{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,4]],"date-time":"2026-06-04T06:27:47Z","timestamp":1780554467919,"version":"3.54.1"},"reference-count":70,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2023,8,22]],"date-time":"2023-08-22T00:00:00Z","timestamp":1692662400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"funder":[{"name":"Institut Pasteur de Madagascar"},{"DOI":"10.13039\/100016285","name":"TDR","doi-asserted-by":"publisher","award":["B80105"],"award-info":[{"award-number":["B80105"]}],"id":[{"id":"10.13039\/100016285","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008883","name":"Northern Arizona University","doi-asserted-by":"publisher","award":["Hooper Undergraduate Research Grant"],"award-info":[{"award-number":["Hooper Undergraduate Research Grant"]}],"id":[{"id":"10.13039\/100008883","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Swiss Embassy - Antananarivo","award":["771.22.00-1-MAE\/RML"],"award-info":[{"award-number":["771.22.00-1-MAE\/RML"]}]}],"content-domain":{"domain":["www.plosntds.org"],"crossmark-restriction":false},"short-container-title":["PLoS Negl Trop Dis"],"abstract":"<jats:sec id=\"sec001\"><jats:title>Background<\/jats:title><jats:p>Plague, caused by the bacterium<jats:italic>Yersinia pestis<\/jats:italic>, remains an important disease in Madagascar, where the oriental rat flea,<jats:italic>Xenopsylla cheopis<\/jats:italic>, is a primary vector. To control fleas, synthetic pyrethroids (SPs) have been used for &gt;20 years, resulting in resistance in many<jats:italic>X<\/jats:italic>.<jats:italic>cheopis<\/jats:italic>populations. The most common mechanisms of SP resistance are target site mutations in the voltage-gated sodium channel (VGSC) gene.<\/jats:p><\/jats:sec><jats:sec id=\"sec002\"><jats:title>Methodology\/Principal findings<\/jats:title><jats:p>We obtained 25 collections of<jats:italic>X<\/jats:italic>.<jats:italic>cheopis<\/jats:italic>from 22 locations across Madagascar and performed phenotypic tests to determine resistance to deltamethrin, permethrin, and\/or dichlorodiphenyltrichloroethane (DDT). Most populations were resistant to all these insecticides. We sequenced a 535 bp segment of the VGSC gene and identified two different mutations encoding distinct substitutions at amino acid position 1014, which is associated with knockdown resistance (<jats:italic>kdr<\/jats:italic>) to SPs in insects.<jats:italic>Kdr<\/jats:italic>mutation L1014F occurred in all 25 collections; a rarer mutation, L1014H, was found in 12 collections. There was a significant positive relationship between the frequency of<jats:italic>kdr<\/jats:italic>alleles and the proportion of individuals surviving exposure to deltamethrin. Phylogenetic comparisons of 12 VGSC alleles in Madagascar suggested resistant alleles arose from susceptible lineages at least three times. Because genotype can reasonably predict resistance phenotype, we developed a TaqMan PCR assay for the rapid detection of<jats:italic>kdr<\/jats:italic>resistance alleles.<\/jats:p><\/jats:sec><jats:sec id=\"sec003\"><jats:title>Conclusions\/Significance<\/jats:title><jats:p>Our study provides new insights into VGSC mutations in Malagasy populations of<jats:italic>X<\/jats:italic>.<jats:italic>cheopis<\/jats:italic>and is the first to report a positive correlation between VGSC genotypes and SP resistance phenotypes in fleas. Widespread occurrence of these two SP resistance mutations in<jats:italic>X<\/jats:italic>.<jats:italic>cheopis<\/jats:italic>populations in Madagascar reduces the viability of these insecticides for flea control. However, the TaqMan assay described here facilitates rapid detection of<jats:italic>kdr<\/jats:italic>mutations to inform when use of these insecticides is still warranted to reduce transmission of plague.