Eisen RJ, Gage KL, 2012. Transmission of flea-borne zoonotic agents. Annu Rev Entomol 57: 61–82.
Bertherat EG, 2019. Plague around the world. Wkly Epidemiol Rec 94: 289–292.
Andrianaivoarimanana V, Piola P, Wagner DM, Rakotomanana F, Maheriniaina V, Andrianalimanana S, Chanteau S, Rahalison L, Ratsitorahina M, Rajerison M, 2019. Trends of human plague, Madagascar, 1998–2016. Emerg Infect Dis 25: 220–228.
Chanteau S, 2006. Atlas de la Peste à Madagascar. Paris, France: IRD Editions, Institut Pasteur/AUF.
Coulanges P, Clerc Y, Randrianantoanina E, 1982. Etude de X. cheopis et S. fonquerniei, puces pestigènes malgaches—Mise en évidence de leur résistance aux DDT, Dieldrin et Malathion. Archives de l’Institut. Pasteur de Madagascar 49: 171–191.
Ratovonjato J, Duchemin J-B, Duplantier J-M, Chanteau S, 2000. Xenopsylla cheopis (Siphonaptera: Xenopsyllinae), puces des foyers ruraux de peste des Hautes Terres malgaches: Niveau de sensibilité au DDT, aux pyréthrinoïdes et aux carbamates après 50 années de lutte chimique. Arch Inst Pasteur Madagascar 66: 9–12.
Boyer S, Miarinjara A, Elissa N, 2014. Xenopsylla cheopis (Siphonaptera: Pulicidae) susceptibility to deltamethrin in Madagascar. PLoS One 9: e111998.
Miarinjara A, Boyer S, 2016. Current perspectives on plague vector control in Madagascar: Susceptibility status of Xenopsylla cheopis to 12 insecticides. PLoS Negl Trop Dis 10: e0004414.
Rahelinirina S, Harimalala M, Rakotoniaina J, Randriamanantsoa MG, Dentinger C, Zohdy S, Girod R, Rajerison M, 2022. Tracking of mammals and their fleas for plague surveillance in Madagascar, 2018-2019. Am J Trop Med Hyg 106: 1601–1609.
Miarinjara A, Vergain J, Kavaruganda JM, Rajerison M, Boyer S, 2017. Plague risk in vulnerable community: Assessment of Xenopsylla cheopis susceptibility to insecticides in Malagasy prisons. Infect Dis Poverty 6: 141.
Rivero A, Vézilier J, Weill M, Read AF, Gandon S, 2010. Insecticide control of vector-borne diseases: When is insecticide resistance a problem? PLOS Pathog 6: e1001000.
Brogdon WG, McAllister JC, 1998. Insecticide resistance and vector control. Emerg Infect Dis 4: 605–613.
Alderson J, Quastel M, Wilson E, Bellamy D, 2020. Factors influencing the re-emergence of plague in Madagascar. Emerg Top Life Sci 4: 411–421.
World Health Organization, 1970. Insecticide resistance and vector control. Seventeenth Report of the WHO Expert Committee on Insecticides. World Health Organ Tech Rep Ser 443: 1–279.
Patel TB, Bhatia SC, Deobhankar RB, 1960. A confirmed case of DDT-resistance in Xenopsylla cheopis in India. Bull World Health Organ 23: 301–312.
World Health Organization, 1958. Insect Resistance and Vector Control. Eighth Report of the Expert Committee on Insecticides. Geneva, Switzerland: WHO, 67.
World Health Organization, 1980. Resistance of Vectors of Disease to Pesticides: Fifth Report of the WHO Expert Committee on Vector Biology and Control. Geneva, Switzerland: WHO.
World Health Organization, 1986. Resistance of Vectors and Reservoirs of Diseases to Pesticides: Tenth Report of the WHO Expert Committee on Vector Biology and Control. Geneva, Switzerland: WHO.
Randriamaherijaona S, Velonirina HJ, Boyer S, 2016. Susceptibility status of Anopheles arabiensis (Diptera: Culicidae) commonly used as biological materials for evaluations of malaria vector control tools in Madagascar. Malar J 15: 338.
Fontenille D, Coulanges P, 1987. Notes sur la sensibilité des puces Xenopsylla cheopis de la région d’Antananarivo à la déltamethrine et au propoxur. Arch Inst Pasteur Madagascar 53: 209–213.
