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Eurosurveillance, Volume 20, Issue 47, 26 November 2015
Systematic Review
Hassing, Alsma, Arcilla, van Genderen, Stricker, and Verbon: International travel and acquisition of multidrug-resistant Enterobacteriaceae: a systematic review

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Citation style for this article: 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. DOI:

Received:10 March 2015; Accepted:23 September 2015



Worldwide, the number of international travellers has grown from 25 million in 1950 to 1,087 million in 2013 [1]. According to the World Tourism Organization, this number is expected to increase by an average of 3.3% a year [1]. Of the international travellers visiting developing countries, 22–64% have self-reported health problems and about 8% require medical care during or after travel [2,3]. Healthy travellers may be exposed to a broad range of microorganisms while travelling, including drug-resistant Enterobacteriaceae, which may subsequently be introduced into their home country [4,5].

Enterobacteriaceae are Gram-negative bacteria that are part of the human body’s normal commensal flora, called microbiota. Enterobacteriaceae, such as Escherichia coli and Klebsiella species, are capable of causing both healthcare-associated and community-acquired infections [6]. Multidrug-resistant Enterobacteriaceae (MRE), including extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae (ESBL-E) and plasmid-mediated Amp C-producing Enterobacteriaceae (pAmp C-E) are emerging worldwide [7]. Cases of carbapenemase-producing Enterobacteriaceae (CPE) are also reported more frequently [8].

Since 2003, community carriage rates of MRE have increased dramatically in various regions, such as South-East Asia, the Western Pacific and the Eastern Mediterranean [7]. During visits to such areas, travellers might acquire MRE and become asymptomatic carriers of MRE. In their home country, they may cause spread in the community and contribute to worldwide emerging antimicrobial resistance [6,9,10]. Acquired MRE in the digestive tract are considered apathogenic, however carriage of such Enterobacteriaceae have resulted in clinically relevant infections [8]. International travel has been reported as a risk factor for urinary tract infections caused by ESBL-E [11,12]. The question arises if these observations warrant clinicians being aware of MRE in recently returned otherwise healthy, international travellers who seek medical attention even for unrelated conditions.


The aim of this systematic review was to determine the effect of international travel on the risk of acquisition of faecal carriage of MRE. A secondary objective was to determine risk factors for acquisition of drug resistance.


Protocol and registration

A specific protocol was designed and used to conduct the study. The study is registered in the international prospective register of systematic reviews (PROSPERO) under registration number CRD42015024973.

Search strategy and selection criteria

The systematic review was conducted according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [13]. The following databases were searched, attempting to identify all relevant studies: Embase, MEDLINE, Web of Science, Scopus, Cochrane Library, PubMed and Google Scholar. The latest search was conducted on 17 August 2015.

The topic search terms used for searching the databases were ‘Gram negative bacteria’, ‘Gram negative bacterial infections’, ‘Enterobacteriaceae’, ‘Escherichia’, ‘Klebsiella’, ‘Campylobacter’, ‘Salmonella’, ‘Shigella’, ’Yersinia’, ‘travel’, ‘traveller’, ‘tourist’, ‘tourism’, ‘turista’, ‘aviation’, ‘air transport’, ‘airport’, ‘colonisation’, ‘carriage’, ‘carrier’, ‘susceptibility’ and ‘(multiple) drug resistance’.

The queries differed per database searched and were developed with help of a biomedical information specialist (Box). Articles written in English, German, French and Dutch were included.


Search strategy for systematic review of the acquisition of multidrug-resistant Enterobacteriaceae in international travel
('Gram negative bacterium'/exp OR 'Gram negative infection'/de OR Enterobacteriaceae/de OR Escherichia/exp OR Klebsiella/exp OR Salmonella/exp OR Shigella/exp OR Yersinia/exp OR 'Enterobacteriaceae infection'/exp OR ('Gram negative' OR Enterobacteri* OR (Enter* NEXT/1 bacteria*) OR Enterobacter* OR Escherichia* OR 'e coli' OR Klebsiella* OR Salmonell* OR Shigell* OR Yersinia*):ab,ti) AND (travel/de OR 'traveller diarrhoea'/de OR aviation/exp OR (travel* OR touris* OR turista OR aviation OR 'air transport' OR airport*):ab,ti) AND ('antibiotic resistance'/exp OR 'multidrug resistance'/de OR 'drug resistance'/de OR 'antibiotic sensitivity'/de OR 'bacterial colonization'/exp OR 'bacterium carrier'/de OR (resistan* OR coloni* OR ((antibiotic* OR antimicrob*) NEAR/3 sensitivit*) OR susceptib* OR carriage* OR carrier*):ab,ti) NOT ([animals]/lim NOT [humans]/lim)

(exp “Gram-Negative Bacteria”/ OR exp “Gram-Negative Bacterial Infections”/ OR Enterobacteriaceae/ OR exp Escherichia/ OR exp Klebsiella/ OR exp Salmonella/ OR exp Shigella/ OR exp Yersinia/ OR exp “Enterobacteriaceae infections”/ OR (“Gram negative” OR Enterobacteri* OR (Enter* ADJ bacteria*) OR Enterobacter* OR Escherichia* OR “e coli” OR Klebsiella* OR Salmonell* OR Shigell* OR Yersinia*).ab,ti.) AND (travel/ OR “Travel Medicine”/ OR exp aviation/ OR (travel* OR touris* OR turista OR aviation OR “air transport” OR airport*).ab,ti.) AND (exp “Drug Resistance, Microbial”/ OR exp “Drug Resistance, Multiple”/ OR “drug resistance”/ OR “bacterium carrier”/ OR (resistan* OR coloni* OR ((antibiotic* OR antimicrob*) ADJ3 sensitivit*) OR susceptib* OR carriage* OR carrier*).ab,ti.) NOT (exp animals/ NOT humans/)

