A social-ecological systems approach to dengue-chikungunya-zika in urban coastal Ecuador

Anna M. Stewart-Ibarra
SUNY Upstate Medical University, USA

Latin America and the Caribbean (LAC) are facing an unprecedented crisis of co-occurring epidemics of dengue fever, chikungunya and zika fever. These febrile viral diseases are transmitted by the urbanized and anthropophilic Aedes aegypti mosquito, which thrives in Latin America, where over 80% of the population live in urban areas (Figure 1). In the absence of effective therapeutics and vaccines, the public health sector is in urgent need of novel surveillance tools, vector control and management strategies to respond to this public health emergency.

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Figure 1. Urbanization is a major driver of Aedes aegypti transmitted diseases in Latin America and the Caribbean. The mosquito vector breeds in containers with standing water around the urban home (Guayaquil, Ecuador). Photo credit: W. Lash-Marshall and A. Stewart-Ibarra.

Over the last three decades the distribution, severity, and incidence of dengue fever have continued to increase, from 16.4 cases per 100,000 in the 1980’s to 71.5 cases per 100,000 from 2000 to 2007 (Brathwaite et al., 2012; San Martin et al., 2010).  Current estimates of apparent dengue fever infection in LAC range from 1.5 million to 13.3 million cases each year (Stanaway et al., 2016; Bhatt et al., 2013). Symptoms range from mild infections (fever, rash, and joint pain), to severe illness resulting in hemorrhage, shock and death (WHO, 2009). In many countries in the Americas, dengue has replaced malaria as the predominant cause of vector-borne febrile illness. The first cases of Chikungunya (CHIKV: family Togaviridae, genus alphavirus) were reported in the Americas in 2013, resulting in approximately 2 million cases to date. Clinical chikungunya infections are similar to mild dengue infections, and are characterized by intense and sometimes chronic joint pain. Zika fever (ZIKV: family Flaviviridae, genus flavivirus) emerged in the Americas in 2015 in Brazil (Zanluca et al., 2015). The region is now experiencing a major epidemic, with 492,820 suspected cases reported from 45 countries and territories (cumulative suspected cases reported through September 1, 2016). On February 1, 2016, the World Health Organization declared a Public Health Emergency of International Concern in response to the neurological and auto immune complications associated with zika infections (e.g., Guillain-Barré syndrome and congenital syndrome in newborns).

Figure 2. Social-ecological factors influencing dengue risk in Latin America. Disease dynamics are influenced by interacting local systems (social, political-institutional, biophysical) that are influenced by external drivers.
Figure 2. Social-ecological factors influencing dengue risk in Latin America. Disease dynamics are influenced by interacting local systems (social, political-institutional, biophysical) that are influenced by external drivers.

Rapidly evolving social and environmental conditions have facilitated the emergence and persistence of these diseases, including unprecedented rates of urban population growth, land use change, atmospheric and climate change, the development of insecticide-resistance, increased movement of humans and vectors, and global and governmental management failure ( Harrus & Baneth, 2005; Pimentel et al., 1998; Pimental et al., 2007; McMichael, 2004; Mayer, 2000) (Figure 2). In response to this complexity, the global health community has proposed integrated disease management strategies, such as the IMS-Dengue, as policy frameworks for managing multiple, interacting social-ecological drivers of diseases. However, implementing these policies on the ground requires knowledge of local social-ecological systems, which in many instances is lacking. The social-ecological systems (SES) approach is a transdisciplinary research framework for understanding disease dynamics (Wilcox & Colwell, 2005; Spiegel et al., 2005; Parkes et al., 2005), focusing on the interactions between biophysical and social systems, and drawing on methodological tools and perspectives from a broad range of disciplines and actors (Table 1). The SES approach is not specific to the field of public health, but rather builds on a conceptual framework developed by ecologists to address natural resource management issues at the interface of “coupled human and natural systems” (Wilcox & Colwell, 2005; Liu et al., 2007; Berkes et al., 2003). The SES approach is complementary to the emerging field of sustainability science, which has called for a renewed focus on the interactions among social, economic, and environmental systems to address the challenge of developing a healthy and sustainable global society (Kates et al., 2001; Rapport, 2007).  The objective of this paper is to describe the SES approach as a framework for studying these diseases, and present examples from our studies of dengue fever, chikungunya and zika in Ecuador.

table-1

The emergence of dengue, chikungunya, and zika in Ecuador.