World Health Organization, 1998. Test Procedures for Insecticide Resistance Monitoring in Malaria Vectors, Bioefficacy and Persistence of Insecticides on Treated Surfaces. Geneva, Switzerland: WHO.
Hutton SM et al., 2023. Knockdown resistance mutations are common and widely distributed in Xenopsylla cheopis fleas that transmit plague in Madagascar. PLOS Negl Trop Dis 17: e0011401.
Ilg T, Schmalz S, Werr M, Cramer J, 2010. Acetylcholinesterases of the cat flea Ctenocephalides felis: Identification of two distinct genes and biochemical characterization of recombinant and in vivo enzyme activities. Insect Biochem Mol Biol 40: 153–164.
Brunet S, Le Meter C, Murray M, Soll M, Audonnet J-C, 2009. rdl gene polymorphism and sequence analysis and relation to in vivo fipronil susceptibility in strains of the cat flea. J Econ Entomol 102: 366–372.
Li X, Schuler MA, Berenbaum MR, 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52: 231–253.
Enayati AA, Ranson H, Hemingway J, 2005. Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3–8.
Ghavami MB, Haghi FP, Alibabaei Z, Enayati AA, Vatandoost H, 2018. First report of target site insensitivity to pyrethroids in human flea, Pulex irritans (Siphonaptera: Pulicidae). Pestic Biochem Physiol 146: 97–105.
Rust MK et al., 2015. Susceptibility of adult cat fleas (Siphonaptera: Pulicidae) to insecticides and status of insecticide resistance mutations at the rdl and knockdown resistance loci. Parasitol Res 114 (Suppl 1 ):7–18.
Bossard RL, Hinkle NC, Rust MK, 1998. Review of insecticide resistance in cat fleas (Siphonaptera: Pulicidae). J Med Entomol 35: 415–422.
Ames AD, 2011. DDT and Pyrethroid Resistance in Xenopsylla cheopis (Rothschild), the Oriental Rat Flea in Northern Uganda. PhD Thesis, Department of Microbiology, Immunology, and Pathology, Colorado State University: Fort Collins, CO.
Miarinjara A, Rahelinirina S, Razafimahatratra NL, Girod R, Rajerison M, Boyer S, 2019. Field assessment of insecticide dusting and bait station treatment impact against rodent flea and house flea species in the Madagascar plague context. PLOS Negl Trop Dis 13: e0007604.
Ratovonjato J, Duchemin J-B, Chanteau S, 2000. Méthode optimisée d’élevage de pulicidés (Xenopsylla cheopis et Synopsyllus fonquerniei). Arch Inst Pasteur Madagascar 66: 75–77.
Finney DJ, 1952. Probit analysis, 2nd edition. J Inst Actuaries 78: 388–390.
Mann HB, Whitney DR, 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann Math Statist 18: 50–60.
R Core Team, 2021. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Busvine JR, Lien J, 1961. Methods for measuring insecticide susceptibility levels in bed-bugs, cone-nosed bugs, fleas and lice. Bull World Health Organ 24: 509–517.
Brogdon WG, Chan A, 2010. Guidelines for evaluating insecticide resistance in vectors using the CDC bottle bioassay. Methods in Anopheles Research. Atlanta, GA: CDC.
Hemingway J, 1995. Efficacy of etofenprox against insecticide susceptible and resistant mosquito strains containing characterized resistance mechanisms. Med Vet Entomol 9: 423–426.
Seidy S, Tavassoli M, Malekifard F, 2022. Pyrethroids resistance in Pulex irritans and Ctenocephalides canis in west and northwest Iran. Vet Res Forum 13: 529–535.
Brogdon WG, 1989. Biochemical resistance detection: An alternative to bioassay. Parasitol Today 5: 56–60.
Boyer S, 2006. Résistance Métabolique des Larves de Moustiques Aux Insecticides: Conséquences Environnementales. Thesis, Université Joseph-Fourier–Grenoble I, Grenoble, France.
Ugaki M, Shono T, Fukami J-I, 1985. Metabolism of fenitrothion by organophosphorus-resistance and susceptibility house flies, Musca domestica L. Pestic Biochem Phys 23: 33–40.
Pethuan S, Jirakanjanakit N, Saengtharatip S, Chareonviriyaphap T, Kaewpa D, Rongnoparut P, 2007. Biochemical studies of insecticide resistance in Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Thailand. Trop Biomed 24: 7–15.
