Travel and the Spread of Drug-Resistant Bacteria

  • Kevin L. SchwartzEmail author
  • Shaun K. Morris
Tropical, Travel, and Emerging Infections (L Chen and A Boggild, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Tropical, Travel and Emerging Infections


Purpose of Review

The rise in antimicrobial resistance is an urgent public health threat which, in the absence of intervention, may result in a post-antibiotic era limiting the effectiveness of antibiotics to treat both common and serious infections. Globalization and human migration have profoundly contributed to the spread of drug-resistant bacteria. In this review, we summarize the recent literature on the importance of travelers in the spread of drug-resistant bacterial organisms. Our goal was to describe the importance of travel on a variety of clinically relevant drug-resistant bacterial organisms including extended-spectrum β-lactamase-producing Enterobacteriaceae, carbapenem-resistant Enterobacteriaceae, methicillin-resistant Staphylococcus aureus, Salmonella species, as well as other enteric infections.

Recent Findings

Travelers from high income countries, visiting low and middle income countries, frequently acquire drug-resistant bacteria, particularly extended-spectrum β-lactamase-producing Enterobacteriaceae. The highest risk is associated with travel to the Indian subcontinent. Multidrug-resistant enteric infections in travelers from Salmonella spp., Campylobacter spp., and Shigella spp. are increasing. Refugees, pilgrimages, and medical tourists are associated with considerable risk of multiple forms of drug resistance.


This review highlights the importance of antimicrobial stewardship, infection control, and surveillance; particularly in low and middle income countries. International leadership with global coordination is vital in the battle against antimicrobial resistance.


Travel Migration Antimicrobial stewardship Antimicrobial resistance Public health 



We would like to thank Sean Marshall from Public Health Ontario for creating the map figure.

