World Health Organization, 2013. Fact sheet on Diarrheal disease No. 330. Available at: http://www.who.int.
World Health Organization, 2013. End Preventable Deaths: Global Action Plan for Prevention and Control of Pneumonia and Diarrhea. France: UNICEF.
Kotloff K, Nataro J, Blackwelder W, Nasrin D, Farag T, Panchalingam S, Wu Y, Sow S, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso P, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng J, Omore R, Oundo J, Hossain A, Das S, Ahmed S, Qureshi S, Quadri F, Adegbola R, Antonio M, Hossain M, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly C, Mintz E, Berkeley L, Muhsen K, Sommerfelt H, Robins-Browne R, Levine M, 2013. Burden and aetiology of diarrheal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
Davidson G, Barnes G, Bass D, Cohen M, Fasano A, Fontaine O, Guandalini S, 2002. Infectious diarrhea in children: Working Group Report of the First World Congress of Pediatric Gastroenterology, Hepatology,and Nutrition. J Pediatr Gastroenterol Nutr 35 (Suppl 2): S143–S150.
Fauci A, Morens D, 2012. The perpetual challenge of infectious diseases. N Engl J Med 366: 454–461.
Thielman N, Guerrant R, 2004. Acute infectious diarrhea. N Engl J Med 350: 38–47.
Eisenberg J, Brookhart A, Rice G, Brown M, Cloford J, 2002. Disease transmission models for public health decision making: analysis of epidemic and endemic conditions caused by waterborne pathogens. Environ Health Perspect 110: 783–790.
Cabral J, 2010. Water microbiology. Bacterial pathogens and water. Int J Environ Res Public Health 7: 3657–3703.
Graham S, 2002. Salmonellosis in children in developing and developed countries and populations. Curr Opin Infect Dis 15: 507–512.
Ministerio de Salud Pública del Ecuador, 2012. Indicadores del Sistema de Vigilancia Epidemiológica SIVE-ALERTA. Available at: http://www.salud.gob.ec/. Dirección Nacional de Vigilancia Epidemiológica.
Guderian R, Ordoñez G, Bozano R, 1987. Diarrhea Aguda Asociada a Campylobacter y Otros Agentes Patógenos En Quito, Ecuador. Bol Oficina Sanit Panam 102: 333–339.
Briand S, Leyrit M, Escalante S, 1994. Proyecto Atucucho: Proyecto Franco-Ecuatoriano para el Control de las Enfermedades Diarreicas y Cólera. Quito: Autor.
Guderian R, Sandoval C, Mackenzie C, 1986. Crytosporidiosis in Ecuadorian children with acute diarrhea. J Trop Pediatr 32: 290–292.
Vieira N, Bates S, Solberg O, Ponce K, Howsmon R, Cevallos W, Trueba G, Riley L, Eisenberg J, 2007. High prevalence of enteroinvasive Escherichia coli isolated in a remote region of northern coastal Ecuador. Am J Trop Med Hyg 76: 528–533.
Escobar J, Bhavnani D, Trueba G, Ponce K, Cevallos W, Eisenberg J, 2012. Plesiomonas shigelloides Infection, Ecuador, 2004–2008. Emerg Infect Dis 18: 322–324.
Bhavnani D, Goldstick J, Cevallos W, Trueba G, Eisenberg J, 2012. Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: evidence from a community-based study in northwestern Ecuador. Am J Epidemiol 176: 387–395.
Guambo J, 2012. Detección y Genotipifificación de Norovirus GI/GII mediante Real Time (TaqMan) Reverse Transcription Polymerase Chain Reaction (RT-PCR) en muestras de Heces de Niños menores de 5 años de edad que presentaron episodios esporádicos de Diarrea Aguda en el Cantón Quinindé, Provincia de Esmeraldas-Ecuador. Available at: http://repositorio.espe.edu.ec.
Suzuki H, Aman Y, Kinebuchi H, Gutierrez Vera E, Davila A, Lopez J, Gustabo R, Konno T, Ishida N, 1981. Rotavirus infection in children with acute gastroenteritis in Ecuador. Am J Trop Med Hyg 30: 293–294.
Suzuki H, Sato T, Kitaoka S, Tazawa F, Konno T, Amano Y, Alava Alprecht A, Gutiérrez Vera E, Lopez Villalta J, Numazaki Y, 1986. Epidemiology of rotavirus in Guayaquil, Ecuador. Am J Trop Med Hyg 35: 372–375.
Endara P, Trueba G, Solberg O, Bates S, Ponce K, Cevallos W, Matthijnssens J, Eisenberg J, 2007. Symptomatic and subclinical infection with rotavirus P[8]G9, rural Ecuador. Emerg Infect Dis 13: 574–580.
Naranjo A, Cedeño C, Teran E, Castello A, 2008. Prevalence of VP4 and VP7 genotypes of human rotavirus in Ecuadorian children with acute diarrhea. J Med Virol 80: 1106–1111.
