A review and comparative perspective on health benefits of probiotic and fermented foods

Abstract

Fermented foods such as yogurt, kefir and sauerkraut have been part of the human diet throughout history and have gained attention in recent years due to their immense health and nutritional benefits. As a result, fermented foods are considered biofuel for the human microbiome which helps to boost the immune system. Fermented foods are those foods and beverages that are produced by employing specific microbial-based fermentation aids such as yeasts and bacteria, particularly lactic acid bacteria (LAB). Through controlled enzymatic reactions, these microbial cultures transform food components as substrates into value-added products promoting various healthy fermentative activities. These microbes in fermented foods also produce compounds that can inhibit food spoilage and pathogenic microorganisms, thereby extending the product shelf of fermented products. Probiotics are live microbiota with beneficial health properties, prevent gastrointestinal diseases and modulate the human microbiome. Thus, foods that are fermented by certain strains of probiotic bacteria that exhibit evidence of health benefits are referred to as probiotic fermented foods. This review describes fermented and functional foods, probiotics and their relationship to human health. In addition, we offer our perspective on the distinct differences between probiotic and fermented foods to promote awareness for consumers and key stakeholders regarding these highly functional and nutritionally fermented food products.

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Introduction

Humans had a long-standing practice of consuming fermented foods, particularly for the health benefits, organoleptic qualities and ability of these nutritionally significant products to have an extended shelf life (Castellone et al., 2021). Globally, it has been estimated that fermented foods comprises one-third of the human diet (Borresen et al., 2012), and the consumption of these foods continues to shape the dietary patterns of many consumers. From a human health perspective, ancestral dietary patterns such as the traditional Japanese and Mediterranean diets have contributed immensely to the popularity of fermented foods (Hugenholtz, 2013; Selhub et al., 2014). Fermented foods and beverages include all foods or beverages produced by microbial activities under controlled enzymatic conditions that transform food components into value-added products (Marco et al., 2017). According to the International Scientific Association for Probiotics and Prebiotics (ISAPP), a broader definition of fermented food and beverages relates to: ‘foods made through desired microbial growth and enzymatic conversions of food components’ (Marco et al., 2021).

In classifying fermented foods, two schools of thought are linked to the method by which foods are fermented. Primarily, the fermentation of foods can be accomplished by employing starter cultures otherwise known as fermentative aids for food products including yogurt, kombucha and kefir. Second, foods such as kimchi and sauerkraut can undergo fermentation spontaneously or naturally. This phenomenon is often termed ‘wild ferments’ and involves the inherent presence of fermentative microbes in unprocessed and natural food or their presence in the food processing environment (Dimidi et al., 2019). During the past decade, the term probiotics have gained much attention as consumers have become more aware of the importance of healthy diets. According to the standard definition by the International Scientific Association for Probiotics and Prebiotics (ISAPP) under the framework established by the Food and Agriculture Organization (FAO) and the World Health Organization (WHO), probiotics include ‘all live microorganisms that, when administered in an appropriate amount confers beneficial effect to the host’ (Hill et al., 2014). Functional foods—as also defined by the Functional Food Center (FFC)—refer to ‘natural or unprocessed foods that possess inherent or undetermined bioactive compounds that are highly efficient, not harmful and proven scientifically to confer health benefits and reported with evidence for the treatment and prevention of diseases’ (Arshad et al., 2021). Both fermented foods and probiotics are functional foods.

Consequently, several fermented foods are categorised as functional foods as they contain beneficial microbes that promote the health of consumers (Orisakwe et al., 2020). Moreover, these fermentative microorganisms support the human microbiome through their by-products and metabolites and help in the prevention of gastrointestinal diseases (Castellone et al., 2021). Generally, a diverse range of microorganisms are employed for fermented foods and include acetic acid bacteria (AAB), yeasts or fungi and lactic acid bacteria (LAB). The most widely employed microorganisms for fermented foods (vegetables, dairy and meat) evolved from the genus lactobacillus (Marco et al., 2021). LAB has extensively been employed for fermented dairy foods such as yogurt which contains the important probiotic strain Lactobacillus delbreuckii subsp. bulgaricus, which has been solely credited with the health claim of alleviating lactose intolerance, a gastrointestinal disease (Ayivi & Ibrahim, 2022). However, due to the diverse use of functional food terminology, consumers may experience some confusion regarding understanding the distinct differences between fermented foods and probiotics. For example, in recent years, consumers have often heard primary care providers and dieticians recommend fermented food products as a source of probiotics. Moreover, as food scientists working in fermentation, we typically receive inquiries regarding which foods are the best sources of probiotics, we are also asked which probiotic supplements can be replaced by fermented foods. Therefore, this review aimed to provide here a comprehensive overview of these important concepts and present information that will help consumers to make better decisions. For example, the content in this review is structurally organised by defining probiotics, fermented foods the concept of functional foods and our perspective on the distinction between fermented functional foods and probiotics. In addition, we tinted-advocate the consumption of more fermented foods and probiotics intolerance for human health and well-being.

Definition of probiotics

Probiotics in food

Probiotic cultures have been around since humans first began drinking fermented milk and eating fermented foods, though the history of probiotics dates to 1907 when Russian French zoologist Elie Metchnikoff discovered the effects of gut microflora on health. Using host-friendly bacteria discovered in Bulgarian milk, Metchnikoff hypothesised that human health could be improved and senility could be delayed (Mackowiak, 2013). His hypothesis boomed for some period and today, probiotics are not only an interest in medical research but also a global industry.

Selection criteria for probiotics

In addition to possessing human health effects that have been clinically confirmed and documented, a successful potential probiotic strain is anticipated to possess several other desirable traits. Probiotic strains are safe to use for a very long period as ingredients in and animal food. These rains are acceptable because probiotic organisms are found naturally in the intestines of healthy people and animals. Additionally, probiotic microorganisms are chosen for the ability to endure the harsh conditions of the gastrointestinal tract, including low pH and elevated bile acid concentrations. The strain of choice should be able to withstand the processes of production, distribution, storing and application while retaining viability and desirable qualities.

