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      Emergence of multi-acaricide resistant Rhipicephalus ticks and its implication on chemical tick control in Uganda

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          Abstract

          Background

          Acaricide failure has been on the rise in the western and central cattle corridor of Uganda. In this study, we identified the tick species associated with acaricide failure and determined their susceptibility to various acaricide molecules used for tick control in Uganda.

          Methods

          In this cross sectional study, tick samples were collected and identified to species level from 54 purposively selected farms (from 17 districts) that mostly had a history of acaricide failure. Larval packet test was used to screen 31 tick populations from 30 farms for susceptibility at discriminating dose (DD) and 2 × DD of five panels of commercial acaricide molecules belonging to the following classes; amidine, synthetic pyrethroid (SP), organophosphate (OP) and OP-SP co-formulations (COF). Resistance was assessed based on World Health Organization criteria for screening insecticide resistance.

          Results

          Of the 1357 ticks identified, Rhipicephalus ( Rhipicephalus) appendiculatus and Rhipicephalus ( Boophilus) decoloratus were the major (95.6 %) tick species in farms sampled. Resistance against SP was detected in 90.0 % (27/30) of the tick populations tested. Worryingly, 60.0 % (18/30) and 63.0 % (19/30) of the above ticks were super resistant (0 % mortality) against 2 × DD cypermethrin and deltamethrin, respectively. Resistance was also detected against COF (43.3 %), OP chlorfenvinphos (13.3 %) and amitraz (12.9 %). In two years, 74.1 % (20/27) of the farms had used two to three acaricide molecules, and 55.6 % (15/27) rotated the molecules wrongly. Multi-acaricide resistance (at least 2 molecules) was detected in 55.2 % (16/29) of the resistant Rhipicephalus ticks and significantly associated with R. decoloratus ( p = 0.0133), use of both SP and COF in the last 2 years (p < 0.001) and Kiruhura district ( p = 0.0339). Despite emergence of amitraz resistance in the greater Bushenyi area, it was the most efficacious molecule against SP and COF resistant ticks.

          Conclusion

          This study is the first to report emergence of super SP resistant and multi-acaricide resistant Rhipicephalus ticks in Uganda. Amitraz was the best acaricide against SP and COF resistant ticks. However, in the absence of technical interventions, farmer-led solutions aimed at troubleshooting for efficacy of multitude of acaricides at their disposal are expected to potentially cause negative collateral effects on future chemical tick control options, animal welfare and public health.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13071-015-1278-3) contains supplementary material, which is available to authorized users.

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          Most cited references55

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          Molecular biology of insect sodium channels and pyrethroid resistance.

          Voltage-gated sodium channels are essential for the initiation and propagation of the action potential in neurons and other excitable cells. Because of their critical roles in electrical signaling, sodium channels are targets of a variety of naturally occurring and synthetic neurotoxins, including several classes of insecticides. This review is intended to provide an update on the molecular biology of insect sodium channels and the molecular mechanism of pyrethroid resistance. Although mammalian and insect sodium channels share fundamental topological and functional properties, most insect species carry only one sodium channel gene, compared to multiple sodium channel genes found in each mammalian species. Recent studies showed that two posttranscriptional mechanisms, alternative splicing and RNA editing, are involved in generating functional diversity of sodium channels in insects. More than 50 sodium channel mutations have been identified to be responsible for or associated with knockdown resistance (kdr) to pyrethroids in various arthropod pests and disease vectors. Elucidation of molecular mechanism of kdr led to the identification of dual receptor sites of pyrethroids on insect sodium channels. Many of the kdr mutations appear to be located within or close to the two receptor sites. The accumulating knowledge of insect sodium channels and their interactions with insecticides provides a foundation for understanding the neurophysiology of sodium channels in vivo and the development of new and safer insecticides for effective control of arthropod pests and human disease vectors.
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            Acaricide resistance in cattle ticks and approaches to its management: the state of play.