<\/jats:p><\/jats:sec>","DOI":"10.1371\/journal.pntd.0011401","type":"journal-article","created":{"date-parts":[[2023,8,22]],"date-time":"2023-08-22T17:24:46Z","timestamp":1692725086000},"page":"e0011401","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["Knockdown resistance mutations are common and widely distributed in Xenopsylla cheopis fleas that transmit plague in Madagascar"],"prefix":"10.1371","volume":"17","author":[{"given":"Shelby M.","family":"Hutton","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adelaide","family":"Miarinjara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathan E.","family":"Stone","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fara N.","family":"Raharimalala","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annick O.","family":"Raveloson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ravo","family":"Rakotobe Harimanana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mireille","family":"Harimalala","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Soanandrasana","family":"Rahelinirina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryelan F.","family":"McDonough","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abbe D.","family":"Ames","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Crystal","family":"Hepp","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Minoarisoa","family":"Rajerison","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph D.","family":"Busch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David M.","family":"Wagner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8084-7372","authenticated-orcid":true,"given":"Romain","family":"Girod","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,8,22]]},"reference":[{"issue":"8","key":"pntd.0011401.ref001","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0008251","article-title":"Human plague: An old scourge that needs new answers","volume":"14","author":"X Valles","year":"2020","journal-title":"Plos Neglected Tropical Diseases"},{"key":"pntd.0011401.ref002","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1146\/annurev.ento.50.071803.130337","article-title":"Natural history of plague: perspectives from more than a century of research","volume":"50","author":"KL Gage","year":"2005","journal-title":"Annu Rev Entomol"},{"issue":"1","key":"pntd.0011401.ref003","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1128\/CMR.10.1.35","article-title":"Yersinia pestis\u2014etiologic agent of plague","volume":"10","author":"RD Perry","year":"1997","journal-title":"Clin Microbiol Rev"},{"issue":"3","key":"pntd.0011401.ref004","doi-asserted-by":"crossref","first-page":"460","DOI":"10.3201\/eid1203.051051","article-title":"Pneumonic plague cluster, Uganda, 2004","volume":"12","author":"EM Begier","year":"2006","journal-title":"Emerg Infect Dis"},{"issue":"17","key":"pntd.0011401.ref005","doi-asserted-by":"crossref","first-page":"2281","DOI":"10.1001\/jama.283.17.2281","article-title":"Plague as a biological weapon: medical and public health management","volume":"283","author":"TV Inglesby","year":"2000","journal-title":"J Am Med Assoc"},{"issue":"12","key":"pntd.0011401.ref006","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1038\/ng.705","article-title":"Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity","volume":"42","author":"G Morelli","year":"2010","journal-title":"Nat Genet"},{"issue":"25","key":"pntd.0011401.ref007","first-page":"289","article-title":"Plague around the world in 2019","volume":"94","author":"E. Bertherat","year":"2019","journal-title":"Weekly Epidemiological Record = Relev\u00e9 \u00e9pid\u00e9miologique hebdomadaire"},{"key":"pntd.0011401.ref008","first-page":"79","article-title":"Epidemiology of the plague at Madagascar","volume":"2626","author":"ER Brygoo","year":"1966","journal-title":"Med Trop"},{"issue":"1\u20132","key":"pntd.0011401.ref009","first-page":"51","article-title":"Epidemiological data on the plague in Madagascar","volume":"68","author":"M Ratsitorahina","year":"2002","journal-title":"Arch Inst Pasteur Madagascar"},{"issue":"1","key":"pntd.0011401.ref010","doi-asserted-by":"crossref","first-page":"e00623","DOI":"10.1128\/mBio.00623-12","article-title":"A decade of plague in Mahajanga, Madagascar: insights into the global maritime spread of pandemic plague","volume":"4","author":"AJ Vogler","year":"2013","journal-title":"mBio"},{"issue":"5","key":"pntd.0011401.ref011","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/S1473-3099(18)30730-8","article-title":"Epidemiological characteristics of an urban plague epidemic in Madagascar, August-November, 2017: an outbreak report","volume":"19","author":"R Randremanana","year":"2019","journal-title":"Lancet Infect Dis"},{"issue":"11","key":"pntd.0011401.ref012","doi-asserted-by":"crossref","first-page":"e2382","DOI":"10.1371\/journal.pntd.0002382","article-title":"Understanding the persistence of plague foci in Madagascar","volume":"7","author":"V