Enterococci: Between Emerging Pathogens and Potential Probiotics

Ben Braïek, Olfa; Smaoui, Slim

doi:https://doi.org/10.1155/2019/5938210

BioMed Research International

On this page

Abstract Introduction Conclusion Conflicts of Interest References Copyright Related Articles

Special Issue

Controversial Aspects Displayed by Enterococci: Probiotics or Pathogens?

View this Special Issue

Review Article | Open Access

Volume 2019 | Article ID 5938210 | https://doi.org/10.1155/2019/5938210

Enterococci: Between Emerging Pathogens and Potential Probiotics

Olfa Ben Braïek¹and Slim Smaoui²

Guest Editor: Chrissanthy Papadopoulou

Received25 Jan 2019

Revised06 Apr 2019

Accepted14 May 2019

Published23 May 2019

Abstract

Enterococci are ubiquitous microorganisms that could be found everywhere; in water, plant, soil, foods, and gastrointestinal tract of humans and animals. They were previously used as starters in food fermentation due to their biotechnological traits (enzymatic and proteolytic activities) or protective cultures in food biopreservation due to their produced antimicrobial bacteriocins called enterocins or as probiotics, live cells with different beneficial characteristics such as stimulation of immunity, anti-inflammatory activity, hypocholesterolemic effect, and prevention/treatment of some diseases. However, in the last years, the use of enterococci in foods or as probiotics caused an important debate because of their opportunistic pathogenicity implicated in several nosocomial infections due to virulence factors and antibiotic resistance, particularly the emergence of vancomycin-resistant enterococci. These virulence traits of some enterococci are associated with genetic transfer mechanisms. Therefore, the development of new enterococcal probiotics needs a strict assessment with regard to safety aspects for selecting the truly harmless enterococcal strains for safe applications. This review tries to give some data of the different points of view about this question.

1. Introduction

In recent years, probiotics are being consumed increasingly. Several studies have shown that probiotics, viable microorganisms, are known for their beneficial health effects in human and animal such as immune system strengthening, metabolic disorder reduction, and feed digestibility improvement [1].

In order to screen and select microbial strains with probiotic abilities, the Food and Agriculture Organisation (FAO) and World Health Organisation (WHO) have established some basic criteria, such as the examination of tolerance to the orogastrointestinal transit, production of antimicrobial substances and antibiotic susceptibility, adherence to human intestinal mucosa, and desired immunomodulation activity [1]. Previously, only lactic acid bacteria (LAB) isolated from human gastrointestinal tract were recommended by FAO and WHO for human use [2]. However, many research studies showed that some strains isolated from animals, fermented or nonfermented food products, could be potential candidates to be used as promising probiotics for humans and animals [2]. Among several microorganisms, LAB are popular as probiotic candidates due to their being generally recognised as safe status (GRAS). Bacteria belonging to the genera Bifidobacterium and Lactobacillus are more commonly used in the fermented food production. Nevertheless, probiotic potential of several other genera of LAB, such as Aerococcus, Carnobacterium, and Enterococcus, were also explored, due to their technological advantage in the food industry and their health-promoting properties [3]. Enterococcus, one of the main genera belonging to the LAB group with nearly 50 species, could include strains that are known to be opportunistic microorganisms causing several diseases in humans [4].

In addition, many recent studies have demonstrated an alarming increase in multidrug resistant enterococci, particularly vancomycin-resistant strains and their ability to acquire and transfer antibioresistance genes and virulence factors [5]. Hence, based on these findings, the use of enterococci as probiotics generates serious concern leading to the need of deep research studies to better understand the pathogenicity of these versatile microorganisms and elaborate urgent and accurate measures to distinguish safe strains and select them as efficient probiotics.

The main aims of this review are to summarise the pros and cons of enterococci in view of their future use as probiotics and discuss their dual and controversial features between opportunistic pathogens or promising probiotics.

2. General Characteristics of Enterococci

2.1. Taxonomy

Enterococci are Gram-positive cocci that occur in pairs or short chains, nonspore forming, catalase and oxidase-negative, and facultative anaerobic [6, 7]. The genus Enterococcus belongs to lactic acid bacteria (LAB) and represents the third-largest LAB genus after Lactobacillus and Streptococcus with 37 species classified based on phylogenetic assessment using 16S rRNA sequencing and DNA-DNA hybridisation [3]. Indeed, new species have been recently discovered such as E. thailandicus, E. ureasiticus, E. pallens, E. caccae, E. cammelliae, E. lactis, etc. [8–12]; however, E. faecium and E. faecalis remain the most important enterococcal species. Taxonomically, enterococci were classified separately in 1984 [13] after being described as streptococci. Some authors recommend revising the classification of some taxa because of insufficient differences between them to be described as separate species such as E. flavescens and E. casseliflavus or to regroup species due to similar characteristics such as the case for E. avillorum and E. porcinus [14].

2.2. Physiological and Biochemical Traits

Enterococci are mesophilic bacteria that could grow from 10°C to 45°C with optimal temperature comprised between 30°C and 35°C [15, 16]. Also, they are able to grow in a huge range of pH from 4.4 and 9.6 and in hyper salty media with 6.5% NaCl. Traits that differentiate enterococci from streptococci are their abilities to survive after 30 min of heating at 60°C, to grow in broth supplemented with 40% of bile salts and to hydrolyse esculin [17, 18].

2.3. Habitat

Enterococci are ubiquitous microorganisms that could be present in different environments such soil, water, sewage and plants. Furthermore, they are known to belong to the commensal microbiota of human and animals [19]. Currently, E. faecalis predominates the Entercoccus species of the gastrointestinal tract followed by E. faecium, then E. durans, and E. hirae [20–22].

2.4. Occurrence in Foods

Enterococci occur in different foods; dairy products (cheeses, raw milk) [23–26], fermented vegetables (olives, fermented sorghum) [27–33], meats, fish, and sea foods [34–38].

2.4.1. Enterococci in Dairy Products

The prevalence of enterococci in milk has been traditionally considered as a result of faecal contamination, but many studies have reported that this occurrence is not always related to faecal contamination [7, 23, 24]. In fact, Enterococcus spp. has the capacity of adaptation to diverse substrates and growth conditions. Indeed, enterococci could be present in both raw and pasteurised milk of cow, sheep, goat, or camel [7, 39, 40]. Enterococcal strains examples that have been isolated from raw milk are E. faecalis and E. casseliflavus [41], E. lactis [42], E. italicus, and E. faecium [43].

Enterococci could also occur in cheeses made from raw or pasteurised milk and were commonly E. faecium, E. faecalis, E. durans, E. casseliflavus, and E. lactis [41, 44–46]. This prevalence is different among cheeses resulting in cheese type, milk used in the manufacture, production season, and conditions of production, and ripening [47, 48]. Moreover, it is important to denote that Enterococcus spp. play a beneficial role in cheese fermentation as well as in cheese ripening and development of specific flavour, texture, and taste probably through proteolytic, esterolytic and lipolytic activities, citrate breakdown and production of diacetyl, and other important volatile compounds [47–51].

2.4.2. Enterococci in Fermented Vegetables

Enterococci can be present in fermented vegetables due to the fermentation reaction with the predominance of E. faecium and E. faecalis in fermented soya, sorghum, and olives [18, 52–55].

2.4.3. Enterococci in Meat

Since enterococci are part of the commensal microflora of animal gastrointestinal tract, they could thus occur in meat when slaughtering. The common species are E. faecium, E. faecalis, E. mundtii, E. durans, E. casseliflavus, E. gilvus, and E. hirae [56–58]. Fermented salamis and sausages could also host enterococci [59, 60].

2.4.4. Enterococci in Fish and Sea Food

Several enterococcal species have been isolated from fish (viscera and skin): E. mundtii, E. faecium, and E. durans [61–66]. Regarding sea food, the prevalence of enterococci is lower than that in fermented or raw fish [67]. The common isolated strains were E. faecium, E. faecalis, E. casseliflavus, and E. hirae [68]. In regard to fresh shrimps, strains of E. faecium, E. faecalis, E. lactis, E. casseliflavus, and E. gallinarum have been isolated and reported in many studies [69–72].

3. Enterocins

3.1. Classification

Enterocins are the bacteriocins produced by Enterococcus spp. They are ribosomally synthesised, cationic, hydrophobic, and heat stable peptides with small molecular weight containing about 20-60 amino acids [19, 37, 66, 74–77]. They are insensitive to rennet and stable over a wide range of pH values [78, 79]. They are classified into four classes: lantibiotic enterocins (class I) such as cytolysin, nonlantibiotic enterocins (class II) with three subclasses (1, 2, and 3) such as enterocin A (class II-1), enterocin Q (class II-2), and enterocin B (class II-3), followed by cyclic enterocins (class III) such as enterocin AS-48 and enterocins with high molecular weights (class IV) such as enterolysin A [73]. Table 1 represents with details the enterocins’ classification. Most of the characterised enterocins belong to the class II.

The hemolytic bacteriocin (cytolysin) and the circular AS-48 were known as E. faecalis bacteriocins and were genetically and biochemically well characterised [80–84].

The subclass II.1 represents the largest enterocin subclass which includes the most abundant enterocins of enterococci. These enterocins share the consensus sequence YGNGV in their N-terminal part which is a prerequisite for their antimicrobial activity and particularly antilisterial activity. It is important to note in this context that enterocin A is among the most potent antimicrobial bacteriocin in this subclass [85–89]. Interestingly, enterocin A is known to be coproduced with other bacteriocins, often in combination with enterocin B [90] and occasionally with enterocin P, enterocins L50, or enterocin Q [91, 92]. Hence, enterococci seem to have the genetic capacity to produce more than one enterocin, as commonly observed among some other multiple-producing bacteriocin lactic acid bacteria (LAB) [93–95].

3.2. Spectrum of Action

Enterocins produced by enterococci are small antimicrobial peptides known to display broad-spectrum of inhibitory activity against spoilage bacteria and foodborne pathogens [96–99]. Remarkable antimicrobial inhibitions were observed towards Listeria monocytogenes, Bacillus cereus, Staphylococcus spp., and Clostridium spp. [71, 78, 79, 83, 97, 100]. Antagonistic activities against Gram-negative bacteria such as Pseudomonas aeruginosa, Escherichia coli, and Vibrio cholera, against fungi and yeasts, as well as against virus, were also observed with enterocins [66, 101, 102].

