Editorial Type:
Article
Article Type:
Research Article

Reexamining El Niño and Cholera in Peru: A Climate Affairs Approach

Iván J. Ramírez Division of Social Sciences, New College of Florida, Sarasota, Florida

Search for other papers by Iván J. Ramírez in
Current site
Google Scholar
PubMed Close
,
Sue C. Grady Department of Geography, Michigan State University, East Lansing, Michigan

Search for other papers by Sue C. Grady in
Current site
Google Scholar
PubMed Close
, and
Michael H. Glantz Consortium for Capacity Building, University of Colorado, Boulder, Colorado

Search for other papers by Michael H. Glantz in
Current site
Google Scholar
PubMed Close
Print Publication:
01 Apr 2013
DOI:
https://doi.org/10.1175/WCAS-D-12-00032.1
Page(s):
148–161
Restricted access

Abstract

In the 1990s Peru experienced the first cholera epidemic after almost a century. The source of emergence was initially attributed to a cargo ship, but later there was evidence of an El Niño association. It was hypothesized that marine ecosystem changes associated with El Niño led to the propagation of V. cholerae along the coast of Peru, which in turn initiated the onset of the epidemic in 1991. Earlier studies supported this explanation by demonstrating a relationship between elevated temperatures and increased cholera incidence in Peru; however, other aspects of El Niño–Southern Oscillation (ENSO) and their potential impacts on cholera were not investigated. Therefore, this study examines the relationship between El Niño and cholera in Peru from a holistic view of the ENSO cycle. A “climate affairs” approach is employed as a conceptual framework to incorporate ENSO’s multidimensional nature and to generate new hypotheses about the ENSO and cholera association in Peru. The findings reveal that ENSO may have been linked to the cholera epidemic through multiple pathways, including rainfall extremes, La Niña, and social vulnerability, with impacts depending on the geography of teleconnections within Peru. When the definition of an ENSO event is examined, cholera appears to have emerged either during ENSO neutral or La Niña conditions. Furthermore, the analysis herein suggests that the impact of El Niño arrived much later, possibly resulting in heightened transmission in the austral summer of 1992. In conclusion, a modified hypothesis with these new insights on cholera emergence and transmission in Peru is presented.

Corresponding author address: Iván J. Ramírez, Division of Social Sciences, New College of Florida, 5800 Bay Shore Road, Sarasota, FL 34234. E-mail: iramirez@ncf.edu

Abstract

In the 1990s Peru experienced the first cholera epidemic after almost a century. The source of emergence was initially attributed to a cargo ship, but later there was evidence of an El Niño association. It was hypothesized that marine ecosystem changes associated with El Niño led to the propagation of V. cholerae along the coast of Peru, which in turn initiated the onset of the epidemic in 1991. Earlier studies supported this explanation by demonstrating a relationship between elevated temperatures and increased cholera incidence in Peru; however, other aspects of El Niño–Southern Oscillation (ENSO) and their potential impacts on cholera were not investigated. Therefore, this study examines the relationship between El Niño and cholera in Peru from a holistic view of the ENSO cycle. A “climate affairs” approach is employed as a conceptual framework to incorporate ENSO’s multidimensional nature and to generate new hypotheses about the ENSO and cholera association in Peru. The findings reveal that ENSO may have been linked to the cholera epidemic through multiple pathways, including rainfall extremes, La Niña, and social vulnerability, with impacts depending on the geography of teleconnections within Peru. When the definition of an ENSO event is examined, cholera appears to have emerged either during ENSO neutral or La Niña conditions. Furthermore, the analysis herein suggests that the impact of El Niño arrived much later, possibly resulting in heightened transmission in the austral summer of 1992. In conclusion, a modified hypothesis with these new insights on cholera emergence and transmission in Peru is presented.

Corresponding author address: Iván J. Ramírez, Division of Social Sciences, New College of Florida, 5800 Bay Shore Road, Sarasota, FL 34234. E-mail: iramirez@ncf.edu
Save
Cover Weather, Climate, and Society
Weather, Climate, and Society

  • Akanda, A. S., Jutla A. S. , and Islam S. , 2009: Dual peak cholera transmission in Bengal Delta: A hydroclimatological explanation. Geophys. Res. Lett., 36, L19401, doi:10.1029/2009GL039312.

