Quinolone nonsusceptibility among enteric pathogens isolated from international travelers – Foodborne Diseases Active Surveillance Network (FoodNet) and National Antimicrobial Monitoring System (NARMS), 10 United States sites, 2004 – 2014

Autoři: Julian E. Grass aff001;  Sunkyung Kim aff001;  Jennifer Y. Huang aff001;  Stephanie M. Morrison aff002;  Andre E. McCullough aff001;  Christy Bennett aff001;  Cindy R. Friedman aff001;  Anna Bowen aff001
Působiště autorů: Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America aff001;  Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225800


Gastrointestinal illnesses are the most frequently diagnosed conditions among returning U.S. travelers. Although most episodes of travelers’ diarrhea do not require antibiotic therapy, fluoroquinolones (a type of quinolone antibiotic) are recommended for treatment of moderate and severe travelers’ diarrhea as well as many other types of severe infection. To assess associations between quinolone susceptibility and international travel, we linked data about isolate susceptibility in NARMS to cases of enteric infections reported to FoodNet. We categorized isolates as quinolone-nonsusceptible (QNS) if they were resistant or had intermediate susceptibility to ≥1 quinolone. Among 1,726 travel-associated infections reported to FoodNet with antimicrobial susceptibility data in NARMS during 2004–2014, 56% of isolates were quinolone-nonsusceptible, of which most (904/960) were Campylobacter. International travel was associated with >10-fold increased odds of infection with quinolone-nonsusceptible bacteria. Most QNS infections were associated with travel to Latin America and the Caribbean (390/743; 52%); however, the greatest risk of QNS infection was associated with travel to Africa (120 per 1,000,000 passenger journeys). Preventing acquisition and onward transmission of antimicrobial-resistant enteric infections among travelers is critical.

Klíčová slova:

Antibiotics – Antimicrobial resistance – Bacterial pathogens – Campylobacter – Diarrhea – Shigella – Shigellosis – United States


1. World Tourism Organization (UNWTO). Tourism Highlights. 2016 edition. [cited 2016 Dec 14]. http://www.e-unwto.org/doi/pdf/10.18111/9789284418145

2. Harvey K, Esposito DH, Han P, Kozarsky P, Freedman DO, Plier DA, et al. Surveillance for travel-related disease—GeoSentinel Surveillance System, United States, 1997–2011. MMWR Morb Mortal Wkly Rep. 2013;62:1–23. 23863769

3. Riddle MS, Connor BA, Beeching NJ, DuPont HL, Hamer DH, Kozarsky P, et al. Guidelines for the prevention and treatment of travelers’ diarrhea: a graded expert panel report. J Travel Med. 2017;24(suppl_1):S57–S74. doi: 10.1093/jtm/tax026 28521004

4. Bowen A, Hurd J, Hoover C, Khachadourian Y, Traphagen E, Harvey E, et al. Importation and domestic transmission of Shigella sonnei resistant to ciprofloxacin—United States, May 2014–February 2015. MMWR Morb Mortal Wkly Rep. 2015;64:318–320. 25837241

5. 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 Nov;36:2101–2107. doi: 10.1007/s10096-017-3032-6 28623550

6. Centers for Disease Control and Prevention. Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet Surveillance Report for 2015 (Final Report). Atlanta: U.S. Department of Health and Human Services, CDC. 2017.

7. Kendall ME, Crim S, Fullerton K, Han PV, Cronquist AB, Shiferaw B, et al. Travel-associated enteric infections diagnosed after return to the United States, Foodborne Diseases Active Surveillance Network (FoodNet), 2004–2009. Clin Infect Dis. 2012;54 Suppl 5:S480–487. doi: 10.1093/cid/cis052 22572673

8. Centers for Disease Control and Prevention. National Antimicrobial Monitoring System for Enteric Bacteria (NARMS): human isolates surveillance report, 2015. Atlanta: U.S. Department of Health and Human Services, CDC. 2018.

9. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 27th ed. CLSI supplement M100. CLSI, Wayne, Pennsylvania, 2017.

10. World Health Organization. Composition of macro geographical (continental) regions, geographical sub-regions, and selected economic and other groupings. 2016. [cited 2016 July 6]. http://unstats.un.org/unsd/methods/m49/m49regin.htm.