3.3. Mode of Action

Enterocins, as most bacteriocins, have the cytoplasmic membrane as their primary target [103–106]. They form pores in the cell membrane, thus depleting the transmembrane potential and/ or the pH gradient which result in the leakage of indispensable intracellular molecules [107–109]. The mode of action enterolysin A is quite different from the other enterocins because it attacks susceptible bacteria by degrading the cell wall structure, which eventually leads to lysis of the cells of target strains [110].

4. Pathogenicity of Enterococci

Enterococci are among the most common nosocomial pathogens that could cause important infections and diseases such as endocarditis, bacteremia, urinary, intra-abdominal and pelvic infections, central nervous system infections, etc. [4]. Among these infections, approximately 80% were associated with E. faecalis [111]. Enterococci, previously viewed as microorganisms of minimal clinical impact, have emerged now as common opportunistic pathogens of humans [112].

Traits implicated in their pathogenicity are virulence factors and the increase of antibiotic resistant strains, especially vancomycin-resistant enterococci (VRE) [5, 113, 114]. As a result, Enterococcus spp. represent a main challenge to health staff when identified as the principal cause of infection or illness, particularly in immunocompromised patients [115]. Infections caused by enterococcal strains are originated from the intestinal microbiota of the patient and can be transferred from one person to another or can be acquired by the consumption of contaminated food and water [116]. Enterococcus spp. is capable of transferring the antibiotic resistant genes (ARG) to produce β-haemolysis, gelatinase and aggregation substance that are common enterococcal virulent traits [117].

4.1. Virulence Factors

A virulence factor is an effector molecule that enhances the capacity of a microorganism to cause illness. Virulence factors of enterococci play a significant role in the pathogenicity of enterococcal strains. These factors have been intensively investigated in the last few years. The most common and well described virulence determinants in enterococci are aggregation substances (agg, asa1), cytolysin (cyl), gelatinase (gelE), extracellular surface protein (esp), adhesion to collagen (ace, acm), and adhesion-like endocarditis antigens (efaAfs and efaAfm) [118].

Aggregation substances (agg and asa1) are virulence factors inducing surface protein of Enterococcus spp. strains which promote aggregate formation during bacterial conjugation and mediate the specific binding to epithelial cells for colonisation and exchange of plasmids carrying virulence traits and antibiotic resistance genes as well [119, 120]. In addition, the aggregation substances could bind to extracellular matrix proteins such as collagen type I, fibronectin, and thrombospondin [3]. Regarding agg gene increases the hydrophobicity of the enterococcal surface inducing localisation of cholesterol to phagosomes and delaying fusion with lysosomal vesicules [121]. Up to date, agg determinant is exclusively found in E. faecalis strains [122, 123].

Cytolysin (or β-haemolysin) is known as protein bacteriocin/heamolysin bifunctionality and is the most studied virulence factor in enterococci. It constitutes a peptidic toxin able to lyse cells by forming pores in the cytoplasmic membrane of bacterial target cells [124]. The frequency of death caused by infection due to a cytolysin-producing Enterococcus is five times higher than that observed in a noncytolysin-producing enterococcal infection [125]. Studies on endocarditis have shown that there is a synergism between cyl and agg genes.

Gelatinase is an extracellular Zn-metallo-endopeptidase (EC 3.4.24.30) implicated in the hydrolysis of gelatin, collagen, β-insulin, haemoglobin, casein, and other bioactive peptides [126]. Gelatinase is able to cleave fibrin and damage host tissue allowing thus bacterial migration and spread which raise its implication in virulence of enterococci particularly E. faecalis[3]. Furthermore, this protease plays an important role in the formation of biofilm which allows enterococci to colonise tissues and persist in some infection sites [126]. It is necessary to mention that some researchers reported that even when the gelE determinant gene is detected, a negative phenotype could be found [127, 128].

Extracellular surface protein (esp) is a virulent gene determinant associated with the cell-cell adhesion, particularly adhesion to eukaryotic cells and evasion of the immune response of the host [129, 130]. This gene, which promotes colonisation, is located in a highly conserved chromosome region within the genus and is mostly common in E. faecium [129, 130].

The adhesion genes to collagen, ace, and acm, of E. faecalis and E. faecium, respectively, bind to collagen types I and IV enhancing virulence strains, while acm could also bind to laminin [3]. Also, the adhesion acm is known to be part of the subfamily of bacterial adhesions surface called Microbial Surface Components Recognising Adhesive Matrix Molecules (MSCRAMM) that adhere specifically to the protein layer of the extracellular matrix of the host [129, 130].

The efaA virulence gene is strongly involved in endocarditis [3]. The most known are efaAfs and efaAfm for E. faecalis and E. faecium, respectively [131].

Other virulence determinants are less identified in enterococci and not well described that are also implicated in enterococcal infections. Among these virulence factors is sag gene secreted by E. faecium which was able of broad-spectrum binding to extracellular matrix proteins [132]. Another E. faecium adhesion called scm could efficiently bind to collagen type IV [133]. Furthermore, the ebp gene encoding endocarditis and biofilm-associated pili were observed to enhance biofilm formation in E. faecalis [134]. Also, the bee gene (biofilm enhancer in Enterococcus) was shown to confer a high biofilm-forming phenotype to E. faecalis [135]. Finally, a further virulence factor nominated hyl, encoding a hyaluronidase, was shown to hydrolyse hyaluronic acid with a possible role in translocation [136]. This virulence factor was shown to be associated with antibiotic resistance genes and pilin genes on the plasmid [137].

In general, the incidence of all of these virulence factors was lower in E. faecium strains than in E. faecalis strains, and the virulence of enterococci could not be explained only by the presence of virulence determinants; antibiotic resistance genes play an imminent role in the pathogenicity of enterococcal strains [3, 138].

4.2. Antibiotic Resistance

Resistance of some enterococci to commonly used antibiotics is another important virulence trait which strongly enhances the pathogenicity of Enterococcus spp. by making them effective opportunistic microorganisms in nosocomial infections [139–141]. In fact, continuous exposure to antibiotics and their intensive use in human and veterinary medicines as prophylactic agents or growth promoters, respectively, have provoked increase in the incidence of enterococcal strains resistant to multiple different classes of antibiotics and may be through genetic mutations conferring this antibioresistance of enterococci and enabling their survival. Hence, this drug resistance becomes an important public health concern. Antibiotic resistance in enterococci could be generally produced by target modification, alterations that affect access of the drug to the target or enzymatic drug inactivation [142].

Intrinsic antibiotic resistance of enterococci includes resistance to cephalosporins, sulphonamides, lincosamides, β-lactams, and aminoglycosides, located in the chromosomes [130, 143]. Acquired resistances in enterococci from other microorganisms, via plasmids or transposons, could be observed toward chloramphenicol, erythromycin, fluoroquinolones, tetracycline, penicillin, ampicillin, aminoglycosides (gentamicin, kanamycin, and streptomycin) and glycopeptides especially vancomycin [142, 144]. In fact, vancomycin resistance is of special concern because VRE were known to cause serious infections and diseases that could not be treated with conventional antibiotic therapy [63, 145]. So, VRE posed a real challenge to clinicians since this antibiotic has traditionally considered the “drug of last resort” in the treatment of enterococcal infections as it is often used to replace penicillin, ampicillin, and aminoglycosides in patients with allergies [146]. For this reason, new drugs were evaluated as alternative candidates to vancomycin such as quinupristin-dalfopristin, oxazolidinones, everninomycins, and daptomycin [143].

At present, there are six known genes of glycopeptide resistance in enterococci: vanA, vanB, vanC, vanD, vanE, and vanG. The vanA type is the most important operon characterised by strains with high levels of resistance to vancomycin and teicoplanin and its main reservoir is E. faecium [130]. The vanB operon induces several levels of vancomycin resistance but not teicoplanin resistance. Only vanA and vanB genes have the ability to transfer vertically and horizontally and to confer high levels of resistance [130]. The vanC determinant induces low level of vancomycin resistance and intrinsic sensitivity to teicoplanin. The vanD, vanE, and vanG operons encode low to moderate resistance to vancomycin [130]. In general, it is interesting to know that vanA, vanB, vanD, vanE, and vanG genes are considered to be acquired properties, while vanC gene is an intrinsic trait of motile enterococci [130].

On the other hand, several studies performed in European and American countries reported that VRE colonisation occurs in the community besides human reservoir; animal, environmental, and food reservoirs could act as community sources for VRE outside the health care setting [143]. In this context, VRE were detected with vanA gene cluster in animal husbandry due to the use of avoparcin as a feed additive [143]. Effectively, in 1975 avoparcin was used as growth promoter in Europe, Australia, and several other countries, but was not allowed in the USA and Canada [145]. Interestingly, high level occurrence of VRE was observed in European animal farms; however, no VRE were detected in animal farms in the US [147]. Thus, the use of the glycopeptide avoparcin for animal growth promotion was prohibited in Europe and as a likely result, there was a rapid decline of VRE in European farms but no a total disappear [145]. Many hypotheses were suggested to explain this VRE persistence; the first one reports the fact that the use of macrolide tylosin could coselect for VR since both the resistance determinants are located on the same plasmid or that plasmid addiction systems could be implicated in the retention of the resistance [145].

Furthermore, VRE could also occur in human outside hospitals confirming that a transfer of resistance genes between animal and human or a clonal spread of resistant strains could explain this prevalence. In addition, VRE could reach foods via environmental contamination from different sources; waste water from sewage treatment, livestock faeces, and manure from poultry farms [143, 148].

Other antibiotic resistant enterococci have been found among food animals and environment worldwide. In fact, high gentamicin-, kanamycin-, streptomycin-, tetracycline- and glycopeptides-resistances have been observed among enterococci (E. faecalis, E. faecium, E. casseliflavus, and E. gallinarum) isolated from bovine mastitis (80%), chickens (62-64%), pigs (57%), food of animal origin (e.g., white and red meats), uncooked food (e.g., lettuce), sewage, and water [145, 149–151].

In general, the emergence of this high antibiotic resistance in all of these various reservoirs and environments suggests interstrain transmission of resistance genes.

