1 Department of Toxicology, Faculty of Pharmacy, “Carol Davila” University of Medicine and Pharmacy, 3-6, Traian Vuia Street, Sector 2, 020945 Bucharest, Romania; or.dcfmu.drd@nacirdnim-atinoi.acnaib-aniroc (C.-B.I.-M.); or.dcfmu@iergen.anilorac (C.N.)
Find articles by Corina-Bianca Ioniță-Mîndrican2 Department of Clinical Laboratory and Food Safety, Faculty of Pharmacy, “Carol Davila” University of Medicine and Pharmacy, 3-6, Traian Vuia Street, Sector 2, 020956 Bucharest, Romania; or.dcfmu@nasorom.anele
Find articles by Khaled Ziani2 Department of Clinical Laboratory and Food Safety, Faculty of Pharmacy, “Carol Davila” University of Medicine and Pharmacy, 3-6, Traian Vuia Street, Sector 2, 020956 Bucharest, Romania; or.dcfmu@nasorom.anele
Find articles by Magdalena Mititelu3 Microbiology Department, Faculty of Biology, University of Bucharest, 1-3 Portocalilor Way, 060101 Bucharest, Romania
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Find articles by Elena Moroșan5 Department of Organic Chemistry, Faculty of Pharmacy, “Ovidius” University of Constanta, 6, Căpitan Aviator Al Șerbănescu Street, 900470 Constanta, Romania; or.suidivo-vinu@ucsertimud.asined
Find articles by Denisa-Elena Dumitrescu6 Department of Drug Analysis, Biopharmacy and Biological Medicines, Faculty of Pharmacy, “Ovidius” University of Constanta, 6, Căpitan Aviator Al Șerbănescu Street, 900470 Constanta, Romania; or.suidivo-vinu@acsor.nimsoc
Find articles by Adrian Cosmin Roșca7 Department of Pharmaceutical Physics and Informatics, Faculty of Pharmacy, Carol Davila University of Medicine and Pharmacy, 6, Traian Vuia Street, 020956 Bucharest, Romania; or.dcfmu@ucsenagard.aniod
Find articles by Doina Drăgănescu1 Department of Toxicology, Faculty of Pharmacy, “Carol Davila” University of Medicine and Pharmacy, 3-6, Traian Vuia Street, Sector 2, 020945 Bucharest, Romania; or.dcfmu.drd@nacirdnim-atinoi.acnaib-aniroc (C.-B.I.-M.); or.dcfmu@iergen.anilorac (C.N.)
Find articles by Carolina Negrei Isabel Goñi, Academic Editor1 Department of Toxicology, Faculty of Pharmacy, “Carol Davila” University of Medicine and Pharmacy, 3-6, Traian Vuia Street, Sector 2, 020945 Bucharest, Romania; or.dcfmu.drd@nacirdnim-atinoi.acnaib-aniroc (C.-B.I.-M.); or.dcfmu@iergen.anilorac (C.N.)
2 Department of Clinical Laboratory and Food Safety, Faculty of Pharmacy, “Carol Davila” University of Medicine and Pharmacy, 3-6, Traian Vuia Street, Sector 2, 020956 Bucharest, Romania; or.dcfmu@nasorom.anele
3 Microbiology Department, Faculty of Biology, University of Bucharest, 1-3 Portocalilor Way, 060101 Bucharest, Romania
4 Professional Farma Line, 116 Republicii Street, 105200 Baicoi, Romania; or.amrafp@uscaen.leniros5 Department of Organic Chemistry, Faculty of Pharmacy, “Ovidius” University of Constanta, 6, Căpitan Aviator Al Șerbănescu Street, 900470 Constanta, Romania; or.suidivo-vinu@ucsertimud.asined
6 Department of Drug Analysis, Biopharmacy and Biological Medicines, Faculty of Pharmacy, “Ovidius” University of Constanta, 6, Căpitan Aviator Al Șerbănescu Street, 900470 Constanta, Romania; or.suidivo-vinu@acsor.nimsoc
7 Department of Pharmaceutical Physics and Informatics, Faculty of Pharmacy, Carol Davila University of Medicine and Pharmacy, 6, Traian Vuia Street, 020956 Bucharest, Romania; or.dcfmu@ucsenagard.aniod
† These authors contributed equally to this work. Received 2022 May 29; Accepted 2022 Jun 23. Copyright © 2022 by the authors.Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Throughout history, malnutrition and deficiency diseases have been a problem for our planet’s population. A balanced diet significantly influences everyone’s health, and fiber intake appears to play a more important role than previously thought. The natural dietary fibers are a category of carbohydrates in the constitution of plants that are not completely digested in the human intestine. High-fiber foods, such as fruits, vegetables and whole grains, have consistently been highly beneficial to health and effectively reduced the risk of disease. Although the mode of action of dietary fiber in the consumer body is not fully understood, nutritionists and health professionals unanimously recognize the therapeutic benefits. This paper presents the fiber consumption in different countries, the metabolism of fiber and the range of health benefits associated with fiber intake. In addition, the influence of fiber intake on the intestinal microbiome, metabolic diseases (obesity and diabetes), neurological aspects, cardiovascular diseases, autoimmune diseases and cancer prevention are discussed. Finally, dietary restrictions and excess fiber are addressed, which can cause episodes of diarrhea and dehydration and increase the likelihood of bloating and flatulence or even bowel obstruction. However, extensive studies are needed regarding the composition and required amount of fiber in relation to the metabolism of saprotrophic microorganisms from the enteral level and the benefits of the various pathologies with which they can be correlated.
