Toxigenic Molds in Ripened Foods and Biocontrol Strategies: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Jessie Wu and Version 1 by Mar Rodríguez.

Ripened foods of animal origin comprise meat products and dairy products, being transformed by the wild microbiota which populates the raw materials, generating highly appreciated products over the world. Together with this beneficial microbiota, toxigenic molds such as Penicillium spp. and Aspergillus spp., can contaminate these products and pose a risk for the consumers. Thus, effective strategies to hamper these hazards are required. Additionally, consumer demand for clean label products is increasing. Therefore, the manufacturing sector is seeking new efficient, natural, low-environmental impact and easy to apply strategies to counteract these microorganisms.

  • dry-cured meat
  • ripened cheese
  • molds
  • yeasts
  • lactic acid bacteria
  • essential oils
  • mycotoxins

1. Introduction

Some molds can cause a wide variety of human diseases such as allergic or invasive infections due to excessive inhalation of spores (mainly from Aspergillus spp.) or their transmission through infected wounds, as well as through the smoking of contaminated plants [149][1]. However, these infections are infrequent, and from the food safety view, the main problem associated with the mold contamination of ripened animal products is the production of mycotoxins, which are secondary metabolites with a wide range of toxic effects. The most important mycotoxins in dry-cured meat products are the ochratoxin A (OTA) and aflatoxins (AFs), due to their frequency and their toxicity, although other mycotoxins can be detected in these products, such as cyclopiazonic acid (CPA), sterigmatocystin (STG) and citrinin (CIT) [24,25][2][3]. Similarly, the abovementioned mycotoxins have also been described in cheeses as well as PR toxin, roquefortine C and patulin [23,150][4][5]. The main molds that produce mycotoxins in animal-origin ripening foods are described below.

2. Biocontrol Strategies against Ochratoxin A-Producing Molds

Ochratoxin A (OTA) can be produced by different species of Penicillium and Aspergillus, such as Penicillium nordicum, Penicillium verrucosum, Aspergillus westerdijkiae and Aspergillus carbonarius. Within these species, P. nordicum has been described as the main OTA producer in dry-cured meat products and cheeses [151][6]. This mycotoxin is nephrotoxic, hepatotoxic, teratogenic, immunotoxic and has been classified as a possible human carcinogen (group 2B) by the International Agency for Research on Cancer (IARC) [152,153,154][7][8][9]. Preserved meats and cheeses are the main contributors to dietary exposure to OTA in several European countries [154][9].
The biocontrol of ochratoxigenic molds employed in dry-cured meat products includes the use of starter and protective cultures which contain lactic acid bacteria (LAB),  gram-positive catalase-positive cocci (GCC+), yeasts and non-toxigenic molds, as displayed in Table 1 [31,37,155,156,157,158,159,160,161][10][11][12][13][14][15][16][17][18]. Different strains from Enterococcus faecium were demonstrated to control OTA production via growing P. nordicum in a dry-cured fermented sausage based medium, although they did not affect the OTA produced by P. verrucosum [157][14]. GCC+, as Staphylococcus xylosus, successfully decreased the OTA content using different strains of P. nordicum (Pn15, Pn92 and Pn856) a in dry-cured ham-based medium, although no effect was detected in sausages inoculated with the same strain of S. xylosus and Pn15 [31,160][10][17]. Fermented extracts developed from the fermentation of a meat model system (BFS) by L. plantarum and P. pentosaceus were able to totally eliminate the presence of P. nordicum and P. verrucosum using different concentrations depending on the bacterium and the mold strain tested [162][19]. Meftah et al. [159][16] revealed the ability of the yeasts Candida zeylanoides and Rhodotorula mucilaginosa to reduce the OTA concentration produced by P. nordicum and A. westerdijkiae in three matrices (ham, and dry-cured sausages with industrial and traditional processing). Other yeasts, such as Debaryomyces hansenii and Saccharomycopsis fibuligera, were able to completely inhibit the OTA produced by P. nordicum and Aspergillus ochraceus in speck, a typical meat product in the European Alpine area [37][11]. D. hansenii has also been displayed as an effective BCA against P. nordicum, P. verrucosum and A. westerdijkiae tested in other studies in dry-cured meat products or meat-model systems [31,159,161,163,164][10][16][18][20][21]. Additionally, the strain of D. hansenii used in some of these studies did not negatively modify the sensorial quality of dry-cured fermented sausages which contained it [30][22]. The non-toxigenic mold Penicillium chrysogenum, producer of the antifungal protein PgAFP, was proposed as a BCA against P. nordicum in a dry-cured ham-based medium [158][15] and in a meat-model system [165][23], showing in both studies possible nutrient competition. Similarly, this strain of P. chrysogenum controlled the growth of potentially ochratoxigenic molds, reducing the OTA accumulation in dry-cured Iberian hams which had undergone industrial processing [166][24]. This strain was also proposed as a good protective culture with no technological drawbacks during the ripening of dry-cured fermented sausages [30][22]. The protective potential of a commercial starter culture of Penicillium nalgiovense was displayed by the decrease in the OTA concentration produced by P. verrucosum in the dry-cured fermented sausage “salchichón” [167][25].
Table 1.
Main effects of biocontrol agents on toxigenic molds in ripening food matrices of animal origin.
Ochratoxin A (OTA) Producers
Matrix Mold Biocontrol Agent Effect on Growth or Mycotoxin Production Reference
Dry-cured fermented sausage medium Penicillium nordicum Enterococcus faecium ↓ 1 OTA

