Spontaneous Food Fermentations and Potential Risks for Human Health
Abstract
:1. Fermented Foods and Beverages: Scientific Dimension, Social Relevance, and Economic Significance
2. The Microbiology of Fermented Foods and Beverages: “Microbiodiversity”, Impact on Food Qualities and on Human Health
3. Risks for Human Health Associated with Fermentations
4. Spontaneous Versus Induced Fermentation: Starter Cultures, Scientific Evidence and Actual Trends
5. How to Conciliate Fermented Food Safety with Instances of an Enhanced Contribution of Microbes Associated to Spontaneous Fermentation
6. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Major Groups Global Fermented Foods | Fermented Product (Raw Material, Geographical Diffusion): Microorganisms Involved in the Fermentation Process |
---|---|
(a) Fermented cereals | Sourdough (Rye, wheat; America, Europe, Australia): Lb. sanfranciscensis, Lb. alimentarius, Lb. buchneri, Lb. casei, Lb. delbrueckii, Lb. fructivorans, Lb. plantarum, Lb. reuteri, Lb. johnsonii, Cand. humili, Issatchenkia orientalis |
Ogi (Maize, sorghum, millet; Nigeria): Lb. plantarum, Lb. pantheris, Lb. vaccinostercus, Corynebacterium sp., Aerobacter sp., Candida krusei, Clavispora lusitaniae, Sacch. cerevisiae, Rhodotorula sp., Cephalosporium sp., Fusarium sp., Aspergillus sp., Penicillium sp. | |
Idli (Rice, black gram or other dehusked pulses; India, Sri Lanka, Malaysia, Singapore): Leuc. mesenteroides, Lb. delbrueckii, Lb. fermenti, Lb. coryniformis, Ped. acidilactis, Ped. cerevisae, Streptococcus sp., Ent. faecalis, Lact. lactis, B. amyloliquefaciens, Cand. cacaoi, Cand. fragicola, Cand. glabrata, Cand. kefyr, Cand. pseudotropicalis, Cand. sake, Cand. tropicalis, Deb. hansenii, Deb. tamarii, Issatchenkia terricola, Rhiz. graminis, Sacch. cerevisiae, Tor. candida, Tor. holmii | |
(b) Fermented vegetables and bamboo shoots | Table Olives (Olive; USA, Spain, Portugal, Italy, Greece, Peru, Chile): Leuc. mesenteroides, Ped. pentosaceus; Lb. plantarum Lb. pentosus/Lb. plantarum, Lb. paracollinoides, Lb. vaccinostercus/Lb. suebicus and Pediococcus sp. non-lactics (Gordonia sp./Pseudomonas sp., Halorubrum orientalis, Halosarcina pallid, Sphingomonas sp./Sphingobium sp./Sphingopyxis sp., Thalassomonas agarivorans) and yeasts (Candida cf. apicola, Pichia sp., Pic. manshurica/Pic. galeiformis, Sacch. cerevisiae) |
Kimchi (Cabbage, green onion, hot pepper, ginger; Korea): Leuc. mesenteroides, Leuc. citreum, Leuc. gasicomitatum, Leuc. kimchii, Leuc. inhae, W. koreensis, W. kimchii, W. cibaria, Lb. plantarum, Lb. sakei, Lb. delbrueckii, Lb. buchneri, Lb. brevis, Lb. fermentum, Ped. acidilactici, Ped. pentosaceus, Lc. lactis, yeasts species of Candida, Halococcus, Haloterrigena, Kluyveromyces, Lodderomyces, Natrialba, Natronococcus, Pichia, Saccharomyces, Sporisorium, Trichosporon | |
Soibum (Bamboo shoot; India): Lb. plantarum, Lb. brevis, Lb. coryniformis, Lb. delbrueckii, Leuc. fallax, Leuc. Lact. lactis, Leuc. mesenteroides, Ent. durans, Strep. lactis, B. subtilis, B. lichniformis, B. coagulans, B. cereus, B. pumilus, Pseudomonas fluorescens, Saccharomyces sp., Torulopsis sp. | |
(c) Fermented legumes | Tempeh (Soybean; Indonesia, The Netherlands, Japan, USA): Rhiz. oligisporus, Rhiz. arrhizus, Rhiz. oryzae, Rhiz. stolonifer, Asp. niger, Citrobacter freundii, Enterobacter cloacae, K. pneumoniae, K. pneumoniae subsp. ozaenae, Pseudomas fluorescens, Lb. fermentum, Lb. lactis, Lb. plantarum, Lb. reuteri |
Dawadawa (Locust bean; Ghana, Nigeria): B. pumilus, B. licheniformis, B. subtilis, B. firmus, B. atrophaeus, B. amyloliquefaciens, B. mojavensis, Lysininbacillus sphaericus. | |
