Mosquito-Disseminated Insecticide for Citywide Vector Control and Its Potential to Block Arbovirus Epidemics: Entomological Observations and Modeling Results from Amazonian Brazil

1. Weaver SC, Reisen WK. Present and future arboviral threats. Antiviral Res. 2010;85:328–45. doi: 10.1016/j.antiviral.2009.10.008 19857523

2. Institute of Medicine. Vector-borne diseases: understanding the environmental, human health, and ecological connections. Washington (DC): National Academies Press; 2008.

3. World Health Organization, Special Programme for Research and Training in Tropical Diseases. Dengue: guidelines for diagnosis, treatment, prevention and control. Geneva: World Health Organization; 2009.

4. Petersen LR, Brault AC, Nasci RS. West Nile virus: review of the literature. JAMA. 2013;310:308–15. doi: 10.1001/jama.2013.8042 23860989

5. Weaver SC, Lecuit M. Chikungunya virus and the global spread of a mosquito-borne disease. N Engl J Med. 2015;372:1231–9. doi: 10.1056/NEJMra1406035 25806915

6. Fauci AS, Morens DM. Zika virus in the Americas—yet another arbovirus threat. N Engl J Med. 2016;374:601–4. doi: 10.1056/NEJMp1600297 26761185

7. Faria NR, Azevedo R do S, Kraemer MU, Souza R, Cunha MS, Hill SC, et al. Zika virus in the Americas: early epidemiological and genetic findings. Science. 2016;352:345–9. doi: 10.1126/science.aaf5036 27013429

8. Mlakar J, Korva M, Tul N, Popović M. Zika virus associated with microcephaly. N Engl J Med. 2016;374:951–8. doi: 10.1056/NEJMoa1600651 26862926

9. Rubin EJ, Greene MF, Baden LR. Zika virus and microcephaly. N Engl J Med. 2016;374:984–5. doi: 10.1056/NEJMe1601862 26862812

10. Cauchemez S, Besnard M, Bompard P, Dub T, Guillemette-Artur P, Eyrolle-Guignot D, et al. Association between Zika virus and microcephaly in French Polynesia, 2013–2015: a retrospective study. Lancet. 2016;387:2125–32. doi: 10.1016/S0140-6736(16)00651-6 26993883

11. Besnard M, Eyrolle-Guignot D, Guillemette-Artur P, Lastère S, Bost-Bezeaud F, Marcelis L, et al. Congenital cerebral malformations and dysfunction in fetuses and newborns following the 2013 to 2014 Zika virus epidemic in French Polynesia. Euro Surveill. 2016;21:30181.

12. Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR. Zika virus and birth defects—reviewing the evidence for causality. N Engl J Med. 2016;374:1981–7. doi: 10.1056/NEJMsr1604338 27074377

13. Cao-Lormeau VM, Blake A, Mons S, Lastère S, Roche C, Vanhomwegen J, et al. Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet. 2016;387:1531–9. doi: 10.1016/S0140-6736(16)00562-6 26948433

14. Villar L, Dayan GH, Arredondo-García JL, Rivera DM, Cunha R, Deseda C, et al. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med. 2015; 372:113–23. doi: 10.1056/NEJMoa1411037 25365753

15. Abbink P, Larocca RA, De La Barrera RA, Bricault CA, Moseley ET, Boyd M, et al. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science. 2016;353:1129–32. doi: 10.1126/science.aah6157 27492477

16. Thomas SJ. Preventing dengue—is the possibility now a reality? N Engl J Med. 2015;372:172–3. doi: 10.1056/NEJMe1413146 25365706

17. Lipsitch M, Cowling BJ. Zika vaccine trials. Science. 2016;353:1094–5. doi: 10.1126/science.aai8126 27609872

18. Morrison AC, Zielinski-Gutierrez E, Scott TW, Rosenberg R. Defining challenges and proposing solutions for control of the virus vector Aedes aegypti. PLoS Med. 2008;5:e68. doi: 10.1371/journal.pmed.0050068 18351798

19. Wilder-Smith A, Renhorn KE, Tissera H, Abu Bakar S, Alphey L, Kittayapong P, et al. DengueTools: innovative tools and strategies for the surveillance and control of dengue. Glob Health Action. 2012;5:17273.

20. Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8:e1002588. doi: 10.1371/journal.ppat.1002588 22496640

21. Heffernan JM, Smith RJ, Wahl LM. Perspectives on the basic reproductive ratio. J R Soc Interface. 2005;2:281–93. doi: 10.1098/rsif.2005.0042 16849186

22. Anderson RM, May RM. Infectious diseases of humans: dynamics and control. Oxford: Oxford University Press; 1991.

23. Shepard DS, Coudeville L, Halasa YA, Zambrano B, Dayan GH. Economic impact of dengue illness in the Americas. Am J Trop Med Hyg. 2011;84:200–7. doi: 10.4269/ajtmh.2011.10-0503 21292885

24. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013;496:504–7. doi: 10.1038/nature12060 23563266

25. Bowman LR, Donegan S, McCall PJ. Is dengue vector control deficient in effectiveness or evidence?: systematic review and meta-analysis. PLoS Negl Trop Dis. 2016;10:e0004551. doi: 10.1371/journal.pntd.0004551 26986468

26. Itoh T. Utilization of blood-fed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator, pyriproxyfen, to larval habitats. Trop Med. 1994;36:243–8.

27. Devine GJ, Perea EZ, Killeen GF, Stancil JD, Clark SJ, Morrison AC. Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc Natl Acad Sci U S A. 2009;106:11530–4. doi: 10.1073/pnas.0901369106 19561295

28. World Health Organization. Pyriproxyfen in drinking-water: use for vector control in drinking-water sources and containers. Background document for development of WHO guidelines for drinking-water quality. Geneva: World Health Organization; 2008.