The desired properties of probiotic strains are listed below (Ayivi et al., 2020):

• Health effects with clinical validation and documentation;

• Acid and bile stability;

• GI tract colonisation and attachment/adherence to gut/intestinal cells;

• The strain should be documented with the code;

• Must have a human origin;

• Withstand the different production-related technological processes;

• Safety evaluation: non-pathogenic, non-toxic, non-allergic, non-mutagenic;

• Antibiotic resistance and sensitivity, as well as desired metabolic activity.

Probiotic microorganisms

Most of the probiotic strains are classified as LAB, and among them, the genera Lactobacillus is considered the most important followed by the genera Streptococcus and Lactococcus. These groups have the most significant features in practical applications. Certain species of Enterococcus and Escherichia coli could also be regarded as probiotics. Gram-positive, nonsporulating, catalase-negative organisms known as LAB are a varied group that may be found in a variety of locations (Carr et al., 2002). These organisms are typically present in dairy, meat, plants and fermented products with a commercial value and are referred to as gut-related organisms (Carr et al., 2002). Because of their long history of anthropological use in food preservation and their ability to quickly ferment carbohydrates into lactic acid, LAB are used in a wide range of industrial and agricultural fermentations around the world. Food is acidified because of LAB development, which preserves the food products and gives it distinctive textures, flavours and nutritional value (Kleerebezem & Hugenholtz, 2003). Lactobacillus acidophilus is one of the common probiotic strains that is generally regarded to possess probiotic effects and is most suggested for dietary use (Shah, 2007). According to Sanders & Klaenhammer (2001), this strain could be found in yogurt and fermented milk and was originally isolated from the digestive, genital and vaginal tracts, as a component of the native human microbiota (Bull et al., 2013).

Another economically significant and commercial strain of LAB that has probiotic properties and is used all over the world in the manufacturing of yogurt is Lactobacillus delbrueckii ssp. bulgaricus (L. bulgaricus). During the production of yogurt and fermented milk, L. bulgaricus is used and this strain plays a significant role in the development of the organoleptic, hygienic and probiotic characteristics of these foods (Teixeira, 2014).

The only probiotic yeast whose impact has been examined in double-blind clinical investigations is Saccharomyces boulardii (S. boulardii), a patented product. S. boulardii, a non-pathogenic yeast, was isolated from litchis in Indochina and is not a member of the native flora. Since the middle of the 20th century, this organism (S. boulardii) has been recommended, offering empirical proof of its effectiveness as an adjuvant drug for the treatment of diarrhoea. To assess S. boulardii's advantages for the host organism and to understand its methods of action, studies were conducted beginning in the 1980s. The effects of this yeast on infectious diseases and its impact on the mucosa and its immunomodulatory capabilities were investigated. The chances of survival of this strain during transit through the gastrointestinal tract, the optimal growth temperature of 37 °C and S. boulardii's capacity to suppress the development of several microbial pathogens are some properties that make it a potential probiotic agent. For the treatment and prevention of diarrhoea and other related gastrointestinal diseases caused due to on using antibiotics, S. boulardii is utilised in many different nations (Fietto et al., 2004). Some microorganisms commonly used as probiotics are listed in Table 1.

Health benefits of probiotics

Probiotic-rich foods are referred to be functional foods since these food products go beyond simple dietary needs to offer distinct beneficial health effects and disease-prevention characteristics. The health benefits of probiotics are one of the admired research interests within the food field for which a significant number of scientific researchers have demonstrated therapeutic evidence.

Increased resistance to infectious illness

The primary factors contributing to poor gut health include intestinal infections brought on by ingesting harmful bacteria from contaminated water and food. Probiotics can help to manage the challenging condition of foodborne illness. According to Gill et al. (2000), Bifidobacterium lactis HN019 can minimise the severity of infections caused by the pathogen Escherichia coli O157: H7 and this reduction may be associated with the probiotic's superior immune protection. By improving several immune function parameters important to the immunological regulation of salmonellosis, B. lactis HN019 can also offer a considerable amount of protection against Salmonella infection (Shu et al., 2000). The intestinal barrier protects the body from bacterial or dietary antigens that might trigger inflammatory processes and cause intestinal illnesses such as inflammatory bowel diseases by preserving the epithelial integrity. By competing with pathogenic bacteria for epithelial binding sites, probiotic microorganisms prevent Salmonella spp. and Escherichia coli strains from colonising the tissue (Lin et al., 2008). In addition, the probiotic yeast S. boulardii offers a defence mechanism against the intestinal damage and inflammation caused by Clostridium difficile's toxin A. This is possible because S. boulardii inhibits the activation of extracellular signal-regulated ½ (ERK ½) and mitogen-activated protein (MAP) kinases, thus modulating host signalling pathways (Chen et al., 2006). Mice fed S. boulardii and immunised with a Clostridium difficile toxin A exhibited an increase in a particular intestinal anti-toxin A level, which may protect them from diarrheal illnesses. A study by Qamar et al. (2001) reported that aflatoxin B1 can be bound by LAB both in vivo and in vitro, however, this ability appears to be strain dependent. In a study conducted by Gratz et al. (2006), rats were given Lacticaseibacillus rhamnosus strain through oral gavage while simultaneously receiving doses of aflatoxin B1. According to the study, Lacticaseibacillus casei was found to be the most effective binder of aflatoxin compared to other strains such as Lactiplantibacillus plantarum and Limosilactobacillus fermentum. Additionally, it was shown that Saccharomyces cerevisiae has a strong capacity to bind this aflatoxin. According to the FAO/WHO (2001), probiotics have beneficial health effects such as protection against a variety of gastrointestinal tract disorders, such as protection against diarrhoea brought on by specific pathogenic bacteria and viruses, activity against Helicobacter pylori infection, activity against complications of inflammatory diseases and bowel syndromes, the ability to prevent or delay the onset of specific cancers and the capacity to treat constipation.

