Starter Cultures in Foods: History
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Subjects: Veterinary Sciences
Contributor:
Juan García-Díez

Starter cultures can be defined as preparations with a large number of cells that include a single type or a mixture of two or more microorganisms that are added to foods in order to take advantage of the compounds or products derived from their metabolism or enzymatic activity.

  • starter cultures
  • foodborne pathogens
  • fermented meats

1. Introduction

Starter cultures can be defined as preparations with a large number of cells, either of a single type or a mixture of two or more microorganisms that are added to foods in order to take advantage of the compounds or products derived from their metabolism or enzymatic activity [1].

Since starter cultures are used to perform fermentation processes in food production, its use is a common practice in the food industry worldwide. This has resulted in the commercialisation of several products such as bioprotective cultures, starters or probiotics aimed to provide foods with specific sensory and nutritional characteristics, potential health benefits and guarantee food safety [2].

Starter cultures are used in a wide range of food industries such as the dairy industry for cheese, yogurt and other fermented dairy products’ manufacture [3], the meat industry, mainly for sausage manufacture [4], alcohol production for the beer and wine industry [5][6], vinegar production [7], preparation of oriental products based on rice and soy [8], baking, fermented cereals [9] and production of fermented fruits and vegetables [10][11][12]. Since starter cultures are adapted to the substrates, they allow us control of the fermentation process to obtain predictable results [13].

The most promising microorganisms selected as starter culture are those that are isolated from the native microbiota of traditional products [14] since they are well adapted to the environmental conditions of food and are capable of controlling spoilage and pathogenic microbiota of food [15].

To select a microorganism(s) as a starter or starter culture, it is necessary to carry out a proper study regarding its metabolism and activities, since in some cases, its effects and/or properties may vary between laboratory conditions and food products [16]. Also, starter culture must be recognised as safe, capable of being produced on a large scale and remain viable and stable during storage [17].

Microorganisms used as starter cultures are bacteria, moulds and yeast. Within the group of bacteria, lactic acid bacteria (LAB) are the most representative group, being used in fermentation processes of meat and dairy products [18]. In addition, other bacterial groups such as Gram-positive, catalase-positive cocci, mainly coagulase-negative staphylococci (CNS), and Micrococcaceae are also used [19][20]. Yeasts are mainly used for the fermentation of alcoholic beverages [21], with wine and beer production being the most representative. Regarding starter moulds, they are used to obtain fermented vegetable products, cheeses and meat products [22].

2. Use of Starter Cultures to Improve the Food Safety in Fermented Meat Products

Fermented meat products represent the oldest known way of preserving meat to achieve a microbiologically stable product with particular sensory characteristics that can be kept for several months [23]. Fermented meat sausages are products that are made with minced meat and fat mixed with salt, spices and authorised additives which are mixed and stuffed into natural or artificial casings and subjected to a drying process in which a microbial fermentation takes place, resulting in a drop of pH and water activity (aW) levels [24]. Traditionally, the fermentation process of these meat products is developed by the natural microbiota existing in meat. However, the use of commercial starter cultures is currently widespread in the meat industry. Starter cultures can be defined as microorganisms selected according to their specific properties that are added to meat batter to improve some characteristics such as appearance, texture, aroma and flavour. Use of starter cultures enables homogenisation of production and avoids possible defects. In addition, they improve the safety of fermented meat products by production of several compounds such as lactic acid, acetic acid, propionic acid, benzoic acid, hydrogen peroxide or bactericidal proteins (i.e., bacteriocins), among others [25]. Thus, starter cultures become the predominant microbiota, directing the fermentation and excluding the undesirable flora, decreasing hygienic and manufacturing risks due to deficiencies of microbial origin.

Regarding organic acids, they inhibit spoilage and foodborne pathogens mainly by reduction of pH. The acid environment interferes with the maintenance of the cell membrane that alters both the structure and functionality, leading to cell death. The antimicrobial effect of organic acids in food has been investigated [26][27][28]. Thus, acetic acid is used to inhibit the growth of both Gram-positive and Gram-negative bacteria, yeasts and fungi. Its inhibitory effect is more pronounced at low pH and presented special importance in fermented vegetables and vinegar industry but is less interesting in foods of animal origin [29]. Benzoic acid occurs naturally in fermented milk products (e.g., kefir, yogurt), produced by microorganisms such as Lactobacillus acidophilus, Lacticaseibacillus casei or Lactobacillus helveticus [30]. Its antimicrobial effect against Staphylococcus aureus and Pseudomonas has been recently evaluated [31]. Antimicrobial effect of diacetyl, acetic acid and propionic acid against Salmonella typhimurium, Escherichia coli, S. aureus and Listeria monocytogenes has also been evaluated [32][33]. Regarding phenyllactic acid, produced by several LAB genera [34], it displayed both bactericidal (against L. monocytogenes and S. aureus) [35] and antifungal effects [36]. As described, the organic acids produced by LAB contribute to the safety of foods by creating an adverse environment (by low pH) that interferes in the cell membrane permeability. However, it is important to highlight that research about the antimicrobial effect of these organic acids has been carried out by addition as a “natural additive” and not during fermentation processes in foods. Indeed, based on the low quantity of organic acid produced [30], the inhibitory effect of these organic acids may result from the synergistic action together with other metabolites produced by starters and not by the individual action of each one [37].

There are many microbial genera used as starter cultures for fermented meat products. Although the most used belong to the group of lactic acid bacteria and Gram-positive catalase-positive cocci (GCC+), mainly represented by Staphylococcus spp. and Kocuria spp. [4], other starter cultures belong Lactococcus spp., Leuconostoc spp., Enterococcocus spp. and Pediococcus spp. are also used [13]. Moreover, yeast and moulds, that confer specific sensory characteristics, are also added as starter cultures. Starter yeast and moulds are mainly represented by Debaromyces spp. and Aspergillus spp., respectively. Moulds, since they are aerobic, are used as surface microbiota aimed to improve particular sensory and external characteristics.

Regarding food safety, fermented meat products are considered as safe products due to the development of unfavourable or inhibitory conditions to the growth of spoilage and/or pathogenic microorganisms. Low values of pH and aW, presence of salt, nitrites, spices and other ingredients, called hurdle technology, are responsible for the pathogenic and spoilage microorganism inhibition [38]. But these hurdles, in some cases, are not enough, and foodborne pathogens can survive, causing outbreaks [39].

Thus, some industrial practices such as the reduction of fermentation times to increase the production yield, slicing, decreased salt content or decrease/absence of nitrites allow conditions for the survival of foodborne pathogens [40][41][42][43]. In addition, low initial natural microbial load of meat batter for fermented sausage manufacture may pose a risk for pathogen multiplication due to the reduced competition [44]. In this context, starter cultures present a key role in the guarantee of the safety of these products. Starter cultures are also used in combination with other techniques (e.g., essential oils, packaging) to improve its efficiency, guaranteeing the food safety [45].

2.1. Antimicrobial Effect of Selected Starter Cultures Against Foodborne Pathogens

LAB represent the main starter cultures used in the meat industry. Its antimicrobial effect has already been described decades ago, not only based on the reduction of the pH derived from the transformation of sugar into lactic acid but also by the competitive effect against natural microbiota, production of other organic acids (e.g., lactic acid, acetic acid, propionic acid, benzoic acid), hydrogen peroxide, enzymes or bactericidal peptides called bacteriocins [46], for which the action mechanism has been described elsewhere [4].

The antimicrobial effect of organic acids lies in the reduction of pH and in the action of undissociated acid molecules. Also, low pH facilitates the diffusion of organic acids across the cell membrane, collapsing the electrochemical proton gradient, affecting the cell membrane permeability and leading to the cell death [47]. Bacteriocins, most of them produced by LAB, are peptides or proteins of low molecular weight, synthesised in the ribosomes of the producer bacteria. Most bacteriocins act on the cellular membrane, destabilising and permeabilising through the formation of ionic channels or pores, which will release compounds such as phosphate, potassium, amino acids and adenosine triphosphate (ATP), decreasing the synthesis of macromolecules and consequently, cell death [48].

As previously discussed, starter cultures improve the safety of fermented meat products but evaluation of its antimicrobial effect, both in vitro and in food matrix, should be previously investigated. This study should be carried out both for commercial starters as well as in-house starters isolated from meat products or its environment of a specific meat industry [49]. This fact is important since less antimicrobial effect is usually described in real meat sausages than in in vitro assays related to the interaction with food compounds. Thus, Reference [16] verified that 1 out of 13 strains of Latilactobacillus sakei isolated from traditional meat sausages displayed an in vitro antimicrobial effect against L. monocytogenes, Salmonella spp. and S. aureus. Other research [50] observed that only 14 out of 39 commercial starter cultures for meat sausage manufacture displayed antimicrobial effect. In contrast, other authors [51] observed, both in broth and in fermented Greek sausage, that autochthonous strains of Lb. sakei displayed antimicrobial effect against E. coli and L. monocytogenes. Similar results were described [52] in meat model media and fermented sausage against L. monocytogenes using Enterococcus mundtii as a starter culture. However, differences observed in the antimicrobial effect of starter cultures can be related to the microorganism, strain, the target microorganism and/or characteristics of sausage manufacture [53]. Thus, it was observed [54] that addition of Lacticasebacillus rhamnosus as a starter culture, isolated from human intestinal tract, did not suppress the growth of enterotoxin-producing S. aureus.

Antimicrobial effect of meat-borne LAB has been described in the literature against main foodborne pathogens and main spoilage bacteria (Table 1). The antimicrobial effect is characterised by reducing or eliminating pathogenic and/or spoilage microorganisms in a shorter time during the manufacturing process. Thus, it allows meat producers to obtain safer products more quickly, being able to optimise the production processes. It is important to remark that the ability of starter cultures to compete with the natural microbiota of the raw material and to undertake the metabolic activities expected is conditioned by its growth rate and survival in the conditions prevailing in the fermented sausage (i.e., anaerobic atmosphere, NaCl concentration, ingredients, temperature of fermentation and ripening and low pH) [55].

Table 1. Antimicrobial effect of selected starter cultures (added as ingredients during fermented meat manufacture) against main foodborne pathogens.

