Fermented foods refer to beverages or foods made by carefully regulated microbial growth and the enzymatic conversion of dietary components. Fermented foods have recently become more popular. Studies on fermented foods suggest the types of bacteria and bioactive peptides involved in this process, revealing linkages that may have impacts on human health. By identifying the bacteria and bioactive peptides involved in this process, studies on fermented foods suggest relationships that may have impressions on human health. Fermented foods have been associated with obesity, cardiovascular disease, and type 2 diabetes.
1. Introduction
Fermentation is a food processing technique, and its origins date back many centuries. The existence of fermented products has been demonstrated to be started in India, Iraq, and Egypt in the years BC
[1]. The definition of fermentation according to the International Scientific Probiotic and Prebiotic Association (ISAPP) is “foods made through desired microbial growth and enzymatic conversions of food components”. Fermentation has been used by humans for as long as recorded history to preserve and modify food, resulting in more stable and varied food with distinctive organoleptic, sensory, and functional features
[2]. Due to their distinctive flavors, fermented foods are being produced and consumed in greater quantities. There has also been a scientific concentration on the health benefits of fermented foods and their components
[3]. In the fermentation procedure, microorganisms, specifically bacteria, yeasts, and mycelial fungus, as well as their enzymes, produce fermented foods. Milk, cereals, vegetables, fruits, legumes, meats, and products are food groups used in fermentation
[4].
Food fermentation’s main purposes are to increase food safety and lengthen shelf life; additionally, fermented foods have grown to be known for their positive effects on health
[5]. Foods that have undergone fermentation may produce bioactive compounds as byproducts of the process, and fermented foods may contain live microorganisms that have health benefits
[6]. The main metabolites and microorganisms involved in food fermentation may be divided into categories: alcohol, carbon dioxide (from yeast), propionic acid (from
Propionibacterium freudenreichii), lactic acid (from lactic acid bacteria (LAB) from genera such as
Lactobacillus and
Streptococcus), acetic acid (from
Acetobacter), ammonia, and fatty acids (from
Bacillus and molds)
[7]. The metabolites produced by the fermenting organisms limit the expansion of spoilage, and pathogenic organisms during food fermentation extend the shelf life of perishable foods
[8]. During fermentation, macronutrients are broken down, and digestion is facilitated. Many fermented foods include probiotic-potential bacteria in them
[5]. Probiotics are defined in the FAO/WHO report as “Live microorganisms which when administered in adequate amounts confer a health benefit on the host”
[9]. According to the ISAPP, these concentrations of probiotics can vary daily from 100 million to over a trillion CFU. The majority have been studied at concentrations of 1 to 10 billion CFU/d
[10]. Fermented foods may serve as probiotic carriers, effectively delivering the probiotic to the host and conferring health advantages
[11]. Although there may be a fermentation process involved, consumed fermented foods may not contain live bacteria. The term “probiotic” is only used when a product has clearly shown health advantages brought about by the action of well-defined and characterized living microorganisms
[2]. The metabolic activity of microorganisms during fermentation results in a number of biochemical alterations that have impacts on the nutritive and bioactive qualities of fermented foods. The bioactive components showing health benefits include exopolysaccharides, bioactive peptides, phenolic compounds, short-chain fatty acids (SCFAs), conjugated linoleic acid (CLA), and γ-aminobutyric acids (GABAs)
[12]. Fermented foods and their components can have many health effects such as antioxidant, antidiabetes, anti-inflammatory, anti-hypercholesterolemic, and microbiota modulation effects
[13][14][15][16].
2. Fermented Dairy Products
Milk is an important source of macro- and micronutrients. Protein, conjugated linoleic acid, calcium, riboflavin, and phosphorus are macro- and micronutrients that are commonly found in milk. These nutrients have impacts on health and diseases
[17]. Milk proteins (whey and casein) have positive effects on satiety and body weight control; have hypotensive, antimicrobial, anti-inflammatory, anticancer, and antioxidant effects; and cause insulin release and glucose regulation
[18]. Many fermented products such as yogurt, cheese, and kefir are obtained via the fermentation of milk. In the production of fermented milk products, LAB play a crucial role
[19]. Milk fermentation using yeasts, propionibacteria, and LAB may result in the synthesis or increase in the number of bioactive compounds that show some health benefits. These include vitamins, CLA, exopolysaccharides (EPSs), GABAs, bioactive peptides, and oligosaccharides
[20]. For example, lactic acid bacteria and propionibacteria can increase the amounts of B
12 and folic acid in fermented milk products
[21][22][23]. In addition, the fermentation of lactic acid in milk reduces the amount of lactose, which may make fermented dairy products tolerable for people with lactose intolerance
[24].
