Some enterococci of food origin produce bacteriocins that exert anti-Listeria activity. Enterococci are used as probiotics to improve the microbial balance of the. Enterococci can cause food intoxication through production of biogenic amines and can be a reservoir for .. Enterococci at the crossroads of food safety. C. M. A. P. Franz, W. H. Holzapfel and M. E. Stiles, “Enterococci at the Crossroads of Food Safety” International Journal of Food Microbiology, Vol. 47, No.
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Enterococci have recently emerged as nosocomial pathogens. Their ubiquitous nature determines their frequent finding in foods as contaminants. In addition, the notable resistance of enterococci to adverse environmental conditions explains their ability to colonise different ecological niches and their spreading within the food chain through contaminated animals and foods.
Enterococci can also contaminate finished products, such as fermented foods and, for this reason, their presence in many foods such as cheeses and fermented sausages can only be limited but not completely eliminated using traditional processing technologies. Enterococci are low grade pathogens but their intrinsic resistance to many antibiotics and their acquisition of resistance to the few antibiotics available for treatment in clinical therapy, such as the glycopeptides, have led to difficulties and a search for new drugs and therapeutic options.
Enterococci can cause food intoxication through production of biogenic amines and can be a reservoir for worrisome opportunistic infections and for virulence traits.
Clearly, there is no consensus on the acceptance of their presence in foodstuffs and their role as primary pathogens is still a question mark. In this review, the following topics will be covered: Because of their high heat tolerance and survival under adverse environmental conditions, enterococci can colonise diverse niches and may then serve as indicators of the sanitary quality of food.
Indeed, enterococci commonly occur in large numbers in vegetables, plant material and foods, especially those of animal origin such as fermented sausages and cheeses. In processed meats, enterococci are generally not desirable because they cause spoilage. On the contrary, enterococci have important implications in the dairy industry. They play an acknowledged role in the development of organoleptic characteristics during the ripening of many cheeses and they have been also used as components of cheese starter cultures .
Some enterococci of food origin also share a number of useful biotechnological traits e. Unfortunately, enterococci have recently assumed major importance in clinical microbiology as well. Enterococci have traditionally been regarded as low-grade pathogens. However, there is no consensus on the significance of their presence in foodstuffs. Their newly accentuated ambiguity concerning the relationships of enterococci with human beings is related to their enteric habitattheir entering the food chain, their antibiotic resistance and their possible involvement in food-borne illnesses due to the presence of virulence factors, such as the production of adhesins and aggregation substances.
Over the last two decades, enterococci have emerged as important hospital-acquired pathogens in immune-suppressed patients and intensive-care units. The rise in hospital-acquired enterococcal infections has been in part due to the increased use of broad-spectrum antibiotics and the rising number of severely ill patients. Enterococci are not only intrinsically resistant to several antibiotics, but are also characterised by a potent and unique ability to exchange genetic material.
The increasing prevalence of strains resistant to ampicillin, aminoglycosides and glycopeptides and the acquisition of resistance to the few antibiotics available for treatment such as vancomycin pose serious difficulties in clinical therapy.
In addition, selective pressure exerted by the use of antibiotics as growth promoters in food animals appears to have created large reservoirs of transferable antibiotic resistance in various ecosystems.
With the emergence of glycopeptide resistance in Enterococcus faecium outside hospitals, a large reservoir of transferable resistance vanA gene cluster was identified in animal husbandry due to the use of avoparcin as a feed additive.
The spread of resistance, which enters the human enterococcal flora via the food chain, and the transfer of this trait to pathogenic species i. Therefore, the barrier separating enterococci as inoffensive contaminants from pathogens appears most fragile. The identification of the enterococci has always been problematic.
Numerous enterococcal isolates, especially from an environmental source, often remain unidentified when their identification is based on phenotypic traits alone. It is difficult to unequivocally categorise isolates into one of the Enterococcus species by physiological tests because heterogeneity in phenotypic features is very high, regardless of the origin of the isolate [ 2—5 ]. The problem with the taxonomy of enterococci is generally that they are a heterogeneous group of Gram-positive cocci sharing many characteristics with the genera Streptococcus and Lactococcus.
