Dengue fever is a mosquito-borne viral illness that causes an estimated 96 million new apparent (symptomatic) infections per year worldwide, with 16 million infections in the Americas annually [1
]. Dengue increased in geographic distribution and incidence in recent decades [3
]. Dengue infections typically present with febrile symptoms, and, although rare, severe cases of dengue can be fatal, resulting in an estimated 20,000 deaths per year worldwide [4
]. Recently, Bhatt and colleagues [1
] estimated an additional 294 million inapparent cases occurred in 2010, where individuals either experienced mild symptoms or were asymptomatic. These individuals would not have been detected by regular public health surveillance and, therefore, represent a large potential infection reservoir. The impact of these individuals is important to consider when assessing social and ecological (socio-ecological) factors associated with dengue risk and mosquito vector presence.
The dengue virus (DENV, family Flaviviridae
, genus Flavivirus
) is primarily transmitted by Aedes
spp. mosquitoes. In recent years, new arboviruses transmitted by the same mosquito vectors (Ae. aegypti
and Ae. albopictus
) emerged in the Americas, including the chikungunya (CHIKV) and Zika (ZIKV) viruses [5
]. Mosquito control by the public health sector is the primary means of controlling arbovirus outbreaks in the Americas. Control programs maintained by local health/government offices and organizations typically include fumigation to control adult mosquitoes, larvicide applications, and active mosquito surveillance. Unfortunately, existing vector control efforts are largely unsuccessful at preventing epidemics. Furthermore, abatement programs that rely heavily on chemical control methods are also problematic due to the rise of insecticide resistance in Aedes
]. Emerging insecticide resistance can further drive intervention failure while wasting public health agency resources [7
]. New strategies that consider the nuances of socio-ecological conditions and risk factors are urgently needed to inform local targeted control campaigns in the context of household-level strategies and behaviors.
In Ecuador, dengue is transmitted primarily by the Ae. aegypti
mosquito vector, an urbanized anthropophilic mosquito. The dengue virus and Ae. aegypti
were eradicated on mainland Ecuador in the 1950s through successful dichlorodiphenyltrichloroethane (DDT) campaigns [8
]. Following drastic reductions in vector control programs and rapid, uncontrolled urbanization in the 1970s and 1980s, dengue re-emerged in Ecuador in 1989; by the early 2000s, all four dengue virus serotypes co-circulated in the coastal lowland mainland region [9
]. The primary means of preventing dengue transmission in Ecuador is through vector control, by reducing the density of Ae. aegypti
in high-risk households, since a dengue vaccine is not yet available for widespread use. Dengue control is conducted by the Ministry of Health, using repeated cycles of ultra-low-volume fumigation of neighborhoods throughout the rainy (peak transmission) season, and indoor residual spraying in and around homes with suspected dengue cases. The Ministry of Health also conducts routine visits to homes to apply larvicide (temefos/abate) to water-bearing containers and destroys larval habitat in and around homes.
Dengue emerged on the Galápagos Islands of Ecuador in the early 2000s [12
]. Islands are valuable epidemiological study locations as they can be used to study outbreaks of disease in relative isolation. This approach also allows for the identification of socio-ecological factors associated with disease transmission. Dengue was also found on the relatively isolated Easter Island of Chile and the Hawaiian Islands of the United States. These islands are ideal case studies for measuring the response of disease transmission to local factors without regional influences [13
The Galápagos Islands of Ecuador, a World Heritage Site, are located 1000 kilometers from the mainland (Figure 1
). The islands are renowned for their biodiversity due to their relative isolation and minimal impact by people, who first settled on the islands in the mid-1800s [14
]. In recent decades, the population increased rapidly, from 1346 people in 1950 [14
] to 30,890 people residing on four islands in 2017 [15
]. Tourism is the most important economic activity [14
], with 215,691 tourists visiting the islands in 2014 [16
]. Invasive species introduced to the islands through human activity are recognized as a serious threat to endemic species on the islands [17
]. The introduction of pathogens is an additional concern, but previous work focused primarily on pathogen impact on native animals (e.g., West Nile virus risk to an endemic bird species [18
]). Less attention is paid to emerging pathogens in humans.
