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Abstract

Background

While 20–80% of regular visitors to (sub)tropical regions become colonised by extended-spectrum β-lactamase-producing (ESBL-PE), those hospitalised abroad often also carry other multidrug-resistant (MDR) bacteria on return; the rates are presumed to be highest for interhospital transfers.

Aim

This observational study assessed MDR bacterial colonisation among patients transferred directly from hospitals abroad to Helsinki University Hospital. We investigated predisposing factors, clinical infections and associated fatalities.

Methods

Data were derived from screening and from diagnostic samples collected between 2010 and 2019. Risk factors of colonisation were identified by multivariable analysis. Microbiologically verified symptomatic infections and infection-related mortality were recorded during post-transfer hospitalisation.

Results

Colonisation rates proved highest for transfers from Asia (69/96; 71.9%) and lowest for those within Europe (99/524; 18.9%). Of all 698 patients, 208 (29.8%) were colonised; among those, 163 (78.4%) carried ESBL-PE, 28 (13.5%) MDR species, 25 (12.0%) meticillin-resistant , 25 (12.0%) vancomycin-resistant , 14 (6.7%) carbapenemase-producing , and 12 (5.8%) MDR ; 46 strains tested carbapenemase gene-positive. In multivariable analysis, geographical region, intensive care unit (ICU) treatment and antibiotic use abroad proved to be risk factors for colonisation. Clinical MDR infections, two of them fatal (1.0%), were recorded for 22 of 208 (10.6%) MDR carriers.

Conclusions

Colonisation by MDR bacteria was common among patients transferred from foreign hospitals. Region of hospitalisation, ICU treatment and antibiotic use were identified as predisposing factors. Within 30 days after transfer, MDR colonisation manifested as clinical infection in more than 10% of the carriers.

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/content/10.2807/1560-7917.ES.2021.26.39.2001360
2021-09-30
2024-12-09
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2021.26.39.2001360
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References