Andrianaivoarimanana","year":"2013","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0011401.ref013","volume-title":"Pesticides and their application: for the control of vectors and pests of public health importance","author":"World Health Organization","year":"2006"},{"issue":"2","key":"pntd.0011401.ref014","doi-asserted-by":"crossref","first-page":"e0004414","DOI":"10.1371\/journal.pntd.0004414","article-title":"Current Perspectives on Plague Vector Control in Madagascar: Susceptibility Status of Xenopsylla cheopis to 12 Insecticides","volume":"10","author":"A Miarinjara","year":"2016","journal-title":"PLoS Negl Trop Dis"},{"issue":"5","key":"pntd.0011401.ref015","first-page":"731","article-title":"The impact of insecticide-resistance on control of vectors and vector-borne diseases","volume":"40","author":"JR Busvine","year":"1969","journal-title":"Bull World Health Organ"},{"issue":"11","key":"pntd.0011401.ref016","doi-asserted-by":"crossref","first-page":"e111998","DOI":"10.1371\/journal.pone.0111998","article-title":"Xenopsylla cheopis (Siphonaptera: Pulicidae) susceptibility to Deltamethrin in Madagascar","volume":"9","author":"S Boyer","year":"2014","journal-title":"PLoS One"},{"issue":"1","key":"pntd.0011401.ref017","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40249-017-0356-5","article-title":"Plague risk in vulnerable community: assessment of Xenopsylla cheopis susceptibility to insecticides in Malagasy prisons","volume":"6","author":"A Miarinjara","year":"2017","journal-title":"Infect Dis Poverty"},{"key":"pntd.0011401.ref018","first-page":"1","article-title":"Seventeenth Report of the WHO Expert Committee on Insecticides","volume":"443","author":"Insecticide resistance and vector control","year":"1970","journal-title":"World Health Organ Tech Rep Ser"},{"issue":"6","key":"pntd.0011401.ref019","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1002\/ps.1574","article-title":"Pyrethroids, knockdown resistance and sodium channels","volume":"64","author":"DM Soderlund","year":"2008","journal-title":"Pest Manag Sci"},{"key":"pntd.0011401.ref020","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1038\/191884a0","article-title":"Pattern of pyrethrin-resistance in houseflies","volume":"191","author":"BC Fine","year":"1961","journal-title":"Nature"},{"key":"pntd.0011401.ref021","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ibmb.2014.03.012","article-title":"Molecular biology of insect sodium channels and pyrethroid resistance","volume":"50","author":"K Dong","year":"2014","journal-title":"Insect Biochem Mol Biol"},{"issue":"2","key":"pntd.0011401.ref022","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1042\/BJ20051925","article-title":"Modelling insecticide-binding sites in the voltage-gated sodium channel","volume":"396","author":"AO O\u2019Reilly","year":"2006","journal-title":"Biochem J"},{"issue":"11","key":"pntd.0011401.ref023","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1002\/ps.1617","article-title":"Knockdown resistance to DDT and pyrethroids: from target-site mutations to molecular modelling","volume":"64","author":"O Davies TE","year":"2008","journal-title":"Pest Manag Sci"},{"key":"pntd.0011401.ref024","article-title":"DDT and pyrethroid resistance in Xenopsylla cheopis (Rothschild), the Oriental rat flea in northern Uganda","author":"AD Ames","year":"2011","journal-title":"Citeseer"},{"issue":"1","key":"pntd.0011401.ref025","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1186\/s13071-019-3775-2","article-title":"First detection of the kdr mutation (L1014F) in the plague vector Xenopsylla cheopis (Siphonaptera: Pulicidae)","volume":"12","author":"N Liu","year":"2019","journal-title":"Parasit Vectors"},{"key":"pntd.0011401.ref026","volume-title":"RStudio: Integrated Development Environment for R","author":"Team R","year":"2021"},{"issue":"10","key":"pntd.0011401.ref027","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1038\/nrg3054","article-title":"Haplotype phasing: existing methods and new developments","volume":"12","author":"SR Browning","year":"2011","journal-title":"Nat Rev Genet"},{"issue":"6","key":"pntd.0011401.ref028","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"S Kumar","year":"2018","journal-title":"Mol Biol Evol"},{"key":"pntd.0011401.ref029","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1093\/oso\/9780195135848.001.0001","volume-title":"Molecular evolution and phylogenetics","author":"M