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Among the most serious obstacles in vector control programs for human diseases is the development of resistance to the insecticides used. According to WHO, approximately 40% of the 506 medically important arthropods show some degree of insecticide resistance. Of these species, about 50% are species of mosquitoes that vector malaria, dengue, yellow fever and filariasis. The two principal mechanisms of insecticide resistance are alterations in the target site or an increase in the detoxification rate of the insecticide. Once resistance is detected in a vector population it is crucial to determine its molecular and biochemical basis. Identification of resistance mechanisms permits the selection of insecticides to use in control programs and the evaluation of potential development of resistance to alternative insecticides. This review presents basic information regarding the main mechanisms of insecticide resistance identified in mosquito vectors of human diseases and the methodologies most used to monitor and detect them.

FONSECA, I., & QUIÑONES, M. L. (2005). Insecticide resistance in mosquitoes (Diptera: Culicidae): mechanisms, detection and monitoring in public health. Revista Colombiana De Entomología, 31(2), 107–115. https://doi.org/10.25100/socolen.v31i2.9429

BEALL, C.; FYRBERG, C.; SONG, S.; FYRBERG, E. 1992. Isolation of a Drosophila gene encoding glutathione Stransferase. Biochemical Genetics 30: 515527.

BERGE, J. B.; FEYEREISEN, R.; AMICHOT, M. 1998. Cytochrome P450 monooxygenases and insecticide resistance in insects. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353: 1701-1705.

BERMÚDEZ, I.; HAWKINS, C. A.; TAYLOR,A. M.; BEADLE, D. J. 1991. Actions of insecticides on the insect GABA receptor complex. Journal of Receptor Research 11: 221-232.

BERTICAT, C.; BOQUIEN, G.; RAYMOND, M.; CHEVILLON, C. 2002. Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genetical Research 79: 41-47.

BRANDT, A.; SHART, M.; PEDRA, J. H. F.; HOLMES, G.; DEAN, A.; KREITMAN, M.; PITTENDRIGH, B. R. 2002. Differential expression and induction of two Drosophila cytochrome P450 genes near the Rst(2)DDt locus. Insect Molecular Biology 11: 337-341.

BRENGUES, C.; HAWKES, N. J.; CHANDRE, F.; MCCARROLL, L.; DUCHON, S.; GUILLET, P.; MANGUIN, S.; MORGAN, J. C.; HEMINGWAY, J. 2003. Pyrethroid and DDT cross-resistance in Aedes aegypti is correlated with novel mutations in the voltage-gated sodium channel gene. Medical and Veterinary Entomology 17: 87-94.

BROGDON, W. G. 1984. Mosquito protein microassay. I. Protein determinations from small portions of single-mosquito homogenates. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 79: 457-9.

BROGDON, W. G; MCALLISTER, J. C. 1998a. Insecticide Resistance and Vector Control. Emerging Infectious Diseases 4: 605-613.

BROGDON, W. G; MCALLISTER, J. C. 1998b. Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. Journal of the American Mosquito Control Association 14: 159-164.

BROOKE, B. D.; KLOKE, G.; HUNT, R. H.; KOEKEMOER, L. L.; TEMU, E. A.; TAYLOR, M. E.; SMALL, G.; HEMINGWAY, J.; COETZEE, M. 2001. Bioassay and biochemical analysis of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bulletin of Entomological Research 91: 265-272.

BROWN, A. W. A. 1986. Insecticide resistance in mosquitoes: a pragmatic review. Journal of the American Mosquito Control Association 2: 123-140.

CALZI, M.; RAVILO, C.; GHIBAUNDI, E.; DE GIOIA, L.; SALMONA, M.; CAZZANIGA, G.; KUROSAKI, M.; TERAO, M.; GARATTINI, E. 1995. Purification, cDNA cloning and tissue distribution of bovine liver aldehyde oxidase. The Journal of Biological Chemistry 270: 31037-31045.

