Abstract
Aedes aegypti mosquitoes are primary vectors of dengue, yellow fever, chikungunya and Zika viruses. Ae. aegypti is highly anthropophilic and relies nearly exclusively on human blood meals and habitats for reproduction. Socioeconomic factors may be associated with the spread of Ae. aegypti due to their close relationship with humans. This paper describes and summarizes the published literature on the association between socioeconomic variables and the distribution of Ae. aegypti mosquitoes in the mainland United States. A comprehensive search of PubMed/Medline, Scopus, Web of Science, and EBSCO Academic Search Complete through June 12, 2019 was used to retrieve all articles published in English on the association of socioeconomic factors and the distribution of Ae. aegypti mosquitoes. Additionally, a hand search of mosquito control association websites was conducted in an attempt to identify relevant grey literature. Articles were screened for eligibility using the process described in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Initially, 3,493 articles were identified through the database searches and previously known literature. After checking for duplicates, 2,145 articles remained. 570 additional records were identified through the grey literature search for a total of 2,715 articles. These articles were screened for eligibility using their titles and abstracts, and 2,677 articles were excluded for not meeting the eligibility criteria. Finally, the full text for each of the remaining articles (n=38) was read to determine eligibility. Through this screening process, 11 articles were identified for inclusion in this review. The findings for these 11 studies revealed inconsistent relationships between the studied socioeconomic factors and the distribution and abundance of Ae. aegypti. The findings of this review suggest a gap in the literature and understanding of the association between anthropogenic factors and the distribution of Ae. aegypti that could hinder efforts to implement effective public health prevention and control strategies should a disease outbreak occur.
Funding source: Pacific Southwest Center of Excellence in Vector-Borne Diseases, funded by the US Centers for Disease Control and Prevention
Award Identifier / Grant number: 1U01CK000516
Funding source: Arizona Technology Research and Initiative Fund
Funding source: Arizona Biomedical Research Center
Research Funding: This work has been supported by the following funds awarded to CMH: New Investigator Award from the Arizona Biomedical Research Center, start-up funds from the Arizona Technology Research and Initiative Fund, and a training grant to support WHE, from the Pacific Southwest Regional Center of Excellence for Vector-Borne Diseases funded by the U.S. Centers for Disease Control and Prevention (Cooperative Agreement 1U01CK000516).
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
Informed Consent: Informed consent is not applicable.
Ethical approval: The conducted research is not related to either human or animal use.
References
1. Gould, E, Pettersson, J, Higgs, S, Charrel, R, de Lamballerie, X. Emerging arboviruses: why today? One Health 2017;4:1–13. https://doi.org/10.1016/j.onehlt.2017.06.001.Search in Google Scholar
2. Moreno-Madriñán, MJ, Turell, M. History of mosquitoborne diseases in the United States and implications for new pathogens. Emerg Infect Dis 2018;24:821–826. https://doi.org/10.3201/eid2405.171609.Search in Google Scholar
3. Uribe, LJ. The problems of Aedes aegypti control in the Americas. Bull Pan Am Health Organ 1983;17:133–41.Search in Google Scholar
4. Hotez, PJ. Zika in the United States of America and a fateful 1969 decision. PLoS Negl Trop Dis 2016;10:e0004765. https://doi.org/10.1371/journal.pntd.0004765.Search in Google Scholar
5. Kraemer, MUG, Sinka, ME, Duda, KA, Mylne, AQN, Shearer, FM, Barker, CM, et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. Albopictus. Elife 2015;4:e08347. https://doi.org/10.7554/eLife.08347.Search in Google Scholar
