Susceptibilidade de Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) a piretróides e suas associações em Pernambuco, Brasil

Breno Barros de Santana1 

Rafael Antonio Nascimento Ramos2  3 

Marília de Andrade Santana3 

Leucio Cãmara Alves3 

Gílcia Aparecida de Carvalho1  * 

1Unidade Acadêmica de Garanhuns, Universidade Federal Rural de Pernambuco - UFRPE, Garanhuns, PE, Brasil, Unidade Acadêmica de Garanhuns, Universidade Federal Rural de Pernambuco – UFRPE, Garanhuns, PE, Brasil

2Dipartimento di Medicina Veterinaria, Universitá degli Studi di Bari, Valenzano, Bari, Italy

3Laboratório de Doenças Parasitárias dos Animais Domésticos, Departamento de Medicina Veterinária, Universidade Federal Rural de Pernambuco - UFRPE, Recife, PE, Brasil, Laboratório de Doenças Parasitárias dos Animais Domésticos, Departamento de Medicina Veterinária, Universidade Federal Rural de Pernambuco – UFRPE, Recife, PE, Brasil


ABSTRACT

The synthetic pyrethroids and their associations have been widely used for controlling Rhipicephalus (Boophilus)microplus. The frequent use of acaricides has been inducing the development of resistance in the tick populations. The aim of this study was to assess the susceptibility of R. (B.)microplus populations to pyrethroids and their associations in the region of Garanhuns, Pernambuco, Brazil. In addition, the level of information among farm owners regarding tick control measures was investigated. Ticks were collected directly from naturally infested dairy cattle in the region and were exposed to pyrethroids and their associations. At the same time, an epidemiological questionnaire was applied with the aim of investigating the level of information among the farmers. The results reported here indicate thatR. (B.) micropluspopulations in the dairy region of Garanhuns show resistance to pyrethroids and their associations, except when the product is associated with piperonyl butoxide. Regarding the results from the epidemiological survey, it was seen that there is a considerable lack of information among the farmers in relation to ixodid control measures. The level of ticks resistance to acaricides varied widely across the region studied. No alternative control programs have been implemented among these farms, thus demonstrating that there is a need for more information relating to the biology and control of R.(B.) microplus.

Key words: Ticks; resistance; acaricide; in vitro test; bovine; microregion of Garanhuns

RESUMO

Os piretróides sintéticos e associações são acaricidas amplamente utilizados para o controle do Rhipicephalus (Boophilus) microplus. O uso frequente destes fármacos tem induzido o surgimento de populações de carrapatos resistentes. Objetivou-se neste estudo avaliar a susceptibilidade de populações de R. (B.) microplus aos piretróides e associações. Além disso, investigou-se o nível de informações dos proprietários com relação ás medidas de controle utilizadas. Os carrapatos foram coletados diretamente de bovinos naturalmente infestados na região leiteira de Garanhuns, Pernambuco e expostos a piretróides e suas associações. Contemporaneamente, foi aplicado um questionário epidemiológico com o objetivo de avaliar o nível de informação dos produtores. Os resultados aqui obtidos demonstram que populações de R. (B.) microplus provenientes da região leiteira de Garanhuns apresentam resistência aos piretróides, exceto quando o produto está associado com butóxido de piperonila. Em se tratando dos resultados referentes ao inquérito epidemiológico, verificou-se considerável falta de informação por parte dos produtores com relação ás medidas de controle de ixodídeos. Assim, verifica-se que o nível de resistência aos acaricidas é muito variável na região estudada e que não há, nas propriedades, a adoção de programas alternativos de controle, demonstrando a necessidade de maiores informações relacionadas á biologia e ao controle do R. (B.) microplus.

Palavras-Chave: Carrapatos; resistência; acaricida; teste in vitro; bovino; microrregião de Garanhuns

Introduction

Rhipicephalus (Boophilus)microplus (Canestrini, 1888) is considered the main tick species affecting cattle in tropical and subtropical areas (MURRELL; BARKER, 2003; CANÇADO et al., 2009). Its importance is related to several types of harm that it causes to these animals, such as reduction in productivity (MARQUES, 2006) and transmission of pathogens (DANTAS-TORRES, 2007).

Currently, its control is based on use of chemical acaricides (SILVA, 2008). Intensive use of acaricides has been inducing the development of resistantR. (B.) microplus populations (CAMPOS JÚNIOR; OLIVEIRA, 2005; GOMES et al., 2011). This resistance may be developed due to increased gene expression or enzyme activity, as well as neuroreceptor and sodium channel mutations that impede penetration by these chemical products (MARTIN et al., 2003; OAKESHOTT et al., 2003).

Ticks resistance has been reported in various countries (LI et al., 2004; ROSADO-AGUILAR et al., 2008), including Brazil (CAMPOS JÚNIOR; OLIVEIRA, 2005; GOMES et al., 2011), where, there are reports in Rio Grande do Sul (PATARROYO; COSTA, 1980), Minas Gerais, Bahia and Espírito Santo (LEITE et al., 1995), and São Paulo (SOARES et al., 2001). In the state of Pernambuco, Santana et al. (2001) verified that synthetic pyrethroids and amitraz showed lower effectiveness, whereas organophosphates and carbamates displayed good action.

