High Frequency of Antimicrobial Drug Resistance of Diarrheagenic Escherichia coli in Infants in Peru

Theresa J. Ochoa Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Theresa J. Ochoa in
Current site
Google Scholar
PubMed
Close
,
Joaquím Ruiz Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Joaquím Ruiz in
Current site
Google Scholar
PubMed
Close
,
Margarita Molina Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Margarita Molina in
Current site
Google Scholar
PubMed
Close
,
Luis J. Del Valle Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Luis J. Del Valle in
Current site
Google Scholar
PubMed
Close
,
Martha Vargas Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Martha Vargas in
Current site
Google Scholar
PubMed
Close
,
Ana I. Gil Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Ana I. Gil in
Current site
Google Scholar
PubMed
Close
,
Lucie Ecker Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Lucie Ecker in
Current site
Google Scholar
PubMed
Close
,
Francesca Barletta Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Francesca Barletta in
Current site
Google Scholar
PubMed
Close
,
Eric Hall Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Eric Hall in
Current site
Google Scholar
PubMed
Close
,
Thomas G. Cleary Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Thomas G. Cleary in
Current site
Google Scholar
PubMed
Close
, and
Claudio F. Lanata Instituto de Medicina Tropical, Universidad Peruana Cayetano Heredia, Lima, Peru; Center for Infectious Diseases, University of Texas School of Public Health, Houston, Texas; Centre de Recerca en Salut Internacional de Barcelona, Hospital Clinic/Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Instituto de Investigación Nutricional, Lima, Peru; Departament d’Enginyeria Agroalimentària i Biotecnologia, Escola Superior d’Agricultura de Barcelona, Universitat Politécnica de Catalunya, Castelldefels, Spain; U.S. Naval Medical Research Center, Lima, Peru; Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima, Peru

Search for other papers by Claudio F. Lanata in
Current site
Google Scholar
PubMed
Close
Restricted access

In a prospective passive diarrhea surveillance cohort study of 1,034 infants of low socioeconomic communities in Lima, Peru, we determined the prevalence and antimicrobial drug susceptibility of the diarrheagenic Escherichia coli . The prevalence of diarrheagenic E. coli was 29% (161 of 557) in children with gastroenteritis and 30% (58 of 195) in the control group without diarrhea. The most common E. coli pathogens in diarrhea were enteroaggregative E. coli (EAEC) (14%), enteropathogenic E. coli (EPEC) (7%), diffusely adherent E. coli (DAEC) (4%), and enterotoxigenic E. coli (ETEC) (4%). Diarrheagenic E. coli as a group exhibited high levels of antimicrobial drug resistance in diarrheal cases to ampicillin (85%), cotrimoxazole (79%), tetracycline (65%), and nalidixic acid (28%). Among individual E. coli groups in patients with diarrhea, DAEC and EAEC exhibited significant higher frequencies of resistance to ampicillin, cotrimoxazole, tetracycline and nalidixic acid than EPEC and ETEC. Antimicrobial drug resistance to ampicillin and cotrimoxazole were more frequent in E. coli isolated from diarrheal samples than controls, which reflected greater antibiotic exposure in patients with gastroenteritis.

