Prebiotic (nutrition)

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Prebiotics are compounds in food that foster growth or activity of beneficial microorganisms such as bacteria and fungi. [1] The most common environment concerning their effects on human health is the gastrointestinal tract, where prebiotics can alter the composition of organisms in the gut microbiome.

Contents

Dietary prebiotics are typically nondigestible fiber compounds that pass undigested through the upper part of the gastrointestinal tract and help growth or activity of advantageous bacteria in the colon by acting as substrates for them. [1] They were first identified and named by Marcel Roberfroid in 1995. [1] [2] Depending on the jurisdiction, they may have regulatory scrutiny as food additives for the health claims made for marketing purposes. Common prebiotics used in food manufacturing include beta-glucan from oats, resistant starch from grains and beans, and inulin from chicory root.

Definition

The definition of prebiotics and the food ingredients that can fall under this classification, has evolved since its first definition in 1995. [3] In its earliest definition, the term prebiotics was used to refer to non-digestible food ingredients that were beneficial to the host through their selective stimulation of specific bacteria within the colon. [3] [4] Further research has suggested that selective stimulation has not been scientifically demonstrated. [5] As a result of research suggesting that prebiotics could impact microorganisms outside of the colon, in 2016 the International Scientific Association for Probiotics and Prebiotics (ISAPP) produced the following definition of prebiotics: a substrate that is selectively used by a host microorganism to produce a health benefit. [3] In 2021, The Global Prebiotic Association (GPA) defined a prebiotic as a product or ingredient that is utilized in the microbiota producing a health or performance benefit. [6]

Compounds that can be classified as prebiotics must also meet the following criteria: [3] [4] [6]

Thus, consumption of prebiotics may facilitate the health of the host. [7] Based on the previous classifications, plant-derived carbohydrate compounds called oligosaccharides as well as resistant starch are the main source of prebiotics that have been identified. [8] [4] [9] [10] Specifically, fructans and galactans are two oligosaccharide sources which have been found to stimulate the activity and growth of beneficial bacterial colonies in the gut. [7] [3] Fructans are a category of carbohydrate consisting of fructooligosaccharides (FOS) and inulins, while galactans consist of galactooligosaccharides. [3] Resistant starch has been shown to shift the intestinal bacteria, as well as improve biomarkers for numerous health conditions. [11] [12] [13] Other dietary fibers also fit the definition of prebiotics, such as pectin, [14] beta-glucans, [15] and xylooligosaccharides. [16]

The European Food Safety Authority (EFSA), the regulatory agency for product labeling, differentiates between "prebiotic" and "dietary fiber", stating that "a cause and effect relationship has not been established between the consumption of the food constituents which are the subject of the health claims and a beneficial physiological effect related to increasing numbers of gastrointestinal microbiota". [17] Consequently, under EFSA rules individual ingredients cannot be labeled as prebiotics, but only as dietary fiber and with no implication of health benefits. [17]

Function

When the prebiotic concept was first introduced in 1995, the primary focus was on the effects that prebiotics confer on Bifidobacteria and Lactobacillus. [3] [4] [18] With improved mechanistic techniques in recent years, the current prebiotic targets have expanded to a wider range of microbes, including Roseburia spp., Eubacterium spp., Akkermansia spp., Christensenella spp., Propionibacterium spp. and Faecalibacterium spp. [19] These bacteria have been highlighted as key probiotics and beneficial gut bacteria as they may have several beneficial effects on the host in terms of improving digestion (including but not limited to enhancing mineral absorption) [20] and the effectiveness and intrinsic strength of the immune system. [21] Both Bifidobacteria and Lactobacillus have been shown to have differing prebiotic specificity and to selectively ferment prebiotic fiber based on the enzymes characteristic of the bacterial population. [22] Thus, Lactobacilli prefer inulin and fructooligosaccharides, while Bifidobacteria display specificity for inulin, fructooligosaccharides, xylooligosaccharides and galactooligosaccharides. [22] Studies have also shown that prebiotics, besides helping growth of beneficial gut bacteria, can also inhibit detrimental and potentially pathogenic microbes in the gut, [9] [4] such as clostridia. [4]

