Prevalence and potential risk factors for organophosphate and pyrethroid resistance in Boophilus microplus ticks on cattle ranches from the State of Yucatan, Mexico

doi:10.1016/j.vetpar.2005.05.069

Veterinary Parasitology

Volume 136, Issues 3–4, 31 March 2006, Pages 335-342

https://doi.org/10.1016/j.vetpar.2005.05.069 Get rights and content

Abstract

A cross-sectional study was carried out in order to investigate the association between management risk factors and the prevalence of organophosphate (OP) and synthetic pyrethroid (SP) resistance in Boophilus microplus ticks in Yucatan State, Mexico. Ninety-eight cattle ranches were randomly selected and a sample of 20–30 engorged female B. microplus ticks was collected at each. The modified larvae packet test was used to detect OP and SP tick resistance. A questionnaire was administered on each ranch. For risk factors, four reference types of response were used: Tuxpan (resistant to coumaphos, chlorfenvinphos and diazinon), Parkhurst (resistant to flumethrin, deltamethrin and cypermethrin), Lamington (resistant to flumethrin in absence of deltamethrin and cypermethrin) and Marmor (resistant to flumethrin and cypermethrin in absence of flumethrin). A primary screening was performed using 2 × 2 contingency tables of exposure variables. All variables with p ≤ 0.20 were analyzed by a logistic regression. The prevalence of B. microplus resistance to OP and SP groups were 83.70% and 66.32%, respectively. The prevalence for a single chemical compound was: diazinon (80.60%), coumaphos (45.90%), chlorfenvinphos (35.70%), flumethrin (63.28%), deltamethrin (61.22%), and cypermethrin (59.18%). The prevalence type of response was: Tuxpan (34.16%), Parkhurst (58.16%), Lamington (4.08%), and Marmor (4.08%). The use of a different tick control program was the risk management factor associated with the Parkhurst type of response. It is concluded that the prevalence of cattle ranches with B. microplus resistant to OPs and SPs in Yucatan, Mexico, is a current problem, and a treatment interval of ≥6 times/year and use of a tick control program (macrocyclic lactones and pasture burn) different from standard recommended programs are risk factors associated with the Parkhurst type of response.

Introduction

Boophilus microplus (Canestrini) is an endemic cattle pest in tropical and subtropical regions of the world, causing major economic losses to cattle producers through direct physical effects on the parasitized animal and indirectly through diseases transmitted by the tick's bite (Solorio et al., 1999).

Acaricides, including organophosphates (OP), synthetic pyrethroids (SP), amidines and macrocyclic lactones (Taylor, 2001, Aguilar-Tipacamu and Rodriguez-Vivas, 2003) play a major role in controlling Boophilus ticks in Mexico and the intensive use of these chemicals has led to the development of resistant tick populations (Fragoso et al., 1995).

In Mexico, resistance of B. microplus to OP and chlorinated hydrocarbon acaricides was first documented in 1981, 7 years after intensive use was instigated. It was demonstrated that the prevalence of the resistance was higher in the eastern and northeastern region of Mexico, and therefore the federal authorities of the Animal Health Division in 1986 authorized the use of SPs and recently, amidines, as an alternative to control OP resistant ticks (Aguirre and Santamaría, 1986). Seven years later, in 1993, the first cases of SP resistance were detected by the larval packet test with discriminating doses (Stone & Haydock); and B. microplus-resistant strains were identified as co-resistant to SPs and OPs, with a wide geographical distribution in the livestock regions of the Gulf of Mexico, northeastern and southern Tamaulipas, eastern San Luis Potosi, southeastern Tabasco, northeastern Chiapas, and all of the State of Veracruz (Ortiz et al., 1995). However, in southeastern Mexico, no epidemiological study has yet been carried out. For this reason, a cross-sectional study was performed in order to investigate the possible association between management risk factors and the prevalence of B. microplus resistant to OPs and SPs in cattle ranches from the State of Yucatan, Mexico.