Author Notes

  • 1

    Bryce J, Boschi-Pinto C, Shibuya K, Black RE; WHO Child Health Epidemiology Reference Group, 2005 . WHO estimates of the causes of death in children. Lancet 365 :1147– 1152.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Niehaus MD, Moore SR, Patrick PD, Derr LL, Lorntz B, Lima AA, Guerrant RL, 2002 . Early childhood diarrhea is associated with diminished cognitive function 4 to 7 years later in children in a northeast Brazilian shantytown. Am J Trop Med Hyg 66 :590– 593.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM, 2002 . Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359 :564– 571.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Lorntz B, Soares AM, Moore SR, Pinkerton R, Gansneder B, Bovbjerg VE, Guyatt H, Lima AM, Guerrant RL, 2006 . Early childhood diarrhea predicts impaired school performance. Pediatr Infect Dis J 25 :513– 520.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Steiner TS, Samie A, Guerrant RL, 2006 . Infectious diarrhea: new pathogens and new challenges in developed and developing areas. Clin Infect Dis 43 :408– 410.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Petri WA, Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL, 2008 . Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 118 :1277– 1290.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Morris SS, Cousens SN, Kirkwood BR, Arthur P, Ross DA, 1996 . Is prevalence of diarrhea a better predictor of subsequent mortality and weight gain than diarrhea incidence? Am J Epidemiol 144 :582– 588.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Vila J, Vargas M, Casals C, Urassa H, Mshinda H, Schellemberg D, Gascon J, 1999 . Antimicrobial resistance of diarrheagenic Escherichia coli isolated from children under the age of 5 years from Ifakara, Tanzania. Antimicrob Agents Chemother 43 :3022– 3024.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Franzolin MR, Alves RC, Keller R, Gomes TA, Beutin L, Barreto ML, Milroy C, Strina A, Ribeiro H, Trabulsi LR, 2005 . Prevalence of diarrheagenic Escherichia coli in children with diarrhea in Salvador, Bahia, Brazil. Mem Inst Oswaldo Cruz 100 :359– 363.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Nguyen TV, Le PV, Le CH, Weintraub A, 2005 . Antibiotic resistance in diarrheagenic Escherichia coli and Shigella strains isolated from children in Hanoi, Vietnam. Antimicrob Agents Chemother 49 :816– 819.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Estrada-García T, Cerna JF, Pacheco-Gil L, Velázquez RF, Ochoa TJ, Torres J, DuPont HL, 2005 . Drug-resistant diarrheogenic Escherichia coli, Mexico. Emerg Infect Dis 11 :1306– 1308.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Nataro JP, Kaper JB, 1998 . Diarrheagenic Escherichia coli . Clin Microbiol Rev 11 :142– 201.

  • 13

    Guion CE, Ochoa TJ, Walker CM, Barletta F, Cleary TG, 2008 . Diagnosis of the diarrheagenic Escherichia coli using melting curve analysis of a real-time multiplex polymerase chain reaction. J Clin Microbiol 46 :1752– 1757.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Clinical Laboratory Standards Institute (CLSI), 2006 . Performance Standards for Antimicrobial Susceptibility Testing. Sixteenth Informational Supplement. M100-S16 . Vol. 26, No. 3. Wayne, PA: The Institute.

    • PubMed
    • Export Citation
  • 15

    Pickering LK, 2004 . Antimicrobial resistance among enteric pathogens. Semin Pediatr Infect Dis 15 :71– 77.

  • 16

    Cabada MM, White AC Jr, 2008 . Travelers’ diarrhea: an update on susceptibility, prevention, and treatment. Curr Gastroenterol Rep 10 :473– 479.

  • 17

    Leibovitz E, Janco J, Piglansky L, Press J, Yagupsky P, Reinhart H, Yaniv I, Dagan R, 2000 . Oral ciprofloxacin vs. intramuscular ceftriaxone as empiric treatment of acute invasive diarrhea in children. Pediatr Infect Dis J 19 :1060– 1067.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    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.

  • 19

    Vanden Eng J, Marcus R, Hadler JL, Imhoff B, Vugia DJ, Cieslak PR, Zell E, Deneen V, McCombs KG, Zansky SM, Hawkins MA, Besser RE, 2003 . Consumer attitudes and use of antibiotics. Emerg Infect Dis 9 :1128– 1135.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Magee JT, Pritchard EL, Fitzgerald KA, Dunstan FD, Howard AJ, 1999 . Antibiotic prescribing and antibiotic resistance in community practice: retrospective study, 1996–8. BMJ 319 :1239– 1240.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Bojalil R, Calva JJ, 1994 . Antibiotic misuse in diarrhea. A household survey in a Mexican community. J Clin Epidemiol 47 :147– 156.