    • Search Google Scholar
    • Export Citation

  • Barber, R. T., and Chavez F. P. , 1983: Biological consequences of El Niño. Science, 222, 1203–1210.

  • Bell, G. D., and Halpert M. S. , 1998: Climate assessment for 1997. Bull. Amer. Meteor. Soc., 79, S1–S50.

  • Bertuzzo, E., Mari L. , Righetto L. , Gatto M. , Casagrandi R. , Rodriguez-Iturbe I. , and Rinaldo A. , 2012: Hyrdoclimatology of dual-peak annual cholera incidence: Insights from a spatially explicit model. Geophys. Res. Lett., 39, L05403, doi:10.1029/2011GL050723.

    • Search Google Scholar
    • Export Citation

  • Blokesch, M., and Schoolnik G. K. , 2007: Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog., 3 (6), e81, doi:10.1371/journal.ppat.0030081.

    • Search Google Scholar
    • Export Citation

  • Brooke, J., 1990: Peru’s poor feel hardship of “Fuji shock” austerity. New York Times, August 12. [Available online at http://www.nytimes.com/1990/08/12/world/peru-s-poor-feel-hardship-of-fuji-shock-austerity.html.]

  • Caviedes, C. N., 2001: El Niño in History: Storming through the Ages. University Press of Florida, 279 pp.

  • Cazelles, B., Chavez M. , Constantin de Magny G. , Guegan J. , and Hales S. , 2007: Time-dependent spectral analysis of epidemiological time-series with wavelets. J. Roy. Soc. Interface, 4, 625–636.

    • Search Google Scholar
    • Export Citation

  • CCB, 2011: Climate affairs: What do we mean and why? Consortium for Capacity Building. [Available online at http://www.ccb-boulder.org.]

  • Chavez, F. P., 1996: Forcing and biological impact of onset of the 1992 El Niño in central California. Geophys. Res. Lett., 23, 265–268.

    • Search Google Scholar
    • Export Citation

  • Chavez, F. P., Bertrand A. , Guevarro-Carrasco R. , Soler P. , and Csirke J. , 2008: The northern Humboldt Current system: Brief history, present status and a view towards the future. Prog. Oceanogr., 79, 95–105.

    • Search Google Scholar
    • Export Citation

  • Checkley, W., Epstein L. D. , Gilman R. H. , Figueroa D. , Cama R. I. , Patz J. A. , and Black R. E. , 2000: Effect of El Niño and ambient temperature on hospital admissions for diarrhoeal diseases in Peruvian children. Lancet, 355, 442–450.

    • Search Google Scholar
    • Export Citation

  • Chin, C. C., and Coauthors, 2011: The origin of the Haitian cholera outbreak strain. N. Engl. J. Med., 364, 33–42.

  • Codeco, C. T., 2001: Endemic and epidemic dynamics of cholera: The role of the aquatic reservoir. BMC Infect. Dis., 1 (1), doi:10.1186/1471-2334-1-1.

    • Search Google Scholar
    • Export Citation

  • Colwell, R. R., 1996: Global climate and infectious disease: The cholera paradigm. Science, 274, 2025–2031.

  • Colwell, R. R., and Spira W. M. , 1992: The ecology of Vibrio cholerae. Cholera, D. Barua and W. B. Greenough III, Eds., Plenum Medical, 107–127.

  • Constantin de Magny, G., Cazelles B. , and Guegan J. F. , 2007: Cholera threat to humans in Ghana is influenced by both global and regional climate variability. EcoHealth, 3, 223–231.

    • Search Google Scholar
    • Export Citation

  • Constantin de Magny, G., and Coauthors, 2008: Environmental signatures associated with cholera epidemics. Proc. Natl. Acad. Sci. USA, 105, 17 676–17 681.

