Skip to main content
Top
Published in: Malaria Journal 1/2008

Open Access 01-12-2008 | Research

Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka

Authors: M Devika B Perera, Janet Hemingway, SHP Parakrama Karunaratne

Published in: Malaria Journal | Issue 1/2008

Login to get access

Abstract

Background

The current status of insecticide resistance and the underlying resistance mechanisms were studied in the major vector of malaria, Anopheles culicifacies, and the secondary vector, Anopheles subpictus in five districts (Anuradhapura, Kurunegala, Moneragala, Puttalam and Trincomalee) of Sri Lanka. Eight other anophelines, Anopheles annularis, Anopheles barbirostris, Anopheles jamesii, Anopheles nigerrimus, Anopheles peditaeniatus, Anopheles tessellatus, Anopheles vagus and Anopheles varuna from Anuradhapura district were also tested.

Methods

Adult females were exposed to the WHO discriminating dosages of DDT, malathion, fenitrothion, propoxur, λ-cyhalothrin, cyfluthrin, cypermethrin, deltamethrin, permethrin and etofenprox. The presence of metabolic resistance by esterase, glutathione S-transferase (GST) and monooxygenase-based mechanisms, and the sensitivity of the acetylcholinesterase target site were assessed using synergists, and biochemical, and metabolic techniques.

Results

All the anopheline species had high DDT resistance. All An. culicifacies and An. subpictus populations were resistant to malathion, except An. culicifacies from Kurunegala, where there was no malathion carboxylesterase activity. Kurunegala and Puttalam populations of An. culicifacies were susceptible to fenitrothion. All the An. culicifacies populations were susceptible to carbamates. Both species were susceptible to the discriminating dosages of cypermethrin and cyfluthrin, but had different levels of resistance to other pyrethroids. Of the 8 other anophelines, only An. nigerrimus and An. peditaeniatus were resistant to all the insecticides tested, probably due to their high exposure to the insecticides used in agriculture. An. vagus showed some resistance to permethrin.
Esterases, GSTs and monooxygenases were elevated in both An. culicifacies and An. subpictus. AChE was most sensitive to insecticides in Kurunegala and Trincomalee An. culicifacies populations and highly insensitive in the Trincomalee An. subpictus population.

