Biocontrol of Pathogenic Bacteria and Yeasts in Foods: Comparison
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Ripened foods of animal origin can be divided into two main groups: meat products (dry-cured pieces and dry-cured fermented products, the latter commonly made via mincing and stuffing) and dairy products (mainly, ripened cheeses). The environmental conditions throughout the ripening process of which these animal-derived products undergo favor the growth of diverse microbial populations that deeply contribute to their transformation. The presence of this beneficial microbiota is not unique in these products since they are generally exposed to the wild microbiota of the processing environment. Additionally, this processing rarely entails any sanitizing step; pasteurization in artisanal dairy products could be performed, although it is not common; for meat products, however, it is negligible. Thus, the contamination of these products with pathogenic  microorganisms usually leads to their development during the industrial ripening of these meat products. In this respect, bacteria such as Listeria monocytogenes, Salmonella spp., Staphylococcus aureus,

 Clostridium perfringens, Clostridium botulinum, Bacillus cereus and Escherichia coli are of most concern for ripened foods. In addition, fungal growth on their surface is also common, harboring some pathogenic yeasts such as Candida spp. Biocontrol strategies are required for controlling these hazards.
  • biocontrol agents
  • foodborne pathogens
  • dry-cured meat
  • ripened cheese

1. Pathogenic Bacteria in Ripened Foods and Biocontrol Strategies

1.1. Pathogenic Bacteria

It is important to monitor the growth of the microorganisms described below as they can grow in ripened food of animal origin that has not undergone any sanitizing process. Thus, these products will be mostly considered as ready-to-eat (RTE). The presence of the following described pathogens in these foods pose a considerable risk which must be controlled using different strategies, with BCAs being among the most appropriate ones.

1.1.1. Listeria monocytogenes

L. monocytogenes is a gram-positive, motile, facultative anaerobic bacterium that causes listeriosis. This foodborne pathogen can present flu-like symptoms such as fever, fatigue and gastrointestinal symptoms (nausea, vomiting and diarrhea). However, it can cause more severe life-threatening infections in high-risk population groups, such as septicemia, meningitis, meningoencephalitis, spontaneous abortion, still birth or fetal infection [46,47,48][1][2][3]. This pathogen has the capacity to pass three important barriers in the human host, namely the intestinal epithelium, the blood–brain barrier and the placenta, and subsequently disseminate to other organs [49][4].
There have been sixty-seven notifications since 2020 for milk and milk products in the whole of the European Union according to RASFF, of which about 50% were notifications in France for raw milk cheeses. Only eight notifications about the presence of L. monocytogenes in dry-cured meat products arose from diverse countries from the European Union [26][5]. In 2021 and 2022, among the total risks identified via the RASFF system, notifications due to the presence of L. monocytogenes in soft cheeses comprised 33.5% of the cases [26][5]. Specifically, in 2022, within biological contaminants, notifications due to L. monocytogenes accounted for 31.5%, with cheeses made with raw milk being involved in 57% of cases, with 100% of them originating in Europe and with France being the origin in 45.5% of cases.

1.1.2. Salmonella enterica

S. enterica is a gram-negative, motile bacterium that causes salmonellosis. Clinical manifestations are usually fever, weight loss, headache, lethargy, malaise, gastrointestinal bleeding, decreased white blood cells and platelets, and even neurological complications [46][1].
S. enterica invades the intestinal epithelium due to virulence factors that allow for intracellular multiplication in intestinal and immune cells such as macrophages. In this way, the bacteria reach the bloodstream, evading immune activity, and eventually reach the liver, spleen and bone marrow, where they continue to proliferate.
Eight cases of Salmonella in ripened cheese and sixteen cases in dry-cured meat products have been identified from 2020 to the present in the European Union [26][5].

1.1.3. Staphylococcus aureus

S. aureus is a gram-positive, nonmotile, coagulase-positive and ubiquitous bacterium. It can grow and produce thermostable enterotoxins resistant to digestive enzymes, which are responsible for staphylococcal food poisoning (SFP) [50,51][6][7]. The main symptoms of SFP are nausea, vomiting, diarrhea and abdominal pain [52][8], although more serious and life-threatening infections such as sepsis, necrotizing fasciitis, infective endocarditis, necrotizing pneumonia and toxic shock syndrome [53][9], although by far less common, are provoked directly by S. aureus invasion.
In fact, S. aureus has the ability to colonize the skin and mucous membranes of humans and warm-blooded animals. This bacterium has been isolated from a wide range of foods, such as fermented meat and cheese [54,55][10][11]. In addition, S. aureus has many virulence factors that enable for colonization, increasing its ability to trigger diseases [56][12].