    • Search Google Scholar
    • Export Citation

  • Cravioto, A., Lanata C. F. , Lantagne D. S. , and Nair G. B. , 2011: Final report of the independent panel of experts on the cholera outbreak in Haiti. United Nations, 32 pp. [Available online at http://www.un.org/News/dh/infocus/haiti/UN-cholera-report-final.pdf.]

  • Cueto, M., 2001: The Return of Epidemics: Health and Society in Peru during the Twentieth Century. Ashgate, 176 pp.

  • Cutter, S. L., Emrich C. T. , Webb J. J. , and Morath D. , 2009: Social vulnerability to climate variability hazards: A review of the literature. Final report to Oxfam America; Hazards and Vulnerability Research Institute, 44 pp. [Available online at http://adapt.oxfamamerica.org/resources/Literature_Review.pdf.]

  • El Tiempo, 1991: Se agudiza deficiencia energética y de agua (Energy and water deficiencies worsen). 28 January, Piura.

  • El Tiempo, 1992a: Critica situación afrontan los distritos por lluvias (Districts face a critical situation caused by rains). 18 March, Piura.

  • El Tiempo, 1992b: 60 familias afectadas por las lluvias en El Indio (60 families are affected by rains in El Indio). 19 March, Piura.

  • Emch, M., Yunus M. , Escamilla V. , Feldacker C. , and Ali M. , 2010: Local population and regional environmental drivers of cholera in Bangladesh. Environ. Health, 9 (2), doi:10.1186/1476-069X-9-2.

    • Search Google Scholar
    • Export Citation

  • Enfield, D. B., 1981: Annual and nonseasonal variability of monthly low-level wind fields over the southeastern tropical Pacific. Mon. Wea. Rev., 109, 2177–2190.

    • Search Google Scholar
    • Export Citation

  • Enserink, M., 2011: Despite sensitivities, scientists seek to solve Haiti’s cholera riddle. Science, 331, 388–389.

  • Epstein, P. R., 1992: Cholera and the environment. Lancet, 339, 1167–1168.

  • Epstein, P. R., 1993: Algal blooms in the spread and persistence of cholera. Biosystems, 31, 209–221.

  • Epstein, P. R., Ford T. E. , and Colwell R. R. , 1993: Health and climate change: Marine ecosystems. Lancet, 342, 1216–1219.

  • Epstein, P. R., Ford T. E. , Puccia C. , and Possas C. D. , 1994: Marine ecosystem health: Implications for public health. Ann. N.Y. Acad. Sci.,740, 13–23.

  • Flores, M., 1998: Fisheries. Assessment of the use of remote sensing and other information related to ENSO: The use of ENSO information in Peru, M. H. Glantz, Ed., NASA/NCAR/Peru Project Final Report, NCAR Environmental and Societal Impacts Group, 37–42.

  • Franco, A. A., and Coauthors, 1997: Cholera in Lima, Peru, correlates with prior isolation of Vibrio cholerae from the environment. Amer. J. Epidemiol., 146, 1067–1075.

    • Search Google Scholar
    • Export Citation

  • Gangarosa, E. J., and Tauxe R. V. , 1992: Epilogue: The Latin American cholera epidemic. Cholera, D. Barua and W. B. Greenough III, Eds., Plenum Medical, 351–357.

  • Gil, A. I., and Coauthors, 2004: Occurrence and distribution of Vibrio cholerae in the coastal environment of Peru. Environ. Microbiol., 6, 699–706.

    • Search Google Scholar
    • Export Citation

  • Glantz, M. H., Ed., 1997: A systems approach to ENSO: An NCAR colloquium, 20 July–1 August 1997, Boulder, Colorado. NCAR Environmental and Societal Impacts Group, 194 pp. [Available online at http://www.ilankelman.org/glantz/Glantz1997SystemsENSO.pdf.]

  • Glantz, M. H., 2001a: Currents of Change: Impacts of El Niño and La Niña on Climate and Society. 2nd ed. Cambridge University Press, 252 pp.

  • Glantz, M. H., 2001b: Once Burned, Twice Shy: Lessons Learned from the 1997–98 El Niño. United Nations University Press, 294 pp.