4.3. Transfer of Virulence Factors and AR Genes

Enterococci are known for their genome plasticity [142]. Indeed, they are able to integrate and use some mobile genetic elements like plasmids, transposons, prophages, and insertions sequences allowing them to easily transfer acquired determinants among strains of the same species, or species of the same genus or other pathogenic and nonpathogenic bacteria as well. In this context, enterococcal virulence factors and AR genes are renowned to be associated with some highly transmissible plasmids [127]. Virulence traits and antibioresistance in enterococci were previously reported to be caused by gene horizontal or vertical transfer mechanisms and by ability to receive genetic material [143]. In this context, Coburn et al. [152] demonstrated the horizontal transfer of a 150 kb cluster called “pathogenicity island” (PAI), previously described in E. faecalis by Shankar et al. [153] that contain about 100 operons some of which code for virulence genes (toxins, cytolysin, surface proteins, and aggregation). This horizontal transfer of the pathogenicity island was carried by a plasmid in response to pheromones. Regarding resistance to macrolide antibiotics, lincosamides, and streptogramins (MLS), De Leener et al. [154] have demonstrated, through a genetic marker (ermB), the horizontal transfer of these AR genes from an E. faecium strain of animal origin to a strain of human origin. This mechanism of propagation via the transfer of genetic elements (plasmids and/or transposons) is more important than clonal dispersal of antibiotic resistant strains [155]. These experiments were conducted on animal models and did not take into account the natural environment that strongly influences the transfer of moving elements.

Of concern, transconjugation in which enterococci acquired virulence and AR determinants could represents a real risk to a safe enterococcal strain that is free of these virulent determinants could unfortunately acquire such genes in both of human or nonhuman reservoirs which raises serious worry regarding their safety for use as probiotics.

5. Enterococci as Probiotics

Probiotics are defined as “live microorganisms which when consumed in sufficient amounts, affect beneficially the health of the host.” Health benefits that confer probiotic microorganisms include modulating immunity, enhancing intestinal barrier function, or altering pain perception [1].

Most probiotics are of intestinal origins and belong to the lactic acid bacteria (LAB) particularly to genera of Bifidobacterium and Lactobacillus, while enterococcal strains are occasionally used [3]. In this context, many studies have been conducted to evaluate the probiotic characteristics of Enterococcus strains and clear beneficial and significant health-promoting effects of enterococci were reported [3, 156–160]. Indeed, enterococci were used as probiotics for several purposes and these different applications include pharmaceutical industry, human and veterinary medicines and food industry since some probiotic enterococci could be used in the production of functional foods [1].

In fact, some enterococcal strains such as E. faecium M74 and E. faecium SF-68 are included as food supplements in several probiotic preparations that have been proved to be effective and safe, such as FortiFlora® and Cernivet® (containing E. faecium SF68®, Cerbios-Pharma SA, Switzerland), and Symbioflor® 1 with E. faecalis (Symbiopharm, Herborn, Germany) [142, 161, 162].

Enterococcal probiotics can be used in treatment and/or prevention of certain human and animal diseases such as alleviation of irritable bowel syndrome symptoms and antibiotic-induced diarrhea and prevention of different functional and chronic intestinal diseases [163]. Moreover, some enterococci exhibit antimutagenic, anticarcinogenic, hypocholesterolemic, and immune regulation effects [17].

E. durans M4-5 has been found to generate butyrate, short chain fatty acids (SCFAs), that induce significant anti-inflammatory effects and contribute to the integrity of the intestinal epithelium [164, 165].

E. mundtii ST4SA was recently presented as another potential probiotic strain [166] and E. durans KLDS 6.0930 has been postulated as a probiotic candidate through lowering human serum cholesterol levels [167].

More recently, the strain E. durans LAB18s was recommended useful for use as a source of dietary selenium supplementation [168], while E. faecium LCW 44 and E. durans 6HL were shown highly potent against Gram-positive [169] and Gram-negative bacteria [169, 170], respectively.

In feed regulation, the European Food Standards Agency (EFSA) authorised certain strains of enterococci for use as silage additive and dietary supplements. For instance, some enterococcal probiotics were included in the group of feed additives for stabilising the microbial communities of the digestive tract in both monogastric and ruminant animals [171]. Strains of E. faecium NCIMB 11181 and E. faecium DSM 7134 were approved as feed additives for calves and piglets by EFSA. The probiotics E. faecium SF68® and E. faecalis Symbioflor 1 are also used to prevent or treat diarrhea in pigs, poultry, livestock, and pets [3]. Furthermore, among the claimed advantages of probiotic enterococci is its positive effects on the performance characteristics of the growth and health of farm animals. In this context, feeding pigs with a probiotic Enterococcus spp. was found to reduce intestinal pathogens [172]. Likewise, oral administration of E. faecium NHRD IHARA by postweaning piglets has increased serum and fecal IgA levels and improved piglets growth [173]. In chickens, E. faecium was demonstrated to improve growth, intestinal morphology, and the caecal microbiota homeostasis [174]. E. faecium was also reported to enhance the metabolic efficiency and decrease inflammatory responses in broilers [175].

On the other hand, numerous studies have shown the beneficial effects of enterococci in aquaculture. In fact, several works reported a wide spectrum of inhibition by E. faecium toward aquatic pathogens including Yersinia ruckeri, Vibrio harveyi, Streptococcus agalactiae, and Aeromonas veronii [176]. In addition, many trials have investigated the efficacy of E. faecium incorporated in feed to improve fish growth and stimulate immune response [177].

Due to safety concerns, lack of safety information, and legislation, only a limited number of enterococcal probiotics are commercialised. Enterococcus has not yet obtained the status GRAS [3]. However, some well characterised enterococcal strains are used as starter cultures, cocultures, or protective cultures in food industry and/or probiotics due to their positive attributes. The dual trait of being good candidates as probiotics and opportunistic pathogens of enterococci remains a controversial issue which turns about the question whether enterococci are safe for probiotic use that also remains difficult to answer. The main concern for Enterococcus spp. as probiotics is their pathogenicity based on horizontal transfer of virulence factors and AR genes, as explained above, and the increasing number of enterococcal infections in recent decades [1, 178]. Nevertheless, the most important and interesting evidence is that enterococci are not suggested as foodborne pathogens [179]. Indeed, after being suspected of causative agents of foodborne illness in 1926, many studies on enterococci, particularly E. faecalis and E. faecium, including experiments on animals and volunteer humans were carried out to prove that enterococci cause foodborne illness, but investigations yielded negative results because these bacteria are generally identified in mixed presence with other pathogens such as staphylococci or others [180]. Subsequently, enterococci have emerged as nosocomial- and community-acquired pathogens rather than foodborne pathogens [181, 182]. Still, the safety of enterococci before their use in foods or in probiotic preparations should be carefully assessed. Effectively, when selecting an enterococcal probiotic strain, a number of properties should be considered involving safety aspect and functional and beneficial traits. Since probiotic effect is strain dependent, it should be thus well characterised (phenotypically and genotypically) and must be safe and free of any pathogenicity such as the absence of virulence factors and acquired AR genes [183, 184]. Desirable characteristics for probiotic strain include also the ability to survive and retain viability at harsh gastrointestinal tract conditions of a healthy human (low pH, pepsin, pancreatin, bile salts), their unability to translocate the intestinal mucosa, their susceptibility to phagocytic killing, and the ability to produce antimicrobial substances such as enterocins [1, 183, 184]. Further considerable trait for potential enterococcal probiotics is that they should have limited ability to exchange DNA in vivo [1].

6. Conclusion

Enterococci are ubiquitous microorganisms that could be naturally present in several food products. Many studies have reported the beneficial effects of enterocin-producing Enterococcus strains as starters, adjunct starters, protective cultures, or probiotics. However, very few enterococci have been used as probiotics or feed additives because of the safety concern associated with their pathogenic trait as opportunistic microorganisms capable of causing severe infections and diseases due to their potential virulence factors and antibiotic resistance genes. To date, there have been no reports of disease caused by probiotic enterococci that are currently on the market such the case of E. faecium SF68 and E. faecalis Symbioflor, which is a great indication of the safety of these enterococcal probiotic strains.

Hence, enterococcal strains in view of future use as probiotics must be well characterised and perfectly assessed regarding safety aspects. For this, modern scientific techniques, up-to-date knowledge of enterococci and their properties, implementation of adequate guidance, and appropriate legislation are strongly recommended to differentiate between pathogenic and safe enterococcal strains and thus could help industrials, health staff, and consumers to accept these strains as potential candidates for useful and beneficial applications as probiotics, like other LAB strains. These measures should be complemented by a more prudent use of antibiotics in human and veterinary medicines and a strict control regarding the presence of enterococci in environmental and food sources to prevent or limit the spread of pathogenic enterococcal strains. Finally, a specific assessment of community transmission is also needed.

Therefore, until now, the debate remains open. In fact, as a coin with two sides, for enterococci, despite their health-promoting properties, they may possess detrimental traits which make it difficult to establish a clear decision within enterococcal strains between emerging pathogens and potential probiotics.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

