Insecticide resistance in invasive mosquito species of the genus Aedes (Diptera: Culicidae) (review)

The review is devoted to invasive species of mosquitoes of the genus Aedes (Ae. albopictus, Ae. aegypti, Ae. koreicus) registered on the Black Sea coast of the Russian Federation. The main attention paid to Ae. albopictus and Ae. aegypti mosquitoes, having significant epidemiological importance, primarily as vectors of arboviral diseases. The main strategy for controlling the number of mosquitoes is the use of substances from different chemical groups with insecticidal activity, mainly pyrethroids, organophosphates (OP) and carbamates. Long-term use of pesticides with the same mechanism of action inevitably leads to the formation of resistance in arthropods based on specific and nonspecific mechanisms. In modern conditions, the problem of mosquito resistance to insecticides has a global character. We analyzed literature data on the mechanisms of resistance to different groups of insecticides at the molecular level in Ae. albopictus and Ae. aegypti mosquitoes. In particular, information is provided on the known: 1) kdr mutations leading to amino acid substitutions in voltage-sensitive sodium channels affected by pyrethroids and DDT; 2) rdl-mutations causing changes in GABA receptors and, as a consequence, resistance to phenylpyrazoles and a number of organochlorine compounds; 3) ace-mutations that reduce the sensitivity of the active center of acetylcholinesterase to ОP. The presence of nonspecific mechanisms of resistance, i.e. increase in the activity of enzyme systems involved in detoxification of xenobiotics, has also been shown in resistant individuals. Data on the occurrence of kdr-mutations in mosquitoes in different countries presented. It is noted that in Russia in Krasnodar region, populations of Ae. albopictus mosquitoes remain susceptible to pyrethroid insecticides. The strategy of controlling the number of invasive species of mosquitoes should include monitoring of their resistance to insecticides, which will allow timely selection of effective control tactics in case of epidemiological threat.

1. World Health Organization. Vector-borne diseases, 2024; [Электронный ресурс]. URL: https: //www.who.int/ru/news-room/fact-sheets/detail/vector-borne-diseases (дата обращения 10.06.2025).

2. Lühken R., Brattig N., Becker N. Introduction of invasive mosquito species into Europe and prospects for arbovirus transmission and vector control in an era of globalization // Infect. Dis. Poverty. 2023; 12(1): 109. DOI: 10.1186/s40249-023-01167-z.

3. Zé-Zé L., Freitas I.C., Silva M., Soares P., Alves M.J., Osório H.C. The spread of the invasive mosquito Aedes albopictus (Diptera: Culicidae) in Portugal: a first genetic analysis // Parasit. Vectors. 2024; 17(1): 389. DOI: 10.1186/s13071-024-06460-w.

4. Yu.Yu. Dgebuadze, V.G. Petrosyan, L.A. Khlyap. M. The most dangerous invasive species of Russia (TOP-100) // KMK Scientific Press, 2018, 688 p. (in Russian)

5. World Health Organization. Dengue – Global situation, 2023; [Электронный ресурс]. URL: https: //www.who.int/emergencies/disease-outbreak-news/item/2023-DON498 (дата обращения 03.05.2025).

6. Fedorova М.V., Shvez O.G., Patraman I.V., Medyanik I. M., Otstavnova A. D., Lenshin S. V., Vyshemirskiy O. I. Invasive mosquito species оf the Black sea coast of the Caucasus: current ranges // Med. Parasitol. (Mosk). 2019; 1: 47-55. (in Russian) DOI: 10.33092/0025-8326mp2019.1.47-55.

7. Asgarian T.S., Vatandoost H., Hanafi-Bojd A.A., Nikpoor F. Worldwide status of insecticide resistance of Aedes aegypti and Ae. albopictus, vectors of arboviruses of Chikungunya, Dengue, Zika and Yellow Fever // J. Arthropod Borne Dis. 2023; 17(1): 1-27. DOI: 10.18502/jad.v17i1.13198.

8. Smith L.B., Sears C., Sun H., Mertz R.W., Kasai S., Scott J.G. CYP-mediated resistance and cross-resistance to pyrethroids and organophosphates in Aedes aegypti in the presence and absence of kdr// Pestic. Biochem. Physiol. 2019; 160: 119-126. DOI: 10.1016/j.pestbp.2019.07.011.