  • Glantz, M. H., 2002: La Niña and Its Impacts: Facts and Speculation. United Nations University Press, 271 pp.

  • Glantz, M. H., 2003: Climate Affairs: A Primer. Island Press, 291 pp.

  • Glantz, M. H., and Adeel Z. , 2000: Climate affairs as a next-generation environmental science. Global Environ. Change, 10, 81–85.

  • Glantz, M. H., and Jamieson D. , 2000: Societal response to Hurricane Mitch and intra- versus intergenerational equity issues: Whose norms should apply? Risk Anal., 6, 869–882.

    • Search Google Scholar
    • Export Citation

  • Goddard, L., and Graham N. E. , 1997: El Niño in the 1990s. J. Geophys. Res., 102, 10 423–10 436.

  • Gomez Pando, V., and Pineda S. R. , 1991: Endemicidad del Vibrio cholerae en Lima (Endemicity of Vibrio cholerae in Lima). Salud Publica y Medicina Preventiva en el Desarollo (Public Health and Preventive Medicine in Development), V. Gomez Pando, Ed., Fondo Editorial de la UNMSM, 345–350.

  • Gueri, A., 1984: Lessons learned: Health effects of El Niño in Peru. Disasters: Preparedness and Mitigation, Vol. 19, Pan American Health Organization, Washington, DC. [Available online at http://helid.digicollection.org/en/d/Jdi019e/2.html.]

  • Halpert, M. S., and Bell G. D. , 1997: Climate assessment for 1996. Bull. Amer. Meteor. Soc., 78, S1–S49.

  • Hashizume, M., Armstrong B. , Hajat S. , Wagatsuma Y. , Faruque A. S. , Hayashi T. , and Sack D. , D. 2008: The effect of rainfall on the incidence of cholera in Bangladesh. Epidemiology, 19, 103–110.

    • Search Google Scholar
    • Export Citation

  • Hashizume, M., Faruque A. S. , Wagatsuma Y. , Hayashi T. , and Armstrong B. , 2010: Cholera in Bangladesh: Climatic components of seasonal variation. Epidemiology, 21, 706–710.

    • Search Google Scholar
    • Export Citation

  • Hernan Vargas, F., Harrison S. , Rea S. , and Macdonald D. W. , 2006: Biological effects of El Niño on the Galapagos penguins. Biol. Conserv., 127, 107–114.

    • Search Google Scholar
    • Export Citation

  • Huanca, R. I., 2004: El fenómeno El Niño y su influencia en el desarollo de algunos brotes epidémicos: Cono norte-Lima (The El Niño phenomenon and its influence on the emergence of epidemics: North Lima). Rev. Viernes Med., 29, 38–43.

    • Search Google Scholar
    • Export Citation

  • Huq, A., and Coauthors, 2005: Critical factors influencing the occurrence of vibrio cholerae in the environment of Bangladesh. Appl. Environ. Microbiol., 71, 4645–4654.

    • Search Google Scholar
    • Export Citation

  • IRI, cited 2008: The ENSO system. International Research Institute for Climate and Society. [Available online at http://iri.columbia.edu/climate/ENSO/enso.html.]

  • Jiménez, C., and Cortés J. , 2001: Effects of the 1991-92 El Niño on scleractinian corals of the Costa Rican central Pacific coast. Rev. Biol. Trop., 49, 239–250.

    • Search Google Scholar
    • Export Citation

  • Jutla, A. S., Akanda A. S. , Griffiths J. K. , Colwell R. R. , and Islam S. , 2011: Warming oceans, phytoplankton, and river discharge: Implications for cholera outbreaks. Amer. J. Trop. Med. Hyg., 85, 303–308.

    • Search Google Scholar
    • Export Citation

  • Kessler, W. S., and McPhaden M. J. , 1995: Oceanic equatorial waves and the 1991–93 El Niño. J. Climate, 8, 1757–1774.

  • Koelle, K., Rodó X. , Pascual M. , Yunus M. , and Mostafa G. , 2005: Refractory periods and climate forcing in cholera dynamics. Nature, 436, 696–700.

