Modulation of Gut Microbiota in the Management of Metabolic Disorders: The Prospects and Challenges
Abstract
:1. Introduction
2. Role of Gut Microbiota in Metabolic Disorders
3. Modulation of Gut Microbiota in the Management of Metabolic Disorders: The Prospects
3.1. Modulation with Probiotics
3.2. Modulation with Prebiotics
3.3. Modulation with Antimicrobial Agents
3.4. Modulation with Surgery
3.5. Modulation with Weight Loss Strategies
4. Modulation of Gut Microbiota in the Management of Metabolic Disorders: The Challenges
5. Conclusions
Review Criteria
Conflicts of Interest
References
- Dhaliwal, S.S.; Welborn, T.A. Central obesity and cigarette smoking are key determinants of cardiovascular disease deaths in Australia: A public health perspective. Prev. Med. 2009, 49, 153–157. [Google Scholar]
- Matheus, A.S.; Tannus, L.R.; Cobas, R.A.; Palma, C.C.; Negrato, C.A.; de Gomes, M.B. Impact of diabetes on cardiovascular disease: An update. Int. J. Hypertens. 2013, 2013, 653789. [Google Scholar]
- Rao, H. Use of secondary prevention drugs for cardiovascular disease in the community in high-income middle-income and low-income countries (the PURE Study): A prospective epidemiological survey. Indian Heart J. 2012, 64, 113. [Google Scholar]
- McCarthy, M.I. Genomics type 2 diabetes and obesity. N. Engl. J. Med. 2010, 363, 2339–2350. [Google Scholar]
- Grenham, S.; Clarke, G.; Cryan, J.F.; Dinan, T.G. Brain-gut-microbe communication in health and disease. Front. Physiol. 2011, 2, 94. [Google Scholar]
- Leser, T.D.; Molbak, L. Better living through microbial action: The benefits of the mammalian gastrointestinal microbiota on the host. Environ. Microbiol. 2009, 11, 2194–2206. [Google Scholar]
- Purchiaroni, F.; Tortora, A.; Gabrielli, M.; Bertucci, F.; Gigante, G.; Ianiro, G.; Ojetti, V.; Scarpellini, E.; Gasbarrini, A. The role of intestinal microbiota and the immune system. Eur. Rev. Med. Pharmacol. Sci. 2013, 17, 323–333. [Google Scholar]
- Jumpertz, R.; Le, D.S.; Turnbaugh, P.J.; Trinidad, C.; Bogardus, C.; Gordon, J.I.; Krakoff, J. Energy-balance studies reveal associations between gut microbes caloric load and nutrient absorption in humans. Am. J. Clin. Nutr. 2011, 94, 58–65. [Google Scholar]
- Blumberg, R.; Powrie, F. Microbiota disease and back to health: A metastable journey. Sci. Transl. Med. 2012, 4, 137rv7. [Google Scholar]
- Karlsson, F.; Tremaroli, V.; Nielsen, J.; Backhed, F. Assessing the human gut microbiota in metabolic diseases. Diabetes 2013, 62, 3341–3349. [Google Scholar]
- Musso, G.; Gambino, R.; Cassader, M. Gut microbiota as a regulator of energy homeostasis and ectopic fat deposition: Mechanisms and implications for metabolic disorders. Curr. Opin. Lipidol. 2010, 21, 76–83. [Google Scholar]
- Coates, M.E. Gnotobiotic animals in research: Their uses and limitations. Lab. Anim. 1975, 9, 275–282. [Google Scholar]
- Backhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004, 101, 15718–15723. [Google Scholar]
- Backhed, F.; Manchester, J.K.; Semenkovich, C.F.; Gordon, J.I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl. Acad. Sci. USA 2007, 104, 979–984. [Google Scholar]
- Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444, 1027–1031. [Google Scholar]
- Ley, R.E.; Backhed, F.; Turnbaugh, P.; Lozupone, C.A.; Knight, R.D.; Gordon, J.I. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 2005, 102, 11070–11075. [Google Scholar]
- Turnbaugh, P.J.; Backhed, F.; Fulton, L.; Gordon, J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008, 3, 213–223. [Google Scholar]
- Turnbaugh, P.J.; Hamady, M.; Yatsunenko, T.; Cantarel, B.L.; Duncan, A.; Ley, R.E.; Sogin, M.L.; Jones, W.J.; Roe, B.A.; Affourtit, J.P.; et al. A core gut microbiome in obese and lean twins. Nature 2009, 457, 480–484. [Google Scholar]
- Kim, K.A.; Gu, W.; Lee, I.A.; Joh, E.H.; Kim, D.H. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 2012, 7, e47713. [Google Scholar]