CHANDRE, F.; DARRIER, F.; MANGA, L.; AKOGBETO, M.; FAYE, O.; MOUCHET, J.; GUILLET, P. 1999. Status of pyrethorid resistance in Anopheles gambiae sensu lato. Bulletin of the World Health Organization 77(3): 230-234.

CLARK, A. G.; SHAMAAN, N. A. 1984. Evidence that DDT-dehydrochlorinase from the housefly is a glutathione Stransferase. Pesticide Biochemistry and Physiology 22: 249-261.

COLEMAN, M.; VONTAS, J. G.; HEMINGWAY, J. 2002. Molecular characterization of the amplified aldehyde oxidase from insecticide resistant Culex quinquefasciatus. European Journal of Biochemistry 269: 768-779.

CORBEL, V.; DARRIET, F.; CHANDRE, F.; HOUGARD, J. M. 2002. Insecticide Mixtures for Mosquito Net Impregnation Against Malaria Vectors. Parasite 9: 255-259.

CORBETT, J. R. 1974. The Biochemical mode of action of pesticides. Academic Press, London, UK. pp. 102-130.

CURTIS, C. F. 1993. Workshop on bednets at the International Congress of Tropical Medicine. Japanese Journal of Sanitary Zoology. 44: 65-68.

CURTIS, C. F. 2002. Should the use of DDT be revived for malaria vector control? Biomedica 22: 455-61.

CURTIS, C. F.; TOWNSON, H. 1998. Malaria: existing methods of vector control and molecular entomology. British Medical Bulletin 54: 311-325.

CYGLER, M.; SCHRAG, J. D.; SUSSMAN, J. L.; HAREL, M.; SILMAN, I.; GENTRY, M. K. 1993. Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases and related proteins. Protein Science 2: 366-82.

DABORN, P. J.; YEN, J. L.; BOGWITZ, M. R.; LEGOFF, G.; FEIL, E.; JEFFERS, S.; TIJET, N.; PERRY, T.; HECKEL, D.; BATTERMAN, P.; FEYEREISEN, R.; WILSON, T. G.; FFRENCH-CONSTANT, R. H. 2002. A single P450 allele associated with insecticide resistance in Drosophila. Science 297: 2253-2256.

DING, Y.; ORTELLI, F.; ROSSITER, L. C.; HEMINGWAY, J.; RANSON, H. 2003. The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. Genomics 13: 4-35.

DONG, K. 1997. A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroaches. Insect Molecular Biology 27: 93-100.

FFRENCH-CONSTANT, R. H.; STEICHEN, J.; ROCHELAU, T. A.; ARONSTEIN, K.; ROUSH, R. T. 1993a. A single amino-acid substitution in a g-aminobutyric acid subtype. A receptor locus associated with Ciclodiene insecticide resistance in Drosophila populations. Proceedings of the National Academy of Sciences of the United States of America 90: 1957-1961.

FFRENCH-CONSTANT, R. H.; ROCHELAU, T. A.; STEICHEN, J. C.; CHALMERS, A. E. 1993b. A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363: 449-451.

FFRENCH-CONSTANT, R. H.; PITTENDRIGH, B.; VAUGHAN, A.; ANTHONY, N. 1998. Why are there so few resistanceassociated mutations in insecticide target genes? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 353: 1685-1693.

GAZAVE, E.; CHEVILLON, C.; LENORMAND, T.; MARQUINE, M.; RAYMOND, M. 2001. Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pippiens. Heredity 87: 441-448.

GEORGHIOU, G. P. 1990. Overview of insecticide resistance. Pages 18-41. In: M. B. Green, H.M. LeBaron and W. K. Moberg (eds.). Managing resistance to agrochemical from fundamental research to practical strategies. American Chemical Society Series. 421, Washington. DC. 421 p.

GUILLEMAUD, T.; MAKATE, N.; RAYMOND, M.; HIRST, B.; CALLAGHAN, A. 1997. Esterase gene amplification in Culex pipiens. Insect Molecular Biology 6: 319-327.