Conclusion

The complexity of the resistance segregating in these field populations underlines the need for new molecular tools to identify the genomic diversity, differential upregulation and different binding specificities of resistance conferring genes, and the presence of different subspecies with different vectorial capacities.
Appendix
Available only for authorised users
Literature
1.
go back to reference Wickramasinghe MB: Malaria and its control in Sri Lanka. Ceylon Med J. 1981, 26 (3): 107-115.PubMed Wickramasinghe MB: Malaria and its control in Sri Lanka. Ceylon Med J. 1981, 26 (3): 107-115.PubMed
2.
go back to reference Konradsen F, Amerasinghe FP, Hoek Van der W, Amerasinghe PH: Malaria in Sri Lanka; current knowledge on transmission and control. 2000, International Water management Institute, Colombo, Sri Lanka Konradsen F, Amerasinghe FP, Hoek Van der W, Amerasinghe PH: Malaria in Sri Lanka; current knowledge on transmission and control. 2000, International Water management Institute, Colombo, Sri Lanka
3.
go back to reference Carter CF, Jacocks WP: Observations on the transmission of malaria by Anopheline mosquitoes in Ceylon. Ceylon Journal of Science. 1929, 2: 67-86. Carter CF, Jacocks WP: Observations on the transmission of malaria by Anopheline mosquitoes in Ceylon. Ceylon Journal of Science. 1929, 2: 67-86.
4.
go back to reference Amerasinghe PH, Amerasinghe FP, Wirtz RA, Indrajith NG, Somapala W, Perera LR, Rathnayake AMS: Malaria transmission by Anopheles subpictus (Diptera: Culicidae) in a new irrigation project in Sri Lanka. J Med Entomol. 1992, 29: 577-581.CrossRefPubMed Amerasinghe PH, Amerasinghe FP, Wirtz RA, Indrajith NG, Somapala W, Perera LR, Rathnayake AMS: Malaria transmission by Anopheles subpictus (Diptera: Culicidae) in a new irrigation project in Sri Lanka. J Med Entomol. 1992, 29: 577-581.CrossRefPubMed
5.
go back to reference Amerasinghe PH, Amerasinghe FP, Konradsen F, Fonseka KT, Wirtz RA: Malaria vectors in a traditional dry zone village in Sri Lanka. Am J Trop Med Hyg. 1999, 60: 421-429.PubMed Amerasinghe PH, Amerasinghe FP, Konradsen F, Fonseka KT, Wirtz RA: Malaria vectors in a traditional dry zone village in Sri Lanka. Am J Trop Med Hyg. 1999, 60: 421-429.PubMed
6.
go back to reference Anti-Malaria Campaign: Malaria control programme of Sri Lanka: Five Year strategic plan 2005–2009. Colombo. 2005 Anti-Malaria Campaign: Malaria control programme of Sri Lanka: Five Year strategic plan 2005–2009. Colombo. 2005
7.
go back to reference Hemingway J, Hawkes NJ, McCarroll L, Ranson H: The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004, 34: 653-665.CrossRefPubMed Hemingway J, Hawkes NJ, McCarroll L, Ranson H: The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004, 34: 653-665.CrossRefPubMed
8.
go back to reference World Health Organization: Insecticide resistance and vector control. Technical Report Series, Geneva. 1963, 265: 41-47. World Health Organization: Insecticide resistance and vector control. Technical Report Series, Geneva. 1963, 265: 41-47.
9.
go back to reference World Health Organization: Instructions for determining the susceptibility or resistance of adult mosquitoes to organochlorine, organophosphate and carbamate insecticides-diagnostic test. WHO/VBC.81.806. World Health Organization: Instructions for determining the susceptibility or resistance of adult mosquitoes to organochlorine, organophosphate and carbamate insecticides-diagnostic test. WHO/VBC.81.806.
10.
go back to reference Karunaratne SHPP: Insecticide resistance spectra and underlying resistance mechanisms of Sri Lankan Anopheline vectors of malaria. Southeast Asian J Trop Med Public Health. 1999, 30: 460-469.PubMed Karunaratne SHPP: Insecticide resistance spectra and underlying resistance mechanisms of Sri Lankan Anopheline vectors of malaria. Southeast Asian J Trop Med Public Health. 1999, 30: 460-469.PubMed
11.
go back to reference Matsumara F: Toxicology of insecticides. Plenum Press, New York, 598- Matsumara F: Toxicology of insecticides. Plenum Press, New York, 598-
12.
go back to reference World Health Organization: Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. 1998, WHO, WHO/CDS/CPC/MAL/98.12 World Health Organization: Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. 1998, WHO, WHO/CDS/CPC/MAL/98.12