Nei","year":"2000"},{"issue":"4","key":"pntd.0011401.ref030","doi-asserted-by":"crossref","first-page":"783","DOI":"10.2307\/2408678","article-title":"Confidence Limits on Phylogenies: An Approach Using the Bootstrap","volume":"39","author":"J. Felsenstein","year":"1985","journal-title":"Evolution"},{"key":"pntd.0011401.ref031","author":"World Health Organization GMP","year":"2011","journal-title":"The technical basis for coordinated action against insecticide resistance: preserving the effectiveness of modern malaria vector control: meeting report. Geneva"},{"issue":"12","key":"pntd.0011401.ref032","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1016\/j.ibmb.2004.09.002","article-title":"Identification of mutations associated with pyrethroid resistance in the para-type sodium channel of the cat flea, Ctenocephalides felis","volume":"34","author":"C Bass","year":"2004","journal-title":"Insect Biochem Mol Biol"},{"key":"pntd.0011401.ref033","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.pestbp.2018.03.004","article-title":"First report of target site insensitivity to pyrethroids in human flea, Pulex irritans","volume":"146","author":"MB Ghavami","year":"2018","journal-title":"Pestic Biochem Physiol"},{"key":"pntd.0011401.ref034","article-title":"R\u00e9sistance aux insecticides des puces pestig\u00e8nes \u00e0 Madagascar et implications pour la lutte antivectorielle","author":"S Laventure","year":"1996","journal-title":"Proceedings of the 5\u00e8me Congr\u00e8s International de M\u00e9decine Tropicale de Langue Fran\u00e7aise"},{"issue":"7","key":"pntd.0011401.ref035","doi-asserted-by":"crossref","first-page":"e11681","DOI":"10.1371\/journal.pone.0011681","article-title":"Molecular ecology of pyrethroid knockdown resistance in Culex pipiens pallens mosquitoes","volume":"5","author":"L Chen","year":"2010","journal-title":"PLoS One"},{"key":"pntd.0011401.ref036","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1186\/1471-2334-14-441","article-title":"High frequency of kdr L1014F is associated with pyrethroid resistance in Anopheles coluzzii in Sudan savannah of northern Nigeria","volume":"14","author":"SS Ibrahim","year":"2014","journal-title":"BMC Infect Dis"},{"key":"pntd.0011401.ref037","first-page":"456","article-title":"Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico","volume":"7","author":"NE Stone","year":"2014","journal-title":"Parasit Vectors"},{"issue":"12","key":"pntd.0011401.ref038","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1016\/S0965-1748(98)00094-0","article-title":"Role of the kdr and super-kdr sodium channel mutations in pyrethroid resistance: correlation of allelic frequency to resistance level in wild and laboratory populations of horn flies (Haematobia irritans)","volume":"28","author":"RC Jamroz","year":"1998","journal-title":"Insect Biochem Mol Biol"},{"issue":"23","key":"pntd.0011401.ref039","doi-asserted-by":"crossref","first-page":"5938","DOI":"10.1073\/pnas.1801826115","article-title":"Associated patterns of insecticide resistance in field populations of malaria vectors across Africa","volume":"115","author":"PA Hancock","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"key":"pntd.0011401.ref040","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/1475-2875-6-52","article-title":"Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea","volume":"6","author":"BL Sharp","year":"2007","journal-title":"Malar J"},{"key":"pntd.0011401.ref041","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.actatropica.2018.12.021","article-title":"Mechanisms of pyrethroid resistance in Aedes (Stegomyia) aegypti from Colombia","volume":"191","author":"A Aponte","year":"2019","journal-title":"Acta Trop"},{"issue":"1","key":"pntd.0011401.ref042","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s40249-018-0471-y","article-title":"Correlation between adult pyrethroid resistance and knockdown resistance (kdr) mutations in Aedes albopictus (Diptera: Culicidae) field populations in China","volume":"7","author":"JP Gao","year":"2018","journal-title":"Infect Dis Poverty"},{"issue":"2","key":"pntd.0011401.ref043","first-page":"159","article-title":"Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles","volume":"14","author":"WG Brogdon","year":"1998","journal-title":"J Am Mosq Control Assoc"},{"key":"pntd.0011401.ref044","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1186\/s13071-015-0971-6","article-title":"Comparability