- Verdam, F.J.; Fuentes, S.; de Jonge, C.; Zoetendal, E.G.; Erbil, R.; Greve, J.W.; Buurman, W.A.; de Vos, W.M.; Rensen, S.S. Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity (Silver Spring) 2013, 21, E607–E615. [Google Scholar]
- Ley, R.E.; Turnbaugh, P.J.; Klein, S.; Gordon, J.I. Microbial ecology: Human gut microbes associated with obesity. Nature 2006, 444, 1022–1023. [Google Scholar]
- Million, M.; Angelakis, E.; Maraninchi, M.; Henry, M.; Giorgi, R.; Valero, R.; Vialettes, B.; Raoult, D. Correlation between body mass index and gut concentrations of Lactobacillus reuteri Bifidobacterium animalis Methanobrevibacter smithii and Escherichia coli. Int. J. Obes. (Lond.) 2013, 37, 1460–1466. [Google Scholar]
- Million, M.; Maraninchi, M.; Henry, M.; Armougom, F.; Richet, H.; Carrieri, P.; Valero, R.; Raccah, D.; Vialettes, B.; Raoult, D. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int. J. Obes. (Lond.) 2012, 36, 817–825. [Google Scholar]
- Serino, M.; Fernandez-Real, J.M.; Fuentes, E.G.; Queipo-Ortuno, M.; Moreno-Navarrete, J.M.; Sanchez, A.; Burcelin, R.; Tinahones, F. The gut microbiota profile is associated with insulin action in humans. Acta Diabetol. 2012, 50, 753–761. [Google Scholar]
- Zhang, H.; DiBaise, J.K.; Zuccolo, A.; Kudrna, D.; Braidotti, M.; Yu, Y.; Parameswaran, P.; Crowell, M.D.; Wing, R.; Rittmann, B.E.; et al. Human gut microbiota in obesity and after gastric bypass. Proc. Natl. Acad. Sci. USA 2009, 106, 2365–2370. [Google Scholar]
- Greiner, T.; Backhed, F. Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol. Metab. 2011, 22, 117–123. [Google Scholar]
- Brown, A.J.; Goldsworthy, S.M.; Barnes, A.A.; Eilert, M.M.; Tcheang, L.; Daniels, D.; Muir, A.I.; Wigglesworth, M.J.; Kinghorn, I.; Fraser, N.J.; et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 2003, 278, 11312–11319. [Google Scholar]
- Manco, M.; Putignani, L.; Bottazzo, G.F. Gut microbiota lipopolysaccharides and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr. Rev. 2010, 31, 817–844. [Google Scholar]
- Cani, P.D.; Amar, J.; Iglesias, M.A.; Poggi, M.; Knauf, C.; Bastelica, D.; Neyrinck, A.M.; Fava, F.; Tuohy, K.M.; Chabo, C.; et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761–1772. [Google Scholar]
- Rodes, L.; Khan, A.; Paul, A.; Coussa-Charley, M.; Marinescu, D.; Tomaro-Duchesneau, C.; Shao, W.; Kahouli, I.; Prakash, S. Effect of probiotics Lactobacillus and Bifidobacterium on gut-derived lipopolysaccharides and inflammatory cytokines: An in vitro study using a human colonic microbiota model. J. Microbiol. Biotechnol. 2013, 23, 518–526. [Google Scholar]
- Murri, M.; Leiva, I.; Gomez-Zumaquero, J.M.; Tinahones, F.J.; Cardona, F.; Soriguer, F.; Queipo-Ortuno, M.I. Gut microbiota in children with type 1 diabetes differs from that in healthy children: A case-control study. BMC Med. 2013, 11, 46. [Google Scholar]
- Larsen, N.; Vogensen, F.K.; van den Berg, F.W.; Nielsen, D.S.; Andreasen, A.S.; Pedersen, B.K.; Al-Soud, W.A.; Sorensen, S.J.; Hansen, L.H.; Jakobsen, M. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 2010, 5, e9085. [Google Scholar]
- Qin, J.; Li, Y.; Cai, Z.; Li, S.; Zhu, J.; Zhang, F.; Liang, S.; Zhang, W.; Guan, Y.; Shen, D.; et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012, 490, 55–60. [Google Scholar]
- Tagliabue, A.; Elli, M. The role of gut microbiota in human obesity: Recent findings and future perspectives. Nutr. Metab. Cardiovasc. Dis. 2013, 23, 160–168. [Google Scholar]
- Stachowicz, N.; Kiersztan, A. The role of gut microbiota in the pathogenesis of obesity and diabetes. Postep. Hig. Med. Dosw. 2013, 67, 288–303. [Google Scholar]
- Caricilli, A.M.; Saad, M.J. The role of gut microbiota on insulin resistance. Nutrients 2013, 5, 829–851. [Google Scholar]
- FAO/WHO. Guidelines for the Evaluation of Probiotics in Food, Report of a Joint Food and Agriculture Organization of the United Nations/World Health Organization Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food, London, Ontario, Canada, 30 April and 1 May 2002; Available online: http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf?ua=1.
