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Insecticide/Acaricide Resistance in Fleas and Ticks Infesting Dogs and Cats Tad B Coles1* and Michael W Dryden2

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Insecticide/Acaricide Resistance in Fleas and Ticks Infesting Dogs and Cats Tad B Coles1* and Michael W Dryden2 Coles and Dryden Parasites & Vectors 2014, 7:8 http://www.parasitesandvectors.com/content/7/1/8 REVIEW Open Access Insecticide/acaricide resistance in fleas and ticks infesting dogs and cats Tad B Coles1* and Michael W Dryden2 Abstract This review defines insecticide/acaricide resistance and describes the history, evolution, types, mechanisms, and detection of resistance as it applies to chemicals currently used against fleas and ticks of dogs and cats and summarizes resistance reported to date. We introduce the concept of refugia as it applies to flea and tick resistance and discuss strategies to minimize the impact and inevitable onset of resistance to newer classes of insecticides. Our purpose is to provide the veterinary practitioner with information needed to investigate suspected lack of efficacy, respond to lack of efficacy complaints from their clients, and evaluate the relative importance of resistance as they strive to relieve their patients and satisfy their clients when faced with flea and tick infestations that are difficult to resolve. We conclude that causality of suspected lack of insecticide/acaricide efficacy is most likely treatment deficiency, not resistance. Keywords: Flea, Ctenocephalides felis, Tick, Rhipicephalus sanguineus, Dog, Cat, Insecticide, Acaricide, Resistance, Refugia, Refugium Review nuisance pests of dogs, cats, and their human owners: Background Ctenocephalides felis felis (cat flea), C. canis (dog flea), In this paper we will review the current information relative Echidnophaga gallinacea (sticktight flea), Pulex irritans to resistance of fleas and ticks to insecticides and acaricides, (human flea), and the closely related P. simulans [2-4]. respectively, as it applies to canine and feline veterinary Ctenocephalides felis is by far the most common flea practitioners. Veterinarians must provide answers to pet infesting dogs and cats around the world [2,4,5]. In one owners with unmet expectations and there are many rea- study, all of the 972 flea field isolates obtained from dogs sons clients voice dissatisfaction. Investigating possible in- and cats from 2001 to 2005 in the United States, the United consistency regarding insecticide/acaricide treatment of all Kingdom, and Germany were Ctenocephalides felis [6]. pet mammals in the household and determining if neigh- Dogs and cats reportedly serve as bridging hosts for a boring pets or flea-infested wildlife might be serving as a variety of flea species, acquiring fleas from wild animals source of reinfestation is imperative and will often point to and bringing them home to infest other domestic animals obvious strategies to improve efficacy and client satisfaction and pester people [2], but it is more likely that dogs and [1]. Clients often bring up resistance to insecticides/ cats serve as an original flea source in that they carry acaricides as soon as they see evidence of fleas or ticks Ctenocephalides felis to urban wild animals, which serve on their recently treated pet. The following general review as reservoir hosts maintaining a flea population that of insecticide/acaricide resistance, focusing on species of reinfests pet dogs and cats after treatment. fleas and ticks that infest dogs and cats, will help veterinar- Dogs in North America are most commonly infested ians respond to client concerns. with the following tick species: Amblyomma americanum Some 2,500 flea species have been described, at least (Lone Star tick), A. maculatum (Gulf Coast tick), 15 of which occasionally infest dogs and cats [2]. However, Dermacentor variabilis (American dog tick), D. andersoni only a few flea species are significant disease-carrying and (Rocky Mountain wood tick), D. occidentalis (Pacific Coast tick), Ixodes pacificus (western black-legged tick), * Correspondence: [email protected] I. scapularis (black-legged tick), Otobius megnini (spinose 1Medical Writing and Veterinary Consulting, Overland Park, KS 66212, USA ear tick), and Rhipicephalus sanguineus (brown dog tick) Full list of author information is available at the end of the article © 2014 Coles and Dryden; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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. Coles and Dryden Parasites & Vectors 2014, 7:8 Page 2 of 10 http://www.parasitesandvectors.com/content/7/1/8 [5,7]. Cats, while not as commonly infested as dogs, of pesticides, such that the resistant individuals sur- are parasitized by