References

N. I. Agudelo Higuita and M. M. Huycke, “Enterococcal disease, epidemiology, and implications for treatment,” in Enterococci: From Commensals to Leading Causes of Drug Resistant Infection, pp. 65–99, Massachusetts Eye and Ear Infirmary, Boston, Mass, USA, 2014.
View at: Google Scholar
D. Zielińska and D. Kolożyn-Krajewska, “Food-origin lactic acid bacteria may exhibit probiotic properties: review,” BioMed Research International, vol. 2018, Article ID 5063185, 15 pages, 2018.
View at: Publisher Site | Google Scholar
C. M. A. P. Franz, M. Huch, H. Abriouel, W. Holzapfel, and A. Gálvez, “Enterococci as probiotics and their implications in food safety,” International Journal of Food Microbiology, vol. 151, no. 2, pp. 125–140, 2011.
View at: Publisher Site | Google Scholar
T. O’Driscoll and C. W. Crank, “Vancomycin-resistant enterococcal infections: Epidemiology, clinical manifestations, and optimal management,” Infection and Drug Resistance, vol. 8, pp. 217–230, 2015.
View at: Google Scholar
C. M. A. P. Franz, A. B. Muscholl-Silberhorn, N. M. K. Yousif, M. Vancanneyt, J. Swings, and W. H. Holzapfel, “Incidence of virulence factors and antibiotic resistance among enterococci isolated from food,” Applied and Environmental Microbiology, vol. 67, no. 9, pp. 4385–4389, 2001.
View at: Publisher Site | Google Scholar
D. Anagnostopoulos, D. Bozoudi, and D. Tsaltas, “Enterococci isolated from cypriot green table olives as a new source of technological and probiotic properties,” Fermentation, vol. 4, no. 2, p. 48, 2018.
View at: Publisher Site | Google Scholar
Z. Kadri, F. Spitaels, M. Cnockaert et al., “Enterococcus bulliens sp. nov., a novel lactic acid bacterium isolated from camel milk,” Antonie van Leeuwenhoek-Journal of Microbiology, vol. 108, no. 5, pp. 1257–1265, 2015.
View at: Publisher Site | Google Scholar
S. Morandi, T. Silvetti, and M. Brasca, “Biotechnological and safety characterization of Enterococcus lactis, a recently described species of dairy origin,” Antonie van Leeuwenhoek-Journal of Microbiology, vol. 103, no. 1, pp. 239–249, 2013.
View at: Publisher Site | Google Scholar
W. Holzapfel, A. Arini, M. Aeschbacher, R. Coppolecchia, and B. Pot, “Enterococcus faecium SF68 as a model for efficacy and safety evaluation of pharmaceutical probiotics,” Beneficial Microbes, vol. 9, no. 3, pp. 375–388, 2018.
View at: Publisher Site | Google Scholar
A. C. Anderson, D. Jonas, I. Huber et al., “Enterococcus faecalis from food, clinical specimens, and oral sites: prevalence of virulence factors in association with biofilm formation,” Frontiers in Microbiology, vol. 6, article no 1534, 2016.
View at: Publisher Site | Google Scholar
E. Bargossi, G. Tabanelli, C. Montanari et al., “Growth, biogenic amine production and tyrDC transcription of Enterococcus faecalis in synthetic medium containing defined amino acid concentrations,” Journal of Applied Microbiology, vol. 122, no. 4, pp. 1078–1091, 2017.
View at: Publisher Site | Google Scholar
C. Henning, D. Gautam, and P. Muriana, “Identification of multiple bacteriocins in enterococcus spp. using an enterococcus-specific bacteriocin PCR array,” Microorganisms, vol. 3, no. 1, pp. 1–16, 2015.
View at: Publisher Site | Google Scholar
K. H. Schleifer and R. Kilpper-Bälz, “Transfer of Streptococcus faecalis and Streptococcus faecium to the genus Enterococcus nom. rev. as Enterococcus faecalis comb. nov. and Enterococcus faecium comb. nov.,” International Journal of Systematic Bacteriology, vol. 34, no. 1, pp. 31–34, 1984.
View at: Publisher Site | Google Scholar
P. Descheemaeker, C. Lammens, B. Pot, P. Vandamme, and H. Goossens, “Evaluation of arbitrarily primed PCR analysis and pulsed-field gel electrophoresis of large genomic DNA fragments for identification of enterococci important in human medicine,” International Journal of Systematic Bacteriology, vol. 47, no. 2, pp. 555–561, 1997.
View at: Publisher Site | Google Scholar
B. E. Murray, “The life and times of the Enterococcus,” Clinical Microbiology Reviews, vol. 3, no. 1, pp. 46–65, 1990.
View at: Publisher Site | Google Scholar
M. García-Solache and L. B. Rice, “The Enterococcus: a model of adaptability to its environment,” Clinical Microbiology Reviews, vol. 32, no. 2, Article ID e00058-18, 2019.
View at: Publisher Site | Google Scholar
M. R. Foulquié Moreno, P. Sarantinopoulos, E. Tsakalidou, and L. De Vuyst, “The role and application of enterococci in food and health,” International Journal of Food Microbiology, vol. 106, no. 1, pp. 1–24, 2006.
View at: Publisher Site | Google Scholar
N. Ben Omar, A. Castro, R. Lucas et al., “Functional and safety aspects of enterococci isolated from different Spanish foods,” Systematic and Applied Microbiology, vol. 27, no. 1, pp. 118–130, 2004.
View at: Publisher Site | Google Scholar
O. Ben Braïek, H. Ghomrassi, P. Cremonesi et al., “Isolation and characterisation of an enterocin P-producing Enterococcus lactis strain from a fresh shrimp (Penaeus vannamei),” Antonie van Leeuwenhoek Journal of Microbiology, vol. 110, no. 6, pp. 771–786, 2017.
View at: Publisher Site | Google Scholar
N. Russo, C. Caggia, A. Pino, T. M. Coque, S. Arioli, and C. L. Randazzo, “Enterococcus spp. in ragusano PDO and pecorino siciliano cheese types: a snapshot of their antibiotic resistance distribution,” Food and Chemical Toxicology, vol. 120, pp. 277–286, 2018.
View at: Publisher Site | Google Scholar
L. S. Monticelli, F. Decembrini, A. Bergamasco, and G. Caruso, “Water quality assessment of transitional and coastal marine Sicilian waters (Italy): ecological and epidemiological significance of multiple antimicrobial resistant Enterococcus spp,” Estuarine, Coastal and Shelf Science, vol. 217, pp. 173–184, 2019.
View at: Publisher Site | Google Scholar
H. Hanchi, W. Mottawea, K. Sebei, and R. Hammami, “The genus Enterococcus: Between probiotic potential and safety concerns-an update,” Frontiers in Microbiology, vol. 9, 2018.
View at: Google Scholar
S. Morandi, P. Cremonesi, M. Povolo, and M. Brasca, “Enterococcus lactis sp. nov., from Italian raw milk cheeses,” International Journal of Systematic and Evolutionary Microbiology, vol. 62, no. 8, pp. 1992–1996, 2012.
View at: Publisher Site | Google Scholar
N. Gaaloul, O. Ben Braiek, J. M. Berjeaud et al., “Evaluation of antimicrobial activity and safety aspect of enterococcus italicusGGN10 strain isolated from Tunisian bovine raw milk,” Journal of Food Safety, vol. 34, no. 4, pp. 300–311, 2014.
View at: Publisher Site | Google Scholar
S. Pieniz, R. Andreazza, B. C. Okeke, F. A. Camargo, and A. Brandelli, “Antimicrobial and antioxidant activities of Enterococcus species isolated from meat and dairy products,” Brazilian Journal of Biology, vol. 75, no. 4, pp. 923–931, 2015.
View at: Publisher Site | Google Scholar
A. Elmoslih, M. Zanzan, R. Aissa et al., “Isolation and characterization of bacteriocinogenic enterococcal and lactococcal strains from south of Morocco dairy product,” Biotechnology Journal International, vol. 18, no. 4, pp. 1–16, 2017.
View at: Publisher Site | Google Scholar
J. P. Tamang, K. Watanabe, and W. H. Holzapfel, “Diversity of microorganisms in global fermented foods and beverages,” Frontiers in Microbiology, vol. 7, p. 377, 2016.
View at: Google Scholar
S. Rezac, C. R. Kok, M. Heermann, and R. Hutkins, “Fermented foods as a dietary source of live organisms,” Frontiers in Microbiology, vol. 9, p. 1785, 2018.
View at: Google Scholar
N. Shah and A. Patel, “Fermented foods: an overview,” in Microorganisms in Sustainable Agriculture, Food, and the Environment, pp. 25–88, Apple Academic Press, 2017.
View at: Google Scholar
S. Kandasamy, D. Kavitake, and P. H. Shetty, “Lactic acid bacteria and yeasts as starter cultures for fermented foods and their role in commercialization of fermented foods,” in Innovations in Technologies for Fermented Food and Beverage Industries, pp. 25–52, Springer, Cham, Switzerland, 2018.
View at: Google Scholar
A. Lianou, E. Z. Panagou, and G. J. Nychas, “Microbiological spoilage of foods and beverages,” in The Stability and Shelf Life of Food, pp. 3–42, Woodhead Publishing, 2nd edition, 2016.
View at: Google Scholar
N. Thapa and J. P. Tamang, “Functionality and therapeutic values of fermented foods,” in Health Benefits of Fermented Foods and Beverages, pp. 111–168, CRC Press, 2015.
View at: Google Scholar
D. P. Latha, S. M. Reddy, K. S. Youn, and P. Ravindra, “Starter culture technology: fermented foods,” in Advances in Bioprocess Technology, pp. 435–454, Springer, Cham, Switzerland, 2015.
View at: Google Scholar
N. Noordiana, A. B. Fatimah, and A. S. Mun, “Antibacterial agents produced by lactic acid bacteria isolated from Threadfin Salmon and Grass Shrimp,” International Food Research Journal, vol. 20, no. 1, pp. 117–124, 2013.
View at: Google Scholar
M. Sarra, G. Taoufik, L. C. Patrick, B. Benjamin, F. Yannick, and H. Khaled, “Isolation and characterization of enterococci bacteriocinic strains from Tunisian fish viscera,” Journal of Food and Nutrition Sciences, vol. 04, no. 06, pp. 701–708, 2013.
View at: Publisher Site | Google Scholar
H. Ghomrassi, O. B. Braiek, Y. Choiset et al., “Evaluation of marine bacteriocinogenic enterococci strains with inhibitory activity against fish-pathogenic Gram-negative bacteria,” Diseases of Aquatic Organisms, vol. 118, no. 1, pp. 31–43, 2016.
View at: Publisher Site | Google Scholar
O. Ben Braïek, S. Morandi, P. Cremonesi, S. Smaoui, K. Hani, and T. Ghrairi, “Biotechnological potential, probiotic and safety properties of newly isolated enterocin-producing Enterococcus lactis strains,” LWT- Food Science and Technology, vol. 92, pp. 361–370, 2018.