(d) Fermented roots/tubers | Fufu (Cassava; West Africa): Bacillus sp., Lb. plantarum, Leuc. mesenteroides, Lb. cellobiosus, Lb. brevis; Lb. coprophilus, Lc. lactis; Leuc. lactis, Lb. bulgaricus, Klebsiella sp., Leuconostoc sp., Corynebacterium sp., Candida sp. |
Tapé (Cassava; Indonesia): Streptococcus sp., Rhizopus sp., Saccharomycopsis fibuligera | |
(e) Fermented milk products | Cheese (Animal milk; Worldwide): Lc. lactis subsp. cremoris, Lc. lactis subsp. lactis, Lb. delbrueckii subsp. delbrueckii, Lb. delbrueckii subsp. lactis, Lb. helveticus, Lb. casei, Lb. plantarum, Lb. salivarius, Leuconostoc spp., Strep. thermophilus, Ent. durans, Ent. faecium, and Staphylococcus spp., Brevibacterium linens, Propionibacterium freudenreichii, Debaryomyces hansenii, Geotrichum candidum, Penicillium camemberti, P. roqueforti |
Kefir (Goat, sheep, cow; Russia): Lb. brevis, Lb. caucasicus, Lb. kefiri, Strep. thermophilus, Lb. bulgaricus, Lb. plantarum, Lb. casei, Lb. brevis, Tor. holmii, Tor. delbruechii | |
(f) Fermented and preserved meat products | Chorizo (Pork; Spain): Lb. sake, Lb. curvatus, Lb. plantarum |
Nem-chua (Pork, salt, cooked rice; Vietnam): Lb. pentosus, Lb. plantarum, Lb. brevis, Lb. paracasei, Lb. fermentum, Lb. acidipiscis, Lb. farciminis, Lb. rossiae, Lb. fuchuensis, Lb. namurensis, Lc. lactis, Leuc. citreum, Leuc. fallax, Ped. acidilactici, Ped. pentosaceus, Ped. stilesii, Weissella cibaria, W. paramesenteroides | |
(g) Fermented, dried and smoked fish products | Ngari (Fish, salt; India): Lact. lactis, Lb. plantarum, Lb. pobuzihii, Lb. fructosus, Lb. amylophilus, Lb. coryniformis, Ent. faecium, B. subtilis, B. pumilus, B indicus, Micrococcus sp., Staphy. cohnii subsp. cohnii, Staphy. carnosus, Tetragenococcus halophilus subsp. flandriensis, Clostridium irregular, Azorhizobium caulinodans, Candida sp., Saccharomycopsis sp. |
Surströmming (Fish; Sweden): Haloanaerobium praevalens | |
(h) Miscellaneous fermented products | Balsamic Vinegar (Grape must; Italy): Acetobacter aceti subsp. aceti, Acetobacter pasteurianus, Acetobacter polyxygenes, Acetobacter xylinum, Acetobacter malorum, Acetobacter pomorum, Candida lactis-condensi, Candida stellata, Hanseniaspora valbyensis, Hanseniaspora osmophila, Saccharomycodes ludwigii, Sacch. cerevisiae, Zygosaccharomyces bailii, Zygosaccharomyces bisporus, Zygosaccharomyces lentus, Zygosaccharomyces mellis, Zygosaccharomyces Pseudorouxii, Zygosaccharomyces Rouxii |
Pidan (duck eggs; Chinese): B. cereus, B. macerans, Staph. cohnii, Staph. epidermidis, Staph. Haemolyticus, Staph. warneri | |
(i) Alcoholic beverages | Wine (Grape must; Worldwide): Saccharomyces and non-Saccharomyces (so-called “wild”) yeasts (e.g., Candida colliculosa, C. stellata, Hanseniaspora uvarum, Kloeckera apiculata, Kl. thermotolerans, Torulaspora delbrueckii, Metschnikowia pulcherrima, Pichia fermentans, Schizosaccharomyces pombe, Hanseniaspora uvarum); bacteria (Oenococcus oeni, Lactobacillus plantatum) |
Pulque (cactus (Agave) plant of Mexico): LAB (Lc. lactis subsp. lactis, Lb. acetotolerans, Lb. acidophilus, Lb. hilgardii, Lb. kefir, Lb. plantarum, Leuc. citreum, Leuc. kimchi, Leuc. mesenteroides, Leuc. pseudomesenteroides), the γ-Proteobacteria (Erwinia rhapontici, Enterobacter spp., and Acinetobacter radioresistens, several α-Proteobacteria), Zymomonas mobilis, Acetobacter malorum, A. pomorium, Microbacterium arborescens, Flavobacterium johnsoniae, Gluconobacter oxydans, Hafnia alvei | |