Mechanism of action

Fermentation is the main mechanism of action by which prebiotics are used by beneficial bacteria in the colon. [7] [4] Both Bifidobacteria and Lactobacillus are bacterial populations which use saccharolytic metabolism to break down substrates. [4] The bifidobacterial genome contains many genes that encode for carbohydrate-modifying enzymes as well as genes that encode for carbohydrate uptake proteins. The presence of these genes indicates that Bifidobacteria contain specific metabolic pathways specialized for the fermentation and metabolism of plant-derived oligosaccharides, or prebiotics. These pathways in Bifidobacteria ultimately produce short chain fatty acids, [4] [7] which have diverse physiological roles in body functions. [23] [3]

Sources

Prebiotic sources must be proven to confer a benefit to the host in order to be classified as a prebiotic. [3] Fermentable carbohydrates derived from fructans and xylans are one well documented example of prebiotics. [3] Resistant starch from starchy foods are also well documented prebiotics and have historically been the highest source of prebiotics in the diet, as 4-10% of starch in mixed diets has been shown to reach the large intestine. [24] One study reported that individuals consuming a traditional diet in Africa consumed 38 grams of resistant starch/day. [25]

Endogenous

An endogenous source of prebiotics in humans is human breast milk, which contains oligosaccharides structurally similar to galactooligosaccharides, referred to as human milk oligosaccharides. [26] [9] [22] [3] Human milk oligosaccharides were found to increase the Bifidobacteria bacterial population in breastfed infants, and to strengthen the infant immune system. [3] [9] Furthermore, human milk oligosaccharides help establish a healthy intestinal microbiota composition in newborns. [3]

Exogenous

Indigestible carbohydrate compounds classified as prebiotics are a type of fermentable fiber, and thus can be classified as dietary fiber. [4] However, not all dietary fiber can be classified as a prebiotic source. [4] In addition to the food sources highlighted in the following table, raw oats, [18] unrefined barley, [18] yacón, [18] and whole grain breakfast cereals [4] are also classified as prebiotic fiber sources. The predominant type of prebiotic fiber may vary according to the food. For instance, oats and barley have high amounts of beta-glucans, fruit and berries contain pectins, seeds contain gums, onions and Jerusalem artichokes are rich in inulin and oligofructose, and bananas and legumes contain resistant starch. [27]

Top 10 Foods Containing Prebiotics [28]
FoodPrebiotic Fiber by Weight
Raw, Dry Chicory Root 64.6%
Raw, Dry Jerusalem Artichoke 31.5%
Raw, Dry Dandelion Greens24.3%
Raw, Dry Garlic 17.5%
Raw, Dry Leek 11.7%
Raw, Dry Onion 8.6%
Raw Asparagus 5%
Raw Wheat bran 5%
Whole Wheat flour, Cooked4.8%
Raw Banana 1%

While there is no broad consensus on an ideal daily serving of prebiotics, recommendations typically range from 4 to 8 grams (0.14–0.28 oz) for general digestive health support, to 15 grams (0.53 oz) or more for those with active digestive disorders. Given an average 6 grams (0.21 oz) serving, below are the amounts of prebiotic foods required to achieve a daily serving of prebiotic fiber:

Amount of food needed for 6 g of fructan [28]
FoodAmount
Raw Chicory Root9.3 g (0.33 oz)
Raw Jerusalem Artichoke19 g (0.67 oz)
Raw Dandelion Greens24.7 g (0.87 oz)
Raw Garlic34.3 g (1.21 oz)
Raw Leek51.3 g (1.81 oz)
Raw Onion69.8 g (2.46 oz)
Cooked Onion120 g (4.2 oz)
Raw Asparagus120 g (4.2 oz)
Raw Wheat Bran120 g (4.2 oz)
Whole Wheat Flour, Cooked125 g (4.4 oz)
Raw Banana600 g (1.3 lb)

