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EcoHealth

, Volume 13, Issue 1, pp 83–99 | Cite as

El Niño, Climate, and Cholera Associations in Piura, Peru, 1991–2001: A Wavelet Analysis

  • Iván J. Ramírez
  • Sue C. Grady
Original Contribution

Abstract

In Peru, it was hypothesized that epidemic cholera in 1991 was linked to El Niño, the warm phase of El Niño–Southern Oscillation. While previous studies demonstrated an association in 1997–1998, using cross-sectional data, they did not assess the consistency of this relationship across the decade. Thus, how strong or variable an El Niño–cholera relationship was in Peru or whether El Niño triggered epidemic cholera early in the decade remains unknown. In this study, wavelet and mediation analyses were used to characterize temporal patterns among El Niño, local climate variables (rainfall, river discharge, and air temperature), and cholera incidence in Piura, Peru from 1991 to 2001 and to estimate the mediating effects of local climate on El Niño–cholera relationships. The study hypothesis is that El Niño-related connections with cholera in Piura were transient and interconnected via local climate pathways. Overall, our findings provide evidence that a strong El Niño–cholera link, mediated by local hydrology, existed in the latter part of the 1990s but found no evidence of an El Niño association in the earlier part of the decade, suggesting that El Niño may not have precipitated cholera emergence in Piura. Further examinations of cholera epicenters in Peru are recommended to support these results in Piura. For public health planning, the results may improve existing efforts that utilize El Niño monitoring for preparedness during future climate-related extremes in the region.

Keywords

El Niño El Niño–Southern Oscillation cholera climate wavelet mediation 

Notes

Acknowledgments

The authors would like to thank the Department of Geography, Michigan State University for the financial support for data collection in Peru. We also thank The New School for providing the space and funding to complete the manuscript (Research Faculty Fund and ReNew School Project 14k Grant Award). We are also grateful to our Peruvian collaborators, including Ing. Norma Ordinola and Ing. Rodolfo Rodriguez, University of Piura, Ing. Grover Otero, Proyecto Chira-Piura and Dr. Elsa Galarza, University of Pacific, as well as the Departments of Epidemiology at the Ministries of Health, and the Institute for Statistics and Information in Lima and Piura, Peru.