            Cattle ticks are an important constraint on livestock production, particularly in tropical and subtropical areas. Use of synthetic acaricides is the primary method of tick control; therefore, it would be imperative to develop strategies to preserve the efficacy of existing acaricides. This paper summarizes the status of acaricide resistance in cattle ticks from different parts of the world and reviews modes of action of currently used acaricides, mechanism of resistance development, contributory factors for the development and spread of resistance, management of resistant strains and strategies to prolong the effect of the available acaricides. Use of vaccines, synthetic and botanical acaricides and educating farmers about recommended tick control practices are discussed, along with the integration of currently available options for the management of drug resistance and, ultimately, the control of cattle ticks. Copyright © 2014 Elsevier B.V. All rights reserved.
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              The molecular biology of knockdown resistance to pyrethroid insecticides.

              The term "knockdown resistance" is used to describe cases of resistance to diphenylethane (e.g. DDT) and pyrethroid insecticides in insects and other arthropods that result from reduced sensitivity of the nervous system. Knockdown resistance, first identified and characterized in the house fly (Musca domestica) in the 1950's, remains a threat to the continued usefulness of pyrethroids in the control of many pest species. Research since 1990 has provided a wealth of new information on the molecular basis of knockdown resistance. This paper reviews these recent developments with emphasis on the results of genetic linkage analyses, the identification of gene mutations associated with knockdown resistance, and the functional characterization of resistance-associated mutations. Results of these studies identify voltage-sensitive sodium channel genes orthologous to the para gene of Drosophila melanogaster as the site of multiple knockdown resistance mutations and define the molecular mechanisms by which these mutations cause pyrethroid resistance. These results also provide new insight into the mechanisms by which pyrethroids modify the function of voltage-sensitive sodium channels.
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                Author and article information

                Contributors
                vpato@covab.mak.ac.ug
                jokwee@yahoo.co.uk
                tayebwa.dickson@gmail.com
                josephjbvincent@gmail.com
                ksteven310@gmail.com
                ewampande@yahoo.co.uk
                omararoberto@gmail.com
                mjeannebukeka@gmail.com
                rtweyongyere@covab.mak.ac.ug
                dowiny@covab.mak.ac.ug
                htakeshi@med.kitasato-u.ac.jp
                tsujin@med.kitasato-u.ac.jp
                umemiya@obihiro.ac.jp
                gen@obihiro.ac.jp
                harukana@koalanet.ne.jp
                acarikf@nifty.com
                hisuzuki@obihiro.ac.jp
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                4 January 2016
                4 January 2016
                2016
                : 9
                : 4
                Affiliations
                [ ]Department of Veterinary Pharmacy, Clinics and Comparative Medicine, School of Veterinary Medicine and Animal Resources, College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, P. O Box 7062, Kampala, Uganda
                [ ]Central Diagnostic Laboratory, College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, P. O Box 7062, Kampala, Uganda
                [ ]National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555 Japan
                [ ]Drug Information Department, National Drug Authority, P. O. Box 23096, Kampala, Uganda
                [ ]Directorate of Research and Graduate Training, Makerere University, P.O Box 7062, Kampala, Uganda
                [ ]Laboratory of Parasitic Diseases, National Institute of Animal Health, National Agricultural and Food Research Organization, 3-1-5 Kannondai, Tsukuba, Ibaraki 305-0856 Japan
                [ ]Present Address: Department of Parasitology, Kitasato University School of Medicine, Kitasato, Minami-ku, Sagamihara, Kanagawa 252-0374 Japan
                [ ]Present Address: Japan International Cooperation Agency, Nibancho Center Building, 5-25, Nibancho, Chiyoda-ku, Tokyo, 108-8012 Japan
                Article
                1278
                10.1186/s13071-015-1278-3
                4700616
                26727991
                471ff18d-6d83-4228-b4df-d245adb48619
                © Vudriko et al. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 27 August 2015
                : 21 December 2015
                Funding
                Funded by: Japan International Cooperation (JICA)
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Parasitology
                ticks,rhipicephalus appendiculatus,rhipicephalus (boophilus) decoloratus,acaricide,resistance,amitraz,synthetic pyrethroids,organophosphates

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