Immune system modulation

It has been proposed that consuming probiotic organisms may modify the host's immune system. To preserve intestinal homeostasis, Galdeano et al. (2009) investigated the effects of fermented milk containing Lacticaseibacillus casei DN114001, which caused mucosal immune activation and reinforced the non-specific barrier. The capacity of several Bifidobacterium longum strains to stimulate the generation of cytokines by peripheral blood mononuclear cells was examined by Medina et al. in 2007. All strains of Bifidobacterium longum produced distinct cytokine patterns in living cells, indicating that bifidobacteria could influence immune responses differently.

Gill et al. (2000) and Arunachalam et al. (2000) found that adding Lacticaseibacillus rhamnosus (HN001, DR20), Lactobacillus acidophilus (HN017), Bifidobacterium lactis HN019 and B. lactis (HN019, DR10) strains to the diet improved various measures of both acquired immunity and natural immunity. Probiotics may influence the maturation of immune cells and their products not only in the gut but also in systemic immunological organs like the lymph node and spleen, resulting in tumour inhibition and these suggest that probiotics could be useful dietary supplements against neoplastic susceptibility due to their wide influence on the host's local and systemic immune mechanisms (Yu & Li, 2016; Yeboah et al., 2023).

Increased resistance malignancy

Anti-carcinogenic effect of probiotics has also been evaluated in several studies. In vitro studies have shown that certain strains of Lactobacillus and Bifidobacteria, along with Escherichia coli, possess the ability to metabolise and neutralise mutagenic substances, thus exhibiting anti-mutagenic activity. Mice were given the cytoplasmic fractions of Lacticaseibacillus casei YIT9029 and Bifidobacterium longum HY8001, and with this, they exhibited the ability to prevent the growth of tumour cells (Geier et al., 2006). It has been demonstrated that Lacticaseibacillus casei strain Shirota, when administered intranasally to mice, improved the cellular immune response by inducing the release of the antiviral proteins' interleukin-12, interferon-gamma and tumour necrosis factor-alpha, all of which are essential for eliminating influenza virus from the body (Hori et al., 2002).

In response to probiotic ingestion, Roller et al. (2004) found a correlation between the suppression of carcinogenesis in rats and changes in immune activity. Moreover, studies using animal models indicate that consuming probiotics may increase the activity of killer cells in the body, which may delay the formation of tumours. For instance, Takagi et al. (2008) employed the dietary strain Shirota of Lacticaseibacillus casei to prevent the growth of tumours in mice that were generated by the carcinogen methylcholanthrene.

Protection against allergies

Several studies have confirmed that probiotics can protect individuals against certain allergies. Isolauri et al. (2000) examined how twenty-seven breastfed children with atopic eczema responded to hydrolysed whey formulae supplemented with probiotics (Bifidobacterium lactis Bb12 and Lacticaseibacillus rhamnosus). They discovered that after 2 months, both groups' clinical atopic eczema symptoms and signs had diminished. A randomised controlled placebo experiment was also conducted by Kalliomäki et al. (2001) with 132 pregnant women who had atopic disorders such as atopic eczema, allergic rhinitis or asthma to varying degrees. For 2–4 weeks, these mothers took two capsules of a formulation containing Lacticaseibacillus rhamnosus, and the infant took the same formulation for 6 months postpartum. Throughout the first 2 years, the children were examined. According to the findings, just 23% of participants in the probiotic group had atopic eczema, compared to 46% of those in the placebo group. These studies provided insightful observations on the use of probiotic supplements in the prevention of various allergies. Certain bacterial species, such as Lactobacillus, Lactococcus, Pediococcus and Leuconostoc, are known for their ability to suppress or restrict the formation of mycotoxigenic mould (Gerez et al., 2009).

Beneficial effects on blood cholesterol

Probiotics may also have some beneficial influence on people beyond certain metabolic illnesses like hypertension. Many factors can lead to primary hypertension; however, hypercholesterolaemia is one of the main contributors (Lye et al., 2009). A considerable decrease in blood cholesterol may be caused by ingesting lactobacilli and bifidobacteria. This is because most of the cholesterol production takes place in the intestines, and the microbiota in the gut hence supports impacts on lipid metabolism. Probiotics have been shown in certain trials to encourage a reduction in blood cholesterol levels and an increase in low-density lipoprotein's resistance to oxidation, which can lower blood pressure. In vitro tests performed by Liong & Shah (2005) demonstrated that cholesterol could be eliminated from a medium by Lactobacillus acidophilus both through digestion during growth and by the binding of cholesterol to the cellular surface. This process was proposed after it was discovered that both dead and non-growing cells could eliminate cholesterol. The capacity of some probiotic bacteria to catalyse the enzymatic deconjugation of bile acids by bile salt hydrolase is another hypocholesterolaemic mechanism that has been reported. There was evidence of enzyme activity in the gut microbiota, including Lactobacillus and bifidobacteria species (Liong & Shah, 2005).

Potential reduction of risk of long-term diseases

Throughout human life, the gastrointestinal tract (GIT) acts as a reservoir for a diverse range of microorganisms, predominantly bacteria, known as gut microbiota. These microorganisms have a significant impact on the host's health and well-being through periods of homeostasis and illness (Yeboah et al., 2023). Consuming probiotics can aid in preserving an individual's overall health and wellness, particularly in those who are already in good health. Additionally, it has been suggested that this practice may also reduce the likelihood of developing colon, kidney, respiratory and heart conditions in the long run (FAO/WHO, 2001).