- Duan, F.; Curtis, K.L.; March, J.C. Secretion of insulinotropic proteins by commensal bacteria: Rewiring the gut to treat diabetes. Appl. Environ. Microbiol. 2008, 74, 7437–7438. [Google Scholar]
- Hsieh, F.C.; Lee, C.L.; Chai, C.Y.; Chen, W.T.; Lu, Y.C.; Wu, C.S. Oral administration of Lactobacillus reuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutr. Metab. 2013, 10, 35. [Google Scholar]
- Sakai, T.; Taki, T.; Nakamoto, A.; Shuto, E.; Tsutsumi, R.; Toshimitsu, T.; Makino, S.; Ikegami, S. Lactobacillus plantarum OLL2712 regulates glucose metabolism in C57BL/6 mice fed a high-fat diet. J. Nutr. Sci. Vitaminol. 2013, 59, 144–147. [Google Scholar]
- Bejar, W.; Hamden, K.; Salah, R.B.; Chouayekh, H. Lactobacillus plantarum TN627 significantly reduces complications of alloxan-induced diabetes in rats. Anaerobe 2013, 24, 4–11. [Google Scholar]
- Park, J.E.; Oh, S.H.; Cha, Y.S. Lactobacillus plantarum LG42 isolated from gajami sik-hae decreases body and fat pad weights in diet-induced obese mice. J. Appl. Microbiol. 2014, 116, 145–156. [Google Scholar]
- Yadav, H.; Jain, S.; Sinha, P.R. Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J. Dairy Res. 2008, 75, 189–195. [Google Scholar]
- Kang, J.H.; Yun, S.I.; Park, M.H.; Park, J.H.; Jeong, S.Y.; Park, H.O. Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PLoS One 2013, 8, e54617. [Google Scholar]
- Kim, S.W.; Park, K.Y.; Kim, B.; Kim, E.; Hyun, C.K. Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem. Biophys. Res. Commun. 2013, 431, 258–263. [Google Scholar]
- Zhang, Y.; Wang, L.; Zhang, J.; Li, Y.; He, Q.; Li, H.; Guo, X.; Guo, J.; Zhang, H. Probiotic Lactobacillus casei Zhang ameliorates high-fructose-induced impaired glucose tolerance in hyperinsulinemia rats. Eur. J. Nutr. 2014, 53, 221. [Google Scholar]
- Andreasen, A.S.; Larsen, N.; Pedersen-Skovsgaard, T.; Berg, R.M.; Moller, K.; Svendsen, K.D.; Jakobsen, M.; Pedersen, B.K. Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br. J. Nutr. 2010, 104, 1831–1838. [Google Scholar]
- Asemi, Z.; Samimi, M.; Tabassi, Z.; Naghibi Rad, M.; Rahimi Foroushani, A.; Khorammian, H.; Esmaillzadeh, A. Effect of daily consumption of probiotic yoghurt on insulin resistance in pregnant women: A randomized controlled trial. Eur. J. Clin. Nutr. 2013, 67, 71–74. [Google Scholar]
- Ejtahed, H.S.; Mohtadi-Nia, J.; Homayouni-Rad, A.; Niafar, M.; Asghari-Jafarabadi, M.; Mofid, V.; Akbarian-Moghari, A. Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J. Dairy Sci. 2011, 94, 3288–3294. [Google Scholar]
- Ejtahed, H.S.; Mohtadi-Nia, J.; Homayouni-Rad, A.; Niafar, M.; Asghari-Jafarabadi, M.; Mofid, V. Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition 2012, 28, 539–543. [Google Scholar]
- Asemi, Z.; Zare, Z.; Shakeri, H.; Sabihi, S.S.; Esmaillzadeh, A. Effect of multispecies probiotic supplements on metabolic profiles hs-CRP and oxidative stress in patients with type 2 diabetes. Ann. Nutr. Metab. 2013, 63, 1–9. [Google Scholar]
- Kadooka, Y.; Sato, M.; Imaizumi, K.; Ogawa, A.; Ikuyama, K.; Akai, Y.; Okano, M.; Kagoshima, M.; Tsuchida, T. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur. J. Clin. Nutr. 2010, 64, 636–643. [Google Scholar]
- Jung, S.P.; Lee, K.M.; Kang, J.H.; Yun, S.I.; Park, H.O.; Moon, Y.; Kim, J.Y. Effect of lactobacillus gasseri BNR17 on overweight and obese adults: A randomized double-blind clinical trial. Korean J. Fam. Med. 2013, 34, 80–89. [Google Scholar]
- Panwar, H.; Calderwood, D.; Grant, I.R.; Grover, S.; Green, B.D. Lactobacillus strains isolated from infant faeces possess potent inhibitory activity against intestinal alpha- and beta-glucosidases suggesting anti-diabetic potential. Eur. J. Nutr. 2014. [Google Scholar] [CrossRef]