Compliance with Ethical Standards

Conflict of Interest

Kevin Schwartz and Shaun Morris declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    United Nations Press Release on Antimicrobial Resistance. Link available at: Accessed 14 Sept 2017.
  2. 2.
    • O’Neil J. Review on antimicrobial resistance. Antimicrobial resistance: tackling a crisis for the Health and Wealth of Nations 2014. 2014. This report makes economic and mortality predictions on the impact that antimicrobial resistance will have in the future in the absence of significant intervention. Google Scholar
  3. 3.
    Tangden T, Cars O, Melhus A, Lowdin 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. Scholar
  4. 4.
    Vading M, Kabir MH, Kalin M, Iversen A, Wiklund S, Naucler P, et al. Frequent acquisition of low-virulence strains of ESBL-producing Escherichia coli in travellers. J Antimicrob Chemother. 2016;71:3548–55. Scholar
  5. 5.
    •• Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MC, van Genderen PJ, Goorhuis A, et al. Import and spread of extended-spectrum beta-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis. 2017;17:78–85. This is the largest study to date evaluating the importance of travel to the acquisition of ESBL Enterobacteriaceae. CrossRefPubMedGoogle Scholar
  6. 6.
    Reuland EA, Al Naiemi N, Kaiser AM, Heck M, Kluytmans JA, Savelkoul PH, et al. Prevalence and risk factors for carriage of ESBL-producing Enterobacteriaceae in Amsterdam. J Antimicrob Chemother. 2016;71:1076–82. Scholar
  7. 7.
    • Kantele A, Laaveri 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. This study highlights the risk of resistance from treating traveler's diarrhea with antibiotics. CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Kantele A, Mero S, Kirveskari J, Laaveri T. Increased risk for ESBL-producing bacteria from co-administration of loperamide and antimicrobial drugs for travelers' diarrhea. Emerg Infect Dis. 2016;22:117–20. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Barreto Miranda I, Ignatius R, Pfuller R, Friedrich-Janicke B, Steiner F, Paland M, et al. High carriage rate of ESBL-producing Enterobacteriaceae at presentation and follow-up among travellers with gastrointestinal complaints returning from India and Southeast Asia. J Travel Med. 2016;23(2):tav024. Scholar
  10. 10.
    Ruppe E, Armand-Lefevre 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;61:593–600. Scholar
  11. 11.
    Lubbert C, Straube L, Stein C, Makarewicz O, Schubert S, Mossner J, et al. Colonization with extended-spectrum beta-lactamase-producing and carbapenemase-producing Enterobacteriaceae in international travelers returning to Germany. Int J Med Microbiol. 2015;305:148–56. Scholar
  12. 12.
    Sole M, Pitart C, Oliveira I, Fabrega A, Munoz L, Campo I, et al. Extended spectrum beta-lactamase-producing Escherichia coli faecal carriage in Spanish travellers returning from tropical and subtropical countries. Clin Microbiol Infect. 2014;20:O636–9. Scholar
  13. 13.
    Kuenzli E, Jaeger VK, Frei R, Neumayr A, DeCrom S, Haller S, et al. High colonization rates of extended-spectrum beta-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 Infect Dis. 2014;14:528. Scholar
  14. 14.
    Paltansing S, Vlot JA, Kraakman ME, Mesman R, Bruijning ML, Bernards AT, et al. Extended-spectrum beta-lactamase-producing enterobacteriaceae among travelers from the Netherlands. Emerg Infect Dis. 2013;19:1206–13. Scholar
  15. 15.
    Ostholm-Balkhed A, Tarnberg M, Nilsson M, Nilsson LE, Hanberger H, Hallgren A, et al. Travel-associated faecal colonization with ESBL-producing Enterobacteriaceae: incidence and risk factors. J Antimicrob Chemother. 2013;68:2144–53. Scholar
  16. 16.
    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;11:857–64. Scholar
  17. 17.
    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. Scholar
  18. 18.
    Rogers BA, Kennedy KJ, Sidjabat HE, Jones M, Collignon P, Paterson DL. Prolonged carriage of resistant E. coli by returned travellers: clonality, risk factors and bacterial characteristics. Eur J Clin Microbiol Infect Dis. 2012;31(9):2413–20. Scholar