    • Search Google Scholar
    • Export Citation

  • Kovats, R. S., Bouma M. J. , Hajat S. , Worrall E. , and Haines A. , 2003: El Niño and health. Lancet, 362, 1481–1489.

  • Lagos, P., and Buizer J. , 1992: El Niño and Peru: A nation’s response to interannual climate variability. Natural and Technological Disasters: Causes, Effects and Preventive Measures, S. K. Majumdar, Ed., The Pennsylvania Academy of Science, 223–238.

  • Lagos, P., Silva Y. , Nickl E. , and Mosquera K. , 2008: El Niño-related precipitation variability in Peru. Adv. Geosci., 14, 231–237, doi:10.5194/adgeo-14-231-2008.

    • Search Google Scholar
    • Export Citation

  • Lam, C., Octavia S. , Reeves P. , Wang L. , and Lan R. , 2010: Evolution of seventh cholera pandemic and origin of 1991 epidemic, Latin America. Emerg. Infect. Dis., 16, 1130–1132, doi:10.3201/eid1607.100131.

    • Search Google Scholar
    • Export Citation

  • Lama, J. R., Seas C. R. , Leon-Barua R. , Gotuzzo E. , and Sack R. B. , 2004: Environmental temperature, cholera, and acute diarrhea in adults in Lima, Peru. J. Health Popul. Nutr., 22, 399–403.

    • Search Google Scholar
    • Export Citation

  • Lavado Casimiro, W. S., Ronchail J. , Labat D. , Espinoza J. C. , and Guyot J. L. , 2012: Basin-scale analysis of rainfall and run-off in Peru (1969-2004): Pacific, Titicaca and Amazonas drainages. Hydrol. Sci. J.,57, 625–642, doi:10.1080/02626667.2012.672985.

  • Lipp, E. K., and Coauthors, 2003: Direct detection of Vibrio cholerae and ctxA in Peruvian coastal water and plankton by PCR. Appl. Environ. Microbiol., 69, 3676–3680, doi:10.1128/AEM.69.6.3676-3680.2003.

    • Search Google Scholar
    • Export Citation

  • Madico, G., Checkley W. , Gilman R. H. , Bravo N. , Cabrera L. , Calderon M. , and Ceballos A. , 1996: Active surveillance for Vibrio cholerae O1 and vibriophages in sewage water as a potential tool to predict cholera outbreaks. J. Clin. Microbiol., 34, 2968–2972.

    • Search Google Scholar
    • Export Citation

  • Marchant, M., Hebbeln D. , and Wefer G. , 1998: Seasonal flux patterns of planktic foraminifera in the Peru–Chile Current—Past and present circulation. Deep-Sea Res. I, 45, 1161–1185.

    • Search Google Scholar
    • Export Citation

  • Marengo, J. A., 1999: Estudios sobre tendencias y variabilidad climatica en el tropico sudamericano: Peru y Brasil (A study of climate influences and variability in the South American tropics: Peru and Brazil). Peru: Vulnerabilidad Frente al Cambio Climático: Aproximaciones a la Experiencia con El Fenómeno El Niño (Peru: Vulnerability to Climate Change: The Experience of the El Niño Phenomenon as an Analogue), B. Marticorena, Ed., Consejo Nacional de Ambiente, 185–204.

  • Marengo, J. A., and Coauthors, 2008: The drought of Amazonia in 2005. J. Climate, 21, 495–516.

  • Mari, L., Bertuzzo E. , Righetto L. , Casagrandi R. , Gatto M. , Rodriguez-Iturbe I. , and Rinaldo A. , 2012: Modelling cholera epidemics: The role of waterways, human mobility and sanitation. J. Roy. Soc. Interface, 9, 376–388.

    • Search Google Scholar
    • Export Citation

  • Martinez-Urtaza, J., Huapaya B. , Gavilan R. G. , Blanco-Abad V. , Ansede-Bermejo J. , Cadarso-Suarez C. , Figueiras A. , and Trinanes J. , 2008: Emergence of Asiatic vibrio diseases in South America in phase with El Niño. Epidemiology, 19, 829–837.

