Duration of travel-associated faecal colonisation with ESBL-producing enterobacteriaceae - A one year follow-up study

PLoS ONE

Volumn 13, Issue 10, 2018, Pages

  ÖstholmBalkhed, Åse ^a   Tärnberg, Maria ^a   Nilsson, Maud ^a   Nilsson, Lennart E ^a   Hanberger, Håkan ^a   Hällgren, Anita ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMOXICILLIN PLUS CLAVULANIC ACID; CARBAPENEM DERIVATIVE; CEFEPIME; CEFOTAXIME; CEFTAZIDIME; CIPROFLOXACIN; COTRIMOXAZOLE; ERTAPENEM; FOSFOMYCIN; GENTAMICIN; IMIPENEM; MECILLINAM; MEROPENEM; NITROFURANTOIN; PIPERACILLIN PLUS TAZOBACTAM; TEMOCILLIN; TIGECYCLINE; TOBRAMYCIN; BACTERIAL PROTEIN; BETA LACTAMASE;

ADULT; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIUM CARRIER; BACTERIUM ISOLATE; CONTROLLED STUDY; DIARRHEA; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ESCHERICHIA COLI; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING KLEBSIELLA PNEUMONIAE; FECES ANALYSIS; FEMALE; FOLLOW UP; HUMAN; MAJOR CLINICAL STUDY; MALE; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; QUESTIONNAIRE; RISK FACTOR; TRAVEL; ANTIBIOTIC RESISTANCE; CLINICAL TRIAL; DRUG EFFECT; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTION; ENZYMOLOGY; FECES; LONGITUDINAL STUDY; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MULTICENTER STUDY; PROSPECTIVE STUDY; TIME FACTOR; TRAVEL RELATED DISEASE;

ADULT; BACTERIAL PROTEINS; BETA-LACTAMASES; DIARRHEA; DRUG RESISTANCE, BACTERIAL; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; FECES; FEMALE; FOLLOW-UP STUDIES; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; RISK FACTORS; TIME FACTORS; TRAVEL; TRAVEL-RELATED ILLNESS;

EID: 85055449450     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0205504     Document Type: Article

References (42)

