Environmental and Social Change Drive the Explosive Emergence of Zika Virus in the Americas

PLoS Neglected Tropical Diseases

Volumn 11, Issue 2, 2017, Pages

  Ali, Sofia ^a   Gugliemini, Olivia ^a   Harber, Serena ^a   Harrison, Alexandra ^a   Houle, Lauren ^a   Ivory, Javarcia ^a   Kersten, Sierra ^a   Khan, Rebia ^a   Kim, Jenny ^a   LeBoa, Chris ^a   Nez Whitfield, Emery ^a   O’Marr, Jamieson ^a   Rothenberg, Emma ^a   Segnitz, R Max ^a   Sila, Stephanie ^a   Verwillow, Anna ^a   Vogt, Miranda ^a   Yang, Adrienne ^a   Mordecai, Erin A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABORTION; AEDES AEGYPTI; AEDES ALBOPICTUS; CHIKUNGUNYA; CLIMATE CHANGE; DEFORESTATION; DENGUE; DISEASE RE-EMERGENCE; ENVIRONMENTAL CHANGE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL SANITATION; EPIDEMIC; GUILLAIN BARRE SYNDROME; HUMAN; LAND USE; MICROCEPHALY; NONHUMAN; POPULATION; POVERTY; PUBLIC HEALTH; REVIEW; SOCIAL ASPECT; SOCIAL CHANGE; TEMPERATURE; VECTOR CONTROL; VIRUS TRANSMISSION; WESTERN HEMISPHERE; ZIKA FEVER; ZIKA VIRUS; CLIMATE; DISEASE CARRIER; ENVIRONMENTAL EXPOSURE; GROWTH, DEVELOPMENT AND AGING; MOSQUITO VECTOR; ZIKA VIRUS INFECTION;

AMERICAS; CLIMATE; DISEASE RESERVOIRS; ENVIRONMENTAL EXPOSURE; EPIDEMICS; HUMANS; MOSQUITO VECTORS; SOCIAL CHANGE; ZIKA VIRUS INFECTION;

EID: 85014468997     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0005135     Document Type: Review

References (82)

1. Gubler DJ, Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 2002Feb1;10(2):100–3. 11827812
2. Gubler DJ, Dengue and dengue hemorrhagic fever. Clin Microbiol Rev. 1998Jul;11(3):480–96. 9665979
3. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013Apr25;496(7446):504–7. doi: 10.1038/nature1206023563266
4. PAHO WHO | Chikungunya | Statistic Data [Internet]. [cited 2016 Jul 10]. http://www.paho.org/hq/index.php?option=com_topics&view=readall&cid=5927&Itemid=40931&lang=en
5. Kindhauser MK, Allen T, Frank V, Santhana RS, Dye C, Zika: the origin and spread of a mosquito-borne virus. Bull World Health Organ [Internet]. 2016Feb9 [cited 2016 May 4]; http://www.who.int/bulletin/online_first/16-171082.pdf
6. Pan American Health Organization / World Health Organization. Zika Epidemiological Update, 14 July 2016. Washington, D.C.: PAHO/WHO; 2016 Jul.
7. Pan American Health Organization / World Health Organization. Cumulative Zika suspected and confirmed cases reported by countries and territories in the Americas, 2015–2016. [Internet]. Washington, D.C.: PAHO/WHO; 2016 Jul [cited 2016 Jul 2]. http://ais.paho.org/phip/viz/ed_zika_cases.asp
8. Confirmação do Zika Vírus no Brasil [Internet]. Portal da Saúde–Ministério da Saúde. 2015 [cited 2016 Aug 3]. http://portalsaude.saude.gov.br/index.php/o-ministerio/principal/secretarias/svs/noticias-svs/17702-confirmacao-do-zika-virus-no-brasil
9. Paul L, Carlin E. Dengue Virus Antibodies Enhance Zika Virus Infection. bioRxiv. 2016 Apr 25;
10. Faria NR, Azevedo R do S da S, Kraemer MUG, Souza R, Cunha MS, Hill SC, et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science. 2016Apr15;352(6283):345–9. doi: 10.1126/science.aaf503627013429
11. Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR, Zika virus and birth defects—reviewing the evidence for causality. N Engl J Med. 2016Apr13;374:1981–7. doi: 10.1056/NEJMsr160433827074377
12. Marcondes CB, Ximenes M de FF de M, Marcondes CB, Ximenes M de FF de M, Zika virus in Brazil and the danger of infestation by Aedes (Stegomyia) mosquitoes. Rev Soc Bras Med Trop. 2016Feb;49(1):4–10. doi: 10.1590/0037-8682-0220-201526689277
13. 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. 2016Mar3;10(3):e0004543. doi: 10.1371/journal.pntd.000454326938868
14. Hayes EB, Zika Virus Outside Africa. Emerg Infect Dis. 2009Sep;15(9):1347–50. doi: 10.3201/eid1509.09044219788800
15. Morse SS, Price-Smith AT, Factors in the Emergence of Infectious Diseases. In: Plagues and Politics [Internet]. Palgrave Macmillan UK; 2001 [cited 2016 Apr 24]. p. 8–26. (Global Issues Series). http://link.springer.com/chapter/10.1057/9780230524248_2
16. Gubler DJ, Dengue/dengue haemorrhagic fever: history and current status. Novartis Found Symp. 2006;277:3-16-22, 71–3, 251–3.