↓ Growth		 [157][14]
Dry-cured ham based medium P. nordicum Staphylococcus xylosus ↓ OTA

↓ Growth		 [160][17]
Fermented meat model system P. nordicum and

Penicillium verrucosum Lactiplantibacillus plantarum and Pediococcus pentosaceus ↓ Growth [162][19]
Ham, industrial and traditional dry-cured sausages P. nordicum and

Aspergillus westerdijkiaie Candida zeylanoides and Rothia mucilaginosa ↓ OTA

↓ Growth		 [159][16]
Speck P. nordicum and

Aspergillus ochraceus Debaryomyces hansenii and Saccharomycopsis fibuligera ↓ OTA

↓ Growth		 [37][11]
Dry-cured fermented sausages P. nordicum D. hansenii ↓ OTA [31,161,163][10][18][20]
Dry-cured meat model systems P. verrucosum,

P. nordicum D. hansenii ↓ OTA

↓ Growth		 [156,164][13][21]
Dry-cured fermented sausage medium A. westerdijkiae D. hansenii ↓ OTA [155][12]
Dry-cured ham based medium P. nordicum Penicillium chrysogenum ↓ OTA [158][15]
Meat model system P. nordicum P. chrysogenum ↓ OTA

↓ Growth		 [165][23]
Dry-cured Iberian ham Wild mycobiota containing OTA producer strains P. chrysogenum ↓ OTA [166][24]
Dry-cured fermented sausage P. verrucosum Penicillium nalgiovense ↓ OTA [167][25]
Dry-cured fermented sausage medium P. nordicum Rosemary and oregano leaves ↓ OTA [30][22]
Dry-cured fermented sausage medium P. nordicum Smoked paprika “pimentón” ↓ OTA [44][26]
Dry-cured fermented sausages P. nordicum Rosemary leaves ↓ OTA [163][20]
Dry-cured fermented sausage medium P. nordicum Rosemary leaves and rosemary essential oil (EO) ↓ OTA [40][27]
Cheeses P. nordicum Lactobacillus buchneri and Lacticaseibacillus casei ↓ OTA [168][28]
Aflatoxins (AFs) producers
Dry-cured ham based medium Aspergillus flavus S. xylosus ↓ AFB1

↓ Growth		 [160][17]
Dry-cured ham based medium Aspergillus parasiticus S. xylosus ↓ AFB1 and AFG1

↓ Growth		 [160][17]
Fermented meat model system A. flavus and A. parasiticus L. plantarum and P. pentosaceus ↓ Growth [162][19]
Dry-cured fermented sausages slices A. parasiticus D. hansenii + PgAFP + Pediococcus acidilactici ↓ AFB1 and AFG1

↓ Growth		 [169][29]
Dry-cured fermented sausages; dry-cured ham A. parasiticus D. hansenii ↓ AFB1 and AFG1 [39][30]
Dry-cured meat model system A. parasiticus Smoked paprika“pimentón” ↓ AFB1 and AFG1 [44][26]
Cheese slices A. parasiticus D. hansenii + PgAFP + P. acidilactici ↓ AFG1