Keywords: dietary fiber, metabolic disorders, health effects, dietary fiber characterisation, metabolic syndrome, type 2 diabetes, dyslipidaemia, short-chain fatty acids
From a quantitative point of view, to ensure a daily energy intake of 2000 kcalorie, a typical food macronutrient distribution should be provided by 250–275 g carbohydrates (from which 30–40 g of fiber), 100–125 g protein and under 66.66 g of primarily unsaturated fats [1]. An optimal amount of fiber can be obtained by the daily consumption of vegetables, legumes, whole grains and oilseeds in the diet. These foods are rich in essential nutrients (vitamins, minerals and antioxidants) and in fiber, thereby, providing all the benefits of a healthy and balanced diet. Nutritionists recommend that, for excellent digestion, a normal body weight and a low risk of developing cardiovascular diseases, at least 50% of all cereals consumed should be unprocessed. Most nutritionists recommend an intake of 18–38 g of fiber/day for adults, which is around 8–20 g per 1000 kcal [2,3,4]. The WHO/FAO and EFSA recommend an average daily intake of 25 g of fiber per adult [5,6].
A higher natural dietary fiber (NDF) intake is associated with fewer metabolic diseases (obesity, diabetes and cardiovascular disease) and plays an essential role in intestinal health. Increased NDF intake causes various physiological effects, both locally in the gut and systemically. For example, NDF can significantly alter the intestinal environment, affecting the intestinal microbiome and influencing the intestinal barrier, gastrointestinal immune and endocrine responses, the nitrogen cycle and microbial metabolism. These changes associated with the gut can then alter the physiology and biochemistry of the other major organs in the management of nutrients and detoxification of the body (liver and kidneys) [7].
Fiber intake is associated with other lifestyle factors, such as the increased consumption of fruits and vegetables and exercise. In addition, high fiber diets are usually lower in fat and energy density and help to maintain a healthy body weight [8]. E. H. Hipsley first used the name dietary fiber in 1953 for non-digestible constituents of plant origin [9]. Dietary fibers are found naturally in food and can be added to food for nutritional and therapeutic roles simultaneously, such as functional or processed fiber. Thus, functional fibers are extracted from natural sources and added to processed foods [10].
NDF refer to edible plant parts or carbohydrate equivalents in the composition of edible plants that are resistant to digestion and absorption in the small intestine but can be fermented partially or entirely in the colon. Polysaccharides, oligosaccharides, lignin and various chemicals linked with these categories in plants fall under this group (waxes, phytates, saponins, tannins, etc.). The laxative action, cholesterol reduction and serum glucose reduction are vital physiological effects of these nutrients [11,12,13]. A classification of the dietary fibers obtained from food is presented below ( Table 1 ).