 In 1988 the first new cases of dengue in the Ecuador were reported from Guayaquil, after no reported transmission since the 1950s.  The emergence of dengue coincided with a period of rapid urbanization, economic policy reform (neoliberalization), and a major recession, leading to the establishment of large peri-urban settlements, which facilitated the reinvasion of the mosquito vector and virus. This pattern of settlement continues today, resulting in many people living in suboptimal housing conditions where they are at greater risk of exposure to infectious mosquito bites. Guayaquil was recently rated one of the most vulnerable cities in Latin America on the basis of poor shelter indicators, including insufficient living area, access to safe water, access to improved sanitation, and access to sewerage (Martinez et al., 2008).

Dengue fever is now hyper-endemic in the tropical coastal lowland region. Over a five year period (2010 to 2014), 72,060 cases of dengue were reported in Ecuador (annual average of 14,412 cases), as compared to 1,138 cases of malaria. The first cases of autochtonous chikungunya cases were reported in Ecuador at the end of 2014, resulting in a major epidemic in 2015, with over 33,000 cases reported. The first cases of zika were confirmed in Ecuador on January 7, 2016, and currently (01 Sept 2016) 2,182 suspected cases of zika have been reported. The true burden of dengue, chikungunya and zika is much higher than the number of reported cases due to a high proportion of asymptomatic or mild cases and limited access to laboratory diagnostics.

An integrated epidemic surveillance platform in Machala, Ecuador

figure-3a

figure-3b
Figure 3. Dengue, chikungunya and zika are urban diseases that cause significant illness in Machala, Ecuador, the site of an integrated surveillance study. Top: A patient with severe dengue has been admitted to the regional hospital in Machala for observation and care. Bottom: A young mother in the urban periphery is concerned because her neighbor was recently diagnosed with dengue. Photo credits: Dany Krom.

In response to the growing burden of dengue, chikungunya and zika, the National Institute of Meteorology and Hydrology (INAMHI), the Ministry of Health (MSP) of Ecuador, and an international team of investigators have co-developed an integrated vector-virus-climate research and surveillance platform in the city of Machala, El Oro Province, Ecuador  (Figure 3). Machala, a port city located in southern coastal Ecuador, is a strategic sentinel surveillance site, due to its location along the Pan American highway near the Peruvian border and the high historical burden of mosquito-borne illness.

This comprehensive surveillance system is generating fine-scale spatiotemporal data on the true burden of dengue, chikungunya and zika illness, and risk factors, including microclimate, virus and vector dynamics, nutrition, and sociodemographics. Results from these and other studies will help to address urgent questions regarding the true burden of zika infections, the immunological implications of multiple flavivirus infections, alternative mosquito vectors and zoonotic hosts capable of transmitting the disease, and the efficacy of new vaccines and therapeutics.

Research Findings

Extreme climate events are linked to disease outbreaks. An analysis of epidemiological records and climate data from El Oro Province revealed that dengue epidemics were associated with warm, rainy El Niño events (Stewart-Ibarra & Lowe, 2013). When sea surface temperatures become anomalously warm, teleconnections between the ocean-atmospheric system result in warming of local air temperatures and an increase in rainfall. Field entomology studies revealed that the most important local climate triggers were minimum temperature and rainfall (Stewart-Ibarra & Lowe, 2013; Stewart-Ibarra et al., 2013). Other recent studies also found that temperature is a key predictor of dengue, zika and chikungunya transmission across Latin America (Mordecai et al., 2016).

figure-4b
Figure 4. On February 26, 2016, over 170 mm of rain fell in the city of Machala, Ecuador, in 10 hours [29], creating climate conditions that were ideal for the proliferation of the Aedes aegypti mosquito. Photo credits: Dany Krom

figure-4aMachala is a low-lying coastal city build on top of mangroves and is highly susceptible to flooding. During El Niño events, the city experiences major flooding, as observed in February 26, 2016, when over 170 mm of rain fell in 10 hours, creating climate conditions that were ideal for the proliferation of the Ae. aegypti mosquito (Figure 4). The timing of the flood coincided with the first cases of zika in the city, reported on February 1, 2016, likely fueling the outbreak in the city. Global climate changes are projected to increase the frequency of extreme El Niño events (Cai et al., 2014), increasing the vulnerability of the population to mosquito-borne disease epidemics.  Investigators on the team have worked to improve the seasonal climate forecasts in the region, generating forecasts with considerable skill (i.e., predictive ability) that could be used in epidemic forecasts (Recalde-Coronell et al., 2014).  The Latin America Observatory (OLE2), a regional network of climate centers, has provided critical technical support and a means of rapidly disseminating climate products and tools, including tailored climate-zika maps that are freely available online.