Starter(s) Culture(s) Used Origin of the Starter Culture Characterisation of the Inhibition Mechanism Reference
(a) Starter cultures selected against L. innocua
Pediococcus acidilactici Isolated from alheira (Portuguese fermented pork sausage) Not determined [56]
(b) Starter cultures selected against L. monocytogenes
Lactiplantibacillus plantarum (strain 178) (formerly Lactobacillus plantarum) Isolated from pork meat Not determined [57]
Lactiplantibacillus plantarum Isolated from poto-poto, an ethnic maize fermented food Production of plantaricin [58]
Latilactobacillus sakei (formerly Lactobacillus sakei) Isolated from chouriço (fermented cured pork sausage) made from wine-marinated meat Not determined [16]
Latilactobacillus curvatus 54M16 (formerly Lactobacillus curvatus) isolated from traditional fermented sausages of Campania region (Italy) Bacteriocing genes detection by PCR [59]
Pediococcus pentosaceus IOTEC culture collection (Thailan) Not determined [60]
Mix of Staphylococcus xylosus DD-34, Pediococcus acidilactici PA-2, Lactobacillus bavaricus MI-401 Commercial starter culures (FloraCarn LC, Mœller RM 52) Production of pediocin (indicated by manufacturer) [61]
Pediococcus acidilactici Commercial stater cultures from Chr. HansenLaboratories (Denmark) Bacteriocin purification and amino acid sequencing [50]
Latilactobaciullus sakei 8416
Latilactobacilus sakei 4413		 Natural Greek dry-fermented sausage Not determined [51]
Lacticaseibacillus rhamnosus E-97800 (formely Lactobacillus rhamnosus) E-97800;
Lacticaseibacillus rhamnosus LC-705;
Lactiplantibacillus plantarum ALC01;
Pediococcus pentosaceus RM2000		 Lacticaseibacillusrhamnosus E-97800: isolated from human faeces;
Lacticaseibacillus rhamnosus LC-705: isolated from dairy;
Lactiplantibacillus plantarum ALC01: commercial starter
Pediococcus pentosaceus RM2000: commercial starter		 Not determined [62]
(c) Starter cultures selected against Clostridium perfringens
Lactiplantibacillus plantarum PCS20 Microbial Strain Collection of Latvia, Not determined [63]
Pediococcus acidilactici Commercial stater cultures from Chr. HansenLaboratories (Denmark) Bacteriocin purification and amino acid sequencing [50]
(d) Starter cultures selected against Salmonella spp.
Enterococcus faecalis (strains A-48-32 and S-32-81) Isolated from cheese Production of enterocin [64]
Latilactobaciullus sakei Isolated from chouriço (fermented cured pork sausage) made from wine-marinated meat Not determined [16]
Latilactobacillus sakei 23K
Latilactobacillus sakei BMG 95
Latilactobacillus sakei BMG 37
Staphylococcus xylosus		 Latilactobacillussakei 23K: isolated from a French sausage
Latilactobacillus sakei BMG 95: isolated from anchovies
‘Latilactobacillus sakei BMG 37: isolated from sheep meat
Staphylococcus xylosus: isolated from artisanal Tunisian fermented sausages		 Not determined [65]
(e) Starter cultures selected against Escherichia coli
Lactiplantibacillus plantarum (strain 178) Isolated from pork meat Not determined [57]
Lactiplantibacillus plantarum Isolated from poto-poto, an ethnic maize fermented food Production of plantaricin [58]
Lacticaseibacillus rhamnosus (strains GG, E-97800 and LC-705) and Pediococcus pentosaceus Lacticaseibacillus rhamnosus (strains GG, LC-705): commercial starter (Valio Ltd., Helsinki, Finland)
Lacticaseibacillus rhamnosus E-97800: commercial starter (VTT Biotechnology, Finland)
Pediococcus pentosaceus: commercial (Gewurzmuller, Germany)		 Not determined [66]
Latilactobaciullus sakei
Leuconostoc mesenteroides		 Fermented game meat sausages Not determined [67]
Limosilactobacillus reuteri ATCC 55730 (formerly Lactobacillus reuteri) American Type Culture Collection Production of reuterin [63]
Latilactobaciullus sakei 8416
Latilactobacilus sakei 4413		 Natural Greek dry-fermented sausage Not determined [51]
(f) Starter cultures selected against Staphylococcus aureus
Enterococcus faecalis Isolated from cheese Production of enterocin [64]
Lactiplantibacillus plantarum (strain 178) Isolated from pork meat Not determined [57]
Latilactobaciullus sakei Isolated from chouriço (fermented cured pork sausage) made from wine-marinated meat Not determined [16]
Latilactobacillus sakei 23K
Latilactobacillus sakei BMG 95
Latilactobacillus sakei BMG 37
Staphylococcus xylosus		 Latilactobacillussakei 23K: isolated from a French sausage
Latilactobacillus sakei BMG 95: isolated from anchovies
Latilactobacillus sakei BMG 37: isolated from sheep meat
Staphylococcus xylosus: isolated from artisanal Tunisian fermented sausages		 Not determined [65]
Lacticaseibacillus rhamnosus FERM P-15120
Lacticaseibacillus paracasei subsp. paracasei FERM P-15121 (formerly Lactobacillus paracasei)		 Isolated from intestinal tracts Not determined [54]
(g) Starter cultures selected against Enterobacteriaceae
Mix of Pediococcus acidilactici (MC184, MS198 and MS200) plus Staphylococcus vitulus RS34 Isolated from traditional Iberian dry-fermented salchichón Not determined [68]
(h) Starter cultures selected against Yersinia enterocolitica
Latilactobacillus sakei ATCC 15521
Pediococcus acidilactici		 Latilactobacillus sakei ATCC 15521: obtained from the American Type Culture Collection
Pediococcus acidilactici: obtained from the Food Microbiology Culture Collection (Kansas State University, Manhattan, Kan., USA)		 Not determined [69]

PCR: polymerase chain reaction. The nomenclature of the genus Lactobacillus was presented according to the new taxonomic classification [83].

Thus, technological agents such as salt and curing agent may interfere in the bacteriocin production of Lb. sakei [56]. Also, spices seem to influence the growth of starter cultures. Thus, it was observed [57] that garlic enhanced bacteriocin production, lactic acid production was stimulated by pepper, while nutmeg decreased the bacteriocin production. In contrast, addition of garlic in Turkish soudjuk manufacture did not present any significant effect on the survival of S. typhimurium [58].

In addition, in case of high microbial contamination, the antimicrobial effect of starter cultures can be compromised. For example, if the initial contamination level is high, the use of a starter culture cannot improve the quality of the food product [44]. Thus, it has been reported [70] that the antimicrobial effect of natural microbiota cannot be enough in high microbial contamination of meat batter of Italian salami with 7 log cfu/g of Salmonella spp. and L. monocytogenes. Although Salmonella spp. decreased about 4 log cfu/g after fermentation, L. monocytogenes reduced less than 1 log cfu/g.

Also, the way in which starter cultures are added to the meat batter may influence its antimicrobial effect. Thus, microencapsulation of Limosillactobacillus reuteri decreased its antimicrobial effect against E. coli O157:H7 in dry fermented sausages [63].

Use of starter cultures combined with other compounds (Table 2), such as essential oils, organic acids, wine or spices, have been added to meat batter to improve the safety of these products [68][71][72][73][74][75]. However, previous assessment on potential interaction with starter cultures must be addressed since an inhibitory effect may be present, as discussed above.

Table 2. Combination of starter cultures and other hurdle technology to improve antimicrobial effect against foodborne pathogens in meat products’ manufacture.

Starter Culture Origin of Starter Cultures Combined by Antimicrobial Effect against References
Latilactobacillus sakei Isolated from meat sausages Garlic powder and wine L. monocytogenes [71]
Mix of starters Commercial starter cultures Mustard L. monocytogenes [72]
E. coli  
Latilactobaciullus sakei Isolated from meat sausages Garlic powder and wine Salmonella spp. [71]
Latilactobaciullus sakei Isolated from meat sausages Essential oils Salmonella spp [73]
E. coli
L. monocytogenes
Mix of S. xylosus and Lactiplantibacillus plantarum Isolated from meat sausages Vaccum packagaing Enterobacteriaceae [74]

The nomenclature of the genus Lactobacillus was presented according to the new taxonomic classification [83].

2.2. Control of Biogenic Amine Formation in Meat Products by Addition of Selected Starter Cultures

Biogenic amines (BA) are nitrogenous compounds that are found in fermented foods and beverages formed by the microbial decarboxylation of amino acids [76]. The main BAs in foods are histamine, tyramine, putrescine, cadaverine, tryptamine, spermine and spermidine. In some cases, they have been considered hazardous substances due to their ability to react with nitrites and form potentially carcinogenic nitrosamines [77].

Regarding consumers’ health, ingestion of BA may display some adverse dose-dependent effect, from allergy symptoms (e.g., skin rash, hives, itching) to systemic clinical signs (e.g., difficulty breathing, diarrhoea, vomiting, abdominal pain, joint pain, fatigue, seasickness, among others) [78]. In addition, due to the fact that BA are thermostable, further processing of foods will not eliminate them once formed [79].

Since concentration of BA in foods can display negative effects on the health of consumers, research about application of some manufacturing techniques and/or procedures, such as use of high hydrostatic pressure, control of NaCl concentration, freezing of raw materials, use of starter cultures, seasoning mixtures, product diameter, reduction in the amount of sugar added, use of additives, variation of the time/temperature parameters during fermentation and ripening, among others, have been investigated to decrease the BA contents in final product [80][81][82][83][84][85][86][87]. The microbiological quality of meat sausage ingredients is related to the aminogenesis process. Although hygienic quality is essential, other technological measures are needed. Thus, use of starter cultures represents one of the main measures to control BA formation [83]. The action mechanism of starter cultures is based on its competitive effect against the natural microbiota. Several studies have demonstrated the role of starter cultures in reducing the accumulation of BA in meat products. For example, combination of S. xylosus and Lactiplantibacillus plantarum decreases the content of cadaverine, putrescine, tryptamine, 2-phenylethylamine, histamine and tyramine by about 50% in Chinese Harbin dry sausage [88]. Addition of Lb. plantarum decreases the BA content by about 20%, but addition of both of them displayed a synergistic effect in which starter mix reduced tryptamine, phenylethylamine, putrescine, cadaverine, histamine and tyramine contents by nearly 100%, 100%, 86%, 63%, 82% and 43%, respectively [89].

Other research indicated that the combination of Enterococcus thailandicus and Enterococcus faecalis displayed better antibiogenic formation than the combination of Staphylococcus carnosus and Lb. sakei [90]. Since pH affects the BA formation, the lower level of pH achieved by the combination of E. thailandicus/E. faecalis than those achieved by the combination of S. carnosus/Lb. sakei may explain this difference on the anti-biogenic properties.

In contrast, addition of starter Lb. sakei and S. xylosus in the manufacture of Italian sausages displayed a higher level of BA compared to those made without starters [91]. This result can be explained by the aminobiogenic capacity of both starter cultures in which histidine [92] and tyramine [93] decarboxilase activity was reported in artisanal fermented sausages. This fact was also reported in foal dry sausage, in which the use of a mix of Pediococcus pentosaceus and S. xylosus displayed higher accumulation of BA than those made without starter [94]. Combination of Staphylococcus equorum S2M7/Lb. sakei CV3C2 displayed better anti-biogenic performance than S. xylosus CECT7057/Lb. sakei CECT7056 in finished dry-cured sausage Paio Alentejano. However, addition of yeast 2RB4 together S. equorum S2M7/Lb. sakei CV3C2 reduced the BA content in the finished product by about 10%. The yeast effect may probably be associated to an improved competitive effect against other naturally bacterial strains presented in dry-cured sausage able to produce biogenic amines [95].

As indicated above, starter cultures may prevent the BA formation by its competitive effect against spoilage bacteria, however, recent research reported that LAB have been considered as main BA producers [77]. It indicates that selected starter cultures used in fermented sausage manufacture must be previously assessed regarding their decarboxilase activity. Since starters used in fermented meat products are usually isolated from natural microbiota, aminobiogenic capacity vary among LAB [96]. Thus, it has been reported that 80% of indigenous E. faecium and E. faecalis presented tyramine-producing capacity [97][98]. However, the combination of E. thailandicus and E. faecalis produced the lowest BA concentration [90]. With regards to S. xylosus, only 7 out of 50 strains isolated from artisanal Italian sausages presented potential capacity to produce spermine, spermidine, tryptamine or tyramine [93]. Regarding Lb. sakei, this LAB has been reported as non-aminobiogenic [96] and may explain why manufacture of Italian sausage with a mix of Lb. sakei and S. xylosus displayed lower BA content than addition of a starter mix composed of P. pentosaceus and S. xylosus [99].