13.
go back to reference World Health Organization: Techniques to detect insecticide resistance mechanisms (field and laboratory manual). Geneva. 1998 World Health Organization: Techniques to detect insecticide resistance mechanisms (field and laboratory manual). Geneva. 1998
14.
go back to reference Hemingway J, Miyamoto J, Herath PRJ: A possible novel link between organophosphorus and DDT insecticide resistance gene in anopheles supporting evidence from fenitrothion metabolism studies. Pesticide Biochemistry and Physiology. 1991, 39: 49-56.CrossRef Hemingway J, Miyamoto J, Herath PRJ: A possible novel link between organophosphorus and DDT insecticide resistance gene in anopheles supporting evidence from fenitrothion metabolism studies. Pesticide Biochemistry and Physiology. 1991, 39: 49-56.CrossRef
15.
go back to reference Herath PRJ, Jayawardena KGJ: DDT resistance in Anopheles culicifacies Giles and A. subpictus grassi (Diptera: Culicidae) from Sri Lanka: a field study on the mechanisms and changes in gene frequency after on the mechanisms and changes in gene frequency after cessation of DDT spraying. Bull Entomol Res. 1988, 78: 717-723.CrossRef Herath PRJ, Jayawardena KGJ: DDT resistance in Anopheles culicifacies Giles and A. subpictus grassi (Diptera: Culicidae) from Sri Lanka: a field study on the mechanisms and changes in gene frequency after on the mechanisms and changes in gene frequency after cessation of DDT spraying. Bull Entomol Res. 1988, 78: 717-723.CrossRef
16.
go back to reference Herath PRJ, Hemingway J, Weerasinghe IS, Jayawardena KGI: The detection and characterization of malathion resistance in field populations of Anopheles culicifacies B in Sri Lanka. Pesticide Biochemistry and Physiology. 1987, 29: 157-162.CrossRef Herath PRJ, Hemingway J, Weerasinghe IS, Jayawardena KGI: The detection and characterization of malathion resistance in field populations of Anopheles culicifacies B in Sri Lanka. Pesticide Biochemistry and Physiology. 1987, 29: 157-162.CrossRef
17.
go back to reference Karunaratne SHPP, Hemingway J: Malathion resistance and prevalence of the malathion carboxylesterase mechanism in populations of Sri Lankan mosquito vectors of disease. Bull World Health Organ. 2001, 79: 1060-1064.PubMedCentralPubMed Karunaratne SHPP, Hemingway J: Malathion resistance and prevalence of the malathion carboxylesterase mechanism in populations of Sri Lankan mosquito vectors of disease. Bull World Health Organ. 2001, 79: 1060-1064.PubMedCentralPubMed
18.
go back to reference Campbell PM, Newcomb RD, Russel RJ, Oakeshott JG: Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol. 1998, 28: 139-50.CrossRef Campbell PM, Newcomb RD, Russel RJ, Oakeshott JG: Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol. 1998, 28: 139-50.CrossRef
19.
go back to reference Heidari R, Devonshire AL, Campbell BE, Bell KL, Dorrian SJ, Oakeshott JG, Russell RJ: Hydrolysis of organophosphorus insecticides by in vitro modified carboxylesterase E3 from Lucilia cuprina. Insect Biochem Mol Biol. 2004, 34: 353-363.CrossRefPubMed Heidari R, Devonshire AL, Campbell BE, Bell KL, Dorrian SJ, Oakeshott JG, Russell RJ: Hydrolysis of organophosphorus insecticides by in vitro modified carboxylesterase E3 from Lucilia cuprina. Insect Biochem Mol Biol. 2004, 34: 353-363.CrossRefPubMed
20.
go back to reference Herath PRJ, Joshi GP: Pesticide selection pressure on Anopheles subpictus in Sri Lanka: Comparison with two other Sri Lankan anophelines. Trans R Soc Trop Med Hyg. 1989, 83: 565-567.CrossRefPubMed Herath PRJ, Joshi GP: Pesticide selection pressure on Anopheles subpictus in Sri Lanka: Comparison with two other Sri Lankan anophelines. Trans R Soc Trop Med Hyg. 1989, 83: 565-567.CrossRefPubMed
21.
go back to reference Amerasinghe FP, Konradsen F, Fonseka KT, Amerasinghe PH: Anopheline (Diptera: Culicidae) breeding in a traditional tank-based village ecosystem in North Central Sri Lanka. J Med Entomol. 1997, 34 (3): 290-297.CrossRefPubMed Amerasinghe FP, Konradsen F, Fonseka KT, Amerasinghe PH: Anopheline (Diptera: Culicidae) breeding in a traditional tank-based village ecosystem in North Central Sri Lanka. J Med Entomol. 1997, 34 (3): 290-297.CrossRefPubMed
22.