Tchoukoutou (spontaneously fermented beer) (sorghum, Benin): S. cerevisiae, Candida krusei, Clavispora lusitaniae, Candida rugosa |
Global Quality | Positive Effect of Fermentations | References |
---|---|---|
hygienic quality | Pyrazines biodegradation | [30] |
Toxins biodegradation | [26,31] | |
Biogenic amines biodegradation | [32] | |
sensory quality | Flavor improvement | [33,34] |
Texturizing properties | [29,35] | |
nutritional quality | Vitamin bio-fortification | [4,27] |
Increased bioaccessibility of minerals | [36] | |
Reduction of antinutritional properties | [37] | |
Reduction of lactose | [38] | |
functional quality | Antioxidant activity enhancement | [35] |
Probiotic properties of selected strains | [28,39] | |
Bio-fortification in microbial β-glucans | [40] | |
Gluten degradation | [41] |
Safety Issue | Evidence | Reference |
---|---|---|
Pathogens | Some fermented foods (ready-to-eat) were found positive for the presence of Listeria monocytogenes in a global survey on several types of food products on sale in Portugal | [42] |
The most commonly encountered pathogens in African fermented foods include Bacillus cereus, Escherichia coli, Salmonella sp., Staphylococcus aureus, Vibrio cholera, Aeromonas, Klebsiella, Campylobacter and Shigella sp. | [43] | |
51 doenjang samples have been found broadly contaminated with Bacillus cereus; while, only one sample was positive for Bacillus thuringiensis. All B. cereus isolates from doenjang were positive for diarrheal toxin genes. | [46] | |
Epidemiologic investigation linked Escherichia coli O157:H7 infection with consumption of a commercial dry-cured salami product distributed in several western U.S. states. | [47] | |
An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. | [48] | |
Two commonly consumed traditional condiments (iru and ogiri) and their respective raw seeds (locust bean and melon) were found contaminated with potentially pathogenic species such as Alcaligenes faecalis, Bacillus anthracis, Proteus mirabilis and Staphylococcus sciuri subsp. sciuri occurred in the samples. | [49] | |
Consumption of fermented raw pork sausage was associated with infection Salmonella enterica serovar Bovismorbificans. | [50] | |
Mycotoxin | Dietary sources of Ochratoxin A including fermented foods. | [44] |
Fermentation influences contamination of cocoa beans by Ochratoxin A. | [51] | |
Biogenic amines | Bioproduction of putrescine, histamine, tyramine and cadaverine in wine is a bacterial strain-dependent character. | [52] |
Bioproduction of tyramine in cheese up to considerable levels (e.g., 2010 mg/kg in Egyptian blue cheese). | [53] | |
In fermented sausages, biogenic amines are mainly produced by fermentative microbial population. | [45] | |
Ethyl carbamate | Ethyl carbamate produced by selected yeasts and lactic acid bacteria in red wine. | [54] |
Safety Issue | Strain | Reference |
---|---|---|
MIC 1 | Aspergillus sp. | [55] |
MIC | Cephalosporium sp. | [56] |
BA 2 | Enterococcus durans | [57] |
BA | Enterococcus faecalis | [57] |
BA | Enterococcus faecium | [58] |
MIC | Fusarium sp. | [55] |
BA | Issatchenkia terricola | [59] |
BA | Lactobacillus buchneri | [60] |
BA | Lactobacillus brevis | [60] |
BA | Lactobacillus curvatus | [61] |
BA | Lactobacillus hilgardii | [60] |
EC 3 | Lactobacillus hilgardii | [62] |
BA | Lactobacillus mali | [60] |
BA | Lactobacillus plantarum | [63] |
BA | Lactobacillus reuteri | [61] |
BA | Leuconostoc mesenteroides | [60] |
BA | Metschnikowia pulcherrima | [59] |
BA | Micrococcus spp. | [61] |
BA | Oenococcus oeni | [60] |
MIC | Penicillium sp. | [55] |
BA | Pichia manshurica | [59] |