- Ataie-Jafari, A.; Larijani, B.; Alavi Majd, H.; Tahbaz, F. Cholesterol-lowering effect of probiotic yogurt in comparison with ordinary yogurt in mildly to moderately hypercholesterolemic subjects. Ann. Nutr. Metab. 2009, 54, 22–27. [Google Scholar]
- Mazloom, Z.; Yousefinejad, A.; Dabbaghmanesh, M.H. Effect of probiotics on lipid profile glycemic control insulin action oxidative stress and inflammatory markers in patients with type 2 diabetes: A clinical trial. Iran. J. Med. Sci. 2013, 38, 38–43. [Google Scholar]
- Rad, H. The effects of probiotic yoghurt on C-Reactive Protein in type 2 diabetic patients. Yafteh 2013, 15, 95–104. [Google Scholar]
- Stsepetova, J.; Sepp, E.; Kolk, H.; Loivukene, K.; Songisepp, E.; Mikelsaar, M. Diversity and metabolic impact of intestinal Lactobacillus species in healthy adults and the elderly. Br. J. Nutr. 2011, 105, 1235–1244. [Google Scholar]
- Gibson, G.R. Prebiotics as gut microflora management tools. J. Clin. Gastroenterol. 2008, 42, S75–S79. [Google Scholar]
- Everard, A.; Lazarevic, V.; Derrien, M.; Girard, M.; Muccioli, G.G.; Neyrinck, A.M.; Possemiers, S.; Van Holle, A.; Francois, P.; de Vos, W.M.; et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 2011, 60, 2775–2786. [Google Scholar]
- Parnell, J.A.; Reimer, R.A. Prebiotic fibres dose-dependently increase satiety hormones and alter Bacteroidetes and Firmicutes in lean and obese JCR:LA-cp rats. Br. J. Nutr. 2012, 107, 601–613. [Google Scholar]
- Dewulf, E.M.; Cani, P.D.; Neyrinck, A.M.; Possemiers, S.; Van Holle, A.; Muccioli, G.G.; Deldicque, L.; Bindels, L.B.; Pachikian, B.D.; Sohet, F.M.; et al. Inulin-type fructans with prebiotic properties counteract GPR43 overexpression and PPARgamma-related adipogenesis in the white adipose tissue of high-fat diet-fed mice. J. Nutr. Biochem. 2011, 22, 712–722. [Google Scholar]
- Neyrinck, A.M.; Possemiers, S.; Druart, C.; Van de Wiele, T.; De Backer, F.; Cani, P.D.; Larondelle, Y.; Delzenne, N.M. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS One 2011, 6, e20944. [Google Scholar]
- Kajiwara, S.; Gandhi, H.; Ustunol, Z. Effect of honey on the growth of and acid production by human intestinal Bifidobacterium spp: An in vitro comparison with commercial oligosaccharides and inulin. J. Food Prot. 2002, 65, 214–218. [Google Scholar]
- Sanz, M.L.; Polemis, N.; Morales, V.; Corzo, N.; Drakoularakou, A.; Gibson, G.R.; Rastall, R.A. In vitro investigation into the potential prebiotic activity of honey oligosaccharides. J. Agric. Food Chem. 2005, 53, 2914–2921. [Google Scholar]
- Erejuwa, O.O.; Sulaiman, S.A.; Wahab, M.S. Oligosaccharides might contribute to the antidiabetic effect of honey: A review of the literature. Molecules 2011, 17, 248–266. [Google Scholar]
- Erejuwa, O.O.; Sulaiman, S.A.; Wahab, M.S.; Sirajudeen, K.N.; Salleh, M.S.; Gurtu, S. Glibenclamide or metformin combined with honey improves glycemic control in streptozotocin-induced diabetic rats. Int. J. Biol. Sci. 2011, 7, 244–252. [Google Scholar]
- Kuo, S.M.; Merhige, P.M.; Hagey, L.R. The effect of dietary prebiotics and probiotics on body weight large intestine indices and fecal bile acid profile in wild type and IL10−/− mice. PLoS One 2013, 8, e60270. [Google Scholar]
- Walsh, A.M.; Sweeney, T.; O’Shea, C.J.; Doyle, D.N.; O’Doherty, J.V. Effect of dietary laminarin and fucoidan on selected microbiota intestinal morphology and immune status of the newly weaned pig. Br. J. Nutr. 2013, 1–9. [Google Scholar]
- Cani, P.D.; Lecourt, E.; Dewulf, E.M.; Sohet, F.M.; Pachikian, B.D.; Naslain, D.; De Backer, F.; Neyrinck, A.M.; Delzenne, N.M. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am. J. Clin. Nutr. 2009, 90, 1236–1243. [Google Scholar]
