SciELO - Scientific Electronic Library Online

 
vol.22 issue1World strategies in salt/sodium reduction in bread author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • Have no similar articlesSimilars in SciELO

Share


Revista Costarricense de Salud Pública

Print version ISSN 1409-1429

Rev. costarric. salud pública vol.22 n.1 San José Jan./Jun. 2013

 

Review

Chemical control of Aedes aegypti: a historical perspective

Control Químico de Aedes aegypti: Una Perspectiva Histórica

Alejandra Manjarres-Suarez1*, Jesus Olivero-Verbel2*


Abstract

Objective: To describe the use of chemical insecticides throughout history as the main tool to fight against Aedes aegypti, a vector of dengue virus.

Methods: A text mining approach was conducted on databases, such as PUBMED and SCIENCE DIRECT, using the keywords “Aedes aegypti”, combined with the words “insecticides”, “resistance”, “organochlorines”, “organophosphates”, “carbamates” and “pyrethroids”. Results related to historical information dealing with the chemical control of Aedes aegypti, in particular those containing data on insecticide resistance for this species, were scrutinized and analyzed.

Results: Different chemical groups have been utilized to control A. aegypti, including organochlorine, organophosphate, carbamate and pyrethroid insecticides. In general, the tendency has been to replace a particular pesticide, for which resistance had been detected, for a new one, mosquito-sensitive, and with little evidence of deleterious effects derived from its use. The spread of resistance has been registered in several countries of America, Asia and Africa. Two mechanisms have been highly cited to be responsible for the resistance; the increase activity of detoxifying enzymes, and structural changes in the insecticide target site, mostly within the central nervous system.

Conclusion: Excessive use of chemical insecticides and the lack of dosing control have led to widespread resistance in A. aegypti, as no “safer” alternative chemical options are available for vector control in different countries, impacting human health

Keywords: Aedes, Vector control, Insecticide Resistance, Toxic Substances. (source: MeSH/NLM).

Resumen

Objetivo: Describir el uso de insecticidas químicos a través de la historia como la principal herramienta contra Aedes aegypti, un mosquito vector del virus del dengue.

Métodos: Una búsqueda en minería de textos fue realizada en bases de datos como PubMedy Science Direct, utilizando las palabras clave “Aedes aegypti”, en combinación con “insecticidas”, “resistencia”, “organoclorados”, “organofosforados”,“carbamatos” y “piretroides”.Resultados afines con la información histórica relacionada con el control químico del mosquito Aedes aegypti, en particular las que contienen datos sobre la resistencia a insecticidas de esta especie, fueron examinados y analizados.

Resultados: Diferentes grupos químicos han sido desarrollados para el control de A. aegypti, siendo los más utilizados organoclorados, organofosforados, carbamatos y piretroides. En general, la tendencia ha sido la de sustituir un pesticida particular, para el que ha sido detectado resistencia, por uno nuevo, mosquito-sensible, y con evidencia de efectos perjudiciales derivados de su uso. La propagación de la resistencia se ha registrado en varios países de América, Asia y África. Dos mecanismos han sido altamente referenciados de ser responsable de la resistencia, el aumento de actividad de las enzimas de desintoxicación, y los cambios estructurales en el sitio de destino de los insecticidas, en su mayoría dentro del sistema nervioso central.

Conclusión: El uso excesivo de insecticidas químicos y la falta de control de dosificación han dado lugar a una resistencia generalizada en Aedes aegypti, y alternativas químicas “más seguras” no están disponibles para el control de vectores en diferentes países, afectando la salud humana.

Palabras claves: Aedes, Control de vectores, Sustancias Tóxicas. (fuente:DeCS/BIREME).


Aedes aegypti (Diptera: Culicidae) is the mosquito responsible for the transmission of dengue in tropical and subtropical regions of the world (1, 2), including the South Pacific, Southeast Asia, India, Africa and the subtropical zone of America (3). This vector is distributed between 35° North and 35° South, but it may extend to 45° North to 40° South. Usually, it is found below 1200 m, although it has been reported around 2400 m (4). A. aegypti is native to Africa and it probably invaded other continents via transport ships that carried freshwater reservoirs on board, and resupplied in African ports during the fifteenth through seventeenth centuries, being introduced into the rest of the world following the same route (5). Breeding sites are essentially artificial: urban (vacant lots, salvage yards, landfills) or domestic (tires, bottles, open cans or containers of any kind, drinking water, tanks, pots and jars, among others) (4).