BA | Staphylococcus carnosus | [61] |
Definition | Reference | |
---|---|---|
Starter cultures | “Starter cultures” are preparations of live microorganisms or their resting forms, whose metabolic activity has desired effects in the fermentation substrate, the food. The preparations may contain unavoidable residues from the culture substrate and additives that support the vitality and technological functionality of the microorganisms (such as antifreeze or antioxidant compounds). | [70] |
Microbial food cultures | “Microbial food cultures” (MFC) are live bacteria, yeasts or molds used in food production. MFC preparations are formulations, consisting of one or more microbial species and/or strains, including media components carried over from the fermentation and components which are necessary for their survival, storage, standardization, and to facilitate their application in the food production process. | [65] |
Commercial starter cultures | “Commercial starter cultures” are standardized inoculum to be used for the production of fermented foods. Starter cultures are produced by specialized manufactures. Rigorous quality assurance and quality control are conducted to ensure performance, composition, and safety of the culture. | [71] |
Matrix | Evidences | Reference |
---|---|---|
Table olives | Selected lactobacilli and yeast showed a fast acidification of brine. Olives inoculated with lactobacilli and yeast showed the lowest biodiversity and the highest appreciation for both texture profile analysis and sensory evaluation | [72] |
Inoculation of brine medium with lactic acid bacteria starters significantly influenced aroma profiles | [76] | |
Autochthonous starter produced same sensory quality as natural traditional table olives in a shorter time | [77] | |
Fermented leek kimchi. | Leeks fermented with Weissella confusa LK4 showed the highest radical scavenging effects and reducing ability. Total flavonoid and poly-phenolic contents changed during fermentation and showed correlation with anti-oxidant effects | [78] |
Soybean fermented product | A reduction of biogenic amines and aflatoxins has been reported in Doenjang samples fermented with various Meju as starter cultures | [73] |
Dry-cured foal sausage | The inclusion of starter cultures contributes to improve the hygienic quality (stronger acidification and reduced count of Enterobacteriaceae) of foal sausages without significant effect on lipolysis, texture and appearance | [79] |
Chinese fermented dry sausages | Nitrite content of all inoculated sausages declined rapidly during ripening compared to non-inoculated | [74] |
Fermented sausage | Selected starter cultures improve quality, safety and sensorial properties of Dacia sausage, a traditional Romanian dry-sausage variety | [80] |
Evidences indicated that the selected Lactobacillus plantarum strain had a strong effect on inhibiting the production of biogenic amines | [81] | |
Starter cultures minimize the formation of biogenic amines during the process of Nham fermentation | [82] | |
Thai fermented shrimp (Kung-Som) | Starter culture enhance GABA content, improved microbiological safety (dominated the total microflora) as well as reduced fermentation time | [75] |
Wine | In cellars where biogenic amines are usually high, repeated experiments showed that in inoculated wines, biogenic amine concentrations were very low, while uninoculated control wines contained all the usual amines | [83] |
