Colonisation with multi-resistant Enterobacteriaceae in hospitalised Danish patients with a history of recent travel: A cross-sectional study

doi:10.1016/j.tmaid.2013.06.004

Travel Medicine and Infectious Disease

Volume 11, Issue 5, September–October 2013, Pages 320-323

https://doi.org/10.1016/j.tmaid.2013.06.004 Get rights and content

Summary

Background

The global spread of multi-resistant Enterobacteriaceae is a new challenge in health care. Travelling in high endemic areas has been associated with colonisation.

This study was performed among patients hospitalised for any reason, with recent travel abroad to identify the rate for colonisation with multi-resistant bacteria.

Methods

In a 3-month period (2011) all patients admitted to a the Department of Infectious Diseases, Aarhus University Hospital, Denmark with a travel history within the last three months were screened for multi-drug resistant bacteria by a rectal swab.

Results

A total of 88 adult patients were included. None were carriers of carbapenemase-producing bacilli. 12.5% were colonised with extended spectrum beta-lactamase producing Escherichia coli (ESBL-EC). Diarrhoea during travel was significantly associated with colonisation.

More than 80% of the ESBL-EC colonised patients had been abroad longer than two weeks (P < 0.05). Less than 40% of patients with ESBL-EC had self-limiting diarrhoea at the time of admission.

Conclusions

A significant proportion of patients with a recent travel history was colonised with ESBL-EC at hospitalisation (12.5%). Less than half of the travellers with ESBL-EC had gastrointestinal symptoms. Diarrhoea during travel and travelling time > two weeks were associated with colonisation with ESBL-EC.

Section snippets

Background

A fast global spread of multi-resistant Enterobacteriaceae has been seen within the last decade. Especially the global spread of carbapenemase-producing gram negative bacteria presents a serious threat to health care systems around the world [1], [2], [3], [4]. The multi-drug resistant bacteria have been reported as a gut colonist suggesting possible transmission by faecal-oral route, hence complicating prevention of the transmission.

Early identification of infected patients and carriers may

Methods

From 6 July to 6 October 2011 all patients admitted to the Department of Infectious Diseases and Internal Medicine, Aarhus University Hospital, Denmark were systematically asked to inform about their travel history; this was independent of the reason for hospitalisation. To be included in the study patients should have travelled outside Denmark within the previous three months. Included patients were questioned about travel destination, length of travel, and illness during travel including

Results

During the study period, 425 patients were hospitalised and 88 patients (38 men and 50 women) had a history of travel within the previous three months and were thus included. Median age was 37 years (range 15–74).

Descriptive data on the 88 travellers according to ESBL-EC carrier status are presented in Table 1 and travel destinations are described in Table 2.

None of the travellers carried carbapenem-resistant Gram-negative Bacilli including the New Delhi Metallo-beta-lactamase (NDM-1).

Eleven of

Discussion

There is an increasing concern for environmental dissemination of multi-drug resistant bacteria. A number of reports have shown multi-drug resistant bacteria colonising the gut of returning travellers [5], [7], [9].

This study analysed the rate of colonisation by multi-resistant Enterobacteriaceae in patients with a recent travel history admitted to our hospital.

In this study of hospitalized returned travellers in Denmark we did not find any patients colonised with carbapenem-resistant

Conclusion

In this study we found 12.5% out of 88 hospitalised patients with a history of recent travel to be colonialised with ESBL-EC. None were colonised with carbapenem-resistant Gram-negative Bacilli. Similar to other studies we found that colonisation was associated with diarrhoea during travelling abroad and a duration of travel of more than two weeks.

Funding

No financial support or grant was received for this study.

Conflict of interest

The authors state that they have no conflicts of interest.

References (13)

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Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study
Lancet Infectious Diseases
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M. Shahid
Environmental dissemination of NDM-1: time to act sensibly
Lancet Infectious Diseases
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S.C. Arya et al.
International travel with acquisition of multi-drug resistant gram negative bacteria containing the New Delhi metallo-beta-lactamase gene, Bla(NDM-1)
Travel Medicine and Infectious Disease
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K.B. Laupland et al.
Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel
Journal of Infection
(2008)
A.M. Hammerum et al.
Faecal carriage of extended-spectrum beta-lactamase-producing and AmpC beta-lactamase-producing bacteria among Danish army recruits
Clinical Microbiology and Infection
(2011)
P.M. Hawkey
Prevalence and clonality of extended-spectrum beta-lactamases in Asia
Clinical Microbiology and Infection
(2008 Jan)

There are more references available in the full text version of this article.