Overall, the aminobiogenic capacity of LAB together with the BA capacity of spoilage microbiota (naturally presented in raw meat) represent a chemical hazard concern in fermented meat products. It highlights the importance of selecting strains with oxidase activity instead of decarboxilase activity as starter cultures [100]. Although production of BA during sausage manufacture is inevitable, rapid overgrowth of selected (non-aminobiogenic starter) LAB at the beginning of fermentation may improve the chemical safety of these products.

Nitrates and nitrites in cured meat products are responsible for the characteristic red colour, inhibit the growth of pathogenic bacteria such as Clostridium botulinum, contribute to the development of the typical aroma of cured meats and act as antioxidants by delaying the development of rancidity and avoiding the appearance of alterations [101].

Overall, nitrates are not toxic, except in case of ingestion of large amounts. However, nitrites may pose a risk derived from their consumption since they can lead to allergic reactions and even cause methemoglobinemia situations. The main concern of nitrites is related to the possibility to act as precursors in the formation of carcinogenic nitrosamines, both in foods and at the organic level (for example, under acidic pH of mouth or stomach, nitrites or nitrates added to food or naturally occurring may combine with amines to form nitrosamines) [102]. Nitrosamine is a general term used to designate a vast group of N-nitroso compounds (NOCs). Its importance relies on the evidence of their carcinogenic properties [103]. Specifically, nitrosamines are formed by the reaction of compounds derived from nitrites, such as nitrous acid, with secondary amines throughout a nitrosation reaction. The presence of amines and the addition of nitrates and nitrites during the preparation of cured meat products can favour the development of this type of reaction in them. In meat products, the most commonly detected volatile nitrosamines are N-nitrosodimethylamine (NDMA), N-nitrosopyrrolidine (NPYR), N-nitrosopiperidine (NPIP), N-nitrosodiethylamine (NDEA), N- nitrosodi-n-butylamine (NDBA) and N-nitrosomor-folin (NMOR) [40]. Regarding these health issues for consumers, several food processing techniques have been investigated to reduce or replace the use of nitrates and nitrites in meat products (i.e., irradiation and n-nitrosamine blockers such as ascorbic acid) [102].

In this context, starter cultures appear to have a role in the reduction of nitrite levels in cured meat products. Thus, some authors [104][105][106] reported that addition of L. plantarum, L. pentosus, Lb. sakei or Lb. curvatus as starter culture decreased the nitrite content, suggesting the existence of nitrite reductase and heme-independent nitrite reductase that converts nitrite to NO, NO2 or N2O under anaerobic conditions [107]. Also, it has been referred that the rate of nitrite dissipation increases with pH reduction [108]. In contrast, the use of starter culture increased the N-nitrosopiperidine levels in heat-treated Turkish sucuk [109].

2.3. Control of Polycyclic Aromatic Hydrocarbons in Meat Products by Addition of Selected Starter Cultures

Polycyclic aromatic hydrocarbons (PAH) constitute a large group of organic compounds widely distributed in the environment with carcinogenic effects. Food contamination can occur by atmospheric deposition processes as well as during processing mainly related to heat treatments such as smoking, either by traditional methods or by the addition of smoke extracts directly into foods by spraying or dipping [110].

Since PAHs represent a health hazard and meat and meat products are one of the food categories contributing most to the dietary PAHs intake per day of the European Union, maximum levels in foods have been set by specific policy [111] to reduce its exposition. Research about the influence of starter cultures on PAH reduction is scarce.

Recently, it has been reported that immersion of cold smoked pork sausages in a LAB suspension of Lb. sakei, P. acidilactici and P. pentosaceus before ripening or in finished products decreased the benzo[a]pyrene contents [112]. Although the action mechanism of PAHs’ reduction is still unknown, it has been suggested that toxins are removed by specific enzymes produced by cells [113]. However, other studies suggested that biodegradation may be related to PAH binding to wall components of LAB cells [114]. Also, binding mechanisms of ion-exchange and hydrophobic bonds between exopolysaccharides and PAH have been suggested as a biodegradation route [115].

However, the effect of commercial starter (Lactobacillus spp., Micrococcaceae and yeasts) vs experimental starter (Lb. sakei and S. xylosus) on the PAH content in finished Portuguese Paio Alentejano (dry-cured pork sausage) did not evidence significant differences among starters [116]. It may suggest that the presence of specific enzymes or the presence of specific membrane compounds, as previously indicated, can be associated to specific microorganisms and/or strains.

3. Use of Starter Cultures to Improve the Safety in Dairy Products

3.1. Improving the Food Safety of Cheese by Use of Starter Cultures

LAB are the main starter cultures used in the dairy industry for cheese and yogurt production. Most of them are grouped into the genera Lactococcus, Lactobacillus, Leuconostoc and Pediococcus. Along with LAB, species of other genera such as Propionibacterium and Bifidobacterium are also occasionally used.

As previously discussed, use of starter cultures allows manufacturers to control and optimise the fermentation processes aimed to confer specific characteristics to the final product. Thus, starter cultures are related to the flavour and aroma characteristics, proteolytic and lipolytic activities, as well as inhibition of pathogenic microorganisms. In this section, we discuss the use of starter cultures to improve the safety of cheese and yogurt.

In cheese manufacturing, lactic acid bacteria play different roles in the cheese making process. Some species participate more in fermentation while others are mainly involved in ripening. Regarding food safety, the importance of LAB is related to the antimicrobial effect against foodborne and spoilage bacteria throughout production of organic acids, competitive effect and production of antimicrobial substances [25].

Regarding foodborne pathogens, the most commonly involved in cheese outbreaks are enteropathogenic E. coli, particularly 0157:H7, Salmonella spp., S. aureus and L. monocytogenes [1]. This last microorganism represents the most concerning pathogen since they can survive in a wide range of conditions during manufacture, ripening and storage (even in chilled storage).

Use of starter cultures to control L. monocytogenes in cheese has been largely described in the literature (Table 3), mainly based on the bacteriocinogenic properties of starter cultures. Thus, use of bacteriocinogenic starter cultures of sakacin, nisin, pediocin or enterocin represents the most important tool to control L. monocytogenes in cheese [117][118]. However, control of surface contamination by L. monocytogenes by LAB, during ripening or storage, should be carefully assessed since susceptibility of Listeria spp. to the antimicrobial activity of LAB is strain-dependent [119]. This strain susceptibility has been reported by other authors [118], in which addition of starter Lactococcus lactis in fresh cheese displayed a modest decrease of L. monocytogenes counts. The authors of Reference [120] reported that spraying surfaces with E. faecium in Munster cheese did not decrease L. monocytogenes levels but acts as a bacteriostatic. It can be concluded that starter cultures play an important role in the control of L. monocytogenes, but antimicrobial properties should be previously assessed in vitro (as described above for meat products) since L. monocytogenes susceptibility is strain-dependent. This fact was reported in Reference [121], in which nearly one third out of eight hundred LAB strains displayed anti-listerial activity. Also, hygienic practices must be guaranteed since this pathogen and outbreaks are still detected [122][123]. To improve the safety of cheese, combination of starter cultures and other antimicrobial treatments have been studied. Thus, enhancing the anti-listerial effect of starter Lc. lactis with lactic acid and sodium lactate [124] or plus sodium acetate or sodium lactate [118] have been reported. Addition of tartaric, fumaric, lactic or malic acid improves the inhibition of L. monocytogenes [125], but differences among organic acids may be explained by differences in the synergistic effect with lactic or acetic acid naturally produced by LAB during cheese ripening.

Table 3. Antimicrobial effect of selected starter cultures (added as ingredients during cheese manufacture) against main foodborne pathogens.

Cheese Starter(s) Culture(s) Used Origin of Starter Cultures Characterisation of the Inhibition Mechanism Reference
(a) Starter cultures selected against L. monocytogenes
Anari cheese Enterococcus faecium Donkey milk Not determined [126]
Cottage cheese Lactococcus lactis Italian fermented food Nisin producer. PCR detection of bacteriocin genes [127]
Portuguese Pico cheese Lactococcus lactis
Enterococcus faecium		 Isolated from cheese PCR detection of bacteriocin genes [128]
Fresh Minas cheese Lactiplantibacillus plantarum 59 Isolated from fruits Not determined [129]
Munster cheese Enterococcus faecium WHE 81 Isolated from cheese Enterocin producer. Determination by sensitivity to proteolytic and other enzymes [120]
Fresh cheese Lactococcus lactis   Nisin producer. Bacteriocin gene determination [130]
Cheese model Lactiplantibacillus plantarum Isolated from cheese Plantaricin producer. Purification by HPLC [131]
Gongonzola Cheese (Italy) Lactiplantibacillus plantarum
Latilactobacillus sakei
Lactococcus lactis		 Microbial collection (Institute of 108 Sciences of Food Production of the National Research Council of Italy Nisin and enterocin P producers. Characterisation by bacteriocin gene identification [119]
Fresh minas cheese Enterococcus mundtii
Enterococcus faecium CRL 35		 Isolated from cheese Enterocin identification by HPLC and sensitivity to proteolytic and other enzymes [132]
Ripened cheese Pediococcus acidilactici 347
Lactococcus lactis ESI 515
Lactococcus lactis CL1
Lactococcus lactis CL2		 Isolated from dairy products Nisin and pediocin producers [117]
Sicilian cheese Lactococcuslactis, 623
Lacticaseibacillus rhamnosus 971
Enterococcus faecium		 Isolated from dairy environment Not determined [133]
Golka cheese Lactococcus garvieae Lab428
Lactococcus mesenteroides Lab25
Lactiplantibacillus plantarum Lab572		 Isolated from Golka cheese Characterisation by bacteriocin gene identification [121]
(b) Starter cultures selected against Staphylococcus aureus
Probiotic white cheese Commercial lyophilised starter culture
Lacticaseibacillus rhamnosus
Lacticaseibacillus casei Shirota		 Commercial starter cultures Not determined [122]
Commercial cheese Lactococcus lactis L005
Lacticaseibacillus rhamnosus BGP2
Brevibacterium linens 004-0001
Microbacterium lacticum		 Isolated from raw milk Not determined [134]
Ripened cheese Pediococcus acidilactici 347
Lactococcus lactis ESI 515
Lactococcus lactis CL1
Lactococcus lactis CL2		 Isolated from dairy products Nisin producer
Pediocin producer		 [117]
Raw milk Montasio cheese Lactiplantibacillus plantarum Commercial starter mix Not determined [135]
Algerian´s goat cheese Lactococcus lactis ssp. lactis KJ660075 strain Isolated from raw goat milk Detection of bacteriocin by sensitivity to proteolytic and other enzymes [136]
(c) Starter cultures selected against Escherichia coli
Jben (Moroccan fresh cheese) Lactococcus lactis subsp. lactis UL730 Not available Nisin producer [137]
Commercial cheese Lactococcus lactis L005
Lacticaseibacillus rhamnosus BGP2
Brevibacterium linens 004-0001
Microbacterium lacticum		 Isolated from raw milk Not determined [134]
Ripened cheese Pediococcus acidilactici 347
Lactococcus lactis ESI 515
Lactococcus lactis CL1
Lactococcus lactis CL2		 Isolated from dairy products Nisin producer
Pediocin producer		 [117]
(d) Starter cultures selected against Salmonella spp.
Goat cheese Authochthonous Lactobacillus spp. Raw goat milk Not determined [138]
Raw milk Montasio cheese Lactiplantibacillus plantarum Commercial starter cultures Not determined [135]
White Brined Cheese Streptococcus thermophilus
Lactobacillus delbrueckii subsp. bulgaricus
Lacticaseibacillus paracasei K5		 Isolated from Greek Feta cheese Not determined [139]

The nomenclature of the genus Lactobacillus was presented according to the new taxonomic classification [83].