2.1. Kefir
Kefir is an acidic alcoholic fermented dairy product with a creamy consistency and a slightly acidic taste, originating from the Balkans, Eastern Europe, and the Caucasus. Traditionally, kefir is produced using cow, sheep, goat, or buffalo milk
[25]. Kefir exerts its positive effects on health through whole kefir, kefir grains, lactic acid bacteria, yeasts, organic acids, polysaccharides (kefiran and exopolysaccharides), and various other metabolites
[26]. As a result of fermentation, there is an increase in lactic acid and antioxidant activity in kefir compared to normal milk
[27]. In addition,
Propionibacterium freudenreichii bacteria in kefir grains can cause an increase in B
12 and folate levels
[22]. Studies on kefir, kefir grains, and kefir components (lactic acid bacteria, organic acids, bioactive peptides, and polysaccharides) have shown that they have antihypertensive
[28], anticancer
[29], antioxidant
[30], anti-inflammatory
[31], antidiabetic
[32], and hypocholesterolemic effects
[33] in addition to effects on bone health
[34], cognitive function
[35], and microbiota modulation
[36].
The bacteria and yeasts identified in kefir can have positive effects on health.
Kluyveromyces marxianus is one of the yeasts in kefir. Its strain, obtained from kefir, has been shown to remain alive in the digestive system
[37].
Kluyveromyces marxianus B0399 supplementation decreased proinflammatory cytokines (tumor necrosis factor alpha (TNF-α), interleukin (IL)-6, macrophage inflammatory protein-1 (MIP-1) α, IL-12, IL-8, interferon (IFN)-γ) and increased SCFAs (acetate and propionate). Although there was no change in the total bacterial count, the
Bifidobacterium genus count increased
[38].
Kluyveromyces marxianus A4 and A5 supplementation showed good adhesion in Caco-2 cells.
Kluyveromyces marxianus A4 increased
Bacteroidetes,
Bacteroidales, and
Bacteroides, and
Kluyveromyces marxianus A5 increased
Corynebacteriales and
Corynebacterium [39].
2.2. Yogurt
One of the products of the lactic acid fermentation of milk is yogurt. The lactose in its content is converted into lactic acid by bacteria. In this way, it can be tolerated in the case of lactose intolerance. It also has benefits for health due to its protein content, vitamins such as riboflavin, minerals such as calcium, and metabolites that result from fermentation
[40]. One of the components in yogurt that may have a positive effect on health is the CLA content. As a result of the increase in fermentation time, the CLA level in yogurt may increase
[41].
Studies on the consumption of conventional/probiotic yogurt have evaluated its microbiota modulation
[42], hypocholesterolemic
[43], antidiabetic, antioxidant
[44], and anti-obesity effects
[45]. It was found that visceral fat decreased, and the abundances of
Streptococcus thermophilus and
Bifidobacterium animalis subsp.
Lactis species increased in individuals who consumed yogurt. A correlation was observed between
Bifidobacterium animalis subsp.
Lactis and increased fecal 3-hydroxyoctanoic acid contents
[42]. Yogurt supplementation (220 g/day) decreased fasting insulin, insulin resistance, intrahepatic lipid, hepatic fat fraction, serum lipopolysaccharide (LPS), fibroblast growth factor 21, triglycerides, TNF-α, total cholesterol, glutathione peroxidase (GPH-Px), and superoxide dismutase (SOD). In addition, it regulated the microbiota composition
[44].
When the effects of probiotic and conventional yogurts were evaluated, the total cholesterol and total cholesterol/high-density lipoprotein cholesterol (HDL-C) ratio decreased as a result of consuming both yogurts. Both yogurts showed hypocholesterolemic effects
[43]. In the study by Rezazadeh et al.
