{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T23:18:25Z","timestamp":1790810305686,"version":"4.1.0"},"reference-count":62,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2018,11,25]],"date-time":"2018-11-25T00:00:00Z","timestamp":1543104000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>El Ni\u00f1o is a quasi-periodic pattern of climate variability and extremes often associated with hazards and disease. While El Ni\u00f1o links to individual diseases have been examined, less is known about the cluster of multi-disease risk referred to as an ecosyndemic, which emerges during extreme events. The objective of this study was to explore a mapping approach to represent the spatial distribution of ecosyndemics in Piura, Peru at the district-level during the first few months of 1998. Using geographic information systems and multivariate analysis, descriptive and analytical methodologies were employed to map disease overlap of 7 climate-sensitive diseases and construct an ecosyndemic index, which was then mapped and applied to another El Ni\u00f1o period as proof of concept. The main findings showed that many districts across Piura faced multi-disease risk over several weeks in the austral summer of 1998. The distribution of ecosyndemics were spatially clustered in western Piura among 11 districts. Furthermore, the ecosydemic index in 1998 when compared to 1983 showed a strong positive correlation, demonstrating the potential utility of the index. The study supports PAHO efforts to develop multi-disease based and interprogrammatic approaches to control and prevention, particularly for climate and poverty-related infections in Latin America and the Caribbean.<\/jats:p>","DOI":"10.3390\/ijerph15122639","type":"journal-article","created":{"date-parts":[[2018,11,26]],"date-time":"2018-11-26T03:24:27Z","timestamp":1543202667000},"page":"2639","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Mapping Multi-Disease Risk during El Ni\u00f1o: An Ecosyndemic Approach"],"prefix":"10.3390","volume":"15","author":[{"given":"Ivan J.","family":"Ram\u00edrez","sequence":"first","affiliation":[{"name":"Department of Geography and Environmental Sciences, University of Colorado Denver, Denver, CO 80217-3364, USA"},{"name":"Consortium for Capacity Building\/Institute for Arctic and Alpine Research, University of Colorado Boulder, Boulder, CO 80309-0450, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jieun","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Geography and GIS, University of Northern Colorado, Greeley, CO 80639, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sue C.","family":"Grady","sequence":"additional","affiliation":[{"name":"Department of Geography, Environment, and Spatial Sciences, Michigan State University, East Lansing, MI 48824, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2018,11,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/s10708-014-9541-2","article-title":"Cholera resurgence in Piura, Peru: Examining climate associations during the 1997\u201398 El Ni\u00f1o","volume":"80","year":"2015","journal-title":"GeoJournal"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/s10393-015-1095-3","article-title":"El Ni\u00f1o, climate and cholera associations in Piura, Peru, 1991\u20132001: A wavelet analysis","volume":"13","author":"Grady","year":"2016","journal-title":"EcoHealth"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/s13753-017-0151-8","article-title":"Understanding the El Ni\u00f1o costero of 2017: The definition problem and challenges of climate forecasting and disaster responses","volume":"8","author":"Briones","year":"2017","journal-title":"Int. J. Disaster Risk Sci."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Glantz, M.H., Naranjo, L., Baudoin, M., and Ram\u00edrez, I.J. (2018). What does it mean to be El Ni\u00f1o Ready?. Atmosphere, 9.","DOI":"10.3390\/atmos9030094"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1007\/s13753-018-0176-7","article-title":"El Ni\u00f1o and the K\u00f6ppen-Geiger classification: A prototype concept and methodology for mapping impacts in Central America and the Circum-Caribbean","volume":"9","author":"Naranjo","year":"2018","journal-title":"Int. J. Disaster Risk Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1007\/s13753-015-0045-6","article-title":"Shades of chaos: Lessons learned about lessons learned about forecasting El Ni\u00f1o and its impacts","volume":"6","author":"Glantz","year":"2015","journal-title":"Int. J. Disaster Risk Sci."