References

  1. Barron, RM, Kenny, DA (1986) The moderator mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology 51: 1173–1182CrossRefGoogle Scholar
  2. Capotondi, A, Wittenberg, AT, Newman, M, Di Lorenzo, E, Yu, J, Braconnot, P, et al (2015) Understanding ENSO diversity. Bulletin of the American Meteorological Society 96: 921-938. doi: 10.1175/BAMS-D-13-00117.1 CrossRefGoogle Scholar
  3. Cash, BA, Rodó, X, Kinter, JL (2008) Links between tropical Pacific SST and cholera incidence in Bangladesh: role of the eastern and central tropical Pacific. Journal of Climate 21: 4647–4663CrossRefGoogle Scholar
  4. Cazelles, B, Chavez, M, Constantin de Magny, G, Guegan, J, Hales, S (2007) Time-dependent spectral analysis of epidemiological time-series with wavelets. The Journal of the Royal Society Interface 4: 625-636CrossRefGoogle Scholar
  5. Cazelles, B, Chavez, M, McMichael, AJ, Hales, S (2005) Nonstationary influences of El Niño on the synchronous dengue epidemics in Thailand. Public Library of Science 2:e106. doi: 10.1371/journal.pmed.0020106. Accessed February 1, 2015
  6. Chaves, LF, Pascual, M (2006) Climate cycles and forecasts of Cutaneous Leishmaniasis, a nonstationary vector-borne disease. Public Library of Science, 3: e295. doi: 10.1371/journal.pmed.0030295. Accessed February 1, 2015
  7. Checkley, W, Epstein, LD, Gilman, RH, Figueroa, D, Cama, RI, Patz, JA, et al. (2000) Effect of El Niño and ambient temperature on hospital admissions for diarrhoeal diseases in Peruvian children. The Lancet 355: 442–450Google Scholar
  8. Colwell, RR (1996) Global climate and infectious disease: the cholera paradigm. Science 274: 2025-2031CrossRefPubMedGoogle Scholar
  9. Constantin de Magny, G, Cazelles, B, Guegan, JF (2006) Cholera threat to humans in Ghana is influenced by both global and regional climate variability. EcoHealth 3: 223-231CrossRefGoogle Scholar
  10. Curriero FC, Patz JA, Rose JB, Lele S (2001) The Association Between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994. American Journal of Public Health 91:1194-1199CrossRefPubMedPubMedCentralGoogle Scholar
  11. El Tiempo (The Times) (1992) Critica situación afrontan los distritos por lluvias (Districts face a critical situation caused by rains). 18 March, Piura (in Spanish)Google Scholar
  12. Emch M, Yunus M, Escamilla V, Feldacker C, Ali M (2010) Local population and regional environmental drivers of cholera in Bangladesh. Environmental Health 9. http://www.ehjournal.net/content/9/1/2. Accessed Feb 15, 2015
  13. Epstein, PR, Ford, TE, Colwell, RR (1993) Health and climate change: marine ecosystems. The Lancet 342: 1216-1219CrossRefGoogle Scholar
  14. Franco AA, et al. (1997) Cholera in Lima, Peru, correlates with prior isolation of Vibrio cholerae from the Environment. American Journal of Epidemiology 146: 1067-1075CrossRefPubMedGoogle Scholar
  15. Frazier, PA, Tix, AP, Barron, KE (2004) Testing moderator and mediator effects in counseling psychology research. Journal of Counseling Psychology 51: 115-134CrossRefGoogle Scholar
  16. Gil AI, Louis VR, Rivera ING, Lipp E, Huq A, Lanata CF, et al. (2004) Occurrence and distribution of Vibrio cholerae in the coastal environment of Peru. Environmental Microbiology 6: 699–706.CrossRefPubMedGoogle Scholar
  17. Glantz, MH (1991). Introduction. In: Teleconnections linking worldwide climate anomalies, Glantz, MH, Katz, RW, Nicholls, N (editors), New York: Cambridge University Press, pp. 2-12Google Scholar
  18. Grady, SC, Ramirez, IJ (2008) Mediating medical risk factors in the residential segregation and low birthweight relationship by race in New York City. Health and Place 14: 661 – 677CrossRefPubMedGoogle Scholar
  19. Grinsted, A, Moore, JC, Jevrejeva, S (2004) Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Processes in Geophysics 11: 561-566CrossRefGoogle Scholar
  20. Grinsted A, Moore JC, Jevrejeva S (2008) Matlab package for performing cross-wavelet and wavelet coherence. http://noc.ac.uk/using-science/crosswavelet-wavelet-coherence. Accessed Feb 1, 2015
