Prebiotic effects: metabolic and health benefits

Roberfroid, M., Gibson, G.R., Hoyles, L., McCartney A, L., Rastall, R., Rowland, I., Wolvers, D., Watzl, B., Szajewska, H., Stahl, B., Guarner, F., Respondek, F., Whelan, K., Coxam, V., Davicco M-J, Léotoing, L., Wittrant, Y., Delzenne, N.M., Cani, P.D., Neyrinck, A.M. and Meheust, A. 2010. Prebiotic effects: metabolic and health benefits. British Journal of Nutrition. 104 (Suppl 2), pp. S1-S63. doi:10.1017/S0007114510003363

TitlePrebiotic effects: metabolic and health benefits
AuthorsRoberfroid, M., Gibson, G.R., Hoyles, L., McCartney A, L., Rastall, R., Rowland, I., Wolvers, D., Watzl, B., Szajewska, H., Stahl, B., Guarner, F., Respondek, F., Whelan, K., Coxam, V., Davicco M-J, Léotoing, L., Wittrant, Y., Delzenne, N.M., Cani, P.D., Neyrinck, A.M. and Meheust, A.
Abstract

The different compartments of the gastrointestinal tract are inhabited by populations of micro-organisms. By far the most important predominant populations are in the colon where a true symbiosis with the host exists that is a key for well-being and health. For such a microbiota, 'normobiosis' characterises a composition of the gut 'ecosystem' in which micro-organisms with potential health benefits predominate in number over potentially harmful ones, in contrast to 'dysbiosis', in which one or a few potentially harmful micro-organisms are dominant, thus creating a disease-prone situation. The present document has been written by a group of both academic and industry experts (in the ILSI Europe Prebiotic Expert Group and Prebiotic Task Force, respectively). It does not aim to propose a new definition of a prebiotic nor to identify which food products are classified as prebiotic but rather to validate and expand the original idea of the prebiotic concept (that can be translated in 'prebiotic effects'), defined as: 'The selective stimulation of growth and/or activity(ies) of one or a limited number of microbial genus(era)/species in the gut microbiota that confer(s) health benefits to the host.' Thanks to the methodological and fundamental research of microbiologists, immense progress has very recently been made in our understanding of the gut microbiota. A large number of human intervention studies have been performed that have demonstrated that dietary consumption of certain food products can result in statistically significant changes in the composition of the gut microbiota in line with the prebiotic concept. Thus the prebiotic effect is now a well-established scientific fact. The more data are accumulating, the more it will be recognised that such changes in the microbiota's composition, especially increase in bifidobacteria, can be regarded as a marker of intestinal health. The review is divided in chapters that cover the major areas of nutrition research where a prebiotic effect has tentatively been investigated for potential health benefits. The prebiotic effect has been shown to associate with modulation of biomarkers and activity(ies) of the immune system. Confirming the studies in adults, it has been demonstrated that, in infant nutrition, the prebiotic effect includes a significant change of gut microbiota composition, especially an increase of faecal concentrations of bifidobacteria. This concomitantly improves stool quality (pH, SCFA, frequency and consistency), reduces the risk of gastroenteritis and infections, improves general well-being and reduces the incidence of allergic symptoms such as atopic eczema. Changes in the gut microbiota composition are classically considered as one of the many factors involved in the pathogenesis of either inflammatory bowel disease or irritable bowel syndrome. The use of particular food products with a prebiotic effect has thus been tested in clinical trials with the objective to improve the clinical activity and well-being of patients with such disorders. Promising beneficial effects have been demonstrated in some preliminary studies, including changes in gut microbiota composition (especially increase in bifidobacteria concentration). Often associated with toxic load and/or miscellaneous risk factors, colon cancer is another pathology for which a possible role of gut microbiota composition has been hypothesised. Numerous experimental studies have reported reduction in incidence of tumours and cancers after feeding specific food products with a prebiotic effect. Some of these studies (including one human trial) have also reported that, in such conditions, gut microbiota composition was modified (especially due to increased concentration of bifidobacteria). Dietary intake of particular food products with a prebiotic effect has been shown, especially in adolescents, but also tentatively in postmenopausal women, to increase Ca absorption as well as bone Ca accretion and bone mineral density. Recent data, both from experimental models and from human studies, support the beneficial effects of particular food products with prebiotic properties on energy homaeostasis, satiety regulation and body weight gain. Together, with data in obese animals and patients, these studies support the hypothesis that gut microbiota composition (especially the number of bifidobacteria) may contribute to modulate metabolic processes associated with syndrome X, especially obesity and diabetes type 2. It is plausible, even though not exclusive, that these effects are linked to the microbiota-induced changes and it is feasible to conclude that their mechanisms fit into the prebiotic effect. However, the role of such changes in these health benefits remains to be definitively proven. As a result of the research activity that followed the publication of the prebiotic concept 15 years ago, it has become clear that products that cause a selective modification in the gut microbiota's composition and/or activity(ies) and thus strengthens normobiosis could either induce beneficial physiological effects in the colon and also in extra-intestinal compartments or contribute towards reducing the risk of dysbiosis and associated intestinal and systemic pathologies.