1.1.4. Clostridium botulinum

C. botulinum is a gram-positive, obligatory anaerobic and spore-forming rod bacterium [57][13]. Ingestion of this preformed toxins can cause botulism with symptoms such as paralysis, nausea, vomiting, abdominal cramps, irritability, drooping eyelids, fatigue, difficulty feeding and swallowing [58][14].
Among the seven types of botulinum toxins (A to G), types A, B, E and F are well known to cause human illness. The severe form of food poisoning is rare, but it has a significant mortality rate [59][15].
One case of C. botulinum in ripened cheese has been reported since 2020 in the European Union [26][5].

1.1.5. Escherichia coli

E. coli is a gram-negative bacterium that is part of the intestinal microbiota. Symptoms are bloody diarrhea, abdominal pain, vomiting, hemorrhagic colitis, hemolytic uremic syndrome with acute renal failure, thrombotic thrombocytopenia purpura and even septicemia [60,61,62][16][17][18]. E. coli O157:H7 is one of the best-known serotypes to contain pathotypes that can cause food-borne infection in humans [46][1].
Since 2020, thirty-one reports of E. coli in milk and dairy products, with 90% coming from ripened cheese, have been made. Only two cases were reported for the presence of E. coli in cured and matured-meat products, namely in dry-cured sausages in Italy [26][5].

1.2. Microbial Biocontrol Strategies

In this section, biocontrol strategies for all pathogenic bacteria gathered in Section 2.1Section 1.1 are presented jointly, since most of them are used to control more than one pathogen, as displayed in Table 1, and this is how it is addressed in most of the reported studies [63,64][19][20].
Table 1.
Reduction of pathogenic bacteria viability using biocontrol agents in ripening food matrices of animal origin.
Matrix Pathogenic Bacteria Biocontrol Agent Pathogenic Bacteria Viability Reduction Reference
Spanish dry-cured fermented sausages Listeria monocytogenes Latilactobacillus sakei 197 1.77 log CFU g−1 [65][21]
Short-ripening Spanish traditional cheeses L. monocytogenes Lacticaseibacillus casei 116 2.2 log CFU g−1 [66][22]
Brazilian artisanal cheeses L. monocytogenes and

Staphylococcus aureus Lactiplantibacillus plantarum (1QB77) 3 and 2.3 log CFU g−1, respectively [67][23]
Frescal and semi-hard artisanal Minas microcheeses L. monocytogenes Levilactobacillus brevis

L. plantarum

Enterococcus faecalis Inactivation [36][24]
Dry-fermented Greek sausage L. monocytogenes and Escherichia coli L. sakei 8416

L. sakei 4413 2.2 log CFU g−1 [68][25]
Bryndza cheese Salmonella enterica and S. aureus Lactococcus lactis

Lactiplantibacillus paraplantarum Significative reduction [69][26]
Traditional dry-fermented sausage suçuk S. aureus L. sakei