- Parnell, J.A.; Reimer, R.A. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am. J. Clin. Nutr. 2009, 89, 1751–1759. [Google Scholar]
- Sasaki, M.; Ogasawara, N.; Funaki, Y.; Mizuno, M.; Iida, A.; Goto, C.; Koikeda, S.; Kasugai, K.; Joh, T. Transglucosidase improves the gut microbiota profile of type 2 diabetes mellitus patients: A randomized double-blind placebo-controlled study. BMC Gastroenterol. 2013, 13, 81. [Google Scholar]
- McNeil, N.I. The contribution of the large intestine to energy supplies in man. Am. J. Clin. Nutr. 1984, 39, 338–342. [Google Scholar]
- Hu, G.X.; Chen, G.R.; Xu, H.; Ge, R.S.; Lin, J. Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. Med. Hypotheses 2010, 74, 123–126. [Google Scholar]
- Gao, Z.; Yin, J.; Zhang, J.; Ward, R.E.; Martin, R.J.; Lefevre, M.; Cefalu, W.T.; Ye, J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009, 58, 1509–1517. [Google Scholar]
- Lappi, J.; Salojarvi, J.; Kolehmainen, M.; Mykkanen, H.; Poutanen, K.; de Vos, W.M.; Salonen, A. Intake of whole-grain and fiber-rich rye bread versus refined wheat bread does not differentiate intestinal microbiota composition in Finnish adults with metabolic syndrome. J. Nutr. 2013, 143, 648–655. [Google Scholar]
- Weickert, M.O.; Arafat, A.M.; Blaut, M.; Alpert, C.; Becker, N.; Leupelt, V.; Rudovich, N.; Mohlig, M.; Pfeiffer, A.F. Changes in dominant groups of the gut microbiota do not explain cereal-fiber induced improvement of whole-body insulin sensitivity. Nutr. Metab. 2011, 8, 90. [Google Scholar]
- Baer, D.J.; Rumpler, W.V.; Miles, C.W.; Fahey, G.C., Jr. Dietary fiber decreases the metabolizable energy content and nutrient digestibility of mixed diets fed to humans. J. Nutr. 1997, 127, 579–586. [Google Scholar]
- Isken, F.; Klaus, S.; Osterhoff, M.; Pfeiffer, A.F.; Weickert, M.O. Effects of long-term soluble vs insoluble dietary fiber intake on high-fat diet-induced obesity in C57BL/6J mice. J. Nutr. Biochem. 2010, 21, 278–284. [Google Scholar]
- Membrez, M.; Blancher, F.; Jaquet, M.; Bibiloni, R.; Cani, P.D.; Burcelin, R.G.; Corthesy, I.; Mace, K.; Chou, C.J. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J. 2008, 22, 2416–2426. [Google Scholar]
- Carvalho, B.M.; Guadagnini, D.; Tsukumo, D.M.; Schenka, A.A.; Latuf-Filho, P.; Vassallo, J.; Dias, J.C.; Kubota, L.T.; Carvalheira, J.B.; Saad, M.J. Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 2012, 55, 2823–2834. [Google Scholar]
- Bergheim, I.; Weber, S.; Vos, M.; Kramer, S.; Volynets, V.; Kaserouni, S.; McClain, C.J.; Bischoff, S.C. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: Role of endotoxin. J. Hepatol. 2008, 48, 983–992. [Google Scholar]
- Cho, I.; Yamanishi, S.; Cox, L.; Methe, B.A.; Zavadil, J.; Li, K.; Gao, Z.; Mahana, D.; Raju, K.; Teitler, I.; et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012, 488, 621–626. [Google Scholar]
- Bech-Nielsen, G.V.; Hansen, C.H.; Hufeldt, M.R.; Nielsen, D.S.; Aasted, B.; Vogensen, F.K.; Midtvedt, T.; Hansen, A.K. Manipulation of the gut microbiota in C57BL/6 mice changes glucose tolerance without affecting weight development and gut mucosal immunity. Res. Vet. Sci. 2012, 92, 501–508. [Google Scholar]
- Murphy, E.F.; Cotter, P.D.; Hogan, A.; O’Sullivan, O.; Joyce, A.; Fouhy, F.; Clarke, S.F.; Marques, T.M.; O’Toole, P.W.; Stanton, C.; et al. Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity. Gut 2013, 62, 220–226. [Google Scholar]
- Hansen, C.H.; Krych, L.; Nielsen, D.S.; Vogensen, F.K.; Hansen, L.H.; Sorensen, S.J.; Buschard, K.; Hansen, A.K. Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia 2012, 55, 2285–2294. [Google Scholar]