1. Sasaki T, Hirai I, Niki M, Nakamura T, Komalamisra C, Maipanich W, et al. High prevalence of CTX-M beta-lactamase-producing Enterobacteriaceae in stool specimens obtained from healthy individuals in Thailand. J Antimicrob Chemother. 2010; 65: 666-668. https://doi.org/10.1093/jac/dkq008 PMID: 20106863
2. Li B, Sun JY, Liu QZ, Han LZ, Huang XH, Ni YX. High prevalence of CTX-M beta-lactamases in faecal Escherichia coli strains from healthy humans in Fuzhou, China. Scand J Infect Dis. 2011; 43: 170-174. https://doi.org/10.3109/00365548.2010.538856 PMID: 21128708
3. Luvsansharav UO, Hirai I, Nakata A, Imura K, Yamauchi K, Niki M, et al. Prevalence of and risk factors associated with faecal carriage of CTX-M beta-lactamase-producing Enterobacteriaceae in rural Thai communities. J Antimicrob Chemother. 2012; 67: 1769-1774. https://doi.org/10.1093/jac/dks118 PMID: 22514260
4. Zhong YM, Liu WE, Liang XH, Li YM, Jian ZJ, Hawkey PM. Emergence and spread of O16-ST131 and O25b-ST131 clones among faecal CTX-M-producing Escherichia coli in healthy individuals in Hunan Province, China. J Antimicrob Chemother. 2015; 70: 2223-2227. https://doi.org/10.1093/jac/dkv114 PMID: 25957581
5. ECDC, the European Centre for Disease Prevention and Control. Surveillance of antimicrobial resistance in Europe 2016. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). 2017. [cited 2018 Feb 28]. Available from: https://ecdc.europa.eu/sites/portal/files/documents/AMR-surveillance-Europe-2016.pdf.
6. 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: 3564-3568. https://doi.org/10.1128/AAC.00220-10 PMID: 20547788
7. Östholm-Balkhed Å, Tärnberg M, Nilsson M, Nilsson LE, Hanberger H, Hällgren A; Travel Study Group of Southeast Sweden. Travel-associated faecal colonization with ESBL-producing Enterobacteriaceae: incidence and risk factors. J Antimicrob Chemother. 2013; 68: 2144-2153. https://doi.org/10.1093/jac/dkt167 PMID: 23674762
8. 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: 649-657. https://doi.org/10.3201/eid.2004.131718 PMID: 24655888
9. Hassing RJ, Alsma J, Arcilla MS, van Genderen PJ, Stricker BH, Verbon A. International travel and acquisition of multidrug-resistant Enterobacteriaceae: a systematic review. Euro Surveill. 2015; 20(47): pii = 30074. https://doi.org/10.2807/1560-7917.ES.2015.20.47.30074 PMID: 26625301
10. 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: 837-846. https://doi.org/10.1093/cid/ciu957 PMID: 25613287
11. 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: 593-600. https://doi.org/10.1093/cid/civ333 PMID: 25904368
12. Vading M, Kabir MH, Kalin M, Iversen A, Wiklund S, Nauclér P, et al. Frequent acquisition of low-virulence strains of ESBL-producing Escherichia coli in travellers. J Antimicrob Chemother. 2016; 71: 3548-3555. https://doi.org/10.1093/jac/dkw335 PMID: 27566312
13. 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: 78-85. https://doi.org/10.1016/S1473-3099(16)30319-X PMID: 27751772
14. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD. Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect. 2008; 57: 441-448. https://doi.org/10.1016/j.jinf.2008.09.034 PMID: 18990451
15. Pitout JD, Campbell L, Church DL, Gregson DB, Laupland KB. Molecular characteristics of travelrelated extended-spectrum beta-lactamase-producing Escherichia coli isolates from the Calgary Health Region. Antimicrob Agents Chemother. 2009; 53: 2539-2543. https://doi.org/10.1128/AAC.00061-09 PMID: 19364876
16. Søraas 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): e69581. https://doi.org/10.1371/journal.pone.0069581 PMID: 23936052
17. van Loon K, Voor in 't holt AF, Vos MC. A systematic review and meta-analyses of the clinical epidemiology of carbapenem-resistant Enterobacteriaceae. Antimicrob Agents Chemother. 2017 Dec 21. 62: e01730-17. https://doi.org/10.1128/AAC.01730-17 PMID: 29038269
18. Bert F, Larroque B, Paugam-Burtz C, Dondero F, Durand F, Marcon E, et al. Pretransplant fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and infection after liver transplant, France. Emerg Infect Dis. 2012; 18: 908-916. https://doi.org/10.3201/eid1806.110139 PMID: 22607885
19. Cornejo-Juárez P, Suárez-Cuenca JA, Volkow-Fernández P, Silva-Sánchez J, Barrios-Camacho H, Nájera-León E, et al. Fecal ESBL Escherichia coli carriage as a risk factor for bacteremia in patients with hematological malignancies. Support Care Cancer. 2016; 24: 253-259. https://doi.org/10.1007/s00520-015-2772-z PMID: 26014616
20. Cheikh A, Belefquih B, Chajai Y, Cheikhaoui Y, El Hassani A, Benouda A. Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs) colonization as a risk factor for developing ESBL infections in pediatric cardiac surgery patients: "retrospective cohort study". BMC Infect Dis. 2017; 17: 237. https://doi.org/10.1186/s12879-017-2346-4 PMID: 28356079
21. Lübbert C, Straube L, Stein C, Makarewicz O, Schubert S, Mössner 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: 148-156. https://doi.org/10.1016/j.ijmm.2014.12.001 PMID: 25547265
22. 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: 1206-1213. https://doi.org/10.3201/eid.1908.130257 PMID: 23885972