  1. Woerther PL, Andremont A, Kantele A. Travel-acquired ESBL-producing Enterobacteriaceae: impact of colonization at individual and community level. J Travel Med. 2017;24(suppl_1):s29-s34.  https://doi.org/10.1093/jtm/taw101  PMID: 28520999
  2. de Kraker ME, Davey PG, Grundmann H, BURDEN study group. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med. 2011;8(10):e1001104.  https://doi.org/10.1371/journal.pmed.1001104  PMID: 22022233 
  3. Prematunge C, MacDougall C, Johnstone J, Adomako K, Lam F, Robertson J, et al. VRE and VSE bacteremia outcomes in the era of effective VRE therapy: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2016;37(1):26-35.  https://doi.org/10.1017/ice.2015.228  PMID: 26434609 
  4. Kantele A, Lääveri T, Mero S, Häkkinen IMK, Kirveskari J, Johnston BD, et al. Despite predominance of uropathogenic/extraintestinal pathotypes among travel-acquired Extended-spectrum β-Lactamase-producing Escherichia coli, the most commonly associated clinical manifestation is travelers’ diarrhea. Clin Infect Dis. 2020;70(2):210-8.  https://doi.org/10.1093/cid/ciz182  PMID: 31034006 
  5. Fischer D, Veldman A, Schäfer V, Diefenbach M. Bacterial colonization of patients undergoing international air transport: a prospective epidemiologic study. J Travel Med. 2004;11(1):44-8.  https://doi.org/10.2310/7060.2004.13647  PMID: 14769287 
  6. Kaiser AM, Schultsz C, Kruithof GJ, Debets-Ossenkopp Y, Vandenbroucke-Grauls C. Carriage of resistant microorganisms in repatriates from foreign hospitals to The Netherlands. Clin Microbiol Infect. 2004;10(11):972-9.  https://doi.org/10.1111/j.1469-0691.2004.01000.x  PMID: 15521999 
  7. Nemeth J, Ledergerber B, Preiswerk B, Nobile A, Karrer S, Ruef C, et al. Multidrug-resistant bacteria in travellers hospitalized abroad: prevalence, characteristics, and influence on clinical outcome. J Hosp Infect. 2012;82(4):254-9.  https://doi.org/10.1016/j.jhin.2012.08.017  PMID: 23103249 
  8. Josseaume J, Verner L, Brady WJ, Duchateau FX. Multidrug-resistant bacteria among patients treated in foreign hospitals: management considerations during medical repatriation. J Travel Med. 2013;20(1):22-8.  https://doi.org/10.1111/j.1708-8305.2012.00668.x  PMID: 23279227 
  9. Birgand G, Armand-Lefevre L, Lepainteur M, Lolom I, Neulier C, Reibel F, et al. Introduction of highly resistant bacteria into a hospital via patients repatriated or recently hospitalized in a foreign country. Clin Microbiol Infect. 2014;20(11):O887-90.  https://doi.org/10.1111/1469-0691.12604  PMID: 25069719 
  10. Angue M, Allou N, Belmonte O, Lefort Y, Lugagne N, Vandroux D, et al. Risk factors for colonization with multidrug-resistant bacteria among patients admitted to the intensive care unit after returning from abroad. J Travel Med. 2015;22(5):300-5.  https://doi.org/10.1111/jtm.12220  PMID: 26081076 
  11. Kaspar T, Schweiger A, Droz S, Marschall J. Colonization with resistant microorganisms in patients transferred from abroad: who needs to be screened? Antimicrob Resist Infect Control. 2015;4(1):31.  https://doi.org/10.1186/s13756-015-0071-6  PMID: 26213620 
  12. Mutters NT, Günther F, Sander A, Mischnik A, Frank U. Influx of multidrug-resistant organisms by country-to-country transfer of patients. BMC Infect Dis. 2015;15(1):466.  https://doi.org/10.1186/s12879-015-1173-8  PMID: 26508038 
  13. Khawaja T, Kirveskari J, Johansson S, Vaisanen J, Djupsjobacka A, Nevalainen A, et al. Patients hospitalized abroad as importers of multiresistant bacteria-a cross-sectional study. Clin Microbiol Infect. 2017;23(9):673.e1-.e8.  https://doi.org/10.1016/j.cmi.2017.02.003  PMID: 28196696
  14. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373-83.  https://doi.org/10.1016/0021-9681(87)90171-8  PMID: 3558716 
  15. Aro T, Kantele A. High rates of meticillin-resistant Staphylococcus aureus among asylum seekers and refugees admitted to Helsinki University Hospital, 2010 to 2017. Euro Surveill. 2018;23(45).  https://doi.org/10.2807/1560-7917.ES.2018.23.45.1700797  PMID: 30424828 
  16. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters, versions 1.3–9.0 (2011–2019). Växjö: EUCAST; 2020. Available from: https://eucast.org/ast_of_bacteria/previous_versions_of_documents
  17. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 19th informational supplement M100-S19. Wayne: CLSI; 2009.
  18. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ, Goorhuis A, et al. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis. 2017;17(1):78-85.  https://doi.org/10.1016/S1473-3099(16)30319-X  PMID: 27751772 
  19. Tängdén T, Cars O, Melhus A, Löwdin E. 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. 2010;54(9):3564-8.  https://doi.org/10.1128/AAC.00220-10  PMID: 20547788 
  20. Paltansing S, Vlot JA, Kraakman ME, Mesman R, Bruijning ML, Bernards AT, et al. Extended-spectrum β-lactamase-producing enterobacteriaceae among travelers from the Netherlands. Emerg Infect Dis. 2013;19(8):1206-13.  https://doi.org/10.3201/eid1908.130257  PMID: 23885972 