Reducing lactose intolerance

Lactobacillus bulgaricus and Bifidobacterium bifidum are the two main strains that may synthesise the β-galactosidase enzyme, which can also hydrolyse lactose in milk and increase tolerance for dairy products (Kim & Gilliland, 1983). To help people better digest lactose, Kim & Gilliland (1983) examined the impact of L. acidophilus as a dietary supplement in milk. Because the lactose was not hydrolysed before consumption, and concluded that better lactose digestion was not the result of this. This suggests that a good impact must have happened in the digestive system after the ingestion of milk containing L. acidophilus.

Probiotic foods and beverages

The global market for probiotic products is growing rapidly due to increased consumer awareness of the potential health benefits they offer. In 2007, the market for probiotic foods and supplements was valued at $14.9 billion, and yearly growth was predicted to be 4.3%. (Agheyisi, 2008). Over the last decade, approximately 500 new products including yogurt and cheese have some advantages simply because dairy products help to maintain the viability of probiotic. Other commercially available fermented dairy products include Acidophilus milk, Acido-whey, Ice-cream, Lassi, Curd, Nonfermented Goat's Milk Beverage and Kefir (Sheth et al., 2022). The non-dairy probiotic goods may be produced from several raw materials, such as cereals, millet, legumes, fruits and vegetables. Various ranges of non-dairy probiotic foods and beverages have been developed and commercialised worldwide in the last few years throughout the world (Dey, 2018). A common example of traditional rice-based probiotics foods includes Appam. Kimchi and Sauerkraut are probiotic products from vegetables. Ngari and Som-fug are fished-based probiotics foods while Agbelima and Tempeh are made up of Casava. Besides a variety of traditional probioticated foods, many naval probiotic foods and beverages are commercially available as well. Table 2 shows some traditional probiotic foods and beverages.

Fermented foods

Definition and history of fermented foods

One of the oldest and most cost-effective ways to prepare food is through fermentation, which is described as a technology that uses the development and metabolic processes of microbes to preserve food. Foods and beverages that have undergone fermentation typically involve the enzymatic modification of nutritional components, including microorganisms.

Fermentation is the primary method of producing food in several civilisations because it is a low-cost process that uses relatively little energy. There are two types of food fermentation: aerobic fermentation process, which includes fungal and alkaline processes, and anaerobic fermentation process, which includes alcoholic and lactic acid biochemical processes (Wilburn & Ryan, 2017).

The starting ingredient includes the bacteria that cause the fermentation of native foods and sometimes yeast. The fermentation process has been modernised by adding extra beneficial steps like starter culture production, controlled multi-step fermentation and fermented functional food production to avoid contamination with pathogenic microbes, an unsafe by-product created by undesirable microbes during the fermentation and to achieve an improved health-beneficial fermented product (De Vuyst et al., 2016).

Humans have been producing and eating fermented foods since the Neolithic era (about 10.000 BCE) when local tribes in Africa and other emerging nations first started using them. Depending on their geographic location, climatic circumstances and access to a source, different people consume different kinds of fermented foods (Gille et al., 2018). The techniques of preparation have a considerable effect on the quality of fermented meals. In fermentation, the quality and the kind of fermented foods are mostly controlled by the bacteria and yeast engaged in the fermentation process. Common microorganisms involved in fermentation include LAB, Propionibacterium, Acetobacter, yeast, moulds and Bacillus sp. These organisms are responsible for generating lactic, acetic and propionic acids, alcohol, ammonia and fatty acid groups, including those found in meat and fish. According to several epidemiological studies, decreases in many illnesses, including metabolic disorders, cardiovascular and immune-related diseases, as well as cognitive decline, have been associated with fermented dairy products including the prevention of obesity and the reduction of risk for these conditions (Marco et al., 2017) as found in Fig. 1.

International traditional fermented food

Traditionally, fermented meals with probiotic microbes have shown health benefits. Few nations, including Australia, Kenya, South Africa, India, Sri Lanka, Oman, Qatar and Bulgaria, have included recommendations for the intake of fermented foods in their national dietary standards. In the above nations, native and traditional fermented foods are also accessible and constitute an integral part of the national culture. Fruits and vegetables are extremely perishable food products and as such fermentation has been employed across the world to increase their shelf life in addition to the production of foods with a longer shelf life. The quantity of fermented Asian food products, such as sauerkraut, tempeh, kimchi, gundruk, khalpi and sinki, suggests that Asian societies consume more fermented foods frequently than Western ones (Tasdemir & Sanlier, 2020).

Nigerian indigenous fermented foods (IFF) and beverages

In some countries in Sub-Saharan Africa especially Nigeria, IFF comprised most of the population's diet, with some serving as weaning food for newborns, adult meals and beverages. These foods have enormously positive effects on the health, nutrition and socio-economic standing of the population (Adesulu-Dahunsi et al., 2018). Adesulu-Dahunsi et al. (2018) reported that LAB and yeasts play a prominent and significant role in the fermentation processes during the manufacturing of these foods (Adesulu-Dahunsi et al., 2018).

Tempeh

Vegans are particularly interested in tempeh because it includes a significant quantity of vitamin B₁₂. Tempeh is a traditional Indonesian fermented food often prepared from soybeans. Nevertheless, researchers have demonstrated that the generation of B₁₂-enriched lupin tempeh is possible when Propionibacterium freudenreichii and Rhizopus oryzae are co-cultured using lupin as a substitute substrate (Rezac et al., 2018).

Tarhana

Tarhana is a traditionally fermented Turkish food that is often prepared with one half being yogurt and the other being wheat. Additionally, it is also produced by combining a variety of vegetables, such as onions, tomatoes, peppers, with yeast, salt and seasonings, such as mint and chilli pepper, and storing the mixture for about a week (1–7 days) (Şanlier et al., 2019).