Cochrane Library
(('Gram negative' OR Enterobacteri* OR (Enter* NEXT/1 bacteria*) OR Enterobacter* OR Escherichia* OR 'e coli' OR Klebsiella* OR Salmonell* OR Shigell* OR Yersinia*):ab,ti) AND ((travel* OR touris* OR turista OR aviation OR 'air transport' OR airport*):ab,ti) AND ((resistan* OR coloni* OR ((antibiotic* OR antimicrob*) NEAR/3 sensitivit*) OR susceptib* OR carriage* OR carrier*):ab,ti)

Web of Science 
TS = (((“Gram negative” OR Enterobacteri* OR (Enter* NEAR/1 bacteria*) OR Enterobacter* OR Escherichia* OR “e coli” OR Klebsiella* OR Salmonell* OR Shigell* OR Yersinia*)) AND ((travel* OR touris* OR turista OR aviation OR “air transport” OR airport*)) AND ((resistan* OR coloni* OR ((antibiotic* OR antimicrob*) NEAR/3 sensitivit*) OR susceptib* OR carriage* OR carrier*)))

TITLE-ABS-KEY(((“Gram negative” OR Enterobacteri* OR (Enter* W/1 bacteria*) OR Enterobacter* OR Escherichia* OR “e coli” OR Klebsiella* OR Salmonell* OR Shigell* OR Yersinia*)) AND ((travel* OR touris* OR turista OR aviation OR “air transport” OR airport*)) AND ((resistan* OR coloni* OR ((antibiotic* OR antimicrob*) W/3 sensitivit*) OR susceptib* OR carriage* OR carrier*)))

((Gram negative[tiab] OR Enterobacteri*[tiab] OR Entero bacteria*[tiab] OR Enteric bacteria*[tiab] OR Enterobacter*[tiab] OR Escherichia*[tiab] OR e coli[tiab] OR Klebsiella*[tiab] OR Salmonell*[tiab] OR Shigell*[tiab] OR Yersinia*[tiab])) AND ((travel*[tiab] OR touris*[tiab] OR turista[tiab] OR aviation[tiab] OR air transport*[tiab] OR airport*[tiab])) AND ((resistan*[tiab] OR coloni*[tiab] OR ((antibiotic*[tiab] OR antimicrob*[tiab]) AND sensitivit*[tiab]) OR susceptib*[tiab] OR carriage*[tiab] OR carrier*[tiab])) AND publisher[sb]

Google Scholar
“Gram negative”|Enterobacteriaceae|Escherichia|Klebsiella|Salmonella|Shigella|Yersinia travel|traveller|tourist|tourism resistance|resistant|colonization|colonisation|susceptibility|carriage|carrier

For inclusion the article needed to fulfil the following criteria [1]: It needed to be related to foreign travel [2], report on screening in asymptomatic participants [3], present antimicrobial susceptibility data and [4] report on faecal Enterobacteriaceae carriage. We used the following exclusion criteria: case reports, reviews, meta-analyses, veterinary medicine, in vitro studies and studies regarding symptomatic patients. The reference lists of reviews were screened to identify studies possibly missed by the search.

Two researchers (R.H. and J.A.) independently performed the screening of the abstracts. Any discordant result was discussed in consensus meetings. After screening the abstracts, the full text of the articles was assessed for eligibility by the same two researchers and selected or rejected for inclusion in the systematic review. In case of disagreement a third researcher (A.V.) decided on inclusion.

Data collection process

The following data (if available) were extracted from each article: year of publication, country of the study, study period, study design, microorganism studied, study population, study size, age, sex, sample time before and after travel, duration of travel, travelling in pairs or groups, symptoms during travel, countries visited, MRE prevalence before travel, MRE prevalence after travel, MRE resistance acquired during travel, resistance to other antibiotic drugs of acquired MRE, risk factors for acquisition (among which travel to predefined United Nations geographical regions: southern Asia, Asia except southern Asia, Africa, South and Central America, North America, Europe and Oceania [14]), method of MRE susceptibility determination, phenotypic approaches, genotypic characterisation of post-travel MRE isolates, molecular typing of post-travel MRE isolates, duration of MRE colonisation and MRE transmission to household contacts. To obtain missing data, authors of the articles were contacted.

Quality assessment

We assessed the methodological quality and the risk of bias in individual studies that may affect the cumulative evidence, using tools for assessing quality and susceptibility to bias in observational studies as recommended in the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement [15,16].

Data synthesis and analysis

As a result of the design of the studies (cohort studies) and the heterogeneity in patient populations (e.g. travellers, healthcare workers and healthcare students), a formal meta-analysis was not possible. Therefore, the study results were summarised to describe the main outcomes of interest. The principle summary measure was percentage of MRE acquisition during travel, defined as ESBL-E or pAmp C-E. Furthermore, risk factors for acquisition of drug resistance were assessed. If possible, percentages not presented in the articles were calculated from the available data.