The classification of dietary fibers according to the composition, properties and main sources [13,14,15,16].
| Poly-/Oligo-Saccharides Class | Sources | Main Units | References |
|---|---|---|---|
| Non-Starch Polysaccharides, MU ≥ 10 | |||
| Cellulose * | Cereals, pulses—outer layers, root and leafy vegetables, legumes, pears and apples | Glucose monomers | [17] |
| Hemicellulose ** | Cereal bran and whole grains (starchy endosperm and aleurone layer), vegetable and fruit cell walls | D-xylose, D-mannose, D-galactose and L-arabinose | [14] |
| Mannans and heteromannans | Date, green coffee bean seeds and aloe vera Grain legumes (endosperm) Iris seeds and lily bulbs Norway spruce wood pulp | Mannans *, galactomannans # , glucomannans # and galactoglucomannans | [16] |
| Pectins # | Apple and citrus peel (and other fruits), cabbage, whole grains, beetroot and grain legumes | Arabinose, rhamnose, galactose sugars and galacturonic acids | [14] |
| Gums | Xanthan gum * Alginates ** Agar-agar ** Carrageenan ** | Pentose and hexoze monomers | [18] |
| Mucilages # | Aloe vera, Cactus, Okra, Hibiscus | Main glycoproteins | [16] |
| Inulin # and fructans | Jerusalem artichoke, Chicory root, onion and cereal grains | fructofuranosyl residues | [15] |
| Non-Digestible (resistant) oligosaccharides, MU = 3–9 | |||
| α-galactosides ** | Chickpea, bean, lentil, etc. | Raffinose, stachyose, verbascose | [15] |
| β-fructo-oligosaccharides ** | Polymers resulted from polysaccharides hydrolysis (inulin and lactose hydrolysis produce FOS and, respectively, GOS). | β-Fructo- (FOS), α-galacto- (GOS), β-galacto- (TOS), xylo- (XOS), arabino-xylo- (AXOS) oligosaccharides | [15] |
| Resistant dextrins ** | cereal-based vegetable milk, baked goods, dairy products and granola bars | Poly-D-glucose | [15] |
| Polydextrose ** | Cakes, candies, mixes and frozen desserts and beverages | Poly-D-glucose | [15] |
| Resistant Starches * (RS), MU ≥ 10 | |||
| RS type 1 | Grains and legumes (whole or partially milled) | physically inaccessible starch | [15] |
| RS type 2 | High-amylose starches, green bananas | granular starches | [15] |
| RS type 3 | Cooled starches in cooked starchy foods and enzyme-debranched starches | gelatinized and retrograded starches | [19] |
| RS type 4 | chemically modified (mainly cross-linked starches) | [15] | |
| Associated Substances Non-carbohydrates | |||
| Lignin * | Fruits, particularly strawberries and peaches | Coumaryl, coniferyl and sinapyl alcohols (aromatic alcohols) | [17] |
| Waxes * | Wax is present in rice bran, seed and seed hulls of sunflower | Long alkyl chains | [20] |
| Chitins * | Fungus’ cell walls, lobster, crab and shrimp exoskeletons and insects | N-acetylglucosamine | [15] |
| Phytates/Phytic acid # | Plant seeds, mainly in legumes, peanuts, cereals and oilseeds and generally found in almost all plant-based foods | - | [21] |
* Insoluble, ** Slightly soluble, # Soluble; and MU = monomeric units.
There are two forms of dietary fiber based on their capacity to dissolve in water: soluble fibers (those that, in the presence of water, form colloidal solutions in the intestine, slow down digestion and absorption of nutrients, which provides a prolonged feeling of satiety and a decrease in appetite, such as and a reduction in food glycemic index) and insoluble fibers (those that pass primarily intact through the digestive system, accelerating intestinal transit and playing an important role in the body’s detoxification process). Soluble fibers includes gums, pectins, beta-glucans and oligosaccharides [22]. The richest sources of soluble dietary fibers are apples, pears, citrus fruits, carrots, broccoli, peas, cucumbers, celery and oat bran [23].
Insoluble dietary fibers include lignin, cellulose, hemicellulose, chitin, resistant starch and resistant dextrin [24,25], which have a laxative effect, are recommended by specialists to people suffering from constipation. Nuts, beans, whole wheat, barley and roots are the best sources of insoluble dietary fiber [26]. Soluble and insoluble dietary fibers are found in varying amounts in plant-based foods. The foods richest in fiber are cereal bran (wheat and oats), whole grains, legumes (lentils, beans) and dried fruits (plums, apricots).