    • Search Google Scholar
    • Export Citation

  • McPhaden, M. J., cited 1994: TOGA-TAO and the 1991–93 El Niño–Southern Oscillation event. NOAA/Pacific Marine Environmental Laboratory. [Available online at http://www.pmel.noaa.gov/pubs/docs/mcph1401.html.]

  • McPhaden, M. J., Zebiak S. E. , and Glantz M. H. , 2006: ENSO as an integrating concept in earth science. Science, 314, 1740–1745.

  • Mendelsohn, J., and Dawson T. , 2008: Climate and cholera in KwaZulu-Natal, South Africa: The role of environmental factors and implications for epidemic preparedness. Int. J. Hyg. Environ. Health, 211, 156–162.

    • Search Google Scholar
    • Export Citation

  • MINSA, 1994: Recopilación y sistematizacion de las condiciones ambientales y actividades desarrolladas en el control de la epidemia del cólera (A summary of environmental conditions and activities to control the cholera epidemic). Ministerio de Salud, 543 pp.

  • MINSA, 1995: Reporte Epidemiológico (Epidemiology Report). Week 39.

  • MINSA, 1998a: Reporte Epidemiológico (Epidemiology Report), Week 17.

  • MINSA, 1998b: Reporte Epidemiológico (Epidemiology Report), Week 21.

  • MINSA, 1998c: Reporte Epidemiológico (Epidemiology Report), Week 26.

  • MINSA, 1998d: Reporte Epidemiológico (Epidemiology Report), Week 52.

  • MINSA, 1999a: Las últimas consecuencias del fenómeno “La Niña” en el Peru (The phenomenon “La Niña” and recent impacts in Peru). Reporte Epidemiológico (Epidemiology Report), Week 7.

  • MINSA, 1999b: Reporte Epidemiológico (Epidemiology Report), Week 5.

  • MINSA, 2000: Reporte Epidemiológico (Epidemiology Report), Week 10.

  • MINSA, 2005: Reporte Epidemiológico (Epidemiology Report), Week 1.

  • MINSA, 2008: Suspected and clinically confirmed cholera cases in Peru from 1991 to 2002. Department of Epidemiology, Lima, Peru.

  • Mourino-Perez, R. R., 1998: Oceanography and the seventh cholera pandemic. Epidemiology, 9, 355–357.

  • Nash, N. C., 1991: Fujimori in the time of cholera. New York Times, 24 February. [Available online at http://www.nytimes.com/1991/02/24/weekinreview/the-world-fujimori-in-the-time-of-cholera.html.]

  • NOAA, 1992: ENSO advisory, May. Climate Analysis Center.

  • NOAA, 1993: ENSO advisory, May. Climate Analysis Center.

  • NOAA, cited 2011: Frequently asked questions about El Niño and La Niña. Climate Prediction Center. [Available online at http://www.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ensofaq.shtml.]

  • NOAA, cited 2012: Cold and warm episodes by season. Climate Prediction Center. [Available online at http://www.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ensoyears.shtml.]

  • Nusrin, S., and Coauthors, 2009: Peruvian Vibrio cholerae O1 El Tor strains possess a distinct region in the Vibrio seventh pandemic island-II that differentiates them from the prototype seventh pandemic El Tor strains. J. Med. Microbiol., 58, 342–354.

    • Search Google Scholar
    • Export Citation

  • Ordinola, N., 2002: The consequences of cold events for Peru. La Niña and Its Impacts: Facts and Speculation, M. H. Glantz, Ed., United Nations University Press, 146–150.

  • PAHO, 1991: Cholera situation in the Americas: An update. Epidemiol. Bull., 12, 1–16.

  • PAHO, 1998a: Peru: Fenómeno “El Niño”. Informe estratégico No. 2, OPS-Peru, Week 10, Pan American Health Organization.

  • PAHO, 1998b: El Niño and its impact on health. Proc. 122nd PAHO Meeting, Washington, DC, Pan American Health Organization, 4.4. [Available online at http://www.bvsde.paho.org/bvsacd/cd68/ElNino.pdf.]