Study selection

A total of 2,398 studies were identified through database searching after duplicates had been removed (Figure). After screening of titles and summaries, 36 articles were selected for full-text assessment. Eleven articles were included in the qualitative synthesis of the systematic review (see Figure for reasons for exclusion) [17-27].


Flowchart for literature search on the acquisition of multidrug-resistant Enterobacteriaceae in international travel (n = 4,989)


ESBL: extended-spectrum beta-lactamase.

Study characteristics

Eleven prospective cohort studies, conducted in northern and western Europe, Australia and the United States (US) were included [17-27]. The characteristics of these studies are shown in Table 1. Nine studies investigated travellers visiting a travel or vaccination clinic, one study hospital staff and contacts, and one study healthcare students working or studying abroad. The number of study participants ranged from 28 to 574. The median age of travellers in the individual studies varied between 25 and 66 years, with the youngest group being healthcare students. In all studies, the majority of travellers were female (range: 55–78%). The proportion of participants who were lost to follow up varied from 3.8% (4/106) [18] to 30% (12/40) [21]. The mean duration of travel was similar in all studies (14–21 days). In the study by Angelin et al. on healthcare students, median length of stay was 45 days (range: 13–365 days) [22]. In four studies, follow-up samples of MRE carriers were collected at six months after returning from travel, and in one of these studies, samples were collected monthly in the first three months with further follow-up until 12 months after return [25]. Ten studies used a phenotypic method for susceptibility testing, with genotypic confirmation of ESBL positivity by PCR [17-22,24-27]. One study used a PCR-based approach [23]. In one study, only isolated E. coli were included, whereas the other studies included all isolated Enterobacteriaceae, which mainly consisted of E. coli [17-27].

Table 1

Characteristics of prospective cohort studies included for systematic review of the acquisition of multidrug-resistant Enterobacteriaceae in international travel (n = 11)

Study Country Study period Population
Study sizea Median age in years (range or SD) Proportion of women in % Identification of MRE-positive organisms in post-travel isolates Sample method used Sample time (range) before/after travel Mean duration of travel in days (range) Total number of co-travellers participating in study Follow-up of resistant isolates
Tängdén [17] Sweden November 2007–31 January 2009 Travel clinic 100 43
55 Enterobacteriaceae 100% (24/24) E.coli Stool Unknown 14
23 6 months
Kennedy [18] Australia January 2008–April 2009 Hospital staff and contacts 102 45
62 E.coli Rectal or perianal swab Within 2 weeks before and after 21
Unknown 6 months
Östholm-Balkhed [19] Sweden September 2008–April 2009 Vaccination clinic 231 54
59 Enterobacteriaceae
90% (104/116) E.colib
Stool sample 15 (1–114) days/
3 (0–191) days
Unknown None
Kantele [20] Finland March 2009–February 2010 Travel clinic 430 40
61 Enterobacteriaceae
97% (94/97) E. colib
Stool sample Before and first (or second) stool after 19
83 None
Weisenberg [21] United States July 2009–February 2010 Travel clinic 28 66
68 Enterobacteriaceae
100% (7/7) E. colib
Stool sample 1 week before/
1 week after
Unknown None
Angelin [22] Sweden April 2010–January 2014 Healthcare students 99 25
78 Enterobacteriaceae
100% (36/36) E. colic
Stool sample Close to departure/
1 to 2 weeks after returning
Unknown None
von Wintersdorff [23] The Netherlands November 2010–August 2012 Travel clinic 122 43
58 Not done Stool sample Before and immediately after 21
Unknown None
Paltansing [24] The Netherlands March 2011–September 2011 Travel clinic 370 33
63 Enterobacteriaceae
92% (146/158) E. colic
Rectal swab Immediately before and after 21
None 6 months
Ruppé [25] France February 2012–April 2013 Vaccination centres 574 36
(SD 13)
61 Enterobacteriaceae
93% (491/526) E. colib
Stool sample Within 1 week before and after 20
None 12 months
Kuenzli [26] Switzerland December 2012–October 2013 Travel clinic 170 41
56 Enterobacteriaceae
98% (157/161) E. colib
Rectal swab 1 week before/ directly after 18
Unknown None
Lübbert [27] Germany May 2013–April 2014 Travel clinic 205 34
57 Enterobacteriaceae 92% (58/63) E. colib Stool sample Before/within 1 week after 21
22 6 months

E.coli: Escherichia coli; MRE: multidrug-resistant Enterobacteriaceae; SD: standard deviation.

a Number of travellers who provided pre- and post-travel swab.

b Data of MRE-positive isolates newly acquired during travel.

c Data of MRE-positive isolates post-travel.

d Healthcare students, median duration of stay.

Acquisition of multidrug-resistant Enterobacteriaceae

Faecal carriage of MRE varied from 1 to 12% before travel and acquisition of MRE from 21% to 51% (Table 2 [17-21,23-27].

