High colonization rates of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in Swiss Travellers to South Asia– a prospective observational multicentre cohort study looking at epidemiology, microbiology and risk factors

BMC Infectious Diseases

Christoph Hatz⁴  Andrea Endimiani⁵  Manuel Battegay³  Hansjakob Furrer²  Andreas F Widmer³  Johannes Blum⁷  Sabine Haller⁴  Susan DeCrom⁴  Andreas Neumayr⁷  Reno Frei¹  Veronika K Jaeger⁶  Esther Kuenzli⁷ 

[1] Division of Clinical Microbiology, University Hospital Basel, Basel, Switzerland;Department of Infectious Diseases, Bern University Hospital and University of Bern, Bern, Switzerland;Division for Infectious Diseases and Hospital Epidemiology, University Hospital Basel, Basel, Switzerland;Division of Communicable Diseases, Institute for Social and Preventive Medicine, University of Zurich, Zurich, Switzerland;Institute for Infectious Diseases, University of Bern, Bern, Switzerland;Department of Rheumatology, University Hospital Basel, Basel, Switzerland;Swiss Tropical and Public Health Institute, Basel, Switzerland

关键词: South Asia;    Traveller;    ESBL;    Enterobacteriaceae;    Colonization;   

Others  :  1125466
DOI  :  10.1186/1471-2334-14-528

 received in 2014-07-13, accepted in 2014-09-26,  发布年份 2014

【 摘 要 】

Background

International travel contributes to the worldwide spread of multidrug resistant Gram-negative bacteria. Rates of travel-related faecal colonization with extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae vary for different destinations. Especially travellers returning from the Indian subcontinent show high colonization rates. So far, nothing is known about region-specific risk factors for becoming colonized.

Methods

An observational prospective multicentre cohort study investigated travellers to South Asia. Before and after travelling, rectal swabs were screened for third-generation cephalosporin- and carbapenem-resistant Enterobacteriaceae. Participants completed questionnaires to identify risk factors for becoming colonized. Covariates were assessed univariately, followed by a multivariate regression.

Results

Hundred and seventy persons were enrolled, the largest data set on travellers to the Indian subcontinent so far. The acquired colonization rate with ESBL-producing Escherichia coli overall was 69.4% (95% CI 62.1-75.9%), being highest in travellers returning from India (86.8%; 95% CI 78.5-95.0%) and lowest in travellers returning from Sri Lanka (34.7%; 95% CI 22.9-48.7%). Associated risk factors were travel destination, length of stay, visiting friends and relatives, and eating ice cream and pastry.

Conclusions

High colonization rates with ESBL-producing Enterobacteriaceae were found in travellers returning from South Asia. Though risk factors were identified, a more common source, i.e. environmental, appears to better explain the high colonization rates.