23. Monstein HJ, Tärnberg M, Nilsson LE. Molecular identification of CTX-M and blaOXY/K1 beta-lactamase genes in Enterobacteriaceae by sequencing of universal M13-sequence-tagged PCR-amplicons. BMC Infect Dis. 2009; 9: 7. https://doi.org/10.1186/1471-2334-9-7 PMID: 19161622
24. Tärnberg M, Nilsson LE, Monstein HJ. Molecular identification of (bla)SHV, (bla)LEN and (bla)OKP beta-lactamase genes in Klebsiella pneumoniae by bi-directional sequencing of universal SP6- and T7-sequence-tagged (bla)SHV-PCR amplicons. Mol Cell Probes. 2009; 23: 195-200. PMID: 19496249
25. Östholm-Balkhed Å, Tärnberg M, Nilsson M, Johansson AV, Hanberger H, Monstein HJ, Nilsson LE. Prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae and trends in antibiotic consumption in a county of Sweden. Scand J Infect Dis. 2010; 42: 831-838. https://doi.org/10.3109/00365548.2010.498017 PMID: 20608768
26. Pérez-Pérez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol. 2002; 40: 2153-2162. https://doi.org/10.1128/JCM. 40.6.2153-2162.2002 PMID: 12037080
27. EUCAST, the European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters v 7.1. 2017. [cited 2018 jan 8]. Avaliable from: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST-files/Breakpoint-tables/v-7.1-Breakpoint-Tables.pdf.
28. EUCAST, the European Committee on Antimicrobial Susceptibility Testing. Antimicrobial wild type distributions of microorganisms. [cited 2018 Feb 28]. Avaliable from: https://mic.eucast.org/Eucast2/.
29. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2011; 18: 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x PMID: 21793988
30. Valverde A, Grill F, Coque TM, Pintado V, Baquero F, Cantón R, et al. High rate of intestinal colonization with extended-spectrum-beta-lactamase-producing organisms in household contacts of infected community patients. J Clin Microbiol. 2008; 46: 2796-2799. https://doi.org/10.1128/JCM.01008-08 PMID: 18562591
31. Lo WU, Ho PL, Chow KH, Lai EL, Yeung F, Chiu SS. Fecal carriage of CTXM type extended-spectrum beta-lactamase-producing organisms by children and their household contacts. J Infect. 2010; 60: 286-292. https://doi.org/10.1016/j.jinf.2010.02.002 PMID: 20144898
32. Löhr IH, Rettedal S, Natås OB, Naseer U, Oymar K, Sundsfjord A. Long-term faecal carriage in infants and intra-household transmission of CTX-M-15-producing Klebsiella pneumoniae following a nosocomial outbreak. J Antimicrob Chemother. 2013; 68: 1043-1048. https://doi.org/10.1093/jac/dks502 PMID: 23288401
33. Liakopoulos A, van den Bunt G, Geurts Y, Bootsma MCJ, Toleman M, Ceccarelli D, et al. High prevalence of intra-familial co-colonization by extended-spectrum cephalosporin resistant enterobacteriaceae in preschool children and their parents in Dutch households. Front Microbiol. 2018; 9: 293. https://doi.org/10.3389/fmicb.2018.00293 PMID: 29515562
34. Woerther P-L, Andremont A, Kantele A. 2017. 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
35. Östholm Balkhed Å, Tärnberg M, Monstein HJ, Hällgren A, Hanberger H, Nilsson LE. High frequency of co-resistance in CTX-M-producing Escherichia coli to non-beta-lactam antibiotics, with the exceptions of amikacin, nitrofurantoin, colistin, tigecycline, and fosfomycin, in a county of Sweden. Scand J Infect Dis. 2013; 45: 271-278. https://doi.org/10.3109/00365548.2012.734636 PMID: 23113731
36. Ny S, Löfmark S, Börjesson S, Englund S, Ringman M, Bergström J, et al. Community carriage of ESBL-producing Escherichia coli is associated with strains of low pathogenicity: a Swedish nationwide study. J Antimicrob Chemother. 2017; 72: 582-588. https://doi.org/10.1093/jac/dkw419 PMID: 27798205
37. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M. Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis. 2010; 51: 286-294. https://doi.org/10.1086/653932 PMID: 20572763
38. Rogers BA, Sidjabat HE, Paterson DL. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother. 2011; 66: 1-14. https://doi.org/10.1093/jac/dkq415 PMID: 21081548
39. Overdevest I, Haverkate M, Veenemans J, Hendriks Y, Verhulst C, Mulders A, et al. Prolonged colonisation with Escherichia coli O25:ST131 versus other extended-spectrum beta-lactamase-producing E. coli in a long-term care facility with high endemic level of rectal colonisation, the Netherlands, 2013 to 2014. Euro Surveill. 2016; 21(42): pii = 30376. https://doi.org/10.2807/1560-7917.ES.2016.21.42. 30376 PMID: 27784530
40. van Duijkeren E, Wielders CCH, Dierikx CM, van Hoek AHAM, Hengeveld P, Veenman C, et al. Longterm carriage of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in the general population in the Netherlands. Clin Infect Dis. Forthcoming 2018. https://doi.org/10.1093/cid/cix1015 PMID: 29149242
41. Jørgensen SB, Søraas A, Sundsfjord A, Liestøl K, Leegaard TM, Jenum PA. Fecal carriage of extended-spectrum beta-lactamase producing Escherichia coli and Klebsiella pneumoniae after urinary tract infection-A three year prospective cohort study. PLoS ONE. 2017; 12(3): e0173510. https://doi.org/10.1371/journal.pone.0173510 PMID: 28267783
42. Titelman E, Hasan CM, Iversen A, Nauclér P, Kais M, Kalin M, et al. Faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae is common 12 months after infection and is related to strain factors. Clin Microbiol Infect. 2014; 20: O508-O515. https://doi.org/10.1111/1469-0691.12559 PMID: 24450760