↓ Growth		 [169][29]
Minas cheese formulation A. flavus Origanum vulgare EO ↓ Spores germination [170][31]
Cheese slices A. flavus Parsley EO ↓ Growth [171][32]
Kashar cheese A. parasiticus Thymol ↓ Growth [45][33]
Cyclopiazonic acid A (CPA) producers
Dry-cured ham-based model Penicillium griseofulvum S. xylosus ↓ CPA [160][17]
Fermented meat model system P. griseofulvum and Penicillium commune Lc. plantarum and P. pentosaceus ↓ Growth [162][19]
Dry-fermented sausage-based medium; dry-fermented sausages P. griseofulvum PgAFP ↓ CPA [34]
Edam cheese P. commune Clove, thyme, red thyme, litsea, cumin and marjoram eOs ↓ Growth [43][35]
Citrinin (CIT) producer
Arzúa-Ulloa cheese Penicillium citrinum Eugenol and thymol ↓ CIT [172][36]
Iranian and mozzarella cheeses P. citrinum Zataria multiflora Boiss EO ↓ CIT [173,174][37][38]
1 Arrows indicate reduction in growth, mycotoxin production or spore germination.
Regarding the use of plant derivatives as biocontrol agents, some studies demonstrated the efficiency of reducing OTA using ingredients from dry-cured meat sausages such as rosemary, oregano and smoked paprika “pimentón” [41,44][26][39]. Oregano and rosemary leaves added to a dry-cured fermented-sausage medium and “pimentón” to a meat-based medium decreased the amount of OTA produced by P. nordicum [41,44][26][39]. Rosemary leaves were able to decrease the mycotoxin produced by P. nordicum during dry-cured sausage ripening and, together with their essential oil, the OTA produced by A. westerdijkiae in a dry-cured fermented sausage based medium [40,163][20][27]. However, the sensorial impact of these biocontrol agents (BCAs) was not checked, although the concentrations of herb leaves used were expected to have no negative influence on consumer perceptions [41,163][20][39]. Additionally, other essential oils (EOs) such as basil EO, sage EO and oregano EO, and plant derivatives such as carvacrol and eugenol, have also been described as BCAs against ochratoxigenic molds in commercial culture media, but not in meat-based matrices [175[40][41],176], therefore its effectiveness in ripening products is not known yet.
On the other hand, there are few studies focused on the biocontrol of ochratoxigenic molds in cheeses, despite the fact that all kinds of ripened cheeses can be contaminated with this mycotoxin [150,168,177,178][5][28][42][43]. The use of LAB such as Lactobacillus buchneri and Lacticaseibacillus casei against P. nordicum in cheeses covered with films with the bacteria incorporated reached OTA reductions of up to 94%, although no sensory study was carried out to confirm their applicability [168][28]. Another study, which employed twenty-five strains of Lactiplantibacillus plantarum, one Lacticaseibacillus paracasei, one L. casei and one Lacticaseibacillus rhamnosus isolated from a Brazilian artisanal “Serrano Catarinense” cheese, showed the ability of these LAB to decrease the growth of P. nordicum in MRS agar, suggesting a possible future use as preservative agents during cheese manufacturing [179][44]. The lack of studies about the biocontrol of ochratoxigenic molds in cheeses opens up a new field of study necessary to reduce the risk posed by OTA presence in these ripened products.

3. Biocontrol Strategies against Aflatoxin-Producing Molds

AFs are highly toxic secondary metabolites produced by molds such as Aspergillus flavus, Aspergillus parasiticus and Aspergillus nomius [180][45]. Although these fungi are more frequent in cereal crops, they can colonize the surface of ripening products of animal origin [181,182,183][46][47][48]. The most important AFs are B1, B2, G1 and G2. These mycotoxins are carcinogenic (Group 1) and mutagenic for animals and humans according to the IARC [152][7].
Similar to the strategies employed against ochratoxigenic molds, different LAB, GCC+ and yeasts have been studied as BCAs against AF producers in dry-cured meat products. S. xylosus Sx8 was able to control the growth and the AFB1 produced by A. flavus and AFB1 and AFG1 produced by A. parasiticus in a dry-cured ham-based medium at three different temperatures (15, 20 and 25 °C) [160][17]. The BFS extract from L. plantarum and Pediococcus pentosaceus reduced the growth of A. flavus and A. parasiticus in a meat model system by up to 50% using concentrations between 21 and 43 g L−1 [162][19]. D. hansenii combined with the antifungal protein PgAFP and Pediococcus acidilactici on slices of dry-cured fermented sausages successfully diminished AFB1 and AFG1 amounts produced by A. parasiticus and the mold counts [169][29]. In another study, D. hansenii was tested against A. parasiticus and decreased the AFB1 in more than 53.85% and the AFG1 by up to 59.06% in dry-fermented sausages, while the AFG1 was below the limit of quantification in dry-cured ham [39][30].
Regarding the agents of plant origin, the smoked paprika “pimentón” reduced the AFB1 and AFG1 production by A. parasiticus in a dry-cured meat model system, although they did not decrease the mold’s growth [44][26].
The presence of AFs in cheeses has been described worldwide. In addition to the AFM1 that can be present in the milk used for cheese manufacturing, common aflatoxins have been detected due to the surface colonization of the product by aflatoxigenic molds [23,184,185,186][4][49][50][51]. Despite the risk that AFs pose in cheeses, there are only a few studies based on the biocontrol of AFs in this matrix. In cheese slices, the use of the protein PgAFP combined with D. hansenii in the presence or absence of P. acidilactici decreased the A. parasiticus growth and its AFG1 production below the method’s limit of detection [169][29]. On the other hand, the addition of Oreganum vulgare EO (0.02% v/v) to the Minas cheese formulation inhibited the germination of spores of A. flavus for up to 15 days of ripening, and the cheese flavor and taste were accepted by the panelists [170][31]. Moreover, Vitalini et al. [171][32] demonstrated that parsley EO applied on cheese slices was effective in preventing A. flavus growth. Tatlisu et al. [45][33] demonstrated the antifungal activity of thymol (main component of numerous EOs) and nanofibers with thymol applied to “kashar” cheese cube surfaces against A. parasiticus, although no sensory analyses were performed [45][33].

