The susceptibility of Aedes aegypti populations displaying temephos resistance to Bacillus thuringiensis israelensis: A basis for management

Parasites and Vectors

Volumn 6, Issue 1, 2013, Pages

  Araújo, Ana Paula ^a   Araujo Diniz, Diego Felipe ^a   Helvecio, Elisama ^a   De Barros, Rosineide Arruda ^a   De Oliveira, Cláudia Maria Fontes ^a   Ayres, Constância Flávia Junqueira ^a   De Melo Santos, Maria Alice Varjal ^a   Regis, Lêda Narcisa ^a   Silva Filha, Maria Helena Neves Lobo ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Bti; Cross resistance; Metabolic resistance; Susceptibility; Temephos; Vector control

Indexed keywords

ESTERASE; GLUTATHIONE TRANSFERASE; LARVICIDAL AGENT; MIXED FUNCTION OXIDASE; TEMEFOS;

AEDES AEGYPTI; ARTICLE; BACILLUS THURINGIENSIS; BIOASSAY; BRAZIL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DETOXIFICATION; DRUG RESISTANCE; DRUG SENSITIVITY; FEMALE; LC 50; NONHUMAN;

AEDES; ANIMALS; BACILLUS THURINGIENSIS; INSECT VECTORS; INSECTICIDE RESISTANCE; INSECTICIDES; PEST CONTROL, BIOLOGICAL; SURVIVAL ANALYSIS; TEMEFOS;

EID: 84886291958     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-6-297     Document Type: Article

References (64)