【 授权许可】

   
2014 Kuenzli et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Antimicrobial reistance: Global report on surveillance 2014. Geneva: World Health Organization; 2014.
• [2]Pitout JDD, Laupland KB: Extended-spectrum-beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008, 8(3):159-166.
• [3]Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JDD: Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect 2008, 57(6):441-448.
• [4]Seiffert SN, Hilty M, Kronenberg A, Droz S, Perreten V, Endimiani A: Extended-spectrum cephalosporin-resistant Escherichia coli in community, specialized outpatient clinic and hospital settings in Switzerland. J Antimicrob Chemother 2013, 68(10):2249-2254.
• [5]Seiffert SN, Hilty M, Perreten V, Endimiani A: Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health? Drug Resist Updates 2013, 16(1–2):22-45.
• [6]Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, Platteel T, Fluit AC, van de Sande-Bruinsma N, Scharinga J, Bonten MJ, Mevius DJ, National ESBL surveillance group: Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011, 17(6):873-880.
• [7]Seiffert SN, Tinguely R, Lupo A, Neuwirth C, Perreten V, Endimiani A: High prevalence of extended-spectrum-cephalosporin-resistant Enterobacteriaceae in poultry meat in Switzerland: emergence of CMY-2- and VEB-6-possessing Proteus mirabilis. Antimicrob Agents Chemother 2013, 57(12):6406-6408.
• [8]Tängden T, Cars O, Melhus A, Löwdin E: Foreign travel is a major risk factor for colonization with Eschericha coli producing CTX-M-type extended-spectrum beta-lactamase: a prospective study with Swedish volunteers. Antimicrob Agents Chemother 2010, 54(9):3564-3568.
• [9]Kennedy KJ, Collignon P: Colonisation with Escherichia coli resistant to "critically important" antibiotics: a high risk for international travellers. Eur J Clin Microbiol Infect Dis 2010, 29(12):1501-1506.
• [10]Weisenberg SA, Mediavilla JR, Chen L, Alexander EL, Rhee KY, Kreiswirth BN, Jenkins SG: Extended spectrum beta-lactamase-producing Enterobacteriaceae in international travelers and non-travelers in New York City. PLoS ONE 2012, 7(9):e45141.
• [11]Paltansing S, Vlot JA, Kraakman MEM, Mesman R, Bruijning ML, Bernards AT, Visser LG, Veldkamp KE: Extended-spectrum beta-lactamase-producing Enterobacteriaceae among travelers from the Netherlands. Emerg Infect Dis 2013, 19(8):1206-1213.
• [12]Östholm-Balkhed A, Tärnberg M, Nilsson M, Nilsson LE, Harnberger H, Hällgren A, on behalf of the Travel Study Group of Southeast Sweden: Travel-associated faecal colonization with ESBL-producing Enterobacteriaceae: incidence and risk factors. J Antimicrob Chemother 2013, 68(9):2144-2153.
• [13]Solé M, Pitart C, Oliveira I, Fàbrega A, Munoz L, Campo I, Pilar S, Alvarez-Martinez M, Gascon J, Marco F, Vila J: Extended spectrum beta-lactamase (ESBL)-producing Escherichia coli faecal carriage in Spanish travellers returning from tropical and subtropical countries. Clin Microbiol Infect 2014. doi: 10.1111/1469-0691.12592 (Epub ahead of print)
• [14]Dhanji H, Patel R, Wall R, Doumith M, Patel B, Hope R, Livermore DM, Woodford N: Variation in the genetic environments of bla(CTX-M-15) in Escherichia coli from the faeces of travellers returning to the United Kingdom. J Antimicrob Chemother 2011, 66(5):1005-1012.
• [15]World Tourism Organization: International tourism to continue robust growth in 2013. [http://media.unwto.org/en/press-release/2013-01-28/international-tourism-continue-robust-growth-2013 webcite]
• [16]Wilson ME, Chen LH: NDM-1 and the role of travel in its dissemination. Curr Infect Dis Rep 2012, 14(3):213-226.
• [17]Seiffert SN, Perreten V, Johannes S, Droz S, Bodmer T, Endimiani A: OXA-48 Carbapenemase Producing Salmonella enterica Kentucky of ST198 in a Patient Transferred from Lybia to Switzerland. Antimicrob Agents Chemother 2014, 58(4):2446-2449.
• [18]Rokkedal Lausch K, Fuursted K, Schade Larsen C, Storgaard M: Colonisation with multi-resistant Enterobacteriaceae in hospitalised Danish patients with a history of recent travel: a cross-sectional study. Travel Med Infectious Diseases 2013, 11(5):320-323.