HARGREAVES, K.; KOEKEMOER, L. L.; BROOKE, B. D.; HUNT, R. H.; MTHEMBU, J.; COHETES, M. 2000. Anopheles funestus resistant to pyrethorid insecticidas in South Africa. Medical and Veterinary Entomology 14: 181-189.

HEMINGWAY, J.; BODDINGTON, R. G.; HARRIS, J.; DUNBAR, S. J. 1989. Mechanisms of insecticide resistance in Aedes aegypti (L.) (Diptera: Culicidae) from Puerto Rico. Bulletin of Entomological Research 79: 123-130.

HEMINGWAY, J.; HAWKES, N.; PRAPANTHADARA, L.; JAYAWARDENA, K. G. I.; RANSON, H. 1998. The role of gene splicing, gene amplification and regulation in mosquito insecticide resistance. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353: 1695-1699.

HEMINGWAY, J.; KARUNARATNE, S. H. P. P. 1998. Mosquito carboxylesterases: a review of molecular biology and biochemistry of a major insecticide resistance mechanism. Medical and Veterinary Entomology 12: 1-12.

HEMINGWAY, J.; RANSON, H. 2000. Insecticide Resistance in Insect Vectors of Human Disease. Annual Review of Entomology 45: 371-391.

HEMINGWAY, J.; COLEMAN, M.; PATON, M.; MCCARROLL, L.; VAUGHAN, A.; DESILVA, D. 2000. Aldehyde Oxidase is coamplified with the World’s most common Culex mosquito insecticide resistanceassociated esterases. Insect Molecular Biology 9: 93-99.

HEMINGWAY, J.; FIELD, L.; VONTAS, J. 2002. An Overview of Insecticide Resistance. Science 298: 96-97.

KARUNARATNE, S. H. P. P.; JAYAWARDENA, K. G. I.; HEMINGWAY, J.; KETTERMAN, A. J. 1993. Characterization of a B-type esterase involved in insecticide resistance from the mosquito Culex quinquefasciatus. The Biochemical Journal 294: 575-579.

KARUNARATNE, S. H. P. P.; VAUGHAN, A.; PATON, M. G.; HEMINGWAY, J. 1998. Amplification of a serine esterase gene is involved in insecticide resistance in Sri Lankan Culex tritaeniorhynchus. Insect Molecular Biology 7: 307-315.

KOSTAROPOULOS, I.; PAPADOPOULOS, A. I.; METAXAKIS, A.; BOUKOUVALA, E.; PAPADOPOULOU—MOURKIDOU, E. 2001. Glutathione S-transferase in the defense against pyrethroid insecticides. Insect Molecular Biology 31: 313-319.

LENGELER, C.; CATTANI, J.; DE SAVIGNY, D. 1996. Net Gain: A New Method for preventing malaria deaths. International Development Research Center, Otawa and World health Organization, Geneva.

LOUGHNEY, K.; KREBER, R.; GANETZKY, B. 1989. Molecular analysis of the para locus, sodium channel gene in Drosophila. Cell 58: 1143-1154.

MALCOLM, C. A.; BOURGUET, D.; ASCOLILLO, A.; ROOKER, S. J.; GARVEY, C. F. 1998. A sex linked Ace gene, not linked to insensitivity acetylcholinesterase-mediated insecticide resistance in Culex pipiens. Insect Molecular Biology 7: 107-20.

MARTÍNEZ-TORRES, D.; CHANDRE, F.; WILLIAMSON, M. S.; DARRIET, F.; BERGE, J. B.; DEVONSHIRRE, A. L.; GUILLET, P.; PASTEUR, N.; PAURON, D. 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Molecular Biology 7: 179-184.

MARTÍNEZ-TORRES, D.; FOSTER, S. P.; FIELD, L. M.; DEVONSHIRRE, A. L.; WILLIAMSON, M. S. 1999. A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach-potato aphid, Myzuspersicae (Hemiptera: Aphididae). Insect Molecular Biology 8: 339-346.