1. The global distribution and burden of dengue. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI, Nature 2013 496 504 507 10.1038/nature12060 23563266
2. Dengue: a continuing global threat. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martinez E, Nathan MB, Pelegrino JL, Simmons C, Yoksan S, Peeling RW, Nature Rev Microbiol 2010 8 7 S16 10.1038/nrmicro2460
3. Diagnosis and management of dengue. Teixeira MG, Barreto ML, BMJ 2009 339 4338 10.1136/bmj.b4338 19923152
4. Aedes aegypti: history of control in Brazil. Braga IA, Valle D, Epidemiol Serv Saúde 2007 16 113 118
5. Insecticide resistance and vector control. Brogdon WG, McAllister JC, Emerg Infect Dis 1998 4 605 613 10.3201/eid0404.980410 9866736 (Pubitemid 28553684)
6. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Casida JE, Durkin KA, Annu Rev Entomol 2013 58 99 117 10.1146/annurev-ento-120811-153645 23317040
7. The molecular basis of insecticide resistance in mosquitoes. Hemingway J, Hawkes NJ, McCarroll L, Ranson H, Insect Biochem Mol Biol 2004 34 653 665 10.1016/j.ibmb.2004.03.018 15242706 (Pubitemid 38893137)
8. Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control. Lacey LA, J Am Mosq Control Assoc 2007 23 133 163 10.2987/8756-971X(2007)23[133:BTSIAB]2.0.CO;2 17853604 (Pubitemid 47287502)
9. Microbial control of mosquitoes: management of the Upper Rhine mosquito population as a model programme. Becker N, Parasitol Today 1997 13 485 487 10.1016/S0169-4758(97)01154-X 15275138 (Pubitemid 27512900)
10. Distribution of Bacillus thuringiensis subsp. israelensis in soil of a Swiss wetland reserve after 22 years of mosquito control. Guidi V, Patocchi N, Luthy P, Tonolla M, Appl Environ Microbiol 2011 77 3663 3668 10.1128/AEM.00132-11 21498758
11. Use of Bacillus thuringiensis for onchorcercosis control in West Africa. Guillet P, Kurtak DC, Phillipon B, Meyer R, Bacterial control of mosquitoes and black-flies Sutherland. New Brunswick: Rutgers University Press, Barjac H, 1990 187 201
12. Mode of action of mosquitocidal Bacillus thuringiensis toxins. Soberón M, Fernández LE, Pérez C, Gill SS, Bravo A, Toxicon 2007 49 597 600 10.1016/j.toxicon.2006.11.008 17145072 (Pubitemid 46442862)
13. Contribution of the individual components of the delta-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensis subs. israelensis. Crickmore N, Bone EJ, Wiliams JA, Ellar DJ, FEMS Microbiol Lett 1995 131 249 254
14. Multiple receptors as targets of Cry toxins in mosquitoes. Likitvivatanavong S, Chen J, Evans AM, Bravo A, Soberón M, Gill SS, J Agricult Food Chem 2011 59 2829 2838 10.1021/jf1036189
15. Binding of Bacillus thuringiensis subsp. israelensis Cry4Ba to Cyt1Aa has an important role in synergism. Cantón PE, Zanicthe Reyes EZ, De Ruiz Escudero I, Bravo A, Soberón M, Peptides 2011 32 595 600 10.1016/j.peptides.2010.06.005 20558220
16. Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Pérez C, Fernandez LE, Sun J, Folch JL, Gill SS, Soberón M, Bravo A, PNAS USA 2005 102 18303 18308 10.1073/pnas.0505494102 16339907 (Pubitemid 43011221)
17. Bacillus thuringiensis ssp. israelensis Cyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure. Pérez C, Muñoz-Garay C, Portugal LC, Sánchez J, Gill SS, Soberón M, Bravo A, Cell Microbiol 2007 9 2931 2937 10.1111/j.1462-5822. 2007.01007.x 17672866 (Pubitemid 350066576)
18. Influence of exposure to single versus multiple toxins of Bacillus thuringiensis subsp. israelensis on development of resistance in the mosquito Culex quinquefasciatus (Diptera: Culicidae). Georghiou GP, Wirth MC, Appl Environ Microbiol 1997 63 1095 1101 16535542
19. Laboratory selection to investigate the development of resistance to Bacillus thuringiensis var. israelensis H-14 in Culex quinquefasciatus Say (Diptera: Culicidae). Mittal P, Nat Acad Sci Lett India 2005 28 281 283 (Pubitemid 43944009)