Staphylococcus carnosus More than 2 log CFU g−1 [70][27]
Pediococcus acidilactici, Latilactobacillus curvatus, Staphylococcus xylosus More than 2 log CFU g−1
Fermented salami Clostridium perfringens and Clostridium species L. plantarum PCS20, Lactobacillus delbrueckii DSM 20074 2 and 1.5 log CFU g−1, respectively [71][28]
Dry fermented sausages E. coli, L. monocytogenes, Salmonella spp. and sulfite-reducing clostridia Juniperus communis L. Essential oil (EOs) Inactivation [72][29]
Dry cured sausage ‘Chouriço de vinho’ Salmonella spp., L. monocytogenes and S. aureus Bay, garlic, nutmeg, oregano, rosemary and thyme EOs 0.1–2 log CFU g−1 [42][30]
Dry cured sausage ‘Chouriço de vinho’ S. aureus Thyme EOs Inactivation [42][30]
Cured ham-based medium L. monocytogenes Cinnamon, pomegranate and strawberry extracts 3 log CFU mL−1 [73][31]
LAB are one of the most interesting groups of microorganisms that can be used as BCAs [74][32], mainly due to their recognized key role in fermented foods. Additionally, several strains belonging to species that are part of the LAB group have acquired QPS (Qualified Presumption of Safety) status [75][33]. Members of the genera Lactobacilli and members of the genera Lactococcus and Pediococcus were the most commonly explored, namely Latilactobacillus curvatus, L. sakei, Lactiplantibacillus plantarum, Limosilactobacillus fermentum, Lactococcus lactis and Pediococcus acidilactici [71,76,77,78][28][34][35][36]. Furthermore, LAB have frequently been used as starters or protective cultures due to their natural ability to dominate the microbial population of many foods. In fact, they are naturally found due to their ability to produce antimicrobial compounds, such as lactic acid and other organic acids, ethanol, diacetyl, carbon dioxide, hydrogen peroxide or bacteriocins [79,80][37][38]. The only approved bacteriocin for its use in certain ripened foods in the European Union is nisin, produced by L. lactis [81][39]. Pediocin, produced by Pediococcus is another type of bacteriocin which effectively preserves fermented food products such as meat, sausage products and cheeses [82][40].
Most of these metabolites act both individually and synergistically against pathogens [83][41]. It is known that LAB have a higher inhibition efficacy against pathogenic gram-positive bacteria [84][42]. Martín et al. [85][43] reported in vitro antibacterial activity of LAB isolated from traditional Spanish dry-cured fermented sausages and cheeses against L. monocytogenes (Table 1). When the biocontrol capacity of these strains was tested in traditional RTE ripened foods models, two of them were selected (Lacticaseibacillus casei 116 and L. sakei 205) because they provoked reductions higher than 2 log cycles of L. monocytogenes in cheeses and dry-cured fermented sausages models, respectively. In addition, when L. sakei 205 was inoculated into dry-cured fermented sausages, L. monocytogenes was reduced by 1.77 log CFU g−1 at the end of the ripening process of these products [65][21]. Furthermore, Martín et al. [86][44] demonstrated that the inoculation of this strain did not modify the sensory characteristics of dry-cured fermented sausages. L. casei 116 caused a decrease in L. monocytogenes of 2.2 log CFU g−1 when it was inoculated in short-ripening traditional cheeses without modifying their sensory properties [66,87][22][45]. Margalho et al. [67][23] indicated that greater than 3 log reduction in L. monocytogenes in Brazilian artisanal cheeses can be achieved using L. plantarum (1QB77) after 21 days of ripening. However, there have been no studies of sensory modifications due to the addition of this bacterium.
Campagnollo et al. [36][24] evaluated the inhibitory activity of LAB strains (Levilactobacillus brevis 2-392, L. plantarum 1-399 and 4 strains of E. faecalis (1-37, 2-49, 2-388 and 1-400)) against L. monocytogenes in microscale “Minas” Frescal and semi-hard cheese models. They demonstrated that the addition of a pool of LAB with antimicrobial properties resulted in bacteriostatic effects and inactivation of L. monocytogenes in “Minas” Frescal and “Minas” semi-hard cheeses, respectively. However, there are no available studies that display whether the inoculation of this pool of bacteria modifies the sensory characteristics of these products.