JournalBritish Journal of Nutrition
Journal citation104 (Suppl 2), pp. S1-S63
Year2010
Publisher's versionHoyles_et_al_2013.pdf
Digital Object Identifier (DOI)doi:10.1017/S0007114510003363

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Tuohy, K.M., Pinart-Gilberga, M., Jones, M., Hoyles, L., McCartney, A.L. and Gibson, G.R. 2007. Survivability of a probiotic Lactobacillus casei in the gastrointestinal tract of healthy human volunteers and its impact on the faecal microflora. Journal of Applied Microbiology. 102 (4), pp. 1026-1032. doi:10.1111/j.1365-2672.2006.03154.x

Diet, immunity and functional foods
Hoyles, L. and Vulevic, J. 2007. Diet, immunity and functional foods. Advances in Experimental Medicine and Biology. 635, pp. 79-92. doi:10.1007/978-0-387-09550-9_7

In vitro investigations of the effects of orlistat on the human faecal microbiota
Hoyles, L., Daggy, B.P., Gibson, G.R. and McCartney, A.L. 2006. In vitro investigations of the effects of orlistat on the human faecal microbiota. SGM Annual Meeting. University of Warwick, UK 03 Apr 2006

'List of Changes in Taxonomic Opinion': making use of the new lists
Euzéby, J.P., Hoyles, L., Kämpfer, P., Oren, A., Saddler, G.S., Trüper, H.G. and Tindall, B.J. 2004. 'List of Changes in Taxonomic Opinion': making use of the new lists. International Journal of Systematic and Evolutionary Microbiology. 54 (5), pp. 1429-1430. doi:10.1099/ijs.0.63375-0

Corynebacterium caspium sp. nov., from a Caspian seal (Phoca caspica)
Collins M, D., Hoyles, L., Foster, G. and Falsen, E. 2004. Corynebacterium caspium sp. nov., from a Caspian seal (Phoca caspica). International Journal of Systematic and Evolutionary Microbiology. 54 (3), pp. 925-928. doi:10.1099/ijs.0.02950-0

Jeotgalicoccus pinnipedialis sp. nov., from a southern elephant seal (Mirounga leonina)
Hoyles, L., Collins M, D., Foster, G., Falsen, E. and Schumann, P. 2004. Jeotgalicoccus pinnipedialis sp. nov., from a southern elephant seal (Mirounga leonina). International Journal of Systematic and Evolutionary Microbiology. 54 (3), pp. 745-748. doi:10.1099/ijs.0.02833-0

Transfer of members of the genus Falcivibrio to the genus Mobiluncus, and emended description of the genus Mobiluncus
Hoyles, L., Collins, M.D., Falsen, E., Nikolaitchouk, N. and McCartney, A.L. 2004. Transfer of members of the genus Falcivibrio to the genus Mobiluncus, and emended description of the genus Mobiluncus. Systematic and Applied Microbiology. 27 (1), pp. 72-83. doi:10.1078/0723-2020-00260

Practical Microbiology for Secondary Schools: A Resource for Key Stages 3, 4 and Post-16 and the Equivalent Scottish Qualifications
Fry, P., Grainger, J., Hurst, J., Hoyles, L. and Noble, S. Fry, P., Grainger, J. and Hurst, J. (ed.) 2002. Practical Microbiology for Secondary Schools: A Resource for Key Stages 3, 4 and Post-16 and the Equivalent Scottish Qualifications. Reading Society for General Microbiology.