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Although most travellers who become colonised remain asymptomatic [123], travellers may spread the bacteria within the community and facilitate further dissemination of MDR bacteria on their return [130]. TD has been identified as a significant risk factor for colonisation with MDR bacteria such as ESBL-PE in several studies [125,127,128,132,135–138]. The occurrence of diarrhoea or gastrointestinal disorders during travel may increase the risk of acquiring MDR Enterobactericeae by a factor of 2–3 [135].
Travellers’ diarrhoea (TD) is the most frequent illness experienced by international travellers to lower-income countries with bacterial agents considered to account for 80–90% of cases. In this review, we summarise evidence published on bacterial TD over the past 10 years, focusing on the epidemiology and aetiology of TD. Diarrhoeagenic Escherichia coli (DEC) continue to be the most commonly implicated bacteria in TD, although Enteropathogenic E. coli (EPEC) and Enteroaggregative E. coli (EAEC) now appear to be predominant where Enterotoxigenic E. coli (ETEC) was previously considered most prevalent globally. Where fluroquinolone resistance had primarily been documented for Campylobacter in Southeast Asia, widespread resistance has been observed in most regions of the world for multiple enteropathogens, including Shigella, Salmonella, ETEC and EAEC. Implementation of novel molecular methods for pathogen detection has led to identification of bacterial pathogens, including Clostridium difficile (with and without the use of prior antibiotics), Arcobacter species and Bacteroides fragilis, as aetiological agents in TD. The widespread resistance to first-line antibiotics in multiple bacterial enteropathogens warrants continued surveillance and re-evaluation of current treatment practices. Further investigations are required to determine the prevalence and geographical distribution of bacterial enteropathogens that have been more recently implicated in TD.
Screening for antimicrobial-resistant Gram-negative bacteria in hospitalised patients, and risk of progression from colonisation to infection: Systematic review
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Screening in high risk setting (n = 53 studies, 63.9%)14, 16, 20, 22, 25, 26, 28, 30, 32–36, 38–41, 43, 45, 47, 50, 52–60, 64, 65, 67, 69–72, 75–77, 80, 81, 83, 90, 91, 100–104 was performed largely in ICU or ICU and other wards (n = 40; 75.5%)14, 16, 20, 26, 30, 32–34, 38–41, 43, 45, 47, 50, 52–56, 59, 60, 64, 69–71, 73, 75–77, 80, 81, 100–104; the remaining studies were conducted in haematology (n = 6),22, 35, 65, 83, 90, 91 transplant units (n = 5)25, 28, 36, 58, 67 and rehabilitation wards (n = 2).57, 72 One study27 has not been categorised neither as high-risk nor low-intermediate risk ward. Combining target patient groups and setting type, we identified six screening approaches: all admitted patients (AA) to hospital (8 studies, 9.6%),19, 44, 63, 74, 78, 82, 98, 99 AA patients to high risk ward/s (41, 49.4%),14, 16, 20, 25, 26, 28, 32–34, 36, 38–40, 43, 45, 47, 52, 53, 55, 57–60, 64, 67, 69–73, 75–77, 80, 81, 90, 100–104 AA patients to low/intermediate risk wards (LIRW) (10, 12.0%),13, 17, 21, 23, 24, 46, 51, 62, 86, 105 high-risk (HR) patients admitted to hospital (9, 10.8%),18, 48, 49, 61, 66, 79, 81, 82, 85 HR patients admitted to high risk ward/s (12, 14.4%),22, 30, 33, 35, 41, 50, 54, 56, 65, 83, 91 HR patients admitted to low/intermediate risk wards (LIRW) (2; 2.4%).62, 68
Transmission of antimicrobial-resistant Gram-negative bacteria (AMR-GNB) amongst hospitalised patients can lead to new cases of carriage, infection and outbreaks, hence the need for early carrier identification. We aim to explore two key elements that may guide control policies for colonisation/infection in hospital settings: screening practices on admission to hospital wards and risk of developing infection from colonisation.
We searched on PubMed, Scopus and Cochrane databases for studies published from 2010 up to 2021 reporting on adult patients hospitalised in high-income countries.
The search retrieved 11,853 articles. After screening, 100 studies were included. Combining target patient groups and setting type, we identified six screening approaches. The most reported approach was all admitted patients to high-risk (HR) wards (49.4%). The overall prevalence of AMR-GNB was 13.8% (95%CI 9.3–19.0) with significant differences across regions and time. Risk of progression to infection amongst colonised patients was 11.0% (95%CI 8.0–14.3) and varied according to setting and pathogens’ group (p value<0.0001), with higher values reported for Klebsiella species (18.1%; 95%CI 8.9–29.3).
While providing a comprehensive overview of the screening approaches, our study underlines the considerable burden of AMR-GNB colonisation and risk of progression to infection in hospitals by pathogen, setting and time.
