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      Assessment of gastrointestinal nematode anthelmintic resistance and acaricidal efficacy of fluazuron–flumethrin on sheep and goat ticks in the North West province of South Africa

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          Abstract

          Background and Aim:

          Anthelmintic resistance (AR) and acaricide resistance (ACR) pose great economic threat to communal livestock raised by rural communities, limiting sustainable production. This study was conducted to assess the occurrence of AR and ACR against nematodes and ticks that infest small ruminants (sheep and goats) from small-scale farming communities in the North West Province of South Africa, as well as document the associated risk factors.

          Materials and Methods:

          The study was conducted on small-scale farming locations in two districts of the North West Province, namely, Dr. Ruth Segomotsi Mompati district and Dr. Kenneth Kaunda district, from November 2019 to March 2020. A questionnaire survey based specifically on antiparasitic treatment and related management practices was administered to 86 small-scale farmers. A fecal egg count reduction test (FECRT) was used to determine in vivo AR in small ruminants against benzimidazole (BZD), levamisole, and macrocyclic lactone on nine ruminant farms. Then, deoxyribonucleic acid was extracted from L3 larvae and resistant nematodes were identified using a polymerase chain reaction, targeting the internal transcribed spacer 2 gene. An egg hatch assay (EHA) and a larval mortality assay (LMA) were used to determine in vitro AR against thiabendazole (TBZ and BZD) in the same farms. Acaricide resistance against fluazuron–flumethrin (Drastic Deadline eXtreme) pour-on was assessed using an adult immersion test (AIT) on Rhipicephalus evertsi.

          Results:

          Questionnaire results indicated that most farmers (89%) relied solely on anthelmintics. Farmers used visual appraisal to estimate the dosage, which is the primary cause of resistance. The FECRT revealed AR in all the farms. Egg hatch assay results revealed AR development against TBZ in all districts, with >95% of the eggs hatching at variable doses. Larval mortality assay results revealed the development of resistance against BZD, with 50% of L3 larvae surviving at different doses in all farms. Adult immersion test results indicated that fluazuron–flumethrin (>99%) exhibited high acaricidal efficacy against R. evertsi by inhibiting tick oviposition.

          Conclusion:

          This investigation found that sheep and goats in the studied areas are developing AR to gastrointestinal parasites. The findings of in vivo tests showed resistance with fecal egg count reduction percentage of <95% or lower confidence limit of <90%. The results of EHA and LMA revealed no evidence of inhibition of egg development and larval mortality, indicating the development of resistance. Acaricide resistance was not detected against fluazuron–flumethrin, which is commonly used in the study areas. Thus, developing management methods for these economically significant livestock nematodes, including teaching small-scale farmers how to properly administer anthelmintics and acaricides to their livestock, is urgently needed.

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          Most cited references53

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          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.

          Methods have been described to assist in the detection of anthelmintic resistance in strongylid nematodes of ruminants, horses and pigs. Two tests are recommended, an in vivo test, the faecal egg count reduction test for use in infected animals, and an in vitro test, the egg hatch test for detection of benzimidazole resistance in nematodes that hatch shortly after embryonation. Anaerobic storage for submission of faecal samples from the field for use in the in vitro test is of value and the procedure is described. The tests should enable comparable data to be obtained in surveys in all parts of the world.
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            Organic Agriculture, Food Security, and the Environment

            Organic agriculture is often perceived as more sustainable than conventional farming. We review the literature on this topic from a global perspective. In terms of environmental and climate change effects, organic farming is less polluting than conventional farming when measured per unit of land but not when measured per unit of output. Organic farming, which currently accounts for only 1% of global agricultural land, is lower yielding on average. Due to higher knowledge requirements, observed yield gaps might further increase if a larger number of farmers would switch to organic practices. Widespread upscaling of organic agriculture would cause additional loss of natural habitats and also entail output price increases, making food less affordable for poor consumers in developing countries. Organic farming is not the paradigm for sustainable agriculture and food security, but smart combinations of organic and conventional methods could contribute toward sustainable productivity increases in global agriculture.
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              The detection of anthelmintic resistance in nematodes of veterinary importance.

              Before revised World Association for the Advancement of Veterinary Parasitology (WAAVP) guidelines on the detection of anthelmintic resistance can be produced, validation of modified and new methods is required in laboratories in different parts of the world. There is a great need for improved methods of detection of anthelmintic resistance particularly for the detection of macrocyclic lactone resistance and for the detection of resistant nematodes in cattle. Therefore, revised and new methods are provided here for the detection of anthelmintic resistance in nematodes of ruminants, horses and pigs as a basis for discussion and with the purpose that they are evaluated internationally to establish whether they could in the future be recommended by the WAAVP. The interpretation of the faecal egg count reduction test has been modified and suggestions given on its use with persistent anthelmintics and continuous release devices. An egg hatch test for benzimidazole (BZ) resistance is described. A microagar larval development test for the detection of benzimidazole and levamisole resistance provides third stage larvae for the identification of resistant worms. The sensitivity of these two tests can be increased by using discriminating doses rather than LD(50) values. Details are given of a PCR based test for the analysis of benzimidazole resistance in strongyles of sheep and goats, horses and cattle. Although promising for ruminant trichostrongyles, quantitative determination of gene frequency using real time PCR requires further development before PCR tests will be used in the field. Apart from faecal egg count reduction tests there are currently no satisfactory tests for macrocylic lactone resistance despite the great importance of this subject. Except for treatment and slaughter trials there are no validated tests for fasciolicide resistance or for the detection of resistance in cestodes.
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                Author and article information

                Journal
                Vet World
                Vet World
                Veterinary World
                Veterinary World (India )
                0972-8988
                2231-0916
                August 2023
                17 August 2023
                : 16
                : 8
                : 1615-1626
                Affiliations
                [1 ]Unit for Environmental Sciences and Management, North-West University, Potchefstroom, 2520, South Africa
                [2 ]Department of Life and Consumer Sciences, University of South Africa, Florida Campus, Roodepoort, 1709, South Africa
                [3 ]Biometry, Agricultural Research Council, Hatfield, Pretoria, 0083, South Africa
                Author notes
                Article
                Vetworld-16-1615
                10.14202/vetworld.2023.1615-1626
                10521178
                37766712
                d4518112-f95b-40d1-834c-5a571a4bdf54
                Copyright: © Emsley, et al.

                Open Access. This 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
                : 18 October 2022
                : 06 July 2023
                Categories
                Research Article

                acaricidal resistance,adult immersion test,anthelmintic resistance,egg hatch assay,gastrointestinal nematodes,larval mortality assay

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