},{"key":"ref_7","unstructured":"(2018, January 04). El Ni\u00f1o and Health: A Global Overview\u2014January 2016. Available online: http:\/\/www.who.int\/hac\/crises\/el-Ni\u00f1o\/who_el_Ni\u00f1o_and_health_global_report_21jan2016.pdf?ua=1."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1175\/WCAS-D-12-00032.1","article-title":"Reexamining El Ni\u00f1o and cholera in Peru: A climate affairs approach","volume":"5","author":"Grady","year":"2013","journal-title":"Weather Clim. Soc."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s00484-001-0119-6","article-title":"The El Ni\u00f1o southern oscillation and malaria epidemics in South America","volume":"46","author":"Gagnon","year":"2002","journal-title":"Int. J. Biometeorol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"971","DOI":"10.4269\/ajtmh.12-0478","article-title":"Climate and non-climate drivers of dengue epidemics in Southern Coastal Ecuador","volume":"88","author":"Lowe","year":"2013","journal-title":"Am. J. Trop. Hyg. Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.tmaid.2017.11.003","article-title":"Outbreaks caused by Aedes aegyptis due to El Ni\u00f1o in a coastal area of Peru","volume":"21","author":"Ruiz","year":"2018","journal-title":"Travel Med. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Bertuzzo, E., Azaele, S., Maritan, A., Gatto, M., Rodriguez-Iturbe, I., and Rinaldo, A. (2008). On the space-time evolution of a cholera epidemic. Water Res. Res., 44.","DOI":"10.1029\/2007WR006211"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1098\/rsif.2011.0304","article-title":"Modelling cholera epidemics: The role of waterways, human mobility and sanitation","volume":"9","author":"Mari","year":"2012","journal-title":"J. R. Soc. Interface"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Melillo, J.M., Richmond, T., and Yohe, G.W. (2014). Urban systems, infrastructure, and vulnerability. Climate Change Impacts in the United States: The Third National Climate Assessment, US Global Change Research Program.","DOI":"10.7930\/J0Z31WJ2"},{"key":"ref_15","unstructured":"Pan American Health Organization (PAHO) (2018, September 14). El Nino-Southern Oscillation and Health. Available online: http:\/\/www.who.int\/globalchange\/publications\/factsheets\/el-nino-and-health\/en\/."},{"key":"ref_16","unstructured":"Vargas, C.M., and Cupe, J.A. (2018, June 29). Desastres Naturales Y Prevencion De Enfermedades [Natural Disasters and Prevention of Communicable Diseases]. Available online: http:\/\/www.scielo.org.pe\/scielo.php?script=sci_arttext&pid=S1728-59172017000100001."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"214","DOI":"10.4269\/ajtmh.2005.73.214","article-title":"Use of rainfall and sea surface temperature monitoring for malaria warning in Botswana","volume":"73","author":"Thomson","year":"2005","journal-title":"Am. J. Trop. Hyg. Med."},{"key":"ref_18","first-page":"81","article-title":"Application of geographic information systems and remote sensing technologies for assessing and monitoring malaria risk","volume":"47","author":"Ceccato","year":"2005","journal-title":"Parassitologia"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/1475-2875-8-6","article-title":"The role of ENSO in understanding changes in Colombia\u2019s annual malaria burden by region, 1960\u20132006","volume":"8","author":"Mantilla","year":"2009","journal-title":"Malar. J."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1007\/s11524-007-9171-9","article-title":"Urban environmental health hazards and health equity","volume":"84","author":"Kjellstrom","year":"2007","journal-title":"J. Urban Health"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Crimmins, A., Balbus, J., Gamble, J.L., Beard, C.B., Bell, J.E., Dodgen, D., Eisen, R.J., Fann, N., Hawkins, M.D., and Herring, S.C. (2016). Ch.9: Populations of concern. The Impacts of Climate Change on Human Health in the United States: A Scientific Assessment, Global Change Research Program.","DOI":"10.7930\/J0R49NQX"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1179\/136485906X97372","article-title":"Urbanization and tropical health\u2014Then and now","volume":"100","author":"Utzinger","year":"2006","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1177\/0956247810380141","article-title":"Vulnerability of poor urban coastal communities to flooding in Lagos, Nigeria","volume":"2","author":"Adelekan","year":"2010","journal-title":"Environ. Urban"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"11025","DOI":"10.3390\/ijerph120911025","article-title":"Infectious diseases, urbanization and climate change: Challenges in future China","volume":"12","author":"Tong","year":"2015","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_25","unstructured":"Singer, M. (2009). Introduction to Syndemics: A Critical Systems Approach to Public and Community Health, John Wiley and Sons."