Due to the high water concentration, fresh fruits and vegetables provide relatively little fiber when this amount is related to fresh weight. On the other hand, these foods are relatively high in fiber when the amount of fiber per 100 kcal is reported [27]. Thus, cereals provide on average 36% to 65% of the daily fiber intake in industrialized countries, fruits 6% to 24%, leguminous 22% to 47% and green vegetables 2% to 8% [28,29].
This review is structured into nine paragraphs and describes the main influences of fiber from food on the human body, including its impact on metabolic diseases, digestive system, neurologic, cardiovascular, autoimmune diseases, cancer prevention and dietary fiber restrictions. The cited literature was selected using MEDLINE, Embase, Web of Science Core Collection and Google Scholar databases. The search terms included obesity and high fiber consumption, dietary fiber and metabolic diseases, fiber metabolism and health benefits, autoimmune disease and dietary fiber intake, evaluation of high-fiber diet and modern dietary practices, daily fiber intake and chronic disease.
NDF are represented by carbohydrates that are mainly part of the cell walls of plants ( Figure 1 ), natural compounds that are not completely digested by the human intestine, in the category of gums, pectins, mucilages, cellulose, hemicellulose, lignin, etc.
Fiber localization in plants. Created with BioRender.com.
NDF are the fraction of carbohydrates that remains undigested in the upper digestive tract. The bacteria metabolized the soluble, fermentable dietary fiber in the ileum and the ascending colon and the insoluble and high viscosity fiber are partially fermented in the distal colon, where the density of the microbiome is higher and the motility is lower. NDF degradation involves many microorganisms organized in the food chain. At the top of this food chain are fibrolytic bacteria. They degrade complex polysaccharides into oligosides and then into monosaccharides.
At a lower level of this chain are the glycolytic bacteria that ferment the available ozone. Intermediate products (lactate, formate, succinate, etc.) and/or final fermentation products are generated, short-chain fatty acids or SCFAs (acetate, propionate and butyrate), as well as gases (hydrogen and carbon dioxide). The acetate formed is absorbed and metabolized in peripheral tissues, where it is used as a precursor in cholesterol and fatty acid production. Propionate is a precursor to gluconeogenesis and is absorbed and processed in the liver. As a result, liponeogenesis and cholesterol production is also inhibited [30].
Therefore, propionate is proposed as a potential metabolite for preventing obesity and diabetes. Butyrate is metabolized by cells in the colon, and thus butyrate is a primary energy substrate for colonocytes and enterocytes, promoting the development of strains of Bifidobacterium sp., important probiotics for homeostasis of the human body ( Figure 2 ). SCFAs also stimulates intestinal motility, transit and activates the production of satiety hormones [31,32,33].
Fiber fermentation and its utilization pathways. Created with BioRender.com.
The interaction of NDF with the intestinal microbiome depends on their physicochemical properties. Thus, the insoluble dietary fibers are very slightly fermented but stimulate the intestinal transit and reduce the fermentation time of the intestinal contents in the colon. Furthermore, the mechanism of action of insoluble dietary fiber is physical because it increases the stool bowl by increasing the degree of hydration and its volume (since insoluble dietary fibers are organized in the form of a matrix in which water accumulates) and intestinal emptying time decreases [34,35].
Psyllium seeds contain soluble fiber but with high viscosity, which ferments little. They have a high capacity for water absorption and gelling, forming a viscous gel in the intestinal lumen, thus, preventing the absorption of cholesterol, glucose and the reabsorption of bile salts. They have the effect of stabilizing serum cholesterol level by inhibiting its intestinal absorption and by stabilizing the secretion of insulin, which promotes hepatic cholesterol synthesis. Increased intestinal volume fosters a feeling of satiety and reduced appetite [36].
Through intestinal fermentation, soluble dietary fibers with a reduced degree of viscosity (pectins and fructo-oligosaccharides) promote the production of SCFAs, including acetic, propionic and butyric, as well as carboxylic acids, such as lactic acid [37,38]. SCFAs have been found to operate as signaling molecules by binding to the FFA2, FFA3, GPR109a and Olfr78 membrane receptors in the intestine [39,40].
FFAR2 regulates the energy homeostasis of the whole body by modulating lipid differentiation and lipid storage in adipocytes and by regulating the production of leptin. This intestinal hormone inhibits the sensation of hunger in the CNS. SCFA-activated FFAR2 mediates the activation of the intestinal immune and anti-inflammatory response by producing cytokines and chemokines [41,42].