In dry-fermented Greek sausages, Pragalaki et al. [68][25] observed a significant inhibition of L. monocytogenes in the treatments with L. sakei 8416 and L. sakei 4413 compared to the untreated control. Furthermore, sausages produced with these LAB cultures obtained the highest scores for all sensory attributes in the study conducted by Baka et al. [88][46].
Kačániová et al. [69][26] studied the inhibitory capacity of 130 LAB isolated from “Bryndza” cheese. About 84% of the LAB isolates presented an inhibitory effect against S. enterica subsp. enterica and S. aureus subsp. aureus, with L. lactis subsp. lactis and Lactiplantibacillus paraplantarum being the most effective LAB strains to inhibit S. enterica subsp. enterica. Pragalaki et al. [68][25] observed a 2.2 log reduction in the E. coli O157:H7 population when L. sakei 4413 was inoculated in dry-fermented Greek sausage.
E. coli and S. aureus have been frequently studied as pathogens to be inhibited in ripened foods of animal origin. Inhibition of S. aureus growth by LAB has been related with the production of different compounds such as organic acids and bacteriocins, changes in redox potential, or combined effects of environmental stressors [89][47]. In a traditional dry-fermented sausage “suçuk”, the presence of L. sakei and Staphylococcus carnosus decreased S. aureus numbers from the first day on, and no S. aureus growth was observed [70][27]. In the presence of P. acidilactici, L. curvatus and Staphylococcus xylosus, a sub-inoculation level of S. aureus counts was determined from day 3 onwards. These results show that both starter culture preparations can reduce the growth of S. aureus at the initial ripening temperature [70][27]. Margalho et al. [67][23] studied a strain of L. plantarum (1QB77) with production of antimicrobial compounds isolated from a Brazilian artisan cheese (Minas Gerais), which showed an inhibition of S. aureus of approximately 2.3 log CFU g−1 in a microscale Cheeses model (microcheese).
The inoculation of L. plantarum PCS20 and L. delbrueckii DSM 20074 in fermented salami was able to reduce the levels of C. perfringens and Clostridium spp. by 2.0 and 1.5 log CFU g−1, respectively [71][28].
Excluding this reposeartch, there are scarce studies of BCAs being used against C. botulinum in these products; this is probably because of its development requirements—it is relatively easy to control with an HACCP using obstacle theory with a combination of aw, temperature and pH in each of the phases of the processing of these products [90][48]. Additionally, in meat products, the usual inclusion of nitrifying salts (sodium nitrate, potassium nitrate, potassium nitrite and sodium nitrite) confers a high protection against Clostridium species [91][49]. A novel and interesting field deserves to be explored in relation to the substitution of these salts via efficient clean-label strategies, since these preservatives have been related to colorectal cancer [92][50].
Concerning the use of yeasts as BCAs against pathogenic bacteria, some studies have shown the inhibitory effect of Debaryomyces hansenii, Candida spp., Geotrichum candidum and Pichia spp. against certain pathogenic microorganisms and, specifically, against L. monocytogenes [93,94][51][52]. However, most studies about yeasts with antibacterial activity are not carried out on dry-cured fermented food matrices. D. hansenii is one of the main yeasts found in dry-cured fermented meat products and cheeses because it is salt tolerant [3,95][53][54]. Nevertheless, Alía et al. [33][55] showed that D. hansenii 258H presented a limited action and even boosted L. monocytogenes growth in dry-cured ham slices. They also observed the upregulation of some key virulence genes and an unpleasant appearance of the product. Additionally, most of the research about the antibacterial activity of yeasts in ripened dairy products was executed using commercial culture media [96,97,98][56][57][58]. One study focusing on “Tilsit” cheese showed that the yeast Pichia norvegensis achieved a reduction of 1.5 log units (CFU cm−2) of L. monocytogenes in the product [95][54]. To summarize, the lack of studies on food matrices shows the need for further works focusing on how the yeasts act during processing and if they alter the technological or sensory characteristics.