• [19]Peirano G, Laupland KB, Gregson DB, Pitout JDD: Colonization of returning travelers with CTX-M-producing Eschericha coli. J Travel Med 2011, 18(5):299-303.
• [20]Tham J, Odenholt I, Waldner M, Brolund A, Ahl J, Melander E: Extended-spectrum beta-lactamase-producing Eschericha coli in patients with travellers' diarrhoea. Scand J Infect Dis 2010, 42(4):275-280.
• [21]Walsh TR, Weeks J, Livermore DM, Toleman MA: Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 2011, 11(5):355-362.
• [22]Murk JL, Hedderma ER, Hess DL, Bogaards JA, Vandenbroucke-Grauls CM, Debets-Ossenkopp YJ: Enrichment broth improved detection of extended-spectrum-beta-lactamase-producing bacteria in throat and rectal surveillance cultures of samples from patients in intensive care units. J Clin Microbiol 2009, 47(6):1885-1887.
• [23]The European Committee on Antimicrobial Susceptibility Testing: Breakpoint tables for interpretation of MICs and zone diameters. Version 3.1. 2013. [http://www.eucast.org webcite]
• [24]Hansen F, Hammerum AM, Skov RL, Giske CG, Sundsfjord A, Samuelsen O: Evaluation of ROSCO Neo-Sensitabs for phenotypic detection and subgrouping of ESBL-, AmpC- and carbapenemase-producing Enterobacteriaceae. Acta Pathol Microbiol Immunol Scand 2012, 120(9):724-732.
• [25]Hilty M, Betsch BY, Bögli-Stuber K, Heiniger N, Stadler M, Küffer M, Kronenberg A, Rohrer C, Aebi S, Endimiani A, Droz S, Mühlemann K: Transmission dynamics of extended-spectrum beta-lactamase-producing Enterobacteriaceae in the tertiary care hospital and the household setting. Clin Infect Dis 2012, 55(7):967-975.
• [26]Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, Krishnan P, Kumar AV, Maharjan S, Mushtaq S, Noorie T, Paterson DL, Pearson A, Perry C, Pike R, Rao B, Ray U, Sarma JB, Sharma M, Sheridan E, Thirunarayan MA, Turton J, Upadhyay S, Warner M, Welfare W, Livermore DM, Woodford N: Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 2010, 10(9):597-602.
• [27]Sankar S, Narayanan H, Kuppanan S, Nandagopal B: Frequency of extended-spectrum beta-lactamase (ESBL)-producing Gram-negative bacilli in a 200-bed multi-specialty hospital in Vellore district, Tamil Nadu, India. Infection 2012, 40(4):425-429.
• [28]Chen Y-H, Hsueh P-R, Badal RE, Hawser SP, Hoban DJ, Bouchillon SK, Ni Y, Paterson DL: Antimicrobial susceptibility profiles of aerobic and facultative Gram-negative bacilli isolated from patients with intra-abdominal infections in the Asia-Pacific region according to currently established susceptibility interpretive criteria. J Infect 2011, 62(4):280-291.
• [29]Chander A, Shrestha CD: Prevalence of extended spectrum beta lactamase producing Escherichia coli and Klebsiella pneumoniae urinary isolates in a tertiary care hospital in Kathmandu, Nepal. BMC Res Notes 2013, 6:487. BioMed Central Full Text
• [30]ARSP Working Group, The Sri Lanka College of Microbiologists: A multi centre laboratory study of Gram negative bacterial blood stream infections in Sri Lanka. Ceylon Med J 2013, 58(2):56-61.
• [31]Pathak A, Chandran SP, Mahadik K, Macaden R, Stalsby Lundborg C: Frequency and factors associated with carriage of multi-drug resistant commensal Escherichia coli among women attending antenatal clinics in Central India. BMC Infect Dis 2013, 13:199-208. BioMed Central Full Text
• [32]Dhanji H, Murphy NM, Akhigbe C, Doumith M, Hope R, Livermore DM, Woodford N: Isolation of fluoroquinolone-resistant O25b:H4-ST131 Escherichia coli with CTX-M-14 extended-spectrum beta-lactamase from UK river water. J Antimicrob Chemother 2011, 66(3):512-516.
• [33]Manges AR, Johnson JR: Food-borne origins of Escherichia coli causing extraintestinal infections. Clin Infect Dis 2012, 55(5):712-719.
• [34]Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M: Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006, 60(5):1136-1151.
• [35]Ruppé E, Armand-Lefèvre L, Estellat C, El-Mniai A, Boussadia Y, Consigny PH, Girard PM, Vittecoq D, Bouchaud O, Pialoux G, Esposito-Farèse M, Coignard B, Lucet JC, Andremont A, Matheron S: Acquisition of carbapenemase-producing Enterobacteriaceae by healthy travellers to India, France, February 2012 to March 2013. Eurosurveillance 2014, 19(14):pii=20768.