Volume 82, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Few studies have examined the influence of individual-, household-, and community-scale risk factors on carriage of resistant commensal bacteria. We determined children's medical, agricultural, and environmental exposures by household, pharmacy, and health facility surveys and cultures of children, mothers' hands, household animals, and market chickens in Peru. Among 522 children with a positive stool culture, by log-binomial regression, using “any antibiotic” and 1–14 (versus 0) sulfa doses in the past 3 months increased children's risk, respectively, for ampicillin- and sulfamethoxazole-resistant carriage ( = 0.01–0.02). Each household member taking “any antibiotic” increased children's risk for sulfamethoxazole- and multidrug-resistant carriage ( < 0.0001). Residence in a zone where a larger proportion of households served home-raised chicken (as contrasted with intensively antibiotic-raised market chicken) protected against carrying resistant to all drugs ( = 0.0004–0.04). Environmental contamination with drug-resistant bacteria appeared to significantly contribute to children's carriage of antibiotic-resistant .


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  1. Harrison PF, Lederberg J, , 1998. Antimicrobial resistance: issues and options. Workshop Report: Forum on Emerging Infections. Institute of Medicine. Washington, DC: National Academy Press. [Google Scholar]
  2. Swartz MN, , 1997. Use of antimicrobial agents and drug resistance. N Engl J Med 337: 491492.[Crossref] [Google Scholar]
  3. Austin DJ, Kakehashi M, Anderson RM, , 1997. The transmission dynamics of antibiotic-resistant bacteria: the relationship between resistance in commensal organisms and antibiotic consumption. Proc Biol Sci 264: 16291638.[Crossref] [Google Scholar]
  4. Chopra I, Roberts M, , 2001. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65: 232260.[Crossref] [Google Scholar]
  5. Tenover FC, McGowan JE, Jr, 1996. Reasons for the emergence of antibiotic resistance. Am J Med Sci 311: 916.[Crossref] [Google Scholar]
  6. Austin DJ, Kristinsson KG, Anderson RM, , 1999. The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. Proc Natl Acad Sci USA 96: 11521156.[Crossref] [Google Scholar]
  7. Gold HS, Moellering RC, , 1996. Drug therapy: antimicrobial-drug resistance. N Engl J Med 335: 14451453.[Crossref] [Google Scholar]
  8. Kristinsson KG, , 1997. Effect of antimicrobial use and other risk factors on antimicrobial resistance in pneumococci. Microb Drug Resist 3: 117123.[Crossref] [Google Scholar]
  9. Arason VA, Kristinsson KG, Sigurdsson JA, Stefansdottir G, Molstad S, Gudmundsson S, , 1996. Do antimicrobials increase the carriage rate of penicillin resistant pneumococci in children? Cross sectional prevalence study. BMJ 313: 387391.[Crossref] [Google Scholar]
  10. Seppala H, Klaukka T, Vuopio-Varkila J, Muotiala A, Helenius H, Lager K, Houvinen P, , 1997. The effect of changes in the consumption of macrolide antibiotics on erythromycin resistance in group A streptococci in Finland. Finnish Study Group for Antimicrobial Resistance. N Engl J Med 337: 441446.[Crossref] [Google Scholar]
  11. Hannah EL, Angulo FJ, Johnson JR, Haddadin B, Williamson J, Samore MH, . 2005. Drug-resistant Escherichia coli, rural Idaho. Emerg Infect Dis 11: 16141617.[Crossref] [Google Scholar]
  12. Samore MH, Magill MK, Alder SC, Severina E, Morrison-de Boer L, Lyon JL, Carroll K, Leary J, Stone MB, Bradford D, Reading J, Tomasz A, Sande MA, , 2001. High rates of multiple antibiotic resistance in Streptococcus pneumoniae from healthy children living in isolated rural communities: association with cephalosporin use and intrafamilial transmission. Pediatrics 108: 856865.[Crossref] [Google Scholar]
  13. Lietzau S, Raum E, von Baum H, Marre R, Brenner H, , 2007. Household contacts were key factor in children's colonization with resistant Escherichia coli in community setting. J Clin Epidemiol 60: 11491155.[Crossref] [Google Scholar]
  14. Walson JL, Marshall B, Pokhrel BM, Kafle KK, Levy SB, , 2001. Carriage of antibiotic-resistant fecal bacteria in Nepal reflects proximity to Kathmandu. J Infect Dis 184: 11631169.[Crossref] [Google Scholar]
  15. Witte W, , 1998. Medical consequences of antibiotic use in agriculture. Science 279: 996997.[Crossref] [Google Scholar]