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Nosocomial infections (NIs) are a critical issue affecting the quality of healthcare. In this study, we performed a retrospective study to explore the incidence rates, mortality rates, and microbial spectrum of NIs in Beijing Chest Hospital, a tuberculosis (TB) specialized hospital in China. Our data demonstrate that the overall incidence rate of inpatients with NIs slightly decreased from 2012 to 2016, which may be associated with the implementation of hand hygiene measures, while the mortality rates associated with NI did not significantly change. In addition, the species distribution of NIs was quite different from that presented in previous reports, and Klebsiella pneumoniae was the most frequently isolated microorganism.
Colonization with extended-spectrum beta-lactamase-producing and carbapenemase-producing Enterobacteriaceae in international travelers returning to Germany
2015, International Journal of Medical Microbiology
Citation Excerpt :
Thus, the options for empirical antibiotic therapy in cases of clinical infections are limited (Woerther et al., 2013). Several authors from Scandinavia associated gastroenteritis during travel with the risk for ESBL-PE acquisition (Lausch et al., 2013; Östholm-Balkhed et al., 2013; Tängdén et al., 2010). This association was confirmed by the results of our study (p = 0.011).
Two hundred and twenty-five healthy German volunteers traveling to 53 different countries (mostly in Asia, Africa and South America) were enrolled in a prospective cohort study. Stool samples and data on potential travel-associated risk factors (such as type of travel, nutritional habits, occurrence of gastroenteritis) were collected before and after traveling. Screening for extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-PE) and carbapenemase-producing Enterobacteriaceae (CPE) was performed using selective media (CHROMagar™ ESBL/CPE plates). Isolates with confirmed ESBL-phenotype were examined for the presence of blaCTX-M, blaTEM, blaSHV, and blaVIM, blaIMP, blaNDM, blaKPC, blaOXA-48 genes by PCR amplification and sequencing. Antimicrobial susceptibility testing was performed using conventional microbroth dilution. Pre-travel analysis of 205 fully evaluable participants revealed an ESBL-PE prevalence rate of 6.8% (14/205). Among 191 participants that were ESBL-negative before travel, 58 (30.4%) were colonized by ESBL-producing Escherichia coli, and 5 (8.6%) additionally carried ESBL-producing Klebsiella pneumoniae upon return. However, no carbapenem-resistant Enterobacteriaceae were detected. ESBL-genotyping revealed that 52/54 (96.6%) E. coli and 4/4 (100%) K. pneumoniae strains available for sequencing produced CTX-M enzymes, mostly CTX-M-15 (33/56, 58.9%), and 2/54 (3.7%) E. coli strains produced SHV-12 enzymes. Travel to India was associated with the highest ESBL-PE acquisition rate (11/15, 73.3%; p = 0.015), followed by South East Asia (22/46, 47.8%; p = 0.038). Evaluation of travel-associated risk factors demonstrated significance for the occurrence of gastroenteritis (p = 0.011). Strictly practiced hand hygiene and exclusive consumption of packaged beverages showed no protective effect. The ESBL-PE persistence rate after 6 months was 8.6% (3/35). We conclude that global efforts are needed to address the further spread of ESBL-PE in the community. Active surveillance and contact isolation precautions may be recommended at admission to medical facilities especially for patients who traveled to India and South East Asia in the previous 6 months.
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2015, Asian Pacific Journal of Tropical Biomedicine
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Citation Excerpt :
In Swedish studies pre-travel colonization rates was 2.4% in 2013 [9] and 7.1% in 2015 [10], and a Finnish study found a colonization rate of 1.2% in 2015 [11]. A Danish hospital-based study found an equal rate of 12.5% colonization among hospitalized patients and showed a tendency to more extensive travel activity among the colonized cases [8]. The post-travel incidence in this study was slightly higher than previous studies from 2014 to 2017 that found ESBL-E colonization rates after travel to India ranging from 62.5 to 90.6% [5,6,10,21–23].
Travelers to India are often colonized with extended-spectrum beta-lactamase producing Enterobacteriaceae (ESBL-E) or Carbapenemase-producing Enterobacteriaceae (CPE). The aim of this study was to investigate if the probiotic species Lactobacillus Rhamnosus GG (LGG) could prevent the colonization of the gut with multi-drug resistant bacteria.
Adult Danish travelers traveling to India for 10–28 days were randomized to receive either LGG or no probiotics during travel. Rectal swabs and questionnaires were obtained before travel, immediately after and six months after return. Swaps were screened for the presence of ESBL-E and CPE.
31 travelers were randomized to the LGG group and 30 to the control group. Before traveling, 6/50 (12.0%) were colonized with ESBL-E. After return, 41/44 (93.2%) of those not colonized before travel were colonized and 11/36 (30.6%) were still colonized after six months. There was no statistically significant difference in the colonization rate between the group receiving LGG and the control group. No CPE was detected in any cases.
The study confirms the very high incidence of colonization with ESBL-E associated with travel to India with >90% colonized upon return and one third were intestinal carriers for at least six months. Use of LGG did not have any effect on the risk of colonization with ESBL-E.