Research

Preliminary research has demonstrated potential effects on calcium and other mineral absorption, [29] immune system effectiveness, [30] [31] bowel acidity, reduction of colorectal cancer risk, [32] inflammatory bowel disease (Crohn's disease or ulcerative colitis), [33] hypertension [34] and defecation frequency. [35] Prebiotics may be effective in decreasing the number of infectious episodes needing antibiotics and the total number of infections in children aged 0–24 months. [31] [36]

No good evidence shows that prebiotics are effective in preventing or treating allergies. [37]

While research demonstrates that prebiotics lead to increased production of short-chain fatty acids (SCFA), [38] more research is required to establish a direct causal connection. Prebiotics may be beneficial to inflammatory bowel disease or Crohn's disease through production of SCFA as nourishment for colonic walls, and mitigation of ulcerative colitis symptoms. [39]

The sudden addition of substantial quantities of prebiotics to the diet may result in an increase in fermentation, leading to increased gas production, bloating or bowel movement. [40] Production of SCFA and fermentation quality are reduced during long-term diets of low fiber intake. [41] Until bacterial flora are gradually established to rehabilitate or restore intestinal bacteria, nutrient absorption may be impaired and colonic transit time temporarily increased with a rapid addition of higher prebiotic intake. [40] [42]

Genetic modification

Genetically modified plants have been created in research labs with upregulated inulin production. [43] [44]

See also

Related Research Articles

<span class="mw-page-title-main">Dietary fiber</span> Portion of plant-derived food that cannot be completely digested

Dietary fiber or roughage is the portion of plant-derived food that cannot be completely broken down by human digestive enzymes. Dietary fibers are diverse in chemical composition and can be grouped generally by their solubility, viscosity and fermentability which affect how fibers are processed in the body. Dietary fiber has two main subtypes: soluble fiber and insoluble fiber which are components of plant-based foods such as legumes, whole grains, cereals, vegetables, fruits, and nuts or seeds. A diet high in regular fiber consumption is generally associated with supporting health and lowering the risk of several diseases. Dietary fiber consists of non-starch polysaccharides and other plant components such as cellulose, resistant starch, resistant dextrins, inulins, lignins, chitins, pectins, beta-glucans, and oligosaccharides.

<span class="mw-page-title-main">Inulin</span> Natural plant polysaccharides

Inulins are a group of naturally occurring polysaccharides produced by many types of plants, industrially most often extracted from chicory. The inulins belong to a class of dietary fibers known as fructans. Inulin is used by some plants as a means of storing energy and is typically found in roots or rhizomes. Most plants that synthesize and store inulin do not store other forms of carbohydrate such as starch. In 2018, the United States Food and Drug Administration approved inulin as a dietary fiber ingredient used to improve the nutritional value of manufactured food products. Using inulin to measure kidney function is the "gold standard" for comparison with other means of estimating glomerular filtration rate.

<span class="mw-page-title-main">Oligosaccharide</span> Saccharide polymer

An oligosaccharide is a saccharide polymer containing a small number of monosaccharides. Oligosaccharides can have many functions including cell recognition and cell adhesion.

<span class="mw-page-title-main">Fructose malabsorption</span> Medical condition

Fructose malabsorption, formerly named dietary fructose intolerance (DFI), is a digestive disorder in which absorption of fructose is impaired by deficient fructose carriers in the small intestine's enterocytes. This results in an increased concentration of fructose. Intolerance to fructose was first identified and reported in 1956.

<span class="mw-page-title-main">Fructooligosaccharide</span> Oligosaccharide fructans

Fructooligosaccharides (FOS) also sometimes called oligofructose or oligofructan, are oligosaccharide fructans, used as an alternative sweetener. FOS exhibits sweetness levels between 30 and 50 percent of sugar in commercially prepared syrups. It occurs naturally, and its commercial use emerged in the 1980s in response to demand for healthier and calorie-reduced foods.

