Skip to main content
SpringerLink
Log in

Laboratory development of permethrin resistance and cross-resistance pattern of Culex quinquefasciatus to other insecticides

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Resistance of mosquitoes to insecticides is a growing concern in India. Since only a few insecticides are used for public health and limited development of new molecules is expected in the next decade, maintaining the efficacy of control programs mostly relies on resistance management strategies. Developing such strategies requires a deep understanding of factors influencing resistance together with characterizing the mechanisms involved. Among factors likely to influence insecticide resistance in mosquitoes, agriculture and urbanization have been implicated but rarely studied in detail. In the present study, we evaluate the permethrin resistance and cross-resistance pattern of several insecticides in Culex quinquefasciatus mosquitoes. After 10 generation of selection with permethrin, the LC50 value for both larvae and adult Cx. quinquefasciatus was increased by 17.3- and 17.1-folds compared with susceptible strain. Detoxification enzyme profiles and native PAGE electrophoresis of esterase isoenzyme further revealed that esterase and CytP450 may be involved in permethrin resistance (PerRes) strain compared with susceptible strain. In addition to cross-resistance, study revealed that high resistance to cypermethrin (RR = 6.3, 8.8-folds). This study provided important information for understanding permethrin resistance and facilitating a better strategy for the management of resistance. These studies conclude that a strong foundation for further study of permethrin resistance mechanisms observed in Cx. quinquefasciatus mosquitoes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anspaugh DD, Rose LR, Koehler PG, Hodgson E, Roe RM (1994) Multiple mechanism of pyrethroid resistance in the German cockroach, Blattella germanica (L.). Pestic Biochem Physiol 50:138–148

    Article  Google Scholar 

  • Brogdon WG (1989) Biochemical resistance detection: an alternative to bioassay. Parasitol Today 5:56–60

    Article  CAS  PubMed  Google Scholar 

  • CDC (2004) Evaluating mosquitoes for insecticide resistance-web based instruction. Centre for infectious disease, centre for disease control and prevention, (Accessed Oct 2004). www.cdc.gov/ncidod/wbt/resistance/toc.htm (2004)

  • Cheng Guilin LY, Yanchou J (1995) Cross resistant patterns of insecticide-selected strains of cotton bollworm Helicoverpa armigera (Hübner). Res Pest Manag News 7:13–15

    Google Scholar 

  • Feyereisen R (2005) Insect cytochrome P450. In Comprehensive Molecular Insect Science Edited by: Gilbert, L.I., Iatrou, K., Gill, S., Elsevier, Oxford pp. 1–77

  • Fonseca-González I, Cárdenas R, Quiñones ML, McAllister J, Brogdon WG (2009) Pyrethroid and organophosphates resistance in Anopheles (N.) nuneztovari Gabaldón populations from malaria endemic areas in Colombia. Parasitol Res 105:1399–1409

    Article  PubMed  Google Scholar 

  • Grant DF, Dietze EC, Hammock BD (1991) Glutathione S-transferase isozyme in Aedes aegypti: purification, characterization, and isozyme specific regulation. Insect Biochem 4:511–523

    Google Scholar 

  • Gubler D, Jeffery JAL, Thi Yen N, Nam VS, Nghia LT, Hoffmann AA, Kay BH, Ryan PA (2009) Characterizing the Aedes aegypti Population in a Vietnamese Village in Preparation for a Wolbachia-Based Mosquito Control Strategy to Eliminate Dengue. PLoS Negl Trop Dis 3;11: e-552

  • Gunning RV, Easton CS, Balfe M, Ferris IG (1991) Pyrethroid resistance mechanisms in Australian Helicoverpa armigera. Pestic Sci 33:473–490

    Article  CAS  Google Scholar 

  • Hansen IA, Marcombe S, Mathieu RB, Pocquet N, Riaz MA, Poupardin R, Sélior S, Darriet F, Reynaud S, Yébakima (2012) Insecticide resistance in the dengue vector Aedes aegypti from Martinique: distribution, mechanisms and relations with environmental factors. PLoS One 7;2: e30989

  • Hardstone MC, Leichter CA, Scott JG (2009) Multiplicative interaction between the two major mechanisms of Permethrin resistance, kdr and cytochrome P450-monooxygenase detoxification, in mosquitoes. J Evol Biol 22:416–423

    Article  CAS  PubMed  Google Scholar 

  • Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34:653–665

    Article  CAS  PubMed  Google Scholar 

  • Hemingway J, Beaty BJ, Rowland M, Scott TW, Sharp BL (2006) The Innovative Vector Control Consortium: improved control of mosquito-borne diseases. Trends Parasitol 22;7: 308–312

  • Hu Z, Du Y, Nomura Y, Dong KA (2011) Sodium channel mutation identified in Aedes aegypti selectively reduces cockroach sodium channel sensitivity to type I, but not type II pyrethroids. Insect Biochem Mol Biol 41(1):9–13

