Risk factors for community-acquired urinary tract infections caused by ESBL-producing enterobacteriaceae--a case-control study in a low prevalence country

Arne Søraas, Arnfinn Sundsfjord, Irene Sandven, Cathrine Brunborg, Pål A Jenum, Arne Søraas, Arnfinn Sundsfjord, Irene Sandven, Cathrine Brunborg, Pål A Jenum

Abstract

Community-acquired urinary tract infection (CA-UTI) is the most common infection caused by extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae, but the clinical epidemiology of these infections in low prevalence countries is largely unknown. A population based case-control study was conducted to assess risk factors for CA-UTI caused by ESBL-producing E. coli or K. pneumoniae. The study was carried out in a source population in Eastern Norway, a country with a low prevalence of infections caused by ESBL-producing Enterobacteriaceae. The study population comprised 100 cases and 190 controls with CA-UTI caused by ESBL-producing and non-ESBL-producing E. coli or K. pneumoniae, respectively. The following independent risk factors of ESBL-positive UTIs were identified: Travel to Asia, The Middle East or Africa either during the past six weeks (Odds ratio (OR) = 21; 95% confidence interval (CI): 4.5-97) or during the past 6 weeks to 24 months (OR = 2.3; 95% CI: 1.1-4.4), recent use of fluoroquinolones (OR = 16; 95% CI: 3.2-80) and β-lactams (except mecillinam) (OR = 5.0; 95% CI: 2.1-12), diabetes mellitus (OR = 3.2; 95% CI: 1.0-11) and recreational freshwater swimming the past year (OR = 2.1; 95% CI: 1.0-4.0). Factors associated with decreased risk were increasing number of fish meals per week (OR = 0.68 per fish meal; 95% CI: 0.51-0.90) and age (OR = 0.89 per 5 year increase; 95% CI: 0.82-0.97). In conclusion, we have identified risk factors that elucidate mechanisms and routes for dissemination of ESBL-producing Enterobacteriaceae in a low prevalence country, which can be used to guide appropriate treatment of CA-UTI and targeted infection control measures.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Selection of study population.
Figure 1. Selection of study population.
aDementia (n = 1), unable to reach by phone (n = 2) and death (n = 2).
Figure 2. Decreasing risk a of ESBL-positive…
Figure 2. Decreasing riska of ESBL-positive urinary tract infection with increasing number of fishmeals per weekb.
aControlling for the variables: Travelling to Asia, Middle east or Africa, Use of fluoroquinolones the past 90 days, Use of β-lactams except mecillinam the past 90 days, Diabetes mellitus,Recreational freshwater swim past year and age. bReference category: eating ≤1 fishmeal per week.