On the basis of 16S rRNA cataloguing, the genus Streptococcus was separated during the s into the three genera Enterococcus, Lactococcus and Streptococcus. Since this transfer, the total number of species presently included in the Enterococcus genus on the basis of chemotaxonomic and phylogenetic studies is This situation continues to fluctuate from time to time as individual species are moved into other genera or new taxa are discovered.
Enterococci at the crossroads of food safety? 
More recently, other species of enterococci have been proposed on the basis of chemotaxonomic studies and phylogenetic evidence provided by 16S rDNA sequencing [ 78 ]. It is highly probable that phylogenetic system of the genus Enterococcus has not yet been completely elucidated and that some re-classifications may be necessary in the near future. Over the last two decades, enterococci, formerly viewed as organisms of minimal clinical impact, have emerged as important hospital-acquired pathogens in immunosuppressed patients and intensive care units.
Enterococci do not possess the common virulence factors found in many other bacteria, but they have a number of other characteristics, e. Foodborne enterococci have not yet been clearly involved as direct causes of clinical infections .
In this context, reports of hospital-acquired infections attributed to enterococci are difficult to interpret because these bacteria are generally identified in mixed cultures with other primary pathogens, such as staphylococci and others .
Enterococci have been implicated in cases of food poisoning, e. Enterococci are now among the most common nosocomial pathogens; they have been implicated as an important cause of endocarditis, bacteraemia, urinary tract, central nervous system, intra-abdominal and pelvic infections . Epidemiological data also indicate that E. In addition, there is strong evidence that enterococci causing bacteraemias commonly originate from the urinary tract.
In addition to these well-documented infections, the incidence of intra-abdominal infections caused by vancomycin-resistant enterococci is increasing . Enterococci may also contribute to cause abdominal and pelvic abscess formation and sepsis . The clinical significance of enterococci in human infections is poorly understood because of the scarcity of well-documented reports confirming their occurrence in mixed cultures.
The increasing resistance of enterococci to antibiotics and the presence of active mechanisms of gene transfer are exacerbating the increasing findings of these bacteria as nosocomial opportunists. However, the antibiotic resistance alone cannot explain the virulence of these bacteria in the absence of pathogenicity factors. Virulence traits in enterococci include adherence to host tissue, invasion and abscess formation, resistance to and modulation of host defense mechanisms, secretion of cytolysins and other toxic products and production of plasmid-encoded pheromones [ 121421 ].
A number of genes encoding for virulence factors especially in E. Recent molecular screenings of Enterococcus virulence determinants indicated that medical E. Many of these enterococcal virulence traits, such as haemolysin—cytolysin production, the adhesion ability and the antibiotic resistance see laterhave been shown to be transmissible by gene transfer mechanisms [ 23—26 ].
Often, the same plasmid may encode a sex pheromone response and either antibiotic resistance or haemolysin production genes [ 122627 ]. The exchange of genetic material in E. In a recent study, multiple pheromone-encoding genes were identified in both clinical and food enterococcal strains, indicating the potential of these latter to acquire other sex pheromone plasmids.
Trans-conjugation in which starter strains acquired virulence determinants from medical strains was also demonstrated . Sex pheromones are also thought to act as virulence factors by eliciting an inflammatory host response [ 28—30 ].
Virulence of enterococci is strongly enhanced by their frequent resistance to commonly used antibiotics. Antibiotic resistance, which can be both intrinsic and acquired, makes enterococci effective opportunists in nosocomial infections.
Intrinsic resistance to many antibiotics suggests that treatment of infection could be difficult. In addition to these constitutive resistances, enterococci have acquired genetic determinants that confer resistance to all classes of antimicrobials, including chloramphenicol, tetracyclines and glycopeptides.
The major risk related to these latter resistance traits is that they are for the most part transferable. The genes coding for all of these antibiotic-resistant traits may be transferred by pheromone-mediated, conjugative often multiresistant plasmids or transposons to both enterococci and more virulent pathogens, such as S. Within acquired antibiotic resistances, vancomycin-resistant enterococci VRE are possibly the most serious concern that has recently emerged in human clinical infections.