<span class="mw-page-title-main">Resistant starch</span> Dietary fiber

Resistant starch (RS) is starch, including its degradation products, that escapes from digestion in the small intestine of healthy individuals. Resistant starch occurs naturally in foods, but it can also be added as part of dried raw foods, or used as an additive in manufactured foods.

<span class="mw-page-title-main">Fructan</span> Fructose polymer

A fructan is a polymer of fructose molecules. Fructans with a short chain length are known as fructooligosaccharides. Fructans can be found in over 12% of the angiosperms including both monocots and dicots such as agave, artichokes, asparagus, leeks, garlic, onions, yacón, jícama, barley and wheat.

Natural growth promoters (NGPs) are feed additives for farm animals.

Synbiotics refer to food ingredients or dietary supplements combining probiotics and prebiotics in a form of synergism, hence synbiotics. The synbiotic concept was first introduced as "mixtures of probiotics and prebiotics that beneficially affect the host by improving the survival and implantation of live microbial dietary supplements in the gastrointestinal tract, by selectively stimulating the growth and/or by activating the metabolism of one or a limited number of health-promoting bacteria, thus improving host welfare". As of 2018, the research on this concept is preliminary, with no high-quality evidence from clinical research that such benefits exist.

<span class="mw-page-title-main">Galactooligosaccharide</span> Class of prebiotics

Galactooligosaccharides (GOS), also known as oligogalactosyllactose, oligogalactose, oligolactose or transgalactooligosaccharides (TOS), belong to the group of prebiotics. Prebiotics are defined as non-digestible food ingredients that beneficially affect the host by stimulating the growth and/or activity of beneficial bacteria in the colon. GOS occurs in commercially available products such as food for both infants and adults.

<i>Bifidobacterium</i> Genus of bacteria

Bifidobacterium is a genus of gram-positive, nonmotile, often branched anaerobic bacteria. They are ubiquitous inhabitants of the gastrointestinal tract though strains have been isolated from the vagina and mouth of mammals, including humans. Bifidobacteria are one of the major genera of bacteria that make up the gastrointestinal tract microbiota in mammals. Some bifidobacteria are used as probiotics.

FODMAPs or fermentable oligosaccharides, disaccharides, monosaccharides, and polyols are short-chain carbohydrates that are poorly absorbed in the small intestine and ferment in the colon. They include short-chain oligosaccharide polymers of fructose (fructans) and galactooligosaccharides, disaccharides (lactose), monosaccharides (fructose), and sugar alcohols (polyols), such as sorbitol, mannitol, xylitol, and maltitol. Most FODMAPs are naturally present in food and the human diet, but the polyols may be added artificially in commercially prepared foods and beverages.

<span class="mw-page-title-main">Xylooligosaccharide</span> Polymer of the sugar xylose

Xylooligosaccharides (XOS) are polymers of the sugar xylose. They are produced from the xylan fraction in plant fiber. Their C5 structure is fundamentally different from other prebiotics, which are based upon C6 sugars. Xylooligosaccharides have been commercially available since the 1980s, originally produced by Suntory in Japan. They have more recently become more widely available commercially, as technologies have advanced and production costs have fallen. Some enzymes from yeast can exclusively convert xylan into only xylooligosaccharides-DP-3 to 7.

Isomaltooligosaccharide (IMO) is a mixture of short-chain carbohydrates which has a digestion-resistant property. IMO is found naturally in some foods, as well as being manufactured commercially. The raw material used for manufacturing IMO is starch, which is enzymatically converted into a mixture of isomaltooligosaccharides.