between insecticide resistance bioassays for mosquito vectors: time to review current methodology?","volume":"8","author":"HF Owusu","year":"2015","journal-title":"Parasit Vectors"},{"key":"pntd.0011401.ref045","article-title":"The need to harmonize insecticide resistance testing: methodology, intensity concentrations and molecular mechanisms evaluated in Aedes aegypti populations in Central America and Hispaniola","author":"S Ledoux","year":"2020","journal-title":"bioRxiv"},{"issue":"2","key":"pntd.0011401.ref046","doi-asserted-by":"crossref","DOI":"10.1603\/0022-2585-38.2.193","article-title":"Topical application as a method for comparing the effectiveness of insecticides against cat flea (Siphonaptera: Pulicidae)","volume":"38","author":"EW Moyses","year":"2001","journal-title":"Journal of Medical Entomology"},{"key":"pntd.0011401.ref047","first-page":"58","volume-title":"Pesticide resistance in arthropods","author":"Springer","year":"1990"},{"issue":"3","key":"pntd.0011401.ref048","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1085\/jgp.115.3.305","article-title":"Activation of Drosophila sodium channels promotes modification by deltamethrin: reductions in affinity caused by knock-down resistance mutations","volume":"115","author":"H Vais","year":"2000","journal-title":"J Gen Physiol"},{"issue":"3","key":"pntd.0011401.ref049","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/S0048-3575(02)00101-3","article-title":"Metabolic detoxication and the kdr mutation in pyrethroid resistant house flies, Musca domestica","volume":"73","author":"N Liu","year":"2002","journal-title":"Pesticide biochemistry and physiology"},{"issue":"9","key":"pntd.0011401.ref050","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1016\/j.ibmb.2011.05.004","article-title":"Differential resistance of insect sodium channels with kdr mutations to deltamethrin, permethrin and DDT","volume":"41","author":"MJ Burton","year":"2011","journal-title":"Insect Biochem Mol Biol"},{"key":"pntd.0011401.ref051","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/1475-2875-3-22","article-title":"Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance","volume":"3","author":"V Corbel","year":"2004","journal-title":"Malar J"},{"issue":"2","key":"pntd.0011401.ref052","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1093\/jmedent\/45.2.260","article-title":"Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae","volume":"45","author":"L Reimer","year":"2014","journal-title":"J Med Entomol"},{"issue":"2","key":"pntd.0011401.ref053","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1111\/imb.12206","article-title":"Overcoming super-knock down resistance (super-kdr) mediated resistance: multi-halogenated benzyl pyrethroids are more toxic to super-kdr than kdr house flies","volume":"25","author":"H Sun","year":"2016","journal-title":"Insect Mol Biol"},{"issue":"2","key":"pntd.0011401.ref054","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/s00204-011-0726-x","article-title":"Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances","volume":"86","author":"DM Soderlund","year":"2012","journal-title":"Arch Toxicol"},{"issue":"2","key":"pntd.0011401.ref055","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/0048-3575(83)90133-5","article-title":"Evidence for two types of toxic actions of pyrethroids on susceptible and DDT-resistant German cockroaches","volume":"19","author":"JG Scott","year":"1983","journal-title":"Pesticide Biochemistry and Physiology"},{"issue":"12","key":"pntd.0011401.ref056","doi-asserted-by":"crossref","first-page":"1479","DOI":"10.1111\/j.1365-3156.2008.02164.x","article-title":"A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands","volume":"13","author":"N Protopopoff","year":"2008","journal-title":"Trop Med Int Health"},{"issue":"11","key":"pntd.0011401.ref057","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1002\/ps.3395","article-title":"Fitness costs associated with insecticide resistance","volume":"68","author":"A Kliot","year":"2012","journal-title":"Pest Manag Sci"},{"issue":"4","key":"pntd.0011401.ref058","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1051\/apido:2002028","article-title":"Decline in the proportion of mites resistant to fluvalinate in a population of Varroa destructor not treated with pyrethroids","volume":"33","author":"N