6. Kraemer, MUG, Reiner, RC, Brady, OJ, Messina, JP, Gilbert, M, Pigott, DM, et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol 2019;4:854–63. https://doi.org/10.1038/s41564-019-0376-y.Search in Google Scholar
7. Brady, OJ, Golding, N, Pigott, DM, Kraemer, MUG, Messina, JP, Reiner, RCJ, et al. Global temperature constraints on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission. Parasites Vectors 2014;7:338. https://doi.org/10.1186/1756-3305-7-338.Search in Google Scholar
8. Christophers, SR. Aedes aegypti: the yellow fever mosquito. New York: Cambridge University Press; 1960.Search in Google Scholar
9. Brady, OJ, Johansson, MA, Guerra, CA, Bhatt, S, Golding, N, Pigott, DM, et al. Modelling adult Aedes aegypti and Aedes albopictus survival at different temperatures in laboratory and field settings. Parasites Vectors 2013;6:351. https://doi.org/10.1186/1756-3305-6-351.Search in Google Scholar
10. Walker, KR, Williamson, D, Carriere, Y, Reyes-Castro, PA, Haenchen, S, Hayden, MH, et al. Socioeconomic and human behavioral factors associated with Aedes aegypti (Diptera: Culicidae) immature habitat in Tucson, AZ. J Med Entomol 2018;55:955–63. https://doi.org/10.1093/jme/tjy011.Search in Google Scholar
11. Wilke, ABB, Vasquez, C, Petrie, W, Caban-Martinez, AJ, Beier, JC. Construction sites in Miami-Dade County, Florida are highly favorable environments for vector mosquitoes. PLoS One 2018;13:e0209625. https://doi.org/10.1371/journal.pone.0209625.Search in Google Scholar
12. Harrington, LC, Ponlawat, A, Edman, JD, Scott, TW, Vermeylen, F. Influence of container size, location, and time of day on oviposition patterns of the dengue vector, Aedes aegypti, in Thailand. Vector Borne Zoonot 2008;8:415–23. https://doi.org/10.1089/vbz.2007.0203.Search in Google Scholar
13. Abreu, FV, Morais, MM, Ribeiro, SP, Eiras, ÁE. Influence of breeding site availability on the oviposition behaviour of Aedes aegypti. Mem Inst Oswaldo Cruz 2015;110:669–76. https://doi.org/10.1590/0074-02760140490.Search in Google Scholar
14. Wong, J, Stoddard, ST, Astete, H, Morrison, AC, Scott, TW. Oviposition site selection by the dengue vector Aedes aegypti and its implications for dengue control. PLoS Negl Trop Dis 2011;5:e1015. https://doi.org/10.1371/journal.pntd.0001015.Search in Google Scholar
15. Juliano, SA, Lounibos, LP, O’Meara, GF. A field test for competitive effects of Aedes albopictus on A. aegypti in South Florida: differences between sites of coexistence and exclusion? Oecologia 2004;139:583–93. https://doi.org/10.1007/s00442-004-1532-4.Search in Google Scholar
16. Lounibos, LP, O’Meara, GF, Escher, RL, Nishimura, N, Cutwa, M, Nelson, T, et al. Testing predictions of displacement of native Aedes by the invasive Asian Tiger Mosquito Aedes albopictus in Florida, USA. Biol Invasions 2001;3:151–66. https://doi.org/10.1023/A:1014519919099.10.1023/A:1014519919099Search in Google Scholar
17. Harrington, LC, Scott, TW, Lerdthusnee, K, Coleman, RC, Costero, A, Clark, GG, et al. Dispersal of the dengue vector Aedes aegypti within and between rural communities. Am J Trop Med Hyg 2005;72:209–20.10.4269/ajtmh.2005.72.209Search in Google Scholar
18. Juarez, JG, Garcia-Luna, S, Chaves, LF, Carbajal, E, Valdez, E, Avila, C, et al. Dispersal of female and male Aedes aegypti from discarded container habitats using a stable isotope mark-capture study design in South Texas. Sci Rep 2020;10:6803. https://doi.org/10.1038/s41598-020-63670-9.Search in Google Scholar
19. Reiter, P. Oviposition, dispersal, and survival in Aedes aegypti: Implications for the efficacy of control strategies. Vector Borne Zoonot 2007;7:261–73. https://doi.org/10.1089/vbz.2006.0630.Search in Google Scholar
20. Harrington, LC, Edman, JD, Scott, TW. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol 2001;38:411–22. https://doi.org/10.1603/0022-2585-38.3.411.Search in Google Scholar
21. Martina, BE, Barzon, L, Pijlman, GP, de la Fuente, J, Rizzoli, A, Wammes, LJ, et al. Human to human transmission of arthropod-borne pathogens. Curr Opin Virol 2017;22:13–21. https://doi.org/10.1016/j.coviro.2016.11.005.Search in Google Scholar