29. Abad-Franch F, Zamora-Perea E, Ferraz G, Padilla-Torres SD, Luz SLB. Mosquito-disseminated pyriproxyfen yields high breeding-site coverage and boosts juvenile mosquito mortality at the neighborhood scale. PLoS Negl Trop Dis. 2015;9:e0003702. doi: 10.1371/journal.pntd.0003702 25849040

30. Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer; 2002.

31. Vaida F, Blanchard S. Conditional Akaike information for mixed-effects models. Biometrika. 2005;92:351–70.

32. Bates D, Maechler M, Bolker B, Walker S. lme4: mixed-effects models in R using S4 classes and methods with RcppEigen. 2016 [cited 2016 Dec 6]. Available from: https://github.com/lme4/lme4/.

33. R Development Core Team. R: a language and environment for statistical computing. Version 3.1.2. Vienna: R Foundation for Statistical Computing; 2014 [cited 2016 Dec 6]. Available from: https://www.R-project.org.

34. Favier C, Degallier N, Rosa-Freitas MG, Boulanger JP, Costa Lima JR, Luitgards-Moura JF, et al. Early determination of the reproductive number for vector-borne diseases: the case of dengue in Brazil. Trop Med Int Health. 2006;11:332–40. doi: 10.1111/j.1365-3156.2006.01560.x 16553913

35. David MR, Lourenço-de-Oliveira R, Maciel de Freitas R. Container productivity, daily survival rates and dispersal of Aedes aegypti mosquitoes in a high income dengue epidemic neighbourhood of Rio de Janeiro: presumed influence of differential urban structure on mosquito biology. Mem Inst Oswaldo Cruz. 2009;104:927–32. 19876569

36. Harrington LC, Buonaccorsi JP, Edman JD, Costero A, Kittayapong P, Clark GG, et al. Analysis of survival of young and old Aedes aegypti (Diptera: Culicidae) from Puerto Rico and Thailand. J Med Entomol. 2001;38:537–47. 11476334

37. Dutra HLC, dos Santos LMB, Caragata EP, Silva JBL, Villela DAM, Maciel-de-Freitas R, et al. From lab to field: the influence of urban landscapes on the invasive potential of Wolbachia in Brazilian Aedes aegypti mosquitoes. PLoS Negl Trop Dis. 2015;9:e0003689. doi: 10.1371/journal.pntd.0003689 25905888

38. Franca RFO, Neves MHL, Ayres CFJ, Melo-Neto OP, Brandão Filho SP. First International Workshop on Zika Virus held by Oswaldo Cruz Foundation FIOCRUZ in northeast Brazil March 2016—a meeting report. PLoS Negl Trop Dis. 2016;10:e0004760. doi: 10.1371/journal.pntd.0004760 27258065

39. Hervé JP, Dégallier N, Travassos da Rosa APA, Pinheiro FP, Sá Filho GC. Arboviroses—aspectos ecológicos. In: Instituto Evandro Chagas—50 anos de contribuição às ciências biológicas e à medicina tropical. Vol 1. Belém: Fundação Serviços de Saúde Pública, Ministério da Saúde do Brasil; 1986. pp. 409–37.

40. Kyle JL, Harris E. Global spread and persistence of dengue. Annu Rev Microbiol. 2008;62:71–92. doi: 10.1146/annurev.micro.62.081307.163005 18429680

41. Ohashi K, Nakada K, Ishiwatari T, Miyaguchi J, Shono Y, Lucas JR, et al. Efficacy of pyriproxyfen-treated nets in sterilizing and shortening the longevity of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 2012;49:1052–8. 23025186

42. Di Luca M, Severini F, Toma L, Boccolini D, Romi R, Remoli ME, et al. Experimental studies of susceptibility of Italian Aedes albopictus to Zika virus. Euro Surveill. 2016;21:30223.

43. Chouin-Carneiro T, Vega-Rua A, Vazeille M, Yebakima A, Girod R, Goindin D, et al. Differential susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika virus. PLoS Negl Trop Dis; 2016;10:e0004543. doi: 10.1371/journal.pntd.0004543 26938868

44. Sihuincha M, Zamora-Perea E, Orellana-Rios W, Stancil JD, López-Sifuentes V, Vidal-Oré C, et al. Potential use of pyriproxyfen for control of Aedes aegypti (Diptera: Culicidae) in Iquitos, Peru. J Med Entomol. 2005;42:620–30. 16119551

45. Focks DA. A review of entomological sampling methods and indicators for dengue vectors. Geneva: World Health Organization; 2003.

46. Vontas J, Moore S, Kleinschmidt I, Ranson H, Lindsay S, Lengeler C, et al. Framework for rapid assessment and adoption of new vector control tools. Trends Parasitol. 2014;30:191–204. doi: 10.1016/j.pt.2014.02.005 24657042

47. Alphey L. Genetic control of mosquitoes. Annu Rev Entomol. 2014;59:205–24. doi: 10.1146/annurev-ento-011613-162002 24160434

48. Carvalho DO, McKemey AR, Garziera L, Lacroix R, Donnelly CA, Alphey L, et al. Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes. PLoS Negl Trop Dis. 2015;9:e0003864. doi: 10.1371/journal.pntd.0003864 26135160

49. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature. 2011;476:454–7. doi: 10.1038/nature10356 21866160

50. Jeffery JAL, Yen NT, Nam VS, Nghia LT, Hoffmann AA, Kay BH, et al. 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. 2009;3:e0000552.

51. Secretaria de Vigilância em Saúde, Ministério da Saúde do Brasil. Relatório da reunião internacional para implementação de alternativas para o controle do Aedes aegypti no Brasil. Bol Epidemiol. 2016;47:1–9.