Milani","year":"2002","journal-title":"Apidologie"},{"issue":"2","key":"pntd.0011401.ref059","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1002\/ps.1843","article-title":"Inheritance and stability of pyrethroid resistance in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) in Central Africa","volume":"66","author":"J Achaleke","year":"2010","journal-title":"Pest Manag Sci: formerly Pesticide Science"},{"issue":"2\u20134","key":"pntd.0011401.ref060","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.vetpar.2011.09.036","article-title":"Unstable pyrethroid resistance in sheep body lice Bovicola ovis (Schrank),(Phthiraptera: Trichodectidae) and its implications for lice control on sheep","volume":"185","author":"G. Levot","year":"2012","journal-title":"Vet Parasitol"},{"issue":"4","key":"pntd.0011401.ref061","doi-asserted-by":"crossref","first-page":"e60878","DOI":"10.1371\/journal.pone.0060878","article-title":"Assessing the effects of Aedes aegypti kdr mutations on pyrethroid resistance and its fitness cost","volume":"8","author":"LP Brito","year":"2013","journal-title":"PloS one"},{"issue":"3","key":"pntd.0011401.ref062","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.pestbp.2013.01.006","article-title":"Variable fitness costs for pyrethroid resistance alleles in the house fly, Musca domestica, in the absence of insecticide pressure","volume":"105","author":"FD Rinkevich","year":"2013","journal-title":"Pesticide biochemistry and physiology"},{"issue":"6","key":"pntd.0011401.ref063","first-page":"2992","article-title":"The insecticide resistance allele kdr-his has a fitness cost in the absence of insecticide exposure","volume":"111","author":"D Hanai","year":"2018","journal-title":"J Econ Entomol"},{"issue":"16","key":"pntd.0011401.ref064","doi-asserted-by":"crossref","first-page":"4153","DOI":"10.1111\/mec.12848","article-title":"Invasion genetics of a human commensal rodent: the black rat Rattus rattus in Madagascar","volume":"23","author":"C Brouat","year":"2014","journal-title":"Mol Ecol"},{"issue":"1","key":"pntd.0011401.ref065","first-page":"1","article-title":"Genetic structure and gene flow of the flea Xenopsylla cheopis","volume":"10","author":"M Harimalala","year":"2017","journal-title":"Madagascar and Mayotte. Parasit Vectors"},{"issue":"10029","key":"pntd.0011401.ref066","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1016\/S0140-6736(15)00417-1","article-title":"Averting a malaria disaster: will insecticide resistance derail malaria control?","volume":"387","author":"J Hemingway","year":"2016","journal-title":"The Lancet"},{"issue":"8","key":"pntd.0011401.ref067","doi-asserted-by":"crossref","first-page":"e42857","DOI":"10.1371\/journal.pone.0042857","article-title":"Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda","volume":"7","author":"R Kigozi","year":"2012","journal-title":"PloS One"},{"issue":"2","key":"pntd.0011401.ref068","first-page":"434","article-title":"Fipronil Pellets Reduce Flea Abundance on Black-Tailed Prairie Dogs: Potential Tool for Plague Management and Black-Footed Ferret Conservation","volume":"57","author":"DA Eads","year":"2021","journal-title":"J Wildl Dis"},{"issue":"4","key":"pntd.0011401.ref069","first-page":"455","article-title":"An insecticide-bait-box method for the control of sylvatic plague vectors","volume":"56","author":"L. Kartman","year":"1958","journal-title":"J Hyg"},{"issue":"8","key":"pntd.0011401.ref070","doi-asserted-by":"crossref","first-page":"e0007604","DOI":"10.1371\/journal.pntd.0007604","article-title":"Field assessment of insecticide dusting and bait station treatment impact against rodent flea and house flea species in the Madagascar plague context","volume":"13","author":"A Miarinjara","year":"2019","journal-title":"PLoS Negl Trop Dis"}],"container-title":["PLOS Neglected Tropical Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0011401","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,19]],"date-time":"2023-12-19T14:40:51Z","timestamp":1702996851000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0011401"}},"subtitle":[],"editor":[{"given":"Jean-philippe","family":"David","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,8,22]]},"references-count":70,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8,22]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pntd.0011401","relation":{},"ISSN":["1935-2735"],"issn-type":[{"value":"1935-2735","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,22]]}}}