Multiscalar hotspots of risk in the urban environment. Our studies revealed that dengue risk was highly clustered in high-risk neighborhoods at the city-level (Stewart-Ibarra et al., 2014a; Castillo et al., 2011), and in high risk households at the neighborhood-level (Stewart-Ibarra et al., 2013) (Figure 5). For example, we found that during the rainy season, 82% of Ae. aegypti pupae were collected from 11% of households in the study, and during the dry season, 5% of households containing 80% of pupae collected. The heterogenous distribution of disease risk indicates the potential to develop focalized interventions that target high risk areas or vulnerable populations. Ongoing cluster investigations and cohort studies are providing in-depth information about the true prevalence and spatial distribution of dengue, chikungunya, zika, and chagas (co-) infections in the city.

figure-5
Figure 5. The spatial distribution of dengue transmission in Machala, Ecuador during a major epidemic in 2010: (A) Dengue incidence (cases per 10,000 population in 2010) per neighborhood, and (B) significant hot spots (high-high) and outliers (high-low and low-high) identified through LISA analysis (p ≤0.05). Reproduced with permission from Stewart-Ibarra et al., 2014a.

Social determinants of health. Diseases transmitted by Ae. aegypti are highly sensitive to social determinants of health in the urban environment.  At the household and neighborhood level, risk factors included household water access and storage, demographics of the family, and the condition of the house and patio (Stewart-Ibarra et al., 2013; Stewart-Ibarra et al., 2014a). In focus groups, community members identified 30 interrelated biophysical, political-institutional, and community-household risk factors for dengue including climate (the most important biophysical factor) and access to municipal public services and utilities (e.g., garbage collection, sewerage, piped water), indicating that people conceptualized dengue risk within the broader issues of urban development (Figure 6). People in the urban periphery identified many more risk factors than people in the center, a reflection of the greater health needs of marginalized communities. Gaps in knowledge were also a major risk factor (Stewart-Ibarra et al., 2013; Stewart-Ibarra et al., 2014b; Handel et al., 2016), and studies identified specific misconceptions to be targeted in public health education campaigns.

figure-6
Figure 6. Social-ecological risk factors associated with dengue in Ecuador. Font size indicates the number of focus groups in which the theme emerged (range 1 to 6). Themes that emerged only from the peripheral urban area are in italics; themes only from the central area are underlined. Reproduced with permission from Stewart-Ibarra et al., 2014b.

Conclusion

By applying an SES approach, the team has strengthened local research and surveillance capacities, and generated the evidence base for the effects of climate and other social-ecological risk factors on disease transmission. This initiative has provided the foundation for an epidemic early warning system (EWS) and other decision support tools that improve the ability of decision makers to incorporate social-ecological information into public health planning.

Reducing the burden of diseases transmitted by Ae. aegypti is one of the greatest challenges of our lifetime, especially when faced with the continued growth of urban populations and the increasing frequency of extreme climate events. However, major advances are being made with nanotechnology, such as low-cost point of care diagnostics using iphones (Erickson et al., 2014), and smarter urban planning and design of mosquito-proof housing (Knols et al., 2016). It is also worth noting that the public health sector in El Oro Province was able to effectively eradicate malaria in 2011 through effective intersectoral collaboration, operational research to monitor drug and insecticide-resistance, binational partnerships with the public health sector in Peru, and strong surveillance systems (Krisher et al., in review). These studies indicate the importance of policy-relevant research that can be translated to strengthen the design, implementation, and evaluation of new innovative strategies that reflect local realities. The findings from these studies contribute to a growing body of research in this area, highlighting the value of the social-ecological systems (SES) approach to health.


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Dr. Anna M. Stewart-Ibarra is Assistant Professor of Medicine at the SUNY Upstate Medical Center in Syracuse, New York, USA.
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Header Image: GUAYAQUIL, ECUADOR – OCTOBER – 2015 – People crossing a bridge at the famous Malecon 2000 located at riverfront of the guayas river in the city of Guayaquil in Ecuador.  Credit: DFLC Prints / Shutterstock.com

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