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1016\/S0140-6736(17)30003-X","article-title":"Syndemics and the biosocial conception of health","volume":"389","author":"Singer","year":"2017","journal-title":"Lancet"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"98","DOI":"10.5172\/hesr.2013.22.1.98","article-title":"Respiratory health and ecosyndemics in a time of global warming","volume":"22","author":"Singer","year":"2013","journal-title":"Health Soc. Rev."},{"key":"ref_28","unstructured":"Gueri, A. (2018, January 04). Lessons Learned: Health Effects of El Ni\u00f1o in Peru. Available online: http:\/\/helid.digicollection.org\/en\/d\/Jdi019e\/2.html."},{"key":"ref_29","unstructured":"Sandoval, P.S. (1999). Evaluaci\u00f3n De Da\u00f1os Y Acciones Del Fen\u00f3meno El Ni\u00f1o (Evaluation of Damages Caused by the El Ni\u00f1o Phenomenon and Actions Taken), Oficina de Planificaci\u00f3n, Direcci\u00f3n de Salud Regional (Planning Office, Regional Health Post). (In Spanish)."},{"key":"ref_30","unstructured":"Ministerio de Salud en Piura [Ministry of Health] (MINSA) (2001). Enfermedades Emergentes\u2014Reemergentes Y Modificaciones en El Perfil Epidemiologico Del Noroeste Peruano Post Fenomeno El Ni\u00f1o. [Emerging and Reemerging Diseases and Impacts on Epidemiology in Northern Peru, Post-El Ni\u00f1o], MINSA. (In Spanish)."},{"key":"ref_31","unstructured":"Lluvia e Inundaciones en Peru (2017, June 06). Reporte De Situation [Rains and Floods in Peru. Situation Report]. (In Spanish)."},{"key":"ref_32","unstructured":"Cromley, E.K., and McLafferty, S.L. (2003). GIS and Public Health, Guilford Press."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1080\/19475683.2015.1008572","article-title":"Disease cluster detection methods: Recent developments and public health implications","volume":"21","author":"Mclafferty","year":"2015","journal-title":"Ann. GIS"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Ehrenberg, J.P., and Ault, S.K. (2005). Neglected diseases of neglected populations: Thinking to reshape the determinants of health in Latin America and the Caribbean. BMC Public Health, 5.","DOI":"10.1186\/1471-2458-5-119"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Hotez, P.J., Bottazzi, M.E., Franco-Paredes, C., Ault, S.K., and Periago, M.R. (2008). The neglected tropical diseases of Latin America and the Caribbean: A review of disease burden and distribution and a roadmap for control and elimination. PLOS Neglected Trop. Dis., 2.","DOI":"10.1371\/journal.pntd.0000300"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Schneider, M.C., Aguilera, X.P., da Silva Junior, J.B., Ault, S.K., Najera, P., Martinez, J., Requejo, R., Nichols, R.S., Yadon, Z., and Silva, J.C. (2011). Elimination of neglected diseases in Latin America and the Caribbean: A mapping of selected diseases. PLOS Neglected Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0000964"},{"key":"ref_37","unstructured":"United Nations Development Programme (UNDP) (2018, June 29). Human Development Index. Available online: http:\/\/hdr.undp.org\/en\/content\/human-development-index-hdi."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1111\/1540-6237.8402002","article-title":"Social vulnerability to environmental hazards","volume":"84","author":"Cutter","year":"2003","journal-title":"Soc. Sci. Q."},{"key":"ref_39","unstructured":"Instituto Nacional de Estad\u00edstica e Inform\u00e1tica (National Institute for Statistics and Information, Peru) (INEI) (2017, October 05). Necesidades Basicas Insatisfechas (Basic Needs Unmet). (In Spanish)."},{"key":"ref_40","unstructured":"Organization for Economic Co-operation and Development (OECD) (2018, June 29). Handbook for constructing composite indicators: methodology and user guide. Available online: https:\/\/www.oecd.org\/sdd\/42495745.pdf."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s11069-012-0152-2","article-title":"Social vulnerability indices: A comparative assessment using uncertainty and sensitivity analysis","volume":"63","author":"Tate","year":"2012","journal-title":"Nat. Hazards"},{"key":"ref_42","first-page":"67","article-title":"Methods for constructing composite indices: One for all or all for one?","volume":"67","author":"Mazziota","year":"2013","journal-title":"Riv. Ital. Econ. Demogr. Stat."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3354\/cr00808","article-title":"Public health vulnerability to climate change in Brazil","volume":"40","author":"Confalonieri","year":"2009","journal-title":"Clim. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/j.dendro.2005.05.002","article-title":"\u201cEl Ni\u00f1o\u201d events recorded in dry-forest species of the lowlands of northwest Peru","volume":"22","author":"Rodriguez","year":"2005","journal-title":"Dendrochronologia"},{"key":"ref_45","unstructured":"INEI (2000). Encuesta Demogr\u00e1fica y de Salud Familiar 2000 (Study of Family Demography and Health 2000), INEI. (In Spanish)."},{"key":"ref_46","unstructured":"(2017, December 03). Monthly Atmospheric and SST Indices, Available online: http:\/\/www.cpc.ncep.noaa.gov\/data\/indices\/."},{"key":"ref_47","unstructured":"INEI (1995). Impacto Del Fenomeno Del Ni\u00f1o Durante 1982\/83 en El Departamento De Piura (Impact from the 1982\u201383 El Ni\u00f1o in the Department of Piura), INEI. (In Spanish)."},{"key":"ref_48","unstructured":"INEI (2018, June 01). Censo Nacionales 1993 (National Census 1993). (In Spanish)."},{"key":"ref_49","unstructured":"(1998). Fenomeno Del El Ni\u00f1o 1998: Empradonamiento De La Poblacion Residents en Areas Afectadas Por El Fenomeno De El Ni\u00f1o (The 1998 El Ni\u00f1o Phenomenon: Survey of the Population in Areas Affected by the 1998 El Ni\u00f1o Phenomenon), INEI. (In Spanish)."},{"key":"ref_50","unstructured":"(2018, June 01). How Inverse Distance Weighted (IDW) Interpolation Works. Available online: http:\/\/webhelp.esri.com\/arcgisdesktop\/9.2\/index.cfm?TopicName=How_Inverse_Distance_Weighted_(IDW)_interpolation_works."},{"key":"ref_51","unstructured":"(2018, June 01). Spatial Autocorrelation (Global Moran\u2019s I). Available online: http:\/\/desktop.arcgis.com\/en\/arcmap\/10.3\/tools\/spatial-statistics-toolbox\/spatial-autocorrelation.htm."},{"key":"ref_52","unstructured":"(2017, December 23). Reports to the Nation: El Ni\u00f1o and Climate Prediction. Available online: https:\/\/atmos. washington.edu\/gcg\/RTN\/rtnt.html."},{"key":"ref_53","unstructured":"(2018, June 20). History of the Array, Available online: http:\/\/tao.ndbc.noaa.gov\/proj_overview\/taohis_ndbc.shtml."},{"key":"ref_54","unstructured":"PAHO (1998). Per\u00fa: Fen\u00f3meno \u201cEl Ni\u00f1o\u201d. Informe Estrat\u00e9gico #2, OPS-Per\u00fa. (In Spanish)."},{"key":"ref_55","first-page":"33","article-title":"Assessing malaria transmission in a low endemicity area of North-Western Peru","volume":"12","author":"Speybroeck","year":"2013","journal-title":"Malar. J."},{"key":"ref_56","unstructured":"(2018, June 02). Cholera. Available online: http:\/\/www.who.int\/news-room\/fact-sheets\/detail\/cholera."},{"key":"ref_57","unstructured":"(2018, June 02). Alerta Epidemiologica: Conjuntivitis Hermorragico Aguda [Epidemiological Alert: Acute Hemorrhagic Conjunctivitis]. Available online: https:\/\/www.paho.org\/hq\/dmdocuments\/2013\/alertas-epi-2009-9-octubre-conjunctivitis.pdf."},{"key":"ref_58","unstructured":"(2018, June 20). Vamos a Prevenir: Plan De Communicacion: Fen 2015 (Let\u2019s Prevent: Communication Plan for El Ni\u00f1o 2015). (In Spanish)."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1007\/s11524-011-9607-0","article-title":"Urban health inequities and the added pressure of climate change: An action-oriented research agenda","volume":"88","author":"Friel","year":"2011","journal-title":"J. Urban Health"},{"key":"ref_60","first-page":"5","article-title":"Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector Anopheles darling","volume":"81","author":"Vittor","year":"2009","journal-title":"Am. J. Trop. Hyg. Med."},{"key":"ref_61","first-page":"172","article-title":"Asymptomatic malaria and its challenges in the malaria elimination program in Iran: A systematic review","volume":"11","author":"Hassanpour","year":"2017","journal-title":"J. Arthropod-Borne Dis."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Carrillo-Hern\u00e1ndez, M.Y., Ruiz-Saenz, J., Jaimes Villamizar, L., Gomez-Rangel, S.Y., and Martinez-Gutierrez, M. (2018). Co-circulation and simultaneous co-infection of dengue, chikungunya, and zika viruses in patients with febrile syndrome at the Colombian-Venezuelan border. BMC Infect. Dis., 18.","DOI":"10.1186\/s12879-018-2976-1"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/15\/12\/2639\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:31:59Z","timestamp":1760196719000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/15\/12\/2639"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,11,25]]},"references-count":62,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["ijerph15122639"],"URL":"https:\/\/doi.org\/10.3390\/ijerph15122639","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,11,25]]}}}