Microbiota-accessible carbohydrates (MACs) are carbohydrates that are resistant to digestion by a host's metabolism, and are made available for gut microbes, as prebiotics, to ferment or metabolize into beneficial compounds, such as short chain fatty acids. The term, ‘‘microbiota-accessible carbohydrate’’ contributes to a conceptual framework for investigating and discussing the amount of metabolic activity that a specific food or carbohydrate can contribute to a host's microbiota.

Bifidobacterium breve is a bacterial species of the genus Bifidobacterium which has probiotic properties. Bifidobacteria are a type of bacteria that live symbiotically in the intestines of humans. They have been used to treat a number of conditions including constipation, diarrhea, irritable bowel syndrome and even the cold and flu. Some of these uses have been backed up by scientific research, but others have not. B. breve is a gram positive, anaerobic, rod shaped organism that is non motile and forms branches with its neighbors.

Psychobiotics is a term used in preliminary research to refer to live bacteria that, when ingested in appropriate amounts, might confer a mental health benefit by affecting microbiota of the host organism. Whether bacteria might play a role in the gut-brain axis is under research. A 2020 literature review suggests that the consumption of psychobiotics could be considered as a viable option to restore mental health although lacking randomized controlled trials on clear mental health outcomes in humans.

<span class="mw-page-title-main">Human milk microbiome</span> Community of microorganisms in human milk

The human milk microbiota, also known as human milk probiotics (HMP), encompasses the microbiota–the community of microorganisms–present within the human mammary glands and breast milk. Contrary to the traditional belief that human breast milk is sterile, advancements in both microbial culture and culture-independent methods have confirmed that human milk harbors diverse communities of bacteria. These communities are distinct in composition from other microbial populations found within the human body which constitute the human microbiome.

<span class="mw-page-title-main">Kestose</span> Sugar from fructooligosaccharide group

Kestose is a class of sugars that belongs to a group of fructooligosaccharides.