    Article  PubMed Central  PubMed  Google Scholar 

  • Kao CH, Hung CF, Sun CN (1989) Parathion and methyl parathion resistance in diamondback moth (Lepidoptera: Plutellidae) larvae. J Econ Entomol 82:1299–1304

    Article  CAS  Google Scholar 

  • Kasai S, Shono T, Komagata O, Tsuda Y, Kobayashi M, Motoki M, Kashima I, Tanikawa T, Yoshida M, Tanaka I, Shinjo G, Hashimoto T, Ishikawa T, Takahashi T, Higa Y, Tomita T (2007) Insecticide resistance in potential vector mosquitoes for West Nile virus in Japan. J. Med. Entomol 44; 5: 822– 829

  • Koelle K, Gambhir M, Michael E (2008) Complex Ecological Dynamics and Eradicability of the Vector Borne Macroparasitic Disease, Lymphatic Filariasis. PLoS One 3;8: e-2874

  • Kranthi KR (2005) Insecticide resistance monitoring, mechanisms and management manual. Central Institute for Cotton Research. India pp. 78–82

  • Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folins phenol reagent. J Bio Chem 193:265–275

    CAS  Google Scholar 

  • Mebrahtu YB, Norem J, Taylor M (1997) Inheritance of larval resistance to permethrin in Aedes aegypti and association with sex ratio distortion and life history variation. Am J Trop Med Hyg 56:456–465

    CAS  PubMed  Google Scholar 

  • Miller TA (1998) Mechanisms of resistance to pyrethroid insecticides. Parasitol. Today 4; 7: s3–s7

  • Molyneux DH, Malecela MN (2011) Neglected tropical diseases and the millennium development goals: why the “other diseases” matter: reality versus rhetoric. Parasit Vect 4:234

    Article  Google Scholar 

  • Muthusamy R, Shivakumar MS (2014) Resistance selection and molecular mechanisms of cypermethrin resistance in red hairy caterpillar (Amsacta albistriga Walker). Pestic. Biochem. Physiol In Press

  • Muthusamy R, Shivakumar MS (2015) Effect of lambda cyhalothrin and temephos on detoxification enzyme systems in Cx. quinquefasciatus (Diptera: Culicidae). J Env Biol 36:235–239

    CAS  Google Scholar 

  • Muthusamy R, Suganya R, Gowri M, Shivakumar M (2013) Biochemical mechanisms of organophosphate and pyrethroid resistance in red hairy caterpillar Amsacta albistriga (Lepidoptera: Arctiidae). J Saudi Society of Agric Sci 12:47–52

    Google Scholar 

  • Nardini L, Christian RN, Coetzer N, Ranson H, Coetzee M, Koekemoer L.L (2012) Detoxification enzymes associated with insecticide resistance in laboratory strains of Anopheles arabiensis of different geographic origin. Parasit. Vect 5; 1: 113

  • Nazni WA, Kamaludin MY, Lee HL, Rogayah T, Sa’diyah I (2000) Oxidase activity in relation to insecticide resistance in vectors of public health importance. Trop Biomed 17:69–79

    Google Scholar 

  • Paeporn P, Supaphathom K, Srisawat R, Komalamisra N, Deesin V, Ya umphan P, Leeming Sawat S (2004) Biochemical detection of pyrethroid resistance mechanism in Aedes aegypti in Ratchaburi province. Thailand. Trop. Med 21; 2:145–151

  • Peng R, Maklokova VI, Chandrashekhar JH, Lan Q (2011). In vivo functional genomics studies of sterol carrier protein-2 gene in the yellow fever mosquito. PLoS One. 6; 3: e-18030

  • Powers AM, Soumahoro MK, Boelle PY, Gaüzere BA, Atsou K, Pelat C, Lambert B, La Ruche G, Gastellu-Etchegorry M, Renault P (2011) The Chikungunya Epidemic on La Réunion Island in 2005–2006: a cost-of-illness study. PLoS Negl. Trop. Dis 5; 6: e1197

  • Ramkumar G, Karthi S, Muthusamy R, Natarajan D, Shivakumar MS (2015) Adulticidal and smoke toxicity of Cipadessa baccifera (Roth) plant extracts against Anopheles stephensi, Aedes aegypti, and Culex quinquefasciatus. Parasitol Res 114:167–173

    Article  PubMed  Google Scholar 

  • Recep A, Sibel Y (2012) Inheritance and detoxification enzyme levels in Tetranychus urticae Koch (Acari: Tetranychidae) strain selected with chlorpyrifos. J Pest Sci 83:85–93

