O'Ryan M, Prado V, Pickering LK, 2005. A millennium update on pediatric diarrheal illness in the developing world. Semin Pediatr Infect Dis 16: 125–136.
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM, 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicentre Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB, 2013. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26: 822–880.
Guion CE, Ochoa TJ, Walker CM, Barletta F, Cleary TG, 2008. Detection of diarrheagenic Escherichia coli by use of melting-curve analysis and real-time multiplex PCR. J Clin Microbiol 46: 1752–1757.
Lanata CF, Mendoza W, 2002. Improving Diarrhoea Estimates. Available at: http://www.who.int/child_adolescent_health/documents/pdfs/improving_diarrhoea_estimates.pdf. Accessed February 24, 2016.
Al-Gallas N, Bahri O, Bouratbeen A, Haasen AB, Aissa RB, 2007. Etiology of acute diarrhea in children and adults in Tunis, Tunisia, with emphasis on diarrheagenic Escherichia coli: prevalence, phenotyping, and molecular epidemiology. Am J Trop Med Hyg 77: 571–582.
Ifeanyi CI, Ikeneche NF, Bassey BE, Al-Gallas N, Ben Aissa R, Boudabous A, 2015. Diarrheagenic Escherichia coli pathotypes isolated from children with diarrhea in the Federal Capital Territory Abuja, Nigeria. J Infect Dev Ctries 9: 165–174.
Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S, Edberg SC, Braden CR, Glenn Morris J Jr, Hirshon JM, 2006. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis 43: 402–407.
Ochoa TJ, Ecker L, Barletta F, Mispireta ML, Gil AI, Contreras C, Molina M, Amemiya I, Verastegui H, Hall ER, Cleary TG, Lanata CF, 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 TJ, Mercado EH, Durand D, Rivera FP, Mosquito S, Contreras C, Riveros M, Lluque A, Barletta F, Prada A, Ruiz J, 2011. Frequency and pathotypes of diarrheagenic Escherichia coli in Peruvian children with and without diarrhea. Rev Peru Med Exp Salud Publica 28: 13–20.
Levine MM, Ferreccio C, Prado V, Cayazzo M, Abrego P, Martinez J, Maggi L, Baldini MM, Martin W, Maneval D, Bradford K, Guers L, Lior H, Wasserman SS, Nataro JP, 1993. Epidemiologic studies of Escherichia coli diarrheal infections in a low socioeconomic level peri-urban community in Santiago, Chile. Am J Epidemiol 138: 849–869.
Qadri F, Saha A, Ahmed T, Al Tarique A, Begum YA, Svennerholm AM, 2007. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect Immun 75: 3961–3968.
Steiner TS, Lima AA, Nataro JP, Guerrant RL, 1998. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis 177: 88–96.
Baqui AH, Black RE, Yunus M, Hoque AR, Chowdhury HR, Sack RB, 1991. Methodological issues in diarrhoeal diseases epidemiology: definition of diarrhoeal episodes. Int J Epidemiol 20: 1057–1063.
Tobias J, Kassem E, Rubinstein U, Bialik A, Vutukuru SR, Navaro A, Rokney A, Valinsky L, Ephros M, Cohen D, Muhsen K, 2015. Involvement of main diarrheagenic Escherichia coli, with emphasis on enteroaggregative E. coli, in severe non-epidemic pediatric diarrhea in a high-income country. BMC Infect Dis 15: 79.
Osawa K, Raharjo D, Wasito EB, Harijono S, Shigemura K, Osawa R, 2013. Frequency of diarrheagenic Escherichia coli among children in Surabaya, Indonesia. Jpn J Infect Dis 66: 446–448.
Lozer DM, Souza TB, Monfardini MV, Vicentini F, Kitagawa SS, Scaletsky IC, Spano LC, 2013. Genotypic and phenotypic analysis of diarrheagenic Escherichia coli strains isolated from Brazilian children living in low socioeconomic level communities. BMC Infect Dis 13: 418.
Araujo JM, Tabarelli GF, Aranda KS, Fabbricotti SH, Mendes CMF, Fagundes-Neto U, Scaletsky IC, 2007. Typical enteroaggregative and atypical enteropathogenic types of Escherichia coli are the most prevalent diarrhea-associated pathotypes among Brazilian children. J Clin Microbiol 45: 3396–3399.
Moreno AC, Fernandes Filho A, Gomes TAT, Ramos STS, Montemor KPG, Tavares VC, Santos Filho L, Irino K, Martinez MB, 2010. Etiology of childhood diarrhea in the northeast of Brazil: significant emergent diarrheal pathogens. Diagn Microbiol Infect Dis 66: 50–57.