MILATOVIC, D.; MORETTO, A.; OSMAN, K. A.; LOTTI, M. 1997. Phenyl valerate esterases other than neuropathy target esterase and the promotion of organophosphate polyneuropathy. Chemical Research in Toxicology 10(9): 1045-1048.

MUTERO, A.; PRALAVORIO, M.; BRIDE, J. M.; FOURNIER, D. 1994. Resistanceassociated point mutations in insecticide insensitive acetylcholinesterase. Proceedings of the National Academy of Sciences of the United States of America 91: 59225926.

NAJERA, J. A.; ZAIM, M. 2002. Malaria Vector Control: Decision making criteria and procedures for judicious use of insecticides. WHO Pesticide Evaluation Scheme (WHOPES), World Health Organization, Geneva.

NARANG, S.; SEAWRIGHT, J. A. 1983. Genetic mapping and characterization of an aldehyde oxidase of Anopheles albimanus. Biochemical Genetics 21: 653-660.

ORTELLI, F.; ROSITER, L. C.; VONTAS, J.; RANSON, H.; HEMINGWAY, J. 2003. Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide resistance locus, from the malaria vector Anopheles gambiae. The Biochemical Journal 373: 957-963.

PATIL, N. S.; LOLE, K. S.; DEOBAGKAR, D. N. 1996. Adaptive larval thermotolerance and induced cross-tolerance to propoxur insecticide in mosquitoes Anopheles stephensi and Aedes aegypti. Medical and Veterinary Entomology 10: 277-82.

PATON, M. G.; KARUNARATNE, S. H. P. P.; GIAKOUMAKI, E.; ROBERTS, N.; HEMINGWAY, J. 2000. Quantitative analysis of gene amplification in insecticide resistant Culex mosquitoes. The Biochemical Journal 346: 17-24.

PENILLA, R. P.; RODRÍGUEZ, A. D.; HEMINGWAY, J.; TORRES, J. L.; ARREDONDO-JIMÉNEZ, J. I.; RODRÍGUEZ, M. H. 1998. Resistance management strategies in malaria vector mosquito control. Baseline data for a large-scale field trial against Anopheles albimanus in Mexico. Medical and Veterinary Entomology 12: 217-233.

PHILLIPS, R. S. 2001. Current status of malaria and potential for control. Clinical Microbiology Reviews 14: 208-226.

QUIÑÓNES, M. L.; SUÁREZ, M. F.; FLEMING, G. A. 1987. Estado de la susceptibilidad al DDT de los principales vectores de malaria en Colombia y su implicación epidemiológica. Biomedica 7: 81-86.

RANSON, H.; COLLINS, F. H.; HEMINGWAY, J. 1998. The role of alternative mRNA splicing in generating heterogeneity within Anopheles gambiae class I GST family. Proceedings of the National Academy of Sciences of the United States of America. 95: 14284-14289.

RANSON, H.; JENSEN, B.; VULULE, J. M.;WANG, X.; HEMINGWAY, J.; COLLINS, F. H. 2000a. Identification of a novel mutation in the voltage-gated sodium channel gene of Anopheles gambiae associated with resistance to pyrethroid insecticides. Insect Molecular Biology 9: 491-497.

RANSON, H.; JENSEN, B.; WANG, X.; PRAPANTHADARA, L.; HEMINGWAY, J.; COLLINS, F. H. 2000b. Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Molecular Biology 9: 499-507.

RANSON, H.; ROSSITER, L.; ORTELLI, F.; JENSEN, B.; WANG, X.; ROTH, C. H.; COLLINS, F. H.; HEMINGWAY, J. 2001. Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. The Biochemical Journal 359: 295-304.

RANSON, H.; CLAUDIANOS, C.; ORTELLI, F.; ABGRALL, C.; HEMINGWAY, J.; SHARAKHOVA, M. V.; UNGER, M. F.; COLLINS, F. H.; FEYEREISEN, R. 2002a. Evolution of supergene families associated with insecticide resistance. Science 298: 179-181.