9. McGregor B.L., Connelly C.R. A Review of the Control of Aedes aegypti (Diptera: Culicidae) in the Continental United States // J. Med. Entomol. 2021; 58(1): 10-25. DOI: 10.1093/jme/tjaa157.

10. Barrera-Illanes A.N., Ledesma L., Alvarez-Costa A., Balsalobre A., Toloza C.J., Hernandez-Maiztegui A., Jait A., Sierra I., Micieli M.V., Manteca-Acosta M., Ons S. Monitoring of pyrethroid resistance in Aedes aegypti: first report of double and triple kdr mutations in Buenos Aires Province // Parasit. Vectors. 2024; 17(1): 458. DOI: 10.1186/s13071-024-06547-4.

11. Devillers J., David J.-P., Barrès B., Alout H., Lapied B., Chouin S., Dusfour I., Billault C., Mekki F., Attig I., Corbel V. Integrated plan of insecticide resistance surveillance in mosquito vectors in France // Insects. 2023; 14(5): 457. DOI: 10.3390/insects14050457.

12. Chen M., Du Y, Nomura Y., Zhorov B.S., Dong K. Chronology of sodium channel mutations associated with pyrethroid resistance in Aedes aegypti // Arch. Insect. Biochem. Physiol. 2020; 104 (2): e21686. DOI: 10.1002/arch.21686.

13. Moyes C.L., Vontas J., Martins A.J., Ng L.C., Koou S.Y., Dusfour I., Raghavendra K., Pinto J., Corbel V., David J.P., Weetman D. Correction: Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans // PLoS Negl. Trop. Dis. 2021; 15(1): e0009084. DOI: 10.1371/journal.pntd.0009084.

14. Chen M., Zhou X., Chen G., Xu Z., Qian J., Zhu G., Yan R. Glycine to valine substitution in the short intracellular linkers of domain II enhances I1011M-mediated sodium channel resistance to Type I pyrethroids, but not Type II pyrethroids // Pestic. Biochem. Physiol. 2024; 203: 105994. DOI: 10.1016/j.pestbp.2024.105994.

15. Eremina O.Yu., Lopatina Yu.V. Molecular genetic mechanisms of insecticide resistance in insects // Med. Parasitol. (Mosk). 2017; 4: 44-52 (in Russian).

16. Cha D.J., Lee S.H. Evolutionary origin and status of two insect acetylcholinesterases and their structural conservation and differentiation // Evol. Dev. 2015; 17(1): 109–119. DOI: 10.1111/ede.12111.

17. Gan S.J., Leong Y.Q., Bin Barhanuddin M.F.H., Wong S.T., Wong S.F., Mak J.W., Ahmad R.B. Dengue fever and insecticide resistance in Aedes mosquitoes in Southeast Asia: a review // Parasit Vectors. 2021; 14(1): 315. DOI: 10.1186/s13071-021-04785-4.

18. Taylor-Wells J., Brooke B.D., Bermudez I., Jones A.K. The neonicotinoid imidacloprid, and the pyrethroid deltamethrin, are antagonists of the insect Rdl GABA receptor // J. Neurochem. 2015; 135(4): 705-713. DOI: 10.1111/jnc.13290.

19. Wang Y., Wang X., Brown D.J., An M., Xue R.D., Liu N. Insecticide resistance: Status and potential mechanisms in Aedes aegypti // Pestic. Biochem. Physiol. 2023; 195: 105577. DOI: 10.1016/j.pestbp.2023.105577.

20. Vontas J., Katsavou E., Mavridis K. Cytochrome P450-based metabolic insecticide resistance in Anopheles and Aedes mosquito vectors: Muddying the waters // Pestic. Biochem. Physiol. 2020; 170: 104666. DOI: 10.1016/j.pestbp.2020.104666.

21. Rault L.C., Johnson E.J., O'Neal S.T., Chen R., McComic S.E., Swale D.R., Anderson T.D. Age- and sex-related ABC transporter expression in pyrethroid-susceptible and -resistant Aedes aegypti // Sci. Rep. 2019; 9(1): 19551. DOI: 10.1038/s41598-019-56134-2.

