Professional Documents
Culture Documents
3, 393–400
doi: 10.1093/ilar/ilx034
Article
Abstract
Environmental changes have a huge impact on the emergence and reemergence of certain infectious diseases, mostly in
countries with high biodiversity and serious unresolved environmental, social, and economic issues. This article
summarizes the most important findings with special attention to Brazil and diseases of present public health importance
in the country such as Chikungunya, dengue fever, yellow fever, Zika, hantavirus pulmonary syndrome, leptospirosis,
leishmaniasis, and Chagas disease. An extensive literature review revealed a relationship between infectious diseases
outbreaks and climate change events (El Niño, La Niña, heatwaves, droughts, floods, increased temperature, higher rainfall,
and others) or environmental changes (habitat fragmentation, deforestation, urbanization, bushmeat consumption, and
others). To avoid or control outbreaks, integrated surveillance systems and effective outreach programs are essential. Due to
strong global and local influence on emergence of infectious diseases, a more holistic approach is necessary to mitigate or
control them in low-income nations.
Key words: climate change; disease emergence; EIDs; environmental drivers; landscape change; vector-borne diseases;
weather; zoonoses
© The Author(s) 2017. Published by Oxford University Press on behalf of the National Academy of Sciences.
All rights reserved. For permissions, please email: journals.permissions@oup.com
393
394 | Nava et al.
environmental changes, planet Earth has entered a new geologi- and disruption of important ecosystems and ecosystem services
cal epoch termed the Anthropocene (Crutzen and Stoermer 2000). driven by these projects in Brazil may result in the emergence of
Building on the Millennium Ecosystem Assessment definition of infectious diseases in wildlife, domestic animals, and humans in
drivers of ecosystem change (Millennium Ecosystem Assessment the surrounding communities. To develop effective control or
2003), Nelson et al. (2006) define drivers of ecosystem change as mitigation measures, it is necessary to understand the impact
“a complex web of interactions between humans and their sur- these environmental drivers have in the modification of ecologi-
roundings as humans seek to satisfy their basic needs and im- cal processes associated with emerging infectious disease out-
prove their wellbeing.” There are many anthropogenic drivers of breaks, as well as to analyze the impact of specific drivers on
Table 1 Key drivers of environmental changes affecting the emergence and spillover of infectious diseases between wild animals, domestic
animals, and humans globally
El Niño Vector-borne Epstein (1999)a Increasing outbreaks of emerging diseases were linked to El Niño.
Haines and Patz (2004)a Outbreaks and epidemic of malaria positively connected with El
Niño.
Lindsay et al. (2000)a Strikingly less malaria found in El Niño years in Tanzania.
Hjelle and Glass (2000)a Hantavirus cardiopulmonary syndrome found to be related to El
Continued
396 | Nava et al.
Table 1 Continued
Vianna and Ignotti (2013) Hottest months present the highest incidence of dengue in Brazil
Imai et al. (2016) Increased minimum temperature associated with increase in
malaria incidence in Papua New Guinea with differing lag
times according to different regions (local scale)
Barcellos and Lowe (2014) Increase in mean temperature associated with higher incidence
of dengue fever in Brazil
Modified from Wu et al. (2016). Highlighted cells detail incidence of disease emergence or spillover in Brazil.
a
References cited in Wu et al. (2016).
Ebola virus and other zoonotic pathogens. Multiple anthropo- cities in the vicinity of hydroelectric dams. Building dams re-
genic factors can be involved in the emergence of an Ebola quires a large workforce, many of whom remain in the region
virus outbreak through bushmeat consumption (Alexander post construction, which not only dramatically increases the
et al. 2015), deforestation (Fahr et al. 2006), and land use change impact of humans upon the environment but also increases
(Wallace et al. 2014). Bushmeat consumption is also a driver for opportunity for disease spillover (Fearnside 1999; Patz et al.
emerging infectious disease in Brazil (Gonçalves et al. 2012; 2004; Randell 2015; Vaz et al. 2007). The lack of epidemiological
Sangenis et al. 2016). The wildlife trade and especially the pet surveillance and risk assessment prior to the construction of
trade have been heavily implicated as a driver of disease emer- hydroelectric plants increases the exposure of neighboring
gence (Chomel et al. 2007; Gomez and Aguirre 2008; Matias human populations to zoonotic diseases.
et al. 2016; Ripple et al. 2016). The higher incidence of leptospirosis in Brazil has been
The construction of hydroelectric dams has direct and indi- associated with densely populated urban and flooded areas
rect ecological impacts due to massive deforestation, biodiver- (Gracie et al. 2014). Similarly, Zika virus outbreaks in Brazil
sity loss, and socioeconomic changes brought upon local have been associated with urbanization or deforestation, which
communities and surrounding ecosystems (Lees et al. 2016). likely favor the habitat of the mosquito vector (Ali et al. 2017).