[46], probiotic yogurt decreased blood glucose, insulin, HOMA-IR, Quantitative Insulin Sensitivity Calculation Index (QUICKI), vascular cell adhesion molecule cell (VCAM)-1, and plasminogen activator inhibitor (PAI)-1 values
[46]. Various
Lactobacillus and
Bifidobacterium species in probiotic yogurts have been shown to lower cholesterol; regulate plasma glucose levels; have antioxidant, anti-inflammatory, and microbiota modulation effects; and have positive effects on cancer and ulcerative colitis
[47][48][49][50][51][52].
2.3. Cheese
Cheese has been produced and consumed for many years. There are 1500 cheese varieties defined in the world. The microorganism content of cheese varies based on the milk used, cheese type, and production
[53]. The pH changes that occur during the production and ripening of cheese are heavily influenced by both lactic acid bacteria and yeasts
[54]. A meta-analysis study evaluating cheese consumption and its health effects found that cheese consumption (especially 40 g/day) had neutral to moderate benefits for human health, and was moderately inversely connected with all-cause mortality, cardiovascular disease, coronary heart disease, and stroke incidence. It also showed a negative association with the risks of type 2 diabetes and dementia. It is emphasized that these effects are due to the nutrients and bioactive components in cheese
[55].
One of the components of cheese that have positive effects on health is bioactive peptides. The type of milk used during cheese ripening, starter culture, and native milk microbiota affect the bioactive peptides formed. Bioactive peptides are composed of certain protein fragments and offer various advantages for regulating bodily processes
[56][57][58].
Bioactive peptides in different types of cheese have been shown to have antioxidant, antihypertensive (ACE inhibitory), antimicrobial, and dipeptidyl-peptidase-IV (DPP-IV) inhibitory activity effects
[58][59][60][61][62]. In one study,
Lactobacillus helveticus A1, which releases the peptide as a key factor in ACE inhibition, was the strain with the strongest ACE inhibitory activity
[63]. The number of peptides with angiotensin-converting enzyme (ACE), dipeptidyl peptidase-IV (DPP-IV), and antioxidant activity increased with ripening
[64]. The proteolysis of cheese for more than 90 days resulted in increased antioxidant activity. Bioactive peptides derived from αs1-casein and β-CN were detected in cheese. The radical scavenging activity, reducing power, chelate capacity, and ACE inhibition effects of cheese extract derived from these peptides were revealed
[59].
The other compound of cheese associated with health is conjugated linoleic acid. The CLA content in cheeses was found to be 0.44 to 1.04 g/100 g of fat in the study by Donmez et al.
[65], and 7.5 to 7.9 mg/g of fat in the study by Luna et al.
[65]. It was shown that there is an increase in the CLA levels during cheese ripening, but increased storage time decreases the concentration
[66]. CLA may have antidiabetic, anticancer, anticarcinogenic, anti-atherosclerotic, antihypertensive, and endothelial function effects
[67][68][69].
The development of biogenic amines may occur in cheese as a result of the bioactivities of some microorganisms. Histamine, cadaverine, putrescine, spermine, spermidine, and tyramine biogenic amines have been detected in different cheese types. High levels of biogenic amine consumption have some drawbacks. For example, histamine has effects such as nausea, vomiting, diarrhea, and stomach upset, while tyramine may cause hypertensive effects and may have a negative relationship with monoamine oxidase inhibitors (MAOIs)
[70]. It was emphasized that
Lacticaseibasillus casei 4a and 5b isolated from cheese reduced tyramine and histamine accumulation, and therefore may be suitable to be used as co-cultures in order to lessen the amount of biogenic amines
[71].
3. Fermented Meats
Red meat is any unprocessed mammalian muscle flesh, including frozen or minced meat (such as cattle, veal, pork, or lamb). Meat that has undergone salting, fermenting, smoking, curing, or other methods so as to improve preservation or flavor is well known as processed meat. Pork or beef are typically found as processed meats
[72]. The majority of the time, it is agreed that meat and its products provide excellent and high biologic values of proteins, B group vitamins, minerals, trace elements, and some other bioactive components
[73].
Figure 1 shows the changes throughout the meat fermentation.
Table 1 lists the effects of fermented meat and certain bioactive compounds on health.
Figure 1. Schematic summary of changes throughout meat fermentation.