  16. Chen S, Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott PF, Ayers S, Meng J, , 2004. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 70: 17.[Crossref] [Google Scholar]
  17. Price LB, Graham JP, Lackey LG, Roess A, Vailes R, Silbergeld E, , 2007. Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environ Health Perspect 115: 17381742.[Crossref] [Google Scholar]
  18. Wegener HC, Aarestrup FM, Jensen LB, Hammerum AM, Bager F, , 1999. Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg Infect Dis 5: 329335.[Crossref] [Google Scholar]
  19. Manges AR, Smith SP, Lau BJ, Nubal CJ, Eisenberg JH, Dietrich PS, Riley LW, , 2007. Retail meat consumption and the acquisition of antimicrobial resistant Escherichia coli causing urinary tract infections: a case-control study. Foodborne Pathog Dis 4: 419431.[Crossref] [Google Scholar]
  20. Kassenborg HD, Smith KE, Vugia DJ, Rabatsky-Her T, Bates MR, Carter MA, Dumas NB, Cassidy MP, Marano N, Tauxe RV, Angulo FJ, , for the Emerging Infections Program FoodNet Working Group, 2004. Fluoroquinolone-resistant Campylobacter infections: eating poultry outside of the home and foreign travel are risk factors. Clin Inf Dis 38 (Suppl 3): S279S284. [Google Scholar]
  21. Garau J, Xercavins M, Rodriguez-Carballeira M, Gomez-Vera JR, Coll I, Vidal D, Llovet T, Ruiz-Bremon A, , 1999. Emergence and dissemination of quinolone-resistant Escherichia coli in the community. Antimicrob Agents Chemother 43: 27362741. [Google Scholar]
  22. Baquero F, Negri MC, Morosini MI, Blazquez J, , 1997. The antibiotic selective process: concentration-specific amplification of low-level resistant populations. Ciba Found Symp 207: 93105. [Google Scholar]
  23. Indalo AA, , 1997. Antibiotic sale behavior in Nairobi: a contributing factor to antimicrobial drug resistance. East Afr Med J 74: 121123. [Google Scholar]
  24. Murray J, Mosazghi A, Kifleyesus B, Orobaton N, , 1998. Rural Drug Vendors in Eritrea: A Study of Practices and Training Needs. Arlington, VA: published for USAID by the Basic Support for Institutionalizing Child Survival (BASICS) Project. [Google Scholar]
  25. Okeke IN, Lamikanra A, Edelman R, , 1999. Socioeconomic and behavioral factors leading to acquired bacterial resistance to antibiotics in developing countries. Emerg Infect Dis 5: 1827.[Crossref] [Google Scholar]
  26. Bartoloni A, Bartalesi F, Mantella A, Dell'Amico E, Roselli M, Strohmeyer M, Barahona HG, Barron VP, Paradisi F, Rossolini GM, , 2004. High prevalence of acquired antimicrobial resistance unrelated to heavy antimicrobial consumption. J Infect Dis 189: 12911294.[Crossref] [Google Scholar]
  27. Gaur A, Ramteke PW, Pathak SP, Bhattacherjee JW, , 1992. Transferable antibiotic resistance among thermotolerant coliforms from rural drinking water in India. Epidemiol Infect 109: 113120. [Google Scholar]
  28. Schmidt AS, Bruun MS, Dalsgaard I, Larsen JL, , 2001. Incidence, distribution and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile Aeromanads from a fish farming environment. Appl Environ Microbiol 67: 56755682.[Crossref] [Google Scholar]
  29. Andersen SR, Sandaa RA, , 1994. Distribution of tetracycline resistance determinants among gram-negative bacteria isolated from polluted and unpolluted marine sediments. Appl Environ Microbiol 60: 908912. [Google Scholar]
  30. Petersen A, Andersen JS, Kaewmak T, Somsiri T, Dalsgaard A, , 2002. Impact of integrated fish farming on antimicrobial resistance in a pond environment. Appl Environ Microbiol 68: 60366042.[Crossref] [Google Scholar]
  31. Kruse H, Sorum H, , 1994. Transfer of multiple drug resistance plasmids between bacteria of diverse origins in natural microenvironments. Appl Environ Microbiol 60: 40154021. [Google Scholar]
  32. Lester SC, del Pilar PM, Wang F, Perez SI, Jiang H, O'Brien TF, , 1990. The carriage of Escherichia coli resistant to antimicrobial agents by healthy children in Boston, in Caracas, Venezuela, and in Qin Pu, China. N Engl J Med 323: 285289.[Crossref] [Google Scholar]
  33. 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: 116123.[Crossref] [Google Scholar]
  34. Oswald WE, Lescano AG, Bern C, Calderon MM, Cabrera L, Gilman RH, , 2007. Fecal contamination of drinking water within peri-urban households, Lima, Peru. Am J Trop Med Hyg 77: 699704. [Google Scholar]