View at: Publisher Site | Google Scholar
G. Vinderola, P. Burns, and J. Reinheimer, “Probiotics in nondairy products,” Vegetarian and Plant-Based Diets in Health and Disease Prevention, pp. 809–835, 2017.
View at: Google Scholar
Z. M. Alzubaidy, K. O. Khthir, and R. Kamal, “Determination of some antibiotic resistances genes by polymerase chain reaction of lactic acid bacteria isolates from local dairy products,” International Journal of Medical Sciences, vol. 2, no. 1, pp. 12–28, 2019.
View at: Google Scholar
H. El Hatmi, Z. Jrad, O. Oussaief et al., “Fermentation of dromedary camel (Camelus dromedarius) milk by Enterococcus faecium, Streptococcus macedonicus as a potential alternative of fermented cow milk,” LWT- Food Science and Technology, vol. 90, pp. 373–380, 2018.
View at: Publisher Site | Google Scholar
R. Gelsomino, M. Vancanneyt, T. M. Cogan, S. Condon, and J. Swings, “Source of enterococci in a farmhouse raw-milk cheese,” Applied and Environmental Microbiology, vol. 68, no. 7, pp. 3560–3565, 2002.
View at: Publisher Site | Google Scholar
R. Bauer, J. P. Bekker, N. V. Wyk, C. du Toit, L. M. T. Dicks, and J. Kossmann, “Exopolysaccharide production by lactose-hydrolyzing bacteria isolated from traditionally fermented milk,” International Journal of Food Microbiology, vol. 131, no. 2-3, pp. 260–264, 2009.
View at: Publisher Site | Google Scholar
N. Gaaloul, O. Ben Braiek, K. Hani, A. Volski, M. L. Chikindas, and T. Ghrairi, “Isolation and characterization of large spectrum and multiple bacteriocin-producing Enterococcus faecium strain from raw bovine milk,” Journal of Applied Microbiology, vol. 118, no. 2, pp. 343–355, 2015.
View at: Publisher Site | Google Scholar
G. Giraffa, “Functionality of enterococci in dairy products,” International Journal of Food Microbiology, vol. 88, no. 2-3, pp. 215–222, 2003.
View at: Publisher Site | Google Scholar
T. Ghrairi, M. Manai, J. M. Berjeaud, and J. Frère, “Antilisterial activity of lactic acid bacteria isolated from rigouta, a traditional Tunisian cheese,” Journal of Applied Microbiology, vol. 97, no. 3, pp. 621–628, 2004.
View at: Publisher Site | Google Scholar
R. Burdychova and T. Komprda, “Biogenic amine-forming microbial communities in cheese,” FEMS Microbiology Letters, vol. 276, no. 2, pp. 149–155, 2007.
View at: Publisher Site | Google Scholar
L. Favaro, A. L. Barretto Penna, and S. D. Todorov, “Bacteriocinogenic LAB from cheeses - Application in biopreservation?” Trends in Food Science & Technology, vol. 41, no. 1, pp. 37–48, 2015.
View at: Publisher Site | Google Scholar
E. Vandera, A. Kakouri, A. Koukkou, and J. Samelis, “Major ecological shifts within the dominant nonstarter lactic acid bacteria in mature Greek Graviera cheese as affected by the starter culture type,” International Journal of Food Microbiology, vol. 290, pp. 15–26, 2019.
View at: Publisher Site | Google Scholar
D. Yunita and C. E. R. Dodd, “Microbial community dynamics of a blue-veined raw milk cheese from the United Kingdom,” Journal of Dairy Science, vol. 101, no. 6, pp. 4923–4935, 2018.
View at: Publisher Site | Google Scholar
S. Portilla-Vázquez, A. Rodríguez, M. Ramírez-Lepe, P. G. Mendoza-García, and B. Martínez, “Biodiversity of bacteriocin-producing lactic acid bacteria from Mexican regional cheeses and their contribution to milk fermentation,” Food Biotechnology, vol. 30, no. 3, pp. 155–172, 2016.
View at: Publisher Site | Google Scholar
A. L. B. Penna and S. D. Todorov, “Bio preservation of cheese by lactic acid bacteria,” EC Nutrition, vol. 4, pp. 869–871, 2016.
View at: Google Scholar
M. Perricone, E. Arace, G. Calò, and M. Sinigaglia, “Ethnic fermented foods,” in Starter Cultures in Food Production, pp. 384–406, Wiley-Blackwell, 2017.
View at: Google Scholar
S. D. Todorov and W. H. Holzapfel, “Traditional cereal fermented foods as sources of functional microorganisms,” in Advances in Fermented Foods and Beverages, pp. 123–153, Woodhead Publishing, 2015.
View at: Google Scholar
D. Kavitake, S. Kandasamy, P. B. Devi, and P. H. Shetty, “Recent developments on encapsulation of lactic acid bacteria as potential starter culture in fermented foods – a review,” Food Bioscience, vol. 21, pp. 34–44, 2018.
View at: Publisher Site | Google Scholar
D. Liptáková, Z. Matejčeková, and Ľ. Valík, “Lactic acid bacteria and fermentation of cereals and pseudocereals,” in Fermentation Processes, pp. 223–254, InTech, 2017.
View at: Google Scholar
A. Panghal, S. Janghu, K. Virkar, Y. Gat, V. Kumar, and N. Chhikara, “Potential non-dairy probiotic products – a healthy approach,” Food Bioscience, vol. 21, pp. 80–89, 2018.
View at: Publisher Site | Google Scholar
R. K. Barakat, M. W. Griffiths, and L. J. Harris, “Isolation and characterization of Carnobacterium, Lactococcus, and Enterococcus spp. from cooked, modified atmosphere packaged, refrigerated, poultry meat,” International Journal of Food Microbiology, vol. 62, no. 1-2, pp. 83–94, 2000.
View at: Publisher Site | Google Scholar
J. Barbosa, V. Ferreira, and P. Teixeira, “Antibiotic susceptibility of enterococci isolated from traditional fermented meat products,” Food Microbiology, vol. 26, no. 5, pp. 527–532, 2009.
View at: Publisher Site | Google Scholar
A. Zgomba Maksimovic, M. Zunabovic-Pichler, I. Kos et al., “Microbiological hazards and potential of spontaneously fermented game meat sausages: a focus on lactic acid bacteria diversity,” LWT- Food Science and Technology, vol. 89, pp. 418–426, 2018.
View at: Publisher Site | Google Scholar
U. ur Rahman, M. I. Khan, M. Sohaib, A. Sahar, and A. Ishaq, “Exploiting microorganisms to develop improved functional meat sausages: a review,” Food Reviews International, vol. 33, no. 2, pp. 195–215, 2017.
View at: Publisher Site | Google Scholar
A. S. Valenzuela, N. Benomar, H. Abriouel, M. M. Cañamero, and A. Gálvez, “Isolation and identification of Enterococcus faecium from seafoods: antimicrobial resistance and production of bacteriocin-like substances,” Food Microbiology, vol. 27, no. 7, pp. 955–961, 2010.
View at: Publisher Site | Google Scholar
C. A. Campos, Ó. Rodríguez, P. Calo-Mata, M. Prado, and J. Barros-Velázquez, “Preliminary characterization of bacteriocins from Lactococcus lactis, Enterococcus faecium and Enterococcus mundtii strains isolated from turbot (Psetta maxima),” Food Research International, vol. 39, no. 3, pp. 356–364, 2006.
View at: Publisher Site | Google Scholar
S. Migaw, T. Ghrairi, Y. Belguesmia et al., “Diversity of bacteriocinogenic lactic acid bacteria isolated from Mediterranean fish viscera,” World Journal of Microbiology and Biotechnology, vol. 30, no. 4, pp. 1207–1217, 2014.
View at: Publisher Site | Google Scholar
R. El-Jeni, K. Böhme, M. El Bour et al., “Rapid genus identification of selected lactic acid bacteria isolated from Mugil cephalis and Oreochromis niloticus organs using MALDI-TOF,” Annals of Microbiology, vol. 69, no. 1, pp. 1–15, 2019.
View at: Publisher Site | Google Scholar
R. El-Jeni, M. El Bour, P. Calo-Mata et al., “In vitro probiotic profiling of novel Enterococcus faecium and Leuconostoc mesenteroides from Tunisian freshwater fishes,” Canadian Journal of Microbiology, vol. 62, no. 1, pp. 60–71, 2015.
View at: Publisher Site | Google Scholar
O. Ben Braïek, P. Cremonesi, S. Morandi, S. Smaoui, K. Hani, and T. Ghrairi, “Safety characterisation and inhibition of fungi and bacteria by a novel multiple enterocin-producing Enterococcus lactis 4CP3 strain,” Microbial Pathogenesis, vol. 118, pp. 32–38, 2018.
View at: Publisher Site | Google Scholar
P. S. Nair and P. K. Surendran, “Biochemical characterization of lactic acid bacteria isolated from fish and prawn,” Journal of Culture Collections, vol. 4, pp. 48–52, 2005.
View at: Google Scholar
L. Ben Said, N. Klibi, R. Dziri et al., “Prevalence, antimicrobial resistance and genetic lineages of Enterococcus spp. from vegetable food, soil and irrigation water in farm environments in Tunisia,” Journal of the Science of Food and Agriculture, vol. 96, no. 5, pp. 1627–1633, 2016.
View at: Publisher Site | Google Scholar
Y. Cai, P. Suyanandana, P. Saman, and Y. Benno, “Classification and characterization of lactic acid bacteria isolated from common carp and freshwater prawns,” Journal of General and Applied Microbiology, vol. 45, no. 4, pp. 177–184, 1999.
View at: Google Scholar
P. Dalgaard and L. V. Jørgensen, “Cooked and brined shrimps packed in a modified atmosphere have a shelf-life of >7 months at 0°C, but spoil in 4-6 days at 25°C,” International Journal of Food Science & Technology, vol. 35, no. 4, pp. 431–442, 2000.
View at: Publisher Site | Google Scholar
O. Ben Braïek, S. Smaoui, K. Ennouri, K. Hani, and T. Ghrairi, “Genetic Analysis with random amplified polymorphic DNA of the multiple enterocin-producing enterococcus lactis 4CP3 strain and its efficient role in the growth of listeria monocytogenes in raw beef meat,” BioMed Research International, vol. 2018, Article ID 5827986, 10 pages, 2018.
View at: Publisher Site | Google Scholar
W. Chajecka-Wierzchowska, A. Zadernowska, and Ł. Łaniewska-Trokenheim, “Virulence factors, antimicrobial resistance and biofilm formation in Enterococcus spp. isolated from retail shrimps,” LWT- Food Science and Technology, vol. 69, pp. 117–122, 2016.
View at: Publisher Site | Google Scholar
C. M. A. P. Franz, M. J. Van Belkum, W. H. Holzapfel, H. Abriouel, and A. Gálvez, “Diversity of enterococcal bacteriocins and their grouping in a new classification scheme,” FEMS Microbiology Reviews, vol. 31, no. 3, pp. 293–310, 2007.