4. Biocontrol Strategies against Cyclopiazonic Acid-Producing Molds

CPA can be produced by different molds, such as A. flavus, A. parasiticus and Penicillium griseofulvum, in ripened meats, and mainly Penicillium commune, Penicillium roqueforti and Penicillium camemberti in cheeses [24,182,187][2][47][52]. Due to the little amount of toxicological data, the IARC has not declared an acceptable CPA toxicity level yet, but it is well known that it includes sever gastrointestinal and neurological disorders and organ necrosis [188][53]. Therefore, this lack of data and legal limits results in a shortage of studies about the biocontrol of molds that only produce CPA.
Concerning the biocontrol studies in dry-cured meat products, the bacterium S. xylosus Sx8 decreased CPA production using two strains of P. griseofulvum grown in a dry-cured ham-based medium after 30 days of incubation at 25 °C [160][17]. Concentrations of 85 g L−1 of BFS extract from L. plantarum and between 21 and 85 g L−1 from P. pentosaceus did not allow for the growth of P. griseofulvum and P. commune in a meat model system [162][19]. Moreover, Delgado et al. [34] showed that P. chrysogenum, producer of the antifungal protein PgAFP, was able to diminish CPA amounts produced by P. griseofulvum under the limit of detection on a dry-fermented sausage-based medium and more than 97% on dry-cured fermented sausages after 21 days following industrial ripening [34].
In Edam cheeses, the clove, thyme, red thyme and litsea EOs completely inhibited the growth of two CPA producer strains of P. commune, while cumin and marjoram EOs showed high antifungal activity, although they did not totally inhibit the growth of the molds [43][35]. In this restudy, earch, the evaluators recognized some EOs in sensory evaluation via the triangle test, but they did not have a negative effect on the taste and smell of the treated cheeses [43][35].

5. Biocontrol Strategies against Sterigmatocystin-Producing Molds

STG is a precursor of AFB1, so the producing molds mainly include different Aspergillus species, although there are other ones such as Eurotium, Fusarium and Podospora spp., which demonstrate an ability to produce this mycotoxin [189][54]. Concerning its toxicity, it has been found that STG induces tumors in animals and humans [189][54]. In spite of this evidence, the IARC only classified STG into Group 2B (possible human carcinogen) [190][55].
Regarding the biocontrol strategies, the BCA against AF producers could be applied for the toxigenic molds which produce both mycotoxins (AFs and STG), but STG production deserves to be further studied. Within the ripened animal products, STG has been mainly described in a wide range of cheeses contaminated with Aspergillus versicolor, A. flavus or A. parasiticus [189,191][54][56]. However, there are no studies of ripened matrices of animal origin based on the biocontrol of molds that only produce STG, although EOs from tarragon, oregano and savory showed the inhibition of two producers of STG isolated from cheeses, Aspergillus puulaauensis and Aspergillus jenseii [192][57].

6. Biocontrol Strategies against Citrinin-Producing Molds

Citrinin (CIT) is produced by different species of Penicillium and Aspergillus, including P. cambemberti, Penicillium expansum, P. verrucosum, Penicillium citrinum, Penicillium viridicatum Aspergillus carneus and Aspergillus niveus [23][4]. Several studies have shown frequent cooccurrence of OTA and CIT in dry-cured meat products and cheeses [25,193][3][58]. CIT is nephrotoxic and hepatotoxic to humans and has been classified into Group 3 by the IARC [190][55] due to evidence of its in vivo carcinogenicity [194,195][59][60].
Given that some toxigenic strains can produce both OTA and CIT, the strategies to prevent OTA producers may also be effective for CIT accumulation. However, it must be considered that some molds can switch the production of OTA to CIT or vice versa to deal with different stressful environments [196,197][61][62]. Therefore, different strategies might be needed for reducing both mycotoxins. To our knowledge, there are no studies only focused on the biocontrol of this mycotoxin in dry-cured meat products. However, in cheeses a concentration of 150 µg mL−1 of eugenol and thymol inhibited CIT production by P. citrinum in “Arzúa-Ulloa” cheese, while in “Cabreriro” cheese these antifungal agents did not affect the CIT amounts [172][36]. In other studies, the Zataria multiflora Boiss EO decreased the growth and CIT production by P. citrinum in Iranian cheese and mozzarella [173,174][37][38]. Despite the use of EOs and compounds with a strong flavor in the above-mentioned studies, only the organoleptic effect of Zataria multiflora Boiss EO was tested. Concentrations over 600 ppm, which were more effective against CIT production, were disliked by the consumers and, consequently, their applications were limited [174][38].
Despite the studies about the presence of mycotoxins in ripened products of animal origin, no notifications were made regarding the presence of mycotoxins in both meat and dairy products (RASFF).