1.3. Plant-Derivative Biocontrol Agents

Another biocontrol method to prevent the presence of pathogens is the use of plant derivatives, of which the most reported are EOs [99][59]. These EOs are aromatic and volatile oily extracts obtained from plant materials, including flowers, buds, roots, bark and leaves; they are composed of a mixture of phenylpropenes, terpenes and other volatile components such as thymol, carvacrol and eugenol, which are known for their high antimicrobial capacity [100,101][60][61]. The majority of EOs are safe for consumer use when used at the proper concentrations and have been generally recognized as safe (GRAS) [102][62]. The hydrophilic or lipophilic properties of EO constituents, type of microorganism studied and structure of their cell wall are the factors that affect the Eos’ antimicrobial activity [99][59]. Their application depends on the sensory impact of EOs that has been reported as one of the most negative aspects of their use [42][30].
The presence of Juniperus communis L. EO (0.01; 0.05 and 0.10 µL g−1) in fermented sausages inhibited the growth of foodborne pathogens such as E. coli, L. monocytogenes and Salmonella spp. and sulfite-reducing clostridia, although concentrations of more than 0.10 µL g−1 had an untypical flavor [72][29]. In another dry-cured sausage, ‘Chouriço de vinho’, the antimicrobial effect of EOs from herbs and spices traditionally used in seasoning against Salmonella spp., L. monocytogenes and S. aureus was assessed [42][30]. The bay, garlic, nutmeg, oregano, rosemary and thyme EOs at 0.005% (sensory-acceptable as assessed by consumers) reduced the counts of Salmonella spp. and L. monocytogenes in the first steps of drying. However, the thyme EO was the only one that completely inhibited the presence of S. aureus after 21 days [42][30]. Cinnamon, pomegranate and strawberry extracts were able to reduce the growth of L. monocytogenes in a study conducted on a cured ham-based medium. Cinnamon at 1% concentration was the most effective, reducing up to 3 log CFU mL−1 [73][31]. The incorporation of oregano EO in alginate films applied to slices of ham resulted in a reduction of up to 2.5 log CFU g−1 of L. monocytogenes [103][63]. Tea tree oil at a concentration of 0.25% was able to completely inhibit the growth of E. coli through several mechanisms of action [104][64]. On the other hand, S. aureus growth has been shown to be reduced, even at low concentrations of T-cadinol, which is present in a variety of essential plant oils and can lead to disintegration of the cell envelope and leakage of cytoplasm [105][65]. Ethanolic extract of rosemary leaves showed antimicrobial activity against Shigella sonnei, Salmonella Typhimurium and L. monocytogenes bacteria [106][66]. Rosemary EO showed inhibition and a bactericidal effect in vitro against S. aureus with a minimum bactericidal concentration of 5 μL mL−1 [107][67].
BCAs for the control of pathogenic bacteria in dry-cured ham and jerky have been little studied since these products are considered safe products due to their low water activity (aw) and salt content [108][68]. The inactivation of pathogens during cured ham processing has been demonstrated [109][69].