View at: Publisher Site | Google Scholar
F. R. Fields, K. E. Carothers, R. D. Balsara, V. A. Ploplis, F. J. Castellino, and S. W. Lee, “Rational design of syn-safencin, a novel linear antimicrobial peptide derived from the circular bacteriocin safencin AS-48,” The Journal of Antibiotics, vol. 71, no. 6, pp. 592–600, 2018.
View at: Publisher Site | Google Scholar
G. N. Tenea and L. Yépez, ““Bioactive compounds of lactic acid bacteria. Case study: Evaluation of antimicrobial activity of bacteriocin-producing lactobacilli Isolated from native ecological niches of Ecuador,” in Probiotics and prebiotics in Human Nutrition and Health, pp. 149–167, InTech, 2016.
View at: Google Scholar
J. J. Jiménez, D. B. Diep, J. Borrero et al., “Cloning strategies for heterologous expression of the bacteriocin enterocin A by Lactobacillus sakei Lb790, Lb. plantarum NC8 and Lb. casei CECT475,” Microbial Cell Factories, vol. 14, no. 1, article no. 166, 2015.
View at: Publisher Site | Google Scholar
J. J. Jiménez, J. Borrero, L. Gútiez et al., “Use of synthetic genes for cloning, production and functional expression of the bacteriocins enterocin A and bacteriocin E 50-52 by Pichia pastoris and Kluyveromyces lactis,” Molecular Biotechnology, vol. 56, no. 6, pp. 571–583, 2014.
View at: Publisher Site | Google Scholar
A. Chakchouk-Mtibaa, L. Elleuch, S. Smaoui et al., “An antilisterial bacteriocin BacFL31 produced by Enterococcus faecium FL31 with a novel structure containing hydroxyproline residues,” Anaerobe, vol. 27, pp. 1–6, 2014.
View at: Publisher Site | Google Scholar
A. Chakchouk-Mtibaa, L. Elleuch, S. Smaoui et al., “Characterization of the bacteriocin BacJ1 and its effectiveness for the inactivation of Salmonella typhimurium during turkey escalope storage,” Food Chemistry, vol. 152, pp. 566–572, 2014.
View at: Publisher Site | Google Scholar
M. Gilmore, P. Coburn, S. Nallapareddy, and B. Murray, “Enterococcal virulence,” in The Enterococci: Pathogenesis, Molecular Biology and Antibiotic Resistance, pp. 301–354, American Society Microbiology Press, Washington, DC, USA, 2002.
View at: Google Scholar
W. Haas, B. D. Shepard, and M. S. Gilmore, “Two-component regulator of Enterococcus faecalis cytolysin responds to quorum-sensing autoinduction,” Nature, vol. 415, no. 6867, pp. 84–87, 2002.
View at: Publisher Site | Google Scholar
S. El-Ghaish, A. El-Baz, N. Hwanhlem et al., “Bacteriocin production and safety evaluation of non-starter Enterococcus faecium IM1 and Enterococcus hirae IM1 strains isolated from homemade Egyptian dairy products,” European Food Research and Technology, vol. 240, no. 6, pp. 1211–1223, 2015.
View at: Publisher Site | Google Scholar
S. Arbulu, C. T. Lohans, M. J. Van Belkum et al., “Solution Structure of Enterocin HF, an Antilisterial Bacteriocin Produced by Enterococcus faecium M3K31,” Journal of Agricultural and Food Chemistry, vol. 63, no. 49, pp. 10689–10695, 2015.
View at: Publisher Site | Google Scholar
A. van Heel, “Prediction, production and characterization of post-translationally modified antimicrobial peptides,” Expert Opinion Drug Metabolism and Toxicology, vol. 7, no. 6, pp. 675–680, 2016.
View at: Google Scholar
R. Daillère, M. Vétizou, N. Waldschmitt et al., “Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects,” Immunity, vol. 45, no. 4, pp. 931–943, 2016.
View at: Publisher Site | Google Scholar
A. K. Al Atya, K. Drider-Hadiouche, R. Ravallec, A. Silvain, A. Vachee, and D. Drider, “Probiotic potential of enterococcus faecalis strains isolated from meconium,” Frontiers in Microbiology, vol. 6, p. 227, 2015.
View at: Google Scholar
A. S. Vasilchenko, E. A. Rogozhin, and A. V. Valyshev, “Purification of a novel bacteriocin-like inhibitory substance produced by enterococcus faecium ICIS 8 and characterization of its mode of action,” Microbial Drug Resistance, vol. 23, no. 4, pp. 447–456, 2017.
View at: Publisher Site | Google Scholar
A. G. Beukers, R. Zaheer, N. Goji et al., “Comparative genomics of Enterococcus spp. isolated from bovine feces,” BMC Microbiology, vol. 17, no. 1, p. 52, 2017.
View at: Google Scholar
A. Lauková, R. Szabóová, P. Pleva, L. Buňková, and Ľ. Chrastinová, “Decarboxylase-positive Enterococcus faecium strains isolated from rabbit meat and their sensitivity to enterocins,” Food Science & Nutrition, vol. 5, no. 1, pp. 31–37, 2017.
View at: Publisher Site | Google Scholar
P. Casaus, T. Nilsen, L. M. Cintas, I. F. Nes, P. E. Hernández, and H. Holo, “Enterocin B, a new bacteriocin from enterococcus faecium T136 which can act synergistically with enterocin A,” Microbiology, vol. 143, no. 7, pp. 2287–2294, 1997.
View at: Publisher Site | Google Scholar
R. Criado, D. B. Diep, Å. Aakra et al., “Complete sequence of the enterocin Q-encoding plasmid pCIZ2 from the multiple bacteriocin producer Enterococcus faecium L50 and genetic characterization of enterocin Q production and immunity,” Applied and Environmental Microbiology, vol. 72, no. 10, pp. 6653–6666, 2006.
View at: Publisher Site | Google Scholar
A. Basanta, J. Sánchez, B. Gómez-Sala, C. Herranz, P. E. Hernández, and L. M. Cintas, “Antimicrobial activity of Enterococcus faecium L50, a strain producing enterocins L50 (L50A and L50B), P and Q, against beer-spoilage lactic acid bacteria in broth, wort (hopped and unhopped), and alcoholic and non-alcoholic lager beers,” International Journal of Food Microbiology, vol. 125, no. 3, pp. 293–307, 2008.
View at: Publisher Site | Google Scholar
E. Vandera, G. Tsirka, A. Kakouri, A.-I. Koukkou, and J. Samelis, “Approaches for enhancing in situ detection of enterocin genes in thermized milk, and selective isolation of enterocin-producing Enterococcus faecium from Baird-Parker agar,” International Journal of Food Microbiology, vol. 281, pp. 23–31, 2018.
View at: Publisher Site | Google Scholar
M. Merzoug, K. Mosbahi, D. Walker, and N.-E. Karam, “Screening of the enterocin-encoding genes and their genetic determinism in the bacteriocinogenic enterococcus faecium GHB21,” Probiotics and Antimicrobial Proteins, 2018.
View at: Google Scholar
A. Merlich, M. Galkin, Y. Choiset et al., “Characterization of the bacteriocin produced by Enterococcus italicus ONU547 isolated from Thai fermented cabbage,” Folia Microbiologica, 2019.
View at: Publisher Site | Google Scholar
A. Ahmadova, S. D. Todorov, Y. Choiset et al., “Evaluation of antimicrobial activity, probiotic properties and safety of wild strain Enterococcus faecium AQ71 isolated from Azerbaijani Motal cheese,” Food Control, vol. 30, no. 2, pp. 631–641, 2013.
View at: Publisher Site | Google Scholar
P. M. O'Connor, R. P. Ross, C. Hill, and P. D. Cotter, “Antimicrobial antagonists against food pathogens: A bacteriocin perspective,” Current Opinion in Food Science, vol. 2, pp. 51–57, 2015.
View at: Publisher Site | Google Scholar
J. L. Arqués, E. Rodríguez, S. Langa, J. M. Landete, and M. Medina, “Antimicrobial activity of lactic acid bacteria in dairy products and gut: effect on pathogens,” BioMed Research International, vol. 2015, Article ID 584183, 9 pages, 2015.
View at: Publisher Site | Google Scholar
A. Baños, J. D. García-López, C. Núñez, M. Martínez-Bueno, M. Maqueda, and E. Valdivia, “Biocontrol of Listeria monocytogenes in fish by enterocin AS-48 and Listeria lytic bacteriophage P100,” LWT- Food Science and Technology, vol. 66, pp. 672–677, 2016.
View at: Publisher Site | Google Scholar
D. L. Caly, M. Chevalier, C. Flahaut et al., “The safe enterocin DD14 is a leaderless two-peptide bacteriocin with anti-Clostridium perfringens activity,” International Journal of Antimicrobial Agents, vol. 49, no. 3, pp. 282–289, 2017.
View at: Publisher Site | Google Scholar
A. C. Simonetta, L. G. Moragues De Velasco, and L. N. Frisón, “Antibacterial activity of enterococci strains against Vibrio cholerae,” Letters in Applied Microbiology, vol. 24, no. 2, pp. 139–143, 1997.
View at: Publisher Site | Google Scholar
E. A. Svetoch, B. V. Eruslanov, V. P. Levchulk et al., “Antimicrobial activity of bacteriocin S760 produced by Enterococcus faecium strain LWP760,” Antibiot Khimioter, vol. 56, pp. 3–9, 2011.
View at: Google Scholar
N. S. Ríos Colombo, M. C. Chalón, S. A. Navarro, and A. Bellomio, “Pediocin-like bacteriocins: new perspectives on mechanism of action and immunity,” Current Genetics, vol. 64, no. 2, pp. 345–351, 2018.
View at: Publisher Site | Google Scholar
E. D. Coelho, J. P. Arrais, and J. L. Oliveira, “Fighting fire with fire: Computational prediction of microbial targets for bacteriocins,” in Proceedings of the International Conference on Bioinformatics and Biomedical Engineering, pp. 221–234, Springer, Cham, Switzerland, 2018.
View at: Google Scholar
S. W. Bisset, S.-H. Yang, Z. Amso et al., “Using chemical synthesis to probe structure-activity relationships of the glycoactive bacteriocin glycocin F,” ACS Chemical Biology, vol. 13, no. 5, pp. 1270–1278, 2018.
View at: Publisher Site | Google Scholar
A. Tanhaeian, M. S. Damavandi, D. Mansury, and K. Ghaznini, “Expression in eukaryotic cells and purification of synthetic gene encoding enterocin P: a bacteriocin with broad antimicrobial spectrum,” AMB Express, vol. 9, no. 1, 2019.
View at: Publisher Site | Google Scholar
T. A. Krulwich, G. Sachs, and E. Padan, “Molecular aspects of bacterial pH sensing and homeostasis,” Nature Reviews Microbiology, vol. 9, no. 5, pp. 330–343, 2011.
View at: Publisher Site | Google Scholar
R. W. Hutkins and N. L. Nannen, “pH homeostasis in lactic acid bacteria,” Journal of Dairy Science, vol. 76, no. 8, pp. 2354–2365, 1993.