References

  1. Shabeer, S.; Asad, S.; Jamal, A.; Ali, A. Aflatoxin contamination, its impact and management strategies: An updated review. Toxins 2022, 14, 307.
  2. Lešić, T.; Vulić, A.; Vahčić, N.; Šarkanj, B.; Hengl, B.; Kos, I.; Polak, T.; Kudumija, N.; Pleadin, J. The Occurrence of five unregulated mycotoxins most important for traditional dry-cured meat products. Toxins 2022, 14, 476.
  3. Markov, K.; Pleadin, J.; Bevardi, M.; Vahčić, N.; Sokolić-Mihalak, D.; Frece, J. Natural occurrence of aflatoxin B1, ochratoxin A and citrinin in Croatian fermented meat products. Food Control 2013, 34, 312–317.
  4. Dobson, A.D.W. Mycotoxins in Cheese. In Cheese. Chemistry, Physics & Microbiology; McSweeney, P.L.H., Fox, P.F., Cotter, P.D., Everett, D.W., Eds.; Academic Press: Cambridge, MA, USA; Elsevier Ltd.: Amsterdam, The Netherlands, 2017; Volume 1, ISBN 9780122636530.
  5. Pattono, D.; Grosso, A.; Stocco, P.P.; Pazzi, M.; Zeppa, G. Survey of the presence of patulin and ochratoxin A in traditional semi-hard cheeses. Food Control 2013, 33, 54–57.
  6. Malir, F.; Ostry, V.; Pfohl-Leszkowicz, A.; Malir, J.; Toman, J. Ochratoxin A: 50 years of research. Toxins 2016, 8, 12–15.
  7. IARC Aflatoxins. A Review of Human Carcinogens. Chemical Agents and Related Occupations; IARC: Lyon, France, 2012; pp. 225–248. ISBN 978 92 832 1323 9.
  8. IARC; Ochratoxin, A. IARC Monogr Eval Carcinog Risk Chem to Humans; IARC: Lyon, France, 1993; pp. 489–521.
  9. Schrenk, D.; Bodin, L.; Chipman, J.K.; del Mazo, J.; Grasl-Kraupp, B.; Hogstrand, C.; Hoogenboom, L.; Leblanc, J.; Nebbia, C.S.; Nielsen, E.; et al. Risk assessment of ochratoxin A in food. EFSA J. 2020, 18, 6113.
  10. Cebrián, E.; Núñez, F.; Álvarez, M.; Roncero, E.; Rodríguez, M. Biocontrol of ochratoxigenic Penicillium nordicum in dry-cured fermented sausages by Debaryomyces hansenii and Staphylococcus xylosus. Int. J. Food Microbiol. 2022, 375, 109744.
  11. Iacumin, L.; Manzano, M.; Andyanto, D.; Comi, G. Biocontrol of ochratoxigenic moulds (Aspergillus ochraceus and Penicillium nordicum) by Debaryomyces hansenii and Saccharomycopsis fibuligera during speck production. Food Microbiol. 2017, 62, 188–195.
  12. Álvarez, M.; Núñez, F.; Delgado, J.; Andrade, M.J.; Rodrigues, P. Proteomic evaluation of the effect of antifungal agents on Aspergillus westerdijkiae ochratoxin A production in a dry-cured fermented sausage-based medium. Int. J. Food Microbiol. 2022, 379, 109858.
  13. Álvarez, M.; Delgado, J.; Núñez, F.; Cebrián, E.; Andrade, M.J. Proteomic analyses reveal mechanisms of action of biocontrol agents on ochratoxin A repression in Penicillium nordicum. Food Control 2021, 129, 108232.
  14. Álvarez, M.; Rodríguez, A.; Peromingo, B.; Núñez, F.; Rodríguez, M. Enterococcus faecium: A promising protective culture to control growth of ochratoxigenic moulds and mycotoxin production in dry-fermented sausages. Mycotoxin Res. 2019, 36, 137–145.
  15. Delgado, J.; Núñez, F.; Asensio, M.A.; Owens, R.A. Quantitative proteomic profiling of ochratoxin A repression in Penicillium nordicum by protective cultures. Int. J. Food Microbiol. 2019, 305, 108243.
  16. Meftah, S.; Abid, S.; Dias, T.; Rodrigues, P. Effect of dry-sausage starter culture and endogenous yeasts on Aspergillus westerdijkiae and Penicillium nordicum growth and OTA production. LWT—Food Sci. Technol. 2018, 87, 250–258.
  17. Cebrián, E.; Núñez, F.; Gálvez, F.J.; Delgado, J.; Bermúdez, E.; Rodríguez, M. Selection and evaluation of Staphylococcus xylosus as a biocontrol agent against toxigenic moulds in a dry-cured ham model system. Microorganisms 2020, 8, 793.