Table 2

Risk of multidrug-resistant Enterobacteriaceae in travellers (n = 11 studies)

Study Method of MRE determination Phenotypic approaches Results genotypic characterisation post-travel MRE isolates Results molecular typing of post-travel MRE isolates MRE prevalence pre-travel
% (ratio)
MRE prevalence post-travel
% (ratio)
New MRE acquisition during travel
% (ratio)a
Persistent newly acquired MRE carriage 6 months after travel
% (ratio)
Results univariate/ multivariate risk factor
analysis for MRE acquisition
MRE in non-travelling household contacts
% (ratio)
Tängdén [17] Phenotypic approach with genotypic confirmation by PCR Enrichment broth, selective media, AST: Etest, MRE confirmation: disc diffusion TEM (n = 11), SHV (n = 3), CTX-M group 1 (n = 14) of which CTX-M-15 (n = 13), CTX-M-1 (n=1), CTX-M group 4 (n = 10) of which CTX-M-9 (n = 3), CTX-M-14 (n = 5), CTX-M-27 (n = 2)b No data 1
No data 24
Gastroenteritis; travel to Indiac No data
Kennedy [18] Phenotypic approach with genotypic confirmation by PCR Enrichment broth, selective media, AST: Vitek2, MRE confirmation: disc diffusion TEM or SHV (n = 4), CTX-M group 1 (n = 12), CTX-M group 9 (n = 6), and pAmp C genes(n =4)d No data 2
Gastroenteritis; use of antibiotics; travelling to Asia, South
America and/or Middle East/Africae,c
No data
Östholm-Balkhed [19] Phenotypic approach with genotypic confirmation by PCR Selective media, AST: Etest, MRE confirmation: Etest TEM-19 (n = 1), SHV (n = 6), CTX-M-15-like (n = 36), CTX-M-14-like (n = 36), CTX-M-27-like (n = 5), CTX-M-53-like (n = 5), CTX-M-1/61 like (n = 3), CTX-M-2 like (n = 2), CTX-M-3-like (n = 1), pAmpC genes (n = 15), no genes detected (n = 13)b No data 2
No data Age; diarrhoea or other gastrointestinal symptoms; travel to Asia, Africa (north
of equator), Indian subcontinentf
No data
Kantele [20] Phenotypic approach with genotypic confirmation by PCR Selective media, AST: Vitek2, MRE confirmation: disc diffusion 79% CTX-M-type (CTX-M-1 and CTX-M-9 most prevalent), other common strains TEM and OXA (data not published)b No data 1
No data Traveller’s diarrhoea; age; use of antibiotics for traveller’s diarrhoeaf No data
Weisenberg [21] Phenotypic approach with genotypic confirmation by PCR Selective media, AST: Vitek2, MRE confirmation: disc diffusion SHV-12 (n = 1), CTX-M-14 (n = 3), CTX-M-15 (n = 2), no gene detected (n = 1)b MLST typing
7 multidrug-resistant E. coli isolates: ST 39,
8 (n = 2), 37, 399, 437, 83
No data No data No data
Angelin [22] Phenotypic approach for detection of ESBL, pAmp C and phenotypic approach with genotypic characterisation for detection of OXA-48/OXA-181 Selective media, AST: disc diffusion, MRE confirmation: Etest (ESBL), disc diffusion (pAmpC) No data No data 7
No data Travel to the South-East Asia region
(India, Nepal, Vietnam, Indonesia, Sri Lanka); antibiotic treatment during travelg
No data
von Wintersdorff [23] Metagenomic approach
(detection blaCTX-M)
No data bla CTX-M (n = 41)d No data 9
No data Travel to Indian subcontinentf No data
Paltansing [24] Phenotypic approach with genotypic characterisation by microarray Enrichment broth, selective media, AST: Vitek2, MRE confirmation: disc diffusion SHV (n = 1), CTX-M group 1 (n = 110) of which CTX-M-1-like (n = 4), CTX-M-3-like (n = 1), CTX-M-15-like (n = 85),CTX-M-32-like (n = 20), CTX-M-group 9 (n = 42), CTX-M-group 2 (n = 2), CTX-M-group 8/25 (n = 1), pAmpC genes (n = 3)d MLST typing: 146 multidrug-resistant E. coli isolates: most prevalent ST 38 (n = 17), ST10 (n = 10), ST131 (n = 9) 9
36 (133/370) 33
Travel to South or East Asiaf 18
Ruppé [25]h Phenotypic approach with genotypic confirmation by PCR Enrichment broth, selective media, AST: disc diffusion Predominant CTX-M-type (95.4%) among which CTX-M-group 1 predominated (83.7% of all CTX-M), OXA-181 (n = 2), NDM-1 (n = 1)b No data 12
No data 51
After 1 month
34 (83/245);
after 2 months
19 (45/236);
after 3 months
10 (24/233);
after 6 months
5 (11/230);
after 12 months
2 (5/227)
Travel to Asia or sub-Saharan Africa; beta-lactam use during travel; diarrhoea during travel; type of travelf No data
Kuenzli [26] Phenotypic approach with genotypic screening by microarray and confirmation by PCR/DNA sequence analysis Enrichment broth, selective media, AST: Vitek2, MIC for meropenem and ertapenem: Etest, MRE confirmation: disc diffusion, modified Hodge test TEM-1-like (n = 33), SHV238S/240K (n = 7), SHV238S (n = 1), SHV-5/12-like (n = 1), SHV-2/3-like (n = 1),CTX-M-15-like (n = 48), CTX-M group 9 (n = 1), CTX-M group 1 (n = 24), predominant ESBL gene was CTX-M-15 (80 representative E. coli isolates analysed)b, NDM-1 (n = 1) 80 representative E. coli isolates analysed by rep-PCR: not clonally related. MLST performed on 34 randomly selected E. coli isolates: only 3 pandemic strains found (ST131 n = 2; ST648 n = 1) 3
No data 70
No data Travel to India, Bhutan or Nepal;
visiting friends and relatives;
consumption of ice cream and pastry;, length of stayf
No data
Lübbert [27] Phenotypic approach with genotypic confirmation by PCR Selective media, AST: microbroth dilution method, MRE confirmation: Etest SHV-12 (n = 1), CTX-M group 1 (n = 37) of which CTX-M-15 (n = 33), CTX-M-55 (n = 4), CTX-M group 9 (n = 19) of which CTX-M-14 (n = 9), CTX-M-27 (n = 1), CTX-M-65 (n = 1)b 7
Travel to India or South-East Asia;
No data