Section snippets

Study background

The State of Yucatan is located in the southeast of Mexico between the co-ordinates 19°30′ and 21°35′ north latitude and 90°24′ west longitude. The climate of the state is sub-humid tropical with a summer rainy season. The monthly maximum temperature varies from 35 °C to 40 °C and the mean temperature is 26.6 °C. The relative humidity (RH) varies from 65% to 100% (mean RH is 80%) and the annual rainfall varies from 415 mm to 1290 mm depending on the area. There are two distinct seasons: rainy (from

Questionnaire survey

The questionnaire survey described the management practices of ranchers from Yucatan, Mexico. With regard to ranch size, 29.6% of the ranches had <50 animals, 27.6% had 50–100 animals, 21.4% had 101–200 animals and 21.4% had >200 animals. In relation with stocking density, 73.5% of the ranches had ≤1 animal/ha and 26.5% had >1 animal/ha. A large proportion of ranches (79.6%) used crossbred Bos indicus, 16.3% Bos indicus and 4.1% Bos taurus.

All ranches used acaricides to control ticks. With

Discussion

The present study is the first in Mexico to detect the prevalence and possible risk factors associated with OP and SP resistance in B. microplus using a simple random sampling model. In Mexico, the presence of resistance to OP and SP acaricides has developed within a period of approximately 7 years of intensive use of different classes of acaricides (Ortiz et al., 1995).

In the present study, the prevalence of B. microplus resistance in Yucatan to OPs tested was 83.7%. This prevalence is higher

Acknowledgments

This project was founded by CONACYT-SAGARPA Mexico (SAGARPA-2002-C01-1754). We are very grateful to CONACYT for supporting Miguel Alonso-Diaz and Flavio Rodriguez-Arevalo in their Masters Degree course. Thanks are also due to the ranchers (UGROY and UGRY) who generously gave their time and hospitality. The authors gratefully acknowledge the technical assistance of the staff of the Centro Nacional de Servicios de Constatación en Salud Animal, SAGARPA, Jiutepec, Morelos. Our thanks to Dr. Phil