  19. 19.
    Weisenberg SA, Mediavilla JR, Chen L, Alexander EL, Rhee KY, Kreiswirth BN, et al. Extended spectrum beta-lactamase-producing Enterobacteriaceae in international travelers and non-travelers in New York City. PLoS One. 2012;7:e45141. Scholar
  20. 20.
    Jorgensen SB, Samuelsen O, Sundsfjord A, Bhatti SA, Jorgensen I, Sivapathasundaram T, et al. High prevalence of faecal carriage of ESBL-producing Enterobacteriaceae in Norwegian patients with gastroenteritis. Scand J Infect Dis. 2014;46:462–5. Scholar
  21. 21.
    Vasoo S, Madigan T, Cunningham SA, Mandrekar JN, Porter SB, Johnston B, et al. Prevalence of rectal colonization with multidrug-resistant Enterobacteriaceae among international patients hospitalized at Mayo Clinic, Rochester, Minnesota. Infect Control Hosp Epidemiol. 2014;35:182–6. Scholar
  22. 22.
    Angelin M, Forsell J, Granlund M, Evengard B, Palmgren H, Johansson A. Risk factors for colonization with extended-spectrum beta-lactamase producing Enterobacteriaceae in healthcare students on clinical assignment abroad: a prospective study. Travel Med Infect Dis. 2015;13:223–9. Scholar
  23. 23.
    Blyth DM, Mende K, Maranich AM, Beckius ML, Harnisch KA, Rosemann CA, et al. Antimicrobial resistance acquisition after international travel in U.S. travelers. Trop Dis Travel Med Vaccines. 2015;2:4. Scholar
  24. 24.
    Valverde A, Turrientes MC, Norman F, San Martin E, Moreno L, Perez-Molina JA, et al. CTX-M-15-non-ST131 Escherichia coli isolates are mainly responsible of faecal carriage with ESBL-producing Enterobacteriaceae in travellers, immigrants and those visiting friends and relatives. Clin Microbiol Infect. 2015;21:252.e1–4. Scholar
  25. 25.
    von Wintersdorff CJ, Penders J, Stobberingh EE, Oude Lashof AM, Hoebe CJ, Savelkoul PH, et al. High rates of antimicrobial drug resistance gene acquisition after international travel, The Netherlands. Emerg Infect Dis. 2014;20:649–57. Scholar
  26. 26.
    Pires J, Kuenzli E, Kasraian S, Tinguely R, Furrer H, Hilty M, et al. Polyclonal intestinal colonization with extended-spectrum cephalosporin-resistant Enterobacteriaceae upon traveling to India. Front Microbiol. 2016;7:1069. Scholar
  27. 27.
    • Karanika S, Karantanos T, Arvanitis M, Grigoras C, Mylonakis E. Fecal colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae and risk factors among healthy individuals: a systematic review and metaanalysis. Clin Infect Dis. 2016;63:310–8. This is a nice review summarizing the literature on ESBL colonization in health individuals. CrossRefPubMedGoogle Scholar
  28. 28.
    Soraas A, Sundsfjord A, Sandven I, Brunborg C, Jenum PA. Risk factors for community-acquired urinary tract infections caused by ESBL-producing enterobacteriaceae -a case-control study in a low prevalence country. PLoS One. 2013;8(7):(no pagination).
  29. 29.
    Tham J, Odenholt I, Walder M, Andersson L, Melander E. Risk factors for infections with extended-spectrum beta-lactamase-producing Escherichia coli in a county of Southern Sweden. Infection. 2013;6:93–7. Scholar
  30. 30.
    Osthoff M, McGuinness SL, Wagen AZ, Eisen DP. Urinary tract infections due to extended-spectrum beta-lactamase-producing Gram-negative bacteria: identification of risk factors and outcome predictors in an Australian tertiary referral hospital. Int J Infect Dis. 2015;34:79–83. Scholar
  31. 31.
    Talan DA, Takhar SS, Krishnadasan A, Abrahamian FM, Mower WR, Moran GJ, et al. Fluoroquinolone-resistant and extended-spectrum beta-lactamase-producing Escherichia coli infections in patients with pyelonephritis, United States(1). Emerg Infect Dis. 2016;22.
  32. 32.
    Patel U, Dasgupta P, Amoroso P, Challacombe B, Pilcher J, Kirby R. Infection after transrectal ultrasonography-guided prostate biopsy: increased relative risks after recent international travel or antibiotic use. BJU Int. 2012;109:1781–5. Scholar
  33. 33.
    Strysko JP, Mony V, Cleveland J, Siddiqui H, Homel P, Gagliardo C. International travel is a risk factor for extended-spectrum beta-lactamase-producing Enterobacteriaceae acquisition in children: a case-case-control study in an urban U.S. hospital. Travel Med Infect Dis. 2016;14:568–71. Scholar