Over the last 25 years there has been a global increase in both the distribution of A. aegypti and the epidemic dengue virus activity (5). It has been estimated that worldwide, 2.5 billion people are at risk of acquiring the disease, approximately 50–100 million cases of dengue fever are reported each year, 500,000 people with severe dengue require hospitalization, and around 2.5% of diseased people die (6). The expansion of the mosquito populations may be explained by many factors, including demographic explosion, global warming, and the traffic of people between the infested communities and those previously vector free (7).

The control of Aedes populations is performed using several strategies, such as environmental management, chemical, biological and integrated control. The first is the most effective, preventing or reducing the breeding of mosquitoes and human-vector pathogen contact. Environmental management is focused on the destruction, alteration, disposal or recycling of containers, and natural larval habitats, that produce the greatestnumber of adult Aedesmosquitoes in each community. These activities are concurrently developed with health education programs, utilizing communication strategies that encourage community participation in the planning, execution, and evaluation of container–management programs. Three types of environmental management programs have been defined: first, environmental modification based on long lasting physical transformations of vector habitats; second, environmental manipulations, aimed to generate temporary changes to vector habitat, as a result of planned activity to produce unfavorable conditions to vector breeding; and third, changes in human habitat or behavior (8). However, the most widely used control for Aedes populations, due to its effectiveness in regulating larval and adult populations, is the utilization of chemical insecticides (9).

There are three methods of applying chemical control. Larvicide application or focal control, used to treat household drinking water containers, has low, relative toxicity, and is safe for humans. Another method is perifocal treatment, which utilizes sprinklers in larval habitats and destroys not only larvae but also adult mosquitoes. Finally, space spraying is generally employed in emergency outbreaks of dengue (8).

It is important to emphasize that larvicides should be considered as a complementary method to environmental management and those are intended to impact the mosquito density and longevity, as well as other transmission parameters. Another strategy is biological control, which introduces predators or parasites to compete or reduce the populations of the target species. Larvivorous fish and the biocide Bacillus thuriengensis H -14 (BTI) are the two most frequently employed organisms. According to McCall and Kittayapong (10), the pyriproxyfen, and insect growth regulator, has also been used for the control of the dengue vector. This method has been documented to only be effective in the immature stages of the vector mosquitoes (11). Finally, integrated control is the combination of the available control methods in the most effective, economical, and safe manner to decrease vector populations (8).

As chemical insecticides have been the most important tools employed for the management of dengue vector mosquito, the objective of this review was to describe those pesticides that have been used throughout history in the control of Aedes aegypti.

Methods

This paper consists of a thematic review that was done searching in databases such as PUBMED, SCIENCE DIRECT, books, and webpages of public health organizations from several countries, including as well theWorldHealthOrganizationandPanamericanHealth Organization. Keywords as “chemical insecticides”, “Aedes aegypti”, “resistance”, “organochlorines”, “organophosphates”, “carbamates” and “pyrethroids”, were employed to carry out the search. Aspects such as the history of chemical insecticide use, resistance development, resistance mechanisms, and effects of pesticides on human health, constituted the inclusion criteria to consider citations in the review.

Results

Evolution of mosquito control with chemical insecticides

Initially, insect control was carried out with natural products, but the development of chemical insecticides slowed down basic research on this issue (12).

Throughout history, four common classes of chemical insecticides have been used to control A. aegypti: organochlorines, organophosphates, carbamates and pyrethroids (13). Organochlorine pesticides are lipophilic compounds with low vapor pressures and slow degradation rates (14). These are known for their toxicity, persistence in the environment, and bioaccumulation in the food chain. This last property was one of the main reasons why these were replaced by organo phosphate espesticides, as they could be more asily degraded in the environment (15). Organochlorine insecticides were widely used between 1940s and mid 1960s, when they were discontinued due to their environmental effects (14). Organophosphates (OPs) are pesticides of low persistence in the environment, which are hydrolysed to high or low pH (16). These were developed during World War II as nerve gases, and their insecticidal properties were discovered shortly thereafter (17). The OPs have become widely used as replacements for organochlorine insecticides because they do not bioaccumulate in organism tissues or the environment (14). Carbamates are derivatives of the carbamic acid. These chemicals share the same mode of action with OPs, inhibiting the activity of acetylcholinesterase, although this effect can be more easily reversed, and the insects may recover at low doses (18). These last two types of insecticides have a broad spectrum of activity, rapid environmental degradation (19), relatively short biological half-lives, and are rapidly metabolized and excreted (14). The fourth group comprises pyrethroids, the most recently introduced insecticides (20), entering the marketplace in 1980 (21). They are considered safe due to their high insecticidal properties at low application rates, short persistence in the environment, no bioaccumulation and low mammalian toxicity (22), reasons supporting their extensive use (23).