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Rhipicephalus microplus is a cattle tick widely distributed in tropical and subtropical areas. Various acaricides are used and applied to control the ticks, but resistance is common. The objectives of this study were to evaluate the spatial distribution of resistance to the most commonly applied acaricides (amitraz, ivermectin, and alpha-cypermethrin) in ticks and assess potential risk factors associated with tick resistance in a strip between ±0.5° latitude of the continental part of Ecuador. Larval package tests were used to evaluate the level of acaricide resistance in 96 cattle farms. The association between 11 farm management and 8 ecological variables and acaricide resistance and multi-resistance was evaluated. Dose-response models were used to study the level of resistance. 72 % (69/96), 70 % (67/96), and 64 % (61/96) of farms had ticks resistant to amitraz, ivermectin, and alpha-cypermethrin, respectively. Multi-resistance was also widespread. Larger herds and dairy farms had a significantly higher probability of resistance for three commonly used acaricides. Environmental factors related to rainfall were also associated with acaricidal resistance presence. Ivermectin resistance was associated with use of the acaricide (OR = 8.9909; 7.7519-10.2300), mean temperature (OR = 1.3205;1.0742-1.6799)), and inversely associated with paddock rotation (OR = 0.1753; 0.0294-0.7836), and precipitation of the wettest month (BIO13) (OR = 0.9903; 0.9839-0.9957); amitraz with use of the acaricide (OR = 4.3934; 3.3679-5.4188), precipitation seasonality (BIO15) (OR=0.9742; 0.9542-0.9925), and precipitation (OR = 0.9995; 0.9994-0.9999); and alpha-cypermethrin with precipitation (OR=0.9995; 0.9990-0.9999) and use of the acaricide (OR = 14.4597; 13.4343-15.4852). In conclusion, acaricide resistance was widespread in our study area. Better-integrated tick management and environmentally friendly control strategies are required to reduce the use of acaricides while limiting tick-associated damage in herds.
Identification of the G184C, C190A and T2134A mutations in the para-sodium channel gene of the southern cattle tick Rhipicephalus (Boophilus) microplus associated with resistance to cypermethrin in northern Veracruz, Mexico
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The southern cattle tick (Rhipicephalus microplus) represents one of the ectoparasites with the greatest distribution worldwide. Infestations by this arthropod can cause a decrease in the production of meat and milk, as well as anaemia and the transmission of bacterial and parasitic agents. For this reason, several active molecules have been developed to control these arthropods. A widely used group of ixodicides are pyrethroids, especially cypermethrin, which have knockdown effects on ticks. Resistance to cypermethrin has been reported in ticks since the 2000s; it was registered for the first time in Mexico in 2009. Even though multiple studies have evaluated resistance with conventional tests, there are few studies in Mexico that have identified the presence of single nucleotide polymorphisms (SNPs) associated with resistance. Hence, the aim of this work was to monitor three mutations associated with resistance in the sodium/chlorine channel in eight populations of ticks from northern Veracruz. Engorged adult females were collected from which genomic DNA was extracted. Subsequently, three mutations in domains II and III of para‑sodium channel gene were detected by conventional PCR and sequencing. Global alignments were done with the reference sequences deposited in GenBank. A total of 116 engorged females were analysed, of which 10 tested positive for G184C and C190A of domain II of the para‑sodium channel gene. T2134A was present in domain III in a single production unit. This is the first work where molecular monitoring of cypermethrin resistance has been carried out in the northern zone of the state of Veracruz.
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Ticks are important ectoparasites with a worldwide distribution. The most commonly used method for tick control involves the use of acaricides. The main problem is that its indiscriminate use has led to the selection of resistant tick populations. Glutathione transferases (GSTs) are enzymes that play an important role in the detoxification of several types of compounds used in commercial tick control products. This work aims to find new bioactive molecules through in vitro assays with a panel of 160 molecules with putative inhibitory activity on the Rhipicephalus microplus GST enzyme (RmGST). Also, selected molecules were tested against GSTs from other tick species; Rhipicephalus decoloratus, Amblyomma variegatum, Rhipicephalus appendiculatus, and Haemaphysalis longicornis. The first screening on RmGST identified 30 compounds with the ability to modify the enzymatic activity of this enzyme. These compounds included different chemical families, like chalcones, diarylideneketones, flavone, thiazoles, thiourea, steroids, thiadiazines, indazoles, and hydrazine. The most potent compounds against RmGST belong to the diarylideneketones family with an inhibition concentration of 50% of activity (IC₅₀) between 7-50 μM. Interestingly, one of the most potent compounds was also an inhibitor of the GST from other tick species. Experiments with R. microplus adults and larvae showed toxicity at 150 μM, suggesting a potential acaricidal effect of these molecules.
Resistance in ectoparasites
2022, Insect Resistance Management: Biology, Economics, and Prediction, Third Edition
Significant amounts of pesticides are used to control ectoparasites of humans, livestock, pets, and even domesticated honey bees. Thus it should not be surprising that many of these ectoparasites have evolved resistance to the pesticides. The various case studies in this chapter demonstrate that alternatives to pesticides must be considered. Improving integrated pest management through knowledge of the pest’s behavior should be the focus of future research.
Development of acaricide resistance in tick populations of cattle: A systematic review and meta-analysis
2022, Heliyon
The development of acaricide resistance in ticks infesting cattle is a major problem in the livestock industry in tropical and subtropical regions worldwide. To determine the current global trends and prevalence of acaricide resistance development (ARD) in tick populations of cattle, a systematic review and meta-analysis with an emphasis on Rhipicephalus (Boophilus) microplus was conducted. Data searches from five English electronic databases yielded 88 journal articles published between 1992 and 2020. In total, 218 in-vitro bioassays were used to investigate 3939 tick populations of cattle; of these, the 57.6% that exhibited ARD were largely limited to South America (Brazil), Central America (Mexico), and Asia (India). A total of 3391 of these tick populations were R. (B.) microplus, of which 2013 exhibited ARD. Random effects meta-analyses indicated that the exhibition of ARD was higher in R. (B.) microplus (66.2%) than in other tick species. Global prevalence estimates of ARD in R. (B.) microplus vary as a function of geography, detection methods, and acaricide compounds. In general, high heterogeneity was noted among the studies. However, homogeneity was observed among studies from India, suggesting the establishment of acaricide resistance in Indian R. (B.) microplus populations. Current tick control interventions are urgently required to limit the evolution and implications of resistance development.
Monitoring the resistance of Rhipicephalus microplus to amitraz, flumethrin, coumaphos, and ivermectin on cattle farms in Mexico
2021, Veterinary Parasitology: Regional Studies and Reports
Citation Excerpt :
Despite the fewer number of farms with high resistance level to permethrin in this study, collateral resistance with other molecules of the same family is expected. Cypermethrin and deltamethrin have been used in Mexico to control ticks on cattle and collateral resistance were detected in previous studies in Mexico (Rodriguez-Vivas et al., 2006a). The mode of action of SP might explain the collateral resistance.
The prevalence, resistance ratios and factor associated with Rhipicephalu microplus populations resistant to amitraz, flumethrin, coumaphos, and ivermectina (IVM) in Mexico were studied. Field tick populations were collected from 54 farms in 15 different states of Mexico. The dose–response bioassays were carried out using the larval immersion test (amitraz and IVM) and the modified larval packet test (flumethrin and coumaphos) against R. microplus. Mortality data were subjected to probit analysis to calculate lethal concentrations at 50%. A logistic regression model was used to evaluate the relation between resistance and possible associated factors. The phenotype was defined as high resistant (HR), low resistant (LR) or susceptible (S). The overall prevalence of cattle farms with R. microplus resistant to coumaphos, amitraz, flumethrin and IVM were 25.9, 46.2, 31.5 and 68.5%, respectively. For coumaphos, 74.1, 22.2, and 3.7% were classified as S, LR, and HR, respectively, whereas, for amitraz, 53.7, 24.1, and 22.2% of phenotypes were S, LR, and HR, respectively, for flumethrin 68.5, 14.8, and 16.7% were S, LR and HR respectively, and for IVM, 31.5, 46.3, and 22.2% were S, LR, and HR, respectively. We identified that cattle farms without acaricide rotation program (OR: 7.66, CL_95%: 1.70–34.47, P: 0.008) had a higher probability of developing R. microplus resistant to amitraz. We concluded that amitraz and IVM resistance in R. microplus is frequent, but mainly at a low level in cattle farms of Mexico. Cattle farms without acaricide rotation program had higher probability of developing R. microplus resistant to amitraz.