View at: Publisher Site | Google Scholar
Y. Kakinuma, “Inorganic cation transport and energy transduction in Enterococcus hirae and other streptococci,” Microbiology and Molecular Biology Reviews, vol. 62, no. 4, pp. 1021–1045, 1998.
View at: Google Scholar
T. Nilsen, I. F. Nes, and H. Holo, “Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333,” Applied and Environmental Microbiology, vol. 69, no. 5, pp. 2975–2984, 2003.
View at: Publisher Site | Google Scholar
G. Werner, T. M. Coque, A. M. Hammerum et al., “Emergence and spread of vancomycin resistance among enterococci in Europe,” Euro Surveillance, vol. 13, no. 47, p. 19046, 2008.
View at: Google Scholar
L. M. Teixeira and V. L. C. Merquior, “Enterococcus,” in Molecular Typing in Bacterial Infections, pp. 17–26, Humana Press Inc., Totowa, NJ, USA, 2013.
View at: Google Scholar
L. Mannu, A. Paba, E. Daga et al., “Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin,” International Journal of Food Microbiology, vol. 88, no. 2-3, pp. 291–304, 2003.
View at: Publisher Site | Google Scholar
H. Abriouel, N. B. Omar, A. C. Molinos et al., “Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water and soil, and clinical samples,” International Journal of Food Microbiology, vol. 123, no. 1-2, pp. 38–49, 2008.
View at: Publisher Site | Google Scholar
L. M. Mundy, D. F. Sahm, and M. Gilmore, “Relationships between enterococcal virulence and antimicrobial resistance,” Clinical Microbiology Reviews, vol. 13, no. 4, pp. 513–522, 2000.
View at: Publisher Site | Google Scholar
A. N. Brilliantova, G. A. Kliasova, A. V. Mironova et al., “Spread of vancomycin-resistant Enterococcus faecium in two haematological centres in Russia,” International Journal of Antimicrobial Agents, vol. 35, no. 2, pp. 177–181, 2010.
View at: Publisher Site | Google Scholar
L. M. Perin, R. O. Miranda, S. D. Todorov, B. D. G. D. M. Franco, and L. A. Nero, “Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterococci isolated from goat milk,” International Journal of Food Microbiology, vol. 185, pp. 121–126, 2014.
View at: Publisher Site | Google Scholar
J. Barbosa, P. A. Gibbs, and P. Teixeira, “Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal,” Food Control, vol. 21, no. 5, pp. 651–656, 2010.
View at: Publisher Site | Google Scholar
W. Chajęcka-Wierzchowska, A. Zadernowska, and Ł. Łaniewska-Trokenheim, “Virulence factors of Enterococcus spp. presented in food,” LWT- Food Science and Technology, vol. 75, pp. 670–676, 2017.
View at: Publisher Site | Google Scholar
G. N. Tanih, Genotypic and phenotypic characterization of enterococci from cow dung and environmental water sources in three selected dairy farms [Doctoral dissertation], University of Fort Hare, 2016.
R. V. Vineet and M. Nayak, “Enterococcus faecalis: an enigma in root canal infections,” International Research Journal of Pharmaceutical and Biosciences, vol. 3, no. 1, pp. 12–21, 2016.
View at: Google Scholar
A. M. Guzman Prieto, W. van Schaik, M. R. C. Rogers et al., “Global emergence and dissemination of enterococci as nosocomial pathogens: attack of the clones?” Frontiers in Microbiology, vol. 7, p. 788, 2016.
View at: Google Scholar
I. Gawryszewska, D. Żabicka, W. Hryniewicz, and E. Sadowy, “Linezolid-resistant enterococci in Polish hospitals: species, clonality and determinants of linezolid resistance,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 36, no. 7, pp. 1279–1286, 2017.
View at: Publisher Site | Google Scholar
D. Le Blanc, “Enterococcus,” Prokaryotes, vol. 4, pp. 175–204, 2006.
View at: Google Scholar
M. M. Huycke, C. A. Spiegel, and M. S. Gilmore, “Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis,” Antimicrobial Agents and Chemotherapy, vol. 35, no. 8, pp. 1626–1634, 1991.
View at: Publisher Site | Google Scholar
M. F. Del Papa, L. E. Hancock, V. C. Thomas, and M. Perego, “Full activation of Enterococcus faecalis gelatinase by a C-terminal proteolytic cleavage,” Journal of Bacteriology, vol. 189, no. 24, pp. 8835–8843, 2007.
View at: Publisher Site | Google Scholar
T. J. Eaton and M. J. Gasson, “Molecular screening of enterococcus virulence determinants and potential for genetic exchange between food and medical isolates,” Applied and Environmental Microbiology, vol. 67, no. 4, pp. 1628–1635, 2001.
View at: Publisher Site | Google Scholar
V. Vankerckhoven, T. Van Autgaerden, C. Vael et al., “Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among european hospital isolates of Enterococcus faecium,” Journal of Clinical Microbiology, vol. 42, no. 10, pp. 4473–4479, 2004.
View at: Publisher Site | Google Scholar
P. M. Tendolkar, A. S. Baghdayan, and N. Shankar, “Pathogenic enterococci: New developments in the 21st century,” Cellular and Molecular Life Sciences, vol. 60, no. 12, pp. 2622–2636, 2003.
View at: Publisher Site | Google Scholar
T. F. Araújo and C. L. D. L. F. Ferreira, “The genus enterococcus as probiotic: Safety concerns,” Brazilian Archives of Biology and Technology, vol. 56, no. 3, pp. 457–466, 2013.
View at: Publisher Site | Google Scholar
Y. L. Low, N. S. Jakubovics, J. C. Flatman, H. F. Jenkinson, and A. W. Smith, “Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecafis,” Journal of Medical Microbiology, vol. 52, no. 2, pp. 113–119, 2003.
View at: Publisher Site | Google Scholar
F. Teng, M. Kawalec, G. M. Weinstock, W. Hryniewicz, and B. E. Murray, “An Enterococcus faecium secreted antigen, SagA, exhibits broad-spectrum binding to extracellular matrix proteins and appears essential for E. faecium growth,” Infection and Immunity, vol. 71, no. 9, pp. 5033–5041, 2003.
View at: Publisher Site | Google Scholar
J. Sillanpää, S. R. Nallapareddy, V. P. Prakash et al., “Identification and phenotypic characterization of a second collagen adhesin, Scm, and genome-based identification and analysis of 13 other predicted MSCRAMMs, including four distinct pilus loci, in Enterococcus faecium,” Microbiology, vol. 154, no. 10, pp. 3199–3211, 2008.
View at: Publisher Site | Google Scholar
S. R. Nallapareddy, K. V. Singh, J. Sillanpää et al., “Endocarditis and biofilm-associated pili of Enterococcus faecalis,” The Journal of Clinical Investigation, vol. 116, no. 10, pp. 2799–2807, 2006.
View at: Publisher Site | Google Scholar
P. M. Tendolkar, A. S. Baghdayan, and N. Shankar, “Putative surface proteins encoded within a novel transferable locus confer a high-biofilm phenotype to Enterococcus faecalis,” Journal of Bacteriology, vol. 188, no. 6, pp. 2063–2072, 2006.
View at: Publisher Site | Google Scholar
L. B. Rice, L. Carias, S. Rudin et al., “A potential virulence gene, hylEfm, predominates in Enterococcus faecium of clinical origin,” The Journal of Infectious Diseases, vol. 187, no. 3, pp. 508–512, 2003.
View at: Publisher Site | Google Scholar
J. A. Laverde Gomez, W. van Schaik, A. R. Freitas et al., “A multiresistance megaplasmid pLG1 bearing a hyl_Efm genomic island in hospital Enterococcus faecium isolates,” International Journal of Medical Microbiology, vol. 301, no. 2, pp. 165–175, 2011.
View at: Publisher Site | Google Scholar
S. F. Opera and M. J. Zervos, “Enterococcus and its association with foodborne illness,” in Infectious Disease: Foodborne Diseases, pp. 157–174, Humana Press Inc., Totowa, NJ, USA, 2007.
View at: Google Scholar
J. M. Landete, Á. Peirotén, M. Medina, J. L. Arqués, and E. Rodríguez-Mínguez, “Virulence and antibiotic resistance of enterococci isolated from healthy breastfed infants,” Microbial Drug Resistance, vol. 24, no. 1, pp. 63–69, 2018.
View at: Publisher Site | Google Scholar
R. M. van Harten, R. J. L. Willems, N. I. Martin, and A. P. A. Hendrickx, “Multidrug-resistant enterococcal infections: new compounds, novel antimicrobial therapies?” Trends in Microbiology, vol. 25, no. 6, pp. 467–479, 2017.
View at: Publisher Site | Google Scholar
J. Ch’ng, K. K. Chong, L. N. Lam, J. J. Wong, and K. A. Kline, “Biofilm-associated infection by enterococci,” Nature Reviews Microbiology, vol. 17, no. 2, pp. 82–94, 2019.
View at: Publisher Site | Google Scholar
V. Economou, H. Sakkas, G. Delis, and P. Gousia, “Antibiotic resistance in enterococcus spp. friend or foe?” in Foodborne Pathogens and Antibiotic Resistance, pp. 365–395, John Wiley & Sons, Inc., 2017.
View at: Google Scholar
G. Giraffa, “Enterococci from foods,” FEMS Microbiology Reviews, vol. 26, no. 2, pp. 163–171, 2002.
View at: Publisher Site | Google Scholar
M. Jahan and R. A. Holley, “Transfer of antibiotic resistance from Enterococcus faecium of fermented meat origin to Listeria monocytogenes and Listeria innocua,” Letters in Applied Microbiology, vol. 62, no. 4, pp. 304–310, 2016.
View at: Publisher Site | Google Scholar
F. Lebreton, R. J. L. Willems, and M. S. Gilmore, “Enterococcus diversity, origins in nature, and gut colonization,” in Enterococci: From Commensals to Leading Causes of Drug Resistant Infection, pp. 5–63, Massachusetts Eye and Ear Infirmary, Boston, Mass, USA, 2014.
View at: Google Scholar
C. Franz and W. Holzapfel, “The genus Enterococcus: biotechnological and safety issues,” in Lactic Acid Bacteria. Microbiological and Functional Aspects, pp. 199–248, Marcel Dekker, Inc., New York, NY, USA, 2004.
View at: Google Scholar
A. M. Hammerum, “Enterococci of animal origin and their significance for public health,” Clinical Microbiology and Infection, vol. 18, no. 7, pp. 619–625, 2012.
View at: Publisher Site | Google Scholar