22. Arthropod Pesticide Resistance Database; [Электронный ресурс]. URL: https: //pesticideresistance.org (дата обращения 13.09.2025).

23. Ritchie S.A. Dengue vector bionomics: why Aedes aegypti is such a good vector. In: Gubler D.J., Ooi E.E., Kuno G., Vasudevan S., Farrar J., eds. Dengue and dengue hemorrhagic fever. 2-nd edition // Oxfordshire, United Kingdom: CAB International. 2014: 455–480. DOI: 10.1079/9781845939649.0455.

24. Facchinelli L., Badolo A., McCall P.J. Biology and Behaviour of Aedes aegypti in the Human Environment: Opportunities for Vector Control of Arbovirus Transmission // Viruses. 2023; 15(3): 636. DOI: 10.3390/v15030636.

25. Laporta G.Z., Potter A.M., Oliveira J.F.A., Bourke B.P., Pecor D.B., Linton Y.M. Global Distribution of Aedes aegypti and Aedes albopictus in a Climate Change Scenario of Regional Rivalry // Insects. 2023; 14(1): 49. DOI: 10.3390/insects14010049.

26. Shaikevich E.V., Patraman I.V., Bogacheva A.S., Rakova V.M., Zelya O.P., Ganushkina L.A. Invasive mosquito species Aedes albopictus and Ae. aegypti on the Black sea coast of the Caucasus: genetics (COI, ITS2), Wolbachia and Dirofilaria infections // Vavilov Journal of Genetics and Breeding. 2018; 22: 856-867. DOI: 10.18699/VJ18.397.

27. Fedorova M.V., Shvets O.G., Yunicheva Yu.V., Medyanik I.M., Ryabova T.E., Otstavnova A.D. Dissemination of Invasive Mosquito Species, Aedes (Stegomyia) aegypti (L., 1762) and Aedes (Stegomyia) albopictus (Skuse, 1895) in the South of Krasnodar Region, Russia // Problems of Particularly Dangerous Infections. 2018; 2: 101-105 (in Russian). DOI: 10.21055/0370-1069-2018-2-101-105.

28. Bega A.G., Moskaev А.V., Gordeev М.I. Ecology and distribution of invasive mosquito species Aedes albopictus (Skuse, 1895) in the south of European part of Russia // Rus. J. Biol. Invasions. 2021; 1: 27–37 (in Russian). DOI: 10.35885/1996-1499-2021-14-1-27-37.

29. Samal R.R., Panmei K., Lanbiliu P., Kumar S. Reversion of CYP450 monooxygenase-mediated acetamiprid larval resistance in dengue fever mosquito, Aedes aegypti L. Bull // Entomol. Res. 2022; 112(4): 557-566. DOI: 10.1017/S0007485321001140.

30. Khan M.A., Riaz M., Kamran M., Shad S. A. Unstable fipronil resistance associated with fitness costs in fipronil-selected Aedes aegypti L. Exp // Parasitol. 2023; 250: 108543. DOI: 10.1016/j.exppara.2023.108543.

31. Rodríguez M.M., Bisset J.A., Fernandez D. Levels of insecticide resistance and resistance mechanisms in Aedes aegypti from some Latin American countries // J. Am. Mosq. Control. Assoc. 2007; 23: 420–429. DOI: 10.2987/5588.1.

32. Auteri M., La Russa F., Blanda V., Torina A. Insecticide resistance associated with kdr mutations in Aedes albopictus: an update on world-wide evidences // Biomed. Res. Int. 2018; 2018: 1-10. DOI: 10.1155/2018/3098575.

33. Amelia-Yap Z.H., Chen C.D., Sofian-Azirun M., Low V.L. Pyrethroid resistance in the dengue vector Aedes aegypti in Southeast Asia: present situation and prospects for management // Parasit. Vectors. 2018; 11(1): 332. DOI: 10.1186/s13071-018-2899-0.

34. Francis S, Campbell T, McKenzie S., Wright D., Crawford J., Hamilton T., Huntley-Jones S., Spence S., Belemvire A., Alavi K., Torres Gutierrez C. Screening of insecticide resistance in Aedes aegypti populations collected from parishes in Eastern Jamaica // PLoS Negl. Trop. Dis. 2020; 14(7): e0008490. DOI: 10.1371/journal.pntd.0008490.