The central vector control team for the Galápagos is based in Puerto Ayora, due to the greater burden of disease, and a smaller team is based in Puerto Baquerizo Moreno. Household-level Ae. aegypti control interventions require significant investment of resources including financial resources, personnel, field transportation, chemicals, and material supplies. The Ministry of Health in the Galápagos engages in multisectoral collaborations for dengue prevention, including dengue education in local schools in partnership with the Ministry of Education, and community clean-up campaigns with private institutions and non-profit organizations.
The aim of our study was to identify socio-ecological factors that were associated with an increased risk of dengue fever transmission and Ae. aegypti
presence in households of Puerto Ayora and Puerto Baquerizo Moreno of the Galápagos Islands. To our knowledge, this is the first report on dengue fever risk in the Galápagos Islands. Prior studies in other Latin American locations showed that risk factors such as water storage practices, knowledge and risk perception, human movement patterns, and housing conditions influence vector abundance and risk of dengue infection [21
]. Identifying household-level risk factors for dengue transmission in the Galápagos would, therefore, provide specific targets for public health interventions on the islands.
We interviewed the head of house of 100 households, where PA households (n = 50) represented 196 household members, and PB households (n = 50) represented 194 household members. At the household level, prior dengue infections were reported by more households in PB (28%) than in PA (20%), although the difference was not significant (p > 0.05, chi-square test). Most people on both islands reported seeking medical care when ill with suspected dengue (PA = 64%, PB = 78%, p > 0.05, Fisher’s exact test).
Water-bearing containers (n
= 248) were inspected for the presence of Ae. aegypti
(PA = 119, PB = 129). Significantly more houses were found to have containers with juvenile Ae. aegypti
in PB than in PA (p
= 0.012, Table 2
). The house index (number of homes with juvenile Ae. aegypti
per 100 homes) was 20 in PB and 6 in PA (Table 2
). The Breteau index (number of containers with juvenile Ae. aegypti
per 100 homes) was 26 in PB and 6 in PA (Table 2
). A greater proportion of surveyed containers were found with Ae. aegypti
juveniles in PB than in PA (p
= 0.019). The predominant characteristics of containers positive for juvenile Ae. aegypti
= 16) were low water tanks made of cement or plastic (92%), containers that were completely or partially uncovered (92%), containers located outdoors (85%), containers that were shaded (85%), containers filled with tap water as opposed to rain water (100%), and containers intended for domestic use (i.e., used for cooking, cleaning, and laundry, as opposed to abandoned containers) (77%). Very few houses on either island had adult Ae. aegypti
present (PA = 2, PB = 7).
3.1. Risk Perceptions and Practices
Most households in PA (82%) and PB (94%) reported that dengue was a serious problem in their community (p
= 0.1) and a severe disease (PA = 86%, PB = 98%, p
= 0.06) (Table 1
). Significantly more PB households reported that it was difficult or impossible to prevent dengue (p
= 0.02, Table 1
). The majority of heads of households knew that dengue was transmitted by a mosquito (94% on both islands), and most people had received information about dengue prevention from multiple sources. However, few people had participated in dengue prevention campaigns (PA = 12%, PB = 10%). Sources of dengue information were similar between islands, with media (television, newspaper, radio) as the primary source of information on both islands, and social networks as the least likely source of information (Table 1
Overall, PB households implemented more prevention strategies than PA households (PA mean = 1.48, SD = 0.76, PB mean = 3.76, SD = 2.09, p
< 0.001). PB households reported several prevention strategies significantly more frequently than PA households, including use of screens on windows and doors (p
< 0.001), topical repellent (p
= 0.03), keeping the property clear of trash (p
= 0.02), closing windows and doors (p
< 0.001), cutting grass and plants (p
= 0.01), adding chemicals to standing water (p
= 0.004), and eliminating standing water (p
< 0.001) (Table 1
). Fumigation and use of mosquito nets were the least commonly reported mosquito control actions in both locations.