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^☆: This paper was presented at the 4th Northern European Conference on Travel Medicine, June 6–8, 2012, Dublin as an oral presentation.

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Travel Medicine and Infectious Disease

Summary

Background

Methods

Results

Conclusions

Section snippets

Background

Methods

Results

Discussion

Conclusion

Funding

Conflict of interest

References (13)

Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study

Lancet Infectious Diseases

Environmental dissemination of NDM-1: time to act sensibly

Lancet Infectious Diseases

International travel with acquisition of multi-drug resistant gram negative bacteria containing the New Delhi metallo-beta-lactamase gene, Bla(NDM-1)

Travel Medicine and Infectious Disease

Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel

Journal of Infection

Faecal carriage of extended-spectrum beta-lactamase-producing and AmpC beta-lactamase-producing bacteria among Danish army recruits

Clinical Microbiology and Infection

Prevalence and clonality of extended-spectrum beta-lactamases in Asia

Clinical Microbiology and Infection

Cited by (32)

Bacterial travellers’ diarrhoea: A narrative review of literature published over the past 10 years

Screening for antimicrobial-resistant Gram-negative bacteria in hospitalised patients, and risk of progression from colonisation to infection: Systematic review

Nosocomial Infection Surveillance in a Tuberculosis Specialized Hospital in China

Colonization with extended-spectrum beta-lactamase-producing and carbapenemase-producing Enterobacteriaceae in international travelers returning to Germany

Nosocomial infections and their control strategies

Do probiotics prevent colonization with multi-resistant Enterobacteriaceae during travel? A randomized controlled trial

Colonisation with multi-resistant Enterobacteriaceae in hospitalised Danish patients with a history of recent travel: A cross-sectional study☆

Summary

Background

Methods

Results

Conclusions

Section snippets

Background

Methods

Results

Discussion

Conclusion

Funding

Conflict of interest

Lancet Infectious Diseases

Lancet Infectious Diseases

Travel Medicine and Infectious Disease

Journal of Infection

Clinical Microbiology and Infection

Clinical Microbiology and Infection