Combination of essential oils and starter cultures during cheese manufacture should be assessed since survival of starter can be compromised with further impacts on sensory and safety characteristics [130,131].

S. aureus is a concerning pathogen in cheese making. The importance of its control is related to the capacity of toxin production that, once formed in food, are extremely difficult to eliminate. These toxins are responsible for most staphylococcal food poisoning associated with the consumption of contaminated food. Thus, control of S. aureus contamination is of great importance, with special relevance in those cheeses made from raw milk since prevalence of S. aureus in milk is high [140]. Indeed, microbiological criteria for S. aureus in cheese has been set by law [141].

Research about control of S. aureus by addition of starter cultures is less than observed for L. monocytogenes (Table 3). Reduction of S. aureus was only achieved in bacteriocin producer Lc. lactis strains [127]. However, other reports suggest that the presence of S. aureus in raw milk is inhibited at different stages of ripening [134]. It has been observed that S. aureus survives in 60-day ripened white cheese made with commercial starter, although combination with probiotic [142] L. rhamnosus and Lactobacillus casei Shirota displayed an inhibitory effect up to 5 Log cfu/g, probably associated with the increased effect of bacteriocins arising during the ripening period. In contrast, use of starter L. rhamnosus did not display an inhibitory effect against S. aureus in Brazilian minas frescal cheese [143]. Survival of S. aureus in Jben, a Moroccan fresh cheese, was also reported [137], but addition of nisin-producer starter Lactococcus lactis subsp. lactis UL730 increased the safety of fresh cheese by elimination of S. aureus after 4 days. Combination of Lc. lactis subsp. cremoris and oregano essential oil (EO) to inhibit L. monocytogenes and S. aureus has been studied [144], however its efficacy may be compromised due to the inhibitory effect of oregano EO against added starter culture. A similar inhibition effect of EO was observed in a combination of thymus EO and starter Lc. lactis subsp. lactis and Lc. lactis subsp. cremoris against S. aureus [145]. Combination of Mentha longifolia L. EO in combination with starter Lb. casei in concentrations over 50 ppm displayed a synergistic effect against growth of S. aureus [146]. In addition to the negative effect of EO on starter LABs, as described above, sensory cheese analysis is necessary since inhibitory concentrations of EO may be incompatible with consumer acceptance.

Application of high-pressure treatment (HPT) at lower pressure in combination with bacteriocin-producing LAB [147] improves the safety of raw cheese against S. aureus. Since HPT disrupts the structure of S. aureus, including its cell membrane, it may explain the enhanced effect of bacteriocins produced by starter LAB.

In cheese processing, Salmonella spp. decreases along the ripening and storage periods [148][149]. Factors such as salt concentration, storage temperature and pH are the main barriers that disrupt its growth. However, Salmonella spp. may survive until the finished product [150][151]. Thus, it has been suggested that reduction of S. typhymurium along ripening in Montasio cheese is associated with the drop of pH after the negative antagonistic effect of starter Lb. plantarum by the spot method [135]. Survival of Salmonella spp. in low-salt cheddar cheese made with commercial starter Lactococcus lactis, Lc. lactis subsp. cremoris and Lb. helveticus was detected for up to 90 days when stored at 4 or 10 °C and for up to 30 days at 21 °C. Addition of starter cultures in cheese making improved the decrease of Salmonella spp. [138][139], probably associated to the enhanced effect of the pH by lactic acid production [152]. However, the survival of this pathogen indicates that the antimicrobial effect of starter cultures used in cheese making must be previously verified together with high hygienic quality of ingredients and storage temperature conditions.

Presence of E. coli in cheese has been reported in the literature. During cheese making, E. coli increased in the first hours of ripening [153][154]. Thus, the use of starter cultures to inhibit E. coli growth has been investigated as a biopreservative tool [153]. Addition of nisin- and pediocin-producing Lc. lactis CL2 inhibited E. coli after 15 and 30 days of ripening. However, addition of non-bacteriocinogenic Lc. lactis ESI 153 [117] displayed an unexpected better inhibitory effect than pediocin-producer P. acidilactici.

It was also reported that the inhibitory effect of starter cultures (Hafnia alvei, Lb. plantarum and Lc. Lactis) against E. coli may be influenced by the initial LAB load of raw milk [155]. It suggests that the acidification rate carried out by natural LAB microbiota together with starter cultures is related to the inhibitory effect of E. coli. However, it has been suggested that survival of E. coli during ripening may be associated to the initial microbial load of raw milk [156]. The synergistic effect of essential oil and starter cultures to control E. coli have been also studied [157], in which the combination of Zataria multiflora EO and Lb. acidophilus decreased the growth rate of E coli. In contrast, total growth inhibition of E. coli was achieved by combination of Lb. acidophilus LA-5 with oregano and rosemary EO [158].

Combination of bacteriocinogenic starter cultures and high hydrostatic pressure can reduce E. coli counts with lower pressure intensity in ripened cheese [117]. Other authors showed that addition of Lb. reuteri or glycerol in semi-hard cheese manufacture does not inhibit the growth of E. coli O157:H7 up to 30 days of ripening. However, combination of Lb. reuteri and glycerol eliminates E. coli completely after 24 h [159].

3.2. Improving the Food Safety of Yogurt by Use of Starter Cultures

Yogurt is a food product obtained by lactic fermentation of milk previously subjected to a heat treatment, at least, to pasteurisation, through the action of some microorganisms such as Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus. Also, other lactobacilli and bifidobacteria are sometimes added during or after culturing yogurt as probiotics [160]. Yogurt is considered a safe food since its manufacture includes two hurdle steps that make the survival of foodborne pathogens difficult, such as heated milk and low pH resulting from fermentation. To the best knowledge of the authors, no information regarding recent bacterial outbreaks in yogurt is available, although older scientific studies have reported the presence of foodborne pathogens such as L. monocytogenes, E. coli or Yersinia enterocolitica [161][162] related to cross-contamination issues.

Because yogurt manufacture is carried out by addition of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus starters, scarce research is available regarding the role of other starter cultures added to improve its safety.

Addition of bacteriocinogenic Streptococcus thermophilus as a starter displayed an inhibitory effect against L. monocytogenes during fermentation [163]. However, a scarce inhibitory effect was observed against S. aureus by the same starter. Counts of L. monocytogenes and E. coli increased during fermentation but decreased during storage, influenced by storage temperature, with a higher decrease at 10 than at 4 °C [164]. In addition, fermentation at two consecutive periods (43 °C for 3 h and 30 °C for 21 h) revealed better inhibition effect against E. coli O157:H7, L. monocytogenes 4b and Y. enterocolitica O3 [161]. Greater inhibition results against E. coli were also observed at 17 and 22 °C than at 4 and 8 °C during yogurt storage, suggesting that E. coli presented more adaptation capacity to pH variation than refrigeration temperatures [165].

Regarding Salmonella spp., it was observed that S. enteritidis and S. typhimurium survived throughout the fermentation process [166]. Also, S. enteritidis can survive up to 12 days at 4 °C and up to 60 h at 25 °C [166]. Overall, Gram-negative bacteria discussed above presented variable capabilities of survival throughout fermentation and storage of yogurt [167]. So, contamination after fermentation may represent a risk for foodborne poisoning. This survival on acid conditions can be related to development of acid, gene-encoded survival mechanisms [168]. It indicates that safety of yogurt cannot be based on the antimicrobial effect of starter cultures added. Since one of the antimicrobial effects of starters is based on the competitive effect, the survival mechanisms of enterobacteriaceae at acid environment may overlap the growth capacity of the starter. Also, the fact that not all starter cultures presented bacteriocinogenic capacity may imply a previous testing, as already discussed in the text. In consequence, good microbial quality of milk, proper thermal treatment of milk, together with good hygienic manufacturing practices and proper starter cultures selection must be implemented [169].