3.2. Model Selection Outcomes
The top-ranked model of a prior self-reported case of dengue in the household (AICc = 70.04, κ = 12.52) included the following suite of positively associated variables: the number of people per room in the home, the head of the household earning more than minimum wage, household members who travel between islands, frequent interruptions in the piped water supply, waste water disposal by a sewage system, and being aware of dengue cases in their community (Table 3
, Figure 4
). Having the perception that dengue is a serious problem in the community, and visiting other neighborhoods daily were negatively associated with self-reported dengue. Fourteen additional models were found within 2 AICc units of the top model (Supplementary Table S1
The top-ranked model to predict the presence of Ae. aegypti
in and around households (AICc = 60.14, κ = 8.68) included the following positively associated variables: use of mosquito nets in the home, air conditioning, water being piped into and out of the house, and the perception that dengue is a severe and difficult disease to prevent, although this last parameter estimate was unreliable in the model (Table 4
, Figure 4
). Negatively associated variables included covering water containers, using repellants, closing doors and windows, and treating water with chemicals. Eight additional models were found within 2 AICc units of the top model, comprising alternating selections of similar variables to the top model (Supplementary Table S2
This study provides the first insights into the nature of household-level dengue fever risk and Aedes aegypti
presence on the Galápagos Islands of Ecuador, where the disease emerged in the last 20 years. We found several suites of socio-ecological variables that Galápagos residents identified as important factors associated with reported dengue and were associated with mosquito presence (Figure 4
): human movement, demographics, housing characteristics, knowledge and attitudes, and mosquito abatement practices. These findings can be readily interpreted and used to inform the design and implementation of targeted vector control campaigns that reflect the local social-ecological context [22
We found that higher income and education of the head of the household were positively associated with frequent travel by household members and greater awareness of dengue. The role of human movement in dengue transmission was documented in prior studies in Iquitos, Peru [23
]. We also found that self-reported prior dengue infections were associated with housing conditions, dengue awareness, and frequent travel by household members (Figure 4
, Table 3
). Increased general dengue awareness by residents may also inflate self-reported infections. However, we were able to identify many socio-ecological factors that are associated with self-reported dengue infections, as well as Ae. aegypti
presence, which can offer valuable insights for prevention and control.
Greater housing density (people per bedroom) and frequent interruptions in the piped water supply were also indicative of greater dengue risk. These variables likely reflect greater risk of exposure to infectious mosquito bites, due to larval habitat in water storage containers, and increased probability of infectious bites due to human crowding. These findings are consistent with other studies, both on mainland Ecuador [21
] and elsewhere [40
We found several important variables when assessing our model of Ae. aegypti
presence, including housing conditions, dengue risk perception, and prevention practices. We found that homes were more likely to have Ae. aegypti
if they had no screens on windows or doors, if they did not cover water containers, and if they perceived that dengue was difficult to prevent (Figure 4
). These risk factors are consistent with prior studies from Ecuador, Taiwan, and India [22
]. Interventions to address these factors include dengue awareness and community mobilization campaigns [44
], water container covers, and programs to provide low-cost screening to homeowners. Paradoxically, we found that the use of mosquito nets was positively correlated with Ae. aegypti
presence. We believe that this may be the result of a causal reverse in correlation, wherein bed nets are more likely to be used when mosquitoes are perceptibly present. Although Aedes aegypti
have a small range and will bite during the day (in contrast to other mosquito genera such as Anopheles
), suggesting that bed nets are an inappropriate intervention for dengue, another study on the mainland found that bed nets were protective against dengue infections [45
We found that the use of air conditioning was positively associated with Ae. aegypti
presence. This result is counterintuitive, because one would expect homes with air conditioning to have closed windows and subsequently fewer mosquitoes and lower dengue risk, as shown in prior studies [46
]. It is possible that water buildup and puddles created by air conditioning units could create additional mosquito habitat, which would require further investigation. A more comprehensive understanding of air-conditioning practices would provide information on the context in which air-conditioning units are used versus installed. For example, if rooms are only cooled for a few hours a day, and, in the evening, open windows are used to cool houses, an air-conditioning unit would be a false signal of closed-window behavior.
Water access and storage practices were among the most important household risk factors for both of our models for prior dengue infections and the presence of Ae. aegypti
. This result concurs with previous work in mainland Ecuador [22
]. Water access is a serious concern on the Galápagos Islands, which has a limited supply of fresh water [47
]. As a result, many inhabitants store water around the home for daily use [49
], creating the ideal habitat for Ae. aegpyti
juveniles, especially in PB. A recent study on dengue transmission in Barbados, a water-scarce Caribbean island nation, found drought conditions increased the likelihood of dengue outbreaks [50
]. The characteristics of containers positive for juvenile Ae. aegypti
(uncovered water storage containers located outdoors) indicate that community clean-up campaigns focusing on the elimination of rubbish in the patio may have a limited effect on Ae. aegypti
abundance, at least during the cool season, when this study was conducted. The creation of sealed (Aedes
-proof) water storage containers used by households and located outdoors in the patio may be a more effective campaign than current rubbish removal efforts. This result highlights the importance of integrated household water management strategies in regions that are water-scarce and at risk of dengue.