  21. Ruppé E, Armand-Lefèvre L, Estellat C, El-Mniai A, Boussadia Y, Consigny PH, et al. Acquisition of carbapenemase-producing Enterobacteriaceae by healthy travellers to India, France, February 2012 to March 2013. Euro Surveill. 2014;19(14):20768.  https://doi.org/10.2807/1560-7917.ES2014.19.14.20768  PMID: 24739981 
  22. ÖstholmBalkhed Å, Tärnberg M, Nilsson M, Nilsson LE, Hanberger H, Hällgren A, Southeast Sweden Travel Study Group. Duration of travel-associated faecal colonisation with ESBL-producing Enterobacteriaceae - A one year follow-up study. PLoS One. 2018;13(10):e0205504.  https://doi.org/10.1371/journal.pone.0205504  PMID: 30356258 
  23. Schaumburg F, Sertic SM, Correa-Martinez C, Mellmann A, Kock R, Becker K. Acquisition and colonization dynamics of antimicrobial-resistant bacteria during international travel: a prospective cohort study. Clin Microbiol Infect. 2019;25(10):1287.e1-.e7.  https://doi.org/10.1016/j.cmi.2019.03.002  PMID: 30898722
  24. Chanderraj R, Millar JA, Patel TS, Read AF, Washer L, Kaye KS, et al. Vancomycin-resistant Enterococcus acquisition in a tertiary care hospital: testing the roles of antibiotic use, proton pump inhibitor use, and colonization pressure. Open Forum Infect Dis. 2019;6(4):ofz139.  https://doi.org/10.1093/ofid/ofz139  PMID: 31024976 
  25. Falagas ME, Kopterides P. Risk factors for the isolation of multi-drug-resistant Acinetobacter baumannii and Pseudomonas aeruginosa: a systematic review of the literature. J Hosp Infect. 2006;64(1):7-15.  https://doi.org/10.1016/j.jhin.2006.04.015  PMID: 16822583 
  26. Tacconelli E, De Angelis G, Cataldo MA, Pozzi E, Cauda R. Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? A systematic review and meta-analysis. J Antimicrob Chemother. 2008;61(1):26-38.  https://doi.org/10.1093/jac/dkm416  PMID: 17986491 
  27. Kantele A, Lääveri T, Mero S, Vilkman K, Pakkanen SH, Ollgren J, et al. Antimicrobials increase travelers’ risk of colonization by extended-spectrum betalactamase-producing Enterobacteriaceae. Clin Infect Dis. 2015;60(6):837-46.  https://doi.org/10.1093/cid/ciu957  PMID: 25613287 
  28. Ny S, Kozlov R, Dumpis U, Edquist P, Gröndahl-Yli-Hannuksela K, Kling AM, et al. , NoDARS ESBL-carrier working group. Large variation in ESBL-producing Escherichia coli carriers in six European countries including Russia. Eur J Clin Microbiol Infect Dis. 2018;37(12):2347-54.  https://doi.org/10.1007/s10096-018-3382-8  PMID: 30338465 
  29. Ruppé E, Armand-Lefèvre L, Estellat C, Consigny PH, El Mniai A, Boussadia Y, et al. High rate of acquisition but short duration of carriage of multidrug-resistant Enterobacteriaceae after travel to the tropics. Clin Infect Dis. 2015;61(4):593-600.  https://doi.org/10.1093/cid/civ333  PMID: 25904368 
  30. Räisänen K, Jalava J. Bakteerien mikrobilääkeresistenssi Suomessa: Finres 2018. [Antimicrobial resistance of bacteria in Finland: Finres 2018]. Finnish Institute for Health and Welfare. 2019. Available from: http://www.julkari.fi/handle/10024/138818. Finish.
  31. HUSRES HUSRES Herkkyystilastot 2010-2018. [HUSRES Annual reports 2010-2018]. Available from: https://huslab.fi/ohjekirjan_liitteet/mikrobiologian_ohjeet/mikrobiologian_tilastoja/index.html. Finnish.
  32. Moore C, Dhaliwal J, Tong A, Eden S, Wigston C, Willey B, et al. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) acquisition in roommate contacts of patients colonized or infected with MRSA in an acute-care hospital. Infect Control Hosp Epidemiol. 2008;29(7):600-6.  https://doi.org/10.1086/588567  PMID: 18624667 
  33. Reuland EA, Sonder GJ, Stolte I, Al Naiemi N, Koek A, Linde GB, et al. Travel to Asia and traveller’s diarrhoea with antibiotic treatment are independent risk factors for acquiring ciprofloxacin-resistant and extended spectrum β-lactamase-producing Enterobacteriaceae-a prospective cohort study. Clin Microbiol Infect. 2016;22(8):731.e1-7.  https://doi.org/10.1016/j.cmi.2016.05.003  PMID: 27223840 
  34. van Hattem JM, Arcilla MS, Bootsma MC, van Genderen PJ, Goorhuis A, Grobusch MP, et al. Prolonged carriage and potential onward transmission of carbapenemase-producing Enterobacteriaceae in Dutch travelers. Future Microbiol. 2016;11(7):857-64.  https://doi.org/10.2217/fmb.16.18  PMID: 27357522 
  35. Stenhem M, Ortqvist A, Ringberg H, Larsson L, Olsson Liljequist B, Haeggman S, et al. Imported methicillin-resistant Staphylococcus aureus, Sweden. Emerg Infect Dis. 2010;16(2):189-96.  https://doi.org/10.3201/eid1602.081655  PMID: 20113546 
  36. Kantele A, Kuenzli E, Dunn SJ, Dance DAB, Newton PN, Davong V, et al. Dynamics of intestinal multidrug-resistant bacteria colonisation contracted by visitors to a high-endemic setting: a prospective, daily, real-time sampling study. Lancet Microbe. 2021;2(4):e151-8.  https://doi.org/10.1016/S2666-5247(20)30224-X  PMID: 33821248 
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