Koumiss

Koumiss is a traditional fermented dairy food from Central Asia that is often made from mare's milk and is produced by fermenting lactic acid and alcohol (Chen et al., 2010). Koumiss originated with Asia's nomads and is still widely eaten in west and central Asian countries including Mongolia, Kazakhstan, Kyrgyzstan and Russia (Abdel-Salam et al., 2020). Its microflora contains LAB (Lactobacillus acidophilus and Lactobacillus delbrueckii subsp. bulgaricus) lactose-fermenting yeast (Candida koumiss K. Marxianus var. Marxianus and Saccharomyces spp.), non-lactose-fermenting yeast (Saccharomyces cartilaginous) and non-carbohydrate-fermenting yeast (Mycoderma spp.) (Abdel-Salam et al., 2020).

Kefir

Kefir is one of the old fermented milk beverages. It tastes sour, acidic and faintly alcoholic and has a creamy texture, having a creamy texture. Kefir is produced when the bacteria found in kefir grains digest milk in an acidic, alcoholic manner (Kesenkaş et al., 2017). To produce acid-alcoholic fermentation, various yeast, acetic acid and LAB strains collaborate. The possible health advantages of kefir are due to the diverse microbiota and fermentation metabolites produced by these distinct bacteria (Bourrie et al., 2018). Kefir has gained popularity in recent years because of its appealing organoleptic characteristics and beneficial health properties, including those that are anti-hypertensive, hypocholesterolaemic, anti-inflammatory, anti-carcinogenic, anti-allergenic, anti-bacterial, anti-diabetic, antioxidant and probiotic (Rosa et al., 2017). Regular kefir drinking is also excellent for digestive and immunological health. It relieves lactose intolerance effects by controlling blood glucose levels associated with diabetes (Şanlier et al., 2019).

Turnip juice

Traditional Turkish turnip juice is a dark crimson beverage made by fermenting turnips, black carrots, rock salt, bread yeast and bulgur flour. It includes potassium, phosphorus, calcium and iron, among other minerals. High anthocyanin and antioxidant content (Şanlier et al., 2019).

Sucuk (Turkish fermented dry sausage)

Sucuk is one of the most important and popular foods found in Turkey. The process for making this traditional fermented food in Turkey involves first slicing beef or lamb, adding fat, spices, preservatives, colouring agents and starter cultures such as LAB and staphylococci, and then adding the finished product (Akkaya et al., 2014). Whereas sucrose or glucose is provided as a fermentable substrate for LAB during the process, nitrite or nitrate is added because of its antioxidant and antibacterial properties. By producing bacteriocins, organic acids and acidifying carbohydrates, LAB, which are the main microorganisms used in the fermentation of meat, prevent the growth of pathogenic and spoilage microorganisms (Kabak & Dobson, 2011).

Health benefits of fermented foods

Consuming fermented foods has numerous reported health benefits, such as preventing and managing metabolic disorders, cardiovascular diseases, osteoporosis, allergies, atherosclerosis, cognitive improvement, immunological enhancement and even lowering blood cholesterol levels. These benefits are due to the presence of beneficial bacteria in fermented foods. For example, fermented foods containing galactosidase-producing bacteria can enable lactose-intolerant individuals to consume dairy products without experiencing any adverse effects, as reported by Savaiano in 2014. It has been shown that fermented foods are a rich source of bioactive microorganisms with many health benefits. The fermented plant extracts have also been used in the formulation of cosmetics (Sivamaruthi et al., 2018). To establish the functioning of the meal, clinical studies must corroborate the reported results. Research by Şanlier et al. (2019) has demonstrated that adding fermented foods to one's diet can lower the health risks associated with diabetes mellitus. Available cancer therapies have emphasised less harmful and more effective medicines. Evidence from past and present medical and nutritional research indicates that dietary substances may boost anticarcinogenic activity and control physiological functioning (Fang et al., 2018). Natural foods have therefore become more popular in cancer prevention and therapy (Zhang et al., 2015). There are some theories that suggest certain elements found in fermented foods could potentially reduce the risk of cancer (Rai & Jeyaram, 2015). Fermented foods are considered ‘naturally fortified functional nutrients’ because they promote a healthy gut microbiome which helps maintain physiological balance and may aid in preventing various illnesses. Due to their function in the production of secondary metabolites during fermentation, including bacteriocins, ethanol, acetic acid, aromatic compounds, exopolysaccharides, bioactive peptides, vitamins and certain enzymes, LAB are essential to these processes (Sharma et al., 2018). The relationship between fermented foods and their health benefits is found in Table 3.

Principles behind the safety of fermented foods

Fermentation is considered one of the oldest means of food preservation used alongside cooking, slating, and smoking. Before the advent of modern forms of preservation technologies, humans, especially in the African continent, had to choose between starvation and eating contaminated food as a means of survival (Steinkraus, 2018). Over the years, microbial fermentation has played a significant role in food processing by enhancing better ways of food preservation, preserving the nutritional value of foods and reducing the amount of energy needed in cooking some foods. Two main classes of traditionally fermented food are submerged culture fermentations (SCFs) and solid-substrate fermentation (SSFs). In SSFs, the microbial activity occurs on the solid substrate surfaces, while in SCFs, it occurs on low-concentrated biomass in a liquid phase. One of the main differences between SSFs and SCFs is that the processing of SSF takes place in moisture contents ranging between 10% and 20%, which favours the growth of filamentous fungi. However, the microbial interactions in several indigenous fermentations contain mixed and complex combinations of yeast bacterial, fungal yeast and fungal bacteria, making it important to observe the safety principles behind fermented foods to make them safe for human consumption.