  35. Moller JK, Bak AL, Stenderup A, Zachariae H, Afzelius H, , 1977. Changing patterns of plasmid-mediated drug resistance during tetracycline therapy. Antimicrob Agents Chemother 11: 388391.[Crossref] [Google Scholar]
  36. Oteo J, Lazaro E, de Abajo FJ, Baquero F, Campos J, , and Spanish members of EARSS, 2005. Antimicrobial-resistant invasive Escherichia coli, Spain. Emerg Infect Dis 11: 546553.[Crossref] [Google Scholar]
  37. van Treeck U, Schmidt F, Wiedemann B, , 1981. Molecular nature of a streptomycin and sulfonamide resistance plasmid (pBP1) prevalent in clinical Escherichia coli strains and integration of an ampicillin resistance transposon (TnA). Antimicrob Agents Chemother 19: 371380.[Crossref] [Google Scholar]
  38. SAS version 9.1 for Windows, 2002. Cary, NC: SAS Institute Inc. [Google Scholar]
  39. Deeks SL, Palacio R, Ruvinsky R, Kertesz DA, Hortal M, Rossi A, Spika JS, , Di Fabio JL and The Streptococcus pneumoniae Working Group, 1999. Risk factors and course of illness among children with invasive penicillin-resistant Streptococcus pneumoniae . Pediatrics 103: 409413.[Crossref] [Google Scholar]
  40. Hay AD, Thomas M, Montgomery A, Wetherell M, Lovering A, McNulty C, Lewis D, Carron B, Henderson E, MacGowan A, , 2005. The relationship between primary care antibiotic prescribing and bacterial resistance in adults in the community: a controlled observations study using individual patient data. J Antimicrob Chemother 56: 146153.[Crossref] [Google Scholar]
  41. Tan TQ, Mason EO, Kaplan SL, , 2001. Penicillin-resistant systemic pneumococcal infections in children: a retrospective case-control study. Pediatrics 92: 761767. [Google Scholar]
  42. Kristiansson C, Reilly M, Gotuzzo E, Rodriguez H, Bartoloni A, Thorson A, Falkenberg T, Bartalesi F, Tomson G, Larsson M, , 2008. Antibiotic use and health-seeking behaviour in an underprivileged area of Peru. Trop Med Int Health 13: 434441.[Crossref] [Google Scholar]
  43. Yuksel S, Ozturk B, Kavaz A, Ozcakar ZB, Acar B, Guriz H, Aysev D, Ekim M, Yalcinkaya F, , 2006. Antibiotic resistance of urinary tract pathogens and evaluation of empirical treatment in Turkish children with urinary tract infections. Int J Antimicrob Agents 28: 413416.[Crossref] [Google Scholar]
  44. McLoughlin TG, Joseph MM, , 2003. Antibiotic resistance patterns of uropathogens in pediatric emergency department patients. Acad Emerg Med 10: 347351.[Crossref] [Google Scholar]
  45. Allen UD, MacDonald N, Fuite L, Chan F, Stephens D, , 1999. Risk factors for resistance to “first-line” antimicrobials among urinary tract isolates of Escherichia coli in children. CMAJ 160: 14361440. [Google Scholar]
  46. Bartoloni A, Pallecchi L, Benedetti M, Fernandez C, Vallejos Y, Guzman E, Villagran AL, Mantella A, Lucchetti C, Bartalesi F, Strohmeyer M, Bechini A, Gamboa H, Rodríguez H, Falkenberg T, Kronvall G, Gotuzzo E, Paradisi F, Rossolini GM, , 2006. Multidrug-resistant commensal Escherichia coli in children, Peru and Bolivia. Emerg Infect Dis 12: 907913.[Crossref] [Google Scholar]
  47. Albanese BA, Roche JC, Pass M, Whitney CG, McEllistrem MC, Harrison LH, , 2002. Geographic, demographic, and seasonal differences in penicillin-resistant Streptococcus pneumoniae in Baltimore. Clin Infect Dis 34: 1521.[Crossref] [Google Scholar]
  48. Hoban D, Baquero F, Reed V, Felmingham D, , 2005. Demographic analysis of antimicrobial resistance among Streptococcus pneumoniae: worldwide results from PROTEKT 1999–2000. Int J Infect Dis 9: 262273.[Crossref] [Google Scholar]
  49. Weiss K, Guilbault C, Cortes L, Restieri C, Low DE, , and the EQUERE project, 2002. Genotypic characterization of macrolide-resistant strains of Streptococcus pneumoniae isolated in Quebec, Canada, and in vitro activity of ABT-773 and telithromycin. J Antimicrob Chemother 50: 403406.[Crossref] [Google Scholar]
  50. Marquis GS, Ventura G, Gilman RH, Porras E, Miranda E, Carbajal L, Pentafiel M, , 1990. Fecal contamination of shanty town toddlers in households with non-corralled poultry, Lima, Peru. Am J Public Health 80: 146149.[Crossref] [Google Scholar]
  51. Jacobs MR, Johnson CE, , 2003. Macrolide resistance: an increasing concern for treatment failure in children. Pediatr Infect Dis J 22: S131S138.[Crossref] [Google Scholar]

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  • Received : 17 Mar 2009
  • Accepted : 15 Jan 2010
  • Published online : 05 May 2010

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