Dams and other water control projects have been shown to Hantavirus outbreaks in Brazil also have been linked to
drive disease emergence by providing favorable habitats increased contact rates between rodent reservoirs and humans
increasing vector and host species ranges (Patz et al. 2004). in rapidly urbanizing and deforested rural areas (Pinto Junior
Global evidence of markedly increased incidence of emerging et al. 2014). Yellow fever outbreaks occurred in both Congo and
or reemerging pathogens such as Rift Valley fever (Dzingirai Brazil in 2016 and 2017, respectively, and in both instances the
et al. 2017), schistosomiasis (N’Goran et al. 1997), and malaria virus shifted from forested areas to urban populations, raising
(Tadei et al. 1998) has been correlated with dam construction concerns about effective public health response and sufficient
and the consequent environmental changes. vaccine reserves (Dyer 2017; Ortiz-Martínez et al. 2017). The
Trypanosoma spp., the causative agent for trypanosomiasis, outbreak in Congo was associated with high population mobil-
has been isolated in bats captured near a hydroelectric dam in ity and low vaccination coverage (Otshudiema et al. 2017). In
the Brazilian Amazon (Costa et al. 2016). This discovery indi- Brazil, the outbreak was likely driven by anthropogenic defores-
cates the potential risk of zoonotic spillover to the growing tation and forest fragmentation that isolated and stressed the
ILAR Journal, 2017, Vol. 58, No. 3 | 397
Table 2 Key anthropogenic drivers of environmental changes affecting the emergence and spillover of infectious diseases between wild ani-
mals, domestic animals, and humans in Brazil
Urbanization Contact with rodents or Pinto Junior et al. Increased urbanization and deforestation correlated with exposure to
and Deforestation urine (2014) Hantavirus rodent reservoirs
Gracie et al. (2014) Increased urbanization associated outbreaks of leptospirosis.
Vector-borne Ali et al. (2017) Urbanization and deforestation associated with higher incidences of
reservoir monkey species most likely altered the vector geo- in higher altitudes, leading to geographical expansions or shifts
graphic range (Ortiz-Martínez et al. 2017; Ribeiro and Antunes of disease ranges. An example of this scenario is the association
2009; Rosseto et al. 2017). between inter-annual variability in temperature and malaria
transmission in the African highlands (Bouma 2003). Temperature
and rainfall are the most important abiotic factors affecting
Climate Change and Emerging Infectious
dengue prevalence in Brazil as well as the breeding sites for
Diseases the mosquito vector (Vianna and Ignotti 2013). In other re-
Climate change includes variations in temperature, precipita- gions, increased temperatures result in increased sporulation
tion, wind, and sunshine that may affect the survival, repro- of oocysts and geographic distribution of reservoir hosts for
duction, or distribution of disease pathogens and their hosts Toxoplasma gondii, yielding higher infection rates (Yan et al.
(Wu et al. 2016). According to Patz et al. (2005), correlating the 2016). Increased rainfall also enhances infection rate due to
emergence or increased range of infectious diseases with cli- enhanced oocyst survival.
mate change is still not possible due to a dearth of longitudinal, Some vector-borne diseases including malaria, African try-
quality data sets and sociodemographic factors. Still ample evi- panosomiasis, Lyme disease, tick-borne encephalitis, yellow
dence has shown that climate change results in long-term fever, plague, and dengue fever all have expanded ranges fol-
shifts in weather conditions as well as patterns of extreme lowing increased temperatures (Harvell et al. 2002).
weather events, both of which may threaten human health and Imai et al. (2016) studied both local weather and global
well-being (Aguirre and Tabor 2008; Wu et al. 2016). climate associations with malaria incidence in Papua, New
By providing higher landscape suitability for rodent host re- Guinea and determined that there was an association between
servoirs and increasing human-to-host contact rates, climate minimum temperature and increase in malaria incidence with
change and human population growth are predicted to be the different time lags, according to the region studied. For climate
most important drivers of Lassa virus in western Africa by 2070 indices, the authors described a negative association between
(Redding et al. 2016). West Nile virus (WNV) epidemics have modoki El Niño, El Niño Southern Oscillation and Indian Ocean
increased globally as a result of droughts. In periods with low Dipole indices and malaria incidence with a larger time lag,
rainfall, the rate of infection of the WNV mosquito vector in- suggesting it could have happened due to lower precipitation
creases (Paz 2015). Predictive models have shown a potential and malaria transmission or vice versa.