There are clinical studies in laboratory rats that showed that animals fed a high-fiber diet had a lower increase in body mass compared to those fed a standard diet high in carbohydrates (starch) and that animals with a supplemented diet with propionate and butyrate showed a better glucose tolerance compared to those fed a standard diet. Similarly, insulin tolerance was significantly improved in animals on a fiber-supplemented diet or in butyrate and propionate [43,44].
The gastrointestinal tract microbiota in humans is composed of bacteria, fungi, archaea, protozoans and viruses. More than 90% of the 12 different phyla are Proteobacteria, Firmicutes, Actinobacteria and Bacteroidetes, while the main “enterotypes” are from genus Bacteroides, Ruminococcus and Prevotella [45]. Dysbiosis, or imbalances in the microbiota’s composition, hae been linked to digestive (Crohn’s disease, irritable bowel syndrome, etc.), metabolic (obesity, diabetes, etc.) and other disorders (allergies, autism, etc.) [46,47].
Although these disorders are likely complex, the current research increasingly views the microbiome as a component that should not be overlooked when preventing or curing some of these diseases. Current research strategies focus on, among other things, the use of probiotics and/or prebiotics. The microbiota degrades the dietary fiber, releasing a sequence of antioxidant and/or anti-inflammatory chemicals bioavailable to the host. Thus, the colonic microbiota’s breakdown of NDF has a role in avoiding a variety of illnesses, including digestive (colorectal cancer, colitis and infections) and metabolic disorders (diabetes, cardiovascular diseases and obesity) [48], whether it is the strengthening of the immune system affected by various factors, including drugs [49,50].
Dietary fiber consumption has decreased, while sugar and animal protein consumption has increased, and microbial diversity in the human gut microbiome has decreased. These events can affect the microbiome’s function and the creation of SCFAs, leading to the development of chronic inflammatory illnesses [51].
Prebiotics are dietary fibers that specifically encourage the development and/or activity of gut bacteria that may be linked to the health and well-being of the host. They reduce the prevalence and duration of infectious or antibiotic-associated diarrhea, reduce symptoms associated with inflammatory diseases of the digestive tract, exert a protective effect against colorectal cancer, reduce the risk of cardiovascular disease, increase satiety, weight loss and thus prevent obesity, promote mineral bioavailability (calcium, magnesium and iron) and reduce allergies [48].
Short-chain carbohydrates work as prebiotics, promoting the growth of beneficial bacteria in the intestine. For example, inulin is a water-soluble fructose polymer with a polymerization degree of 2 to 60. Inulin undergoes fermentative oxidation in the small intestine’s terminal segment and the colon, resulting in the creation of SCFAs. As a result, they stimulate the growth of Bifidobacterium strains, which are vital probiotics for maintaining human body homeostasis [52].
Propionic acid is absorbed into the portal vein and reaches the liver, where it is metabolized by gluconeogenesis. It also activates FFAR2 receptors, with a role in stimulating the immune system. In addition, some studies confirmed the inhibition of hepatic cholesterol synthesis in the presence of propionate [53].
Colonocytes use butyric acid as an energy substrate. Butyric acid is involved in modulating the growth of intestinal epithelial cells, with benefits in the prevention and treatment of colon cancers. The species of butyrogenic bacteria are Faecalibacterium prausnitzii and Eubacterium rectale. Butyric acid is an energy source for digestive tract cells. This was evidenced by the comparative measurement of ATP produced by simple colonocytes and colonocytes populated with bacteria specific to the gut microbiome. Unpopulated murine intestinal cells with bacteria had a NADH/NAD + ratio that was 16 times lower than homonymous cells populated with intestinal bacteria. The resulting ATP level was also 56% lower [54].
Butyrate promotes epithelial growth in the colon but, paradoxically, has an inhibitory effect on colorectal cancers. This phenomenon is explained by the characteristic Warburg effect of cancer cells. Non-cancerous colonocytes use oxygen to produce energy (aerobic glycolysis), while cancerous colonocytes produce energy by anaerobic glycolysis, even if oxygen is available. The use of pyruvate and butyrate as an energy substrate also decreases in the affected cells. Butyric acid accumulates in the cytoplasm and acts as an HDAC (histone deacetylases) inhibitor, which reduces the underlying mechanisms of cellular apoptosis [55].