E. Guerrero-Ramos, D. Molina-González, S. Blanco-Morán et al., “Prevalence, antimicrobial resistance, and genotypic characterization of vancomycin-resistant enterococci in meat preparations,” Journal of Food Protection, vol. 79, no. 5, pp. 748–756, 2016.
View at: Publisher Site | Google Scholar
F. M. Aarestrup, P. Butaye, and W. Witte, “Non-human reservoirs of enterococci,” in The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance, pp. 55–100, ASM Press, Washington, DC, USA, 2002.
View at: Google Scholar
M. C. Ronconi, L. A. Merino, and G. Fernández, “Detection of Enterococcus with high-level aminoglycoside and glycopeptide resistance in Lactuca sativa (lettuce),” Enfermedades Infecciosas y Microbiología Clínica, vol. 20, no. 8, pp. 380–383, 2002.
View at: Publisher Site | Google Scholar
C. Bouki, D. Venieri, and E. Diamadopoulos, “Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review,” Ecotoxicology and Environmental Safety, vol. 91, pp. 1–9, 2013.
View at: Publisher Site | Google Scholar
P. S. Coburn, A. S. Baghdayan, G. T. Dolan, and N. Shankar, “Horizontal transfer of virulence genes encoded on the Enterococcus faecalis pathogenicity island,” Molecular Microbiology, vol. 63, no. 2, pp. 530–544, 2007.
View at: Publisher Site | Google Scholar
N. Shankar, A. S. Baghdayan, and M. S. Gilmore, “Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis,” Nature, vol. 417, no. 6890, pp. 746–750, 2002.
View at: Publisher Site | Google Scholar
E. De Leener, A. Martel, E. M. De Graef et al., “Molecular analysis of human, porcine, and poultry Enterococcus faecium isolates and their erm(B) genes,” Applied and Environmental Microbiology, vol. 71, no. 5, pp. 2766–2770, 2005.
View at: Publisher Site | Google Scholar
A. Aguilar-Galvez, R. Dubois-Dauphin, J. Destain, D. Campos, and P. Thonart, “Les entérocoques: avantages et inconvénients en biotechnologie (synthèse bibliographique),” Biotechnolobie, Agrononie, Société et Environnement, vol. 61, no. 1, pp. 67–76, 2012.
View at: Google Scholar
M. Zommiti, M. Cambronel, O. Maillot et al., “Evaluation of probiotic properties and safety of Enterococcus faecium isolated from artisanal Tunisian meat "Dried Ossban",” Frontiers in Microbiology, vol. 9, p. 1685, 2018.
View at: Google Scholar
M. Ziadi, S. Mhir, R. Dubois-Dauphin et al., “Analysis of volatile compounds, amino acid catabolism and some technological properties of enterococcus faecalis strain SLT13 isolated from artisanal Tunisian fermented milk,” British Microbiology Research Journal, vol. 14, no. 1, pp. 1–12, 2016.
View at: Publisher Site | Google Scholar
L. C. Nascimento, S. N. Casarotti, S. D. Todorov, and A. L. Penna, “Probiotic potential and safety of enterococci strains,” Annals of Microbiology, vol. 69, no. 3, pp. 241–252, 2019.
View at: Publisher Site | Google Scholar
N. Van Nguyen, S. Onoda, T. Van Khanh et al., “Evaluation of dietary Heat-killed Lactobacillus plantarum strain L-137 supplementation on growth performance, immunity and stress resistance of Nile tilapia (Oreochromis niloticus),” Aquaculture, vol. 498, pp. 371–379, 2019.
View at: Publisher Site | Google Scholar
Y. Nami, R. Vaseghi Bakhshayesh, H. Mohammadzadeh Jalaly, H. Lotfi, S. Eslami, and M. A. Hejazi, “Probiotic properties of enterococcus isolated from artisanal dairy products,” Frontiers in Microbiology, vol. 10, p. 1685, 2019.
View at: Publisher Site | Google Scholar
C. Chaves-López, A. Serio, C. Rossi, A. Pepe, E. Compagnone, and A. Paparella, “Interaction between galactomyces geotrichum KL20B, lactobacillus plantarum LAT3 and Enterococcus faecalis KE06 during milk fermentation,” Fermentation, vol. 3, no. 4, p. 52, 2017.
View at: Publisher Site | Google Scholar
M. Olvera-García, A. Sanchez-Flores, and M. Quirasco Baruch, “Genomic and functional characterisation of two Enterococcus strains isolated from Cotija cheese and their potential role in ripening,” Applied Microbiology and Biotechnology, vol. 102, no. 5, pp. 2251–2267, 2018.
View at: Publisher Site | Google Scholar
A. Ghosh, L. Borst, S. H. Stauffer et al., “Mortality in kittens is associated with a shift in ileum mucosa-associated enterococci from enterococcus hirae to biofilm-forming enterococcus faecalis and adherent escherichia coli,” Journal of Clinical Microbiology, vol. 51, no. 11, pp. 3567–3578, 2013.
View at: Publisher Site | Google Scholar
K. Jeevaratnam and V. Nallala, “Probiotic evaluation of Enterococcus durans VJI19 isolated from gastrointestinal tract of broiler chicken,” International Journal of Advanced Life Sciences, vol. 10, no. 1, pp. 139–155, 2017.
View at: Publisher Site | Google Scholar
L. Avram-Hananel, J. Stock, A. Parlesak, C. Bode, and B. Schwartz, “Edurans strain M4-5 isolated from human colonic flora attenuates intestinal inflammation,” Diseases of the Colon & Rectum, vol. 53, no. 12, pp. 1676–1686, 2010.
View at: Publisher Site | Google Scholar
W. F. van Zyl, S. M. Deane, and L. M. T. Dicks, “Enterococcus mundtii ST4SA and Lactobacillus plantarum 423 excludes Listeria monocytogenes from the GIT, as shown by bioluminescent studies in mice,” Beneficial Microbes, vol. 7, no. 2, pp. 227–235, 2016.
View at: Publisher Site | Google Scholar
H. Liu, L. Zhang, H. Yi et al., “A novel enterocin T1 with anti-Pseudomonas activity produced by Enterococcus faecium T1 from Chinese tibet cheese,” World Journal of Microbiology and Biotechnology, vol. 32, no. 2, p. 21, 2016.
View at: Publisher Site | Google Scholar
S. Pieniz, R. Andreazza, T. Anghinoni, F. Camargo, and A. Brandelli, “Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s,” Food Control, vol. 37, no. 1, pp. 251–256, 2014.
View at: Publisher Site | Google Scholar
A. Vimont, B. Fernandez, R. Hammami, A. Ababsa, H. Daba, and I. Fliss, “Bacteriocin-producing Enterococcus faecium LCW 44: A high potential probiotic candidate from raw camel milk,” Frontiers in Microbiology, vol. 8, p. 865, 2017.
View at: Google Scholar
Y. Nami, N. Abdullah, B. Haghshenas, D. Radiah, R. Rosli, and A. Y. Khosroushahi, “Probiotic assessment of Enterococcus durans 6HL and lactococcus lactis 2HL isolated from vaginal microflora,” Journal of Medical Microbiology, vol. 63, no. 8, pp. 1044–1051, 2014.
View at: Publisher Site | Google Scholar
A. Anadón, M. Rosa Martínez-Larrañaga, and M. Aranzazu Martínez, “Probiotics for animal nutrition in the European Union. Regulation and safety assessment,” Regulatory Toxicology and Pharmacology, vol. 45, no. 1, pp. 91–95, 2006.
View at: Publisher Site | Google Scholar
S. F. Liao and M. Nyachoti, “Using probiotics to improve swine gut health and nutrient utilization,” Animal Nutrition, vol. 3, no. 4, pp. 331–343, 2017.
View at: Publisher Site | Google Scholar
S. Sukegawa, Y. Ihara, K. Yuge et al., “Effects of oral administration of heat-killed Enterococcus faecium strain NHRD IHARA in post-weaning piglets,” Animal Science Journal, vol. 85, no. 4, pp. 454–460, 2014.
View at: Google Scholar
G. T. Cao, X. F. Zeng, A. G. Chen et al., “Effects of a probiotic, Enterococcus faecium, on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88,” Poultry Science, vol. 92, no. 11, pp. 2949–2955, 2013.
View at: Publisher Site | Google Scholar
A. Zheng, J. Luo, K. Meng et al., “Probiotic (Enterococcus faecium) induced responses of the hepatic proteome improves metabolic efficiency of broiler chickens (Gallus gallus),” BMC Genomics, vol. 17, no. 1, p. 89, 2016.
View at: Google Scholar
R. S. Kumar, P. Kanmani, N. Yuvaraj, K. A. Paari, V. Pattukumar, and V. Arul, “Purification and characterization of enterocin MC13 produced by a potential aquaculture probiont Enterococcus faecium MC13 isolated from the gut of Mugil cephalus,” Canadian Journal of Microbiology, vol. 57, no. 12, pp. 993–1001, 2011.
View at: Publisher Site | Google Scholar
L. Román, D. Padilla, F. Acosta et al., “The effect of probiotic Enterococcus gallinarum L-1 on the innate immune parameters of outstanding species to marine aquaculture,” Journal of Applied Animal Research, vol. 43, no. 2, pp. 177–183, 2015.
View at: Publisher Site | Google Scholar
C. A. Arias and B. E. Murray, “The rise of the Enterococcus: beyond vancomycin resistance,” Nature Reviews Microbiology, vol. 10, no. 4, pp. 266–278, 2012.
View at: Publisher Site | Google Scholar
S. F. Oprea and M. J. Zervos, “Enterococcus and its association with foodborne illness,” in Foodborne Diseases, pp. 157–174, Humana Press Inc., 2007.
View at: Google Scholar
H. Riemann and F. L. Bryan, Foodborne Infections and Intoxications, Academic, New York, NY, USA, 1979.
G. Werner, “Current trends of emergence and spread of vancomycin‐resistant enterococci,” in Antibiotic resistant bacteria: A continuous challenge in the New Millennium, pp. 303–354, InTech, Rijeka, Croatia, 2012.
View at: Google Scholar
E. Guerrero-Ramos, J. Cordero, D. Molina-González et al., “Antimicrobial resistance and virulence genes in enterococci from wild game meat in Spain,” Food Microbiology, vol. 53, pp. 156–164, 2016.
View at: Publisher Site | Google Scholar
A. Rehaiem, Z. B. Belgacem, M. R. Edalatian et al., “Assessment of potential probiotic properties and multiple bacteriocin encoding-genes of the technological performing strain Enterococcus faecium MMRA,” Food Control, vol. 37, no. 1, pp. 343–350, 2014.
View at: Publisher Site | Google Scholar
FAO/WHO, “Guidelines for the evaluation of probiotics in food,” Tech. Rep., Food and Health Agricultural Organisation of the United Nations d World Health Organisation (Working group report), 2002.
View at: Google Scholar

Copyright

Copyright © 2019 Olfa Ben Braïek and Slim Smaoui. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

11139

Downloads

3778

Citations