22. Fauci, AS, Morens, DM. Zika virus in the Americas--Yet another arbovirus threat. N Engl J Med 2016;374:601–4. https://doi.org/10.1056/NEJMp1600297.Search in Google Scholar
23. Eisen, L, Moore, CG. Aedes (Stegomyia) aegypti in the continental United States: a vector at the cool margin of its geographic range. J Med Entomol 2013;50:467–78. https://doi.org/10.1603/ME12245.Search in Google Scholar
24. Guzman, MG, Harris, E. Dengue. Lancet 2015;385:453–65. https://doi.org/10.1016/S0140-6736(18)32560-1.Search in Google Scholar
25. Castro, MC, Wilson, ME, Bloom, DE. Disease and economic burdens of dengue. Lancet Infect Dis 2017;17:e70–8. https://doi.org/10.1016/S1473-3099(16)30545-X.Search in Google Scholar
26. Pinheiro, FP, Corber, SJ. Global situation of dengue and dengue haemorrhagic fever, and its emergence in the Americas. World Health Stat Q 1997;50:161–9.Search in Google Scholar
27. Kouri, GP, Guzman, MG, Bravo, JR, Triana, C. Dengue haemorrhagic fever/dengue shock syndrome: Lessons from the Cuban epidemic, 1981. Bull World Health Organ 1989;67:375–80.Search in Google Scholar
28. Shepard, DS, Undurraga, EA, Halasa, YA, Stanaway, JD. The global economic burden of dengue: a systematic analysis. Lancet Infect Dis 2016;16:935–41. https://doi.org/10.1016/S1473-3099(16)00146-8.Search in Google Scholar
29. World Health Organization. WHO Region of the Americas records highest number of dengue cases in history; Cases spike in other regions. Available from: https://www.who.int/news-room/detail/21-11-2019-who-region-of-the-americas-records-highest-number-of-dengue-cases-in-history-cases-spike-in-other-regions.Search in Google Scholar
30. World Health Organization. WHO scales up response to worldwide surge in dengue. Available at: https://www.who.int/news-room/feature-stories/detail/who-scales-up-response-to-worldwide-surge-in-dengue.Search in Google Scholar
31. Murray, KO, Rodriguez, LF, Herrington, E, Kharat, V, Vasilakis, N, Walker, C, et al. Identification of dengue fever cases in Houston, Texas, with evidence of autochthonous transmission between 2003 and 2005. Vector Borne Zoonot 2013;13:835–45. https://doi.org/10.1089/vbz.2013.1413.Search in Google Scholar
32. Radke, EG, Gregory, CJ, Kintziger, KW, Sauber-Schatz, EK, Hunsperger, EA, Gallagher, GR, et al. Dengue outbreak in Key West, Florida, USA, 2009. Emerg Infect Dis 2012;18:135–7. https://doi.org/10.3201/eid1801.110130.Search in Google Scholar
33. Adalja, AA, Sell, TK, Bouri, N, Franco, C. Lessons learned during dengue outbreaks in the United States, 2001-2011. Emerg Infect Dis 2012;18:608–14. https://doi.org/10.3201/eid1804.110968.Search in Google Scholar
34. Brunkard, JM, Luis, J, López, R, Ramirez, J, Cifuentes, E, Rothenberg, SJ, et al. Dengue fever seroprevalence and risk factors, Texas–Mexico border, 2004. Emerg Infect Dis 2007;13:1477–83. https://doi.org/10.3201/eid1310.061586.Search in Google Scholar
35. Monath, TP, Vasconcelos, PFC. Yellow fever. J Clin Virol 2015;64:160–73. https://doi.org/10.1201/9780203752463.Search in Google Scholar
36. Foster, KR, Jenkins, MF, Toogood, AC. The Philadelphia yellow fever epidemic of 1793. Sci Am 1998;279:88–93. https://doi.org/10.1038/scientificamerican0898-88.Search in Google Scholar
37. The Lancet Infectious Diseases. Yellow fever: the consequences of neglect. Lancet Infect Dis 2016;16:753. https://doi.org/10.1016/S1473-3099(15)00169-3.Search in Google Scholar
38. Pialoux, G, Gauzere, BA, Jaureguiberry, S, Strobel, M. Chikungunya, an epidemic arbovirus. Lancet Infect Dis 2007;7:319–27. https://doi.org/10.1016/S1473-3099(07)70107-X.Search in Google Scholar
39. Zeller, H, Van Bortel, W, Sudre, B. Chikungunya: its history in Africa and Asia and its spread to new regions in 2013-2014. J Infect Dis 2016;214:S436–40. https://doi.org/10.1093/infdis/jiw391.Search in Google Scholar
40. Sharp, TM, Ryff, KR, Alvarado, L, Shieh, WJ, Zaki, SR, Margolis, HS, et al. Surveillance for chikungunya and dengue during the first year of chikungunya virus circulation in Puerto Rico. J Infect Dis 2016;214:S475–81. https://doi.org/10.1093/infdis/jiw245.Search in Google Scholar
41. Musso, D, Gubler, DJ. Zika virus. Clin Microbiol Rev 2016;29:487–524. https://doi.org/10.1128/CMR.00072-15.Search in Google Scholar