Although there is abundant information regarding the chronological development of insecticides by chemical group, as shown in Table 1, in most cases, the records of the introduction and date of their use are not accurate. In general, each country has employed these chemicals based on its particular needs, in particular, according to the occurrence or reemergence of dengue outbreaks in a given time. The replacement of each pesticide for a new one depends on the resistance developed by the vector, and the criteria for effective insecticides considered relevant by authorities in each territory. Malathion, for example, has been one of the most frequently used. In Colombia, it has been utilized since 1980, and it is widely employed today (24). Mexico, however, suspended its use in 1999 (25). In Thailand, it was applied since 1950 but its arrest is not documented (26), and in Cuba it was abandoned with the introduction of pyrethroids (27). It is important to highlight that in some cases, pesticide use has been carried out combining different classes of insecticides, such as DDT with pyrethroids, although cross-resistance has been observed (28).

Reports of chemical insecticide use to control dengue virus vectors

During the last decades, the use of chemical insecticides has been an important component to control the populations of dengue vectors (9, 29).

Commercially available insecticides used in different countries are shown in Table 2. All these chemicals are not used simultaneously, but each country has employed specific insecticides throughout history, with peculiarities in both use and dosage form. A total of 40 countries from different continents recorded the use of insecticides for control of dengue during 20032005. The most widely used insecticides for vector control have been organophosphates and pyrethroids. In fact, a total of 262 tons of organophosphate (OP) insecticides and 39 tons of pyrethroids per year have been utilized (30).

Among OPs, in a global context, 76 % were utilized for space spraying, 23 % for larviciding, and 1 % for peri-focal spraying, interestingly, 90 % of the total was used in countries from the Americas. In the case of pyrethroids, 78 % was for space spraying, and the remaining percentage for peri-focal spraying. Pyrethroids were used for peri-focal spraying mainly in countries from the Americas, and a very small quantity in the Western Pacific. About 50% of the total global usage of pyrethroid insecticides took place in countries from the Western Pacific and about 47 % in the Americas. The amount of OPs and pyrethroids used for dengue vector control constituted 60 % and 24 %, respectively, of the total annual use of insecticides (30).

Worldwide, the control of A. aegypti is mostly performed with Ops; being malathion the most frequently utilized, constituting 67 % of the average annual use, followed by temephos (22 %) (30).This last has been the leading pesticide used as larvicide in Malaysia (31), Port Suan City (Red Sea State) (32), Thailand (33), Panama, El Salvador, Cuba, Martinique Island, French Guiana, Peru, Brazil, Argentina, Venezuela and Colombia (22, 24, 27, 34-41).

The main dengue vector control with pyrethroids has been performed with cypermethrin (37 %) and permethrin (45 %), followed by alpha-cypermethrin (14 %) (30). Other insecticides have also been critical for the control of A. aegypti, including fenthion, fenitrothion, chlorpyrifos, deltamethrin, cyhalothrin, cyfluthrin, propoxur, bendiocarb, dichloro diphenyl trichloroethane (DDT) and dieldrin (22, 24, 27, 34-41). According to WHO, during 2001, in terms of coverage, budget, human resources and amount of insecticide used, Brazil was the country with the most extensive program of control of A. aegypti. Reports from 2002 showed that in the Americas, vector control was mainly carried out with insecticides (42). In Colombia, for example, the main strategies conducted by local governments for vector control are aerial spraying of the insecticide, using thermal fogging or ultra-lowvolume spraying, in particular with organophosphates, such as malathion (96 %), fenitrothion (40 %), or the pyrethroid compound, deltamethrin. Currently, insecticide spraying in Colombia is recommended for outbreaks, or when cases of Dengue Haemorrhagic Fever are confirmed (24).