Nguyen TV, Le Van P, Huy L, Gia KN, Weintraub A, 2005. Detection and characterization of diarrheagenic Escherichia coli from young children in Hanoi, Vietnam. J Clin Microbiol 43: 755–760.
Estrada-García T, Lopez-Saucedo C, Thompson-Bonilla R, Abonce M, Lopez-Hernandez D, Santos JI, Rosado JL, DuPont HL, Long KZ, 2009. Association of diarrheagenic Escherichia coli pathotypes with infection and diarrhea among Mexican children and association of atypical enteropathogenic E. coli with acute diarrhea. J Clin Microbiol 47: 93–98.
Scaletsky IC, Fabbricotti SH, Carvalho RLB, Nunes CR, Maranhão HS, Morais MB, Fagundes-Neto U, 2002. Diffusely adherent Escherichia coli as a cause of acute diarrhea in young children in northeast Brazil: a case-control study. J Clin Microbiol 40: 645–648.
Roche JK, Cabel A, Sevilleja J, Nataro J, Guerrant RL, 2010. Enteroaggregative E. coli (EAEC) impairs growth and malnutrition worsens EAEC infection: a novel murine model of the infection malnutrition cycle. J Infect Dis 202: 506–514.
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Diarrheagenic Escherichia coli (DEC) are common pathogens of childhood gastrointestinal infections worldwide. To date, research tracking DEC has mainly been completed in urban areas. This study aims to determine the prevalence and pathotype distribution of DEC strains in children from rural Peruvian communities and to establish their association with malnutrition. In this prospective cohort, 93 children aged 6–13 months from rural communities of Urubamba (Andes) and Moyobamba (jungle) were followed for 6 months. Diarrheal and control stool samples were analyzed using multiplex real-time polymerase chain reaction to identify the presence of virulence genes of DEC strains. The overall isolation rate of DEC was 43.0% (352/820). Enteroaggregative E. coli (EAEC, 20.4%), enteropathogenic E. coli (EPEC, 14.2%), and diffusely aggregative E. coli (DAEC, 11.0%) were the most prevalent pathotypes. EAEC was more frequently found in Moyobamba samples (P < 0.01). EPEC was the only strain significantly more frequent in diarrheal than asymptomatic control samples (P < 0.01). DEC strains were more prevalent among younger children (aged 6–12 months, P < 0.05). A decline in height-for-age Z-score (HAZ) was observed in 75.7% of children overall. EAEC was more frequently isolated among children who had a greater HAZ decline (P < 0.05). In conclusion, DEC strains were frequently found in stool samples from children in rural communities of the highlands and jungle of Peru. In addition, children with a greater decline in their growth rate had higher EAEC isolation rates, highlighting the importance of this pathogen in child malnutrition.
Financial support: This work was supported by the Thrasher Research Funds (Thrasher Award No. 11955) to Mara Zambruni and Theresa J. Ochoa.
Authors' addresses: Gonzalo J. Acosta, Natalia I. Vigo, David Durand, Maribel Riveros, and Sara Arango, Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: gjacosta89@gmail.com, natalia.vigo@outlook.com, david.durand@upch.pe, maribel.riveros@upch.pe, and sara.arango29@gmail.com. Mara Zambruni, Department of Pediatric Infectious Diseases, University of Texas Medical Branch, Galveston, TX, E-mail: mazambru@utmb.edu. Theresa J. Ochoa, Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Lima, Peru, and University of Texas Health Science Center at Houston, School of Public Health, Houston, TX, E-mails: theresa.j.ochoa@uth.tmc.edu or theresa.ochoa@upch.pe.
O'Ryan M, Prado V, Pickering LK, 2005. A millennium update on pediatric diarrheal illness in the developing world. Semin Pediatr Infect Dis 16: 125–136.
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM, 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicentre Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB, 2013. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26: 822–880.
Guion CE, Ochoa TJ, Walker CM, Barletta F, Cleary TG, 2008. Detection of diarrheagenic Escherichia coli by use of melting-curve analysis and real-time multiplex PCR. J Clin Microbiol 46: 1752–1757.
Lanata CF, Mendoza W, 2002. Improving Diarrhoea Estimates. Available at: http://www.who.int/child_adolescent_health/documents/pdfs/improving_diarrhoea_estimates.pdf. Accessed February 24, 2016.
Al-Gallas N, Bahri O, Bouratbeen A, Haasen AB, Aissa RB, 2007. Etiology of acute diarrhea in children and adults in Tunis, Tunisia, with emphasis on diarrheagenic Escherichia coli: prevalence, phenotyping, and molecular epidemiology. Am J Trop Med Hyg 77: 571–582.
Ifeanyi CI, Ikeneche NF, Bassey BE, Al-Gallas N, Ben Aissa R, Boudabous A, 2015. Diarrheagenic Escherichia coli pathotypes isolated from children with diarrhea in the Federal Capital Territory Abuja, Nigeria. J Infect Dev Ctries 9: 165–174.
Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S, Edberg SC, Braden CR, Glenn Morris J Jr, Hirshon JM, 2006. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis 43: 402–407.
Ochoa TJ, Ecker L, Barletta F, Mispireta ML, Gil AI, Contreras C, Molina M, Amemiya I, Verastegui H, Hall ER, Cleary TG, Lanata CF, 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 TJ, Mercado EH, Durand D, Rivera FP, Mosquito S, Contreras C, Riveros M, Lluque A, Barletta F, Prada A, Ruiz J, 2011. Frequency and pathotypes of diarrheagenic Escherichia coli in Peruvian children with and without diarrhea. Rev Peru Med Exp Salud Publica 28: 13–20.
Levine MM, Ferreccio C, Prado V, Cayazzo M, Abrego P, Martinez J, Maggi L, Baldini MM, Martin W, Maneval D, Bradford K, Guers L, Lior H, Wasserman SS, Nataro JP, 1993. Epidemiologic studies of Escherichia coli diarrheal infections in a low socioeconomic level peri-urban community in Santiago, Chile. Am J Epidemiol 138: 849–869.
Qadri F, Saha A, Ahmed T, Al Tarique A, Begum YA, Svennerholm AM, 2007. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect Immun 75: 3961–3968.
Steiner TS, Lima AA, Nataro JP, Guerrant RL, 1998. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis 177: 88–96.
Baqui AH, Black RE, Yunus M, Hoque AR, Chowdhury HR, Sack RB, 1991. Methodological issues in diarrhoeal diseases epidemiology: definition of diarrhoeal episodes. Int J Epidemiol 20: 1057–1063.
Tobias J, Kassem E, Rubinstein U, Bialik A, Vutukuru SR, Navaro A, Rokney A, Valinsky L, Ephros M, Cohen D, Muhsen K, 2015. Involvement of main diarrheagenic Escherichia coli, with emphasis on enteroaggregative E. coli, in severe non-epidemic pediatric diarrhea in a high-income country. BMC Infect Dis 15: 79.
Osawa K, Raharjo D, Wasito EB, Harijono S, Shigemura K, Osawa R, 2013. Frequency of diarrheagenic Escherichia coli among children in Surabaya, Indonesia. Jpn J Infect Dis 66: 446–448.
Lozer DM, Souza TB, Monfardini MV, Vicentini F, Kitagawa SS, Scaletsky IC, Spano LC, 2013. Genotypic and phenotypic analysis of diarrheagenic Escherichia coli strains isolated from Brazilian children living in low socioeconomic level communities. BMC Infect Dis 13: 418.
Araujo JM, Tabarelli GF, Aranda KS, Fabbricotti SH, Mendes CMF, Fagundes-Neto U, Scaletsky IC, 2007. Typical enteroaggregative and atypical enteropathogenic types of Escherichia coli are the most prevalent diarrhea-associated pathotypes among Brazilian children. J Clin Microbiol 45: 3396–3399.
Moreno AC, Fernandes Filho A, Gomes TAT, Ramos STS, Montemor KPG, Tavares VC, Santos Filho L, Irino K, Martinez MB, 2010. Etiology of childhood diarrhea in the northeast of Brazil: significant emergent diarrheal pathogens. Diagn Microbiol Infect Dis 66: 50–57.
Nguyen TV, Le Van P, Huy L, Gia KN, Weintraub A, 2005. Detection and characterization of diarrheagenic Escherichia coli from young children in Hanoi, Vietnam. J Clin Microbiol 43: 755–760.
Estrada-García T, Lopez-Saucedo C, Thompson-Bonilla R, Abonce M, Lopez-Hernandez D, Santos JI, Rosado JL, DuPont HL, Long KZ, 2009. Association of diarrheagenic Escherichia coli pathotypes with infection and diarrhea among Mexican children and association of atypical enteropathogenic E. coli with acute diarrhea. J Clin Microbiol 47: 93–98.
Scaletsky IC, Fabbricotti SH, Carvalho RLB, Nunes CR, Maranhão HS, Morais MB, Fagundes-Neto U, 2002. Diffusely adherent Escherichia coli as a cause of acute diarrhea in young children in northeast Brazil: a case-control study. J Clin Microbiol 40: 645–648.
Roche JK, Cabel A, Sevilleja J, Nataro J, Guerrant RL, 2010. Enteroaggregative E. coli (EAEC) impairs growth and malnutrition worsens EAEC infection: a novel murine model of the infection malnutrition cycle. J Infect Dis 202: 506–514.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1593 | 1402 | 73 |
Full Text Views | 481 | 10 | 2 |
PDF Downloads | 233 | 14 | 4 |