Among the reasons for the safety principles of fermented food include the need to ensure safe food for consumption and the preservation of important nutrients. Fermented foods are usually produced using fungi, which increases the risk of mycotoxin contamination, which is the main cause of food poisoning in fermented foods. During the natural fermentation process, coliforms and food-poisoning microbiota components have the potential to grow alongside the lactic culture. This makes it important to ensure that such microorganism is removed to ensure safety of fermented foods for consumption. Several factors improve the safety of fermented foods. These include soaking and cooking treatments which help in reducing microbial toxins. Another factor is salting and addition of suitable preservative to fermented foods. Several fermented foods are produced by acid formation, especially in indigenous fermentation. These acids include fumaric, acetic and lactic, which act as bacteriostatic and preservative agents in inhibiting the growth of bacteria and maintaining an optimal pH of between 3.6 and 4.1 (Behera et al., 2018). Despite the observation of these factors, it has been evidenced that the quality of some oriental food is still poor, thus making it essential to observe the safety principles of fermented foods critically.

There are several safety principles for fermented products. First, fermentation that involves the use of lactic acid is safe. Using lactic acid in fermentation ensures the conversion of sugars to lactic acid (Marco et al., 2021). For example, in the fermentation of cabbages, with the use of salt, Leuconostoc mesenteries first grow and produce carbon dioxide, acetic and lactic acid. The production of lactic acid under a pH of 4.0 prevents the growth of contaminable microorganisms, thus preserving them for a long time.

Second, the food substrates with edible and desirable organisms do not support the growth of food poisoning and food spoilage microorganisms, which makes it difficult for the undesirable microorganism to compete. This is made possible through correct fermentation temperature, salt levels and enough acid production. The correct salt levels vary from one food product to the other, and range from 2.25% to 13%, especially in meaty products (Marco et al., 2021). It is important for companies to correctly measure the concentration levels of salt and provide a tested recipe for the consumers. The development of food poisoning bacteria during the fermentation of food products is prevented by using the right temperatures. Anyogu et al. (2021) assert that normal temperatures for many foods range between 68 °F and 75 °F. This range allows fermented foods to stay fresh between 3 and 4 weeks. Fermented foods above 75 °F are at an increased risk of spoilage and thus cause food poisoning.

Lastly, producing sufficient acid in fermented foods is important in maintaining their nutritional value and keeping it safe for human consumption. Sufficient acids in food that can lower the equilibrium pH to less than 4.6 are crucial for food safety (Marco et al., 2017). During the fermentation process, it is crucial to countercheck the food pH values during the reaction and ensure an optimal pH of 4.6 and below at the end of the process.

Synbiotics as functional fermented foods

Synbiotics was defined as dietary supplements that combine probiotics and prebiotics (selectively fermentable, non-digestible dietary elements such as inulin and its hydrolytic products, oligofructose, galactooligosaccharides, etc.) (Gibson & Roberfroid, 1995). The definition for synbiotics was defined and updated during the 2019 International Scientific Association for Probiotics and Prebiotics (ISAPP) congress. ‘A combination consisting of live microorganisms and substrate(s) preferentially utilised by host microorganisms, which impart health benefits on the host’. The ISAPP has recently divided synbiotics into two subcategories, according to Swanson et al. (2020). These subcategories are complementary and synergistic respectively. An established probiotic and prebiotic make up a complementary synbiotic, but a synergistic synbiotic also includes a substrate that the co-administered bacteria may use preferentially (not necessarily probiotics). One instance of a synergistic synbiotic is a combination of beneficial and healthy LAB, such as Lactobacillus sp., and their preferred food, lactose (the most common natural sugar in milk), which supports the growth of Lactobacillus sp. specifically rather than feeding all the resident members of the gut microbiota. A health benefit in a human host must be proven for both subgroups. The delivery of synbiotics to humans has several health advantages, including (1) a balanced gut microbiota and higher numbers of lactobacilli and bifidobacteria, (2) enhancing immunomodulatory capacity, (3) preventing bacterial transfer and (4) enhancing liver health and lowering the frequency of nosocomial infections in postoperative patients (Markowiak & Śliżewska, 2017; Batista et al., 2020).

Although certain fermented foods may contain prebiotics and probiotics, not all of them may be referred to be synbiotics. For instance, pickles may include potential biotics, but they are processed so that the microorganisms often do not survive. Information about the microbial levels that foods must present to be considered probiotic is important. According to researchers, conventional food should be considered a source of synbiotics for the creation of innovative functional goods during fermentation.

Many studies have demonstrated the significance of fermented dairy products containing prebiotics and other types of probiotic bacteria as synbiotics (Delgado-Fernández et al., 2020; Li et al., 2020). A broad variety of prebiotics is added to milk-based meals as probiotic protections. In a study by Falah et al. (2021), synbiotics yogurt containing inulin Levilactobacillus brevis was produced. According to this study, the amount of L. brevis PML1 in the product was 10⁸ CFU g⁻¹, and it was resistant to simulated gastric juice. Furthermore, the symbiotically produced yogurt remarkably boosted the secretion of antimicrobial compounds, had the most significant antibacterial property against Salmonella typhimurium (Falah et al., 2021). In separate research by Fazilah et al. (2019), yogurt was enhanced with microencapsulated Lactococcus lactis by spray-drying with a combination of gum Arabic and Synsepalum dulcificum, which gave Lactococcus lactis improved viability than the free form in yogurt formulation. Lactic acid and probiotic bacteria persisted (>6 log CFU g⁻¹) in fermented milk containing organic banana flour after resistant starch (3.0–10.3 g/100 g) was added. With the addition of 3% w/v green banana flour, higher levels of post-acidification, proteolysis, lactic acid and acetic acid were detected (GBF). Nevertheless, it enhanced the fatty acid profile (increasing long-chain fatty acids like oleic, linoleic and -linolenic acid) and helped in bringing out volatile compounds (esters, ketones and carboxylic acids), which influenced how well customers perceived the flavour and aroma of the products. GBF offers value as a functional food, particularly as a synbiotic product, and is used as an alternative component in fermented milk compositions (Batista et al., 2017). Ningtyas et al. (2019) examined the long-term survivability of Lacticaseibacillus rhamnosus in cream cheese. Certain probiotics such as Lactobacillus sp. and Bifidobacterium sp. can thrive and cling to surfaces more effectively due to the fermentable nature of b-high glucan by the intestinal microbiota in the cecum and colon. B-glucan may be able to promote the development and adherence of probiotics like lactobacillus and bifidobacteria because of its fermentability by the gut microbiota in the cecum and colon. During 35 days of refrigerator storage, probiotic cream cheese with b-glucan and phytosterol emulsion showed a minimal decline in Lacticaseibacillus rhamnosus viable counts (Ningtyas et al., 2019). Contrarily, it has been demonstrated that some prebiotics, such as soluble maize fibre, polydextrose and inulin, can change the sensory characteristics of fermented yogurt beverages while also failing to increase the survivability of Bifidobacterium lactis and Lactobacillus acidophilus during storage (Kareb & Aïder, 2019).