Resistance registered in Aedes aegypti

The continued use of insecticides has induced pressure on populations of A. aegypti, leading to widespread resistance (43). Two main mechanisms have been reported to be responsible (28): the first involves an increased activity of detoxifying enzymes, including esterases, mixed function oxidases (cytochrome P450s), and glutathione S-transferases (GSTs) (44); and the second deals with structural changes in the insecticide target site in the central nervous system (45).

The main insecticide targets are acetylcholinesterase, γ -aminobutyric acid (GABA) receptor and the voltage-gated sodium channel (46).

In LatinAmerica and the Caribbean, several A. aegypti populations have shown strong resistance to OPs, carbamates, and pyrethroids, existing correlations with elevated activities of at least one detoxification enzyme family. The resistance to OPs and carbamates is connected with acetylcholinesterase insensitivity (13, 46). In the case of temephos, for example, the resistance detected to this insecticide was related to the increased activity of esterases, specifically esterase A4 (9). In addition, several non-synonymous mutations in the gene encoding the trans-membrane voltage-gated sodium channel (kdr mutations) have been described to confer resistance to pyrethroids and DDT (22).

In countries such as Puerto Rico, Dominican Republic, Cuba, French Guiana, and Colombia, among others, have been recorded the resistance development of Aedes aegypti to insecticides such as temephos (9, 37, 38, 47-50) and pyrethroids (13, 37, 44, 51, 54), showing with these, the evolution of resistance registered worldwide.

Because resistance records, as well as the registered effects in the health of humans, such as immunosuppression; endocrinedisruption; reproductive abnormalities; irritant respiratory symptons; adverse genotoxic and neurological effects; and cancer (5560), control of Aedes populations is being conducted through more environmentally friendly alternatives, such the use of plant extracts, reducing adverse effects on non-target organisms (61).

Conclusions

The vector control for A. aegypti has been one of the main strategies against dengue virus transmission, but it is mostly based on chemical in secticides, which induce resistance in mosquitoes and also cause damage to humans and the environment. This resistance is probably due to the lack of regulation in use and in the dosage of each case. This review supports the need to generate mosquito control strategies that are environmentally friendly with minimal affectations on human populations.

Acknowledgements

The authors acknowledge the financial support of the University of Cartagena, Cartagena, Colombia, and Colciencias, Young Researchers Program, sponsoring Alejandra Manjarres. Technical support from Professor Joseph is highly appreciated.


References

1. Preet S, Sneha A. Biochemical evidence of efficacy of potash alum for the control of dengue vector Aedes aegypti (Linnaeus). Parasitol. Res. 2011; 108 (6):1533-1539.         [ Links ]

2. Morales RE, Ya-Umphan P, Phumala-Morales N, Komalamisra N, Dujardin JP. Climate associated size and shape changes in Aedes aegypti (Diptera: Culicidae) populations from Thailand. Infect. Genet. Evol. 2010; 10(4):580-585.         [ Links ]

3. Suh SJ, Seo YS, Ahn JH, Park EB, Lee SJ, Sohn JU, et al. A case of imported Dengue Fever with acute hepatitis. Korean J. Hepatol. 2007; 13(4):556-559.         [ Links ]

4. Organización Panamericana de la Salud. Sistematización de lecciones aprendidas en proyectos de comunicación para impactar en conductas (COMBI) en dengue en la Región de las Américas. Costa Rica: OPS/OMS. 2011. p. 20-21. Disponible en: guias_normas/lecciones_aprendidas_COMBI.pdf. Consultado en Abril de  2013. http://www.bvs.ins.gob.pe/insprint/SALUD_PUBLICA/DENGUE/.         [ Links ]

5. Jansen CC, Beebe NW. The dengue vector Aedes aegypti: what comes next. Microbes Infect. 2010; 12(4):272-279.         [ Links ]

6. World Health Organization. Dengue and Severe Dengue. 2012. Factsheet No. 117. Disponible en: http://www.who.int/ mediacentre/factsheets/fs117/en/. Consultado el 1 de Abril del 2013.         [ Links ]

7. Espinoza-Gómez F, Hernández-Suárez CM, Coll-Cárdenas R. Educational campaign versus malathion spraying for the control of Aedes aegypti in Colima, Mexico. J. Epidemiol. Commu. H. 2002; 56(2):148-152.         [ Links ]