References

  1. 1 2 3 Hutkins RW; Krumbeck JA; Bindels LB; Cani PD; Fahey G Jr.; Goh YJ; Hamaker B; Martens EC; Mills DA; Rastal RA; Vaughan E; Sanders ME (2016). "Prebiotics: why definitions matter". Curr Opin Biotechnol. 37: 1–7. doi:10.1016/j.copbio.2015.09.001. PMC   4744122 . PMID   26431716.
  2. Gibson GR, Roberfroid MB (June 1995). "Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics". J. Nutr. 125 (6): 1401–12. doi:10.1093/jn/125.6.1401. PMID   7782892.
  3. 1 2 3 4 5 6 7 8 9 10 11 12 13 Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, et al. (August 2017). "Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics" (PDF). Nature Reviews. Gastroenterology & Hepatology. 14 (8): 491–502. doi:10.1038/nrgastro.2017.75. hdl:10468/4142. PMID   28611480. S2CID   11827223.
  4. 1 2 3 4 5 6 7 8 9 10 11 12 Slavin J (April 2013). "Fiber and prebiotics: mechanisms and health benefits". Nutrients. 5 (4): 1417–35. doi: 10.3390/nu5041417 . PMC   3705355 . PMID   23609775.
  5. Bindels, Laure B.; Delzenne, Nathalie M.; Cani, Patrice D.; Walter, Jens (2015). "Towards a more comprehensive concept for prebiotics". Nature Reviews Gastroenterology & Hepatology. 12 (5): 303–310. doi:10.1038/nrgastro.2015.47. PMID   25824997. S2CID   637779.
  6. 1 2 "Learn more about prebiotics". Global Prebiotic Association.
  7. 1 2 3 4 Lamsal BP (August 2012). "Production, health aspects and potential food uses of dairy prebiotic galactooligosaccharides". Journal of the Science of Food and Agriculture. 92 (10): 2020–28. Bibcode:2012JSFA...92.2020L. doi:10.1002/jsfa.5712. PMID   22538800.
  8. Zaman SA, Sarbini SR (7 July 2015). "The potential of resistant starch as a prebiotic" (PDF). Critical Reviews in Biotechnology. 36 (3): 578–84. doi:10.3109/07388551.2014.993590. PMID   25582732. S2CID   25974073.
  9. 1 2 3 4 CK Rajendran SR, Okolie CL, Udenigwe CC, Mason B (1 October 2017). "Structural features underlying prebiotic activity of conventional and potential prebiotic oligosaccharides in food and health". Journal of Food Biochemistry. 41 (5): e12389. doi: 10.1111/jfbc.12389 . ISSN   1745-4514.
  10. Bird, A.; Conlon, M.; Christophersen, C.; Topping, D. (2010). "Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics". Beneficial Microbes. 1 (4): 423–431. doi:10.3920/BM2010.0041. PMID   21831780.
  11. Portincasa, Piero; Bonfrate, Leonilde; Vacca, Mirco; de Angelis, Maria; Farella, Ilaria; Lanza, Elisa; Khalil, Mohamad; Wang, David Q-H; Sperandio, Markus; Di Ciaula, Agostino (2022). "Gut Microbiota and short chain fatty acids: implications in glucose homeostasis". Int J Mol Sci. 23 (3): 1105. doi: 10.3390/ijms23031105 . PMC   8835596 . PMID   35163038.
  12. Warman, Dwina Juliana; Jia, Huijuan; Kato, Hisanori (2022). "The potential roles of probiotics, resistant starch and resistant proteins in ameliorating inflammation during aging (Inflammaging)". Nutrients. 14 (4): 747. doi: 10.3390/nu14040747 . PMC   8879781 . PMID   35215397.
  13. Li, Cheng; Hu, Yiming (2022). "New definition of resistant starch types from the Gut Microbiota perspectives - a review". Critical Reviews in Food Science and Nutrition. 63 (23): 6412–6422. doi:10.1080/10408398.2022.2031101. PMID   35075962. S2CID   246277434.
  14. Gómez B, Gullón B, Remoroza C, Schols HA, Parajó JC, Alonso JL (October 2014). "Purification, characterization, and prebiotic properties of pectic oligosaccharides from orange peel wastes". Journal of Agricultural and Food Chemistry. 62 (40): 9769–82. doi:10.1021/jf503475b. PMID   25207862.