35. Hassan M.R., Azit N.A., Fadzil S.M., Ghani S.R.A., Ahmad N., Nawi A.M. Insecticide resistance of Dengue vectors in South East Asia: a systematic review // Afr. Health. Sci. 2021; 21(3): 1124-1140. DOI: 10.4314/ahs.v21i3.21.

36. Enayati A., Valadan R., Bagherzadeh M., Cheraghpour M., Nikookar S.H., Fazeli-Dinan M., Hosseini-Vasoukolaei N., Sahraei Rostami F., Shabani Kordshouli R., Raeisi A., Nikpour F., Mirolyaei A., Bagheri F., Sedaghat M.M., Zaim M., Weetman D., Hemigway J. Kdr genotyping and the first report of V410L and V1016I kdr mutations in voltage-gated sodium channel gene in Aedes aegypti (Diptera: Culicidae) from Iran // Parasit. Vectors. 2024; 17(1): 34. DOI: 10.1186/s13071-024-06123-w.

37. Endersby-Harshman N.M., Schmidt T.L., Hoffmann A.A. Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae) // J. Med. Entomol. 2024; 61(3): 630-643. DOI: 10.1093/jme/tjae005.

38. Das S., Saha A., Das P. Raha D., Saha D. Target-site mediated insecticide resistance in major mosquito (Diptera: Culicidae) vectors: A systematic review // As. Pacif. J. Trop. Med. 2024; 17(11): 481-490. DOI: 10.4103/apjtm.ap-jtm_946_23.

39. Rahman R.U., Souza B., Uddin I., Carrara L., Brito L.P., Costa M.M., Mahmood M.A., Khan S., Lima J.B.P., Martins A.J. Insecticide resistance and underlying targets-site and metabolic mechanisms in Aedes aegypti and Aedes albopictus from Lahore, Pakistan // Sci. Rep. 2021; 11(1): 4555. DOI: 10.1038/s41598-021-83465-w.

40. Saavedra-Rodriguez K., Campbell C.L., Lenhart A., Penilla P., Lozano-Fuentes S., Black W.C. 4th. Exome-wide association of deltamethrin resistance in Aedes aegypti from Mexico // Insect Mol. Biol. 2019; 28(5): 591-604. DOI: 10.1111/imb.12575.

41. El-Garj F.M.A., Avicor S.W., Wajidi M.F.F. Xenobiotic-induced expression of detoxification genes, CYP4H28v2 and CYP4H31v2 in the dengue mosquito Aedes aegypti // Trop. Biomed. 2016; 33(3): 409-419.

42. Fonseca-González I., Quiñones M.L., Lenhart A., Brogdon W.G. Insecticide resistance status of Aedes aegypti (L.) from Colombia // Pest Manag. Sci. 2011; 67(4): 430-437. DOI: 10.1002/ps.2081.

43. Muthusamy R., Shivakumar M.S. Susceptibility status of Aedes aegypti (L.) (Diptera: Culicidae) to temephos from three districts of Tamil Nadu, India // J. Vector Borne Dis. 2015; 52(2): 159-165. DOI: 10.4103/0972-9062.159502.

44. Al-Amin H.M., Gyawali N., Graham M., Alam M.S., Lenhart A., Hugo L.E., Rašić G., Beebe N.W., Devine G.J. Insecticide resistance compromises the control of Aedes aegypti in Bangladesh // Pest Manag. Sci. 2023; 79(8): 2846-2861. DOI: 10.1002/ps.7462.

45. Rubio-Palis Y., Dzuris N., Sandi C., Vizcaino-Cabarrus R.L., Corredor-Medina C., González J.A., Lenhart A.E. Insecticide resistance levels and associated mechanisms in three Aedes aegypti populations from Venezuela // Mem. Inst. Oswaldo Cruz. 2023; 118: e220210. DOI: 10.1590/0074-02760220210.

46. Chareonviriyaphap T., Bangs M.J., Suwonkerd W., Kongmee M., Corbel V., Ngoen-Klan R. Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand // Parasit. Vectors. 2013; 6: 280. DOI: 10.1186/1756-3305-6-280.