8. World Health Organization. Vector surveillance and control. In: Dengue Haemorrhagic Fever – Diagnosis, treatment, prevention and control. 2nd ed. Geneva, 1997. p. 48-59.         [ Links ]

9. Bisset JA, Rodríguez MM, San Martín JL, Romero JE, Montoya R. Evaluación de la resistencia a insecticidas de una cepa de Aedes aegypti de El Salvador. Rev. Panam. Salud Publ. 2009; 26(3):229-234.         [ Links ]

10. McCall PJ,Kittayapong P. Control of dengue vectors: tools and strategies. In: Report of the Scientif ic Working Group on Dengue, 2006. Geneva. World Health Organization on behalf of the Special Programme for Research and Training in Tropical Diseases. 2007. p. 110-119. Disponible en: http:// www.who.int/tdr/publications/documents/swg_dengue_ 2.pdf. consultado en Febrero de 2012.         [ Links ]

11. World Health Organization and Special Programme for Research and Training in Tropical Diseases. Dengue. Guidelines for diagnosis, treatment, prevention and control.2009. Disponible en: http://whqlibdoc.who.int/pub lications/2009/9789241547871_eng.pdf. Consultado en Marzo del 2011.         [ Links ]

12. Shaalan EA, Canyon D, Younes MW, Abdel-Wahab H, Mansour AH. A review of botanical phytochemicals with mosquitocidal potential. Environ. Int. 2005; 31(8):11491166.         [ Links ]

13. Polson KA, Brogdon WG., Rawlins SC, Chadee DD. Characterization of insecticide resistance in Trinidadian strains of Aedes aegypti mosquitoes. Acta Trop. 2011; 117:31-38.         [ Links ]

14. Williams PL, James RC, Roberts SM. Principles of toxicology: environmental and industrial applications. 2nd ed. New York. John Wiley, 2000. p. 346-353.         [ Links ]

15. Fatta D, Canna-Michaelidou S, Michael C, Demetriou E, Christodoulidou M, Achilleos A, et al. Organochlorine and organophosphoric insecticides, herbicides and heavy metals residue in industrial wastewaters in Cyprus. J. Hazard Mater. 2007; 145(1-2):169-179.         [ Links ]

16. Trebse P, Arcon I. Degradation of organophosphorus compounds by X-ray irradiation. Radiat. Phys. Chem. 2003; 67:527-530.         [ Links ]

17. Grue CE, Gibert PL, Seeley ME. Neurophysiological and Behavioral Changes in Non-Target Wildlife Exposed to Organophosphate and Carbamate Pesticides: Thermoregulation, Food Consumption, and Reproduction. Amer. Zool. 1997; 37 (4):369-388.         [ Links ]

18. Dent D. Insect pest management. 2nd ed. London. CAB International, 2000. p. 85.         [ Links ]

19. Marrs TC, Ballantyne B. Pesticide toxicology and international regulation. John Wiley & Sons, Ltd. 2004. p. 96. ISBN 0-471-49644-8.         [ Links ]

20. Melo-Santos MA, Varjal-Melo JJ, Araújo AP, Gomes TC, Paiva MH, Regis LN, et al. Resistance to the organophosphate temephos: mechanisms, evolution and reversion in an Aedes aegypti laboratory strain from Brazil. Acta Trop. 2010; 113(2):180-189.         [ Links ]

21. Klaassen C. Casarett and Doull´s toxicology: the basic science of poisons. 5th ed. Nueva York. Mc Graw Hill. 1996. p. 10-49.         [ Links ]

22. Marcombe S, Poupardin R, Darriet F, Reynaud S, Bonnet J, Strode C, et al. Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics. 2009; 26 (10):494.         [ Links ]

23. Mani TR, Arunachalam N, Rajendran R, Satyanarayana K, Dash AP. Efficacy of thermal fog application of deltacide, a synergized mixture of pyrethroids, against Aedes aegypti, the vector of dengue. Trop. Med. Int. Health. 2005; 10(12):1298-1304.         [ Links ]

24. Ocampo CB, Salazar-Terreros MJ, Mina NJ, McAllister J, Brogdon W. Insecticide resistance status ofAedes aegypti in 10 localities in Colombia. Acta Trop. 2011; 118 (1):37-44.         [ Links ]