  21. Hashizume M, Armstrong, B, Hajat, S, Wagatsuma, Y, Faruque, AS, Hayashi, T, et al. (2008) The effect of rainfall on the incidence of cholera in Bangladesh. Epidemiology 19: 103–110CrossRefPubMedGoogle Scholar
  22. Hashizume M, Chaves, LF, Farunque, ASG, Yunus, MD, Streatfield, K, Kazuhiko, M (2013) A differential effect of Indian Ocean Dipole and El Nino on cholera dynamics in Bangladesh. PLoS One 8(3): e60001. doi: 10.1371/journal.pone.0060001 CrossRefPubMedPubMedCentralGoogle Scholar
  23. IBM SPSS (2015) Predictive analytics software and solutions. http://01.ib.com/software/analytics/spss. Accessed Mar 22, 2015
  24. Instituto Nacional de Estadistica e Informatica (Institute of National Statistics and Information) (INEI) (2000) Las Estadisticas Vitales en Los Distritos del Peru (Vital Statistics at the District-level in Peru. http://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib0397/Libro.pdf. Accessed Feb 16, 2015
  25. Jutla, A, Whitcombe, E, Hasan, N, Haley, B, Akanda, A, Huq, et al. (2013) Environmental factors influencing epidemic cholera. The American Journal of Tropical Medicine and Hygiene 89: 597-607CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jutla, AS, Akanda, AS, Griffiths, JK, Colwell, RR, Islam, S (2011) Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks. American Journal of Tropical Medicine and Hygiene 85: 303-308CrossRefPubMedPubMedCentralGoogle Scholar
  27. Koelle, K, Rodo, X, Pascual, M, Yunus, M, Mostafa, G (2005) Refractory periods and climate forcing in cholera dynamics. Nature 436: 696–700CrossRefPubMedGoogle Scholar
  28. Lagos P, Silva Y, Nickl E, Mosquera K (2008) El Niño-related precipitation variability in Perú. Advances in Geosciences 14:231–237. http://www.adv-geosci.net/14/231/2008/. Accessed July 20, 2013
  29. Lama, JR, Seas, CR, Leon-Barua, R, Gotuzzo, E, Sack, RB (2004) Environmental temperature, cholera, and acute diarrhea in adults in Lima, Peru. Journal of Health and Population Nutrition, 22 399-403Google Scholar
  30. Lavado Casimiro WS, Ronchail J, Labat D, Espinoza JC, Guyot JL (2012) Basin-scale analysis of rainfall and run-off in Peru (1969–2004): Pacific, Titicaca and Amazonas drainages. Hydrological Sciences Journal 57:625–642. http://www.igp.gob.pe/igp/images/documents/comunicaciones/publicaciones/2012/perutrends_iahs_2012.pdf. Accessed Feb 15, 2015
  31. Lipp, EK, et al. (2003) Direct detection of Vibrio cholerae and ctxA in Peruvian coastal water and plankton by PCR. Applied and Environmental Microbiology 69: 3676-3680CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lobitz, B, Beck, L, Huq, A, Wood, B, Fuchs, G, Faruque, ASG, Colwell, RR (2000) Climate and infectious disease: use of remote sensing for detection of V. cholerae by indirect measurement. Proceedings of the National Academy of Sciences of the United States of America 97: 1438-1443CrossRefPubMedPubMedCentralGoogle Scholar
  33. Madico, GW, Checkley, Gilman, RH, Bravo, N, Cabrera, L, Calderon, M, et al. (1996) Active surveillance for Vibrio cholerae 01 and vibriophages in sewage water as a potential tool to predict cholera outbreaks. Journal of Clinical Microbiology 34: 2968-2972PubMedPubMedCentralGoogle Scholar
  34. Ministerio de Salud (Ministry of Health) (2005) Protocolos de la vigilancia epidemiologica (Protocols for Epidemiological Surveillance), Part 1. Lima: Department of Epidemiology, Ministry of Health (in Spanish)Google Scholar
  35. Moore SM, Shannon KL, Zelaya CE, Azman AS, Lessler J (2014) Epidemic risk from cholera introductions into Mexico. PLOS Currents Outbreaks, Edition 1. DOI: 10.1371/currents.outbreaks.c04478c7fbd9854ef6ba923cc81eb799
  36. Ng EKW, Kwok TW (2012) The software for the bias-rectified wavelet power spectrum, partial wavelet coherence and multiple wavelet coherence. http://www.cityu.edu.hk/gcacic/wavelet. Accessed Sep 10, 2014
  37. NOAA (2015) Cold and warm episodes by season. Climate Prediction Center. http://www.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ensoyears.shtml. Accessed Feb 16, 2015
  38. PAEN/GTZ (2003) Diagnostico zona baja Cuenca Rio Piura con enfoque de gestion del riesgo (Vulnerability Assessment of the Lower Zone of the River Piura Watershed). German Agency for Technical Cooperation (Unpublished, in Spanish)Google Scholar