This entry is adapted from the peer-reviewed paper 10.3390/ijerph18052544

References

  1. Fox, P.F.; Guinee, T.P.; Cogan, T.M.; McSweeney, P.L.H. Pathogens in Cheese and Foodborne Illnesses. In Fundamental of Cheese Science; Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H., Eds.; Springer: New York, NY, USA, 2017; pp. 681–713.
  2. Hammami, R.; Fliss, I.; Corsetti, A. Editorial: Application of protective cultures and bacteriocins for food biopreservation. Frontiers Microbiol. 2019, 10, 1561.
  3. Aryana, K.J.; Olson, D.W.A. 100-Year Review: Yogurt and other cultured dairy products. J. Dairy Sci. 2017, 100, 9987–10013.
  4. Laranjo, M.; Elias, M.; Fraqueza, M.J. The use of starter cultures in traditional meat products. J. Food Qual. 2017, 2017, 9546026.
  5. Romano, P.; Capece, A. Wine microbiology. In Starter Cultures in Food Production; Chapter 13; Speranza, B., Bevilacqua, A., Corbo, M.R., Sinigaglia, M., Eds.; John Wiley & Sons, Ltd: West Sussex, UK, 2017; pp. 255–282.
  6. Vaughan, A.; O’Sullivan, T.; Van Sinderen, D. Enhancing the microbiological stability of malt and beer—A review. J. Inst. Brew. 2005, 111, 355–371.
  7. Mas, A.; Torija, M.J.; García-Parrilla, M.D.C.; Troncoso, A.M. Acetic acid bacteria and the production and quality of wine vinegar. Sci. World J. 2014, 2014, 394671.
  8. Gao, L.; Yang, H.; Wang, X.; Huang, Z.; Ishii, M.; Igarashi, Y.; Cui, Z. Rice straw fermentation using lactic acid bacteria. Biores. Technol. 2008, 99, 2742–2748.
  9. Ashaolu, T.J.; Reale, A.A. Holistic review on Euro-Asian lactic acid bacteria fermented cereals and vegetables. Microorganisms 2020, 8, 1176.
  10. Arroyo-López, F.N.; Garrido-Fernández, A.; Jiménez-Díaz, R. Starter cultures in vegetables with special emphasis on table olives. In Starter Cultures in Food Production; Speranza, B., Bevilacqua, A., Corbo, R.M., Sinigaglia, M., Eds.; John Wiley and Sons: West Sussex, UK, 2017; pp. 283–298.
  11. Brandt, M.J. Starter cultures for cereal based foods. Food Microbiol. 2014, 37, 41–43.
  12. Szutowska, J. Functional properties of lactic acid bacteria in fermented fruit and vegetable juices: A systematic literature review. Eur. Food Res. Technol. 2020, 246, 357–372.
  13. Franciosa, I.; Alessandria, V.; Dolci, P.; Rantsiou, K.; Cocolin, L. Sausage fermentation and starter cultures in the era of molecular biology methods. Int. J. Food Microbiol. 2018, 279, 26–32.
  14. Pereira, G.V.M.; De Carvalho Neto, D.P.; Junqueira, A.C.D.O.; Karp, S.G.; Letti, L.A.; Magalhães Júnior, A.I.; Soccol, C.R. A review of selection criteria for starter culture development in the food fermentation industry. Food Rev. Int. 2020, 36, 135–167.
  15. Laranjo, M.; Potes, M.E.; Elias, M. Role of Starter Cultures on the Safety of Fermented Meat Products. Front. Microbiol. 2019, 26, 583.
  16. Díez, J.G.; Patarata, L. Behavior of Salmonella spp., Listeria monocytogenes, and Staphylococcus aureus in Chouriço de Vinho, a dry fermented sausage made from wine-marinated meat. J. Food Protect. 2013, 76, 588–594.
  17. Taskila, S. Industrial production of starter cultures. In Starter Cultures in Food Production; Chapter 5; Speranza, B., Bevilacqua, A., Corbo, M.R., Sinigaglia, M., Eds.; John Wiley & Sons, Ltd: West Sussex, UK, 2017; pp. 79–100.
  18. Altieri, C.; Ciuffreda, E.; Maggio, B.; Sinigaglia, M. Lactic acid bacteéria as starter cultures. In Starter Cultures in Food Production; Speranza, B., Bevilacqua, A., Corbo, M.R., Sinigaglia, M., Eds.; John Wiley & Sons, Ltd: West Sussex, UK, 2017; pp. 1–15.
  19. Santos, S.C.; Fraqueza, M.J.; Elias, M.; Barreto, A.S.; Semedo-Lemsaddek, T. Traditional dry smoked fermented meat sausages: Characterization of autochthonous enterococci. LWT 2017, 79, 410–415.
  20. Semedo-Lemsaddek, T.; Carvalho, L.; Tempera, C.; Fernandes, M.H.; Fernandes, M.J.; Elias, M.; Barreto, A.S.; Fraqueza, M.J. Characterization and technological features of autochthonous coagulase-negative staphylococci as potential starters for Portuguese dry fermented sausages. J. Food Sci. 2016, 81, M1197–M1202.
  21. Buzzini, P.; Mauro, S.; Turchetti, B. Yeast as starter cultures. In Starter Cultures in Food Production; Speranza, B., Bevilacqua, A., Corbo, M.R., Sinigaglia, M., Eds.; John Wiley & Sons, Ltd: West Sussex, UK, 2017; pp. 16–49.
  22. Dantigny, P.; Bevilacqua, A. Fungal starters: An insight into the factors affecting the germination of conidia. In Starter Cultures in Food Production; Speranza, B., Bevilacqua, A., Corbo, R.M., Sinigaglia, M., Eds.; John Wiley and Sons: West Sussex, UK, 2017; pp. 50–63.
  23. Vignolo, G.; Fontana, C.; Fadda, S. Semidry and dry fermented sausages. In Handbook of Meat Processing; Toldrá, F., Ed.; Blackwell Publishing: Ames, IA, USA, 2010; pp. 379–398.
  24. Ockerman, H.W.; Basu, L. Production and consumption of fermented meat products. In Handbook of Fermented Meat and Poultry; Toldrá, F., Hui, Y.H., Astiarán, I., Sebranek, J.G., Talon, R., Eds.; Willey Blackwell: West Sussex, UK, 2014; pp. 7–11.
  25. Parente, E.; Cogan, T.M.; Powell, I.B. Starter cultures: General aspects. In Cheese, Chemistry, Physics and Microbiology; McSweeney, L.H., Fox, P.F., Cotter, P.D., Evertett, D.W., Eds.; Academic Press: London, UK, 2017; pp. 201–226.
  26. Almasoud, A.; Hettiarachchy, N.; Rayaprolu, S.; Babu, D.; Kwon, Y.M.; Mauromoustakos, A. Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) quorum sensing of Escherichia coli O157: H7 and Salmonella typhimurium. LWT-Food Sci. Technol. 2016, 66, 560–564.
  27. Theron, M.M.; Lues, J.F. Organic acids and meat preservation: A review. Food Rev. Int. 2007, 23, 141–158.
  28. Wang, C.; Chang, T.; Yang, H.; Cui, M. Antibacterial mechanism of lactic acid on physiological and morphological properties of Salmonella enteritidis, Escherichia coli and Listeria monocytogenes. Food Control 2015, 47, 231–236.
  29. Reis, J.A.; Paula, A.T.; Casarotti, S.N.; Penna, A.L.B. Lactic acid bacteria antimicrobial compounds: Characteristics and applications. Food Eng. Rev. 2012, 4, 124–140.
  30. Garmiene, G.; Salomskiene, J.; Jasutiene, I.; Miliauskiene, I.; Macioniene, I. Production of benzoic acid by lactic acid bacteria from Lactobacillus, Lactococcus and Streptococcus genera in milk. Milchwissenschaft 2010, 65, 295.
  31. Sullivan, D.J.; Azlin-Hasim, S.; Cruz-Romero, M.; Cummins, E.; Kerry, J.P.; Morris, M.A. Antimicrobial effect of benzoic and sorbic acid salts and nano-solubilisates against Staphylococcus aureus, Pseudomonas fluorescens and chicken microbiota biofilms. Food Control 2020, 107, 106786.
  32. Lanciotti, R.; Patrignani, F.; Bagnolini, F.; Guerzoni, M.E.; Gardini, F. Evaluation of diacetyl antimicrobial activity against Escherichia coli, Listeria monocytogenes and Staphylococcus aureus. Food Microbiol. 2003, 20, 537–543.
  33. Menconi, A.; Shivaramaiah, S.; Huff, G.R.; Prado, O.; Morales, J.E.; Pumford, N.R.; Morgan, M.; Wolfenden, A.; Bielke, L.R.; Hargis, B.M.; et al. Effect of different concentrations of acetic, citric, and propionic acid dipping solutions on bacterial contamination of raw chicken skin. Poultry Sci. 2013, 92, 2216–2220.
  34. Valerio, F.; Lavermicocca, P.; Pascale, M.; Visconti, A. Production of phenyllactic acid by lactic acid bacteria: An approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol. Lett. 2004, 233, 289–295.
  35. Ning, Y.; Yan, A.; Yang, K.; Wang, Z.; Li, X.; Jia, Y. Antibacterial activity of phenyllactic acid against Listeria monocytogenes and Escherichia coli by dual mechanisms. Food Chem. 2017, 228, 533–540.
  36. Hladíková, Z.; Smetanková, J.; Greif, G.; Greifová, M. Antimicrobial activity of selected lactic acid cocci and production of organic acids. Acta Chim. Slov. 2012, 5, 80–85.
  37. Arena, M.P.; Silvain, A.; Normanno, G.; Grieco, F.; Drider, D.; Spano, G.; Fiocco, D. Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Frontiers Microbiol. 2016, 7, 464.
  38. Puolanne, E.; Petaja-Kanninen, E. Principles of meat fermentation. In Handbook of Fermented Meat and Poultry, 2nd ed.; Toldrá, F., Hui, Y.H., Astiarán, I., Sebranek, J.G., Talon, R., Eds.; Willey Blackwell: West Sussex, UK, 2014; pp. 13–17.
  39. Moore, J.E. Gastrointestinal outbreaks associated with fermented meats. Meat Sci. 2004, 67, 565–568.
  40. Flores, M.; Toldrá, F. Chemistry, safety, and regulatory considerations in the use of nitrite and nitrate from natural origin in meat products. Meat Sci. 2020, 171, 108272.
  41. Fraqueza, M.J.; Laranjo, M.; Elias, M.; Patarata, L. Microbiological hazards associated with salt and nitrite reduction in cured meat products: Control strategies based on antimicrobial effect of natural ingredients and protective microbiota. Curr. Opin. Food Sci. 2020, 38, 32–39.
  42. Lücke, F.K. Quality improvement and fermentation control in meat products. In Advances in Fermented Foods and Beverages. Improving Quality, Technologies and Health Benefit; Holzapfel, W., Ed.; Woodhead Publishing: Sawston, Cambridge, UK, 2015; pp. 357–376.
  43. Taormina, P.J. Implications of salt and sodium reduction on microbial food safety. Crit. Rev. Food Sci. Nut. 2010, 50, 209–227.
  44. Patarata, L.; Novais, M.; Fraqueza, M.J.; Silva, J.A. Influence of meat spoilage microbiota initial load on the growth and survival of three pathogens on a naturally fermented sausage. Foods 2020, 9, 676.
  45. Oliveira, M.; Ferreira, V.; Magalhães, R.; Teixeira, P. Biocontrol strategies for Mediterranean-style fermented sausages. Food Res. Int. 2018, 103, 438–449.
  46. Castellano, P.; Pérez Ibarreche, M.; Blanco Massani, M.; Fontana, C.; Vignolo, G.M. Strategies for pathogen biocontrol using lactic acid bacteria and their metabolites: A focus on meat ecosystems and industrial environments. Microorganisms 2017, 5, 38.
  47. García-Díez, J.; Alheiro, J.; Pinto, A.L.; Soares, L.; Falco, V.; Fraqueza, M.J.; Patarata, L. Influence of food characteristics and food additives on the antimicrobial effect of garlic and oregano essential oils. Foods 2017, 6, 44.
  48. Chikindas, M.L.; Weeks, R.; Drider, D.; Chistyakov, V.A.; Dicks, L.M. Functions and emerging applications of bacteriocins. Curr. Opin. Biotechnol. 2018, 49, 23–28.
  49. Dos Santos Cruxen, C.E.; Funck, G.D.; Haubert, L.; da Silva Dannenberg, G.; de Lima Marques, J.; Chaves, F.C.; Silva, W.P.; Fiorentini, Â.M. Selection of native bacterial starter culture in the production of fermented meat sausages: Application potential, safety aspects, and emerging technologies. Food Res. Int. 2019, 122, 371–382.
  50. Nieto-Lozano, J.C.; Reguera-Useros, J.I.; Peláez-Martínez, M.D.C.; Sacristán-Pérez-Minayo, G.; Gutiérrez-Fernández, A.J.; de la Torre, A.H. The effect of the pediocin PA-1 produced by Pediococcus acidilactici against Listeria monocytogenes and Clostridium perfringens in Spanish dry-fermented sausages and frankfurters. Food Control 2010, 21, 679–685.
  51. Pragalaki, T.; Bloukas, J.G.; Kotzekidou, P. Inhibition of Listeria monocytogenes and Escherichia coli O157: H7 in liquid broth medium and during processing of fermented sausage using autochthonous starter cultures. Meat Sci. 2013, 95, 458–464.
  52. Orihuel, A.; Bonacina, J.; Vildoza, M.J.; Bru, E.; Vignolo, G.; Saavedra, L.; Fadda, S. Biocontrol of Listeria monocytogenes in a meat model using a combination of a bacteriocinogenic strain with curing additives. Food Res. Int. 2018, 107, 289–296.
  53. Ravyts, F.; Barbuti, S.; Frustoli, M.A.; Parolari, G.; Saccani, G.; De Vuyst, L.; Leroy, F. Competitiveness and antibacterial potential of bacteriocin-producing starter cultures in different types of fermented sausages. J. Food Protect. 2008, 71, 1817–1827.
  54. Sameshima, T.; Magome, C.; Takeshita, K.; Arihara, K.; Itoh, M.; Kondo, Y. Effect of intestinal Lactobacillus starter cultures on the behaviour of Staphylococcus aureus in fermented sausage. Int. J. Food Microbiol. 1998, 41, 1–7.
  55. Talon, R.; Leory, S. 2018 Functionalities of meat bacterial startes. In Advanced Technologies for Meat Processing, 2nd ed.; Toldrá, F., Nollet, L.M.L., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 597–614.
  56. Albano, H.; Pinho, C.; Leite, D.; Barbosa, J.; Silva, J.; Carneiro, L.; Magalhães, R.; Hogg, T.; Teixeira, P. Evaluation of a bacteriocin-producing strain of Pediococcus acidilactici as a biopreservative for “Alheira”, a fermented meat sausage. Food Control 2009, 20, 764–770.
  57. Campaniello, D.; Speranza, B.; Bevilacqua, A.; Altieri, C.; Rosaria Corbo, M.; Sinigaglia, M. Industrial validation of a promising functional strain of Lactobacillus plantarum to improve the quality of Italian sausages. Microorganisms 2020, 8, 116.
  58. Diaz-Ruiz, G.; Omar, N.B.; Abriouel, H.; Cantilde, M.M.; Galvez, A. Inhibition of Listeria monocytogenes and Escherichia coli by bacteriocin-producing Lactobacillus plantarum EC52 in a meat sausage model system. Afri. J. Microbiol. Res. 2012, 6, 1103–1108.
  59. Giello, M.; La Storia, A.; De Filippis, F.; Ercolini, D.; Villani, F. Impact of Lactobacillus curvatus 54M16 on microbiota composition and growth of Listeria monocytogenes in fermented sausages. Food Microbiol. 2018, 72, 1–15.
  60. Kingcha, Y.; Tosukhowong, A.; Zendo, T.; Roytrakul, S.; Luxananil, P.; Chareonpornsook, K.; Valyasevi, R.; Sonomoto, K.; Visessanguan, W. Anti-listeria activity of Pediococcus pentosaceus BCC 3772 and application as starter culture for Nham, a traditional fermented pork sausage. Food Control 2012, 25, 190–196.
  61. Lahti, E.; Johansson, T.; Honkanen-Buzalski, T.; Hill, P.; Nurmi, E. Survival and detection of Escherichia coli O157:H7 and Listeria monocytogenes during the manufacture of dry sausage using two different starter cultures. Food Microbiol. 2001, 18, 75–85.
  62. Työppönen, S.; Markkula, A.; Petäjä, E.; Suihko, M.L.; Mattila-Sandholm, T. Survival of Listeria monocytogenes in North European type dry sausages fermented by bioprotective meat starter cultures. Food Control 2003, 14, 181–185.
  63. Di Gioia, D.; Mazzola, G.; Nikodinoska, I.; Aloisio, I.; Langerholc, T.; Rossi, M.; Raimondi, S.; Melero, B.; Rovira, J. Lactic acid bacteria as protective cultures in fermented pork meat to prevent Clostridium spp. growth. Int. J. Food Microbiol. 2016, 235, 53–59.
  64. Ananou, S.; Garriga, M.; Hugas, M.; Maqueda, M.; Martínez-Bueno, M.; Gálvez, A.; Valdivia, E. Control of Listeria monocytogenes in model sausages by enterocin AS-48. Int. J. Food Microbiol. 2005, 103, 179–190.
  65. Najjari, A.; Boumaiza, M.; Jaballah, S.; Boudabous, A.; Ouzari, H.I. Application of isolated Lactobacillus sakei and Staphylococcus xylosus strains as a probiotic starter culture during the industrial manufacture of Tunisian dry-fermented sausages. Food Sci. Nut. 2020, 8, 4172–4184.
  66. Erkkilä, S.; Venäläinen, M.; Hielm, S.; Petäjä, E.; Puolanne, E.; Mattila-Sandholm, T. Survival of Escherichia coli O157:H7 in dry sausage fermented by probiotic lactic acid bacteria. J. Sci. Food Agricul. 2000, 80, 2101–2104.
  67. Fuka, M.M.; Maksimovic, A.Z.; Hulak, N.; Kos, I.; Radovcic, N.M.; Juric, S.; Tanuwidjaja, I.; Vincekovic, M. The survival rate and efficiency of non-encapsulated and encapsulated native starter cultures to improve the quality of artisanal game meat sausages. J. Food Sci. Technol. 2020.
  68. Casquete, R.; Benito, M.J.; Martín, A.; Ruiz-Moyano, S.; Aranda, E.; Córdoba, M.G. Microbiological quality of salchichón and chorizo, traditional Iberian dry-fermented sausages from two different industries, inoculated with autochthonous starter cultures. Food Control 2012, 24, 191–198.
  69. Ceylan, E.; Fung, D.Y.C. Destruction of Yersinia enterocolitica by Lactobacillus sake and Pediococcus acidilactici during low-temperature fermentation of Turkish dry sausage (sucuk). J. Food Sci. 2000, 65, 876–879.
  70. Nightingale, K.K.; Thippareddi, H.; Phebus, R.K.; Marsden, J.L.; Nutsch, A.L. Validation of a traditional Italian-style salami manufacturing process for control of Salmonella and Listeria monocytogenes. J. Food Protec. 2006, 69, 794–800.
  71. Linares, M.B.; Garrido, M.D.; Martins, C.; Patarata, L. Efficacies of garlic and L. sakei in wine-based marinades for controlling Listeria monocytogenes and Salmonella spp. in chouriço de vinho, a dry sausage made from wine-marinated pork. J. Food Sci. 2013, 78, M719–M724.
  72. Luciano, F.B.; Belland, J.; Holley, R.A. Microbial and chemical origins of the bactericidal activity of thermally treated yellow mustard powder toward Escherichia coli O157:H7 during dry sausage ripening. Int. J. Food Microbiol. 2011, 145, 69–76.
  73. García-Díez, J.; Alheiro, J.; Pinto, A.L.; Soares, L.; Falco, V.; Fraqueza, M.J.; Patarata, L. Behaviour of food-borne pathogens on dry cured sausage manufactured with herbs and spices essential oils and their sensorial acceptability. Food Control 2016, 59, 262–270.
  74. Sun, Q.; Sun, F.; Zheng, D.; Kong, B.; Liu, Q. Complex starter culture combined with vacuum packaging reduces biogenic amine formation and delays the quality deterioration of dry sausage during storage. Food Control 2019, 100, 58–66.
  75. Meira, N.V.; Holley, R.A.; Bordin, K.; de Macedo, R.E.; Luciano, F.B. Combination of essential oil compounds and phenolic acids against Escherichia coli O157: H7 in vitro and in dry-fermented sausage production. Int. J. Food. Microbiol. 2017, 260, 59–64.
  76. Doeun, D.; Davaatseren, M.; Chung, M.S. Biogenic amines in foods. Food Sci. Biotechnol. 2017, 26, 1463–1474.
  77. Barbieri, F.; Montanari, C.; Gardini, F.; Tabanelli, G. Biogenic amine production by lactic acid bacteria: A review. Foods 2019, 8, 17.
  78. Jairath, G.; Singh, P.K.; Dabur, R.S.; Rani, M.; Chaudhari, M. Biogenic amines in meat and meat products and its public health significance: A review. J. Food Sci. Technol. 2015, 52, 6835–6846.
  79. Ruiz-Capillas, C.; Herrero, A.M. Impact of biogenic amines on food quality and safety. Foods 2019, 8, 62.
  80. Bover-Cid, S.; Miguelez-Arrizado, M.J.; Moratalla, L.L.L.; Carou, M.C.V. Freezing of meat raw materials affects tyramine and diamine accumulation in spontaneously fermented sausages. Meat Sci. 2006, 72, 62–68.
  81. González-Fernández, C.; Santos, E.M.; Jaime, I.; Rovira, J. Influence of starter cultures and sugar concentrations on biogenic amine contents in chorizo dry sausage. Food Microbiol. 2003, 20, 275–284.
  82. Komprda, T.; Smělá, D.; Pechová, P.; Kalhotka, L.; Štencl, J.; Klejdus, B. Effect of starter culture, spice mix and storage time and temperature on biogenic amine content of dry fermented sausages. Meat Sci. 2004, 67, 607–616.
  83. Latorre-Moratalla, M.; Bover-Cid, S.; Veciana-Nogués, M.T.; Vidal-Carou, M.C. Control of biogenic amines in fermented sausages: Role of starter cultures. Front. Microbiol. 2012, 3, 169.
  84. Miguélez-Arrizado, M.J.; Bover-Cid, S.; Latorre-Moratalla, M.L.; Vidal-Carou, M.C. Biogenic amines in Spanish fermented sausages as a function of diameter and artisanal or industrial origin. J. Sci. Food Agricul. 2006, 86, 549–557.
  85. Roseiro, C.; Santos, C.; Sol, M.; Silva, L.; Fernandes, I. Prevalence of biogenic amines during ripening of a traditional dry fermented pork sausage and its relation to the amount of sodium chloride added. Meat Sci. 2006, 74, 557–563.
  86. Ruiz-Capillas, C.; Colmenero, F.J.; Carrascosa, A.V.; Muñoz, R. Biogenic amine production in Spanish dry-cured “chorizo” sausage treated with high-pressure and kept in chilled storage. Meat Sci. 2007, 77, 365–371.