25. García GP, Flores AE, Fernández-Salas I, Saavedra-Rodríguez K, Reyes-Solis G, Lozano-Fuentes S, et al. Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México. PLoS Neglect Trop. Dis. 2009; 3(10):e531.         [ Links ]

26. Yaicharoen R, Kiatfuengfoo R, Chareonviriyaphap T, Rongnoparut P. Characterization of deltamethrin resistance in field populations of Aedes aegypti in Thailand. J. Vector Ecol. 2005; 30(1):144-150.         [ Links ]

27. Rodríguez M, Bisset J, Ricardo Y, Pérez O, Montada D, Figueredo D, et al. Resistencia a insecticidas organofosforados en Aedes aegypti (Diptera: Culicidae) de Santiago de Cuba, 1997-2009. Rev. Cubana Med. Trop. 2010; 62 (3):217-223.         [ Links ]

28. Hemingway J. Insecticide Resistance In Aedes Aegypti. In: Report of the Scientific Working Group on Dengue, 2006. Geneva. World Health Organization on behalf of the Special Programme for Research and Training in Tropical Diseases. 2007. p. 120-122.         [ Links ]

29. Pontes RJ, Dantas Filho FF, Alencar CH, Regazzi AC, Cavalcanti LP, Ramos AN Jr, et al. Impact of water renewal on the residual effect of larvicides in the control of Aedes aegypti. Mem. I. Oswaldo Cruz. 2010; 105(2): 220-224.         [ Links ]

30. Zaim M, Jambulingam P. Global insecticide use for vector-borne disease control. In World Health Organization. Department of Control of Neglected Tropical Diseases (NTD) WHO Pesticide Evaluation Scheme (WHOPES). 3th ed. Geneva. WHO Library Cataloguing-in-Publication Data; 2007. p. 38-47.         [ Links ]

31. Chen CD, Nazni WA, Lee HL, Sofian-Azirun M. Susceptibility of Aedes aegypti and Aedes albopictus to temephos in four study sites in Kuala Lumpur City Center and Selangor State, Malaysia. Trop. Biomed. 2005; 22 (2):207-216.         [ Links ]

32. Husham (PEH) AO, Abdalmagid (PEH, MPH) MA, Brair (PEH, MPEH) M. Status Susceptibility of dengue vector; Aedes aegypti to different groups of Insecticides in Port Sudan City -Red Sea State. Sudan. J. Public Health. 2010; 5(4):199-202.         [ Links ]

33. Chareonviriyaphap T, Aum-aung B, Ratanatham S. Current insecticide resistance patterns in mosquito vectors in Thailand. Se Asian J. Trop. Med. 1999; 30(1):184-194.         [ Links ]

34. World Health Organization Technical Report Series 899. Chemestry and specifications of pesticides. Sixteenth report of the WHO Expert Committee on Vector Biology and Control. Geneva. 2001. p. 9, 13. ISBN 92 4 120899 6.         [ Links ]

35. Bisset JA, Rodríguez MM, Cáceres L. Niveles de resistencia a insecticidas y sus mecanismos en 2 cepas de Aedes aegypti de Panamá. Rev. Cubana Med. Trop. 2003; 55(3):191-195.         [ Links ]

36. Instituto de Salud, Ambiente y Trabajo. Diagnóstico situacional del uso de DDT y el control de la malaria. Informe regional para México y Centroamérica. México, D.F. Sin año. Disponible en http://www.cec.org/Storage/44/3646_ InfRegDDTb_ES_EN.pdf. consultado en Abril de 2013.         [ Links ]

37. Dusfour I, Thalmensy V, Gaborit P, Issaly J, Carinci R, Girod R. Multiple insecticide resistance in Aedes aegypti (Diptera: Culicidae) populations compromises the effectiveness of dengue vector control in French Guiana. Mem I. Oswaldo Cruz. 2011; 106(3):346-352.         [ Links ]

38. Vargas F, Córdova O, Alvarado A. Determinación de la resistencia a insecticidas en Aedes aegypti, Anopheles albimanus y Lutzomyia peruensis procedentes del norte peruano. Rev. Peru. Med. Exp. Salud Publica. 2006; 23(4): 259-264.         [ Links ]