Table 1. Effects of fermented meat and certain bioactive compounds on health.
Fermented Foods |
Certain Bioactive Compounds |
Effects on Health |
References |
Intestine |
|
Fermented mutton jerky |
x3-2b Lactiplantibacillus plantarum and composite bacteria |
Purine content of fermented mutton jerky by x3-2b Lactobacillus plantarum and composite bacteria ↓ In vitro digestion, decreasing purine content by 37x-3 Pediococcus pentosaceus ↑ |
[74] |
|
Cured beef |
- |
Gastric protein carbonylation ↑ Colonic Ruminococcaceae ↑ Cecal propionate ↑ TBARs and diacetyl in feces ↑ Levels of cecal butyrate, fecal phenol, dimethyl disulfide ↓ Level of fecal carbon disulfide ↑ Colonic Ruminococcaceae ↑ |
[75] |
|
Fermented sausage |
Enterococcus faecium CRL 183 |
Lactobacillus spp. in ascending colon, transverse colon, and descending colon ↓ Bacteroides spp. in descending colon ↓ Enterobacteriaceae in transverse colon and descending colon ↓ Colonic ammonium ions ↑ Butyric acid concentration in transverse colon, ascending colon, and descending colon ↑ Concentration of propionic acids in ascending colon and transverse colon ↑ Concentration of acetic acid in ascending colon, transverse colon, and descending colon ↓ |
[76] |
|
Fermented sausage |
- |
Release of free iron in digestive system ↑ Concentration of gastric N-nitrosamine ↑ |
[77] |
|
Fermented sausage |
Enterococcus faecium S27 |
Transfer of tetracycline resistance determinant (tet(M)) to E. faecium and Enterococcus faecalis ↑ Transfer of Enterococcus faecium’s streptomycin resistance ↑ |
[78] |
|
Fermented sausage |
Bologna sausage (a) Dry fermented sausage (b) |
Calcium transporter in Caco-2 cells: in (a) ↑, in (b) ↓ |
[79] |
|
Fermented salami |
Plant extracts |
Phenol and p-cresol in colon ↓ Acetate, propionate, butyrate in colon ↑ Enterobacteriaceae ↓ Bifidobacteriaceae ↑ |
[80] |
|
Fermented fish |
Staphylococcus sp. DBOCP6 |
Non-hemolytic and non-pathogenic effects against broad and narrow spectrum antibiotics Ability to adhere to the intestinal wall |
[81] |
Cardiovascular diseases and ACE-I inhibitory effects |
|
- |
- |
Cardiovascular disease risk, stroke risk ↑ Total mortality risk ↑ |
[82] |
|
Salami Sausage |
|
Cardiovascular disease risk ↑ |
[83] |
|
|
- |
Cardiovascular disease risk ↑ |
[84] |
|
|
- |
Total stroke incidence ↑ No association between ischemic stroke and coronary heart disease mortality |
[85] |
|
Bacon Sausage |
- |
Cardiovascular death risk ↑ Ischemic heart disease risk ↑ |
[86] |
|
Dry-cured pork ham |
- |
Levels of total cholesterol, LDL, basal glucose ↓ |
[87] |
|
Semi-dry fermented camel sausage |
Lactiplantibacillus plantarum KX881772 |
Inhibition of ACE ↑ Cytotoxicity activity towards Caco-2 cell line ↑ α-amylase inhibition ↑ α-glucosidase inhibition ↑ |
[88] |
|
Fermented pork sausage |
Staphylococcus simulans NJ201 Lactiplantibacillus plantarum CD101 |
ACE inhibition ↑ Superoxide anion scavenging activities ↑ Ferric-reducing antioxidant activity ↑ |
[89] |
|
Dry fermented camel sausage |
Staphylococcus xylosus and Lactiplantibacillus plantarum Staphylococcus caarnosus and Latilactobacillus sakei Staphylococcus xylosus and Lactobacillus pentosus |
Antioxidant capacity by <3 kDa peptides ↑ Maximum ACE inhibition by <3 kDa peptides Maximum ACE inhibition in sausages with S. xylosus and L. plantarum |
[90] |
|
Dry-cured ham |
- |
ACE inhibition ↑ Radical scavenging activity ↑ PAF-AH inhibitory effect ↑ |
[91] |
|
Fermented meat |
- |
