A dengue outbreak in a rural community in Northern Coastal Ecuador: An analysis using unmanned aerial vehicle mapping

Gwenyth O Lee, Luis Vasco, Sully Márquez, Julio C Zuniga-Moya, Amanda Van Engen, Jessica Uruchima, Patricio Ponce, William Cevallos, Gabriel Trueba, James Trostle, Veronica J Berrocal, Amy C Morrison, Varsovia Cevallos, Carlos Mena, Josefina Coloma, Joseph N S Eisenberg, Gwenyth O Lee, Luis Vasco, Sully Márquez, Julio C Zuniga-Moya, Amanda Van Engen, Jessica Uruchima, Patricio Ponce, William Cevallos, Gabriel Trueba, James Trostle, Veronica J Berrocal, Amy C Morrison, Varsovia Cevallos, Carlos Mena, Josefina Coloma, Joseph N S Eisenberg

Abstract

Dengue is recognized as a major health issue in large urban tropical cities but is also observed in rural areas. In these environments, physical characteristics of the landscape and sociodemographic factors may influence vector populations at small geographic scales, while prior immunity to the four dengue virus serotypes affects incidence. In 2019, a rural northwestern Ecuadorian community, only accessible by river, experienced a dengue outbreak. The village is 2-3 hours by boat away from the nearest population center and comprises both Afro-Ecuadorian and Indigenous Chachi households. We used multiple data streams to examine spatial risk factors associated with this outbreak, combining maps collected with an unmanned aerial vehicle (UAV), an entomological survey, a community census, and active surveillance of febrile cases. We mapped visible water containers seen in UAV images and calculated both the green-red vegetation index (GRVI) and household proximity to public spaces like schools and meeting areas. To identify risk factors for symptomatic dengue infection, we used mixed-effect logistic regression models to account for the clustering of symptomatic cases within households. We identified 55 dengue cases (9.5% of the population) from 37 households. Cases peaked in June and continued through October. Rural spatial organization helped to explain disease risk. Afro-Ecuadorian (versus Indigenous) households experience more symptomatic dengue (OR = 3.0, 95%CI: 1.3, 6.9). This association was explained by differences in vegetation (measured by GRVI) near the household (OR: 11.3 95% 0.38, 38.0) and proximity to the football field (OR: 13.9, 95% 4.0, 48.4). The integration of UAV mapping with other data streams adds to our understanding of these dynamics.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Map of Ecuador: The approximate…
Fig 1. Map of Ecuador: The approximate location of the study community is indicated by the star.
This map was constructed using shapefiles downloaded from https://data.humdata.org/, which is available under a CC BY-IGO license (https://data.humdata.org/dataset/ecuador-admin-level-2-boundaries).
Fig 2. Community Map.
Fig 2. Community Map.
The study community. 2a. Neighborhoods are coded by the reported ethnicity of the occupants. ‘Field’ represents the football field that represented a spatial risk factor in the outbreak. 2b. The red circle in indicates the part of the community where Ae. Aegypti were identified. For privacy reasons, we do not identify specific households where dengue cases occurred, or where Ae. Aegypti were identified. These maps were constructed de novo by the study team.
Fig 3. Cases identified by reported date…
Fig 3. Cases identified by reported date of fever onset: Cases identified during the 2019 calendar year.
Suspected index cases are represented by triangles, while adjacent cases (one from a person living in a nearby community, and one from a person diagnosed after returning from a trip to the village) are represented by square. From Jan 1st to May 31st, case detection was based on Ministry of Health (MOH) clinical records, from Jun 1st to December 1st, case detection was based of combined MOH and community-based active surveillance.
Fig 4. Outdoor rain barrels: A photo…
Fig 4. Outdoor rain barrels: A photo of an outdoor rain barrel.
Fig 5
Fig 5
UAV images: Larger, outdoor potential larval habitats such as cisterns and rain barrels can be identified from UAV images (Fig 5A and 5B).