11. International Air Transport Association (IATA). [cited 2016 Sept 15]. http://www.iata.org/services/statistics/intelligence/airportis/Pages/index.aspx

12. Parisi A, Crump JA, Glass K, Howden BP, Furuya-Kanamori L, Vilkins S, et al. Health Outcomes from Multidrug-Resistant Salmonella Infections in High-Income Countries: A Systematic Review and Meta-Analysis. Foodborne Pathog Dis. 2018 Jul;15(7):428–436. doi: 10.1089/fpd.2017.2403 29624414

13. Founou RC, Founou LL, Essack SY. Clinical and economic impact of antibiotic resistance in developing countries: A systematic review and meta-analysis. PLoS One. 2017; 12(12): e0189621. doi: 10.1371/journal.pone.0189621 29267306

14. McNulty CAM, Lecky DM, Xu-McCrae L, Nakiboneka-Ssenabulya D, Chung KT, Nichols T, et al. CTX-M ESBL-producing Enterobacteriaceae: estimated prevalence in adults in England in 2014. J Antimicrob Chemother. 2018 May 1;73(5):1368–1388. doi: 10.1093/jac/dky007 29514211

15. Barreto Miranda I, Ignatius R, Pfüller R, Friedrich-Jänicke 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 Feb 8;23(2):tav024. doi: 10.1093/jtm/tav024 26858272

16. 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 travelers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis. 2017;17:78–85. doi: 10.1016/S1473-3099(16)30319-X 27751772

17. Hicks LA, Taylor TH Jr, Hunkler RJ. U.S. outpatient antibiotic prescribing, 2010. N Engl J Med. 2013;368:1461–1462. doi: 10.1056/NEJMc1212055 23574140

18. Angelo KM, Kozarsky PE, Ryan ET, Chen LH, Sotir MJ. What proportion of international travellers acquire a travel-related illness? A review of the literature. J Travel Med. 2017 Sep 1;24(5). doi: 10.1093/jtm/tax046 28931136

19. Lääveri T, Vilkman K, Pakkanen SH, Kirveskari J, Kantele A. A prospective study of travellers' diarrhoea: analysis of pathogen findings by destination in various (sub)tropical regions. Clin Microbiol Infect. 2018 Aug;24(8):908.e9–908.e16. doi: 10.1016/j.cmi.2017.10.034 29133155

20. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States–Major pathogens. Emerg Infect Dis. 2011;17:1–15. doi: 10.3201/eid1701.101210 21192848

21. Vilkman K, Lääveri T, Pakkanen SH, Kantele A. Stand-by antibiotics encourage unwarranted use of antibiotics for travelers' diarrhea: A prospective study. Travel Med Infect Dis. 2019 Jan-Feb;27:64–71. doi: 10.1016/j.tmaid.2018.06.007 29894796

22. Lääveri T, Vilkman K, Pakkanen S, Kirveskari J, Kantele A. Despite antibiotic treatment of travellers' diarrhoea, pathogens are found in stools from half of travelers at return. Travel Med Infect Dis. 2018 May—Jun;23:49–55. doi: 10.1016/j.tmaid.2018.04.003 29702254

23. Malik U, Armstrong D, Ashworth M, Dregan A, L'Esperance V, McDonnell L, et al. Association between prior antibiotic therapy and subsequent risk of community-acquired infections: a systematic review. J Antimicrob Chemother. 2018 Feb 1;73:287–296. doi: 10.1093/jac/dkx374 29149266

24. Kantele A, Mero S, Kirveskari J, Lääveri T. Increased Risk for ESBL-Producing Bacteria from Co-administration of Loperamide and Antimicrobial Drugs for Travelers' Diarrhea. Emerg Infect Dis. 2016 Jan;22(1):117–20. doi: 10.3201/eid2201.151272 26691898

25. DuPont HL, Ericsson CD, Farthing MJ, Gorbach S, Pickering LK, Rombo L, et al. Expert review of the evidence base for self-therapy of travelers' diarrhea. J Travel Med. 2009 May-Jun;16(3):161–71. doi: 10.1111/j.1708-8305.2009.00300.x 19538576

26. Kantele A. A call to restrict prescribing antibiotics for travellers’ diarrhea—Travel medicine practitioners can play an active role in preventing the spread of antimicrobial resistance. Travel Med Infect Dis. 2015 May-Jun;13(3):213–4. doi: 10.1016/j.tmaid.2015.05.005 26005160

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden