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      Biogenic Amine Production by Lactic Acid Bacteria: A Review

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          Abstract

          Lactic acid bacteria (LAB) are considered as the main biogenic amine (BA) producers in fermented foods. These compounds derive from amino acid decarboxylation through microbial activities and can cause toxic effects on humans, with symptoms (headache, heart palpitations, vomiting, diarrhea) depending also on individual sensitivity. Many studies have focused on the aminobiogenic potential of LAB associated with fermented foods, taking into consideration the conditions affecting BA accumulation and enzymes/genes involved in the biosynthetic mechanisms. This review describes in detail the different LAB (used as starter cultures to improve technological and sensorial properties, as well as those naturally occurring during ripening or in spontaneous fermentations) able to produce BAs in model or in real systems. The groups considered were enterococci, lactobacilli, streptococci, lactococci, pediococci, oenococci and, as minor producers, LAB belonging to Leuconostoc and Weissella genus. A deeper knowledge of this issue is important because decarboxylase activities are often related to strains rather than to species or genera. Moreover, this information can help to improve the selection of strains for further applications as starter or bioprotective cultures, in order to obtain high quality foods with reduced BA content.

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          Biogenic amines: their importance in foods.

          Biogenic amines are important nitrogen compounds of biological importance in vegetable, microbial and animal cells. They can be detected in both raw and processed foods. In food microbiology they have sometimes been related to spoilage and fermentation processes. Some toxicological characteristics and outbreaks of food poisoning are associated with histamine and tyramine. Secondary amines may undergo nitrosation and form nitrosamines. A better knowledge of the factors controlling their formation is necessary in order to improve the quality and safety of food.
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            Enterococci as probiotics and their implications in food safety.

            Enterococci belong to the lactic acid bacteria (LAB) and they are of importance in foods due to their involvement in food spoilage and fermentations, as well as their utilisation as probiotics in humans and slaughter animals. However, they are also important nosocomial pathogens that cause bacteraemia, endocarditis and other infections. Some strains are resistant to many antibiotics and possess virulence factors such as adhesins, invasins, pili and haemolysin. The role of enterococci in disease has raised questions on their safety for use in foods or as probiotics. Studies on the incidence of virulence traits among enterococcal strains isolated from food showed that some can harbour virulence traits, but it is also thought that virulence is not the result of the presence of specific virulence determinants alone, but is rather a more intricate process. Specific genetic lineages of hospital-adapted strains have emerged, such as E. faecium clonal complex (CC) 17 and E. faecalis CC2, CC9, CC28 and CC40, which are high risk enterococcal clonal complexes. These are characterised by the presence of antibiotic resistance determinants and/or virulence factors, often located on pathogenicity islands or plasmids. Mobile genetic elements thus are considered to play a major role in the establishment of problematic lineages. Although enterococci occur in high numbers in certain types of fermented cheeses and sausages, they are not deliberately added as starter cultures. Some E. faecium and E. faecalis strains are used as probiotics and are ingested in high numbers, generally in the form of pharmaceutical preparations. Such probiotics are administered to treat diarrhoea, antibiotic-associated diarrhoea or irritable bowel syndrome, to lower cholesterol levels or to improve host immunity. In animals, enterococcal probiotics are mainly used to treat or prevent diarrhoea, for immune stimulation or to improve growth. From a food microbiological point of view, the safety of the bacteria used as probiotics must be assured, and data on the major strains in use so far indicate that they are safe. The advantage of use of probiotics in slaughter animals, from a food microbiological point of view, lies in the reduction of zoonotic pathogens in the gastrointestinal tract of animals which prevents the transmission of these pathogens via food. The use of enterococcal probiotics should, in view of the development of problematic lineages and the potential for gene transfer in the gastrointestinal tract of both humans and animals, be carefully monitored, and the advantages of using these and new strains should be considered in a well contemplated risk/benefit analysis. Copyright © 2011 Elsevier B.V. All rights reserved.
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              The role and application of enterococci in food and health.

              The genus Enterococcus is the most controversial group of lactic acid bacteria. Studies on the microbiota of many traditional cheeses in the Mediterranean countries have indicated that enterococci play an important role in the ripening of these cheeses, probably through proteolysis, lipolysis, and citrate breakdown, hence contributing to their typical taste and flavour. Enterococci are also present in other fermented foods, such as sausages and olives. However, their role in these products has not been fully elucidated. Furthermore, the production of bacteriocins by enterococci is well documented. Moreover, enterococci are nowadays used as probiotics. At the same time, however, enterococci have been associated with a number of human infections. Several virulence factors have been described and the number of vancomycin-resistant enterococci is increasing. The controversial nature of enterococci has prompted an enormous increase in scientific papers and reviews in recent years, where researchers have been divided into two groups, namely pro and contra enterococci. To the authors' impression, the negative traits have been focused on very extensively. The aim of the present review is to give a balanced overview of both beneficial and virulence features of this divisive group of microorganisms, because it is only acquaintance with both sides that may allow their safe exploitation as starter cultures or co-cultures.
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                Author and article information

                Journal
                Foods
                Foods
                foods
                Foods
                MDPI
                2304-8158
                07 January 2019
                January 2019
                : 8
                : 1
                : 17
                Affiliations
                [1 ]Interdepartmental Center for Industrial Agri-Food Research, University of Bologna, 47521 Cesena, Italy; federica.barbieri16@ 123456unibo.it (F.B.); chiara.montanari8@ 123456unibo.it (C.M.); fausto.gardini@ 123456unibo.it (F.G.)
                [2 ]Department of Agricultural and Food Sciences, University of Bologna, 40126 Bologna, Italy
                Author notes
                [* ]Correspondence: giulia.tabanelli2@ 123456unibo.it ; Tel.: +39-347-032-8294
                Author information
                https://orcid.org/0000-0002-8693-1716
                Article
                foods-08-00017
                10.3390/foods8010017
                6351943
                30621071
                2d6acdaa-8d23-4817-9994-7848c649b0a0
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 26 November 2018
                : 02 January 2019
                Categories
                Review

                biogenic amines,decarboxylase enzymes,lactic acid bacteria,starter cultures

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