References

    1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al.. The global distribution and burden of dengue. Nature. 2013;496: 504–507. doi: 10.1038/nature12060
    1. World Health Organization. Dengue and severe dengue. 2020. [cited 9 Jun 2020]. Available:
    1. Zambrano LI, Rodriguez E, Espinoza-Salvado IA, Rodríguez-Morales AJ. Dengue in Honduras and the Americas: The epidemics are back! Travel Med Infect Dis. 2019;31: 1–4. doi: 10.1016/j.tmaid.2019.07.012
    1. Yoon IK, Getis A, Aldstadt J, Rothman AL, Tannitisupawong D, Koenraadt CJM, et al.. Fine scale spatiotemporal clustering of dengue virus transmission in children and aedes aegypti in rural Thai villages. PLoS Negl Trop Dis. 2012;6. doi: 10.1371/journal.pntd.0001730
    1. Harrington LC, Scott TW, Lerdthusnee K, Coleman RC, Costero A, Clark GG, et al.. Dispersal of the dengue vector Aedes aegypti within and between rural communities. Am J Trop Med Hyg. 2005;72: 209–20. 72/2/209 [pii]
    1. Bhoomiboonchoo P, Gibbons R V., Huang A, Yoon IK, Buddhari D, Nisalak A, et al.. The Spatial Dynamics of Dengue Virus in Kamphaeng Phet, Thailand. PLoS Negl Trop Dis. 2014;8: 6–11. doi: 10.1371/journal.pntd.0003138
    1. Guo C, Zhou Z, Wen Z, Liu Y, Zeng C, Xiao D, et al.. Global epidemiology of dengue outbreaks in 1990–2015: A systematic review and meta-analysis. Front Cell Infect Microbiol. 2017;7: 1–11. doi: 10.3389/fcimb.2017.00001
    1. Schmidt WP, Suzuki M, Thiem V, White RG, Tsuzuki A, Yoshida LM, et al.. Population density, water supply, and the risk of dengue fever in vietnam: Cohort study and spatial analysis. PLoS Med. 2011;8. doi: 10.1371/journal.pmed.1001082
    1. Tsuda Y, Suwonkerd W, Chawprom S, Prajakwong S, Takagi M. Different spatial distribution of Aedes aegypti and Aedes albopictus along an urban-rural gradient and the relating environmental factors examined in three villages in northern Thailand. J Am Mosq Control Assoc. 2006;22: 222–228. doi: 10.2987/8756-971X(2006)22[222:DSDOAA];2
    1. Getis A, Morrison AC, Gray K, Scott TW. Characteristics of the spatial pattern of the dengue vector, Aedes aegypti, in Iquitos, Peru. Am J Trop Med Hyg. 2003;69: 494–505. doi: 10.1007/978-3-642-01976-0
    1. Haddawy P, Wettayakorn P, Nonthaleerak B, Su Yin M, Wiratsudakul A, Schöning J, et al.. Large scale detailed mapping of dengue vector breeding sites using street view images. PLoS Negl Trop Dis. 2019;13: 1–27. doi: 10.1371/journal.pntd.0007555
    1. Carrasco-Escobar G, Manrique E, Ruiz-Cabrejos J, Saavedra M, Alava F, Bickersmith S, et al.. High-accuracy detection of malaria vector larval habitats using drone-based multispectral imagery. PLoS Negl Trop Dis. 2019;13: 1–24. doi: 10.1371/journal.pntd.0007105
    1. Hardy A, Makame M, Cross D, Majambere S, Msellem M. Using low-cost drones to map malaria vector habitats. Parasites and Vectors. 2017;10: 1–13. doi: 10.1186/s13071-016-1943-1
    1. Milligan B. Making terrains: Surveying, drones and media ecology. J Landsc Archit. 2019;14: 20–35. doi: 10.1080/18626033.2019.1673565
    1. Amarasinghe A, Suduwella C, Elvitigala C, Niroshan L, Amaraweera RJ, Gunawardana K, et al.. Poster abstract: A machine learning approach for identifying mosquito breeding sites via drone images. SenSys 2017—Proc 15th ACM Conf Embed Networked Sens Syst. 2017;2017-Janua: 7–8. doi: 10.1145/3131672.3136986
    1. Gomez-Elipe A, Otero A, Van Herp M, Aguirre-Jaime A. Forecasting malaria incidence based on monthly case reports and environmental factors in Karuzi, Burundi, 1997–2003. Malar J. 2007;6: 1–10. doi: 10.1186/1475-2875-6-1
    1. Linthicum KJ, Anyamba A, Tucker CJ, Kelley PW, Myers MF, Peters CJ. Climate and satellite indicators to forecast Rift Valley fever epidemics in Kenya. Science (80-). 1999;285: 397–400. doi: 10.1126/science.285.5426.397
    1. Barredo E, DeGennaro M. Not Just from Blood: Mosquito Nutrient Acquisition from Nectar Sources. Trends Parasitol. 2020;36: 473–484. doi: 10.1016/j.pt.2020.02.003
    1. Little E, Barrera R, Seto KC, Diuk-Wasser M. Co-occurrence patterns of the dengue vector aedes aegypti and aedes mediovitattus, a dengue competent mosquito in Puerto Rico. Ecohealth. 2011;8: 365–375. doi: 10.1007/s10393-011-0708-8