17. Manjarres-Suarez A, Olivero-Verbel J, Chemical control of Aedes aegypti: a historical perspective. Rev Costarric Salud Pública. 2013Jun;22(1):68–75.
18. Musso D, Cao-Lormeau VM, Gubler DJ, Zika virus: following the path of dengue and chikungunya?The Lancet. 2015Jul;386(9990):243–4.
19. Ochieng C, Ahenda P, Vittor AY, Nyoka R, Gikunju S, Wachira C, et al. Seroprevalence of Infections with Dengue, Rift Valley Fever and Chikungunya Viruses in Kenya, 2007. PLoS ONE. 2015Jul15;10(7):e0132645. doi: 10.1371/journal.pone.013264526177451
20. Geser A, Henderson BE, Christensen S, A multipurpose serological survey in Kenya. Bull World Health Organ. 1970;43(4):539–52. 5313066
21. Halstead SB, Reappearance of Chikungunya, Formerly Called Dengue, in the Americas. Emerg Infect Dis [Internet]. 2015Apr [cited 2016 Sep 19];21(4). http://wwwnc.cdc.gov/eid/article/21/4/14-1723_article.htm
22. Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D, Bryden WL, et al. Ecological dynamics of emerging bat virus spillover. Proc R Soc B. 2015Jan7;282(1798):20142124. doi: 10.1098/rspb.2014.212425392474
23. Althouse B, Vasilakis N, Sall A, Diallo M, Weaver S, Hanley K. Potential for Zika virus to establish a sylvatic transmission cycle in the Americas. bioRxiv. 2016;47175.
24. Li MI, Wong PSJ, Ng LC, Tan CH, Turell MJ, Oral Susceptibility of Singapore Aedes (Stegomyia) aegypti (Linnaeus) to Zika Virus. PLoS Negl Trop Dis. 2012Aug28;6(8):e1792. doi: 10.1371/journal.pntd.000179222953014
25. Grard G, Caron M, Mombo IM, Nkoghe D, Mboui Ondo S, Jiolle D, Charrel R, et al. Zika Virus in Gabon (Central Africa)– 2007: A New Threat from Aedes albopictus?PLoS Negl Trop Dis. 2014Feb6;8(2):e2681. doi: 10.1371/journal.pntd.000268124516683
26. Wong P-SJ, Li MI, Chong C-S, Ng L-C, Tan C-H, Aedes (Stegomyia) albopictus (Skuse): A Potential Vector of Zika Virus in Singapore. PLoS Negl Trop Dis. 2013Aug1;7(8):e2348. doi: 10.1371/journal.pntd.000234823936579
27. Mordecai E, Cohen J, Evans MV, Gudapati P, Johnson LR, Miazgowicz K, et al. Temperature determines Zika, dengue and chikungunya transmission potential in the Americas. bioRxiv. 2016 Jul 15;63735.
28. Hales DS, de Wet N, Maindonald J, Woodward A, Potential effect of population and climate change on global distribution of dengue fever: an empirical model. The Lancet [Internet]. 2002Sep14;360(9336). http://www.sciencedirect.com/science/article/pii/S0140673602099646
29. Paz S, Semenza JC, El Niño and climate change—contributing factors in the dispersal of Zika virus in the Americas?The Lancet. 2016Feb;387(10020):745.