2. Pathogenic Yeasts in Ripened Foods and Biocontrol Strategies

2.1. Pathogenic Yeasts

Increasing interest exists in the biodiversity and ecology of yeasts in relation to various food products. This has been driven by the realization that yeasts can interact with other yeast species, as well as with other microorganisms in different ecosystems. These interactions may affect the roles that these fungi play in food [110][70]. The presence of yeasts in ripened foods, as well as their interaction with their autochthonous microbiota, is in most cases directly related to the improvement in the organoleptic characteristics of the final product [111,112][71][72]. In dry-cured meat products, both the proliferation of yeasts during the curing process and the addition of yeasts as starter cultures lead to improvements in texture and the production of pleasant volatile compounds [113][73]. All this is due to yeast metabolic processes of meat constituents, such as lipids and proteins [114][74]. As in meat products, yeasts are capable of deploying high metabolic activity in dairy products. Due to the variety of cheeses made from different types of milk with different maturation times, there are great physicochemical differences, which means that the microbiota, and in particular the kind of yeasts, vary from cheese to cheese.
D. hansenii is the predominant yeast species observed during the ripening of most cheeses [114][74], being present in 79% of all the cheeses in the study performed by Banjara et al. [115][75]. However, strains of Saccharomyces cerevisiae, Yarrowia lipolytica, G. candidum and Kluyveromyces marxianus have also been reported in cheese, although to a lower extent [113,114,115][73][74][75]. This is due to the aptitude of dairy yeasts for growing in the presence of a high salt concentration, low pH and low aw as well as its ability to metabolize lactic and citric acids [116,117,118][76][77][78]. On the other hand, the 91.9% of strains isolated from high moisture soft cheeses were classified as Geotrichum species. [119][79] (Table 2).
D. hansenii is also the dominant species in sausage manufacturing, being found at every manufacturing stage. Trichosporon ovoides, Y. lipolytica, Candida intermedia/curvata, C. parapsilosis, C. zeylanoides and Citeromyces matritensis are also present in Spanish fermented sausages, with most of them being psychrotrophic. C. intermedia/curvata, C. matritensis, C. zeylanoides and T. ovoides were detected only at the first stages of the sausage manufacturing process [120][80]. In Parma dry-cured ham, yeast species such as D. hansenii, Torulopsis candida and Torulopsis famata have been proved to be the predominant species. Studies of Spanish dry-cured ham showed that the yeast population profile changes significantly during processing. C. zeylanoides was the main species at the fresh stage (more than the 90% of isolates), but D. hansenii dominated the yeast population after the post-salting stage [121,122][81][82].
While yeasts are rarely associated with foodborne infections, a few studies have shown the presence of medically relevant yeast species in various cheeses. The presence of these fungi in some types of cheeses might be a regular cause of both economic and public health problems. Examples of yeasts with the ability to cause these problems include Candida spp., K. marxianus, G. candidum, D. hansenii and Pichia spp. [123][83], although wresearchers focused on a narrow population segment. Candida spp. are part of the normal human microbiota. They are commensal in healthy individuals but become pathogenic when the host’s defence system is compromised, causing conditions ranging from superficial mucosal to life-threatening systemic infections [117][77]. The genus Candida contains 163 species found in different ecosystems. Diseases are caused by some species such as C. albicans, C. tropicalis, C. krusei, C. glabrata, C. guilliermondii and C. parapsilosis [124][84]. To the general population, yeasts do not cause serious infections, though some species, such as C. albicans and Cryptococcus neoformans, are opportunistic pathogens that may cause infections in various organ systems, as well as general fungemia [116][76]. C. albicans, C. glabrata, C. parapsilosis and C. tropicalis are responsible for about 95% of Candida blood stream infections, although the vast majority of Candida spp. are not pathogenic [125][85]. It is known that contamination can occur due to a lack of attention to proper hand hygiene during milk production, or even due to improper cleaning of tools used to process milk and its derivatives [110,126][70][86].
Pathogenic species belonging to the genus Candida rarely occur in cheese. For instance, several Candida species, including C. albicans, have been found in cheese brine [127][87], but never in ripened cheese. However, Issatchenkia orientalis (teleomorph of C. krusei), Clavispora lusitaniae (teleomorph of C. lusitaniae) and Candida rugosa were seldom detected in cheese. There are some rare occurrences of species such as Candida famata/D. hansenii or C. krusei/I. orientalis in cheese [118][78]. When 120 samples from traditional Egyptian dairy products were analyzed, yeasts belonging to the Candida genus were identified [110][70] (Table 2). This raises the possibility that dairy products may be carrying pathogenic yeasts [110][70]. C. albicans was not reported in other analyses of yeast populations in cheese, but another opportunistic pathogenic yeast was reported in “feta” cheese [128][88] (Table 2). Although it has been found in brine [127][87], the source of these pathogenic yeasts in dairy products is not well known.
In a study analysing the microbial population of cheese, yeast species isolated from cheese were identified as C. parapsilosis, Candida catenulata, Y. lipolytica, Rhodotorula glutinis and Trichosporon species. C. parapsilosis, C. catenulata and Trichosporon spp. were also found in raw milk from different species and in several types of cheese. This is a public health concern, as it suggests that these species may survive some kind of cheese-making treatments and spread within the human population [129][89]. From the analysis of 45 artisanal cheese samples, a total of 251 Candida strains were isolated [126][86] (Table 2).
Candida non-albicans species were responsible for an increase in the proportion of cases of fungemia and other complex cases of candidiasis [130,131,132][90][91][92]. C. parapsilosis, isolated from some cheeses, is an emerging human pathogen capable of causing invasive candidiasis, but infection due to consumption of contaminated food has not been documented (Table 2). Y. lipolytica, isolated from cheese, is also an emerging opportunistic pathogen, although cases are rare [115][75] (Table 2). Some large-scale studies confirm that Y. lipolytica seldom causes infections. Only 4 isolates of Y. lipolytica were present among 6082 isolates from blood stream infections in 250 medical centers from 32 countries between 1992 and 2001 [133][93]. C. intermedia, rarely reported as a human pathogen, has been reported as one of the most predominant yeast species in some cheeses in which NaCl concentrations range from 2% to 8% (w/v) (Table 2).
Table 2.
The pathogenic capacity of yeasts isolated from different types of cheeses.
Type of Cheese Yeast Pathogenic Capacity Reference
Cottage and cream cheese Geotrichum species No [119][79]
Domiati and Kariesh cheese Candida albicans

Candida lusitaniae (teleomorph of Clavispora lusitaniae)

Candida catenulata Yes [110][70]
Feta cheese Candida tropicalis No [128][88]
Smeared cheese Issatchenkia orientalis (teleomorph of Candida krusei)

C. lusitaniae (teleomorph of C. lusitaniae) Candida rugosa

Candida famata (teleomorph of Debaryomyces hansenii) Yes [134][94]
Several types of cheeses Candida parapsilosis, C. catenulata, Yarrowia lipolytica, Rhodotorula glutinis and Trichosporon species Yes [129][89]
Artisanal cheese C. albicans and 97.6% as Candida non-albicans, distributed in 79.3% of C. krusei, 12.3% of C. glabrata and 6.0% of C. tropicalis No [126][86]
Swiss-type blue cheese,

Goat’s milk Cheddar		 C. parapsilosis No [115][75]
Manteca (Italian cheese) C. parapsilosis No [115][75]
Washed rind cheese Y. lipolytica No [115][75]
Camembert

Blue-veined cheeses		 Candida intermedia No [135][95]
According to the source of contamination of these potentially pathogenic yeasts, and considering the population segment to be protected, the first preventive measure within the HACCP plan should be the highest level of hygiene in the industries. This fact should be maximized in those kinds of cheeses that have not undergone thermal treatment, or in those industrial stages after this treatment.