We found differences in self-reported prior dengue infections, vector abundance, prevention strategies, sources of information, and risk perception between PA and PB. This suggests that there may be differences in a number of factors between the islands, including disease burden, community outreach programs, community awareness, and/or access to information between the two islands. The high proportion of homes with juvenile Ae. aegypti in PB indicates that there was significant risk of another dengue outbreak, even during the low-transmission season when this study was conducted. This increased risk is especially concerning due to the remote nature of San Cristobal, and the Galapagos Islands as a whole.
It is likely that prior dengue infections reported from PB households were from the dengue outbreak that occurred in 2010, four years prior to this study, when most of the population was susceptible to dengue infections. The prevalence of past dengue infections self-reported by surveyed households (28%) was higher than the dengue prevalence reported by the Ministry of Health in 2010 (14.1%). The burden of disease during the outbreak was likely higher than reported by the Ministry of Health, since people rarely seek medical care for mild infections, resulting in underreporting by passive surveillance systems [1
]. This discrepancy may also indicate that people are aware of the symptoms, but did not report those symptoms to authorities; thus, we see considerable self-diagnosed, but unreported dengue. A dengue surveillance study conducted in the same year in southern coastal Ecuador found that 32% of people with acute or recent dengue infections reported no dengue-like symptoms, and there were three additional dengue infections in the community for every case reported by the Ministry of Health [5
]. This discrepancy is worth exploring in future work, as it indicates higher potential rates of infection than is informing current policies.
One of the greatest public health challenges observed during this study was the implementation of uniform vector control and surveillance across the four populated islands, which are more than two hours apart by boat. The higher larval indices in PB may be due to less staffing and resources for vector control, since there were fewer total cases reported in PB than PA. Investigating the sources of these inconsistencies could provide insight into how to better mobilize and engage communities to promote the adoption of preventative behaviors across relatively isolated islands at risk from emerging infectious diseases.
The results of our study indicate that very few households are actively engaged in dengue control campaigns, despite the perceived importance and high awareness of the disease. A survey conducted in PA and PB in the same year found that nine out of ten people felt that they were not prepared for a future dengue outbreak, and about one-third of people reported that they were vulnerable to dengue infections (F. Ortega, personal communication). Studies from mainland Ecuador identified factors that influenced people’s willingness to engage in vector control, including social cohesion and leadership, the perceived role of the government versus the community, and the time and financial costs of household vector control [21
]. Future studies that explore barriers to dengue control could be used to inform the development of community-based interventions to reduce the risk of dengue and other Ae. aegypti
transmitted diseases, through strategies such as Communication for Behavioral Impact (COMBI) [44
], which is supported by the Pan American Health Organization (PAHO) and the Ecuadorian government.
The emergence of dengue in the Galápagos Islands has serious implications for the tourism-based economy of the islands. Tourism is an important and substantial source of income for inhabitants of the Galápagos Islands. The risk of disease could discourage tourists from visiting the islands. Furthermore, the high volume of tourists traveling from mainland Ecuador to the islands, particularly tourists passing through the city of Guayaquil, a dengue endemic city, could present a source of reintroduction of the virus to the islands.
Our findings highlight the importance of human movement in determining dengue transmission, particularly on islands where people travel regularly between islands. Individuals with frequent travel to other islands, as well as between the islands and the continent, may be considered to be at higher risk for dengue infection. Previous studies of dengue on islands emphasized the importance of preventing the transmission of dengue from the mainland [55
], as well as reintroduction from surrounding islands [56
]. Prior studies of West Nile virus risk in the Galápagos found that the transportation of infected mosquitoes via airplanes was the most likely means that the virus would be introduced to the islands [18
]. The transmission dynamics between mainland and island populations may be exacerbated by seasonal differences in the epidemiology of travelers [57
], which may support the restriction of travelers during significant outbreaks on the mainland. The recent emergence of chikungunya and Zika viruses highlights the importance of understanding these regional movement and transmission dynamics [58
]. Our findings also suggest the importance of local, community-based movement dynamics in the transmission dynamics of dengue, as was explored in previous studies [23