30. Stewart Ibarra AM, Ryan SJ, Beltrán E, Mejía R, Silva M, Muñoz Á, Dengue Vector Dynamics (Aedes aegypti) Influenced by Climate and Social Factors in Ecuador: Implications for Targeted Control. 2013Nov;8(11). doi: 10.1371/journal.pone.007826324324542
31. Foote RH. Aedes Aegypti (L.), the Yellow Fever Mosquito. Its life history, bionomics, and structure. Sir S. Rickard Christophers. Cambridge University Press, New York, 1960. xii + 739 pp. Illus. $14.50. Science. 1961 May 12;133(3463):1473–4.
32. World Health OrganizationInternational Travel and Health. World Health Organization; 2009. 251 p.
33. Guzzetta G, Poletti P, Montarsi F, Baldacchino F, Capelli G, Rizzoli A, et al. Assessing the potential risk of Zika virus epidemics in temperate areas with established Aedes albopictus populations. Eurosurveillance [Internet]. 2016Apr14 [cited 2016 Jun 24];21(15). http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=21446
34. 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. 2013May;50(3):467–78. 23802440
35. Cox J, Grillet ME, Ramos OM, Amador M, Barrera R, Habitat Segregation of Dengue Vectors Along an Urban Environmental Gradient. Am J Trop Med Hyg. 2007May1;76(5):820–6. 17488898
36. da Rocha Taranto MF, Pessanha JEM, dos Santos M, dos Santos Pereira Andrade AC, Camargos VN, Alves SN, et al. Dengue outbreaks in Divinopolis, south-eastern Brazil and the geographic and climatic distribution of Aedes albopictus and Aedes aegypti in 2011–2012. Trop Med Int Health. 2015Jan1;20(1):77–88. doi: 10.1111/tmi.1240225328988
37. Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JRC, Dobson AP, et al. Epidemic Dynamics at the Human-Animal Interface. Science. 2009Dec4;326(5958):1362–7. doi: 10.1126/science.117734519965751
38. Pinto N, Lasky J, Bueno R, Keitt TH, Galetti M, Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB, Primate Densities in the Atlantic Forest of~Southeast Brazil: The Role of Habitat Quality and Anthropogenic Disturbance. In: South American Primates [Internet]. New York, NY: Springer New York; 2009 [cited 2016 Jul 2]. p. 413–31. http://link.springer.com/10.1007/978-0-387-78705-3_16
39. Macdonald DW, Primates. New York: Torstar Books; 1985. 160 p. (All the world’s animals).
40. McCrae AWR, Kirya BG, Yellow fever and Zika virus epizootics and enzootics in Uganda. Trans R Soc Trop Med Hyg. 1982Jan1;76(4):552–62. 6304948
41. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, et al. Sylvatic transmission of arboviruses among Bornean orangutans. Am J Trop Med Hyg. 2001May1;64(5):310–6.
42. Darwish MA, Hoogstraal H, Roberts TJ, Ahmed IP, Omar F, A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan. Trans R Soc Trop Med Hyg. 1983Jan1;77(4):442–5. 6314612
43. Johnson BK, Chanas AC, Shockley P, Squires EJ, Gardner P, Wallace C, et al. Arbovirus isolations from, and serological studies on, wild and domestic vertebrates from Kano Plain, Kenya. Trans R Soc Trop Med Hyg. 1977;71(6):512–7. 605465
44. Favoretto S, Araujo D, Oliveira D, Duarte N, Mesquita F, Zanotto P, et al. First detection of Zika virus in neotropical primates in Brazil: a possible new reservoir. bioRxiv. 2016 Apr 20;49395.
45. Mis M. Zika, dengue fever pose “immediate threat” in quake-hit Ecuador-charity. Reuters [Internet]. 2016 Apr 21 [cited 2016 Jul 8]; http://www.reuters.com/article/us-ecuador-quake-disease-idUSKCN0XI1MJ
46. Watson JT, Gayer M, Connolly MA, Epidemics after Natural Disasters. Emerg Infect Dis. 2007Jan;13(1):1–5. doi: 10.3201/eid1301.06077917370508
47. Poverty Analysis—Brazil: A Poverty Assessment [Internet]. [cited 2016 Jul 10]. http://web.worldbank.org/WBSITE/EXTERNAL/TOPICS/EXTPOVERTY/EXTPA/0,,contentMDK:20206734~menuPK:443285~pagePK:148956~piPK:216618~theSitePK:430367,00.html
48. Yellow Fever—Timelines—History of Vaccines [Internet]. [cited 2016 Jul 3]. http://www.historyofvaccines.org/timeline
49. Gubler DJ, Prevention and control of Aedes aegypti-borne diseases: lesson learned from past successes and failures. AsPac J Mol Biol Biotechnol. 2011;19(3):111–114.