tripling of WNV cases over the next three decades in areas of Strong correlations between increased temperature and
increased drought and with low human host immunity (Paull dengue fever incidence have been recorded in New Caledonia
et al. 2017). Climate change has also been associated with (Teurlai et al. 2015), Thailand (Watts et al. 1987), and Brazil
increased intensity of droughts and flooding in the Amazon (Barcellos and Lowe 2014). The regional and global increases in
region (Marengo and Espinoza 2015). Higher incidence of cases humidity and temperature lead to increased leishmaniasis vec-
of Chikungunya, WNV, and Zika virus infection in Brazil is tor (Lutzomyia spp.) activity, breeding, and the geographic
associated with areas with more frequent rainfall and severe expansion in Argentina and other regions of the Americas
droughts, since both increase breeding sites for the vectors (Salomón et al. 2012).
Aedes spp. and Culex spp. Modelling efforts have supported future increasing trends in
Temperature change alone, or together with other variable disease emergence driven by climate change. Predictive models
changes such as rainfall, may alter the transmission of dis- for Brazilian Atlantic forest and the Cerrado describe a strong
eases. Temperature affects the spatial–temporal distribution of association between increased risk of Hantavirus pulmonary
disease vectors on both global and regional scales, and as tem- syndrome and changes in socioeconomic, landscape, and weather
perature continues to rise due climate change and greenhouse factors: low Human Development Index, increase in sugarcane
gas emissions, insect vectors in low-latitude regions may cultivation, decreased forest cover, and increased annual mean
expand into novel habitats in mid- or high-latitude regions and temperature (Prist et al. 2016).
398 | Nava et al.
Conclusions Chomel BB, Beloto A, Meslin FX. 2007. Wildlife, exotic pets, and
emerging zoonoses. Emerg Infect Dis 13(1):6–11.
Several studies have described local climate change, disruption
Chretien JP, Anyamba A, Bedno SA, Breiman RF, Sang R, Sergon
of important ecosystems and ecosystem services, large-scale
K, Powers AM, Onyango CO, Small J, Tucker CJ, Linthicum
deforestation, and urbanization as drivers of a wide range of
KJ. 2007. Drought-associated chikungunya emergence along
life-threatening infectious diseases, including hantavirus pul-
coastal East Africa. Am J Trop Med Hyg 76(3):405–407.
monary syndrome, dengue fever, yellow fever, malaria, try-
CIA. 2017. The World Factbook. Washington, DC: Central Intelligence
panosomiasis, leishmaniasis, and leptospirosis in Brazil. There
Agency. Available online (https://www.cia.gov/library/publications/
is strong evidence that some of these environmental changes
Gonçalves AQ, Asasco C, Santos I, Serra PT, Julião GR, Orlandi PP. Loh E, Murray KA, Nava A, Aguirre A, Daszak P. 2016. Evaluating
2012. Calodium hepaticum: Household clustering transmission the links between biodiversity, land-use change, and infec-
and the finding of a source of human spurious infection tious disease emergence in tropical fragmented landscapes.
in a community of the Amazon region. PLoS Negl Trop In: Aguirre A, Sukumar R, eds. Tropical Conservation. New
Dis 6(12):1349. York: Oxford University Press. p 79–88.
Gracie R, Barcellos C, Magalhães M, Souza-Santos R, Barrocas Machalaba C, Daszak P, Karesh WB. 2015. Anthropogenic dri-
PRG. 2014. Geographical scale effects on the analysis of lep- vers of emerging infectious diseases. In: United Nations
tospirosis determinants. Int J Environ Res Public Health 11 Global Sustainable Development Report Briefs 2015.
N, McLean RG, McMichael T, Morse SS, Norris DE, Ostfeld RS, Parmenter R, Yates T. 2008. The effect of habitat fragmenta-
Pearl MC, Pimentel D, Rakototiana L, Randriamanajara O, tion and species diversity loss on hantavirus prevalence
Riach J, Rosenthal JP, Salazar-Sanchez E, Silbergeld E, in Panama. Animal biodiversity and emerging diseases. Ann
Thomson M, Vittor AY, Yameogo L, Zakarov V. 2004. N Y Acad Sci 1149:80–83.
Unhealthy landscapes: Policy recommendations on land use Tadei WP, Scarpassa VM, Thatcher BD, Santos JM, Rafael MS,
change and infectious disease emergence. Environ Health Rodrigues IB. 1998. Ecologic observations on anopheline vec-
Perspect 112(10):1092–1098. tors of malaria in the Brazilian Amazon. Am J Trop Med Hyg
Paull SH, Horton DE, Ashfaq M, Rastogi D, Kramer LD, 59(2):325–335.