AST: antibiotic susceptibility testing; bla: beta-lactamase; CTX-M: cefotaximase; E. coli: Escherichia coli; ESBL: extended-spectrum beta-lactamase; KPC: Klebsiella pneumoniae carbapenemase; MLST: Multilocus sequence typing; MRE: multidrug-resistant Enterobacteriaceae; NDM: New Delhi metallo-beta-lactamase; OXA: oxacillinase; pAmp C: plasmid-borne AmpC; PCR: polymerase chain reaction; PFGE: pulsed-field gel electrophoresis; rep-PCR: repetitive extragenic palindromic PCR; SHV: Sulphydryl variable; TEM: Temoniera.

a Percentage of MRE-positive post-travel samples in those travellers whose pre-travel sample was MRE-negative.

bAcquired genes detected in post-travel MRE isolates.

c Univariate statistics.

dPrevalent genes detected in post-travel MRE isolates.

e Risk factors for resistance to gentamicin, ciprofloxacin and/or third generation cephalosporins.

f Multivariable logistic regression analysis; participants ESBL-positive before travel were excluded.

gBinary regression analysis.

hCarbapenemase-positive isolates were included in the definition MRE.

In the study by Kuenzli et al. on travellers to the Indian subcontinent only, a much higher MRE acquisition rate of 69% was demonstrated [26]. The risk of acquisition of MRE varied with the geographical region (Table 3) [17-21,23-27]. Travel to southern Asia posed the highest risk (range: 29–88%), followed by other Asian countries (18–67%) and Northern Africa (range: 31–57%). Acquisition of MRE after travelling to sub-Saharan Africa (range: 0–49%) or South and Central America (range: 0–33%) was less frequent, and three studies did not observe any acquisition of MRE after travel to South or Central America (Table 3). Acquisition of MRE after travel to North America, Europe and Oceania was rare. Results of the genotypic characterisation of MRE isolated after travel are presented in Table 2, the majority of the genes belonged to the CTX-M type.

Table 3

Proportion of travellers who acquired multidrug-resistant Enterobacteriaceae, by travel destination (n = 11 studies)

Study Southern Asia
% (ratio)
Asia except southern Asia
% (ratio)
Northern Africa
% (ratio)
Sub-Saharan Africa
% (ratio)
South and Central America
% (ratio)
North America
% (ratio)

% (ratio)

% (ratio)
Tängdén [17]a,b 78
4 (1/23) 0
Kennedy [18]a,c 57
Östholm-Balkhed [19]a,b 71
57 (17/30) 21
No data
Kantele [20]b,d 46
No data
Weisenberg [21]b 29
No data No data No data
Angelin [22] 63
No data 10
No data No data
von Wintersdorff [23]c 58
No data 17
No data
Paltansing [24]b,e 72
41 (60/146) 40
No data No data No data
Ruppé [25]f 88
No data 49
No data No data 0
Kuenzli [26]b 69 No data No data No data No data No data No data No data
Lübbert [27]a,b 72
No data 24
No data

MRE: multidrug-resistant Enterobacteriaceae.

a Travellers visiting more than one region are categorised in all the visited geographical regions.

b Study reports data on MRE acquisition in travellers.

c Study reports data on MRE prevalence in travellers.

d Travellers visiting more than one region are categorised in the geographical region with the longest stay for this study.

e One traveller who visited Iran is categorised in Asia instead of Southern Asia.

f 42 travellers visited more than one country in Asia and may be represented in more than one column in the Table; 28 of them acquired MRE.

g Exact numbers unpublished.

Southern Asia: Afghanistan, Bangladesh, Bhutan, India, Iran, Maldives, Nepal, Pakistan, Sri Lanka.

Asia (without southern Asia): Armenia, Azerbaijan, Bahrain, Brunei, Cambodia, China, Cyprus, Georgia, Hong Kong, Indonesia, Iraq, Israel, Jordan, Japan, Kazakhstan, Kuwait, Kyrgyzstan, Laos, Lebanon, Mongolia, Malaysia, Myanmar, North Korea, Oman, Philippines, Qatar, Saudi Arabia, South Korea, Singapore, Palestine, Syria, Tajikistan, Thailand, Timor-Leste, Turkey, Turkmenistan, United Arab Emirates, Uzbekistan, Viet Nam, Yemen.

Northern Africa: Algeria, Egypt, Libya, Morocco, Sudan, Tunisia, Western Sahara.

Sub-Saharan Africa: Angola, Benin, Botswana, Burkina Faso, Burundi, Cameroon, Cape Verde, Central African Republic, Chad, Comoros, Congo (Brazzaville), Côte d'Ivoire, Democratic Republic of the Congo, Djibouti, Equatorial Guinea, Eritrea, Ethiopia, Gabon, Ghana, Guinea, Guinea-Bissau, Kenya, Lesotho, Liberia, Madagascar, Malawi, Mali, Mauritania, Mauritius, Mozambique, Namibia, Niger, Nigeria, Réunion, Rwanda, São Tomé and Príncipe, Senegal, Seychelles, Sierra Leone, Somalia, South Africa, Sudan, Swaziland, Tanzania, The Gambia, Togo, Uganda, Zambia, Zimbabwe.