  87. Sun, Q.; Zhao, X.; Chen, H.; Zhang, C.; Kong, B. Impact of spice extracts on the formation of biogenic amines and the physicochemical, microbiological and sensory quality of dry sausage. Food Control 2018, 92, 190–200.
  88. Sun, Q.; Chen, Q.; Li, F.; Zheng, D.; Kong, B. Biogenic amine inhibition and quality protection of Harbin dry sausages by inoculation with Staphylococcus xylosus and Lactobacillus plantarum. Food Control 2016, 68, 358–366.
  89. Xie, C.; Wang, H.H.; Nie, X.K.; Chen, L.; Deng, S.L.; Xu, X.L. Reduction of biogenic amine concentration in fermented sausage by selected starter cultures. CyTA J. Food 2015, 13, 491–497.
  90. Kim, H.S.; Lee, S.Y.; Hur, S.J. Effects of different starter cultures on the biogenic amine concentrations, mutagenicity, oxidative stress, and neuroprotective activity of fermented sausages and their relationships. J. Funct. Foods 2019, 52, 424–429.
  91. Parente, E.; Martuscelli, M.; Gardini, F.; Grieco, S.; Crudele, M.A.; Suzzi, G. Evolution of microbial populations and biogenic amine production in dry sausages produced in Southern Italy. J. Appl. Microbiol. 2001, 90, 882–891.
  92. Bover-Cid, S.; Hugas, M.; Izquierdo-Pulido, M.; Vidal-Carou, M.C. Amino acid-decarboxylase activity of bacteria isolated from fermented pork sausages. Int. J. Food Microbiol. 2001, 66, 185–189.
  93. Martuscelli, M.; Crudele, M.A.; Gardini, F.; Suzzi, G. Biogenic amine formation and oxidation by Staphylococcus xylosus strains from artisanal fermented sausages. Lett. App. Microbiol. 2000, 31, 228–232.
  94. Domínguez, R.; Agregán, R.; Lorenzo, J.M. Role of commercial starter cultures on microbiological, physicochemical characteristics, volatile compounds and sensory properties of dry-cured foal sausage. Asian Pac. J. Trop. Dis. 2016, 6, 396–403.
  95. Dias, I.; Laranjo, M.; Potes, M.E.; Agulheiro-Santos, A.C.; Ricardo-Rodrigues, S.; Fialho, A.R.; Véstia, J.; Fraqueza, M.J.; Oliveira, M.; Elias, M. Autochthonous starter cultures are able to reduce biogenic amines in a traditional portuguese smoked fermented sausage. Microorganisms 2020, 8, 686.
  96. Latorre-Moratalla, M.L.; Bover-Cid, S.; Talon, R.; Aymerich, T.; Garriga, M.; Zanardi, E.; Ianieri, A.; Fraqueza, M.J.; Elias, M.; Drosinos, E.H.; et al. Distribution of aminogenic activity among potential autochthonous starter cultures for dry fermented sausages. J. Food Protec. 2010, 73, 524–528.
  97. Komprda, T.; Sládková, P.; Petirová, E.; Dohnal, V.; Burdychová, R. Tyrosine-and histidine-decarboxylase positive lactic acid bacteria and enterococci in dry fermented sausages. Meat Sci. 2010, 86, 870–877.
  98. Landeta, G.; Curiel, J.A.; Carrascosa, A.V.; Muñoz, R.; De Las Rivas, B. Technological and safety properties of lactic acid bacteria isolated from Spanish dry-cured sausages. Meat Sci. 2013, 95, 272–280.
  99. Pasini, F.; Soglia, F.; Petracci, M.; Caboni, M.F.; Marziali, S.; Montanari, C.; Gardini, F.; Grazia, L.; Tabanelli, G. Effect of fermentation with different lactic acid bacteria starter cultures on biogenic amine content and ripening patterns in dry fermented sausages. Nutrients 2018, 10, 1497.
  100. Alfaia, C.M.; Gouveia, I.M.; Fernandes, M.H.; Fernandes, M.J.; Semedo-Lemsaddek, T.; Barreto, A.S.; Fraqueza, M.J. Assessment of coagulase-negative staphylococci and lactic acid bacteria isolated from Portuguese dry fermented sausages as potential starters based on their biogenic amine profile. J. Food Sci. 2018, 83, 2544–2549.
  101. Pegg, R.B.; Honikel, K.O. Principles of curing. In Handbook of Fermented Meat and Poultry, 2nd ed.; Toldrá, F., Hui, Y.H., Astiararan, I., Sebranek, J.G., Talon, R., Eds.; Wiley Blackwell: West Sussex, UK, 2015; pp. 19–30.
  102. De Mey, E.; De Maere, H.; Paelinck, H.; Fraeye, I. Volatile N-nitrosamines in meat products: Potential precursors, influence of processing, and mitigation strategies. Cri. Rev. Food Sci. Nut. 2017, 57, 2909–2923.
  103. Cantwell, M.; Elliott, C. Nitrates, nitrites and nitrosamines from processed meat intake and colorectal cancer risk. J. Clin. Nutr. Diet. 2017, 3, 27.
  104. Sun, F.; Kong, B.; Chen, Q.; Han, Q.; Diao, X. N-nitrosoamine inhibition and quality preservation of Harbin dry sausages by inoculated with Lactobacillus pentosus, Lactobacillus curvatus and Lactobacillus sake. Food Control 2017, 73, 1514–1521.
  105. Xiao, Y.; Li, P.; Zhou, Y.; Ma, F.; Chen, C. Effect of inoculating Lactobacillus pentosus R3 on N-nitrosamines and bacterial communities in dry fermented sausages. Food Control 2018, 87, 126–134.
  106. Chen, X.; Li, J.; Zhou, T.; Li, J.; Yang, J.; Chen, W.; Xiong, Y.L. Two efficient nitrite-reducing Lactobacillus strains isolated from traditional fermented pork (Nanx Wudl) as competitive starter cultures for Chinese fermented dry sausage. Meat Sci. 2016, 121, 302–309.
  107. Molognoni, L.; Motta, G.E.; Daguer, H.; Lindner, J.D.D. Microbial biotransformation of N-nitro-, C-nitro-, and C-nitrous-type mutagens by Lactobacillus delbrueckii subsp. bulgaricus in meat products. Food Chem. Toxicol. 2020, 136, 110964.
  108. Waga, M.; Takeda, S.; Sakata, R. Effect of nitrate on residual nitrite decomposition rate in cooked cured pork. Meat Sci. 2017, 129, 135–139.
  109. Sallan, S.; Kaban, G.; Oğraş, Ş.Ş.; Çelik, M.; Kaya, M. Nitrosamine formation in a semi-dry fermented sausage: Effects of nitrite, ascorbate and starter culture and role of cooking. Meat Sci. 2020, 159, 107917.
  110. Ledesma, E.; Rendueles, M.; Díaz, M. Contamination of meat products during smoking by polycyclic aromatic hydrocarbons: Processes and prevention. Food Control 2016, 60, 64–87.
  111. Commission Regulation (EC) No 1881/2006 of 19 December 2006 Setting Maximum Levels for Certain Contaminants in Foodstuffs. Available online: (accessed on 3 March 2021).
  112. Bartkiene, E.; Bartkevics, V.; Mozuriene, E.; Krungleviciute, V.; Novoslavskij, A.; Santini, A.; Rozentale, I.; Juodeikiene, G.; Cizeikiene, D. The impact of lactic acid bacteria with antimicrobial properties on biodegradation of polycyclic aromatic hydrocarbons and biogenic amines in cold smoked pork sausages. Food Control 2017, 71, 285–292.
  113. Fuchs, S.; Sontag, G.; Stidl, R.; Ehrlich, V.; Kundi, M.; Knasmüller, S. Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food Chem. Toxicol. 2008, 46, 1398–1407.
  114. Haskard, C.; Binnion, C.; Ahokas, J. Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. Chem. Biol. Interar. 2000, 128, 39–49.
  115. Tsuda, H.; Hara, K.; Miyamoto, T. Binding of mutagens to exopolysaccharide produced by Lactobacillus plantarum mutant strain 301102S. J. Dairy Sci. 2008, 91, 2960–2966.
  116. Elias, M.; Potes, M.E.; Roseiro, L.C.; Santos, C.; Gomes, A.; Agulheiro-Santos, A.C. The Effect of starter Cultures on the Portuguese Traditional Sausage Paio do Alentejo in Terms of its Sensory and Textural Characteristics and Polycyclic Aromatic Hydrocarbons Profile. J. Food Res. 2014, 3, 45–56.
  117. Rodrıguez, E.; Calzada, J.; Arqués, J.L.; Rodrıguez, J.M.; Nunez, M.; Medina, M. Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese. Int. Dairy J. 2005, 15, 51–57.
  118. Lourenço, A.; Kamnetz, M.B.; Gadotti, C.; Diez-Gonzalez, F. Antimicrobial treatments to control Listeria monocytogenes in queso fresco. Food Microbiol. 2017, 64, 47–55.
  119. Morandi, S.; Silvetti, T.; Battelli, G.; Brasca, M. Can lactic acid bacteria be an efficient tool for controlling Listeria monocytogenes contamination on cheese surface? The case of Gorgonzola cheese. Food Control 2019, 96, 499–507.
  120. Izquierdo, E.; Marchioni, E.; Aoude-Werner, D.; Hasselmann, C.; Ennahar, S. Smearing of soft cheese with Enterococcus faecium WHE 81, a multi-bacteriocin producer, against Listeria monocytogenes. Food Microbiol. 2009, 26, 16–20.
  121. Sip, A.; Więckowicz, M.; Olejnik-Schmidt, A.; Grajek, W. Anti-listeria activity of lactic acid bacteria isolated from golka, a regional cheese produced in Poland. Food Control 2012, 26, 117–124.
  122. EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018, 16, 5500.
  123. Martinez-Rios, V.; Dalgaard, P. Prevalence of Listeria monocytogenes in European cheeses: A systematic review and meta-analysis. Food Control 2018, 84, 205–214.
  124. Morandi, S.; Silvetti, T.; Vezzini, V.; Morozzo, E.; Brasca, M. How we can improve the antimicrobial performances of lactic acid bacteria? A new strategy to control Listeria monocytogenes in Gorgonzola cheese. Food Microbiol. 2020, 90, 103488.
  125. Tavşanlı, H.; İrkin, R.; Kısadere, İ. The effects of different organic acid treatments on some microflora and pathogen Listeria monocytogenes of white brine cheese. Kafkas Univ. Vet. Fak. Derg. 2019, 25, 201–207.
  126. Aspri, M.; O’Connor, P.M.; Field, D.; Cotter, P.D.; Ross, P.; Hill, C.; Papademas, P. Application of bacteriocin-producing Enterococcus faecium isolated from donkey milk, in the bio-control of Listeria monocytogenes in fresh whey cheese. Int. Dairy J. 2017, 73, 1–9.
  127. Bello, B.D.; Zeppa, G.; Bianchi, D.M.; Decastelli, L.; Traversa, A.; Gallina, S.; Coisson, J.D.; Locatelli, M.; Travaglia, F.; Cocolin, L. Effect of nisin-producing Lactococcus lactis starter cultures on the inhibition of two pathogens in ripened cheeses. Int. J. Dairy Technol. 2013, 66, 468–477.
  128. Coelho, M.C.; Silva, C.C.G.; Ribeiro, S.C.; Dapkevicius, M.L.N.E.; Rosa, H.J.D. Control of Listeria monocytogenes in fresh cheese using protective lactic acid bacteria. Int. J. Food Microbiol. 2014, 191, 53–59.
  129. Costa, W.K.A.; de Souza, G.T.; Brandão, L.R.; de Lima, R.C.; Garcia, E.F.; dos Santos Lima, M.; Leite de Souza, E.; Saarela, M.; Magnani, M. Exploiting antagonistic activity of fruit-derived Lactobacillus to control pathogenic bacteria in fresh cheese and chicken meat. Food Res. Int. 2018, 108, 172–182.