Actinomyces coleocanis sp. nov., from the vagina of a dog
Hoyles, L., Falsen, E., Foster, G. and Collins M, D. 2002. Actinomyces coleocanis sp. nov., from the vagina of a dog. International Journal of Systematic and Evolutionary Microbiology. 52 (4), pp. 1201-1203. doi:10.1099/ijs.0.01934-0

Bifidobacterium scardovii sp. nov., from human sources
Hoyles, L., Inganas, E., Falsen, E., Drancourt, M., Weiss, N., McCartney, A.L. and Collins, M.D. 2002. Bifidobacterium scardovii sp. nov., from human sources. International Journal of Systematic and Evolutionary Microbiology. 52 (3), pp. 995-999. doi:10.1099/ijs.0.02065-0

Arcanobacterium hippocoleae sp. nov., from the vagina of a horse
Hoyles, L., Falsen, E., Foster, G., Rogerson, F. and Collins M, D. 2002. Arcanobacterium hippocoleae sp. nov., from the vagina of a horse. International Journal of Systematic and Evolutionary Microbiology. 52 (2), pp. 617-619. doi:10.1099/ijs.0.01950-0

Arthrobacter nasiphocae sp. nov., from the common seal (Phoca vitulina)
Collins M, D., Hoyles, L., Foster, G., Falsen, E. and Weiss, N. 2002. Arthrobacter nasiphocae sp. nov., from the common seal (Phoca vitulina). International Journal of Systematic and Evolutionary Microbiology. 52, pp. 569-571. doi:10.1099/ijs.0.01932-0

Characterization of some strains from human clinical sources which resemble "Leptotrichia sanguinegens": description of Sneathia sanguinegens sp. nov., gen. nov.
Collins M, D., Hoyles, L., Tornqvist, E., von Essen, R. and Falsen, E. 2001. Characterization of some strains from human clinical sources which resemble "Leptotrichia sanguinegens": description of Sneathia sanguinegens sp. nov., gen. nov. Systematic and Applied Microbiology. 24 (3), pp. 358-361. doi:10.1078/0723-2020-00047

Facklamia miroungae sp. nov., from a juvenile southern elephant seal (Mirounga leonina)
Hoyles, L., Foster, G., Falsen, E., Thomson L, F. and Collins M, D. 2001. Facklamia miroungae sp. nov., from a juvenile southern elephant seal (Mirounga leonina). International Journal of Systematic and Evolutionary Microbiology. 51 (4), pp. 1401-1403. doi:10.1099/00207713-51-4-1401

Corynebacterium testudinoris sp. nov., from a tortoise, and Corynebacterium felinum sp. nov., from a Scottish wild cat
Collins M, D., Hoyles, L., Hutson R, A., Foster, G. and Falsen, E. 2001. Corynebacterium testudinoris sp. nov., from a tortoise, and Corynebacterium felinum sp. nov., from a Scottish wild cat. International Journal of Systematic and Evolutionary Microbiology. 51 (4), pp. 1349-1352. doi:10.1099/00207713-51-4-1349

Actinomyces suimastitidis sp. nov., isolated from pig mastitis
Hoyles, L., Falsen, E., Holmstrom, G., Persson, A., Sjoden, B. and Collins, M.D. 2001. Actinomyces suimastitidis sp. nov., isolated from pig mastitis. International Journal of Systematic and Evolutionary Microbiology. 51 (4), pp. 1323-1326. doi:10.1099/00207713-51-4-1323

Corynebacterium capitovis sp. nov., from a sheep
Collins, M.D., Hoyles, L., Foster, G., Sjoden, B. and Falsen, E. 2001. Corynebacterium capitovis sp. nov., from a sheep. International Journal of Systematic and Evolutionary Microbiology. 51 (3), pp. 857-860. doi:10.1099/00207713-51-3-857