References

    1. Pitout JD, Laupland KB (2008) Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8: 159–166.
    1. Rottier WC, Ammerlaan HS, Bonten MJ (2012) Effects of confounders and intermediates on the association of bacteraemia caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae and patient outcome: a meta-analysis. J Antimicrob Chemother 67: 1311–1320.
    1. Ben-Ami R, Rodriguez-Bano J, Arslan H, Pitout JD, Quentin C, et al. (2009) A multinational survey of risk factors for infection with extended-spectrum beta-lactamase-producing enterobacteriaceae in nonhospitalized patients. Clin Infect Dis 49: 682–690.
    1. Doi Y, Park YS, Rivera JI, Adams-Haduch JM, Hingwe A, et al. (2013) Community-associated extended-spectrum beta-lactamase-producing Escherichia coli infection in the United States. Clin Infect Dis 56: 641–648.
    1. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD (2008) Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect 57: 441–448.
    1. Nicolas-Chanoine MH, Jarlier V, Robert J, Arlet G, Drieux L, et al. (2012) Patient’s origin and lifestyle associated with CTX-M-producing Escherichia coli: a case-control-control study. PLoS One 7: e30498.
    1. Colodner R, Rock W, Chazan B, Keller N, Guy N, et al. (2004) Risk factors for the development of extended-spectrum beta-lactamase-producing bacteria in nonhospitalized patients. Eur J Clin Microbiol Infect Dis 23: 163–167.
    1. Rodriguez-Bano J, Picon E, Gijon P, Hernandez JR, Ruiz M, et al. (2010) Community-onset bacteremia due to extended-spectrum beta-lactamase-producing Escherichia coli: risk factors and prognosis. Clin Infect Dis 50: 40–48.
    1. Cassier P, Lallechere S, Aho S, Astruc K, Neuwirth C, et al. (2011) Cephalosporin and fluoroquinolone combinations are highly associated with CTX-M beta-lactamase-producing Escherichia coli: a case-control study in a French teaching hospital. Clin Microbiol Infect 17: 1746–1751.
    1. Siedelman L, Kline S, Duval S (2012) Risk factors for community- and health facility-acquired extended-spectrum beta-lactamase-producing bacterial infections in patients at the University of Minnesota Medical Center, Fairview. Am J Infect Control 40: 849–853.
    1. Azap OK, Arslan H, Serefhanoglu K, Colakoglu S, Erdogan H, et al. (2010) Risk factors for extended-spectrum beta-lactamase positivity in uropathogenic Escherichia coli isolated from community-acquired urinary tract infections. Clin Microbiol Infect 16: 147–151.
    1. Kang CI, Wi YM, Lee MY, Ko KS, Chung DR, et al. (2012) Epidemiology and risk factors of community onset infections caused by extended-spectrum beta-lactamase-producing Escherichia coli strains. J Clin Microbiol 50: 312–317.
    1. Kim YK, Pai H, Lee HJ, Park SE, Choi EH, et al. (2002) Bloodstream infections by extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in children: epidemiology and clinical outcome. Antimicrob Agents Chemother 46: 1481–1491.
    1. Park SH, Choi SM, Lee DG, Kim J, Choi JH, et al. (2011) Emergence of extended-spectrum beta-lactamase-producing escherichia coli as a cause of community-onset bacteremia in South Korea: risk factors and clinical outcomes. Microb Drug Resist 17: 537–544.
    1. Tian SF, Chen BY, Chu YZ, Wang S (2008) Prevalence of rectal carriage of extended-spectrum beta-lactamase-producing Escherichia coli among elderly people in community settings in China. Can J Microbiol 54: 781–785.
    1. Topaloglu R, Er I, Dogan BG, Bilginer Y, Ozaltin F, et al. (2010) Risk factors in community-acquired urinary tract infections caused by ESBL-producing bacteria in children. Pediatr Nephrol 25: 919–925.
    1. Muvunyi CM, Masaisa F, Bayingana C, Mutesa L, Musemakweri A, et al. (2011) Decreased susceptibility to commonly used antimicrobial agents in bacterial pathogens isolated from urinary tract infections in Rwanda: need for new antimicrobial guidelines. Am J Trop Med Hyg 84: 923–928.
    1. Kim B, Kim J, Seo MR, Wie SH, Cho YK, et al... (2013) Clinical characteristics of community-acquired acute pyelonephritis caused by ESBL-producing pathogens in South Korea. Infection.
    1. Johnson SW, Anderson DJ, May DB, Drew RH (2013) Utility of a clinical risk factor scoring model in predicting infection with extended-spectrum beta-lactamase-producing enterobacteriaceae on hospital admission. Infect Control Hosp Epidemiol 34: 385–392.
    1. Briongos-Figuero LS, Gomez-Traveso T, Bachiller-Luque P, Dominguez-Gil GM, Gomez-Nieto A, et al. (2012) Epidemiology, risk factors and comorbidity for urinary tract infections caused by extended-spectrum beta-lactamase (ESBL)-producing enterobacteria. Int J Clin Pract 66: 891–896.
    1. NORM/NORM-VET 2010 (2011) Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø/Oslo 2011. ISSN:1502-2307 (print)/1890-9965 (electronic).
    1. Berg C, Furu K, Mahic M, Litleskare I, Rønning M, et al... (2011) The Norwegian Prescription Database 2006–2010: The Norwegian Institute of Public Health. ISBN: 978-82-8082-458-5.
    1. European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Available: 13-5-22013.