39. Lima JB, Da-Cunha MP, Da Silva RC, Galardo AK, Soares Sda S, Braga IA, et al. Resistance of Aedes aegypti to organophosphates in several municipalities in the State of Rio de Janeiro and Espírito Santo, Brazil. Am. J. Trop. Med. Hyg. 2003; 68(3):329-333.         [ Links ]

40. Llinás GA, Seccacini E, Gardenal CN, Licastro S. Current resistance status to temephos in Aedes aegypti from different regions of Argentina. Mem. I. Oswaldo Cruz. 2010; 105(1):113-116.         [ Links ]

41. Alvarez L, Briceno A, Oviedo M. Resistance to Temephos in populations of Aedes aegypti (Diptera: Culicidae) of the west of Venezuela. Rev. Colomb. Entomol. 2006; 32(2):172-175.         [ Links ]

42. Rodriguez R. Estrategias para el control del dengue y del Aedes aegypti en las Américas. Rev. Cubana Med. Trop. 2002; 54(3): 189-201.         [ Links ]

43. Montada D, Castex M, Suárez S, Figueredo D, Leyva M. Estado de la resistencia a insecticidas en adultos del mosquito Aedes aegypti del municipio Playa, Ciudad de La Habana, Cuba. Rev. Cubana Med. Trop. 2005; 57(2):137-142.         [ Links ]

44. Lima EP, Paiva MH, de Araújo AP, da Silva EV, da Silva UM, de Oliveira LN, et al. Insecticide resistance in Aedes aegypti populations from Ceará, Brazil. Parasite Vector. 2011; 12(4):5.         [ Links ]

45. Martins AJ, Lins RM, Linss JG, Peixoto AA, Valle D. Voltage-gated sodium channel polymorphism and metabolic resistance in pyrethroid-resistant Aedes aegypti from Brazil. Am. J. Trop. Med. Hyg. 2009; 81(1):108-115.         [ Links ]

46.SeversonDW,AnthonyNM,AndreevO,ffrench-Constant RH. Molecular mapping of insecticide resistance genes in the yellow fever mosquito (Aedes aegypti). J. Hered. 1997; 88(6):520-524.         [ Links ]

47. Kamgang B, Marcombe S, Chandre F, Nchoutpouen E, Nwane P, Etang J, et al. Insecticide susceptibility of Aedes aegypti and Aedes albopictus in Central Africa. Parasit Vector. 2011; 4:79.         [ Links ]

48. Pérez EE, Molina D. Resistencia focal a insecticidas organosintéticos en Aedes aegypti (Linneaus, 1762) (Díptera: Culicidae) de diferentes municipios del estado Aragua, Venezuela. Bol. de Mal. Salud Amb. 2009; 49(1):143-150.         [ Links ]

49. Marcombe S, Mathieu RB, Pocquet N, Riaz MA, Poupardin R, Sélior S, et al. Insecticide Resistance in the Dengue Vector Aedes aegypti from Martinique: Distribution, Mechanisms and Relations with Environmental Factors. PLoS One. 2012; 7(2):e30989.         [ Links ]

50. Vezzani D, CarbajoAE.Aedes aegypti,Aedes albopictus, and dengue in Argentina: current knowledge and future directions. Mem I. Oswaldo Cruz. 2008; 103(1):66-74.         [ Links ]

51. Fonseca-González I, Quiñones ML, Lenhart A, Brogdon WG. Insecticide resistance status of Aedes aegypti (L.) from Colombia. Pest Manag. Sci. 2011; 67(4):430-437.         [ Links ]

52. Chuaycharoensuk T, Juntarajumnong W, Boonyuan W, Bangs MJ, Akratanakul P, Thammapalo S, et al. Frequency of pyrethroid resistance in Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Thailand. J. Vector Ecol. 2011; 36(1):204-212.         [ Links ]

53. Marcombe S, Darriet F, Tolosa M, Agnew P, Duchon S, Etienne M, etal. Pyrethroid resistance reduces the efficacy of space sprays for dengue control on the island of Martinique (Caribbean). PLoS Neglect. Trop. D. 2011; 5(6):e1202.         [ Links ]

54. Mazzarri MB, Georghiou GP. Characterization of resistance to organophosphate, carbamate, and pyrethroid insecticides in field populations of Aedes aegypti from Venezuela. J. Am. Mosq. Control Assoc. 1995; 11(3):315-322.         [ Links ]