  • PAHO, cited 2008: The number of cholera cases in the Americas, 1990–2008. Pan American Health Organization. [Available online at http://www.paho.org/English/AD/DPC/CD/cholera-1990-2008.pdf.]

  • Pascual, M., Rodó X. , Ellner S. P. , Colwell R. R. , and Bouma M. J. , 2000: Cholera dynamics and El Niño–Southern Oscillation. Science, 289, 1766–1769.

    • Search Google Scholar
    • Export Citation

  • Piarroux, R., Barrais R. , Faucher B. , Haus R. , Piarroux M. , Gaudart J. , Magloire R. , and Raoult D. , 2011: Understanding the cholera epidemic, Haiti. Emerg. Infect. Dis., 17, 1161–1167, doi: 10.3201/eid1707.110059.

    • Search Google Scholar
    • Export Citation

  • Pizarro, L., 1999: El Niño phenomenon and natural disasters in Peru. Proc. Int. Workshop on Natural Disaster Management, Beijing, China, 85–92. [Available online at http://cidbimena.desastres.hn/pdf/eng/doc15155/doc15155-contenido.pdf.]

  • Ramírez, I. J., 2012. Cholera in a Time of El Niño and Vulnerability in Piura, Peru: A Climate Affairs Approach. Ph.D. dissertation, Michigan State University, 290 pp.

  • Reiner, R. C., Jr., King A. A. , Emch M. , Yunusd M. , Faruqued A. S. G. , and Pascual M. , 2011: Highly localized sensitivity to climate forcing drives endemic cholera in a megacity. Proc. Natl. Acad. Sci. USA,109, 2033–2036, doi:10.1073/pnas.1108438109.

  • Reyburn, R., Kim D. R. , Emch M. , Khatib A. , von Seidlein L. , and Ali M. , 2011: Climate variability and outbreaks of cholera in Zanzibar, East Africa: A time series analysis. Amer. J. Trop. Med. Hyg., 84, 862–869.

    • Search Google Scholar
    • Export Citation

  • Ries, A. A., and Coauthors, 1992: Cholera in Piura, Peru: A modern urban epidemic. J. Infect. Dis., 166, 1429–1433.

  • Rinaldo, A., and Coauthors, 2012: Reassessment of the 2010–2011 Haiti cholera outbreak and rainfall-driven multiseason projections. Proc. Natl. Acad. Sci. USA,109, 6602–6607, doi:10.1073/pnas.1203333109.

  • Ropelewski, C., and Halpert M. , 1987: Global and regional scale precipitation patterns associated with the El Niño/Southern Oscillation. Mon. Wea. Rev., 115, 1606–1626.

    • Search Google Scholar
    • Export Citation

  • Ruiz-Moreno, D., Pascual M. , Bouma M. , Dobson A. , and Cash B. , 2007: Cholera seasonality in Madras (1901–1940): Dual role for rainfall in endemic and epidemic regions. EcoHealth, 4, 52–62.

    • Search Google Scholar
    • Export Citation

  • Salazar-Lindo, E., Pinell-Salles P. , Maruy A. , and Chea-Woo E. , 1997: El Niño and diarrheoa and dehydration in Lima, Peru. Lancet, 350, 1597–1598.

    • Search Google Scholar
    • Export Citation

  • Salazar-Lindo, E., Seas C. , and Gutiérrez D. , 2008: ENSO and cholera in South America: What can we learn about it from the 1991 cholera outbreak? Int. J. Environ. Health, 2, 30–36.

    • Search Google Scholar
    • Export Citation

  • Sasaki, S., Suzuki H. , Fujino Y. , Kimura Y. , and Cheelo M. , 2009: Impact of drainage networks on cholera outbreaks in Lusaka, Zambia. Amer. J. Pub. Health, 99, 1982–1987.

    • Search Google Scholar
    • Export Citation

  • Seas, C., and Gotuzzo E. , 1996: Cholera: Overview of epidemiologic, therapeutic, and preventive issues learned from recent epidemics. Int. J. Infect. Dis., 1, 37–46.

