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

Abstract

Since Zika virus (ZIKV) was detected in Brazil in 2015, it has spread explosively across the Americas and has been linked to increased incidence of microcephaly and Guillain-Barré syndrome (GBS). In one year, it has infected over 500,000 people (suspected and confirmed cases) in 40 countries and territories in the Americas. Along with recent epidemics of dengue (DENV) and chikungunya virus (CHIKV), which are also transmitted by Aedes aegypti and Ae. albopictus mosquitoes, the emergence of ZIKV suggests an ongoing intensification of environmental and social factors that have given rise to a new regime of arbovirus transmission. Here, we review hypotheses and preliminary evidence for the environmental and social changes that have fueled the ZIKV epidemic. Potential drivers include climate variation, land use change, poverty, and human movement. Beyond the direct impact of microcephaly and GBS, the ZIKV epidemic will likely have social ramifications for women's health and economic consequences for tourism and beyond.

Fig 1. ZIKV epidemic dynamics in 2015–2016 across the Americas, in Brazil, and in an Ecuadorian province struck by an earthquake.

(A) Weekly cumulative suspected and confirmed ZIKV cases (see Glossary for case definitions) across countries in the Americas, on a log scale, colored by the total size of the epidemic. (B) Weekly cumulative confirmed ZIKV-linked microcephaly cases (see Glossary for case definitions) in Brazil. (C) Weekly cumulative confirmed autochthonous cases in Manabi province, Ecuador, where a magnitude 7.8 earthquake struck on April 16, 2016 (indicated by the dashed line). Data are from weekly epidemiological reports from the Pan American Health Organization (PAHO), as compiled by the Centers for Disease Control and Prevention Epidemic Prediction Initiative (CDC EPI; https://github.com/cdcepi/zika; accessed 15 July 2016).

Fig 2. Hierarchy of factors that influence ZIKV transmission, illness, and social consequences.

Climate suitability, mosquito abundance, and human–mosquito contact partly determine rates of ZIKV transmission, which causes illness in some cases. Social consequences depend on both actual and perceived risks of illness. Arrows indicate environmental (green) and social (red) changes hypothesized to contribute to the shifting ecology of vector transmission in the Americas. Figure inspired by Plowright et al. [22].

Fig 3. Confirmed ZIKV-linked microcephaly cases in Brazilian states versus percent light and dense forest cover.

The number of confirmed ZIKV-linked microcephaly cases per 100,000 people (as of July 15, 2016) in Brazilian states with (A) light forest cover (r = -0.27) and (B) dense forest cover (r = -0.35) is shown for states that reported one or more cases. For each state, each hectare with >10% and >50% forest cover is added to the forest cover total for light and dense forest cover calculations, respectively. The x-axis shows forest cover as a percentage of total land area, based on light (A) and dense (B) forest calculations. Microcephaly data are from PAHO case reports, as compiled by the CDC EPI. Population sizes by state were retrieved from the 2014 Brazilian Institute of Geography and Statistics (IBGE) report (ftp://ftp.ibge.gov.br/Estimativas_de_Populacao/Estimativas_2014/estimativa_dou_2014.pdf; accessed 7 July 2016). Forest cover data are from http://rainforests.mongabay.com/20brazil.htm (accessed July 7, 2016).

Fig 4. Confirmed ZIKV-linked microcephaly cases in Brazilian states versus per capita GDP (in log10 US Dollars).

The number of confirmed ZIKV-linked microcephaly cases per 100,000 people (as of July 15, 2016) is negatively correlated (Pearson’s correlation coefficient r = -0.64) with per capita GDP for states with one or more cases. Total GDP data were retrieved from the 2012 IBGE report (http://www.ibge.gov.br/english/estatistica/economia/contasregionais/2012/default.shtm; accessed July 7, 2016). Population sizes by state were retrieved from the 2014 IBGE report. Per capita GDP = Total GDP/population size. Microcephaly data are from weekly epidemiological reports from PAHO, as compiled by the CDC EPI.

Fig 5. Search interest for “chikungunya” and “Zika.”

Search interest, relative to the highest search volume between June 2013 and June 2016, for the terms “chikungunya” in St. Martin (A) and “Zika” in Brazil (B). A value of 100 represents the highest search volume recorded in each country within this time period, so direct comparison of relative search volume is possible without controlling for population or the number of Internet users. Gray dashed lines indicate the first cases of laboratory-confirmed CHIKV and ZIKV in the Americas. The orange bold line indicates declaration of a public health emergency of international concern (PHEIC) by WHO. Data are from Google Trends (https://www.google.com/trends/; accessed 5 July 2016).