Considering this phenomenon of resistance, tick control should be based on prudent and rational use of acaricides coupled with environmental management. Moreover, actions to provide better information are also needed in order to achieve better understanding with regard to correct use of these chemicals products. Therefore, the aim of the present study was to assess the susceptibility ofR. (B.) microplus populations to pyrethroids and their associations. In addition, the level of information among farmers regarding control strategies against this ixodid was investigated.

Materials and Methods

Ticks and study area

From August 2010 to July 2011, engorged females of R.(B.) microplus (150 specimens on each farm) were collected from naturally infested cattle from the municipalities of Caetés, Canhotinho, Garanhuns, São João, Brejão, Terezinha and Bom Conselho, located in the dairy region of Garanhuns, state of Pernambuco. In each municipality, two farms were evaluated. The area studied is characterized by a mild climate during the summer and low temperatures in the winter. The mean annual temperature is about 20 °C and high precipitation is observed between April and June. Over the same period (April - June) higher numbers of engorged females of R. (B.) microplusare detected on the animals. The diet of these cattle is based on Bermuda grass and Elephant grass. During the dry season, forage cactus is also used.

Acaricide tests

The ticks were subjected to the "Adult Immersion Test" (AIT) (DRUMMOND et al., 1973), which is anin vitro resistance detection assay. The following commercial acaricides based on pyrethroids and their associations were used: 1) cypermethrin 20.0 g + chlorpyrifos 50.0 g; 2) cypermethrin 15.0 g + chlorpyrifos 25.0 g + citronellal 1.0 g and 3) cypermethrin 15.0 g + chlorpyrifos 25.0 g + piperonyl butoxide 15.0 g + citronellal 1.0 g. The dilution of the products were realized following the manufacturer's instructions.

Ten engorged females (per group) with homogeneous weight were placed in Petri dishes. The test groups were immersed in the acaricides for five minutes and the controls were immersed in distilled water. The females were maintained in an incubator under controlled conditions (26 ± 1 °C, 80 ± 5% relative humidity and scotophase), for 16 days to lay eggs. After this had taken place, the eggs were placed in individual 10 mL glass vials, which were closed with a cotton plug and kept in the incubator under controlled conditions (see above).

The acaricide efficiency (AE) was obtained using the following parameters: engorged female weight, eggs weight and eggs hatching percentage. The commercial products were considered to be efficient if AE ≥ 95% (DRUMMOND et al., 1973).

Epidemiological questionnaire

Simultaneously with the tick collection, an epidemiological survey was conducted in order to investigate the level of information among the farmers. They were asked about the main problems in the herd, the level of tick infestation (i.e. low infestation: < 20 engorged females/animal; moderate infestation: from 21 to 50 engorged females/animal; high infestation: > 50 engorged females/animal), the degree of production loss and the tick control measures used, such as the acaricide used, frequency of use, instructions for use and alternative control measures.

Results and Discussion

Acaricide tests

The overall results from the acaricide efficacy tests (Adult Immersion Test) are reported in Table 1.

Table 1. Mean efficacy (%) of commercial acaricides formulations based on pyrethroids and their associations, againstRhipicephalus (Boophilus)microplus in the dairy region municipalities of Garanhuns, Pernambuco, Brazil, from August 2010 to July 2011. 

Municipalities Acaricides / Efficacy (%)
cypermethrin + chlorpyrifos (%) cypermethrin + chlorpyrifos + citronellal (%) cypermethrin + chlorpyrifos + piperonyl butoxide + citronellal (%)
Caetés 99.73 98.70 100
Canhotinho 99.79 99.40 100
Garanhuns 78.75 95.95 100
São João 90.30 77.91 100
Brejão 57.08 84.15 100
Terezinha 56.61 68.33 100
Bom Conselho 55.82 70.35 100

% - percentage.

The present study demonstrated that in the microregion of Garanhuns, state of Pernambuco, R. (B.)microplus showed resistance to pyrethroids and their associations, except when associated with piperonyl butoxide. Particularly, the tick populations in Caetés and Canhotinho did not show any resistance to any of the acaricides formulations studied.

According to Mendes et al. (2007), Koller et al. (2009), Camillo et al. (2009) and Gomes et al. (2011), resistance to these compounds is widespread in Rio Grande do Sul, Paraná, Mato Grosso do Sul, São Paulo, Minas Gerais and Rio de Janeiro. Tick populations resistant to various acaricide groups have also been detected in other regions of the country, including the northeastern region (SANTANA et al., 2001; SILVA et al., 2005).