  39. PAHO (2008) The number of cholera cases in the Americas, 1990–2008. http://www.paho.org/English/AD/DPC/CD/cholera-1990-2008.pdf. Accessed Feb 10, 2015
  40. Pan American Health Organization (PAHO) (2014) Atlas of cholera outbreak in La Hispaniola, 2010–2014. http://new.paho.org/hq/images/Atlas_IHR/CholeraHispaniola/atlas.html. Accessed Feb 16, 2015
  41. Pascual M, Bouma, MJ, Dobson, AP (2002) Cholera and climate: revisiting the quantitative evidence. Microbes and Infection 4: 237–245CrossRefPubMedGoogle Scholar
  42. Pascual, M, Rodo, X, Ellner, SP, Colwell, RR, Bouma, MJ (2000) Cholera dynamics and El Niño-Southern Oscillation. Science 289: 1766-1769CrossRefPubMedGoogle Scholar
  43. Preacher, KJ, Hayes, AF (2004) SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments, & Computers 36: 717-731CrossRefGoogle Scholar
  44. Ramirez, IJ (2015) Cholera resurgence in Piura, Peru: examining climate associations during the 1997-98 El Niño. GeoJournal 80: 129-143. DOI:  10.1007/s10708-014-9541-2 CrossRefGoogle Scholar
  45. Ramirez, IJ, Grady, S, Glantz, MH (2013) Reexamining El Niño and cholera in Peru: a climate affairs approach. Weather, Climate and Society 5: 148–161CrossRefGoogle Scholar
  46. Reyburn R, Kim DR, Emch M, Khatib A, von Seidlein L, Ali M (2011) Climate variability and the outbreaks of cholera in Zanzibar, East Africa: a time series analysis. The American Journal of Tropical Medicine and Hygiene 84: 862-869. doi: 10.4269/ajtmh.2011.10-0277 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Ries, AA, Vugia, DJ, Beingolea, L, Palacios, AM, Vasquez, E, Wells, JG, et al. (1992) Cholera in Piura, Perú: a modern urban epidemic. The Journal of Infectious Diseases 166: 1429-1433CrossRefPubMedGoogle Scholar
  48. Rinaldo, A., Bertuzzo, E, Mari, L, Righetto, L, Blokesch, M, Gatto, M, et al. (2012) Reassessment of the 2010-2011 Haiti cholera outbreak and rainfall-driven multiseason projections. Proceedings of the National Academy of Sciences of the United States of America 109: 6602–6607. DOI:  10.1073/pnas.1203333109 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ruiz-Moreno, D, Pascual, M, Bouma, M, Dobson, A, Cash, B (2007) Cholera seasonality in Madras (1901-1940): dual role for rainfall in endemic and epidemic regions. EcoHealth 4: 52-62CrossRefGoogle Scholar
  50. Sandoval PS (1999) Evaluación de Daños y Acciones del Fenómeno El Niño (Evaluation of Damages Caused by the El Niño Phenomenon and Actions Taken). Peru: Oficina de Planificación, Dirección de Salud Regional (Planning Office, Regional Health Post) (in Spanish)Google Scholar
  51. Saskai, S, Suzuki, H, Yasuyuki, F, Yoshinari, K, Meetwell, C (2009): Impact of drainage networks on cholera outbreaks in Lusaka, Zambia. American Journal of Public Health 99: 1982-1987CrossRefGoogle Scholar
  52. Speelmon, EC, Checkley, W, Gilman, RH, Patz, J, Calderon, M, Manga, S (2000) Cholera incidence and El Niño-related higher ambient temperature. Journal of the American Medical Association 283: 3072-3074CrossRefPubMedGoogle Scholar
  53. Takahashi K (2004) The atmospheric circulation associated with extreme rainfall events in Piura, Peru, during the 1997–98 and 2002 El Niño events. Annales Geophysicae 22:3917–3926. http://www.ann-geophys.net/22/3917/2004/angeo-22-3917-2004.pdf. Accessed July 20, 2013
  54. Tauxe, R, Mintz, ED, Quick, RE (1995) Epidemic cholera in the New World: translating field epidemiology into new strategies. Emerging Infectious Diseases, 1. Available: http://wwwnc.cdc.gov/eid/article/1/4/95-0408 [accessed February 15, 2015]
  55. Torrence, C, Compo, GP (1998) A practical guide to wavelet analysis. Bulletin of the American Meteorological Society 79: 61-78CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2016

Authors and Affiliations

  1. 1.Interdisciplinary Science ProgramThe New SchoolNew YorkUSA
  2. 2.Tishman Environment and Design CenterThe New SchoolNew YorkUSA
  3. 3.Department of GeographyMichigan State UniversityEast LansingUSA

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