Soluble dietary fibers play an important role in balancing the gut microbiome (through the proliferation of intestinal bacteria of the species belonging to the genera Eubacterium, Bifidobacterium and Lactobacillus), which is why it is recommended in both the treatment of constipation and the treatment of diarrhea. Studies on the intestinal microbiome are numerous, with the little data currently available. However, the role of the microorganisms in achieving optimal digestion in the synthesis of vitamin K and the absorption of certain minerals or even medicinal substances (digoxin) is known. In addition, some studies relate the gut microbiome to the immune system functions (FFAR2 activation of SCFAs) and to the central nervous system health (the relationship between intestinal microbiome and depression, as a result of serotonergic depletion, was described) [56].
According to clinical investigations in rats, intestinal colonization varies depending on the kind of fiber ingested. For example, laboratory mice fed on diets containing 5–10% cellulose showed a significantly different bacterial community than mice fed a diet with 10% fructo-oligosaccharide (FOS) or inulin [31,57]. Cross-feeding is a fascinating phenomenon that occurs in the gut in the dietary fiber presence: the breakdown of products from one bacterial species’ fermentation of a complex carbohydrate become a substrate for the activity of another bacterial species. Bifidobacteria and Lactobacillus, for example, utilize fructans as a source of energy. Lactic acid and propionic acid are produced during the fermentation of fructans. Eubacterium, Roseburia and Faecalibacterium use it as an energy source when converting lactate and propionate to butyric acid [31].
Soluble dietary fibers also have a physical mechanism of action with an important role in modulating the absorption of certain macro and micronutrients. For example, due to their high molecular weight and water solubility, they increase the viscosity of the intestinal contents, preventing the absorption of cholesterol and glucose and the reabsorption of bile salts. This stabilizes serum cholesterol levels, by inhibiting intestinal absorption and stabilizing insulin secretion, which promotes hepatic cholesterol synthesis. In addition, increasing the intestinal volume promotes the feeling of satiety and reduces appetite [30].
Whole grains, vegetables and fruits high in fiber are considered the richest foods in prebiotic components. In addition, prebiotics can stimulate increased gastrointestinal balance and the growth and metabolism of healthy bacteria in the intestinal tract. Probiotics and prebiotics play an important role in forming of the gut microbiome by affecting immune system development, decreasing inflammation and oxidative stress and creating a balanced immune response that protects against pathogen colonization. In addition, a well-balanced diet promotes the growth of a healthy gut microbiome capable of producing SCFAs, which act as signaling molecules that influence the immune system’s proper functioning and promote cell apoptosis by inhibiting cancer cell development and proliferation [58].
Honey is also a potential source of prebiotic components as well as other bee products (bee-pollen [59], bee-bread [60], propolis [61], etc.). Honey oligosaccharides have a potential prebiotic activity by stimulating the growth of beneficial microorganisms (Lactobacillus sp. and Bifidobacterium sp.): also, most of the antioxidant compounds in honey stimulate their growth. Due to its complex composition, honey may contain probiotic microorganisms and prebiotic components, and the osmotic constitution of honey may have a protective role for probiotic bacteria in the gastrointestinal tract. An 821-week study of malnourished children found that honey intake led to increased plasma levels of short-chain fats [62].
According to a 2019 study done in Brazil on several kinds of honey, the prebiotic impact enhances as the fructose level increases [63]. In a study comparing honey with prebiotics, such as inulin, galacto-oligosaccharide (GOS) and FOS, on Bifidobacterium cultures (Bifidobacterium breve, Bifidobacterium adolescentis, Bifidobacterium longum and Bifidobacterium infantis), it was discovered that lactic and acetic acids increased the production.
The prebiotic effect of honey is similar to that achieved by GOS, FOS and inulin by the proliferation of intestinal bacteria. Implicitly, the formation of acids, such as lactic and acetic, and the reduction of the intestinal pH can be explained by the significant concentration in honey (4–5%) of oligosaccharides [64]. In addition, reducing the intestinal pH inhibits the growth and development of Gram-negative pathogenic bacteria [58].
As with vegetable fiber, honey has a prebiotic effect ensuring good functioning of the digestive system ( Figure 3 ). In addition to colonizing and growing beneficial microorganisms, honey can modulate oxidative stress, stimulating cell apoptosis and reducing cell proliferation [65]. These effects occur through various mechanisms (activation of the mitochondrial pathway, stopping the cell cycle and increasing the permeability of mitochondria) [66].