South and Central America: Anguilla, Antigua and Barbuda, Argentina, Aruba, Bahamas, Barbados, Belize, Bolivia, Bonaire, Sint Eustatius and Saba, Brazil, British Virgin Islands, Cayman Islands, Chile, Colombia, Costa Rica, Cuba, Curaçao, Dominica, Dominican Republic, Ecuador, El Salvador, Falkland Islands, French Guiana, Grenada, Guadeloupe, Guatemala, Guyana, Haiti, Honduras, Jamaica, Martinique, Mexico, Montserrat, Nicaragua, Panama, Paraguay, Peru, Puerto Rico, Saint Kitts and Nevis, Saint Lucia, Saint Martin, Saint Vincent and the Grenadines, Saint-Barthélemy, Sint Maarten, Suriname, Trinidad and Tobago, Turks and Caicos Islands, US Virgin Islands, Uruguay, Venezuela.

North America: Bermuda, Canada, Greenland, Saint Pierre and Miquelon, United States.

Europe: Åland Islands, Albania, Andorra, Austria, Belarus, Belgium, Bosnia and Herzegovina, Bulgaria, Channel Islands, Croatia, Czech Republic, Denmark, Estonia, Faeroe Islands, Finland, the former Yugoslav Republic of Macedonia, France, Germany, Gibraltar, Greece, the Holy See, Hungary, Iceland, Ireland, Isle of Man, Italy, Latvia, Liechtenstein, Lithuania, Luxembourg, Malta, Monaco, Montenegro, Netherlands, Norway, Poland, Portugal, Moldova, Romania, Russia, San Marino, Serbia, Slovakia, Slovenia, Spain, Svalbard and Jan Mayen, Sweden, Switzerland, Ukraine, United Kingdom.

Oceania: American Samoa, Australia, Cook Islands, Fiji, French Polynesia, Guam, Kiribati, Marshall Islands, Micronesia, Nauru, New Caledonia, New Zealand, Niue, Norfolk Island, Northern Mariana Islands, Palau, Papua New Guinea, Pitcairn Islands, Samoa, Solomon Islands, Tokelau, Tonga, Tuvalu, Vanuatu, Wallis and Futuna.

Risk factors for acquisition of multidrug-resistant Enterobacteriaceae

Besides travel destinations, other risk factors for acquiring MRE were age, use of antibiotics during travel (beta-lactam use) and gastroenteritis or other gastrointestinal symptoms (Table 2). The study of Kantele et al., designed to study these risk factors as primary outcome, showed that travel diarrhoea (adjusted odds ratio (AOR) = 31.0; 95% confidence interval (CI): 2.7–358.1)) and antibiotic therapy for travel diarrhoea (AOR = 3.0; 95% CI: 1.4–6.7) proved to be the most important risk factors for acquiring MRE [20]. In the study of Kuenzli et al. in which only travellers to southern Asia were included, risk factors for MRE acquisition were length of stay, visit to family or friend and consumption of ice cream or pastry (Table 2) [26]. Angelin et al. found a significant association for travel to the South-East Asia region (OR = 30; 95% CI: 6.3–147.2), and antibiotic treatment during travel (OR = 5; 95% CI: 1.1–26.2), but found no association with travellers’ diarrhoea or patient-related healthcare work [22].

Resistance of multidrug-resistant Enterobacteriaceae to other antibiotic drugs

Resistance of post-travel MRE isolates to various antibiotics was determined in nine studies (Table 4) [17-19,21-24,26,27]. In the study by Wintersdorff et al., a PCR-based approach was used, therefore it was not possible to determine which microorganism carried the resistance genes [23]. The resistance data to other antibiotic drugs in the study by Kennedy et al. were not part of the publication, but were provided on request [18]. Antimicrobial resistance was high for ciprofloxacin, varying from 31% to 57%, and for cotrimoxazole, varying from 49% to 86% [17-19,21-24,26,27]. Aminoglycoside resistance was high for gentamicin (range: 17–50%) and tobramycin (range: 18–59%) and low for amikacin (range: 2–5%) [17-19,21-24,26,27]. Carbapenemase-producing Enterobacteriaceae were observed in four travellers who had all visited India (in the study by Ruppé et al., two OXA-181 and one New Delhi metallo-beta-lactamase 1 (NDM-1), and in the study by Kuenzli et al., one NDM-1 but this strain was not included in the resistance results) [25,26]. Resistance to nitrofurantoin, colistin and fosfomycin was only analysed in some of the studies (Table 4) [18,19,21-23,26].