50. Severo OP. Eradication of the Aedes aegypti Mosquito from the Americas. 1955 [cited 2016 Jul 3]; http://jdc.jefferson.edu/cgi/viewcontent.cgi?article=1008&context=yellow_fever_symposium
51. Araújo HR, Carvalho DO, Ioshino RS, Costa-da-Silva AL, Capurro ML, Aedes aegypti control strategies in Brazil: incorporation of new technologies to overcome the persistence of dengue epidemics. Insects. 2015;6(2):576–594. doi: 10.3390/insects602057626463204
52. Benelli G, Mehlhorn H, Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitol Res. 2016Mar2;115(5):1747–54. doi: 10.1007/s00436-016-4971-z26932263
53. Alphey L, Genetic Control of Mosquitoes. Annu Rev Entomol. 2014;59(1):205–24.
54. 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 [Internet]. 2015Jul2 [cited 2016 Feb 26];9(7). http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4489809/
55. Insituto Brasileiro de Geografia e Estatistica. 2010 Census: 11.4 million Brazilians (6.0%) live in subnormal agglomerates [Internet]. 2011 [cited 2016 Jul 10]. http://censo2010.ibge.gov.br/en/noticias-censo.html?view=noticia&id=1&idnoticia=2057&busca=1&t=2010-census-11-4-million-brazilians-6-0-live-in-subnormal-agglomerates
56. Heller L, Rezende S, Cairncross S, Water and sanitation in Brazil: the public–private pendulum. Instatution Civ Eng Proc. 2015Aug5;0(ME000):1–9.
57. Biller D. Brazil’s Unemployment Jumps in 2015, Adding to Rousseff’s Woes [Internet]. Bloomberg.com. 2016 [cited 2016 Jul 10]. http://www.bloomberg.com/news/articles/2016-03-15/brazil-s-unemployment-jumps-in-2015-adding-to-rousseff-s-woes
58. Wesolowski A, Qureshi T, Boni MF, Sundsøy PR, Johansson MA, Rasheed SB, et al. Impact of human mobility on the emergence of dengue epidemics in Pakistan. Proc Natl Acad Sci. 2015Sep22;112(38):11887–92. doi: 10.1073/pnas.150496411226351662
59. Stoddard ST, Forshey BM, Morrison AC, Paz-Soldan VA, Vazquez-Prokopec GM, Astete H, et al. House-to-house human movement drives dengue virus transmission. Proc Natl Acad Sci. 2013Jan15;110(3):994–9. doi: 10.1073/pnas.121334911023277539
60. Bogoch II, Brady OJ, Kraemer MUG, German M, Creatore MI, Kulkarni MA, et al. Anticipating the international spread of Zika virus from Brazil. The Lancet. 2016Jan29;387(10016):335–6.
61. Mangili A, Gendreau MA, Transmission of infectious diseases during commercial air travel. The Lancet. 2005Mar18;365(9463):989–96.
62. Bogoch II, Creatore MI, Cetron MS, Brownstein JS, Pesik N, Miniota J, et al. Assessment of the potential for international dissemination of Ebola virus via commercial air travel during the 2014 west African outbreak. The Lancet. 2015Jan9;385(9962):29–35.
63. Jones C, Air travel demand projected to double in 20 years [Internet]. USA TODAY. 2015 [cited 2016 May 3]. http://www.usatoday.com/story/travel/flights/2015/06/08/demand-to-fly-will-likely-double-but-industry-may-not-be-ready/28680637/
64. Pan American Health Organization / World Health Organization. Zika Epidemiological Update, 28 April 2016. Washington, D.C.: PAHO/WHO; 2016 Apr.