Hasing M, Trueba G, Baquero M, Ponce K, Cevallos W, Solberg O, Eisenberg J, 2009. Rapid changes in rotaviral genotypes in Ecuador. J Med Virol 81: 2109–2113.
Mann C, 2003. Observational research methods. Research design II: cohort, cross sectional, and case-control studies. Emerg Med J 20: 54–60.
Breslow N, 1996. Statistics in epidemiology: the case-control study. J Am Stat Assoc 91: 14–28.
Guerrant R, Kirchhoff L, Shields D, Nations M, Leslie J, Sousa M, McClelland K, Trowbridge F, Hughes J, 1983. Prospective study of diarrheal illnesses in northeastern Brazil: patterns of disease, nutritional impact, etiologies, and risk factors. J Infect Dis 148: 986–997.
Tardelli T, Rassi V, MacDonald K, Silva A, Trabulsi L, Vieira M, Guth B, Candeias J, Ivey C, Toledo M, Blake P, 1991. Enteropathogens associated with acute diarrheal disease in urban infants in Sao Paulo, Brazil. J Infect Dis 164: 331–337.
Ochoa T, Ecker L, Baletta F, Mispireta M, Gil A, Contreras C, Molina M, Amemiya I, Verastequi H, Hall E, Cleary T, Lanata C, 2009. Age-related susceptibility to infection with diarrheagenic Escherichia coli among infants from Periurban areas in Lima, Peru. Clin Infect Dis 49: 1694–1702.
Ochoa T, Barletta F, Contreras C, Mercado E, 2008. New insights into the epidemiology of enteropathogenic Escherichia coli infection. Trans R Soc Trop Med Hyg 102: 852–856.
Instituto Nacional de Estadísticas y Censos, 2010. Censo de Población y Vivienda 2010. Available at: www.ecuadorencifras.com.
Instituto Nacional de Meteorología e Hidrología, 2013. Boletín Meteorológico Año XXXVII No. 457 Mes Marzo 2013. Dirección Gestión Meteorológica Estudios e Investigaciones Meteorológicas. Quito, Ecuador.
Instituto Nacional de Meteorología e Hidrología, 2013. Boletín Meteorológico Año XXXVII No. 458 Mes Abril 2013. Dirección Gestión Meteorológica Estudios e Investigaciones Meteorológicas. Quito, Ecuador.
Instituto Nacional de Meteorología e Hidrología, 2013. Anuario Meteorológico 2011 No. 51. Dirección de Gestión Meteorológica Procesamiento y Edición: SIGIHM.
Instituto Nacional de Meteorología e Hidrología, 2013. Boletín Meteorológico Año XXXVII No. 461 Mes Julio 2013. Dirección Gestión Meteorológica Estudios e Investigaciones Meteorológicas. Quito, Ecuador.
Instituto Nacional de Meteorología e Hidrología, 2013. Boletín Meteorológico Año XXXVII No. 462 Mes Agosto 2013. Dirección Gestión Meteorológica Estudios e Investigaciones Meteorológicas. Quito, Ecuador.
Linton D, Lawson A, Owen R, Stamley J, 1997. PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J Clin Microbiol 35: 2568–2572.
Persson S, Olsen K, 2005. Multiplex PCR for identification of Campylobacter coli and Campylobacter jejuni from pure cultures and directly on stool samples. J Med Microbiol 54: 1043–1047.
Gunzburg S, Tornieporth N, Riley L, 1995. Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle-forming pilus gene. J Clin Microbiol 33: 1375–1377.
Tornieporth N, 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J Clin Microbiol 33: 1371–1374.
Pollard D, Johnson W, Lior H, Tyler S, Rozee K, 1990. Rapid and specific detection of verotoxin genes in Escherichia coli by the polymerase chain reaction. J Clin Microbiol 28: 540–545.
Ramos F, Morán P, González E, García G, Ramiro M, Gómez A, León DE, Mdel C, Melendro EI, Valadez A, Ximénez C, 2005. High prevalence rate of Entamoeba histolytica asymptomatic infection in a rural Mexican community. Am J Trop Med Hyg 73: 87–91.
Scallan E, Hoekstra R, Angulo F, Tauxe R, Widdowson M, Roy S, Jones J, Griffin P, 2011. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 17: 16–22.
Muhsen K, Levine M, 2012. A systematic review and meta-analysis of the association between Giardia lamblia and endemic pediatric diarrhea in developing countries. Clin Infect Dis 55 (Suppl 4): S271–S293.
Bilenko N, Levy A, Dagan R, Deckelbaum R, El-On Y, Fraser D, 2004. Does co-infection with Giardia lamblia modulate the clinical characteristics of enteric infections in young children? Eur J Epidemiol 19: 877–883.