  34. 34.
    Wiklund S, Fagerberg I, Ortqvist A, Vading M, Giske CG, Broliden K, et al. Knowledge and understanding of antibiotic resistance and the risk of becoming a carrier when travelling abroad: a qualitative study of Swedish travellers. Scand J Public Health. 2015;43:302–8. Scholar
  35. 35.
    Wiklund S, Fagerberg I, Ortqvist A, Broliden K, Tammelin A. Acquisition of extended spectrum beta-lactamases during travel abroad—a qualitative study among Swedish travellers examining their knowledge, risk assessment, and behaviour. Int J Qual Stud Health Well-being. 2016;11:32378. Scholar
  36. 36.
    Migault C, Kanagaratnam L, Nguyen Y, Lebrun D, Giltat A, Hentzien M, et al. Poor knowledge among French travellers of the risk of acquiring multidrug-resistant bacteria during travel. J Travel Med. 2016;24.
  37. 37.
    • DuPont HLMDMHC, Steffen RM. Use of antimicrobial agents for treatment and prevention of travellers' diarrhoea in the face of enhanced risk of transient fecal carriage of multi-drug resistant enterobacteriaceae: setting the stage for consensus recommendations. J Travel Med. 2016;23 Guideline on the appropriate use of antimicrobials for the treatment and prevention of TD.
  38. 38.
    Surveillance atlas of infectious diseases. The European Centre for Disease Prevention and Control (ECDC) website. Published 2016. Accessed 22 Dec 2017.
  39. 39.
    Ben-David D, Kordevani R, Keller N, Tal I, Marzel A, Gal-Mor O, et al. Outcome of carbapenem resistant Klebsiella pneumoniae bloodstream infections. Clin Microbiol Infect. 2012;18(1):54–60. Scholar
  40. 40.
    Friedman ND, Carmeli Y, Walton AL, Schwaber MJ. Carbapenem-resistant Enterobacteriaceae: a strategic roadmap for infection control. Infect Control Hosp Epidemiol. 2017;38:580–94. Scholar
  41. 41.
    Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-β-lactamase gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009;53(12):5046–54. Scholar
  42. 42.
    Wilson ME, Chen LH. NDM-1 and the role of travel in its dissemination. Curr Infect Dis Rep. 2012;14:213–26. Scholar
  43. 43.
    Mataseje LF, Abdesselam K, Vachon J, Mitchel R, Bryce E, Roscoe D, et al. Results from the Canadian Nosocomial Infection Surveillance Program on carbapenemase-producing Enterobacteriaceae, 2010 to 2014. Antimicrob Agents Chemother. 2016;60:6787–94. Scholar
  44. 44.
    Jain A, Hopkins KL, Turton J, Doumith M, Hill R, Loy R, et al. NDM carbapenemases in the United Kingdom: an analysis of the first 250 cases. J Antimicrob Chemother. 2014;69:1777–84. Scholar
  45. 45.
    Giamarellou H. Epidemiology of infections caused by polymyxin-resistant pathogens. Int J Antimicrob Agents. 2016;48:614–21. Scholar
  46. 46.
    von Wintersdorff CJ, Wolffs PF, van Niekerk JM, Beuken E, van Alphen LB, Stobberingh EE, et al. Detection of the plasmid-mediated colistin-resistance gene mcr-1 in faecal metagenomes of Dutch travellers. J Antimicrob Chemother. 2016;71:3416–9. Scholar
  47. 47.
    Piper Jenks N, Pardos de la Gandara M, D'Orazio BM, Correa da Rosa J, Kost RG, Khalida C, et al. Differences in prevalence of community-associated MRSA and MSSA among U.S. and non-U.S. born populations in six New York Community Health Centers. Travel Med Infect Dis. 2016;14:551–60. Scholar
  48. 48.
    Zanger P, Nurjadi D, Schleucher R, Scherbaum H, Wolz C, Kremsner PG, et al. Import and spread of Panton-Valentine Leukocidin-positive Staphylococcus aureus through nasal carriage and skin infections in travelers returning from the tropics and subtropics. Clin Infect Dis. 2012;54:483–92. Scholar
  49. 49.
    Nurjadi D, Friedrich-Janicke B, Schafer J, Van Genderen PJ, Goorhuis A, Perignon A, et al. Skin and soft tissue infections in intercontinental travellers and the import of multi-resistant Staphylococcus aureus to Europe. Clin Microbiol Infect. 2015;21:567.e1–10. Scholar
  50. 50.
    Ali H, Nash JQ, Kearns AM, Pichon B, Vasu V, Nixon Z, et al. Outbreak of a south West Pacific clone Panton-Valentine leucocidin-positive methicillin-resistant Staphylococcus aureus infection in a UK neonatal intensive care unit. J Hosp Infect. 2012;80:293–8. Scholar