65. Prisant N, Bujan L, Benichou H, Hayot P-H, Pavili L, Lurel S, et al. Zika virus in the female genital tract. Lancet Infect Dis [Internet]. 2016Jul [cited 2016 Jul 13]; http://linkinghub.elsevier.com/retrieve/pii/S1473309916301931
66. World Health OrganizationWHO | Zika virus outbreak global response [Internet]. WHO. 2016 [cited 2016 Jul 8]. http://www.who.int/emergencies/zika-virus/response/en/
67. Harger N. Cultural Approaches to Pediatric Palliative Care in Central Massachusetts [Internet]. 2014 [cited 2016 Apr 19]. http://libraryguides.umassmed.edu/content.php?pid=94770&sid=1101080
68. Archibald C, Cultural Tailoring for an Afro-Caribbean Community: A Naturalistic Approach. J Cult Divers. 2011;18(4):114–9. 22288207
69. Nasci RS, Movement of Chikungunya Virus into the Western Hemisphere. Emerg Infect Dis. 2014Aug;20(8):1394–5. doi: 10.3201/eid2008.14033325061832
70. Wesselhoeft C, Rubella (German Measles). N Engl J Med. 1947Jun26;236(26):978–88. doi: 10.1056/NEJM19470626236260520248435
71. Sandy M. Brazilian Legislators Look to Increase Abortion Penalties in the Wake of Zika Outbreak. Time [Internet]. 2016 Feb 22 [cited 2016 Apr 19]; http://time.com/4230975/brazil-abortion-laws-zika-outbreak/
72. Most Brazilians are against gay marriage, abortion and legalization of marijuana: Ibope poll also shows that most of the population is in favor of maintaining the Bolsa Família. O Globo [Internet]. 2014 Sep 3 [cited 2016 May 1]; http://oglobo.globo.com/brasil/maior-parte-dos-brasileiros-contra-casamento-gay-aborto-legalizacao-da-maconha-13821047
73. San Martin. Pope Francis signals openness to birth control for Zika virus. Crux: Takeing the Catholic Pulse [Internet]. 2016 Feb 18 [cited 2016 Apr 30]; http://www.cruxnow.com/church/2016/02/18/francis-signals-openness-to-birth-control-for-zika-virus/
74. Mohney G, Moran T. Pope Calls Contraception “Lesser of Two Evils” During Zika Outbreak [Internet]. ABC News. 2016 [cited 2016 Apr 30]. http://abcnews.go.com/Health/pope-francis-contraception-lesser-evils-zika-virus-outbreak/story?id=37026017
75. Cabezas J. El Salvador urges against pregnancies until 2018 as Zika virus spreads. Reuters [Internet]. 2016 Jan 21 [cited 2016 May 5]; http://www.reuters.com/article/us-health-zika-el-salvador-idUSKCN0UZ2SP
76. Sedgh G, Singh S, Hussain R, Intended and Unintended Pregnancies Worldwide in 2012 and Recent Trends. Stud Fam Plann. 2014Sep1;45(3):301–14. doi: 10.1111/j.1728-4465.2014.00393.x25207494
77. Understanding and Addressing Violence Against Women: Sexual Violence [Internet]. World Health Organization; 2012. http://apps.who.int/iris/bitstream/10665/77434/1/WHO_RHR_12.37_eng.pdf
78. Katz JM. The dilemma of Zika: Pregnancy warnings rise in a region lacking contraception [Internet]. STAT. 2016 [cited 2016 Apr 30]. https://www.statnews.com/2016/02/01/zika-pregnancy-warnings-latin-america/
79. Tabatabaei SM, Metanat M, Mass Gatherings and Infectious Diseases Epidemiology and Surveillance. Int J Infect [Internet]. 2015Apr25 [cited 2016 Jul 25];2(2). http://www.intjinfection.com/?page=article&article_id=22833
80. Burattini MN, Coutinho F a. B, Lopez LF, Ximenes R, Quam M, Wilder-Smith A, et al. Potential exposure to Zika virus for foreign tourists during the 2016 Carnival and Olympic Games in Rio de Janeiro, Brazil. Epidemiol Infect. 2016Jul;144(9):1904–1906. doi: 10.1017/S095026881600064927040593
81. Grills A, Morrison S, Nelson B, Miniota J, Watts A, Cetron MS, Projected Zika Virus Importation and Subsequent Ongoing Transmission after Travel to the 2016 Olympic and Paralympic Games—Country-Specific Assessment, July 2016. MMWR Morb Mortal Wkly Rep [Internet]. 2016Jul13 [cited 2016 Jul 14];65(28). http://www.cdc.gov/mmwr/volumes/65/wr/mm6528e1.htm
82. Tavernise S. No Zika Cases Reported During Rio Olympics, W.H.O. Says. The New York Times [Internet]. 2016 Sep 2 [cited 2016 Sep 20]; http://www.nytimes.com/2016/09/03/health/zika-rio-olympics.html