  15. Arena MP, Caggianiello G, Fiocco D, Russo P, Torelli M, Spano G, Capozzi V (February 2014). "Barley β-glucans-containing food enhances probiotic performances of beneficial bacteria". International Journal of Molecular Sciences. 15 (2): 3025–39. doi: 10.3390/ijms15023025 . PMC   3958897 . PMID   24562330.
  16. Linares-Pasten JA, Aronsson A, Karlsson EN (2017). "Structural Considerations on the Use of Endo-Xylanases for the Production of prebiotic Xylooligosaccharides from Biomass". Current Protein & Peptide Science. 19 (1): 48–67. doi:10.2174/1389203717666160923155209. PMC   5738707 . PMID   27670134.
  17. 1 2 Delcour JA, Aman P, Courtin CM, Hamaker BR, Verbeke K (January 2016). "Prebiotics, Fermentable Dietary Fiber, and Health Claims". Advances in Nutrition. 7 (1): 1–4. doi:10.3945/an.115.010546. PMC   4717894 . PMID   26773010.
  18. 1 2 3 4 Pandey KR, Naik SR, Vakil BV (December 2015). "Probiotics, prebiotics and synbiotics- a review". Journal of Food Science and Technology. 52 (12): 7577–87. doi:10.1007/s13197-015-1921-1. PMC   4648921 . PMID   26604335.
  19. Cunningham, Marla; Azcarate-Peril, M. Andrea; Barnard, Alan; Benoit, Valerie; Grimaldi, Roberta; Guyonnet, Denis; Holscher, Hannah D.; Hunter, Kirsty; Manarung, Sarmauli; Obis, David; Petrova, Mariya I.; Steinert, Robert E.; Swanson, Kelly S.; van Sinderen, Douwe; Vulevic, Jelena; Gibson, Glenn R. (2021). "Shaping the future of probiotics and prebiotics". Trends in Microbiology. 29 (8): 667–685. doi: 10.1016/j.tim.2021.01.003 . PMID   33551269. S2CID   231864275.
  20. Coxam V (November 2007). "Current data with inulin-type fructans and calcium, targeting bone health in adults". The Journal of Nutrition. 137 (11 Suppl): 2527S–33S. doi: 10.1093/jn/137.11.2527S . PMID   17951497.
  21. Seifert S, Watzl B (November 2007). "Inulin and oligofructose: review of experimental data on immune modulation". The Journal of Nutrition. 137 (11 Suppl): 2563S–67S. doi: 10.1093/jn/137.11.2563S . PMID   17951503.
  22. 1 2 3 Wilson B, Whelan K (March 2017). "Prebiotic inulin-type fructans and galacto-oligosaccharides: definition, specificity, function, and application in gastrointestinal disorders". Journal of Gastroenterology and Hepatology. 32 (Suppl 1): 64–68. doi: 10.1111/jgh.13700 . PMID   28244671.
  23. Byrne CS, Chambers ES, Morrison DJ, Frost G (September 2015). "The role of short chain fatty acids in appetite regulation and energy homeostasis". International Journal of Obesity. 39 (9): 1331–38. doi:10.1038/ijo.2015.84. PMC   4564526 . PMID   25971927.
  24. Cassidy, A.; Bingham, S.A.; Cummings, J.H. (1994). "Starch intake and colorectal cancer risk: an international comparison". Br J Cancer. 69 (5): 937–942. doi:10.1038/bjc.1994.181. PMC   1968884 . PMID   8180027.
  25. O'Keefe, Stephen J.D.; et al. (2015). "Fat, fibre and cancer risk in African Americans and rural Africans". Nat Commun. 6: 6342. Bibcode:2015NatCo...6.6342O. doi:10.1038/ncomms7342. PMC   4415091 . PMID   25919227.
  26. Enam F, Mansell TJ (October 2019). "Prebiotics: tools to manipulate the gut microbiome and metabolome". Journal of Industrial Microbiology & Biotechnology. 46 (9–10): 1445–59. doi: 10.1007/s10295-019-02203-4 . PMID   31201649. S2CID   189819499.
  27. "Definitions of fiber". Micronutrient Information Center, Linus Pauling Institute, Oregon State University, Corvallis, OR. 1 April 2012. Retrieved 27 February 2019.
  28. 1 2 Moshfegh AJ, Friday JE, Goldman JP, Ahuja JK (July 1999). "Presence of inulin and oligofructose in the diets of Americans". Journal of Nutrition. 129 (7 Suppl): 1407S–11S. doi: 10.1093/jn/129.7.1407S . PMID   10395608.
  29. Scholz-Ahrens KE, Schrezenmeir J (November 2007). "Inulin and oligofructose and mineral metabolism: the evidence from animal trials". J. Nutr. 137 (11 Suppl): 2513S–23S. doi: 10.1093/jn/137.11.2513S . PMID   17951495.