2.2. Yeast Biocontrol Strategies Using Microorganisms

One of the most commonly used strategies is to exploit the capacity of some yeasts with QPS status, able to grow in ripened foods and endowed with antagonistic activity against other yeasts. Among these yeasts, D. hansenii is used in the production of ripened food of animal origin. This antagonistic capacity may be caused by the production of toxic proteins or glycoproteins called killer toxins or mycocins, which can kill sensitive yeast, but can be innocuous for consumers. Mycocin activity has been reported in more than 90 yeast species, and their presence is directly related with the presence of chromosomal or extrachromosomal genes (linear plasmids or viruses) [136][96]. This behaviour is not uniform among these species, nor can it be linked to sources of isolation [137][97]. Additionally, this killer phenotype is markedly affected by the substrate physicochemical characteristic where the yeast grows [117][77].
Several studies have reported the ability of mycocins from foodborne yeasts to kill pathogenic yeasts in vitro [138][98]. Killer activity by some yeasts against C. albicans was reported many years ago. Mycocins from D. hansenii have shown activity against opportunistic pathogenic including Candida species. [137][97]. The killer activity of D. hansenii against C. albicans and C. tropicalis in ripened cheeses was demonstrated. Therefore, these observations raise the possibility that D. hansenii could hamper Candida survival [117][77]. On the other hand, K. marxianus and Kluyveromyces lactis inhibited the growth of C. albicans isolated from “Tomme d’orchies” cheese [139][99].
LAB have long been used in dairy and meat products, providing microbial safety and organoleptic benefits. There are patented microorganisms, such as Lacticaseibacillus rhamnosus, for use as “yeast and mold control”, as well as L. plantarum. Some other LAB species, for e.g., Lactobacillus acidophilus and Limosilactobacillus reuteri, also show the capacity to inhibit yeasts producing metabolites with antifungal activity [116][76]. In a study conducted by Makki et al. [140][100], a protective culture combining a mixture of Lacticaseibacillus spp. and Lactiplantibacillus spp. had an effect on the outgrowth of D. hansenii, Meyerozyma guilliermondii and Torulaspora delbrueckii in “cottage” cheese.

2.3. Plant-Derivative Biocontrol Strategies

Concerning the use of plant-derived biocontrol agents, a leaf extract of Lawsonia inermis, an Indian herb, showed a very effective anti-candidal activity with differents sites of action, such as germ tube inhibition, protease, phospholipases and aspartate dehydrogenase inhibitory activity [141][101]. Solanum lycopersicum shows high levels of fungistatic activity against Candida spp., with its suggested mode of action being the targeting of the C. albicans ergosterol pathway via the upregulation of ergosterol genes [142][102]. A four percent Jugulans nigra extract is effective in eradicating C. albicans as clotrimazole due to juglone, an active component found in the black walnut tree [143][103]. The highest antimicrobial activity of clove (Syzygium aromaticum) against C. albicans was achieved at the concentration of 0.2% by causing damage to fungal membranes and cell walls [144,145][104][105]. Papaya seed extracts also cause apoptosis in Candida cells due to the oxidative stress created [146][106], with a similar effect to garlic oil (Allium sativum) against C. albicans [147][107]. Aloe vera, oregano leaf and grapefruit seed extract have all been shown to inhibit the growth of Candida species as well [116][76]. The inhibitory effect of Eugenia caryophyllata thumb leaf EOs on contaminating microorganisms of “Coalho” cheese was investigated, with the lowest minimum inhibitory concentration (MIC) level (200 µL mL−1) against C. albicans, C. parapsilosis and C. krusei being obtained [148][108].
Although these results are promising, it would be necessary to validate these effects of BCAs in food matrices. This should be performed in order to take into account the possible interaction of these agents with each of the ingredients of the cured products, which may modify their antimicrobial capacity. With regard to the effect on the organoleptic characteristics of the product, none of the above studies evaluated the effect on the sensory characteristics of the final product. If these extracts were to be used on an industrial scale, it would be necessary to assess these effects, as these are extracts and plants with a high organoleptic impact.

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