RANSON, H.; NIKOU, D.; HUTCHINSON, M.; WANG, X.; ROTH, C. W.; HEMINGWAY, J.; COLLINS, F. H. 2002b. Molecular analysis of multiple Cytochrome P450 genes from the malaria vector Anopheles gambiae. Insect Molecular Biology 11(5): 409-418.

RAYMOND, M.; CALLAGHAN, A.; FORT, P.; PASTEUR, N. 1991. Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 14; 350: 151-3.

RAYMOND, M.; CHEVILLON, C.; GUILLEMAUD, T.; LENORMAND, T.; PASTEUR, N. 1998. An overview of the evolution of overproduced esterases in the mosquito Culex pipiens. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353: 1707-1711.

REISS, R. A.; JAMES, A. A. 1993. A glutathion S-transferase gene of the vector mosquito Anopheles gambiae. Insect Molecular Biology 2: 25-32.

ROSE, R. L.; GOH, D.; THOMPSON, D. M.; VERMA, K. D.; HECKEL, D. G.; GAHAN, L. J.; ROE, R. M.; HODGSON, E. 1997. Cytochrome P450 CYP9A1. Heliothis virescens: the first member of a new CYP family. Insect Biochemistry and Molecular Biology 27: 605-615.

SALINAS, A. E.; WONG, M. G. 1999. Glutathione S-transferases – a review. Current Medicinal Chemistry 6: 279-309.

SCHULER, T. H.; MARTÍNEZ-TORRES, D.; THOMPSON, A. J.; DENHOLM, I.; DEVONSHIRE, A. L.; DUCE, I. R.; WILLIAMSON, M. S. 1998. Toxicological, electrophysiological, and molecular characterization of knockdown resistance to pyrethroid insecticides in the diamondback moth, Plutella xylostella (L.). Pesticide Biochemistry and Physiology 59: 169-182.

SCOTT, J. G. 1999. Cytochromes P450 and Insecticide Resistance. Insect Biochemistry and Molecular Biology 29: 757-777.

SCOTT, J. G.; WEN, Z. 2001. Cytochromes P450 of insects: the tip of the iceberg. Pest Management Science 57: 958-967.

SEVERINI, C. ; ROMI, R.; MARINUCCI,M.; GUILLEMAUD, T.; RAYMOND, M. 1997. Esterases A5-B5 in organophosphateresistant Culex pipiens from Italy. Medical and Veterinary Entomology 11: 123-126.

SHARF, M. E.; PARIMI, S.; MEINKE, L. J.; CHANDLER, L. D.; SIEGFRIED, B. D. 2001. Expression and induction of three family cytochrome P450 genes identified from insecticide-resistant and susceptible western corn rootworms. Insect Molecular Biology 10: 139-146.

SHEEHAN, D.; MEADE, G.; FOLEY, V. M.; DOWD, C. A. 2001. Structure, function and evolution of glutathione transferase: implications for classification of nonmammalian members of an ancient enzyme superfamily. The Biochemical Journal 360: 1-16.

SODERLUND, D. M.; BLOOMQUIST, J. R. 1989. Neurotoxic action of pyrethroid insecticides. Annual Review of Entomology 34: 77-96.

SUAREZ, M. F.; QUIÑONES, M. L.; PALACIOS, J. D.; CARRILLO, A. 1990. First Record of DDT Resistance in Anopheles darlingi. Journal of the American Mosquito Control Association 6: 72-74.

TABASHNIK, B.E. 1990. Implications of gene amplification for evolution and management of insecticide resistance. Journal of Economic Entomology 83: 1170-1176.

THOMPSON, M.; SHOTKOSKI, F.; FFRENCH-CONSTANT, R.H. 1993. Cloning and sequencing of the cyclodiene insecticide resistance gene from the yellow fever mosquito Aedes aegypti. FEBS Letters (Netherlands). 325: 187-190.

