Quinolone resistance in absence of selective pressure: the experience of a very remote community in the Amazon forest

PLoS Negl Trop Dis. 2012;6(8):e1790. doi: 10.1371/journal.pntd.0001790. Epub 2012 Aug 28.

Abstract

Background: Quinolones are potent broad-spectrum bactericidal agents increasingly employed also in resource-limited countries. Resistance to quinolones is an increasing problem, known to be strongly associated with quinolone exposure. We report on the emergence of quinolone resistance in a very remote community in the Amazon forest, where quinolones have never been used and quinolone resistance was absent in 2002.

Methods: The community exhibited a considerable level of geographical isolation, limited contact with the exterior and minimal antibiotic use (not including quinolones). In December 2009, fecal carriage of antibiotic resistant Escherichia coli was investigated in 120 of the 140 inhabitants, and in 48 animals reared in the community. All fluoroquinolone-resistant isolates were genotyped and characterized for the mechanisms of plasmid- and chromosomal-mediated quinolone resistance.

Principal findings: Despite the characteristics of the community remained substantially unchanged during the period 2002-2009, carriage of quinolone-resistant E. coli was found to be common in 2009 both in humans (45% nalidixic acid, 14% ciprofloxacin) and animals (54% nalidixic acid, 23% ciprofloxacin). Ciprofloxacin-resistant isolates of human and animal origin showed multidrug resistance phenotypes, a high level of genetic heterogeneity, and a combination of GyrA (Ser83Leu and Asp87Asn) and ParC (Ser80Ile) substitutions commonly observed in fluoroquinolone-resistant clinical isolates of E. coli.

Conclusions: Remoteness and absence of antibiotic selective pressure did not protect the community from the remarkable emergence of quinolone resistance in E. coli. Introduction of the resistant strains from antibiotic-exposed settings is the most likely source, while persistence and dissemination in the absence of quinolone exposure is likely mostly related with poor sanitation. Interventions aimed at reducing the spreading of resistant isolates (by improving sanitation and water/food safety) are urgently needed to preserve the efficacy of quinolones in resource-limited countries, as control strategies based only on antibiotic restriction policies are unlikely to succeed in those settings.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Carrier State / microbiology*
  • Carrier State / veterinary*
  • Child
  • Child, Preschool
  • Drug Resistance, Multiple, Bacterial*
  • Escherichia coli / classification
  • Escherichia coli / drug effects*
  • Escherichia coli / genetics
  • Escherichia coli / isolation & purification
  • Escherichia coli Infections / microbiology*
  • Escherichia coli Infections / veterinary*
  • Feces / microbiology
  • Female
  • Genetic Variation
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Middle Aged
  • Plasmids / analysis
  • Quinolones / pharmacology*
  • Rural Population
  • South America
  • Trees
  • Young Adult

Substances

  • Anti-Bacterial Agents
  • Quinolones

Grants and funding

The study was supported by the European Society of Clinical Microbiology and Infectious Diseases (ESCMID Research Grant 2008) and the European Commission through the ALFAII Programme (BACTERIALNET project, contract no. AML/19.0901/06/18414/II-0531-FC-FA-FCD-FI) and the FP7 Health Programme (EvoTAR project, contract no. 282004). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.