Acquisition of multidrug-resistant Enterobacterales during international travel: a systematic review of clinical and microbiological characteristics and meta-analyses of risk factors

Abstract

Background: International tourism increased from 25 million tourist arrivals in 1950 to over 1.3 billion in 2017. These travelers can be exposed to (multi) resistant microorganisms, may become colonized, and bring them back home. This systematic review aims to identify the carriage rates of multidrug-resistant Enterobacterales (MDR-E) among returning travelers, to identify microbiological methods used, and to identify the leading risk factors for acquiring MDR-E during international travel. Methods: Articles related to our research question were identified through a literature search in multiple databases (until June 18, 2019)-Embase, Medline Ovid, Cochrane, Scopus, Cinahl, Web of Science, and Google Scholar. Results: Out of 3211 potentially relevant articles, we included 22 studies in the systematic review, and 12 studies in 7 random-effects meta-analyses. Highest carriage rates of MDR-E were observed after travel to Southern Asia (median 71%), followed by travel to Northern Africa (median 42%). Carbapenemase-producing Enterobacterales (CPE) were identified in 5 out of 22 studies, from a few patients. However, in only eight out of 22 studies (36.4%) the initial laboratory method targeted detection of the presence of CPE in the original samples. The risk factor with the highest pooled odds ratio (OR) for MDR-E was travel to Southern Asia (pooled OR = 14.16, 95% confidence interval [CI] = 5.50 to 36.45), followed by antibiotic use during travel (pooled OR = 2.78, 95% CI = 1.76 to 4.39). Conclusions: Risk of acquiring MDR-E while travelling increases depending on travel destination and if antibiotics are used during travel. This information is useful for the development of guidelines for healthcare facilities with low MDR-E prevalence rates to prevent admission of carriers without appropriate measures. The impact of such guidelines should be assessed.

The hygiene hypothesis, the COVID pandemic, and consequences for the human microbiome

“…Travel restrictions imposed to prevent COVID transmission might be a missed opportunity, and lost diversity may not be easily recoverable (66). Nonetheless, long-distance travelers also risk acquiring antimicrobial drug-resistant bacteria in their journeys, and migrants from certain settings have experienced rapid declines in microbial diversity (67,68). How different kinds of movement affect the microbiomes of different social groups and populations merits additional attention.…”

Antimicrobial Resistance and Human Mobility

“…A recent meta-analysis investigating acquisition of multidrug-resistant Enterobacterales during international travel demonstrated that travel to Southern Asia and antibiotic use during travel appear to be risk factors for acquisition while traveling. 20 Of note, CRE acquisition during travel was relatively rare among pooled studies, however the authors highlight that this may be due to underreporting as most included studies did not use culture methods that specifically target CRE. In addition, consumption of high-risk food such as raw food, milk from open containers, and tap water, which is traditionally associated with traveler's diarrhea and subsequent acquisition of MRE, was not found to be a statistically significant risk factor for travelers and MRE, though recall bias may have affected these results.…”

“…More research is needed to better understand the risk of transmission from recently returned travelers to others in the hospital setting as well as whether carriage among travelers warrants isolation and precaution guidelines for health-care settings. 20 Disruptions in international travel due to COVID-19 may be hypothesized to reduce the total number of MDRO acquisition through this route. However, a countervailing factor in AMR control may be in the general rise in broadspectrum antibiotic use related to COVID-19.…”

Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain

“…Controlling and managing access of humans into and within production and processing facilities is an important facet of biosecurity. Restrictions/quarantine periods may be applied for people who have visited other farms, have travelled abroad recently or have recently suffered from infectious diseases (Voor In ‘t Holt et al., 2020). Control of staff and contractors’ visits through signing‐in procedures, visitor posters, booklets and certificates can raise awareness amongst visitors about the importance of biosecurity.…”