Hemingway J, Miyamoto J, Herath PRJ, 1991. A possible novel link between organophosphorus and DDT insecticide resistance genes in Anopheles: Supporting evidence from fenitrothion metabolism studies. Pestic Biochem Phys 39: 49–56.
Bass C, Schroeder I, Turberg A, Field LM, Williamson MS, 2004. Identification of the rdl mutation in laboratory and field strains of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Pest Manag Sci 60: 1157–1162.
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The Oriental rat flea, Xenopsylla cheopis, is known worldwide as an efficient plague vector, including in Madagascar, where the disease remains a public health concern. Chemical control is the primary response method against X. cheopis in Madagascar. Previous bioassays focusing on different flea populations from Madagascar showed phenotypic resistance to various insecticides, including deltamethrin and fenitrothion, which, respectively, represent the previous and current chemicals for flea vector control. Despite apparent insecticide resistance, the associated mechanisms of this resistance remain poorly known. The aims of this study were to adjust diagnostic doses of deltamethrin and fenitrothion and to investigate the metabolism-based insecticide resistance of X. cheopis in Madagascar. Five available laboratory-reared flea strains of X. cheopis were selected, and their susceptibility statuses to deltamethrin and fenitrothion were determined using the WHO standard bioassay. Diagnostic doses of each insecticide were determined by the probit method, in accordance with concentration gradients. Biochemical microplate-based assays were performed to detect overproduction of cytochrome P450, alpha-/beta-esterases, and glutathione S-transferase (GST), which are signatures of metabolic resistance. The five tested strains showed different susceptibility statuses against deltamethrin and fenitrothion. The diagnostic doses were estimated to be 0.07% for deltamethrin and 1.56% for fenitrothion. Increased activities of cytochrome P450, beta-esterase, and GST enzymes in the resistant strains were revealed in comparison with those of the susceptible strain. In conclusion, readjusted diagnostic doses will help to better understand the susceptibility status of X. cheopis to deltamethrin and fenitrothion. The overproduction of cytochrome P450, beta-esterase, and GST observed on deltamethrin-resistant flea strains suggests metabolic resistance.
The American Society of Tropical Medicine and Hygiene (ASTMH) assisted with publication expenses.
Disclosure: Protocols involving animal handling in the laboratory for flea maintenance were approved by the animal ethics committee of the Institut Pasteur de Madagascar (reference no. 425/2021/IPM/DS/CEA).
Authors’ contributions: Conceptualization: R. Girod, F. N. Raharimalala, and M. Harimalala. Data curation: A. O. Raveloson, F. N. Raharimalala, and M. Harimalala. Formal analysis: A. O. Raveloson, T. Nepomichene, and M. Harimalala. Funding acquisition: R. Girod. Investigation: A. O. Raveloson. Methodology: A. O. Raveloson, F. N. Raharimalala, and M. Harimalala. Project administration: R. Girod. Resources: R. Girod. Supervision: R. Girod and M. Harimalala. Validation: R. Girod and M. Harimalala. Visualization: R. Girod. Writing – original draft preparation: A. O. Raveloson and M. Harimalala. Writing – review & editing: A. O. Raveloson, M. Harimalala, T. Nepomichene, and R. Girod
Current contact information: Annick O. Raveloson, Thiery Nepomichene, Tojo R. Ramihangihajason, Mandimby Rajaonarimanana, Fara N. Raharimalala, and Romain Girod, Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar, E-mails: onimalalaanickr@gmail.com, Jthiery@pasteur.mg, tojor@pasteur.mg, mandimby@pasteur.mg, rfaranantenaina@gmail.com, and romain.girod@pasteur.fr. Mireille Harimalala, Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar, and Ecole Doctorale Science de la Vie et de l’Environnement, Université d’Antananarivo, Antananarivo, Madagascar, E-mail: hmireille@pasteur.mg.
Eisen RJ, Gage KL, 2012. Transmission of flea-borne zoonotic agents. Annu Rev Entomol 57: 61–82.
Bertherat EG, 2019. Plague around the world. Wkly Epidemiol Rec 94: 289–292.
Andrianaivoarimanana V, Piola P, Wagner DM, Rakotomanana F, Maheriniaina V, Andrianalimanana S, Chanteau S, Rahalison L, Ratsitorahina M, Rajerison M, 2019. Trends of human plague, Madagascar, 1998–2016. Emerg Infect Dis 25: 220–228.