    Google Scholar 

  • Rodríguez MM, Bisset JA, Fernandez DM, Soca A (2000) Malathion resistance in Aedes aegypti and Culex quinquefasciatus after its use in Aedes aegypti control programs. J. Am. Mosq. Control Assoc 16; 4: 324–330

  • Rodríguez MM, Bisset JA, Fernandez DM (2007) Levels of insecticide resistance and resistance mechanisms in Aedes aegypti from some Latin American countries. J. Am. Mosq. Control Assoc 23; 4: 510–519

  • Sahgal AS, Kumar MKK (1994) Microplate assay of elevated esterase activity in individual pyrethroid-resistant mosquitoes. J Biosci 19:193–199

    Article  CAS  Google Scholar 

  • Scott JG, Liu N, Wen Z (1998) Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comp Biochem Physiol C 121:147–155

    CAS  PubMed  Google Scholar 

  • Shankarganesh K, Walia S, Dhingra S, Subrahmanyam B, Ramesh Babu S (2012) Effect of dihydrodillapiole on pyrethroid resistance associated esterase inhibition in an Indian strain of Spodoptera litura (Fabricius), Pestic. Biochem Physiol 102:86–90

    CAS  Google Scholar 

  • Somwang P, Yanola J, Suwan W, Walton C, Lumjuan N, Prapanthadara L (2011) Somboon L (2011) Enzymes-based resistant mechanism in pyrethroid resistant and susceptible Aedes aegypti strains from northern Thailand. Parasitol Res 109:531–537

    Article  PubMed  Google Scholar 

  • Strode C, Wondji CS, David JP, Hawkes NJ, Lumjuan N, Parakrama NDR, Karunaratne SHP, Hemingway J, Black WC IV, Ranson H (2008) Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem Mol Biol 38:113–123

    Article  CAS  PubMed  Google Scholar 

  • Styer LM, Lim PY, Louie KL, Albright RG, Kramer LD, Bernard KA (2010) Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol 854:1517–1527

    Google Scholar 

  • Swain V, Seth RK, Mohanty SS, Raghavendra K (2008) Effect of temperature on development, eclosion, longevity and survivorship of malathion-resistant and malathion-susceptible strain of Culex quinquefasciatus. Parasitol Res 103:299–303

    Article  CAS  PubMed  Google Scholar 

  • Swain V, Seth RK, Raghavendra K, Mohanty SS (2009) Characterization of biochemical based insecticide resistance mechanism by thermal bioassay and the variation of esterase activity in Culex quinquefasciatus. Parasitol Res 104:1307–1313

    Article  CAS  PubMed  Google Scholar 

  • Tan W, Wang X, Quan X, Gao H (2012) Cloning and overexpression of transferring gene from cypermethrin-resistant Culex pipiens pallens. Parasitol Res 110:939–959

    Article  PubMed  Google Scholar 

  • Tikar N, Arkaja Kumar GBK, Prasad S (2009) Temephos-induced resistance in Aedes aegypti and its cross-resistance studies to certain insecticides from India. Parasitol Res 105:57–63

    Article  CAS  PubMed  Google Scholar 

  • Urmila J, Vijayan VA (2009) Biochemical characterization of deltamethrin resistance in a laboratory-selected strain of Aedes aegypti. Parasitol Res 104:1431–1438

    Article  Google Scholar 

  • White MT, Griffin JT, Churcher TS, Ferguson NM, Basáñez MG, Ghani AC (2011) Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vect 4:153

    Article  Google Scholar 

  • World Health Organization (1981) Instructions for determining the susceptibility or resistance of adult mosquitoes to organochlorine, organophosphate and carbamate insecticides, WHO/VBC/81.805, World Health Organization, Geneva

  • World Health Organization (2006) Pesticides and their application for the control of vectors and pests of public health importance, WHO/CDS/NTD/WHOPES/ GCDPP/2006

  • Xu Y, Yang M, Sun J, Qian J, Zhang D, Sun Y, Ma L, Zhu C (2008) Glycogen branching enzyme: a novel deltamethrin resistance-associated gene from Culex pipiens pallens. Parasitol Res 103; 2: 449–458

Download references

Acknowledgments

Infrastructural support provided by Department of Biotechnology, Periyar University, Salem, Tamil nadu, India is greatly acknowledged.

Author information

Authors and Affiliations

  1. Molecular Entomology Laboratory, Department of Biotechnology, Periyar University, Salem, Tamil Nadu, India

    Govindaraju Ramkumar & Muthugoundar S. Shivakumar

Authors
  1. Govindaraju Ramkumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muthugoundar S. Shivakumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muthugoundar S. Shivakumar.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramkumar, G., Shivakumar, M.S. Laboratory development of permethrin resistance and cross-resistance pattern of Culex quinquefasciatus to other insecticides. Parasitol Res 114, 2553–2560 (2015). https://doi.org/10.1007/s00436-015-4459-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4459-2

Keywords

Search

Navigation