20. Persistence of Bacillus thuringiensis israelensis (Bti) in the environment induces resistance to multiple Bti toxins in mosquitoes. Paris M, Tetreau G, Laurent F, Lelu M, Després L, David JP, Pest Manag Sci 2011 67 122 128 10.1002/ps.2046 21162152
21. Resistance development in mosquito larvae Culex pipiens to the bacterial agent Bacillus thuringiensis var. israelensis. Saleh MS, El-Meniawi FA, Kelada NL, Zahran HM, J Appl Entomol 2003 127 29 32 10.1046/j.1439-0418.2003.00703.x (Pubitemid 36251557)
22. Bacterial larvicides for vector control: mode of action of toxins and implications for resistance. Ferreira LM, Silva-Filha MHNL, Biocontrol Sci Technol 2013 23 1137 1168 10.1080/09583157.2013.822472
23. Mosquito resistance to bacterial larvicidal proteins. Wirth MC, The Open Toxicol J 2010 3 101 115
24. Aedes albopictus (Diptera: Culicidae) population size survey in the 2007 chikungunya outbreak area in Italy. I. Characterization of breeding sites and evaluation of sampling methodologies. Carrieri M, Angelini P, Venturelli C, Maccagnani B, Bellini R, J Med Entomol 2011 48 1214 1225 10.1603/ME10230 22238882
25. An entomological surveillance system based on open spatial information for participative dengue control. Regis L, Souza WV, Furtado AF, Fonseca CD, Silveira JC Jr, Ribeiro PJ Jr, Melo-Santos MA, Carvalho MS, Monteiro AM, An Acad Bras Cienc 2009 81 655 662 10.1590/S0001-37652009000400004 19893891
26. Sustained reduction of the dengue vector population resulting from an integrated control strategy applied in two brazilian cities. Regis LN, Acioli RV, Silveira JC Jr, Melo-Santos MA, Souza WV, Ribeiro CM, Da Silva JC, Monteiro AM, Oliveira CM, Barbosa RM, Braga C, Rodrigues MA, Silva MG, Ribeiro PJ Jr, Bonat WH, de Castro Medeiros LC, Carvalho MS, Furtado AF, Da Silva JC, Monteiro AM, Oliveira CM, Barbosa RM, Braga C, Rodrigues MA, Silva MG, Ribeiro PJ Jr, Bonat WH, de Castro Medeiros LC, Carvalho MS, Furtado AF, PLoS One 2013 8 67682 10.1371/journal.pone.0067682
27. Resistance of Aedes aegypti (L.) (Diptera: Culicidae) populations to organophosphates temephos in the Paraiba State, Brazil. Beserra EB, Fernandes CR, de Queiroga F, de Castro FPJ, Neotrop Entomol 2007 36 303 307 17607466 (Pubitemid 47041436)
28. Aedes aegypti resistance to temephos during 2001 in several municipalities in the states of Rio de Janeiro, Sergipe, and Alagoas, Brazil. Braga IA, Lima JB, Soares Sda S, Valle D, Mem Inst Oswaldo Cruz 2004 99 199 203 15250476 (Pubitemid 38703211)
29. Insecticide resistance in Aedes aegypti populations from Ceara, Brazil. Lima EP, Paiva MH, De Araujo AP, Da Silva EV, Da Silva UM, De Oliveira LN, Santana AE, Barbosa CN, De Paiva Neto CC, Goulart MO, Wilding CS, Ayres CF, De Melo Santos MA, Parasit Vectors 2011 4 5 10.1186/1756-3305-4-5 21226942
30. Resistance of Aedes aegypti to organophosphates in several municipalities in the State of Rio de Janeiro and Espirito Santo, Brazil. Lima JB, Da-Cunha MP, Da Silva RC, Galardo AK, Soares Sda S, Braga IA, Ramos RP, Valle D, Am J Trop Med Hyg 2003 68 329 333 12685640 (Pubitemid 38240523)
31. Association of insecticide use and alteration on Aedes aegypti susceptibility status. Macoris ML, Andrighetti MT, Otrera VC, Carvalho LR, Caldas Junior AL, Brogdon WG, Mem Inst Oswaldo Cruz 2007 102 895 900 10.1590/S0074-02762007000800001 18209926
32. Resistance of Aedes aegypti populations from the State of São Paulo, Brazil, to organophosphates insecticides. Macoris MLG, Andrighetti MT, Takaku L, Glasser CN, Garbeloto VC, Bracco JE, Mem Inst Oswaldo Cruz 2003 93 703 708 (Pubitemid 38019596)
33. Insecticide resistance mechanisms of Brazilian Aedes aegypti populations from 2001 to 2004. Montella IR, Martins AJ, Viana-Medeiros PF, Lima JB, Braga IA, Valle D, Am J Trop Med Hyg 2007 77 467 477 17827362 (Pubitemid 351844321)