47. Smith B., Tyagi R., Kasai S., Id J.G.S. CYP-mediated permethrin resistance in Aedes aegypti and evidence for trans-regulation // PLoS Negl. Trop. Dis. 2018; 12(11): 1–13. DOI: 10.1371/journal.pntd.0006933.

48. Muja-Bajraktari N., Kadriaj P., Zhushi-Etemi F., Sherifi K., Alten B., Petrić D., Velo E., Schaffner F. The Asian tiger mosquito Aedes albopictus (Skuse) in Kosovo: First record // PLoS One. 2022; 17(3): e0264300. DOI: 10.1371/journal.pone.0264300.

49. Heukelbach J., Alencar C.H., Kelvin A.A., de Oliveira W.K., Pamplona de Góes Cavalcanti L. Zika virus outbreak in Brazil // J. Infect. in Develop. Count. 2016; 10(2): 116–120. DOI: 10/3855/jidc.8217.

50. Ganushkina L.A., Tanygina E.Yu., Bezzhonova O.V., Sergiev V.P. Detection of Aedes (Stegomyia) albopictus Skuse mosquitoes in the Russian Federation // Med. Parasitol. (Mosk). 2012; 1: 3-4 (in Russian).

51. Ermolova N.V., Lazarenko E.V., Artiushina Y.S. Tsapko N.V., Agapitov D.S., Gazieva A.Y., Volynkina A.S., Medianik I.M., Otstavnova A.D., Shvets O.G., Belyaeva A.I. Number and distribution of mosquitoes the Aedes (Stegomyia) albopictus (Skuse, 1895) in the territory of the Southern Federal District of the Russian Federation and the Republic of Abkhazia // Med. Parasitol. (Mosk). 2019; 4: 3-9. (in Russian). DOI: 10.33092/0025-8326mp2019.4.3-9.

52. Ermolova N.V., Artyushina YU.S., Lazarenko E.V. Findings of mosquitoes Aedes (Stegomyia) albopictus (Skuse, 1895) in the Krasnodar and Stavropol regions of the Russian Federation. Lengesova N. A., ed. Current Biodiversity Issues: Proceedings of the II All-Russian Scientific and Practical Conference with International Participation (Ulyanovsk, March 27, 2024). Cheboksary: Publishing House «Sreda», 2024: 67–70. (in Russian).

53. Kovalenko I.S., Yakunin S.N., Abibulaev D.E., Vladychak V.V., Boroday N.V., Smelyansky V.P., Fomina V.K., Zinich L.S., Tikhonov S.N. Reporting of Aedes (Stegomyia) albopictus (Skuse, 1895) in the Territory of Crimea // Problems of Particularly Dangerous Infections. 2020; 2: 135–137. (In Russian). DOI: 10.21055/0370-1069-2020-2-135-137.

54. Martynov V.V., Nikulina T.V. New Records of Asian Tiger Mosquito Aedes (Stegomyia) albopictus (Skuse, 1895) (Diptera: Culicidae) in Crimea // Field Biologist Journal, 2024. 6(3): 273–279 (in Russian). DOI: 10.52575/2712-9047-2024-6-3-273-279.

55. Gao J.P., Chen H.M., Shi H., Peng H., Ma Y.J. Correlation between adult pyrethroid resistance and knockdown resistance (kdr) mutations in Aedes albopictus (Diptera: Culicidae) field populations in China // Infect. Dis. Poverty. 2018; 7(1): 86. DOI: 10.1186/s40249-018-0471-y.

56. Kasai S., Caputo B., Tsunoda T., Cuong T.C., Maekawa Y., Lam-Phua S.G., Pichler V., Itokawa K., Murota K., Komagata O., Yoshida C., Chung H.H., Bellini R., Tsuda Y., Teng H.J., Filho J.L.L., Alves L.C., Ng L.C., Minakawa N., Yen N.T., Phong T.V., Sawabe K., Tomita T. First detection of a Vssc allele V1016G conferring a high level of insecticide resistance in Aedes albopictus collected from Europe (Italy) and Asia (Vietnam), 2016: a new emerging threat to controlling arboviral diseases // Euro Surveill. 2019; 24(5): 1700847. DOI: 10.2807/1560-7917.ES.2019.24.5.1700847.