The use of a selected malolactic starter resulted in reductions in biogenic amines concentrations in wine produced by started malolactic fermentation compared with wine produced by spontaneous malolactic fermentation | [84] |
Major Groups Global Fermented Foods | Product Name | Country | Reference |
---|---|---|---|
(a) Fermented cereals | Ogi | Nigeria | [104] |
(b) Fermented vegetables and bamboo shoots | Soidon | India | [105] |
(c) Fermented legumes | Kedong sufu | China | [106] |
(d) Fermented roots/tubers | Gari | Kenya | [107] |
(e) Fermented milk products | Suero Costeño | Colombia | [108] |
(f) Fermented and preserved meat products | Salchichón | Spain | [109] |
(g) Fermented, dried and smoked fish products | Jeotgal | Korea | [110] |
(h) Miscellaneous fermented products | Vinegar | Italy | [111] |
(i) Alcoholic beverages | Malvar Wine | Philippines. | [112] |
Fermented Foods/Beverages | Autochthonous Variety/Typical Product | Studied Microorganisms | Main Potential Impact on Food Quality | References |
---|---|---|---|---|
Bread | Sourdough for Altamura bread (bread) | Lactic acid bacteria | Sensory quality | [113] |
Cheese | Canestrato Pugliese (cheese) | Lactobacilli and lactococci | Sensory quality | [114] |
Cheese | Mozzarella cheese (cheese) | Lactobacilli, lactococci, streptococci and enterococci | Sensory quality | [115] |
Cheese | Mozzarella cheese (cheese) | Lactobacillus plantarum, Lactobacillus helveticus, Lactobacillus delbrueckii subsp. lactis, Streptococcus thermophilus, Enterococcus faecalis, Enterococcus durans | Sensory quality | [116] |
Table olives | Bella di Cerignola (Olives) | Yeasts | Sensory quality | [117] |
Bread | Sourdough for Altamura bread (bread) | Yeasts | Functional quality | [118] |
Table olives | Bella di Cerignola (Olives) | Lactic acid bacteria | Functional quality | [119] |
Wine | Different yeast species | Hygienic quality | [59] | |
Cheese | Fior di Latte (cheese) | Lactic acid bacteria | Sensory quality | [120] |
Table olives | Cellina di Nardò and Leccino (olives) | Yeasts and lactic acid bacteria | Sensory quality | [121] |
Wine | Uva di Troia (grape) | Oenococcus oeni, Saccharomyces cerevisiae | Sensory quality | [122] |
Wine | Negroamaro (grape) | Hanseniaspora uvarum, Saccharomyces cerevisiae | Sensory quality | [123] |
Wine | Uva di Troia (grape) | Oenococcus oeni, Lactobacillus plantarum | Sensory quality | [124,125,126] |
Wine | Uva di Troia (grape) | Non-Saccharomyces yeasts | Sensory quality | [127] |
Wine | Negroamaro (grape) | Yeasts and lactic acid bacteria | Sensory quality | [128] |
Wine | Uva di Troia (grape) | Yeasts | Sensory quality | [129] |
Wine | Different autochthonous grape varieties | Brettanomyces bruxellensis | Sensory quality | [130,131] |
Wine | Uva di Troia (grape) | Lactobacillus plantarum | Sensory quality | [132] |
Wine | Uva di Troia (grape) | Saccharomyces cerevisiae | Hygienic quality | [133] |
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Capozzi, V.; Fragasso, M.; Romaniello, R.; Berbegal, C.; Russo, P.; Spano, G. Spontaneous Food Fermentations and Potential Risks for Human Health. Fermentation 2017, 3, 49. https://doi.org/10.3390/fermentation3040049
Capozzi V, Fragasso M, Romaniello R, Berbegal C, Russo P, Spano G. Spontaneous Food Fermentations and Potential Risks for Human Health. Fermentation. 2017; 3(4):49. https://doi.org/10.3390/fermentation3040049
Chicago/Turabian StyleCapozzi, Vittorio, Mariagiovanna Fragasso, Rossana Romaniello, Carmen Berbegal, Pasquale Russo, and Giuseppe Spano. 2017. "Spontaneous Food Fermentations and Potential Risks for Human Health" Fermentation 3, no. 4: 49. https://doi.org/10.3390/fermentation3040049