42. Gibney, KB, Fischer, M, Prince, HE, Kramer, LD, St George, K, Kosoy, OL, et al. Chikungunya fever in the United States: a fifteen year review of cases. Clin Infect Dis 2011;52:e121–6. https://doi.org/10.1093/cid/ciq214.Search in Google Scholar
43. Hamel, R, Liégeois, F, Wichit, S, Pompon, J, Diop, F, Talignani, L, et al. Zika virus: epidemiology, clinical features and host-virus interactions. Microb Infect 2016;18:441–9. https://doi.org/10.1016/j.micinf.2016.03.009.Search in Google Scholar
44. Hernández-Ávila, JE, Palacio-Mejía, LS, López-Gatell, H, Alpuche-Aranda, CM, Molina-Vélez, D, González-González, L, et al. Zika virus infection estimates, Mexico. Bull World Health Organ 2018;96:306–13. https://doi.org/10.2471/BLT.17.201004.Search in Google Scholar
45. Díaz-Quiñonez, JA, López-Martínez, I, Torres-Longoria, B, Vázquez-Pichardo, M, Cruz-Ramírez, E, Ramírez-González, JE, et al. Evidence of the presence of the Zika virus in Mexico since early 2015. Virus Genes 2016;52:855–7. https://doi.org/10.1007/s11262-016-1384-0.Search in Google Scholar
46. Pan American Health Organization & World Health Organization. Zika cases and congenital syndrome associated with Zika virus reported by countries and territories in the Americas, 2015-2018 cumulative cases. Available from: https://www.paho.org/hq/index.php?option=com_docman&view=download&category_slug=ccumulativ-cases-pdf-8865&alias=43296-zika-cumulative-cases-4-january-2018-296&Itemid=270&lang=en.Search in Google Scholar
47. The United Nations Development Programme. A socio-economic impact assessment of the Zika virus in Latin America and the Caribbean: with a focus on Brazil, Colombia and Suriname. Available from: http://www.undp.org/content/undp/en/home/librarypage/hiv-aids/a-socio-economic-impact-assessment-of-the-zika-virus-in-latin-am.html.Search in Google Scholar
48. Centers for Disease Control and Prevention. Zika virus, 2016 case counts in the US. Available from: https://www.cdc.gov/zika/reporting/2016-case-counts.html.Search in Google Scholar
49. Martin, CA, Warren, PS, Kinzig, AP. Neighborhood socioeconomic status is a useful predictor of perennial landscape vegetation in residential neighborhoods and embedded small parks of Phoenix, AZ. Landsc Urban Plan 2004;69:355–68. https://doi.org/10.1016/j.landurbplan.2003.10.034.Search in Google Scholar
50. Martin, CA, Stabler, LB. Plant gas exchange and water status in urban desert landscapes. J Arid Environ 2002;51:235–54. https://doi.org/10.1006/jare.2001.0946.Search in Google Scholar
51. Ouyang, Y, Wentz, EA, Ruddell, BL, Harlan, SL. A multi-scale analysis of single-family residential water use in the Phoenix metropolitan area. JAWRA J Am Water Resour Assoc 2014;50:448–67. https://doi.org/10.1111/jawr.12133.Search in Google Scholar
52. Hayden, MH, Uejio, CK, Walker, K, Ramberg, F, Moreno, R, Rosales, C, et al. Microclimate and human factors in the divergent ecology of Aedes aegypti along the Arizona, U.S./Sonora, MX Border. EcoHealth 2010;7:64–77. https://doi.org/10.1007/s10393-010-0288-z.Search in Google Scholar
53. U.S. Department of Health and Human Services. Healthy people 2020, social determinants of health. Available from: https://www.healthypeople.gov/2020/topics-objectives/topic/social-determinants-of-health.Search in Google Scholar
54. Dai, D. Racial/ethnic and socioeconomic disparities in urban green space accessibility: where to intervene? Landsc Urban Plan 2011;102:234–44. https://doi.org/10.1016/j.landurbplan.2011.05.002.Search in Google Scholar
55. Morano, JP, Holt, DA. The social determinants of health contextualized for the Zika virus. Int J Infect Dis 2017;65:142–3. https://doi.org/10.1016/j.ijid.2017.10.006.Search in Google Scholar
56. Sallam, MF, Fizer, C, Pilant, AN, Whung, PY. Systematic review: land cover, meteorological, and socioeconomic determinants of Aedes mosquito habitat for risk mapping. Int J Env Res Pub Health 2017;14:1230. https://doi.org/10.3390/ijerph14101230.Search in Google Scholar