    1. 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. 2007;76: 820–826. doi: 10.4269/ajtmh.2007.76.820
    1. INEC. Fascículo provincial esmeraldas. Resultados del censo de poblacion y vivienda 2010. Fasc Prov Esmeraldas. 2010; 0–7.
    1. Center Rapoport. Forgotten territories, unrealized rights: rural Afro-Ecuadorians and their fight for land, equality, and security. 2009.
    1. Alvarado G, Benavides-Rawson J. From Dengue to Zika: Environmental and Structural Risk Factors for Child and Maternal Health in Costa Rica Among Indigenous and Nonindigenous Peoples. Maternal Death and Pregnancy-Related Morbidity Among Indigenous Women of Mexico and Central America. 2018. pp. 665–682.
    1. Rapoza K. In Ecuador, A Model In How To Protect Indigenous Villages From The Coronavirus. Forbes. 2020.
    1. Ministerio de Salud Publica. Gacetas Vectoriales. [cited 24 May 2021]. Available:
    1. Waggoner JJ, Ballesteros G, Gresh L, Mohamed-Hadley A, Tellez Y, Sahoo MK, et al.. Clinical evaluation of a single-reaction real-time RT-PCR for pan-dengue and chikungunya virus detection. J Clin Virol. 2016;78: 57–61. doi: 10.1016/j.jcv.2016.01.007
    1. Ryan SJ, Lippi CA, Nightingale R, Hamerlinck G, Borbor-Cordova MJ, Cruz B M, et al.. Socio-ecological factors associated with dengue risk and Aedes aegypti presence in the Galápagos Islands, Ecuador. Int J Environ Res Public Health. 2019;16: 1–16. doi: 10.3390/ijerph16050682
    1. Motohka T, Nasahara KN, Oguma H, Tsuchida S. Applicability of Green-Red Vegetation Index for remote sensing of vegetation phenology. Remote Sens. 2010;2: 2369–2387. doi: 10.3390/rs2102369
    1. Schafrick NH, Milbrath MO, Berrocal VJ, Wilson ML, Eisenberg JN. Spatial clustering of Aedes aegypti related to breeding container characteristics in Coastal Ecuador: implications for dengue control. Am J Trop Med Hyg. 2013;89: 758–765. doi: 10.4269/ajtmh.12-0485
    1. . QGIS Geographic Information System. Open Source Geospatial Foundation Project. . 2020.
    1. StataCorp. Stata Statistical Software 15.0. College Station, TX, USA.; 2020.
    1. Sanchez L, Cortinas J, Pelaez O, Gutierrez H, Concepción D, Van Der Stuyft P. Breteau Index threshold levels indicating risk for dengue transmission in areas with low Aedes infestation. Trop Med Int Heal. 2010;15: 173–175. doi: 10.1111/j.1365-3156.2009.02437.x
    1. Salmón-Mulanovich G, Blazes DL, Guezala V MC, Rios Z, Espinoza A, Guevara C, et al.. Individual and Spatial Risk of Dengue Virus Infection in Puerto Maldonado, Peru. Am J Trop Med Hyg. 2018;99: 1440–1450. doi: 10.4269/ajtmh.17-1015
    1. Duong V, Lambrechts L, Paul RE, Ly S, Lay RS, Long KC, et al.. Asymptomatic humans transmit dengue virus to mosquitoes. Proc Natl Acad Sci U S A. 2015;112: 14688–14693. doi: 10.1073/pnas.1508114112
    1. 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 U S A. 2013;110: 994–999. doi: 10.1073/pnas.1213349110
    1. Endy TP, Anderson KB, Nisalak A, Yoon IK, Green S, Rothman AL, et al.. Determinants of inapparent and symptomatic dengue infection in a prospective study of primary school children in Kamphaeng Phet, Thailand. PLoS Negl Trop Dis. 2011;5: e975. doi: 10.1371/journal.pntd.0000975
    1. Yoon IK, Rothman AL, Tannitisupawong D, Srikiatkhachorn A, Jarman RG, Aldstadt J, et al.. Underrecognized mildly symptomatic viremic dengue virus infections in rural thai schools and villages. J Infect Dis. 2012;206: 389–398. doi: 10.1093/infdis/jis357
    1. Balmaseda A, Stettler K, Medialdea-Carrera R, Collado D, Jin X, Zambrana JV, et al.. Antibody-based assay discriminates Zika virus infection from other flaviviruses. Proc Natl Acad Sci U S A. 2017;114: 8384–8389. doi: 10.1073/pnas.1704984114
    1. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A, Bianchi S, et al.. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science (80-). 2016;353: 823–826. doi: 10.1126/science.aaf8505
    1. Mena CF, Arsel M, Pellegrini L, Orta-Martinez M, Fajardo P, Chavez E, et al.. Community-Based Monitoring of Oil Extraction: Lessons Learned in the Ecuadorian Amazon. Soc Nat Resour. 2020;33: 406–417. doi: 10.1080/08941920.2019.1688441

Source: PubMed

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