Some probiotic bacteria have the ability to produce certain capsule needed to become synbiotic foods, such as cereal-based effective foods (Budhwar et al., 2020). Because endogenous enzymes that break down antinutritional substances are activated during fermentation, foods that have undergone fermentation have more nutritional value than unfermented ones. Because of higher levels of compounds like vitamin C and easier release of various health-promoting bioactive components because of a weakening of the grain matrix, fermented foods have more antioxidant potential than their unfermented products. Cereals are one source of staple foods which contain protein, dietary fibre and carbohydrates since these foods are formed of grains. Cereals are also a good source of essential minerals including iron, zinc, magnesium and phosphorus as well as vitamins like those in the B- and E-groups of vitamins (Flight & Clifton, 2006). When cereals are symbiotically administered by probiotics, these products might protect against cardiovascular disease and gastrointestinal malignancies.

Dietary fibres were utilised in the dark chocolate formulation by Erdem et al. (2014), who investigated how the colour and organoleptic properties of dark chocolate were affected by dietary fibres (maltodextrin and lemon fibre) and the probiotic Bacillus indicus HU36. To achieve 6.08 log CFU g⁻¹ of chocolate, chocolate couverture that had been melted at 45 °C in a water bath was combined with lyophilised Bacillus indicus HU36 spores. The survival rate for B. indicus HU36 was between 88% and 91%. While the presence of bacteria and dietary fibre had no adverse influence on the products' sensory or colour qualities, the combination of bacteria and dietary fibre did considerably increase several of these qualities, such as sweetness, firmness and adhesion. However, typical production methods were not employed in this investigation, and quality aspects of the chocolates, including flow behaviour and melting qualities, were not examined (Erdem et al., 2014).

Metchnikoff's concept of probiotics/fermented foods

Elie Metchnikoff initially proposed the basic idea of probiotics in 1907, when he connected the longevity and improved health of Bulgarian farmers to the use of LAB-containing fermented milk products. Using the phrase ‘the pathogenic bacteria reconstituted with beneficial’, Elie Metchnikoff introduced the idea that microbiota may be changed (Dubey et al., 2019). Elie Metchnikoff found that the amount of microbiota in the faeces of children with diarrhoea was significantly low, as shown by the morphologically foreign Y-shaped cells (Guarner et al., 2008). Elie Metchnikoff also looked into proteolytic microorganisms like Clostridium, which break down proteins and create poisonous byproducts like phenols, indoles and ammonia, with helpful microorganisms which may be replaced with antioxidants that could delay the aging process. According to Metchnikoff's research, Lactobacillus bulgaricus can decrease the development of arteriosclerosis and other elements of ageing that result from the unchecked production of gut toxins (Bested et al., 2013). Metchnikoff is now acknowledged as the movement's creator after long-term research studies were published (Ailioaie & Litscher, 2021).

Microorganisms played a significant role in our ancestors' diet; however, urbanised eating habits exposed consumers to microbial foods much less frequently (Logan et al., 2015). Chronic illnesses have been linked to this decreased exposure to microbes (Kramer et al., 2013). Consumers now choose goods with higher helpful values since consumers are more health concerned. These requirements encourage producers to create novel foods. As a result, functions that enhance food value are necessary for both consumer acceptance of innovative goods and effective marketing. Active substances released by biological organisms can be processed into novel food items or naturally added to them. When used in the proper quantity, these chemicals offer health advantages apart from those offered by nutrients. This has given rise to a new field known as functional fermented foods (Akmal et al., 2022; Ghosh et al., 2022).

Our opinion on fermented and probiotic fermented foods

Fermented foods

Fermented foods are foods and drinks produced by controlled microbial growth and the conversion of food components through enzymatic activity (Marco et al., 2021). The results of these microbial growths and enzymatic activities subject fermented foods to a wide range of health benefits due to the live probiotic strains some fermented foods may still contain after fermentation. Yogurt is typically one of the usual fermented foods which are produced because of synergistic interaction between Streptococcus thermophilus and L. bulgaricus (Ayivi and Ibrahim, 2022). The term ‘fermented foods and drinks’ encompasses a wide range of products produced all over the world from various raw ingredients. It comprises a variety of items that are often made by fermentation but may not, at the time of consumption, contain active microbes. Items like leavened bread are baked after they have been fermented, killing the bacteria that caused the fermentation in the process. Although mobile activation or elimination is not a requirement for all fermentation procedures, foods categorised in this way nevertheless meet the definition of fermented foods (Marco et al., 2021). Recent epidemiological research has found that diets high in fermented foods can lower disease risk and improve lifespan, health and quality of life in addition to their value to public health, food preservation and quality. A non-fermented food that has been supplemented with additional microorganisms cannot also be regarded as fermented. For example, mustard, salad dressing and other condiments may contain some ingredients that are produced through fermentation, such as vinegar or sour cream, but these do not qualify such products to satisfy the definition to be classified as fermented foods. Finally, there are fermented foods that are chemically created; these foods are not fermented. For instance, some soft cheeses may be produced using chemical acidification and ‘pickling’ methods are frequently used to preserve fruits and vegetables without the need for forced bacteria. Table 4 shows the classification of fermented foods based on the presence of live microorganisms.