  18. Simoncini, N.; Virgili, R.; Spadola, G.; Battilani, P. Autochthonous yeasts as potential biocontrol agents in dry-cured meat products. Food Control 2014, 46, 160–167.
  19. Nazareth, T.D.M.; Calpe, J.; Luz, C.; Mañes, J. Manufacture of a potential antifungal ingredient using lactic acid bacteria from dry-cured sausages. Foods 2023, 12, 1427.
  20. Álvarez, M.; Delgado, J.; Núñez, F.; Roncero, E.; Andrade, M.J. Proteomic approach to unveil the ochratoxin A repression by Debaryomyces hansenii and rosemary on Penicillium nordicum during dry-cured fermented sausages ripening. Food Control 2022, 137, 108695.
  21. Peromingo, B.; Núñez, F.; Rodríguez, A.; Alía, A.; Andrade, M.J. Potential of yeasts isolated from dry-cured ham to control ochratoxin A production in meat models. Int. J. Food Microbiol. 2018, 268, 73–80.
  22. Álvarez, M.; Andrade, M.J.; García, C.; Rondán, J.J.; Núñez, F. Effects of preservative agents on quality attributes of dry-cured fermented sausages. Foods 2020, 9, 1505.
  23. Álvarez, M.; Núñez, F.; Delgado, J.; Andrade, M.J.; Rodríguez, M.; Rodríguez, A. Competitiveness of three biocontrol candidates against ochratoxigenic Penicillium nordicum under dry-cured meat environmental and nutritional conditions. Fungal. Biol. 2021, 129, 108232.
  24. Rodríguez, A.; Bernáldez, V.; Rodríguez, M.; Andrade, M.J.; Núñez, F.; Córdoba, J.J. Effect of selected protective cultures on ochratoxin A accumulation in dry-cured Iberian ham during its ripening process. LWT—Food Sci. Technol. 2015, 60, 923–928.
  25. Bernáldez, V.; Córdoba, J.J.; Rodríguez, M.; Cordero, M.; Polo, L.; Rodríguez, A. Effect of Penicillium nalgiovense as protective culture in processing of dry-fermented sausage “ salchichón”. Food Control 2013, 32, 69–76.
  26. Sánchez-Montero, L.; Córdoba, J.J.; Alía, A.; Peromingo, B.; Núñez, F. Effect of Spanish smoked paprika “Pimentón de La Vera” on control of ochratoxin A and aflatoxins production on a dry-cured meat model system. Int. J. Food Microbiol. 2019, 308, 108303.
  27. Álvarez, M.; Andrade, M.J.; Delgado, J.; Núñez, F.; Román, Á.C.; Rodrigues, P. Rosmarinus officinalis reduces the ochratoxin A production by Aspergillus westerdijkiae in a dry-cured fermented sausage-based medium. Food Control 2023, 145, 109436.
  28. Guimarães, A.; Ramos, Ó.; Cerqueira, M.; Venâncio, A.; Abrunhosa, L. Active whey protein edible films and coatings incorporating Lactobacillus buchneri for Penicillium nordicum control in cheese. Food Bioprocess Technol. 2020, 13, 1074–1086.
  29. Delgado, J.; Rodríguez, A.; García, A.; Núñez, F.; Asensio, M. Inhibitory effect of PgAFP and protective cultures on Aspergillus parasiticus growth and aflatoxins production on dry-fermented sausage and cheese. Microorganisms 2018, 6, 69.
  30. Peromingo, B.; Andrade, M.J.; Delgado, J.; Sánchez-Montero, L.; Núñez, F. Biocontrol of aflatoxigenic Aspergillus parasiticus by native Debaryomyces hansenii in dry-cured meat products. Food Microbiol. 2019, 82, 269–276.
  31. Leonelli Pires de Campos, A.C.; Saldanha Nandi, R.D.; Scandorieiro, S.; Gonçalves, M.C.; Reis, G.F.; Dibo, M.; Medeiros, L.P.; Panagio, L.A.; Fagan, E.P.; Takayama Kobayashi, R.K.; et al. Antimicrobial effect of Origanum vulgare (L.) essential oil as an alternative for conventional additives in the Minas cheese manufacture. LWT—Food Sci. Technol. 2022, 157, 113063.
  32. Vitalini, S.; Nalbone, L.; Bernardi, C.; Iriti, M.; Costa, R.; Cicero, N.; Giarratana, F.; Vallone, L. Ginger and parsley essential oils: Chemical composition, antimicrobial activity, and evaluation of their application in cheese preservation. Nat. Prod. Res. 2022, 1–6.