Two distinct forms of transferable vancomycin-resistant phenotypes have been described in enterococci: Enterococci can be readily isolated from foods, including a number of traditional fermented foods.
Enterococci at the crossroads of food safety? – Semantic Scholar
A clear picture of the microbial ecology of these bacteria easily explains their presence in foods. Enterococci constitute a large proportion of the autochthonous bacteria associated with the mammalian gastrointestinal if. Once rejected from the environment by means of human faeces or animal ejecta, they are able to colonise enterocodci niches because of their exceptional aptitude to resist or grow in hostile environments. Therefore, enterococci are not only associated with warm-blooded animals, but they also occur in soil, surface waters and on plant and vegetables.
By intestinal or environmental contamination they can then colonise raw foods e. They can also contaminate finished products during food processing. Therefore, many fermented foods made from meat and milk especially fermented meats and cheeses contain enterococci.
A wide variety of fermented meat products is produced in many parts of the world. In Europe the saftey types are Italian salami and German raw sausage with numerous entedococci and regional variants. The technology for the production of most of these products is essentially similar.
After a period of fermentation to biologically stabilise the product, processed meats are typically salted or smoked, and for the most part eaten raw . It was therefore suggested that a proper heat treatment during processing, such as in the case of cooked, unfermented meats, etnerococci be necessary to eliminate enterococci as spoilage microflora in fermented meats . In many cases, however, enterococci are a spoilage problem also in cooked, processed meats because they are foov to survive heat processing, especially if initially present in high numbers .
To this regard, both Crossrods. Gordon and Ahmad  stated that E. Therefore, the presence of enterococci in fermented or non-fermented meat products appears unavoidable by present day applied technologies. The presence of enterococci in dairy products has long been considered an indication of insufficient sanitary conditions during the production and processing of milk.
To the contrary, many authors suggest that certain strains of enterococci in some cheeses may be highly desirable on the basis of their positive contribution to flavour development during the cheese ripening. This beneficial role led to the inclusion of enterococcal strains in certain starter cultures.
Enterococci occur in a variety of cheeses, especially artisanal cheeses produced in southern Europe enterococci raw or pasteurised milk, and in natural milk starters. The isolation of enterococci from natural milk starter cultures, which are still widely used for many Italian soft cheeses made with raw or pasteurised milk, can be explained by their thermal resistance.
The presence of enterococci in pasteurised cheeses is generally due to recontamination after the heat treatment and to entterococci heat resistance. The recovery and persistence of the enterococci in some cheeses during ripening can be attributed to their wide range of growth temperatures and their tolerance to pH and salt. Clearly, the presence of enterococci is ineluctable also in many dairy products.
The croasroads high level of antibiotic resistance observed in enterococci and their widespread finding in raw foods are two key elements contributing to the frequent recovery of antibiotic-resistant enterococci ARE in both unfermented and fermented foods.
ARE have been found in meat products, dairy products, ready-to-eat foods and even within enterococcal strains proposed as probiotics [ 3640—44 ]. In previous studies fodo European cheeses, enterococci mainly belonging to E. Although ARE are found in both pasteurised and, to a much higher extent, raw milk cheeses, their presence in these latter products may represent a more serious risk of expanding antibiotic resistance through the food chain. Strains with high-level resistance to kanamycin and gentamicin were recently isolated from French raw milk cheeses and hospitalised patients .
The same picture emerges from data on meat products. Enterococci resistant to one or more antibiotics including bacitracin, chloramphenicol, erythromycin, gentamicin, penicillin, rifampicin, streptomycin and tetracycline were isolated from minced meat, raw meat crossrkads, ham and tenderloin beef [ 3642 ofod.
The overall data on antibiotic resistance within food-associated enterococci open the question of their entering the food chain. There is strong epidemiological evidence of a link between the use of antibiotics in human medicine and animal husbandry and the emergence, spreading and persistence of resistant strains in animal products enterococfi 4647 ].