go back to reference Feyereisen R: Insect cytochrome P450. Comprehensive Molecular Insect Science. Edited by: Gilbert LI, Latrou K, Gill SS. 2005, Oxford, UK: Elsevier, 4: 1-77.CrossRef Feyereisen R: Insect cytochrome P450. Comprehensive Molecular Insect Science. Edited by: Gilbert LI, Latrou K, Gill SS. 2005, Oxford, UK: Elsevier, 4: 1-77.CrossRef
23.
go back to reference Li X, Schuler MA, Berenbaum MR: Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2007, 52: 231-253.CrossRefPubMed Li X, Schuler MA, Berenbaum MR: Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2007, 52: 231-253.CrossRefPubMed
24.
go back to reference Karunaratne SHPP, Hawkes NJ, Perera MDB, Ranson H, Hemingway J: Mutated sodium channel genes and elevated monooxygenases are found in pyrethroid resistant populations of Sri Lankan malaria vectors. Pesticide Biochemistry and Physiology. 2007, 99: 108-113.CrossRef Karunaratne SHPP, Hawkes NJ, Perera MDB, Ranson H, Hemingway J: Mutated sodium channel genes and elevated monooxygenases are found in pyrethroid resistant populations of Sri Lankan malaria vectors. Pesticide Biochemistry and Physiology. 2007, 99: 108-113.CrossRef
25.
go back to reference Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D: Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae. s.s. Insect Mol Biol. 1988, 7 (2): 179-184.CrossRef Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D: Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae. s.s. Insect Mol Biol. 1988, 7 (2): 179-184.CrossRef
26.
go back to reference O'Reilly AO, Khambay BPS, Williamson MS, Field LM, Wallace BA, Davies TGE: Modelling insecticide binding sites in the voltage-gated sodium channel. Biochem J. 2006, 396: 255-263.PubMedCentralCrossRefPubMed O'Reilly AO, Khambay BPS, Williamson MS, Field LM, Wallace BA, Davies TGE: Modelling insecticide binding sites in the voltage-gated sodium channel. Biochem J. 2006, 396: 255-263.PubMedCentralCrossRefPubMed
27.
go back to reference Abhayawardana TA, Wijesuriya SR, Dilrukshi RK: Anopheles subpictus complex: distribution of sibling species in Sri Lanka. Indian J Malariol. 1996, 33: 53-60.PubMed Abhayawardana TA, Wijesuriya SR, Dilrukshi RK: Anopheles subpictus complex: distribution of sibling species in Sri Lanka. Indian J Malariol. 1996, 33: 53-60.PubMed
28.
go back to reference Kelly-Hope LA, Yapabandara AMGM, Wickramasinghe MB, Perera MDB, Karunaratne SHPP, Fernando WP, Abeysinghe RR, Siyambalagoda RRMLR, Herath PJR, galappaththy GNL, Hemingway J: Spatiotemporal distribution of insecticide resistance in Anopheles culicifacies and Anopheles subpictus in Sri Lanka. Trans R Soc Trop Med Hyg. 2005, 99: 751-761.CrossRefPubMed Kelly-Hope LA, Yapabandara AMGM, Wickramasinghe MB, Perera MDB, Karunaratne SHPP, Fernando WP, Abeysinghe RR, Siyambalagoda RRMLR, Herath PJR, galappaththy GNL, Hemingway J: Spatiotemporal distribution of insecticide resistance in Anopheles culicifacies and Anopheles subpictus in Sri Lanka. Trans R Soc Trop Med Hyg. 2005, 99: 751-761.CrossRefPubMed
29.
go back to reference Surendran SN, Ramasamy MS, De Silva BGDNK, Ramasamy R: Anopheles culicifacies sibling species B and E in Sri Lanka differ in longevity and in their susceptibility to malaria parasite infection and common insecticides. Med Vet Entomol. 2006, 20: 153-156.CrossRefPubMed Surendran SN, Ramasamy MS, De Silva BGDNK, Ramasamy R: Anopheles culicifacies sibling species B and E in Sri Lanka differ in longevity and in their susceptibility to malaria parasite infection and common insecticides. Med Vet Entomol. 2006, 20: 153-156.CrossRefPubMed
30.
go back to reference Herath PRJ: Insecticide resistance status in disease vectors and its practical implications. International Workshop on Insecticide Resistance of Mosquito Vectors, Salatiga, Indonesia. 1997 Herath PRJ: Insecticide resistance status in disease vectors and its practical implications. International Workshop on Insecticide Resistance of Mosquito Vectors, Salatiga, Indonesia. 1997
Metadata
Title
Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka
Authors
M Devika B Perera
Janet Hemingway
SHP Parakrama Karunaratne
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2008
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-7-168

Other articles of this Issue 1/2008

Malaria Journal 1/2008 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.