  51. 51.
    Tristan A, Bes M, Meugnier H, Lina G, Bozdogan B, Courvalin P, et al. Global distribution of Panton-Valentine leukocidin—positive methicillin-resistant Staphylococcus aureus, 2006. Emerg Infect Dis. 2007;13(4):594–600. Scholar
  52. 52.
    Zhou YP, Wilder-Smith A, Hsu LY. The role of international travel in the spread of methicillin-resistant Staphylococcus aureus. J Travel Med. 2014;21:272–81. Scholar
  53. 53.
    World Health Organization. Typhoid. Available online at: Accessed 21 Feb 2018.
  54. 54.
    Azmatullah A, Qamar FN, Thaver D, Zaidi AK, Bhutta ZA. Systematic review of the global epidemiology, clinical and laboratory profile of enteric fever. J Glob Health. 2015;5(2):020407. CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    • Date KA, Newton AE, Medalla F, Blackstock A, Richardson L, McCullough A, et al. Changing patterns in enteric fever incidence and increasing antibiotic resistance of enteric fever isolates in the United States, 2008-2012. Clin Infect Dis. 2016;63:322–9. This is a large study from the U.S. demonstrating the rising rates of resistant enteric fever (typhoid and paratyphoid fever). CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Zhou K, Sauve LJ, Richardson SE, Ford-Jones EL, Morris SK. Enteric fever in a multicultural Canadian tertiary care pediatric setting: a 28-year review. J Pediatric Infect Dis Soc. 2017;6(1):98–101. PubMedCrossRefGoogle Scholar
  57. 57.
    Requena-Mendez A, Berrocal M, Almela M, Soriano A, Gascon J, Munoz J. Enteric fever in Barcelona: changing patterns of importation and antibiotic resistance. Travel Med Infect Dis. 2016;14:577–82. Scholar
  58. 58.
    Nuesch-Inderbinen M, Abgottspon H, Sagesser G, Cernela N, Stephan R. Antimicrobial susceptibility of travel-related Salmonella enterica serovar Typhi isolates detected in Switzerland (2002-2013) and molecular characterization of quinolone resistant isolates. BMC Infect Dis. 2015;15:212. Scholar
  59. 59.
    • Dave J, Warburton F, Freedman J, de Pinna E, Grant K, Sefton A, et al. What were the risk factors and trends in antimicrobial resistance for enteric fever in London 2005-2012? J Med Microbiol. 2017;08:08–705. This is a large U.K. study demonstrating the rising rates of resistant enteric fever. CrossRefGoogle Scholar
  60. 60.
    Hassing RJ, Goessens WH, van Pelt W, Mevius DJ, Stricker BH, Molhoek N, et al. Salmonella subtypes with increased MICs for azithromycin in travelers returned to The Netherlands. Emerg Infect Dis. 2014;20:705–8. Scholar
  61. 61.
    O’Donnell AT, Vieira AR, Huang JY, Whichard J, Cole D, Karp BE. Quinolone-resistant Salmonella enterica serotype Enteritidis infections associated with international travel. Clin Infect Dis. 2014;59(9):e139–41. Scholar
  62. 62.
    Rodriguez I, Rodicio MR, Guerra B, Hopkins KL. Potential international spread of multidrug-resistant invasive Salmonella enterica serovar enteritidis. Emerg Infect Dis. 2012;18:1173–6. Scholar
  63. 63.
    Gunell M, Aulu L, Jalava J, Lukinmaa-Aberg S, Osterblad M, Ollgren J, et al. Cefotaxime-resistant Salmonella enterica in travelers returning from Thailand to Finland. Emerg Infect Dis. 2014;20:1214–7. Scholar
  64. 64.
    Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, et al. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis. 2013;13:672–9. Scholar
  65. 65.
    Day MR, Meunier D, Doumith M, De Pinna E, Woodford N, Hopkins KL. Carbapenemase-producing Salmonella enterica isolates in the UK. J Antimicrob Chemother. 2015;70:2165–7. Scholar
  66. 66.
    Ricotta EE, Palmer A, Wymore K, Clogher P, Oosmanally N, Robinson T, et al. Epidemiology and antimicrobial resistance of international travel-associated Campylobacter infections in the United States, 2005-2011. Am J Public Health. 2014;104:e108–14. CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Post A, Martiny D, van Waterschoot N, Hallin M, Maniewski U, Bottieau E, et al. Antibiotic susceptibility profiles among Campylobacter isolates obtained from international travelers between 2007 and 2014. Eur J Clin Microbiol Infect Dis. 2017;36:2101–7. Scholar