  130. Kondrotiene, K.; Kasnauskyte, N.; Serniene, L.; Gölz, G.; Alter, T.; Kaskoniene, V.; Maruska, A.S.; Malakauskas, M. Characterization and application of newly isolated nisin producing Lactococcus lactis strains for control of Listeria monocytogenes growth in fresh cheese. LWT 2018, 87, 507–514.
  131. Mills, S.; Serrano, L.; Griffin, C.; O’Connor, P.M.; Schaad, G.; Bruining, C.; Hill, C.; Ross, R.P.; Meijer, W.C. Inhibitory activity of Lactobacillus plantarum LMG P-26358 against Listeria innocua when used as an adjunct starter in the manufacture of cheese. Microb. Cell Factories 2011, 1, S7.
  132. Pingitore, E.V.; Todorov, S.D.; Sesma, F.; de Melo Franco, B.D.G. Application of bacteriocinogenic Enterococcus mundtii CRL35 and Enterococcus faecium ST88Ch in the control of Listeria monocytogenes in fresh Minas cheese. Food Microbiol. 2012, 32, 38–47.
  133. Scatassa, M.L.; Gaglio, R.; Cardamone, C.; Macaluso, G.; Arcuri, L.; Todaro, M.; Mancuso, I. Anti-Listeria activity of lactic acid bacteria in two traditional Sicilian cheeses. Ital. J. Food Saf. 2017, 6, 6191.
  134. Masoud, W.; Vogensen, F.K.; Lillevang, S.; Al-Soud, W.A.; Sørensen, S.J.; Jakobsen, M. The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR. Int. J. Food Microbiol. 2012, 153, 192–202.
  135. Stecchini, M.L.; Sarais, I.; de Bertoldi, M. The influence of Lactobacillus plantarum culture inoculation on the fate of Staphylococcus aureus and Salmonella typhimurium in Montasio cheese. Int. J. Food Microbiol. 1991, 14, 99–109.
  136. Sahraoui, Y.; Fayolle, K.; Leriche, F.; Le Flèche-Matéos, A.; Sadoun, D. Antibacterial and technological properties of Lactococcus lactis ssp. lactis KJ660075 strain selected for its inhibitory power against Staphylococcus aureus for cheese quality improving. J. Food Sci. Technol. 2015, 52, 7133–7142.
  137. Hamama, A.; El Hankouri, N.; El Ayadi, M. Fate of enterotoxigenic Staphylococcus aureus in the presence of nisin-producing Lactococcus lactis strain during manufacture of Jben, a Moroccan traditional fresh cheese. Int. Dairy J. 2002, 12, 933–938.
  138. Silva Ferrari, I.; de Souza, J.V.; Ramos, C.L.; da Costa, M.M.; Schwan, R.F.; Dias, F.S. Selection of autochthonous lactic acid bacteria from goat dairies and their addition to evaluate the inhibition of Salmonella typhi in artisanal cheese. Food Microbiol. 2016, 60, 29–38.
  139. Terpou, A.; Bosnea, L.; Kanellaki, M.; Plessas, S.; Bekatorou, A.; Bezirtzoglou, E.; Koutinas, A.A. Growth capacity of a novel potential probiotic Lactobacillus paracasei K5 strain incorporated in industrial white brined cheese as an adjunct culture. J. Food Sci. 2018, 83, 723–731.
  140. Jakobsen, R.A.; Heggebø, R.; Sunde, E.B.; Skjervheim, M. Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Food Microbiol. 2011, 28, 492–496.
  141. Regulation (EC) No 2073/2005 of 15 November 2005 on Microbiological Criteria for Foodstuffs. Available online: (accessed on 3 March 2021).
  142. Kalkan, S. Predicting the antimicrobial effect of probiotic lactic acid bacteria against Staphylococcus aureus in white cheeses, using Fourier series modeling method. J. Food Saf. 2020, 40, e12724.
  143. Prezzi, L.E.; Lee, S.H.; Nunes, V.M.; Corassin, C.H.; Pimentel, T.C.; Rocha, R.S.; Ramos, G.L.P.A.; Guimarães, J.T.; Balthazar, C.F.; Duarte, M.C.; et al. Effect of Lactobacillus rhamnosus on growth of Listeria monocytogenes and Staphylococcus aureus in a probiotic Minas Frescal cheese. Food Microbiol. 2020, 92, 103557.
  144. De Souza, G.T.; De Carvalho, R.J.; De Sousa, J.P.; Tavares, J.F.; Schaffner, D.; De Souza, E.L.; Magnani, M. Effects of the essential oil from Origanum vulgare L. on survival of pathogenic bacteria and starter lactic acid bacteria in semi hard cheese broth and slurry. J. Food Protec. 2016, 79, 246–252.
  145. Carvalho, R.J.; de Souza, G.T.; Honório, V.G.; de Sousa, J.P.; da Conceição, M.L.; Maganani, M.; de Souza, E.L. Comparative inhibitory effects of Thymus vulgaris L. essential oil against Staphylococcus aureus, Listeria monocytogenes and mesophilic starter co-culture in cheese-mimicking models. Food Microbiol. 2015, 52, 59–65.
  146. Ehsani, A.L.I.; Mahmoudi, R. Effects of Mentha longifolia L. essential oil and Lactobacillus casei on the organoleptic properties and on the growth of Staphylococcus aureus and Listeria monocytogenes during manufacturing, ripening and storage of Iranian white-brined cheese. Int. J. Dairy Technol. 2013, 66, 70–76.
  147. Arqués, J.L.; Rodríguez, E.; Gaya, P.; Medina, M.; Guamis, B.; Nunez, M. Inactivation of Staphylococcus aureus in raw milk cheese by combinations of high-pressure treatments and bacteriocin-producing lactic acid bacteria. J. App. Microbiol. 2005, 98, 254–260.
  148. Serraino, A.; Finazzi, G.; Marchetti, G.; Daminelli, P.; Riu, R.; Giacometti, F.; Rosmini, R. Behaviour of Salmonella typhimurium during production and storage of artisan water buffalo mozzarella cheese. Ital. J. An. Sci. 2012, 11, e53.
  149. Tamagnini, L.M.; De Sousa, G.B.; González, R.D.; Revelli, J.; Budde, C.E. Behavior of Yersinia enterocolitica and Salmonella typhimurium in Crottin goat’s cheese. Int. J. Food Microbiol. 2005, 99, 129–134.
  150. Alemdar, S.; Agaoglu, S. Survival of Salmonella typhimurium during the ripening of herby cheese (Otlu Peynir). J. Food Saf. 2010, 30, 526–536.
  151. Leuschner, R.G.; Boughtflower, M.P. Laboratory-scale preparation of soft cheese artificially contaminated with low levels of Escherichia coli O157, Listeria monocytogenes, and Salmonella enterica serovars Typhimurium, Enteritidis, and Dublin. J. Food Protect. 2002, 65, 508–514.
  152. Erkmen, O.; Bozo, T.F. Behaviour of Salmonella typhimurium in feta cheese during its manufacture and ripening. LWT 1995, 28, 259–263.
  153. Callon, C.; Arliguie, C.; Montel, M.C. Control of Shigatoxin-producing Escherichia coli in cheese by dairy bacterial strains. Food Microbiol. 2016, 53, 63–70.
  154. Ramsaran, H.; Chen, J.; Brunke, B.; Hill, A.; Griffiths, M.W. Survival of bioluminescent Listeria monocytogenes and Escherichia coli 0157:H7 in soft cheeses. J. Dairy Sci. 1998, 81, 1810–1817.
  155. Fretin, M.; Chassard, C.; Delbès, C.; Lavigne, R.; Rifa, E.; Theil, S.; Fernandez, B.; Laforce, P.; Callon, C. Robustness and efficacy of an inhibitory consortium against E. coli O26:H11 in raw milk cheeses. Food Control 2020, 115, 107282.
  156. Ioanna, F.; Quaglia, N.C.; Storelli, M.M.; Castiglia, D.; Goffredo, E.L.I.S.A.; Storelli, A.; de Rosa, M.; Normanno, G.; Jambrenghi, C.; Dambrosio, A. Survival of Escherichia coli O157:H7 during the manufacture and ripening of Cacioricotta goat cheese. Food Microbiol. 2018, 70, 200–205.
  157. Mehdizadeh, T.; Narimani, R.; Mojaddar Langroodi, A.; Moghaddas Kia, E.; Neyriz-Naghadehi, M. Antimicrobial effects of Zataria multiflora essential oil and Lactobacillus acidophilus on Escherichia coli O157 stability in the Iranian probiotic white-brined cheese. J. Food Saf. 2018, 38, e12476.
  158. Diniz-Silva, H.T.; Brandão, L.R.; de Sousa Galvão, M.; Madruga, M.S.; Maciel, J.F.; de Souza, E.L.; Magnani, M. Survival of Lactobacillus acidophilus LA-5 and Escherichia coli O157:H7 in Minas Frescal cheese made with oregano and rosemary essential oils. Food Microbiol. 2020, 86, 103348.
  159. Langa, S.; Martín-Cabrejas, I.; Montiel, R.; Peirotén, Á.; Arqués, J.L.; Medina, M. Protective effect of reuterin-producing Lactobacillus reuteri against Listeria monocytogenes and Escherichia coli O157:H7 in semi-hard cheese. Food Control 2018, 84, 284–289.
  160. Das, K.; Choudhary, R.; Thompson-Witrick, K.A. Effects of new technology on the current manufacturing process of yogurt-to increase the overall marketability of yogurt. LWT 2019, 108, 69–80.
  161. Gulmez, M.; Guven, A. Survival of Escherichia coli O157:H7, Listeria monocytogenes 4b and Yersinia enterocolitica O3 in different yogurt and kefir combinations as prefermentation contaminant. J. Appl. Microbiol. 2003, 95, 631–636.
  162. Massa, S.; Trovatelli, L.D.; Canganella, F. Survival of Listeria monocytogenes in yogurt during storage at 4 °C. Letters Appl. Microbiol. 1991, 13, 112–114.
  163. Benkerroum, N.; Oubel, H.; Ben Mimoun, L.A.M.I.A.E. Behavior of Listeria monocytogenes and Staphylococcus aureus in yogurt fermented with a bacteriocin-producing thermophilic starter. J. Food Protec. 2002, 65, 799–805.
  164. Al-Nabulsi, A.A.; Olaimat, A.N.; Osaili, T.M.; Ayyash, M.M.; Abushelaibi, A.; Jaradat, Z.W.; Shaker, R.; Al-Taani, M.; Holley, R.A. Behaviour of Escherichia coli O157: H7 and Listeria monocytogenes during fermentation and storage of camel yogurt. J. Dairy Sci. 2016, 99, 1802–1811.
  165. Bachrouri, M.; Quinto, E.J.; Mora, M.T. Survival of Escherichia coli O157:H7 during storage of yogurt at different temperatures. J. Food Sci. 2002, 67, 1899–1903.
  166. Savran, D.; Pérez-Rodríguez, F.; Halkman, A.K. Modelling survival of Salmonella enteritidis during storage of yoghurt at different temperatures. Int. J. Food Microbiol. 2018, 271, 67–76.
  167. Hervert, C.J.; Martin, N.H.; Boor, K.J.; Wiedmann, M. Survival and detection of coliforms, Enterobacteriaceae, and gram-negative bacteria in Greek yogurt. J. Dairy Sci. 2017, 100, 950–960.
  168. Bearson, S.; Bearson, B.; Foster, J.W. Acid stress responses in enterobacteria. FEMS Microbiol. Let. 1997, 147, 173–180.
  169. Martin, N.H.; Trmčić, A.; Hsieh, T.H.; Boor, K.J.; Wiedmann, M. The evolving role of coliforms as indicators of unhygienic processing conditions in dairy foods. Frontiers Microbiol. 2016, 7, 1549.
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