Table 4

Antibiotic drug resistance of newly acquired multidrug-resistant Enterobacteriaceae in travellers (n = 11 studies)

Study Ciprofloxacin
% (ratio)
% (ratio)
% (ratio)
% (ratio)
% (ratio)
% (ratio)
% (ratio)
% (ratio)
% (ratio)
Tängdén [17]a 50b 79
45b No data 38b 0b 0b No data 8.0b
Kennedy [18]c 55
No data 50
No data 59
No data No data No data No data
Östholm-Balkhed [19]a 31
No data 3
Kantele [20] No data No data No data No data No data No data No data No data No data
Weisenberg [21]a 43
No data No data 0
No data No data No data
Angelin [22] 57
75b 30b No data No data 0
2b No data No data
von Wintersdorff [23]e 37
No data 71
No data No data No data
Paltansing [24]f 36 67 35 No data 37 0 29 0 No data
Ruppé [25] No data No data No data No data No data 0.6
No data No data No data
Kuenzli [26]a 41
No data 5
Lübbert [27]a 43
2b 22b 0b No data 0b 16b

bla: beta-lactamase; CPE: carbapenemase-producing Enterobacteriaceae; ESBL: extended-spectrum beta-lactamase.

a Resistance among acquired ESBL-positive isolates detected in post-travel samples.

b Data extracted from bar chart, exact numbers unpublished.

c Resistance among prevalent ESBL-positive isolates detected in post-travel samples.

d Percentage of susceptibility to levofloxacin.

e Prevalent resistance genes in faecal samples post-travel.

f Resistance among prevalent ESBL-positive isolates detected in pre- and post-travel samples.

g Three acquired CPE detected in post-travel samples.

Duration of multidrug-resistant Enterobacteriaceae carriage after return, risk factors for a long duration and rate of infection after travel

Five studies analysed MRE carriage six months after travel, and the persistence rate of acquired MRE after six months was 6–24% of travellers (Table 2) [17,18,24,25,27]. Ruppé et al. analysed MRE carriage one, two, three, six and twelve months after travel, showing persistence of carriage of an acquired MRE in 34, 19, 10, 5 and 2%, respectively [25]. Travellers to Asia showed longer carriage of MRE compared with other travel destinations. Carriage of multidrug-resistant E. coli had a lower risk for prolonged carriage than other multidrug-resistant species. No other risk factors were found for prolonged carriage of MRE. Eight travellers in this study reported an episode of urinary tract infection after their return, but no microbiological data were available [25]. In the study by Tängdén et al., five of 21 travellers remained carriers of MRE after six months. However, none of these participants reported clinical infections [17]. In the study of Kennedy et al., one person developed a urinary tract infection with a travel-related organism [18]. Kantele et al. performed a one-year laboratory-based follow-up and did not find any clinical samples with MRE [20].

Rate of transmission to household members

Only one study screened household contacts for MRE after return of the index traveller. Household contacts were defined as persons who shared the same household with a participant on a regular basis. Two of 11 contacts were found MRE-positive [24]. Both carried a different ESBL-producing E. coli based on multilocus sequence typing (MLST) than the associated traveller.

Limitations of the studies

The quality of the studies and the susceptibility of bias between the studies were assessed. In all but one study, participants constituted a non-random sample of the general travelling population [17-21,23-27]. However, Angelin et al. studied healthcare students working or studying abroad [22]. Studies were performed on three different continents. Travel destinations and travel behaviour may differ considerably between different nationalities and age groups. Including co-travellers, as done in all studies except Paltansing et al. and Ruppé et al., can result in similar travel behaviour and therefore, similar risk factors. Overall, the main outcome was not influenced by recall or interviewer bias. For other outcomes such as risk factors, the risk of recall bias or interviewer bias was low because of the use of self-administered questionnaires.

Every study had participants lost to follow-up for post-travel stool samples and follow-up stool samples. Asymptomatic faecal carriage of MRE is probably not related to loss to follow-up, therefore, the risk of information bias is small. Ruppé et al. calculated post-travel MRE carriage as those travellers with persisting MRE carriage divided by all travellers with MRE acquisition plus all travellers without MRE post-travel [25]. However, travellers without MRE were not included in the follow-up. As a result, local MRE acquisition was not included in the calculated post-travel MRE carriage prevalence. Therefore the true prevalence can be assumed to be higher.

In five studies, travellers visited multiple regions or even continents during their trip [17-20,27]. In these travellers, it was not possible to attribute MRE prevalence or MRE acquisition to a certain geographical region. However, travellers in these studies were included in the MRE prevalence or MRE acquisition rates of more than one geographical region, which may have introduced information bias.

Seven studies used stool samples for detection of MRE [17,19-21,23,25,27] and three studies used rectal or perianal swabs for detection of MRE [18,24,26]. This might have influenced detection of MRE carriage.


In this systematic review we found a high prevalence of faecal carriage of MRE after international travel. The highest prevalence of MRE was observed in isolates from travellers returning from southern Asia, with up to 88% acquisition of MRE. In addition to the antibiotics not effective against MRE, an alarmingly high prevalence of resistance to other commonly used antibiotics such as cotrimoxazole (49–86%), ciprofloxacin (31–57%) and aminoglycosides (gentamicin 17–71%) was observed in ESBL-positive isolates in travellers in all studies [17-27].

Returning international travellers with MRE may introduce these microorganisms in their home countries. This may cause community-onset infections with MRE in patients without obvious risk factors transmitted by healthy carriers through food or person-to-person contact [9]. Infections caused by MRE are associated with poorer outcome and a higher overall mortality rate than infections caused by susceptible bacteria [28]. In this review, all studies showed an increased prevalence of faecal carriage of ESBL after international travel. It is not possible to evaluate the proportion of travellers who will develop infection with these resistant bacteria. However, studies have demonstrated that international travel is a risk factor associated with developing an infection with an MRE [11,12,29].