  30. Lomax AR, Calder PC (March 2009). "Prebiotics, immune function, infection and inflammation: a review of the evidence". Br J Nutr. 101 (5): 633–58. doi: 10.1017/S0007114508055608 . PMID   18814803.
  31. 1 2 Lohner S, Küllenberg D, Antes G, Decsi T, Meerpohl JJ (2014). "Prebiotics in healthy infants and children for prevention of acute infectious diseases: a systematic review and meta-analysis". Nutr Rev. 72 (8): 523–31. doi: 10.1111/nure.12117 . PMID   24903007.
  32. Geier MS, Butler RN, Howarth GS (October 2006). "Probiotics, prebiotics and synbiotics: a role in chemoprevention for colorectal cancer?". Cancer Biol. Ther. 5 (10): 1265–69. doi:10.4161/cbt.5.10.3296. PMID   16969130.
  33. Hedin C, Whelan K, Lindsay JO (August 2007). "Evidence for the use of probiotics and prebiotics in inflammatory bowel disease: a review of clinical trials". Proceedings of the Nutrition Society. 66 (3): 307–15. doi: 10.1017/S0029665107005563 . PMID   17637082.
  34. Yeo SK, Ooi LG, Lim TJ, Liong MT (2009). "Antihypertensive properties of plant-based prebiotics". Int J Mol Sci. 10 (8): 3517–30. doi: 10.3390/ijms10083517 . PMC   2812835 . PMID   20111692.
  35. Roberfroid M, et al. (2010). "Prebiotic effects: metabolic and health benefits". Br J Nutr. 104 (Suppl 2): S1–63. doi: 10.1017/S0007114510003363 . PMID   20920376.
  36. Koen Venema, Ana Paula do Carmo, ed. (2015). Probiotics and prebiotics : current research and future trends. Norfolk, UK: Caister Academic Press. ISBN   978-1-910190-10-4. OCLC   916950998.
  37. Cuello-Garcia C, Fiocchi A, Pawankar R, Yepes-Nuñez JJ, Morgano GP, Zhang Y, Agarwal A, Gandhi S, Terracciano L, Schünemann HJ, Brozek JL (November 2017). "Prebiotics for the prevention of allergies: A systematic review and meta-analysis of randomized controlled trials". Clin. Exp. Allergy (Systematic review). 47 (11): 1468–77. doi:10.1111/cea.13042. PMID   29035013. S2CID   7314418.
  38. Macfarlane S, Macfarlane GT, Cummings JH (September 2006). "Review article: prebiotics in the gastrointestinal tract". Aliment Pharmacol Ther. 24 (5): 701–14. doi: 10.1111/j.1365-2036.2006.03042.x . PMID   16918875. S2CID   21956124.
  39. Guarner F (2005). "Inulin and oligofructose: impact on intestinal diseases and disorders". Br J Nutr. 93 (Suppl 1): S61–65. doi: 10.1079/BJN20041345 . PMID   15877897.
  40. 1 2 Marteau P, Seksik P (2004). "Tolerance of probiotics and prebiotics". J Clin Gastroenterol. 38 (Suppl 6): S67–69. doi:10.1097/01.mcg.0000128929.37156.a7. PMID   15220662.
  41. El Oufir L, Flourié B, Bruley des Varannes S, Barry JL, Cloarec D, Bornet F, Galmiche JP (June 1996). "Relations between transit time, fermentation products, and hydrogen consuming flora in healthy humans". Gut. 38 (6): 870–77. doi:10.1136/gut.38.6.870. PMC   1383195 . PMID   8984026.
  42. Givson GR, Willems A, Reading S, Collins MD (1996). "Fermentation of non-digestible oligosaccharides by human colonic bacteria". Proceedings of the Nutrition Society. 55 (3): 899–912. doi: 10.1079/PNS19960087 . PMID   9004332.
  43. Ritsema T, Smeekens SC (2003). "Engineering fructan metabolism in plants". J Plant Physiol. 160 (7): 811–20. doi:10.1078/0176-1617-01029. PMID   12940548.
  44. Weyens G, Ritsema T, Van Dun K, Meyer D, Lommel M, Lathouwers J, Rosquin I, Denys P, Tossens A, Nijs M, Turk S, Gerrits N, Bink S, Walraven B, Lefèbvre M, Smeekens S (2004). "Production of tailor-made fructans in sugar beet by expression of onion fructosyltransferase genes". Plant Biotechnol J. 2 (4): 321–27. doi:10.1111/j.1467-7652.2004.00074.x. hdl: 1874/11465 . PMID   17134393. S2CID   42177275.

Further reading