The main chemical used in this study (cypermethrin) was shown to be very effective during the 1980s (PEREIRA; LUCAS, 1987). However, widespread use has reduced its effectiveness over time, with reports of low efficacy, i.e. as low as 40% (SOUZA et al., 2003). The efficacy values obtained in the present study (Table 2) demonstrated that R.(B.) microplus from various locations was resistant to cypermethrin, following the same profile as previously observed (SOUZA et al., 2003).

The results from the present study demonstrated that acaricides containing organophosphates were effective in controlling R.(B.) microplus when combined with piperonyl butoxide. A similar result was observed by Koller et al. (2009) in Mato Grosso do Sul, with 100% efficiency when a combination of cypermethrin and chlorpyrifos with piperonyl butoxide and citronellal was used.

The incorrect use of acaricides has contributed towards the process of induction of tick resistance to various chemical bases and has allowed occurrences of cross-resistance, as reported in Mexico by Amendáriz-González (2003). A similar situation has been seen to occur in Brazil regarding tick control (ROCHA et al., 2006; FARIAS et al., 2008) and management and control of the horn fly (Haematobia irritans) (BARROS, 2005; BARROS et al., 2007). In this case, because of the unspecific nature of most of the products used, controlling one species may interfere with the susceptibility of another species. In addition to the numerous factors mentioned above, it is important to highlight that R. (B.)microplus may present resistance faster than seen in other tick species, due to the shorter time between generations.

Interestingly, in this study, it was also observed that pyrethroids and their associations were effective on farms where rotational grazing was implemented, thus demonstrating the importance of alternative control measures.

Epidemiological questionnaire

Regarding the results from the questionnaire applied, there was a lack of information among the farmers, since in most cases the control measures adopted were implemented erroneously.

From applying the epidemiological questionnaire, it was observed that the degree of tick infestation among the animals was high on 40% of the farms, moderate on 34% and low on 26%. The spraying method (60%) was most frequently used on the farms for applying the acaricides, followed by the injectable method (40%). Application of acaricides through a spray is an important factor that accelerates resistance (BIANCHI et al., 2003; BARROS et al., 2007), because when spraying is not carried out properly, the tick population receives an underdose of acaricide and resistant populations are thus selected.

The chemical groups most frequently used by the farmers were associations of organophosphate and pyrethroid, followed by macrocyclic lactones and formamidines, with rates of 47%, 40% and 13%, respectively. The lack of knowledge among the farmers regarding the main chemical groups induced use of a wide variety of acaricides with the same active agent, in which only the commercial name was changed. Intense use of macrocyclic lactones and pyrethroids was noted in the present study. On the other hand, rotation of chemical bases without any criteria for doing so exposed the ticks to all the chemical groups available on the market, thus favoring selection of multiresistant tick populations. According to Martins et al. (2005), a chemical group should only be changed if the treated population is able to survive and perform oviposition with fertile eggs. Generally, the period between changes should not be less than two years. Based on this evidence, associations of chemical groups available on the market (e.g. pyrethroids and organophosphates) can be used in order to avoid selection of resistant ticks (MARTINS et al., 2005).

When the farmers were asked about their frequency of use of acaricides, 26% reported that application of the acaricide was performed at intervals of 60 days, 20% at intervals of 30 days, 20% at intervals of 21 days, 20% weekly and 14% only when tick infestations were detected visually. Regarding the effectiveness of control, 53% of the farmers reported good levels of control, and 47% fair control. With regard to environmental management, only 7% of the farms were practicing some alternative form of control, in relation to their facilities or the environment. Rotational grazing was the only environmental management reported by the farmers.

Alternative control measures such as care facilities and rotational grazing can be implemented in order to reduce the infestation level of ectoparasites in the environment and consequently reduce parasitism in the animals. The absence of these measures among the farms studied may also have contributed towards the low levels of pesticide efficacy observed.

Conclusions

The level of resistance of the ticks to commercially available acaricides formulations studied here (1. cypermethrin 20.0 g + chlorpyrifos 50.0 g; 2. cypermethrin 15.0 g + chlorpyrifos 25.0 g + citronellal 1.0 g; 3. cypermethrin 15.0 g + chlorpyrifos 25.0 g + piperonyl butoxide 15.0 g + citronellal 1.0 g) varied widely across the dairy region of Garanhuns. The results regarding the levels of resistance of R.(B.) microplus to the acaricides tested are probably related to indiscriminate use of products based on pyrethroids and associations, and absence of any strategic control program, thus demonstrating the need for more information for farmers regarding the biology and control of this tick species.

Unfortunately, the data described here follow the same pattern as seen in other regions of Brazil. Therefore, there is a need for veterinarians to implement actions that also focus on education in the field regarding correct and rational use of acaricides. In addition, use of environmental control measures should be encouraged.

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Received: December 13, 2012; Accepted: April 18, 2013

*Corresponding author: Gílcia Aparecida de Carvalho, Unidade Acadêmica de Garanhuns, Universidade Federal Rural de Pernambuco - UFRPE, Av. Bom Pastor, s/n, Boa Vista, CEP 55292-270, Garanhuns, PE, Brasil,e-mail: gilciasilva@yahoo.com.br

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