Gonzales L, Sanchez S, Zambrana S, Iñiguez V, Wiklund G, Svennerholm A, Sjöling A, 2013. Molecular characterization of enterotoxigenic Escherichia coli ETEC isolated from children with diarrhea during a four year period (2007–2010) in Bolivia. J Clin Microbiol 51: 1219–1225. doi:10.1128/JCM.02971-12.
Schnack F, De-Medeiros L, Barbosa P, Storch L, Meyer M, Martinello C, Barrichello T, Povoa M, Cavasini C, Dantas R, 2003. Enteropathogens associated with diarrheal disease in infants (< 5 years old) in a population sample in Greater Metropolitan Criciúma, Santa Catarina State, Brazil. Cad Saude Publica 19: 1205–1208.
Diniz-Santos D, Santana J, Barreto J, Andrade M, Silva L, 2005. Epidemiological and microbiological aspects of acute bacterial diarrhea in children from Salvador, Bahia, Brazil. Braz J Infect Dis 9: 77–83.
Orlandi P, Magalhães G, Matos N, Silva T, Penatti M, Nogueira P, Pereira da Silva L, 2006. Etiology of diarrheal infections in children of Porto Velho (Rondonia, Western Amazon region, Brazil). Braz J Med Biol Res 39: 507–517.
Moreno A, Filho A, Gomes A, Ramos S, Montemor L, Tavares V, Filho S, Irino K, Martinez M, 2008. Etiology of childhood diarrhea in the northeast of Brazil: significant emergent diarrheal pathogens. Diagn Microbiol Infect Dis 66: 50–57.
Trueba G, Garcés V, Colman R, Seymour M, Vogler A, Keim P, 2013. Escherichia coli O157:H7 in Ecuador: animal reservoirs, yet no human disease. Vector Borne Zoonotic Dis 13: 295–298.
Levine M, Robins-Browne R, 2012. Factors that explain excretion of enteric pathogens by persons without diarrhea. Clin Infect Dis 55 (Suppl 4): S303–S311.
Fernández H, 2011. Campylobacter and campylobacteriosis: a view from South America. Rev Peru Med Exp Salud Publica 28: 121–127.
Roux F, Sproston E, Rotariu O, MacRae M, Sheppard SK, 2013. Elucidating the aetiology of human Campylobacter coli infections. PLoS ONE 8: e64504.
Tosin I, Machado R, 1995. Occurrence of Campylobacter spp. among food handlers in hospital kitchens in urban areas of the southern region of Brazil. Rev Saude Publica 29: 472–477.
Torres M, Pírez M, Schelotto F, Varela G, Parodi V, Allende F, Falconi E, Dell'Acqua L, Gaione P, Méndez M, Ferrari A, Montano A, Zanetta E, Acuña A, Chiparelli H, Ingold E, 2001. Etiology of children's diarrhea in Montevideo, Uruguay: associated pathogens and unusual isolates. J Clin Microbiol 39: 2134–2139.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 12 | 12 | 12 |
Full Text Views | 796 | 258 | 3 |
PDF Downloads | 383 | 121 | 2 |
Continued success in decreasing diarrheal disease burden requires targeted interventions. To develop such interventions, it is crucial to understand which pathogens cause diarrhea. Using a case-control design we tested stool samples, collected in both rural and urban Ecuador, for 15 pathogenic microorganisms. Pathogens were present in 51% of case and 27% of control samples from the urban community, and 62% of case and 18% of control samples collected from the rural community. Rotavirus and Shigellae were associated with diarrhea in the urban community; co-infections were more pathogenic than single infection; Campylobacter and Entamoeba histolytica were found in large numbers in cases and controls; and non-typhi Salmonella and enteropathogenic Escherichia coli were not found in any samples. Consistent with the Global Enteric Multicenter Study, focused in south Asia and sub-Saharan Africa, we found that in Ecuador a small group of pathogens accounted for a significant amount of the diarrheal disease burden.
Financial support: This study was supported by grant No. RO1-AI050038 from the National Institute of Allergy and Infectious Diseases (NIAID) and the Center for Global Health at the University of Michigan.
Authors' addresses: Gabriela Vasco, Gabriel Trueba, and Thamara Andrade, Microbiology Institute, Universidad San Francisco de Quito, Quito, Ecuador, E-mails: piavas_rc@hotmail.com, gtrueba@usfq.edu.ec, and thamaraandrade@yahoo.com. Richard Atherton, Manuel Calvopiña, and William Cevallos, Centro de Biomedicina, Universidad Central del Ecuador, Quito, Ecuador, E-mails: richard.atherton@hotmail.co.uk, mcalvopina@gmail.com, and wcalvopina@gmail.com. Martha Eguiguren, Centro de Salud Guamaní, Ministerio de Salud Pública, Quito, Ecuador, E-mail: m._eguiguren@hotmail.com. Joseph N. S. Eisenberg, School of Public Health, University of Michigan, CA, E-mail: jnse@umich.edu.