Chanteau S, 2006. Atlas de la Peste à Madagascar. Paris, France: IRD Editions, Institut Pasteur/AUF.
Coulanges P, Clerc Y, Randrianantoanina E, 1982. Etude de X. cheopis et S. fonquerniei, puces pestigènes malgaches—Mise en évidence de leur résistance aux DDT, Dieldrin et Malathion. Archives de l’Institut. Pasteur de Madagascar 49: 171–191.
Ratovonjato J, Duchemin J-B, Duplantier J-M, Chanteau S, 2000. Xenopsylla cheopis (Siphonaptera: Xenopsyllinae), puces des foyers ruraux de peste des Hautes Terres malgaches: Niveau de sensibilité au DDT, aux pyréthrinoïdes et aux carbamates après 50 années de lutte chimique. Arch Inst Pasteur Madagascar 66: 9–12.
Boyer S, Miarinjara A, Elissa N, 2014. Xenopsylla cheopis (Siphonaptera: Pulicidae) susceptibility to deltamethrin in Madagascar. PLoS One 9: e111998.
Miarinjara A, Boyer S, 2016. Current perspectives on plague vector control in Madagascar: Susceptibility status of Xenopsylla cheopis to 12 insecticides. PLoS Negl Trop Dis 10: e0004414.
Rahelinirina S, Harimalala M, Rakotoniaina J, Randriamanantsoa MG, Dentinger C, Zohdy S, Girod R, Rajerison M, 2022. Tracking of mammals and their fleas for plague surveillance in Madagascar, 2018-2019. Am J Trop Med Hyg 106: 1601–1609.
Miarinjara A, Vergain J, Kavaruganda JM, Rajerison M, Boyer S, 2017. Plague risk in vulnerable community: Assessment of Xenopsylla cheopis susceptibility to insecticides in Malagasy prisons. Infect Dis Poverty 6: 141.
Rivero A, Vézilier J, Weill M, Read AF, Gandon S, 2010. Insecticide control of vector-borne diseases: When is insecticide resistance a problem? PLOS Pathog 6: e1001000.
Brogdon WG, McAllister JC, 1998. Insecticide resistance and vector control. Emerg Infect Dis 4: 605–613.
Alderson J, Quastel M, Wilson E, Bellamy D, 2020. Factors influencing the re-emergence of plague in Madagascar. Emerg Top Life Sci 4: 411–421.
World Health Organization, 1970. Insecticide resistance and vector control. Seventeenth Report of the WHO Expert Committee on Insecticides. World Health Organ Tech Rep Ser 443: 1–279.
Patel TB, Bhatia SC, Deobhankar RB, 1960. A confirmed case of DDT-resistance in Xenopsylla cheopis in India. Bull World Health Organ 23: 301–312.
World Health Organization, 1958. Insect Resistance and Vector Control. Eighth Report of the Expert Committee on Insecticides. Geneva, Switzerland: WHO, 67.
World Health Organization, 1980. Resistance of Vectors of Disease to Pesticides: Fifth Report of the WHO Expert Committee on Vector Biology and Control. Geneva, Switzerland: WHO.
World Health Organization, 1986. Resistance of Vectors and Reservoirs of Diseases to Pesticides: Tenth Report of the WHO Expert Committee on Vector Biology and Control. Geneva, Switzerland: WHO.
Randriamaherijaona S, Velonirina HJ, Boyer S, 2016. Susceptibility status of Anopheles arabiensis (Diptera: Culicidae) commonly used as biological materials for evaluations of malaria vector control tools in Madagascar. Malar J 15: 338.
Fontenille D, Coulanges P, 1987. Notes sur la sensibilité des puces Xenopsylla cheopis de la région d’Antananarivo à la déltamethrine et au propoxur. Arch Inst Pasteur Madagascar 53: 209–213.
World Health Organization, 1998. Test Procedures for Insecticide Resistance Monitoring in Malaria Vectors, Bioefficacy and Persistence of Insecticides on Treated Surfaces. Geneva, Switzerland: WHO.
Hutton SM et al., 2023. Knockdown resistance mutations are common and widely distributed in Xenopsylla cheopis fleas that transmit plague in Madagascar. PLOS Negl Trop Dis 17: e0011401.
Ilg T, Schmalz S, Werr M, Cramer J, 2010. Acetylcholinesterases of the cat flea Ctenocephalides felis: Identification of two distinct genes and biochemical characterization of recombinant and in vivo enzyme activities. Insect Biochem Mol Biol 40: 153–164.