57. Moher, D, Liberati, A, Tetzlaff, J, Altman, DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097. https://doi.org/10.1371/journal.pmed.1000097.Search in Google Scholar
58. Chambers, DM, Young, LF, Hill, HS. Backyard mosquito larval habitat availability and use as influenced by census tract determined resident income levels. J Am Mosq Control Assoc 1986;2:539–44.Search in Google Scholar
59. Martin, E, Medeiros, MCI, Carbajal, E, Valdez, E, Juarez, JG, Garcia-Luna, S, et al. Surveillance of Aedes aegypti indoors and outdoors using Autocidal Gravid Ovitraps in South Texas during local transmission of Zika virus, 2016 to 2018. Acta Trop 2019;192:129–37. https://doi.org/10.1016/j.actatropica.2019.02.006.Search in Google Scholar
60. Walker, KR, Joy, TK, Ellers-Kirk, C, Ramberg, FB. Human and environmental factors affecting Aedes aegypti distribution in an arid urban environment. J Am Mosq Control Assoc 2011;27:135–41. https://doi.org/10.2987/10-6078.1.Search in Google Scholar
61. Reiter, P, Lathrop, S, Bunning, M, Biggerstaff, B, Singer, D, Tiwari, T, et al. Texas lifestyle limits transmission of dengue virus. Emerg Infect Dis 2003;9:86–9. https://doi.org/10.3201/eid0901.020220.Search in Google Scholar
62. Obenauer, JF, Andrew Joyner, T, Harris, JB. The importance of human population characteristics in modeling Aedes aegypti distributions and assessing risk of mosquito-borne infectious diseases. Trop Med Health 2017;45:38. https://doi.org/10.1186/s41182-017-0078-1.Search in Google Scholar
63. Leisnham, PT, Juliano, SA. Spatial and temporal patterns of coexistence between competing Aedes mosquitoes in urban Florida. Oecologia 2009;160:343–52. https://doi.org/10.1007/s00442-009-1305-1.Search in Google Scholar
64. Braks, MAH, Honório, NA, Lourenço-De-Oliveira, R, Juliano, SA, Lounibos, LP. Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida. J Med Entomol 2003;40:785–94. https://doi.org/10.1603/0022-2585-40.6.785.Search in Google Scholar
65. Rey, JR, Nishimura, N, Wagner, B, Braks, MAH, O’Connell, SM, Lounibos, LP. Habitat segregation of mosquito arbovirus vectors in south Florida. J Med Entomol 2006;43:1134–41. https://doi.org/10.1093/jmedent/43.6.1134.Search in Google Scholar
66. Vitek, CJ, Gutierrez, JA, Dirrigl, FJ. Dengue vectors, human activity, and dengue virus transmission potential in the Lower Rio Grande Valley, Texas, United States. J Med Entomol 2014;51:1019–28. https://doi.org/10.1603/me13005.Search in Google Scholar
67. Resende, MC, Silva, IM, Ellis, BR, Eiras, ÁE. A comparison of larval, ovitrap and MosquiTRAP surveillance for Aedes (Stegomyia) aegypti. Mem Inst Oswaldo Cruz 2013;108:1024–30. https://doi.org/10.1590/0074-0276130128.Search in Google Scholar
68. Sivagnaname, N, Gunasekaran, K. Need for an efficient adult trap for the surveillance of dengue vectors. Indian J Med Res 2012;136:739–49.Search in Google Scholar
69. Little, E, Biehler, D, Leisnham, PT, Jordan, R, Wilson, S, LaDeau, SL. Socio-ecological mechanisms supporting high densities of Aedes albopictus (Diptera: Culicidae) in Baltimore, MD. J Med Entomol 2017;54:1183–92. https://doi.org/10.1093/jme/tjx103.Search in Google Scholar
70. Quintero, J, Carrasquilla, G, Suárez, R, González, C, Olano, VA. An ecosystemic approach to evaluating ecological, socioeconomic and group dynamics affecting the prevalence of Aedes aegypti in two Colombian towns. Cad Saúde Pública 2009;25:S93–103. https://doi.org/10.1590/s0102-311x2009001300009.Search in Google Scholar
71. Ferreira, AC, Neto, FC. Infestation of an urban area by Aedes aegypti and relation with socioeconomic levels. Rev Saude Publica 2007;41:915–22. https://doi.org/10.1590/s0034-89102007000600005.Search in Google Scholar
72. Dickens, BL, Sun, H, Jit, M, Cook, AR, Carrasco, LR. Determining environmental and anthropogenic factors which explain the global distribution of Aedes aegypti and Ae. albopictus. BMJ Glob Health 2018;3:e000801. https://doi.org/10.1136/bmjgh-2018-000801.Search in Google Scholar
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The online version of this article offers supplementary material (https://doi.org/10.1515/REVEH-2020-0028).
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