    1. Birkett CI, Ludlam HA, Woodford N, Brown DF, Brown NM, et al. (2007) Real-time TaqMan PCR for rapid detection and typing of genes encoding CTX-M extended-spectrum beta-lactamases. J Med Microbiol 56: 52–55.
    1. Tofteland S, Haldorsen B, Dahl KH, Simonsen GS, Steinbakk M, et al. (2007) Effects of phenotype and genotype on methods for detection of extended-spectrum-beta-lactamase-producing clinical isolates of Escherichia coli and Klebsiella pneumoniae in Norway. J Clin Microbiol 45: 199–205.
    1. Chaudhry S, Jin L, Meltzer D (2005) Use of a self-report-generated Charlson Comorbidity Index for predicting mortality. Med Care 43: 607–615.
    1. Kleinbaum DG, Klein M (2010) Assessing Discriminatory Performance of a Binary Logistic Model: ROC curves. In: Kleinbaum DG, Klein M. Logistic Regression. A Self-Learning Text. Third edition. In. 346–386.
    1. Tangden T, Cars O, Melhus A, Lowdin E (2010) Foreign travel is a major risk factor for colonization with Escherichia coli producing CTX-M-type extended-spectrum beta-lactamases: a prospective study with Swedish volunteers. Antimicrob Agents Chemother 54: 3564–3568.
    1. Freeman JT, McBride SJ, Heffernan H, Bathgate T, Pope C, et al. (2008) Community-onset genitourinary tract infection due to CTX-M-15-Producing Escherichia coli among travelers to the Indian subcontinent in New Zealand. Clin Infect Dis 47: 689–692.
    1. European Centre for Disease Prevention and Control (2011) Antimicrobial resistance surveillance in Europe 2010. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Stockholm: ECDC.
    1. Rodriguez-Bano J, Navarro MD, Romero L, Martinez-Martinez L, Muniain MA, et al. (2004) Epidemiology and clinical features of infections caused by extended-spectrum beta-lactamase-producing Escherichia coli in nonhospitalized patients. J Clin Microbiol 42: 1089–1094.
    1. Sullivan A, Edlund C, Svenungsson B, Emtestam L, Nord CE (2001) Effect of perorally administered pivmecillinam on the normal oropharyngeal, intestinal and skin microflora. J Chemother 13: 299–308.
    1. Wootton M, Walsh TR, Macfarlane L, Howe RA (2010) Activity of mecillinam against Escherichia coli resistant to third-generation cephalosporins. J Antimicrob Chemother 65: 79–81.
    1. Chen H, Shu W, Chang X, Chen JA, Guo Y, et al. (2010) The profile of antibiotics resistance and integrons of extended-spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environ Pollut 158: 2459–2464.
    1. Tacao M, Correia A, Henriques I (2012) Resistance to broad-spectrum antibiotics in aquatic systems: anthropogenic activities modulate the dissemination of blaCTX-MlLike genes. Appl Environ Microbiol 78: 4134–4140.
    1. Colomer-Lluch M, Jofre J, Muniesa M (2011) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6: e17549.
    1. Samadpour M, Stewart J, Steingart K, Addy C, Louderback J, et al... (2002) Laboratory investigation of an E. coli O157:H7 outbreak associated with swimming in Battle Ground Lake, Vancouver, Washington. J Environ Health 64: 16–20, 26, 25.
    1. Moreno E, Andreu A, Perez T, Sabate M, Johnson JR, et al. (2006) Relationship between Escherichia coli strains causing urinary tract infection in women and the dominant faecal flora of the same hosts. Epidemiol Infect 134: 1015–1023.
    1. Guenther S, Ewers C, Wieler LH (2011) Extended-Spectrum Beta-Lactamases Producing E. coli in Wildlife, yet Another Form of Environmental Pollution? Front Microbiol 2: 246.
    1. Angelakis E, Armougom F, Million M, Raoult D (2012) The relationship between gut microbiota and weight gain in humans. Future Microbiol 7: 91–109.
    1. Kluytmans JA, Overdevest IT, Willemsen I, Kluytmans-van den Bergh MF, van der Zwaluw K, et al. (2013) Extended-spectrum beta-lactamase-producing Escherichia coli from retail chicken meat and humans: comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis 56: 478–487.
    1. NORM/NORM-VET 2011 (2012) Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø/Oslo 2012. ISSN:1502-2307 (print)/1890-9965 (electronic).
    1. Apisarnthanarak A, Kiratisin P, Saifon P, Kitphati R, Dejsirilert S, et al. (2007) Clinical and molecular epidemiology of community-onset, extended-spectrum beta-lactamase-producing Escherichia coli infections in Thailand: a case-case-control study. Am J Infect Control 35: 606–612.
    1. Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, et al. (2002) Health care–associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med 137: 791–797.
    1. Harris AD, Karchmer TB, Carmeli Y, Samore MH (2001) Methodological principles of case-control studies that analyzed risk factors for antibiotic resistance: a systematic review. Clin Infect Dis 32: 1055–1061.
    1. Moor CT, Roberts SA, Simmons G, Briggs S, Morris AJ, et al. (2008) Extended-spectrum beta-lactamase (ESBL)-producing enterobacteria: factors associated with infection in the community setting, Auckland, New Zealand. J Hosp Infect 68: 355–362.

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