Antioxidant activity against OH-radical by GlnTyr-Pro ↑ |
[92] |
|
Dry-fermented sausage |
Starter culture (P200S34) and protease (EPg222) |
ACE inhibition ↑ Antioxidant activity ↑ |
[93] |
|
|
- |
Risk of cardiovascular mortality, stroke, myocardial infarction via reduction in processed meat ↓ |
[94] |
|
|
- |
Risk of all-mortality cause and cardiometabolic disease via lower consumption ↓ |
[95] |
|
|
- |
Risk of heart failure ↑ |
[96] |
Cancer |
|
|
- |
Risk of colon cancer, rectal cancer, breast cancer, lung cancer, and colorectal cancer ↑ |
[97] |
|
Ham Sausage Bacon |
- |
Breast cancer risk ↑ |
[98] |
|
|
- |
Weak positive association with breast cancer |
[99] |
|
|
- |
Breast cancer risk with diet rich in processed meat ↑ |
[100] |
|
Ham Sausage Bacon |
- |
Gastric cancer risk ↑ |
[101] |
|
Ham Sausage Bacon |
- |
Colorectal cancer risk ↑ |
[102] |
|
|
- |
Colorectal cancer risk with lower consumption ↓ |
[103] |
|
|
- |
Colorectal cancer risk with lower consumption ↓ |
[104] |
|
|
- |
Colorectal cancer risk ↑ |
[105] |
|
Ham Sausage Bacon |
- |
Colorectal cancer risk ↑ |
[106] |
|
Ham Sausage Bacon |
- |
Colorectal cancer risk ↑ |
[107] |
|
|
- |
Colorectal adenoma risk ↑ |
[108] |
|
Ham |
- |
Risk of renal cell carcinoma ↑ Risk of bladder cancer ↑ |
[109] |
|
Ham Sausage Bacon |
- |
Bladder cancer risk ↑ |
[110] |
|
Ham Sausage Bacon |
- |
Minimal connection to kidney cancer risk |
[111] |
|
Ham Salami Sausage Bacon |
- |
No association with gliomas |
[112] |
|
|
|
Risk of hepatocellular carcinoma ↑ |
[113] |
Other diseases |
|
|
- |
Risk of type 2 diabetes ↑ |
[114] |
|
Bacon Salami Sausages |
- |
Risk of diabetes as well as stroke and coronary heart disease ↑ |
[115] |
|
|
- |
Risk of type 2 diabetes ↑ |
[116] |
|
|
- |
Type 2 diabetes risk ↑ |
[117] |
|
|
- |
Gestational diabetes mellitus risk ↑ |
[118] |
|
|
- |
No change in Crohn’s disease flares |
[119] |
|
|
- |
Risk of mortality via increase in consumption ↑ |
[120] |
|
|
- |
Mortality risk of all causes (except cancer) and cardiovascular-caused mortality ↑ |
[121] |
|
|
- |
Depression risk ↑ |
[122] |
|
|
N-Nitrosodimethylamine |
No change in glioma |
[123] |
|
|
Diethylnitrosamine |
Probability of hepatocarcinogenesis |
[124] |
Another unhealthy compound that can be found in some fermented foods is salt. High salt consumption has negative health effects. It is therefore important to reduce salt consumption. However, reducing salt in fermented foods may pose a problem with regard to food safety, texture, and flavor
[198]. While ensuring that this reduces salt intake, it may cause the development of pathogenic microorganisms. Reducing the salts used may result in increased yeast,
Enterobacteriaceae, and microbial growths
[199]. Microbial growth can occur due to the decrease in water activity. As a result of the increase in some microorganisms, the formation of biogenic amines and nitrosamines may increase
[190][200][201][202][203][204].
The future growth of the fermented food sector is made possible by the lowering of sodium and nitrosamines in traditional fermented foods. Studies on fermented foods show heterogeneous characteristics. This makes it difficult to compile the studies on a fermented food and to make a general evaluation of the positive and negative properties of that fermented food. In addition, studies on the amounts of fermented foods consumed by people need to be increased. In this way, responses to the effects of the amounts of fermented foods consumed on humans can be evaluated.