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Veterinary Parasitology

Abstract

Introduction

Section snippets

Study background

Questionnaire survey

Discussion

Acknowledgments

References (30)

Effect of moxidectin against natural infestation of the cattle tick Boophilus microplus (Acarina: Ixodidadae) in the Mexican tropics

Vet. Parasitol.

Factors related to cattle infestation level and resistance to acaricides in Boophilus microplus tick populations in New Caledonia

Vet. Parasitol.

Possible risk factors on Queensland dairy farms for acaricide resistance in cattle tick (Boophilus microplus)

Vet. Parasitol.

Managing parasiticide resistance

Vet. Parasitol.

Recent developments in ectoparasiticides

Vet. J.

Determinación de las concentraciones discriminantes como medio de diagnóstico de susceptibilidad en garrapatas. B. microplus

Purificación y caracterización toxicológica de garrapatas B. microplus resistentes a ixodicidas organofosforados y organoclorados

Resistencia de garrapatas en México

Situación de la resistencia de la garrapata B. microplus (Canestrini, 1887) a organofosforados y piretroides en Costa Rica

Rev. Ciencias Vet.

Studies on the effect on infection by Babesia sp. on oviposition of Boophilus microplus engorged females naturally infected in the Mexican tropics

Vet. Parasitol.

Cultivos importantes para la diversificación agrícola en la península de Yucatán

Epidemiología de la resistencia a ixodicidas en garrapatas Boophilus microplus en la República Mexicana

Diagnóstico de la susceptibilidad de la garrapata del ganado Boophilus microplus a los acaricidas en el estado de Minas Gerais, Brasil

Estudios de resistencia a acaricidas en la garrapata bovina Boophilus microplus en América central

Cited by (111)

Widespread acaricide resistance and multi-resistance in Rhipicephalus microplus in Ecuador and associated environmental and management risk factors

Identification of the G184C, C190A and T2134A mutations in the para-sodium channel gene of the southern cattle tick Rhipicephalus (Boophilus) microplus associated with resistance to cypermethrin in northern Veracruz, Mexico

Novel tick glutathione transferase inhibitors as promising acaricidal compounds

Resistance in ectoparasites

Development of acaricide resistance in tick populations of cattle: A systematic review and meta-analysis

Monitoring the resistance of Rhipicephalus microplus to amitraz, flumethrin, coumaphos, and ivermectin on cattle farms in Mexico