Elsevier

Journal of Infection

Volume 73, Issue 4, October 2016, Pages 305-313
Journal of Infection

Review
Enterococcus faecalis urinary-tract infections: Do they have a zoonotic origin?

https://doi.org/10.1016/j.jinf.2016.07.012Get rights and content

Summary

Major human pathogens are frequently isolated from meat-producing animals, particularly poultry. Among them is Enterococcus faecalis, which is known to be one of the main cause of human urinary-tract infections worldwide. Early in 2015, we detected several, consecutive abnormal increases in the weekly number of human E. faecalis infections in various medical settings in the Provence-Alpes-Côte d'Azur region of France, especially including community-acquired urinary-tract infections. Speculating that this region-wide epidemiological event may have originated from animal-based food, we initiated this work to provide an overview of the epidemiology of E. faecalis, with a particular focus on the possible link between E. faecalis clones isolated from food-producing animals and those responsible for human urinary-tract infections. At that time, only one study had clearly identified strong epidemiological links between E. faecalis clones isolated from food-producing animals and human E. faecalis urinary-tract infections. This observation, coupled with our region-wide epidemiological experience, leads us to strongly believe that E. faecalis is a real zoonotic pathogen with potentially highly significant impact on human health. This is of particular concern because of its ability to acquire antibiotic-resistance genes and to infect animals and humans. Various strategies must be urgently implemented to address this public health threat, in particular through the development and implementation of large integrated automated surveillance systems based on animal and human health data to enable us to detect E. faecalis epidemiological events.

Introduction

The global burden of human bacterial infections originating from food-producing animals is increasingly a subject of debate around the world. Recent reviews investigating the possibility of industrial poultry meat production being a zoonotic reservoir for common human bacterial pathogens have confirmed the zoonotic origin of some significant human bacterial pathogens such as Salmonella spp.,1 Campylobacter spp.2 and Escherichia coli.3 They also point to a possible zoonotic origin for other major human bacterial infections involving Staphylococcus aureus, Enteroccus faecalis and Enteroccus faecium.4 These studies also underline the fact that poultry meat production settings may be important sources of antibiotic-resistance genes selected by the use of antibiotics, carried from poultry to humans by zoonotic bacterial clones and possibly transferred to other bacteria present in the consumer's gut microbiota through horizontal gene transfer.1, 2, 4

Urinary-tract infections (UTIs) are one of the most common human bacterial infections. They are responsible for significant levels of morbidity and loss of productivity worldwide, with 150 million human cases per year.5 The annual cost to society has been estimated societal cost evaluated to range from $1 billion to more than $3.5 billion in the USA alone.5, 6 These infections are particularly frequent in women. It has been estimated that one-third of all the worldwide women under 26 years old will experience a treatment-requiring UTI and that almost 50% of them will experience at least one episode of UTI during their lifetime.7 Finally, UTIs can result in life-threatening infections for patients as they can lead to bacteremia, and ultimately to death.

Most UTIs (80%–90%) are due to extraintestinal E. coli strains,8, 9 usually identified to be the patients dominant fecal E. coli isolate.10 Further studies analyzing the clonal relationships between E. coli strains isolated from animals, food and UTI patients have identified close relationships between the various E. coli isolates, strongly suggesting that the E. coli human UTI strains possibly originate from a zoonotic source, particularly chickens.3, 5, 11, 12, 13 Nevertheless, other bacterial species are also known to cause human UTIs, including E. faecalis.14, 15 E. faecalis UTIs are of particular concern, as they are associated with intrinsic resistance to first-line antimicrobial agents16 and with acquired resistance, especially to gentamycin15 and vancomycin.17

Section snippets

Source of the question

Between February and March 2015, our Microsoft Excel-based automated weekly surveillance systems known as BALYSES18 and PACASurvE (surveillance system monitoring clinical microbiological data from seven hospital microbiology laboratories and 151 private microbiology laboratories grouped into five laboratory groups in the Provence-Alpes-Côte d'Azur region of France) (Fig. 1) triggered six consecutive alarms involving human E. faecalis infections (Fig. 2). These alarms were emitted for the four

Is there a seasonality in the E. faecalis infections?

Little is currently known about the possible seasonality of E. faecalis human infections. A German study,19 aimed at investigating the Enterococcal colonization of infants in a neonatal intensive care unit between 1 March 2003 and 28 February 2004, attempted to see whether E. faecalis infections followed seasonal cycles. Although they observed that Enterococci infections were statistically more frequent in winter/spring than in summer/fall, no clear seasonal pattern was identified for E.

Are food-producing animals natural reservoir of E. faecalis? (Table 2)

Enterococci are gut commensals in several food-producing animal species, particularly broiler chickens. It is now well established that the prevalence of E. faecalis is particularly high in poultry farms and may reach more than 94% of tested meat samples in studies using selective enrichments,22 with an average calculated prevalence of 57%.4 Associated antimicrobial resistance mainly concerns gentamicin, while glycopeptides or ampicillin are rarely affected.23 Poultry strains inconsistently

Is there a link between human E. faecalis UTIs and food-producing animals?

Enterococci of animal origin are known to be human pathogens, particularly E. faecium.16 However, knowledge of the human pathogenicity of E. faecalis strains of animal origin is limited. Globally, several studies have shown that some E. faecalis clones can be isolated both in humans and animals, particularly ST16.72, 73 Moreover, in Portugal, ST6 E. faecalis was also recovered from the blood and urine samples of hospitalized patients, swine liquid manure and hospital sewage.30 All cases of E.

Conclusions and future research

E. faecalis has been extensively isolated from various animals' species and animal-based foods (Table 2, Table 3). However, only one study has clearly identified an epidemiological link between an E. faecalis clone responsible for human UTIs and E. faecalis isolates found in poultry.72 This is of significant concern, particularly as our surveillance systems have detected a possible region-wide community-acquired outbreak of E. faecalis human UTIs in the PACA region of France. Taken together,

Conflict of interest and financial disclosure

No potential conflict of interest or financial disclosure issues for any of the authors.

Funding statement

This work was supported by the Centre National de la Recherche Scientifique and the IHU Méditerranée Infection.

Acknowledgments

We thank Trad Online for English correction of this article.

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