  33. Tatlisu, N.B.; Yilmaz, M.T.; Arici, M. Fabrication and characterization of thymol-loaded nanofiber mats as a novel antimould surface material for coating cheese surface. Food Packag. Shelf Life 2019, 21, 100347.
  34. Delgado, J.; Peromingo, B.; Rodríguez, A.; Rodríguez, M. Biocontrol of Penicillium griseofulvum to reduce cyclopiazonic acid contamination in dry-fermented sausages. Int. J. Food Microbiol. 2019, 293, 1–6.
  35. Hlebová, M.; Foltinová, D.; Vešelényiová, D.; Medo, J.; Šramková, Z.; Tančinová, D.; Mrkvová, M.; Hleba, L. The vapor phase of selected essential oils and their antifungal activity in vitro and in situ against Penicillium commune, a common contaminant of cheese. Foods 2022, 11, 3517.
  36. Vázquez, B.I.; Fente, C.; Franco, C.M.; Vazquez, M.J.; Cepeda, A. Inhibitory effects of eugenol and thymol on Penicillium citrinum strains in culture media and cheese. Int. J. Food Microbiol. 2001, 67, 157–163.
  37. Akrami, F.; Misaghi, A.; Gheisari, H.; Akhondzadeh, A.; Amiri, A.; Razi, S.; Derakhshan, Z.; Dehghani, R. The effect of Zataria multi flora Boiss essential oil on the growth and citrinin production of Penicillium citrinum in culture media and cheese. Food Chem. Toxicol. 2018, 118, 691–694.
  38. Noori, N.; Yahyaraeyat, R.; Khosravi, A.; Atefi, P.; Basti, A.A.; Akrami, F.; Bahonar, A.; Misaghi, A.L.I. Effect of Zataria multiflora Boiss essential oil on growth and citrinin production by Penicillium citrinum in culture media and mozzarella cheese. J. Food Sci. 2012, 32, 445–451.
  39. Álvarez, M.; Rodríguez, A.; Núñez, F.; Silva, A.; Andrade, M.J. In vitro antifungal effects of spices on ochratoxin A production and related gene expression in Penicillium nordicum on a dry-cured fermented sausage medium. Food Control 2020, 114, 107222.
  40. Schlösser, I.; Prange, A. Effects of selected natural preservatives on the mycelial growth and ochratoxin A production of the food-related moulds Aspergillus westerdijkiae and Penicillium verrucosum. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess 2019, 36, 1411–1418.
  41. Císarová, M.; Hleba, L.; Medo, J.; Tančinová, D.; Mašková, Z.; Čuboň, J.; Kováčik, A.; Foltinová, D.; Božik, M.; Klouček, P. The in vitro and in situ effect of selected essential oils in vapour phase against bread spoilage toxicogenic aspergilli. Food Control 2020, 110, 107007.
  42. Gützkow, K.L.; Al Ayoubi, C.; Soler Vasco, L.; Rohn, S.; Maul, R. Analysis of ochratoxin A, aflatoxin B1 and its biosynthetic precursors in cheese—Method development and market sample screening. Food Control 2022, 143, 109241.
  43. Rodríguez-Cañás, I.; González-Jartín, J.M.; Alvariño, R.; Alfonso, A.; Vieytes, M.R.; Botana, L.M. Detection of mycotoxins in cheese using an optimized analytical method based on a QuEChERS extraction and UHPLC-MS/MS quantification. Food Chem. 2023, 408, 135182.
  44. Mareze, J.; Ramos-Pereira, J.; Santos, J.A.; Beloti, V.; López-Díaz, T.M. Identification and characterisation of lactobacilli isolated from an artisanal cheese with antifungal and antibacterial activity against cheese spoilage and mycotoxigenic Penicillium spp. Int. Dairy J. 2022, 130, 105367.
  45. Kumar, P.; Mahato, D.K.; Kamle, M.; Mohanta, T.K.; Kang, S.G. Aflatoxins: A global concern for food safety, human health and their management. Front. Microbiol. 2017, 7, 2170.
  46. Pleadin, J.; Zadravec, M.; Brnić, D.; Perković, I.; Škrivanko, M.; Kovačević, D. Moulds and mycotoxins detected in the regional speciality fermented sausage “slavonski kulen” during a 1-year production period. Food Addit. Contam. Part A 2017, 34, 282–290.