Many countries have infection prevention and control guidelines to detect and treat multidrug-resistant organisms (MDROs) including MRE [30]. In countries with low prevalence of MRE, infection prevention and control guidelines mainly include strategies for early identification and isolation of patients recently hospitalised in foreign hospitals [30,31]. Patients with a recent history of travel to MRE-endemic areas but not admitted to healthcare facilities abroad are not normally considered at risk for carriage of MDROs. However, in hospitalised patients with a recent history of travel, increased rates of carriage of MRE have been observed [10,29,30]. Physicians should be aware of the risk that patients with recent travel to areas with high faecal carriage of MRE, as presented in this review, may introduce MRE to the hospital. Routine screening for MRE seems indicated in such patients. Furthermore, empiric antibiotic therapy may fail when an infection by MRE is not taken into account. Therefore, careful recording of travel history needs to be incorporated in each patient evaluation. As shown in this review, there is also an increased risk of resistance against other antibiotics in travellers with MRE carriage. It is likely that this is caused by multiple genes, each encoding resistance to different classes of antibiotics, which are often found on the same bacterial mobile genetic element (e.g. a plasmid) [32]. As a result, other antibiotics, such as aminoglycosides, will also fail in many MRE-positive patients.

Of all MDROs, emergence of CPE is most worrisome because of the limited treatment options for these infections. NDM-1-producing Enterobacteriaceae have been found in environmental samples in endemic regions [33]. CPE (NDM-1) in patients from the United Kingdom with a recent history of travelling or medical tourism to India are already an important public health problem [8]. Case reports have also demonstrated acquisition of CPE in travellers without contact with medical healthcare facilities [34,35]. In this review, four travellers from India were carrying a carbapenemase-producing E. coli [25,26]. Preliminary results of the Carriage Of Multiresistant Bacteria After Travel (COMBAT) study, a large-scale multicentre longitudinal cohort study conducted in the Netherlands among 2001 travellers, show acquisition of CPE in four travellers [36].

There are, besides the destination of travel, additional risk factors for acquiring MRE during travel. Antibiotic therapy was found to increase the risk [20,22]. In five studies, traveller’s diarrhoea or gastroenteritis were associated with an increased risk of MRE acquisition during travel [17-20,25]. Also, in one study, meticulous hand hygiene or strict consumption of bottled water did not lower the risk of acquiring MRE [22]. Therefore, it is not clear whether hygiene-related travel advice will decrease faecal carriage of MRE. Surprisingly, healthcare-related activities did not pose an increased risk of acquiring MRE in one study [22].

MRE and CPE could also be carried by food. International spread of these bacteria by food supply has been reported [37]. In this review, only one study showed that food consumption (ice cream and pastry) was associated with MRE carriage in travellers to southern Asia, whereas most of the studies did not focus on dietary patterns during travel.

One limitation of this review is the recruitment of travellers from travel clinics only, resulting in inclusion of very few travellers with European destinations. Some European countries such as Greece and Cyprus are also endemic for MRE and popular travel destinations [34]. In addition, travellers visiting their country of origin, especially Morocco and Turkey usually do not ask for a pre-travel consultation, although these countries are endemic for MRE and CPE [34]. It is not clear whether not including these patients may have led to an under- or overestimation of MRE acquisition.

Another limitation is the lack of sufficient data regarding the duration of carriage and the transmission among non-travelling household members. The study by Ruppé et al. suggests that three months after return, MRE carriage is comparable with the baseline prevalence before travelling. However, the study did not include baseline prevalence in the follow-up. The COMBAT study will address some of these questions [38].


International travel is a major risk factor for acquisition of MRE. This risk is particularly high after travelling to (southern) Asia and in persons with travel-related diarrhoea and antibiotic use. Carriage of MRE-positive isolates is also associated with a high risk of resistance to ciprofloxacin, cotrimoxazole and aminoglycosides. Further research is needed to assess duration of carriage, spread to household contacts and whether introduction of MRE results in an increase of MRE infections. Our results, combined with the worldwide emergence of CPE, further stress the importance of infection prevention and control guidelines.


We thank Wichor M. Bramer of Erasmus MC Medical Library for performing the literature search. We thank Karina Kennedy, Scott Weisenberg, Anita Hällgren, Christian von Wintersdorff, Anu Kantele, Esther Kuenzli, Thomas Tängdén and Christoph Lübbert for providing additional data concerning their studies.

Conflict of interest

None declared.

Authors’ contributions

Robert-Jan Hassing: This author made substantial contributions to conception and design, acquisition of data and analysis and interpretation of data; this author participated in drafting the article; this authors gave final approval of the version to be submitted and any revised version. Jelmer Alsma: This author made substantial contributions to conception and design, acquisition of data and analysis and interpretation of data; this author participated in drafting the article; this authors gave final approval of the version to be submitted and any revised version. Maris S. Arcilla: This author made substantial contributions to acquisition of data and analysis and interpretation of data; this author participated in drafting the article; this author gave final approval of the version to be submitted and any revised version. Bruno H. Stricker: This author made substantial contributions to conception and design and analysis and interpretation of data; this author participated in revising the article critically for important intellectual content; this authors gave final approval of the version to be submitted and any revised version. Perry J. van Genderen: This author made substantial contributions to conception and design; this author participated in revising the article critically for important intellectual content; this authors gave final approval of the version to be submitted and any revised version. Annelies Verbon: This author made substantial contributions to conception and design and analysis and interpretation of data; this author participated in revising the article critically for important intellectual content; this authors gave final approval of the version to be submitted and any revised version.


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