57. Yan R., Zhou Q., Xu Z., Zhu G., Dong K., Zhorov B.S., Chen M. Three sodium channel mutations from Aedes albopictus confer resistance to Type I, but not Type II pyrethroids // Insect Biochem. Mol. Biol. 2020; 123: 103411. DOI: 10.1016/j.ibmb.2020.103411.

58. Guo X., Zhou S., Wu J., Zhang X., Wang Y., Li Z., Chen X.G., Zhou X. An experimental evaluation of toxicity effects of sodium chloride on oviposition, hatching and larval development of Aedes albopictus // Pathogens. 2022; 11(2): 262. DOI: 10.3390/pathogens11020262.

59. Zhang Y., Wang D., Shi W., Zhou J., Xiang Y., Guan Y., Kong X., Liang W., Hu Y. Resistance to pyrethroids and the relationship between adult resistance and knockdown resistance (kdr) mutations in Aedes albopictus in dengue surveillance areas of Guizhou Province, China // Sci. Rep. 2024; 14(1): 12216. DOI: 10.1038/s41598-024-63138-0.

60. Ishak I.H., Jaal Z., Ranson H., Wondji C.S. Contrasting patterns of insecticide resistance and knockdown resistance (kdr) in the dengue vectors Aedes aegypti and Aedes albopictus from Malaysia // Parasit. Vectors. 2015; 8: 181. DOI: 10.1186/s13071-015-0797-2.

61. Yougang A.P., Kamgang B., Tedjou A.N., Wilson-Bahun T.A., Njiokou F., Wondji C.S. Nationwide profiling of insecticide resistance in Aedes albopictus (Diptera: Culicidae) in Cameroon // PLoS One. 2020; 15(6): e0234572. DOI: 10.1371/journal.pone.0234572.

62. Zulfa R., Lo W.C., Cheng P.C., Martini M., Chuang T.W. Updating the insecticide resistance status of Aedes aegypti and Aedes albopictus in Asia: A systematic review and meta-analysis // Trop. Med. Infect. Dis. 2022; 7(10): 306. DOI: 10.3390/tropicalmed7100306.

63. Lopatina Yu.V., Ushakova E.V., Sycheva K.A., Fyodorova М.V. Susceptibility to cypermethrin of aedes (stegomyia) albopictus (Skuse) mosquitoes in southern Russia. VII Congress of the Parasitological Society: Outcomes and Current Issues, October 16–20, 2023, Petrozavodsk, Russia: Proceedings: Scientific Electronic Edition. Petrozavodsk: Karelian Research Centre, Russian Academy of Sciences, 2023: 203–204. (In Russian).

64. Gutsevich A.V., Monchadski A.S., Shtakelberg A.A. Diptera insects. V. III, Iss. 4. Mosquitoes: family Culicidae (Fauna of the U.S.S.R. New series. No. 100). L.: Nauka, 1970. 384 p. (in Russian).

65. Bezzhonova O.V., Patraman I.V., Ganushkina L.A., Vyshemirskiy O.I., Sergiev V.P. The first finding of invasive species Aedes (Finlaya) koreicus (Edwards, 1917) in the European of Russia // Med. Parasitol. (Mosk). 2014; 1: 16–19 (in Russian).

66. Kovalenko I.S., Tikhonov S.N. Recording of Aedes koreicus (Edwards, 1917) (Diptera, Culicidae) in the territory of Crimea // Parasitology.2019; 53(2): 129-135 (in Russian). DOI: 10.1134/S0031184719020042.

67. Stoops C.A., Kim M.S., Mahabir S., Chong S.T., Cinkovich S.S., Carder J.B. CDC Bottle Bio-assays for detection of insecticide resistance in Culex pipiens, Aedes albopictus, and Aedes koreicus collected on US Army Garrisons, Republic of Korea // J. Am. Mosq. Control. Assoc. 2023; 39(3): 208-211. DOI: 10.2987/23-7119.

68. Miranda L.S., Rudd S.R., Mena O., Hudspeth P.E., Barboza-Corona J.E., Park H.W., Bideshi D.K. The perpetual vector mosquito threat and its eco-friendly nemeses // Biology (Basel). 2024; 13(3): 182. DOI: 10.3390/biology13030182.