  • 22

    Bartoloni A, Cutts F, Leoni S, Austin CC, Mantella A, Guglielmetti P, Roselli M, Salazar E, Paradisi F, 1998 . Patterns of antimicrobial use and antimicrobial resistance among healthy children in Bolivia. Trop Med Int Health 3 :116– 123.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Howteerakul N, Higginbotham N, Dibley MJ, 2004 . Antimicrobial use in children under five years with diarrhea in a central region province, Thailand. Southeast Asian J Trop Med Public Health 35 :181– 187.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Binsztein N, Picandet AM, Notario R, Patrito E, De Lesa ME, De Petris A, Maurel D, Nader O, Rivas M, Szefner M, Vergara M, 1999 . Antimicrobial resistance among species of Salmonella , Shigella , Escherichia , and Aeromonas isolated from children with diarrhea in 7 Argentinian centers [in Spanish]. Rev Latinoam Microbiol 41 :121– 126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Mandomando IM, Macete EV, Ruiz J, Sanz S, Abacassamo F, Vallès X, Sacarlal J, Navia MM, Vila J, Alonso PL, Gascon J, 2007 . Etiology of diarrhea in children younger than 5 years of age admitted in a rural hospital of southern Mozambique. Am J Trop Med Hyg 76 :522– 527.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Okeke IN, Laxminarayan R, Bhutta ZA, Duse AG, Jenkins P, O’Brien TF, Pablos-Mendez A, Klugman KP, 2005 . Antimicrobial resistance in developing countries. Part I: recent trends and current status. Lancet Infect Dis 5 :481– 493.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Okeke IN, Aboderin OA, Byarugaba DK, Ojo KK, Opintan JA, 2007 . Growing problem of multidrug-resistant enteric pathogens in Africa. Emerg Infect Dis 13 :1640– 1646.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Hien BT, Scheutz F, Cam PD, Serichantalergs O, Huong TT, Thu TM, Dalsgaard A, 2008 . Diarrheagenic Escherichia coli and Shigella strains isolated from children in a hospital case-control study in Hanoi, Vietnam. J Clin Microbiol 46 :996– 1004.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Lopes LM, Fabbricotti SH, Ferreira AJ, Kato MA, Michalski J, Scaletsky IC, 2005 . Heterogeneity among strains of diffusely adherent Escherichia coli isolated in Brazil. J Clin Microbiol 43 :1968– 1972.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Harrington SM, Dudley EG, Nataro JP, 2006 . Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol Lett 254 :12– 18.

  • 31

    Brueggemann AB, 2006 . Antibiotic resistance mechanisms among pediatric respiratory and enteric pathogens. Pediatr Infect Dis J 25 :969– 973.

  • 32

    Barbosa TM, Levy SB, 2000 . Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA . J Bacteriol 182 :3467– 3474.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Maira-Litrán T, Allison DG, Gilbert P, 2000 . Expression of the multiple antibiotic resistance operon ( mar ) during growth of Escherichia coli as a biofilm. J Appl Microbiol 88 :243– 247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Gassama A, Aïdara-Kane A, Chainier D, Denis F, Ploy MC, 2004 . Integron-associated antibiotic resistance in enteroaggregative and enteroinvasive Escherichia coli . Microb Drug Resist 10 :27– 30.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Okeke IN, Steinrück H, Kanack KJ, Elliott SJ, Sundström L, Kaper JB, Lamikanra A, 2002 . Antibiotic-resistant cell-detaching Escherichia coli strains from Nigerian children. J Clin Microbiol 40 :301– 305.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Nwaneshiudu AI, Mucci T, Pickard DJ, Okeke IN, 2007 . A second large plasmid encodes conjugative transfer and antimicrobial resistance in O119:H2 and some typical O111 enteropathogenic Escherichia coli strains. J Bacteriol 189 :6074– 6079.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1538 1445 361
Full Text Views 491 13 1
PDF Downloads 191 7 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save