A. americanum, D. variabilis, and I. vive a concentration of the compound(s) that would scapularis [7]. normally be lethal to the species.” Even this latter def- As a point of clarification, fleas and ticks are arthropods, inition is problematic because it includes the term but of these two, only fleas are insects and, as such, we “tolerance.” use insecticides to kill them. Ticks are not insects, but Scientific literature is full of different definitions of are arachnids (class arachnida as are mites and spiders) “resistance,” which should be kept in mind as historical and, as such, we use acaricides to kill them. Different reports of “resistance” are reviewed. After Melander in- compounds have varying degrees of insecticidal and/or troduced the topic of resistance, the most frequently re- acaricidal properties. ported research on insecticide resistance has concerned crop pests and insect vectors of human disease, espe- History and definition of resistance cially mosquitoes. Mosquitoes began to show resistance The first report of insecticide/acaricide resistance was not to DDT at about the same time that housefly resistance in fleas or ticks. Melander raised the general insecticide- to DDT was first noted in Italy in 1946 [14]. Flea resist- resistance topic a century ago in 1914 when he wondered if ance was first noted in 1949 in Peruvian Pulex irritans fruit-tree pest insects could become resistant to insecticide that were resistant to dichlorodiphenyltrichloroethane spray [8]. His answer to the query, “Can insects become (DDT) [15]. Ctenocephalides felis resistance to DDT was resistant to sprays?” was his discovery that certain popu- first reported in 1952 followed by reports of resistance lations of San Jose scale insects at certain locales were to benzene hexachloride (BHC) and dieldrin in 1956 [16]. still alive after being sprayed with sulphur-lime concen- Tick resistance was first noted in 1954 to dieldrin in trations that killed all scale insects at other locales, a re- Rhipicephalus sanguineus [15]. Suspected resistance of port widely referenced as the first documented evidence Dermacentor variabilis to DDT, BHC, and dieldrin was of insecticide resistance. But, while this is often cited as reported in 1959 [16]. The number of arthropod species evidence of resistance, what he actually proved was that with suspected insecticide/acaricide resistance increased different scale insect populations separated by locale to 37 in 1955, with “inescapable and quantitative proof” had different susceptibilities or tolerance to this insecticide. of resistance in 18 of those species [15]. Whether or not the differences were due to acquired For this paper, our definition of insecticide/acaricide genetic resistance is unknown. resistance is the selection of a specific heritable trait While resistance and tolerance are often used inter- (or traits) in a population of arthropods, due to that popula- changeably, they are not the same. In contrast to resist- tion’s contact with a chemical, that results in a significant ance, tolerance is a natural tendency rather than a result of increase in the percentage of the population that will selection pressure [9]. Certain individuals are more tolerant survive a standard dose of that chemical (or a closely of a specific pesticide dose than others. Sometimes it is related chemical in the case of cross resistance). difficult to differentiate true resistance from the natural range of pesticide susceptibility that exists as a bell curve Evolution of resistance in every population of pests [10]. Tolerance is also used to Individuals with genetic traits that allow them to survive describe natural differences between different species or exposure to an insecticide/acaricide will pass genes on to between life stages of organisms [11]. For example ticks the subsequent generation, thereby potentially increasing are naturally more tolerant of imidacloprid than fleas and the percentage of a population that can survive subsequent Trichuris vulpis is more tolerant of pyrantel pamoate than exposure to the chemical [1]. Within this more restricted is Ancylostoma caninum. definition of insecticide/acaricide resistance, the inherent What constitutes proof of resistance and how is resistance bell curve based susceptibility differences in a “normal” defined? The definition of resistance has changed with population should be remembered [17], because the time. The World Health Organization (WHO) has served susceptibility of the new population is compared with the as the global coordinator for information on vector re- old or “normal” population when looking for a significant sistance and on standardization of pesticide-resistance increase in survivability. There are
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