34. Response of Aedes aegypti (Diptera: Culicidae) larvae to three xenobiotic exposures: larval tolerance and detoxifying enzyme activities. Boyer S, David JP, Rey D, Lemperiere G, Ravanel P, Environ Toxicol Chem 2006 25 470 476 10.1897/05-267R2.1 16519308 (Pubitemid 43134248)
35. Influence of insecticide Bacillus thuringiensis subs. israelensis treatments on resistance and enzyme activities in Aedes rusticus larvae (Diptera: Culicidae). Boyer S, Paris M, Jego S, Lemperiere G, Ravanel P, Biol Control 2012 62 75 81 10.1016/j.biocontrol.2012.02.001
36. Differential sensitivity to Bacillus thuringiensis var. israelensis and temephos in field mosquito populations of Ochlerotatus cataphylla (Diptera: Culicidae): toward resistance? Boyer S, Tilquin M, Ravanel P, Environ Toxicol Chem 2007 26 157 162 10.1897/06-205R.1 17269473 (Pubitemid 46174387)
37. Effect of pyriproxyfen in Aedes aegypti populations with different levels of suscetibility to the organophosphate temephos. Andrighetti MT, Cerone F, Rigueti M, Galvani KC, Macoris M, Dengue Bulletin 2008 32 187 198
38. Evidence of cross-resistance to a juvenile hormone analogue in some insecticide-resistant houseflies. Cerf DC, Georghiou GP, Nature 1972 239 401 402 10.1038/239401a0 12635304
39. Long lasting persistence of Bacillus thuringiensis serovar. israelensis larvicidal activity in Aedes aegypti (Diptera: Culicidae) breeding places is associated to bacteria recycling. Melo-Santos MA, Araújo AP, Rios EM, Regis L, Biol Control 2009 49 186 191 10.1016/j.biocontrol.2009.01.011
40. Resistance to the organophosphate temephos: mechanisms, evolution and reversion in an Aedes aegypti laboratory strain from Brazil. Melo-Santos MA, Varjal-Melo JJ, Araújo AP, Gomes TC, Paiva MH, Regis LN, Furtado AF, Magalhães T, Macoris ML, Andrighetti MT, Ayres CF, Acta Trop 2010 113 180 189 10.1016/j.actatropica.2009.10.015 19879849
41. Expression profile of genes during resistance reversal in a temephos selected strain of the dengue vector. Aedes aegypti. Strode C, de Melo-Santos M, Magalhaes T, Araujo A, Ayres C, PLoS One 2012 7 39439 10.1371/journal.pone. 0039439 22870187
42. Brasil, Rede nacional de monitoramento da resistência de Aedes aegypti a inseticidas (rede MoReNAa): metodologia de amostragem Brasília (Brazil): Secretaria de Vigilância em Sáude, Ministério da Saúde 2008
43. WHO, Instructions for determining the susceptibility or resistance of mosquito larvae to insecticides Geneva: World Health Organization 1981
44. Characterization of resistance to organophosphate, carbamate, and pyrethroid insecticides in field populations of Aedes aegypti from Venezuela. Mazzarri MB, Georghiou GP, J Am Mosq Control Assoc 1995 11 315 322 8551300
45. De Barjac H, Larget-Thiéry I, Characteristics of IPS82 as standard for biological assay of Bacillus thuringiensis H-14 preparations Geneve: World Health Organization 1984 Mimiographed document WHO/VCB/84.892
46. Brasil, Metodologia para quantificação de atividade de enzimas relacionadas com a resistência a inseticidas em Aedes aegypti. Secretaria de Vigilância em Sáude Brasília (Brazil): Ministério da Saúde 2006
47. Natural variations: a complicating factor in bioassays with chemical and microbial pesticides. Robertson JL, Preisler HK, Ng SS, Hinkle LA, Gelernter WD, J Econ Entomol 1995 88 1 10
48. Aedes aegypti resistance to temefos in counties of Ceara State. Lima EP, de Oliveira Filho AM, de Oliveira Lima JW, Ramos Junior AN, de Goes Cavalcanti LP, Pontes RJ, Rev Soc Bras Med Trop 2006 39 259 263 10.1590/S0037- 86822006000300006 16906249 (Pubitemid 44167084)