  47. Perrone, G.; Rodriguez, A.; Magistá, D.; Magan, N. Insights into existing and future fungal and mycotoxin contamination of cured meats. Curr. Opin. Food Sci. 2019, 29, 20–27.
  48. Zadravec, M.; Vahčić, N.; Brnić, D.; Markov, K.; Frece, J.; Beck, R.; Lešić, T.; Pleadin, J. A study of surface moulds and mycotoxins in Croatian traditional dry-cured meat products. Int. J. Food Microbiol. 2020, 317, 108459.
  49. Carvajal-Moreno, M.; Vargas-Ortiz, M.; Hernández-Camarillo, E.; Ruiz-Velasco, S.; Rojo-Callejas, F. Presence of unreported carcinogens, Aflatoxins and their hydroxylated metabolites, in industrialized Oaxaca cheese from Mexico City. Food Chem. Toxicol. 2019, 124, 128–138.
  50. Onmaz, N.E.; Çinicioglu, S.; Gungor, C. Moulds and aflatoxins in traditional moldy civil cheese: Presence and public health concerns. J. Hell. Vet. Med. Soc. 2020, 85, 3–11.
  51. Sakin, F.; Tekeli, İ.O.; Yipel, M.; Kürekci, C. Occurrence and health risk assessment of aflatoxins and ochratoxin a in Sürk, a Turkish dairy food, as studied by HPLC. Food Control 2018, 90, 317–323.
  52. Maragos, C.M.; Probyn, C.; Proctor, R.H.; Sieve, K.K. Cyclopiazonic acid in soft-ripened and blue cheeses marketed in the USA. Food Addit. Contam. Part B 2023, 16, 14–23.
  53. Ostry, V.; Toman, J.; Grosse, Y.; Malir, F. Cyclopiazonic acid: 50th anniversary of its discovery. World Mycotoxin J. 2018, 11, 135–148.
  54. Díaz Nieto, C.H.; Granero, A.M.; Zon, M.A.; Fernández, H. Sterigmatocystin: A mycotoxin to be seriously considered. Food Chem. Toxicol. 2018, 118, 460–470.
  55. IARC. Agents Classified by the IARC Monographs, Volumes 1–123; International Agency for Research on Cancer: Lyon, France, 2018; pp. 1–37.
  56. Pietri, A.; Leni, G.; Mulazzi, A.; Bertuzzi, T. Ochratoxin A and sterigmatocystin in long-ripened Grana cheese: Occurrence, wheel rind contamination and effectiveness of cleaning techniques on grated products. Toxins 2022, 14, 306.
  57. Muñoz-Tebar, N.; González-Navarro, E.J.; López-Díaz, T.M.; Santos, J.A.; Ortiz de Elguea-Culebras, G.; García-Martínez, M.M.; Molina, A.; Carmona, M.; Berruga, M.I. Biological activity of extracts from aromatic plants as control agents against spoilage molds isolated from sheep cheese. Foods 2021, 10, 1576.
  58. Coton, M.; Au, A.; Poirier, E.; Debaets, S.; Coton, E.; Dantigny, P. Production and migration of ochratoxin A and citrinin in Comté cheese by an isolate of Penicillium verrucosum selected among Penicillium spp. mycotoxin producers in YES medium. Food Microbiol. 2019, 82, 551–559.
  59. Gayathri, L.; Dhivya, R.; Dhanasekaran, D.; Periasamy, V.S.; Alshatwi, A.A.; Akbarsha, M.A. Hepatotoxic effect of ochratoxin A and citrinin, alone and in combination, and protective effect of vitamin E: In vitro study in HepG2 cell. Food Chem. Toxicol. 2015, 83, 151–163.
  60. Kamle, M.; Mahato, D.K.; Gupta, A.; Pandhi, S.; Sharma, N.; Sharma, B.; Mishra, S.; Arora, S.; Selvakumar, R.; Saurabh, V.; et al. Citrinin mycotoxin contamination in food and feed: Impact on agriculture, human health, and detection and management strategies. Toxins 2022, 14, 85.
  61. Schmidt-Heydt, M.; Stoll, D.; Schütz, P.; Geisen, R. Oxidative stress induces the biosynthesis of citrinin by Penicillium verrucosum at the expense of ochratoxin. Int. J. Food Microbiol. 2015, 192, 1–6.
  62. Schmidt-Heydt, M.; Graf, E.; Stoll, D.; Geisen, R. The biosynthesis of ochratoxin A by Penicillium as one mechanism for adaptation to NaCl rich foods. Food Microbiol. 2012, 29, 233–241.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Video Production Service
Feedback