55. Alavanja MC, Bonner MR. Occupational pesticide exposures and cancer risk: a review. J Toxicol. Environ. Health. 2012; 15(4):238-263.         [ Links ]

56. Oates L, Cohen M. Assessing diet as a modifiable risk factor for pesticide exposure. Int. J. Environ. Res. Public. Health. 2011; 8(6):1792-1804.         [ Links ]

57. Luo Y, Zhang M. Environmental modeling and exposure assessment of sediment-associated pyrethroids in an agricultural watershed. PLoS One. 2011; 6(1):e15794.         [ Links ]

58. Wetterauer B, Ricking M, Otte JC, Hallare AV, Rastall A, Erdinger L, et al. Toxicity, dioxin-like activities, and endocrine effects of DDT metabolites--DDA, DDMU, DDMS, and DDCN. Environ Sci Pollut Res Int. 2012; 19(2):403-415.         [ Links ]

59. Kamel F, Hoppin JA. Association of pesticide exposure with neurologic dysfunction and disease. Environ. Health Perspect. 2004; 112(9):950-958.         [ Links ]

60. Massol RH, Antollini SS, Barrantes FJ. Effect of organochlorine insecticides on nicotinic acetylcholine receptor-rich membranes. Neuropharmacology. 2000; 39(6):1095-1106.         [ Links ]

61. Chowdhury N, Ghosh A, Chandra G. Mosquito larvicidal activities of Solanum villosum berry extract against the dengue vector Stegomyia aegypti. BMC Complement Altern. M. 2008; 8:10.         [ Links ]

62. Dia I, Diagne CT, Ba Y, Diallo D, Konate L, Diallo M. Insecticide susceptibility of Aedes aegypti populations from Senegal and Cape Verde Archipelago. Parasit Vectors. 2012; 5:238. doi: 10.1186/1756-3305-5-238.         [ Links ]

63. Koc F, Yigit Y, Kursad Das Y, Gurel Y, Yarali C. Determination of Aldicarb, Propoxur, Carbofuran, Carbaryl and Methiocarb Residues in Honey by HPLC with Post-column Derivatization and Fluorescence Detection after Elution from a Florisil Column. J. Food Drug Anal. 2008; 16(3):39-45. (ARTÍCULO ADJUNTO)         [ Links ]

64. Kawada H, Higa Y, Komagata O, Kasai S, Tomita T, Thi Yen N, et al. Widespread distribution of a newly found point mutation in voltage-gated sodium channel in pyrethroid-resistant Aedes aegypti populations in Vietnam. PLoS Neglect. Trop. D. 2009; 3(10):e527.         [ Links ]

65. Wan-Norafikah O, Nazni WA, Noramiza S, Shafa’ar­Koohar S, Azirol-Hisham A, Nor-Hafizah R. Vertical dispersal of Aedes (Stegomyia) spp. in high-rise apartments in Putrajaya, Malaysia. Trop. Biomed. 2010; 27(3):662-667.         [ Links ]

66. Montella IR, Martins AJ, Viana-Medeiros PF, Lima JB, Braga IA, Valle D. Insecticide resistance mechanisms of Brazilian Aedes aegypti populations from 2001 to 2004. Am. J. Trop. Med. Hyg. 2007; 77(3):467-477.         [ Links ]

67. Garelli FM, Espinosa MO, Weinberg D, Trinelli MA, Gürtler RE. Water use practices limit the effectiveness of a temephos-based Aedes aegypti larval control program in Northern Argentina. PLoS Neglect. Trop. D. 2011; 5(3): e991.         [ Links ]

68. Yan G, Chadee DD, Severson DW. Evidence for genetic hitchhiking effect associated with insecticide resistance in Aedes aegypti. Genetics. 1998; 148(2):793-800.         [ Links ]

1 Biologist. Environmental and Computational Chemistry Group. University of Cartagena. almas213@yahoo.es

2 Pharmaceutical Chemist. Ph.D. Environmental and Computational Chemistry Group. Faculty of Pharmaceutical Sciences. Campus of Zaragocilla. University of Cartagena. Cartagena, Colombia. joliverov@unicartagena.edu.com


Recibido: 15 diciembre 2012 Aprobado: 25 mayo 2013

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License