Probiotics and probiotic fermented foods

Probiotics are commonly referred to as friendly, beneficial or healthy bacteria live microorganisms which confer a beneficial effect on the health of the host. Probiotic foods are therefore also known as functional foods in ways such as the method of delivery, physiological activity, gastrointestinal transit, etc. In probiotics, the organism must be a live microbe, must be examined and demonstrated to have beneficial health effects, and must deliver a level of live microbes shown to confer benefits.

Probiotic fermented foods, on the other hand, are foods that contain live microbes, tested and shown to have health benefits that result in at least partially from the live microbes present.

Difference between fermented foods and probiotics

To inform consumers that a product contains live, health-promoting microorganisms, producers of associated fermented foods and beverages may occasionally classify or label these products as ‘probiotic foods’ or ‘contains probiotics’. However, the word ‘probiotic’ should be used only when there has been evidence of a health benefit brought about by specific and identifiable living microorganisms (Marco et al., 2021). Any other linked health benefits from eating these products must go beyond any nutritional advantages provided by the food matrix and must be at least partially attributable to the action of the live microbes. As such, the phrases ‘fermented food’ and ‘probiotics’ should not be used interchangeably during sentences (Marco et al., 2021). According to Marco et al. (2021), for a product to be introduced to the market as a probiotic fermented food with an extra predefined beneficial effect, it must have evidence of a strain-specific benefit from a carefully controlled intervention research, as well as safety that has been established and verification that there is enough of that strain in the finished product to deliver the claimed benefit. Even in the lack of strain-specific evidence that the live microorganisms contained in them are helpful to health, some fermented foods might be legitimately promoted as ‘contains probiotics’. This claim is only validated, though, if at least one of the probiotic strains in the food also belongs to a species that has been shown to provide probiotic beneficial properties under the concept of ‘shared benefits’ (Marco et al., 2021). This idea is supported by the understanding that specific bacterial species that are continuously active in investigations involving humans have preserved qualities linked to enhancing health (Sanders et al., 2018). In this regard, different countries recognise and use the term ‘probiotic’ in foods in different ways. For instance, Health Canada acknowledges more than twenty species of the Lactobacillus genus complex and Bifidobacterium provided they are administered at a minimum of 10⁹ colony-forming units per meal (Health Claims, 2013). Depending on the essential presence of the lactase enzyme in yogurt cultures (L. bulgaricus and Streptococcus thermophilus), the European Food and Safety Authority has granted live yogurt cultures and improved lactose digestion health claims in Europe (EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2010). Nevertheless, in this perspective, even though fermented foods contain a number several bacterial species, the phrase ‘contains probiotics’ is only appropriate when the strains present in that fermented food are known down to the genome level, the genome sequences are known, and the strains are present in the proper quantity throughout the product shelf-life (Marco et al., 2021). Most fermented foods that are now available for purchase in supermarkets are likely to not meet the description of ‘probiotic fermented foods’. According to Hill et al. (2014), it is recommended that producers clearly state if their product contains live and active cultures. However, this only applies if the food has not undergone any processing that would kill off the beneficial microorganisms, and if the quantity present is typical for that type of food. If pasteurised fermented foods do not contain live microbes, they can still be labelled as ‘foods prepared by fermentation’ and be legally recognised (Marco et al., 2021). Tables 5 and 6 provide the general guidelines for identifying probiotics, probiotic fermented foods and fermented foods in general.

Conclusion

Fermented foods are essential for enhanced immune function and are highly regarded for their functional properties that promote human health and nutrition. Moreover, the synergistic beneficial effect of probiotics in fermented foods regarding human health cannot be overemphasised. Several genera of probiotic bacteria such as bifidobacteria, Bacillus and lactobacillus as well as other microorganisms such as yeast have been utilised for fermented foods, and a significant number of these foods are produced by LAB. Due to increased consumer interest in fermented functional foods, it would seem worthwhile to provide a framework for assisting consumers in distinguishing between probiotics and fermented foods as functional and high-nutritional foods. Consequently, this summary of our current knowledge will help to promote a greater interest in clean-label products such as fermented foods produced from probiotic microbes. In addition, because fermented foods typically contain LAB, the isolation of these useful bacteria could provide additional functional characteristics that could also serve to improve the digestive health and overall nutritional well-being of consumers.

Acknowledgments

This publication was made possible by grant or project number NC.X308-5-18-170-1 from the National Institute of Food and Agriculture (NIFA). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NIFA. The authors also acknowledge the support of the Department of Family and Consumer Sciences and the Agricultural Research Station at North Carolina Agricultural and Technical State University (Greensboro, NC, 27411 USA).

Author contributions

Abdulhakim S. Eddin: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal). Salam A. Ibrahim: Conceptualization (equal); data curation (equal); formal analysis (equal); funding acquisition (equal); investigation (equal); methodology (equal); project administration (equal); resources (equal); supervision (equal); validation (equal); visualization (equal); writing – review and editing (equal). Namesha D. Wijemanna: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal). Philip J. Yeboah: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal); writing – review and editing (equal). Raphael D. Ayivi: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal); writing – review and editing (equal). Rea V. Bakhshayesh: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal). Saeed Paidari: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal).

Conflict of interest

The authors of this article hereby declare no conflict of interest.

Ethical guidelines

Ethics approval was not required for this research.

Peer review

The peer review history for this article is available at https://www.webofscience.com/api/gateway/wos/peer-review/10.1111/ijfs.16619.

Data availability statement

Data sharing does not apply to this article as no new data were created or analysed in this study.

References