  68. 68.
    Ashkenazi S, Levy I, Kazaronovski V, Samra Z. Growing antimicrobial resistance of Shigella isolates. J Antimicrob Chemother. 2003;51(2):427–9.CrossRefPubMedGoogle Scholar
  69. 69.
    Shiferaw B, Solghan S, Palmer A, Joyce K, Barzilay EJ, Krueger A, et al. Antimicrobial susceptibility patterns of Shigella isolates in Foodborne Diseases Active Surveillance Network (FoodNet) sites, 2000-2010. Clin Infect Dis. 2012;54(Suppl 5):S458–63. CrossRefPubMedGoogle Scholar
  70. 70.
    Li YL, Tewari D, Yealy CC, Fardig D, M'Ikanatha NM. Surveillance for travel and domestically acquired multidrug-resistant human Shigella infections-Pennsylvania, 2006-2014. Health Secur. 2016;14:143–51. Scholar
  71. 71.
    Sadouki Z, Day MR, Doumith M, Chattaway MA, Dallman TJ, Hopkins KL, et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Shigella sonnei isolated from cases of diarrhoeal disease in England and Wales, 2015. J Antimicrob Chemother. 2017;72:2496–502. Scholar
  72. 72.
    Lane CR, Sutton B, Valcanis M, Kirk M, Walker C, Lalor K, et al. Travel destinations and sexual behavior as indicators of antibiotic resistant Shigella strain—Victoria, Australia. Clin Infect Dis. 2016;62(6):722–9. Scholar
  73. 73.
    The UN Refugee Agency. Available online at: Accessed 21 Feb 2018.
  74. 74.
    Reinheimer C, Kempf VA, Gottig S, Hogardt M, Wichelhaus TA, O'Rourke F, et al. Multidrug-resistant organisms detected in refugee patients admitted to a University Hospital, Germany June-December 2015. Euro Surveill. 2016;21.
  75. 75.
    Tenenbaum T, Becker KP, Lange B, Martin A, Schafer P, Weichert S, et al. Prevalence of multidrug-resistant organisms in hospitalized pediatric refugees in an University Children's Hospital in Germany 2015-2016. Infect Control Hosp Epidemiol. 2016;37:1310–4. CrossRefPubMedGoogle Scholar
  76. 76.
    de Murcia KO, Glatz B, Willems S, Kossow A, Strobel M, Stuhmer B, et al. Prevalence of multidrug resistant bacteria in refugees: a prospective case control study in an obstetric cohort. Z Geburtshilfe Neonatol. 2017;221:132–6. Scholar
  77. 77.
    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;22:300–5. Scholar
  78. 78.
    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;20:22–8. Scholar
  79. 79.
    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;11:11. Scholar
  80. 80.
    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;82:254–9. Scholar
  81. 81.
    Olaitan AO, Dia NM, Gautret P, Benkouiten S, Belhouchat K, Drali T, et al. Acquisition of extended-spectrum cephalosporin- and colistin-resistant Salmonella enterica subsp. enterica serotype Newport by pilgrims during Hajj. Int J Antimicrob Agents. 2015;45:600–4. Scholar
  82. 82.
    Leangapichart T, Tissot-Dupont H, Raoult D, Memish ZA, Rolain JM, Gautret P. Risk factors for acquisition of CTX-M genes in pilgrims during Hajj 2013 and 2014. J Antimicrob Chemother. 2017;72:2627–35. Scholar
  83. 83.
    Leangapichart T, Gautret P, Brouqui P, Mimish Z, Raoult D, Rolain JM. Acquisition of mcr-1 plasmid-mediated colistin resistance in Escherichia coli and Klebsiella pneumoniae during Hajj 2013 and 2014. Antimicrob Agents Chemother. 2016;60:6998–9. Scholar
  84. 84.
    Leangapichart T, Gautret P, Griffiths K, Belhouchat K, Memish Z, Raoult D, et al. Acquisition of a high diversity of bacteria during the Hajj pilgrimage, including Acinetobacter baumannii with blaOXA-72 and Escherichia coli with blaNDM-5 carbapenemase genes. Antimicrob Agents Chemother. 2016;60:5942–8. Scholar

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© Crown 2018

Authors and Affiliations

  1. 1.Public Health OntarioTorontoCanada
  2. 2.Dalla Lana School of Public HealthUniversity of TorontoTorontoCanada
  3. 3.St. Joseph’s Health CentreTorontoCanada
  4. 4.Division of Infectious DiseasesThe Hospital for Sick ChildrenTorontoCanada
  5. 5.Department of Pediatrics, Faculty of MedicineUniversity of TorontoTorontoCanada

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