Streptococcus ovis sp. nov., isolated from sheep
Collins M, D., Hutson R, A., Hoyles, L., Falsen, E., Nikolaitchouk, N. and Foster, G. 2001. Streptococcus ovis sp. nov., isolated from sheep. International Journal of Systematic and Evolutionary Microbiology. 51 (3), pp. 1147-1150. doi:10.1099/00207713-51-3-1147

Actinomyces catuli sp. nov., from dogs
Hoyles, L., Falsen, E., Pascual, C., Sjoden, B., Foster, G., Henderson, D. and Collins, M.D. 2001. Actinomyces catuli sp. nov., from dogs. International Journal of Systematic and Evolutionary Microbiology. 51 (2), pp. 679-682. doi:10.1099/00207713-51-2-679

Arcanobacterium/Corynebacterium-like bacterial isolates from sheep
Foster, G., Ritchie, C., Cowie, R.A., Rusbridge, S.M., Collins, M.D. and Hoyles, L. 2001. Arcanobacterium/Corynebacterium-like bacterial isolates from sheep. Veterinary Record. 148 (9), p. 284.

Actinomyces marimammalium sp. nov., from marine mammals
Hoyles, L., Pascual, C., Falsen, E., Foster, G., Grainger, J.M. and Collins, M.D. 2001. Actinomyces marimammalium sp. nov., from marine mammals. International Journal of Systematic and Evolutionary Microbiology. 51 (1), pp. 151-156. doi:10.1099/00207713-51-1-151

Characterization of a Gemella-like organism isolated from an abscess of a rabbit: description of Gemella cunicula sp. nov.
Hoyles, L., Foster, G., Falsen, E. and Collins M, D. 2000. Characterization of a Gemella-like organism isolated from an abscess of a rabbit: description of Gemella cunicula sp. nov. International Journal of Systematic and Evolutionary Microbiology. 50 (6), pp. 2037-2041. doi:10.1099/00207713-50-6-2037

Characterization of Actinomyces isolates from infected root canals of teeth: description of Actinomyces radicidentis sp. nov.
Collins M, D., Hoyles, L., Kalfas, S., Sundquist, G., Monsen, T., Nikolaitchouk, N. and Falsen, E. 2000. Characterization of Actinomyces isolates from infected root canals of teeth: description of Actinomyces radicidentis sp. nov. Journal of Clinical Microbiology. 38 (9), pp. 3399-3403.

Characterization of Actinomyces isolates from samples from the human urogenital tract: description of Actinomyces urogenitalis sp. nov.
Nikolaitchouk, N., Hoyles, L., Falsen, E., Grainger J, M. and Collins M, D. 2000. Characterization of Actinomyces isolates from samples from the human urogenital tract: description of Actinomyces urogenitalis sp. nov. International Journal of Systematic and Evolutionary Microbiology. 50 (4), pp. 1649-1654. doi:10.1099/00207713-50-4-1649

Actinomyces canis sp. nov., isolated from dogs
Hoyles, L., Falsen, E., Foster, G., Pascual, C., Greko, C. and Collins, M.D. 2000. Actinomyces canis sp. nov., isolated from dogs. International Journal of Systematic and Evolutionary Microbiology. 50 (4), pp. 1547-1551. doi:10.1099/00207713-50-4-1547

Vagococcus fessus sp. nov., isolated from a seal and a harbour porpoise
Hoyles, L., Lawson P, A., Foster, G., Falsen, E., Ohlen, M., Grainger J, M. and Collins M, D. 2000. Vagococcus fessus sp. nov., isolated from a seal and a harbour porpoise. International Journal of Systematic and Evolutionary Microbiology. 50 (3), pp. 1151-1154. doi:10.1099/00207713-50-3-1151

Phenotypic and phylogenetic characterization of a new Corynebacterium species from dogs: description of Corynebacterium auriscanis sp. nov.
Collins M, D., Hoyles, L., Lawson P, A., Falsen, E., Robson R, L. and Foster, G. 1999. Phenotypic and phylogenetic characterization of a new Corynebacterium species from dogs: description of Corynebacterium auriscanis sp. nov. Journal of Clinical Microbiology. 37 (11), pp. 3443-3447.

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