49. Susceptibility of Culex pipiens (Diptera: Culicidae) field populations in Cyprus to conventional organic insecticides, Bacillus thuringiensis subsp. israelensis, and methoprene. Vasquez MI, Violaris M, Hadjivassilis A, Wirth MC, J Med Entomol 2009 46 881 887 10.1603/033.046.0421 19645293
50. Baseline susceptibility to bacterial insecticides in populations of Culex pipiens complex (Diptera: Culicidae) from California and from the mediterranean island of Cyprus. Wirth MC, Ferrari JA, Georghiou GP, J Econ Entomol 2001 94 920 928 10.1603/0022-0493-94.4.920 11561853 (Pubitemid 33750081)
51. Insecticide resistance and cross-resistance in Alabama and Florida strains of Culex quinquefasciatus. Liu H, Cupp EW, Micher KM, Guo A, Liu N, J Med Entomol 2004 41 408 413 10.1603/0022-2585-41.3.408 15185942 (Pubitemid 38693191)
52. Susceptility of field populations of Anopheles sinensis (Diptera: Culicidae) to Bacillus thuringiensis subs. israelensis. Lin L, Jingye H, Changju Y, Hongyu Z, Biocontrol Sci Technol 2004 14 321 325 10.1080/ 09583150310001639187 (Pubitemid 38641616)
53. Insecticide suscetibility of the dengue vector Aedes aegypti (Diptera: Culicidae) in Makkah City, Saudi Arabia. Aziz AT, Dieng H, Hassan AA, Satho T, Miake F, Salmah MRC, AbuBakar S, Asian Pac J Trop Dis 2011 1 94 99
54. Investigation on possible resistance in Aedes vexans field populations after 10-year application of Bacillus thuringiensis israelensis. Becker N, Ludwig M, J Am Mosq Control Assoc 1993 9 221 224 8350079
55. Insecticide susceptibility of Aedes aegypti and Aedes albopictus in Central Africa. Kamgang B, Marcombe S, Chandre F, Nchoutpouen E, Nwane P, Etang J, Corbel V, Paupy C, Parasit Vectors 2011 4 79 10.1186/1756-3305-4-79 21575154
56. Susceptibility of laboratory and field-collected Aedes aegypti and Aedes albopictus to Bacillus thuringiensis israelensis H-14. Lee YW, Zairi J, J Am Mosq Control Assoc 2006 22 97 101 10.2987/8756-971X(2006)22[97:SOLAFA]2.0.CO;2 16646329
57. Insecticide resistance in Alabama and Florida mosquito strains of Aedes albopictus. Liu H, Cupp EW, Guo A, Liu N, J Med Entomol 2004 41 946 952 10.1603/0022-2585-41.5.946 15535626 (Pubitemid 39403941)
58. Susceptibility of field-collected Aedes aegypti (L.) (Diptera: Culicidae) to Bacillus thuringiensis israelensis and temephos. Loke SR, Andy-Tan WA, Benjamin S, Lee HL, Sofian-Azirun M, Trop Biomed 2010 27 493 503 21399591
59. Insecticide resistance in Culex pipiens from New York. Paul A, Harrington LC, Zhang L, Scott JG, J Am Mosq Control Assoc 2005 21 305 309 10.2987/8756-971X(2005)21[305:IRICPF]2.0.CO;2 16252522 (Pubitemid 41445260)
60. The mitogen-activated protein kinase p38 is involved in insect defense against Cry toxins from Bacillus thuringiensis. Cancino-Rodezno A, Alexander C, Villasenor R, Pacheco S, Porta H, Pauchet Y, Soberon M, Gill SS, Bravo A, Insect Biochem Mol Biol 2010 40 58 63 10.1016/j.ibmb.2009.12.010 20040372
61. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Ferré J, Van Rie J, Annu Rev Entomol 2002 47 501 533 10.1146/annurev.ento.47.091201.145234 11729083 (Pubitemid 34108589)
62. Role of receptor interaction in the mode of action of insecticidal Cry and Cyt toxins produced by Bacillus thuringiensis. Gómez I, Pardo-López L, Muñoz-Garay C, Fernandez LE, Pérez C, Sánchez J, Soberón M, Bravo A, Peptides 2007 28 169 173 10.1016/j.peptides.2006.06.013 17145116 (Pubitemid 44959190)
63. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Gunning RV, Dang HT, Kemp FC, Nicholson IC, Moores GD, Appl Environ Microbiol 2005 71 2558 2563 10.1128/AEM.71.5.2558-2563.2005 15870346 (Pubitemid 40647001)
64. Heterologous expression and biochemical characterisation of fourteen esterases from Helicoverpa armigera. Teese MG, Farnsworth CA, Li Y, Coppin CW, Devonshire AL, Scott C, East P, Russell RJ, Oakeshott JG, PLoS One 2013 8 65951 10.1371/journal.pone.0065951 23799064