- Erejuwa, O.O.; Gurtu, S.; Sulaiman, S.A.; Ab Wahab, M.S.; Sirajudeen, K.N.; Salleh, M.S. Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats. Int. J. Vitam. Nutr. Res. 2010, 80, 74–82. [Google Scholar]
- Erejuwa, O.O.; Sulaiman, S.A.; Wahab, M.S.; Sirajudeen, K.N.; Salleh, M.S.; Gurtu, S. Differential responses to blood pressure and oxidative stress in streptozotocin-induced diabetic wistar-kyoto rats and spontaneously hypertensive rats: Effects of antioxidant (honey) treatment. Int. J. Mol. Sci. 2011, 12, 1888–1907. [Google Scholar]
- Nemoseck, T.M.; Carmody, E.G.; Furchner-Evanson, A.; Gleason, M.; Li, A.; Potter, H.; Rezende, L.M.; Lane, K.J.; Kern, M. Honey promotes lower weight gain adiposity and triglycerides than sucrose in rats. Nutr. Res. 2011, 31, 55–60. [Google Scholar]
- Jernberg, C.; Lofmark, S.; Edlund, C.; Jansson, J.K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007, 1, 56–66. [Google Scholar]
- O’Sullivan, O.; Coakley, M.; Lakshminarayanan, B.; Conde, S.; Claesson, M.J.; Cusack, S.; Fitzgerald, A.P.; O’Toole, P.W.; Stanton, C.; Ross, R.P. Alterations in intestinal microbiota of elderly Irish subjects post-antibiotic therapy. J. Antimicrob. Chemother. 2013, 68, 214–221. [Google Scholar]
- Kong, L.C.; Tap, J.; Aron-Wisnewsky, J.; Pelloux, V.; Basdevant, A.; Bouillot, J.L.; Zucker, J.D.; Dore, J.; Clement, K. Gut microbiota after gastric bypass in human obesity: Increased richness and associations of bacterial genera with adipose tissue genes. Am. J. Clin. Nutr. 2013, 98, 16–24. [Google Scholar]
- Kashyap, S.R.; Bhatt, D.L.; Wolski, K.; Watanabe, R.M.; Abdul-Ghani, M.; Abood, B.; Pothier, C.E.; Brethauer, S.; Nissen, S.; Gupta, M.; et al. Metabolic effects of bariatric surgery in patients with moderate obesity and type 2 diabetes: Analysis of a randomized control trial comparing surgery with intensive medical treatment. Diabetes Care 2013, 36, 2175–2182. [Google Scholar]
- Lips, M.A.; de Groot, G.H.; van Klinken, J.B.; Aarts, E.; Berends, F.J.; Janssen, I.M.; van Ramshorst, B.; van Wagensveld, B.A.; Swank, D.J.; van Dielen, F.; et al. Calorie restriction is a major determinant of the short-term metabolic effects of gastric bypass surgery in obese type 2 diabetic patients. Clin. Endocrinol. 2013. [Google Scholar] [CrossRef]
- Graessler, J.; Qin, Y.; Zhong, H.; Zhang, J.; Licinio, J.; Wong, M.L.; Xu, A.; Chavakis, T.; Bornstein, A.B.; Ehrhart-Bornstein, M.; et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: Correlation with inflammatory and metabolic parameters. Pharmacogenomics J. 2013, 13, 514–522. [Google Scholar]
- Duncan, S.H.; Belenguer, A.; Holtrop, G.; Johnstone, A.M.; Flint, H.J.; Lobley, G.E. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 2007, 73, 1073–1078. [Google Scholar]
- Duncan, S.H.; Lobley, G.E.; Holtrop, G.; Ince, J.; Johnstone, A.M.; Louis, P.; Flint, H.J. Human colonic microbiota associated with diet obesity and weight loss. Int. J. Obes. (Lond.) 2008, 32, 1720–1724. [Google Scholar]
- Kim, M.S.; Hwang, S.S.; Park, E.J.; Bae, J.W. Strict vegetarian diet improves the risk factors associated with metabolic diseases by modulating gut microbiota and reducing intestinal inflammation. Environ. Microbiol. Rep. 2013, 5, 765–775. [Google Scholar]
- Santacruz, A.; Marcos, A.; Warnberg, J.; Marti, A.; Martin-Matillas, M.; Campoy, C.; Moreno, L.A.; Veiga, O.; Redondo-Figuero, C.; Garagorri, J.M.; et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 2009, 17, 1906–1915. [Google Scholar]
- Nadal, I.; Santacruz, A.; Marcos, A.; Warnberg, J.; Garagorri, J.M.; Moreno, L.A.; Martin-Matillas, M.; Campoy, C.; Marti, A.; Moleres, A.; et al. Shifts in clostridia bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int. J. Obes. (Lond.) 2009, 33, 758–767. [Google Scholar]