TIJET, N.; HELVIG, C.; FEYEREISEN, R. 2001. The cytochrome P450 gene superfamily in Drosophila melanogaster: annotation, intron-exon organization and phylogeny. Gene 262: 189-198.

TOUNG, Y-P. S.; HSIEH, T.; TU, C-P. D. 1993. The glutathione S-transferase D genes: a divergently organized, intronless gene family in Drosophila melanogaster. The Journal of Biological Chemistry 268: 9737-9746.

TURNER, A.; DOYLE, W. A.; VENTOM, A. M.; BRAY, R. C. 1995. Properties of rabbit liver aldehyde oxidase and the relationship of the enzyme to Xanthine Oxidase and dehydrogenase. European Journal of Biochemistry 232: 646-657.

VAIS, H.; WILLIAMSON, M. S.; DEVONSHIRE, A. L.; USHERWOOD, P. N. R. 2001. The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. Pest Management Science 57: 877-888.

VATANDOOST, H.; MCCAFFERY, A. R.; TOWNSON, H. 1996. An electrophysiological investigation of target site insensivity mechanisms in permethrinresistant and susceptibility strains of Anopheles stephensi. Transactions of the Royal Society of Tropical Medicine and Hygiene 90: 216.

VAUGHAN, A.; HAWKES, N.; HEMINGWAY, J. 1997. Co-amplification explains linkage disequilibrium of two mosquito esterase genes in insecticide resistance Culex quinquefasciatus. The Biochemical Journal 325: 359-365.

VAUGHAN, A.; CHADEE, D. D.; FFRENCHCONSTANT, R. H. 1998. Biochemical monitoring of organophosphorus and carbamate insecticide resistance in Aedes aegypti mosquitos from Trinidad. Medical and Veterinary Entomology 12: 318-321.

VONTAS, J. G.; SMALL, G. J.; HEMINGWAY, J. 2001. Glutathione S-transferase as antioxidant defense agents confers pyrethroid resistance in Nilaparvata lugens. The Biochemical Journal 357: 365-372.

VONTAS, J. G.; HEJAZI, M. J.; HAWKES, N. J.; COSMIDIS, N.; LOUKAS, M.; HEMINGWAY, J. 2002. Resistance-associated point mutations of organophosphate insensitive acetylcholinesterase in the olive fruit fly Bactrocera oleae. Insect Molecular Biology 11: 329-336.

WALSH, S. B.; DOLDEN, T. A.; MOORES, G. D.; KRISTENSEN, M.; LEWIS, T.; DEVONSHIRE, A. L.; WILLIAMSON, M. S. 2001. Identification and characterization of mutations in house fly (Musca domestica) acetylcholinesterase involved in insecticide resistance. The Biochemical Journal 359: 175-181.

WHO. 1975. Manual on Practical Entomology in Malaria. Part II. Methods and Techniques. World Health Organization, Geneva.

WHO. 1981. Resistance of vectors and reservoirs of disease to pesticides. WHO Technical Report Series No 737, 87 pp. World Health Organization, Geneva.

WHO. 1992. Vector resistance to pesticides. Fifteenth report of the expert committee on vector biology and control. WHO Technical Report Series No 818, 55 pp World Health Organization, Geneva.

WILLIAMSON, M. S.; DENHOLM, I.; BELL, C. A.; DEVONSHIRE, A. L. 1993. Knockdown resistance (kdr) to DDT and pyrethroid insecticides maps to a sodium channel gene locus in the housefly (Musca domestica). Molecular and General Genetics 240: 17-22.

WILLIAMSON, M. S.; MARTÍNEZ-TORRES, D.; HICK, C. A.; DEVONSHIRE, A. L. 1996. Identification of mutations in the housefly para-type sodium cannel gene associated with knockdown resistance (kdr) to pyrethroids insecticides. Molecular and General Genetics 252:51-60.

ZHOU, Z. H.; SYVANEN, M. 1997. A complex glutathione transferase gene family n the housefly Musca domestica. Molecular and General Genetics 256: 187-194.