    • Search Google Scholar
    • Export Citation

  • Seas, C., Miranda J. , Gil A. I. , Leon-Barua R. , Patz J. , Huq A. , Colwell R. R. , and Sack R. B. , 2000: New insights on the emergence of cholera in Latin America during 1991: The Peruvian experience. Amer. J. Trop. Med. Hyg., 62, 513–517.

    • Search Google Scholar
    • Export Citation

  • SENAMHI, 2004: El evento El Niño Oscilacion Sur 1997–1998: Su impacto en el departamento de Lambayeque (The 1997/98 ENSO event: Impacts in the Department of Lambayeque). Servicio Nacional de Meteorologia e Hidrologia, Chiclayo, Peru. [Available online at http://www.senamhi.gob.pe/.]

  • SENAMHI, 2009: Escanarios de cambio climatico en la cuenca del Rio Urubamba para el ano 2100: Resumen técnico (Climate change scenarios for the Urubamba River Basin in 2100: A technical summary). Servicio Nacional de Meteorologia e Hidrologia, Lima, Peru, 50 pp. [Available online at http://issuu.com/praa/docs/praa-senamhi-eccc-urubamba-2100.]

  • Speelmon, E. C., Checkley W. , Gilman R. H. , Patz J. , Calderon M. , and Manga S. , 2000: Cholera incidence and El Niño-related higher ambient temperature. J. Amer. Med. Assoc., 283, 3072–3074.

    • Search Google Scholar
    • Export Citation

  • Sperling, F., Valdivia C. , Quiroz R. , Valdivia R. , Angulo L. , Seimon A. , and Noble I. , 2008: Transitioning to climate resilient development: Perspectives from communities in Peru. The World Bank, Environment Department Papers, Climate Change Series, No. 115, 103 pp.

  • Tauxe, R., Mintz E. D. , and Quick R. E. , 1995: Epidemic cholera in the New World: Translating field epidemiology into new strategies. Emerg. Infect. Dis., 1, 4. [Available online at http://www.cdc.gov/ncidod/EID/vol1no4/tauxe.htm.]

    • Search Google Scholar
    • Export Citation

  • Trenberth, K. E., 1997: The definition of El Niño. Bull. Amer. Meteor. Soc., 78, 2771–2777.

  • Trenberth, K. E., and Hoar T. J. , 1996: The 1990–1995 El Niño–Southern Oscillation event: Longest on record. Geophys. Res. Lett., 23, 57–60.

    • Search Google Scholar
    • Export Citation

  • UNDRO, cited 1990a: Peru drought June 1990 UNDRO situation reports 1-5. United Nations Office for the Coordination of Humanitarian Affairs. [Available online at http://www.reliefweb.int/rw/rwb.nsf/db900sid/OCHA-64BQQC?OpenDocument.]

  • UNDRO, cited 1990b: Peru Earthquake May 1990 UNDRO Situation Reports 1-7. United Nations Office for the Coordination of Humanitarian Affairs. [Available online at http://www.reliefweb.int/rw/rwb.nsf/db900SID/OCHA-64C3R8?OpenDocument.]

  • Valverde, A., 1998: Influence of El Niño in the systems of hydroelectric generation. Assessment of the use of remote sensing and other information related to ENSO: The use of ENSO information in Peru, M. H. Glantz, Ed., NASA/NCAR/Peru Project Final Report, NCAR Environmental and Societal Impacts Group, 45–48.

  • WMO, 1999: The 1997–1998 El Niño event: A scientific and technical retrospective. WMO-No. 905, 96 pp. [Available online at http://library.wmo.int/pmb_ged/wmo_905_en.pdf.]

  • Wyrtki, K., 1975: Teleconnections in the equatorial Pacific Ocean. Science, 180, 66–68.

  • Youngers, C. A., 2000: Deconstructing democracy: Peru under President Alberto Fujimori. Washington Office on Latin America, 89 pp.

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 1989 850 42
PDF Downloads 954 175 20