Review
Functionality of enterococci in dairy products

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Abstract

Enterococci have important implications in the dairy industry. They occur as nonstarter lactic acid bacteria (NSLAB) in a variety of cheeses, especially artisan cheeses produced in southern Europe from raw or pasteurised milk, and in natural milk or whey starter cultures. They play an acknowledged role in the development of sensory characteristics during ripening of many cheeses and have been also used as components of cheese starter cultures. The positive influence of enterococci on cheese seems due to specific biochemical traits such as lipolytic activity, citrate utilisation, and production of aromatic volatile compounds. Some enterococci of dairy origin have also been reported to produce bacteriocins (enterocins) inhibitory against food spoilage or pathogenic bacteria, such as Listeria monocytogenes, Staphylococcus aureus, Vibrio cholerae, Clostridium spp., and Bacillus spp. The technological application of enterocins, shown to be produced during cheese manufacture, led to propose enterococci as adjunct starter or protective cultures in cheeses. There is evidence that enterococci, either added as adjunct starters or present as nonstarter NSLAB, could find potential application in the processing of some fermented dairy products. Literature suggest that the complex biochemical and ecological phenomena explaining the technological functionality of the enterococci in dairy products, are still to be fully understood. Clearly, the clinical research on enterococci underlines also that the safety of dairy products containing enterococci is an issue that the industry must carefully address before proceeding to their application.

Introduction

Bacteria of the genus Enterococcus, or enterococci (formerly the “faecal” or Lancefield group D streptococci) are ubiquitous Gram-positive, catalase-negative cocci that often occur in large numbers in vegetables, plant material, and foods, especially those of animal origin such as dairy products Giraffa et al., 1997, Franz et al., 1999. Currently, the genus Enterococcus includes more than 20 species, with Enterococcus faecium and Enterococcus faecalis being the two species mostly found, especially in food and related habitats. However, the identification of the enterococci has always been problematic. Numerous enterococcal isolates, especially from 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 Devriese et al., 1993, Ulrich and Muller, 1998, Giraffa, 1999.

Enterococci constitute a large proportion of the autochthonous bacteria associated with the mammalian gastrointestinal tract. Once released in the environment by means of human faeces or animal dejection, they are able to colonise diverse niches because of their exceptional aptitude to resist or grow in hostile extra-enteric 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.g. milk and meat) and multiply in these materials during fermentation because of their ability to survive to adverse environmental conditions such as extreme pH, temperatures, and salinity. This means that these bacteria could withstand normal conditions of food production. They can also contaminate finished products during food processing. Therefore, enterococci can become an important part of the fermented food (especially fermented meats and cheeses) microflora.

Section snippets

Presence in milk and starter cultures

The reason for the prevalence of enterococci in dairy products has long been considered as a result of unhygienic conditions during the production and processing of milk. However, their presence in foods has often been shown to be unrelated with direct faecal contamination. Enterococci may enter the milk either directly from human or animal faeces or indirectly from contaminated water sources, exterior of the animal and/or from the milking equipment and bulk storage tank. Due to their

Acidifying activity

Considerable work on acid production of Enterococcus species in milk has been reported. In general, enterococci exhibit low milk acidifying ability. Morea et al. (1999) showed that the pH of milk 24 h after inoculation with strains isolated from Mozzarella cheese did not drop below 5.5. Recent investigations on enterococci of dairy origin confirmed the poor acidifying capacity of these microorganisms in milk with only a small percentage of the strains showing a pH below 5.0–5.2 after 16–24 h of

Enterococci as starter cultures

The finding of strains with good acidifying and/or proteolytic properties within E. faecium and E. faecalis isolated from various cheeses Wessels et al., 1990, Centeno et al., 1999, Suzzi et al., 2000 and the frequent isolation of enterococci from natural starter cultures used for the manufacture of artisan cheeses Gatti et al., 1994, Villani and Coppola, 1994, Giraffa et al., 1997 encouraged some applications of these microorganisms as primary starter cultures. However, from the early works on

Future trends and final considerations

There seems to be positive evidence that enterococci can find application in cheese. Some well defined strains with a long history of safe use as probiotics are also known. In addition, enterococci could play a beneficial role in the biopreservation or as starter adjuncts to improve the organoleptic characteristics of different cheeses. However, literature data seem to suggest that the a complete picture of the complex biochemical and ecological phenomena explaining the functionality of the

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