Brunet S, Le Meter C, Murray M, Soll M, Audonnet J-C, 2009. rdl gene polymorphism and sequence analysis and relation to in vivo fipronil susceptibility in strains of the cat flea. J Econ Entomol 102: 366–372.
Li X, Schuler MA, Berenbaum MR, 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52: 231–253.
Enayati AA, Ranson H, Hemingway J, 2005. Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3–8.
Ghavami MB, Haghi FP, Alibabaei Z, Enayati AA, Vatandoost H, 2018. First report of target site insensitivity to pyrethroids in human flea, Pulex irritans (Siphonaptera: Pulicidae). Pestic Biochem Physiol 146: 97–105.
Rust MK et al., 2015. Susceptibility of adult cat fleas (Siphonaptera: Pulicidae) to insecticides and status of insecticide resistance mutations at the rdl and knockdown resistance loci. Parasitol Res 114 (Suppl 1 ):7–18.
Bossard RL, Hinkle NC, Rust MK, 1998. Review of insecticide resistance in cat fleas (Siphonaptera: Pulicidae). J Med Entomol 35: 415–422.
Ames AD, 2011. DDT and Pyrethroid Resistance in Xenopsylla cheopis (Rothschild), the Oriental Rat Flea in Northern Uganda. PhD Thesis, Department of Microbiology, Immunology, and Pathology, Colorado State University: Fort Collins, CO.
Miarinjara A, Rahelinirina S, Razafimahatratra NL, Girod R, Rajerison M, Boyer S, 2019. Field assessment of insecticide dusting and bait station treatment impact against rodent flea and house flea species in the Madagascar plague context. PLOS Negl Trop Dis 13: e0007604.
Ratovonjato J, Duchemin J-B, Chanteau S, 2000. Méthode optimisée d’élevage de pulicidés (Xenopsylla cheopis et Synopsyllus fonquerniei). Arch Inst Pasteur Madagascar 66: 75–77.
Finney DJ, 1952. Probit analysis, 2nd edition. J Inst Actuaries 78: 388–390.
Mann HB, Whitney DR, 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann Math Statist 18: 50–60.
R Core Team, 2021. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Busvine JR, Lien J, 1961. Methods for measuring insecticide susceptibility levels in bed-bugs, cone-nosed bugs, fleas and lice. Bull World Health Organ 24: 509–517.
Brogdon WG, Chan A, 2010. Guidelines for evaluating insecticide resistance in vectors using the CDC bottle bioassay. Methods in Anopheles Research. Atlanta, GA: CDC.
Hemingway J, 1995. Efficacy of etofenprox against insecticide susceptible and resistant mosquito strains containing characterized resistance mechanisms. Med Vet Entomol 9: 423–426.
Seidy S, Tavassoli M, Malekifard F, 2022. Pyrethroids resistance in Pulex irritans and Ctenocephalides canis in west and northwest Iran. Vet Res Forum 13: 529–535.
Brogdon WG, 1989. Biochemical resistance detection: An alternative to bioassay. Parasitol Today 5: 56–60.
Boyer S, 2006. Résistance Métabolique des Larves de Moustiques Aux Insecticides: Conséquences Environnementales. Thesis, Université Joseph-Fourier–Grenoble I, Grenoble, France.
Ugaki M, Shono T, Fukami J-I, 1985. Metabolism of fenitrothion by organophosphorus-resistance and susceptibility house flies, Musca domestica L. Pestic Biochem Phys 23: 33–40.
Pethuan S, Jirakanjanakit N, Saengtharatip S, Chareonviriyaphap T, Kaewpa D, Rongnoparut P, 2007. Biochemical studies of insecticide resistance in Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Thailand. Trop Biomed 24: 7–15.
Hemingway J, Miyamoto J, Herath PRJ, 1991. A possible novel link between organophosphorus and DDT insecticide resistance genes in Anopheles: Supporting evidence from fenitrothion metabolism studies. Pestic Biochem Phys 39: 49–56.
Bass C, Schroeder I, Turberg A, Field LM, Williamson MS, 2004. Identification of the rdl mutation in laboratory and field strains of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Pest Manag Sci 60: 1157–1162.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 2495 | 2495 | 1656 |
Full Text Views | 17 | 17 | 10 |
PDF Downloads | 21 | 21 | 8 |