- Hussey, S.; Wall, R.; Gruffman, E.; O’Sullivan, L.; Ryan, C.A.; Murphy, B.; Fitzgerald, G.; Stanton, C.; Ross, R.P. Parenteral antibiotics reduce bifidobacteria colonization and diversity in neonates. Int. J. Microbiol. 2011, 2011. [Google Scholar] [CrossRef]
- Hernandez, E.; Bargiela, R.; Diez, M.S.; Friedrichs, A.; Perez-Cobas, A.E.; Gosalbes, M.J.; Knecht, H.; Martinez-Martinez, M.; Seifert, J.; von Bergen, M.; et al. Functional consequences of microbial shifts in the human gastrointestinal tract linked to antibiotic treatment and obesity. Gut Microbes 2013, 4, 306–315. [Google Scholar]
- Jernberg, C.; Lofmark, S.; Edlund, C.; Jansson, J.K. Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 2010, 156, 3216–3223. [Google Scholar]
- Stefater, M.A.; Kohli, R.; Inge, T.H. Advances in the surgical treatment of morbid obesity. Mol. Aspects Med. 2013, 34, 84–94. [Google Scholar]
- Li, J.V.; Ashrafian, H.; Bueter, M.; Kinross, J.; Sands, C.; le Roux, C.W.; Bloom, S.R.; Darzi, A.; Athanasiou, T.; Marchesi, J.R.; et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 2011, 60, 1214–1223. [Google Scholar]
- Liou, A.P.; Paziuk, M.; Luevano, J.M., Jr; Machineni, S.; Turnbaugh, P.J.; Kaplan, L.M. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med. 2013, 5, 178ra41. [Google Scholar]
- Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J.P.; Druart, C.; Bindels, L.B.; Guiot, Y.; Derrien, M.; Muccioli, G.G.; Delzenne, N.M.; et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 2013, 110, 9066–9071. [Google Scholar]
- Sweeney, T.E.; Morton, J.M. The human gut microbiome: A review of the effect of obesity and surgically induced weight loss. JAMA Surg. 2013, 148, 563–569. [Google Scholar]
- Vetter, M.L.; Wadden, T.A.; Chittams, J.; Diewald, L.K.; Panigrahi, E.; Volger, S.; Sarwer, D.B.; Moore, R.H. Effect of lifestyle intervention on cardiometabolic risk factors: Results of the POWER-UP trial. Int. J. Obes. (Lond.) 2013, 37, S19–S24. [Google Scholar]
- Zhang, C.; Li, S.; Yang, L.; Huang, P.; Li, W.; Wang, S.; Zhao, G.; Zhang, M.; Pang, X.; Yan, Z.; et al. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat. Commun. 2013, 4, 2163. [Google Scholar]
- Phillips, F.; Hackett, A.F.; Stratton, G.; Billington, D. Effect of changing to a self-selected vegetarian diet on anthropometric measurements in UK adults. J. Hum. Nutr. Diet. 2004, 17, 249–255. [Google Scholar]
- Simon, C.; Daniel, R. Metagenomic analyses: Past and future trends. Appl. Environ. Microbiol. 2011, 77, 1153–1161. [Google Scholar]
- Benson, A.K.; Kelly, S.A.; Legge, R.; Ma, F.; Low, S.J.; Kim, J.; Zhang, M.; Oh, P.L.; Nehrenberg, D.; Hua, K.; et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. Natl. Acad. Sci. USA 2010, 107, 18933–18938. [Google Scholar]
- Ferrer, M.; Ruiz, A.; Lanza, F.; Haange, S.B.; Oberbach, A.; Till, H.; Bargiela, R.; Campoy, C.; Segura, M.T.; Richter, M.; et al. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ. Microbiol. 2013, 15, 211–226. [Google Scholar]
- Sousa, T.; Paterson, R.; Moore, V.; Carlsson, A.; Abrahamsson, B.; Basit, A.W. The gastrointestinal microbiota as a site for the biotransformation of drugs. Int. J. Pharm. 2008, 363, 1–25. [Google Scholar]
- Zimmer, J.; Lange, B.; Frick, J.S.; Sauer, H.; Zimmermann, K.; Schwiertz, A.; Rusch, K.; Klosterhalfen, S.; Enck, P. A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur. J. Clin. Nutr. 2012, 66, 53–60. [Google Scholar]
- Nursten, H.E. The Maillard Reaction. Chemistry, Biochemistry, and Implications; Royal Society of Chemistry: Cambridge, UK, 2005. [Google Scholar]
- Zhang, Q.; Ames, J.M.; Smith, R.D.; Baynes, J.W.; Metz, T.O. A perspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: Probing the pathogenesis of chronic disease. J. Proteome Res. 2009, 8, 754–769. [Google Scholar]
- Mills, D.J.; Tuohy, K.M.; Booth, J.; Buck, M.; Crabbe, M.J.; Gibson, G.R.; Ames, J.M. Dietary glycated protein modulates the colonic microbiota towards a more detrimental composition in ulcerative colitis patients and non-ulcerative colitis subjects. J. Appl. Microbiol. 2008, 105, 706–714. [Google Scholar]
- Koeth, R.A.; Wang, Z.; Levison, B.S.; Buffa, J.A.; Org, E.; Sheehy, B.T.; Britt, E.B.; Fu, X.; Wu, Y.; Li, L.; et al. Intestinal microbiota metabolism of l-carnitine a nutrient in red meat promotes atherosclerosis. Nat. Med. 2013, 19, 576–585. [Google Scholar]
- Tang, W.H.; Wang, Z.; Levison, B.S.; Koeth, R.A.; Britt, E.B.; Fu, X.; Wu, Y.; Hazen, S.L. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N. Engl. J. Med. 2013, 368, 1575–1584. [Google Scholar]
- Cotter, P.D.; Stanton, C.; Ross, R.P.; Hill, C. The impact of antibiotics on the gut microbiota as revealed by high throughput DNA sequencing. Discov. Med. 2012, 13, 193–199. [Google Scholar]
- Jakobsson, H.E.; Jernberg, C.; Andersson, A.F.; Sjolund-Karlsson, M.; Jansson, J.K.; Engstrand, L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 2010, 5, e9836. [Google Scholar]
- Trasande, L.; Blustein, J.; Liu, M.; Corwin, E.; Cox, L.M.; Blaser, M.J. Infant antibiotic exposures and early-life body mass. Int. J. Obes. (Lond.) 2013, 37, 16–23. [Google Scholar]
- Cryan, J.F.; Dinan, T.G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012, 13, 701–712. [Google Scholar]
- Manco, M. Gut microbiota and developmental programming of the brain: From evidence in behavioral endophenotypes to novel perspective in obesity. Front. Cell. Infect. Microbiol. 2012, 2, 109. [Google Scholar]
- Carvalho, F.A.; Aitken, J.D.; Vijay-Kumar, M.; Gewirtz, A.T. Toll-like receptor-gut microbiota interactions: Perturb at your own risk! Annu. Rev. Physiol. 2012, 74, 177–198. [Google Scholar]
- De Filippo, C.; Cavalieri, D.; di Paola, M.; Ramazzotti, M.; Poullet, J.B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107, 14691–14696. [Google Scholar]
Reference | Probiotic administered | Rodent/metabolic model | Study design (including treatment, dosage and duration) | Effects on gut microbiota | Effects on metabolic derangements |
---|---|---|---|---|---|
Hsieh et al. [39] | Lactobacillus reuteri | Rats; insulin resistance | Rats fed a high-fructose diet with L. reuteri at a dose of 2 × 109 CFU/rat administered daily for 14 weeks | ↑ numbers of Bifidobacterium and Lactobacillus species. ↓ number of Clostridium species | ↓ Serum levels of insulin, leptin and C-peptide, ↓ Serum levels of glucose, HbA1c and glucose intolerance ↓ Serum LDL-C, TG and TC ↓ Serum levels of AST and ALT ↑ Serum GLP-1 ↓ Adipose tissue concentrations of IL-6 and TNF-α ↓ Elvol6, SREBP-1c and FAS ↑ Hepatic AEs (GR and SOD) |
Yadav et al. [43] | Lactobacillus acidophilus; Lactobacillus casei | Rats; Diabetes mellitus | STZ-induced diabetic rats treated with dahi containing L. acidophilus and L. casei (15 g/rat/day) for 4 weeks | Uncharacterized | ↓ Plasma glucose, TG, LDL-C, TC and LDL/HDL ratio ↑ Plasma insulin and HDL-C ↑ Hepatic glycogen. ↓ Hepatic TC and TG ↓ Panccreatic OD ↑ Pancreatic AEs (SOD, CAT and GPx) |
Zhang et al. [46] | Lactobacillus casei Zhang | Rats; Hyperinsu-linemia; Impaired glucose intolerance | Rats fed fructose water and treated with L. casei Zhang at a dose of 1 × 109 CFU/day/rat | ↑ numbers of Bacteroides fragilis and Bifidobacterium & Lactobacillus species. ↓ number of Clostridium species | ↑ Glucose tolerance ↓ Serum MDA ↓ Serum insulin and GLP-2 ↑ Hepatic expression of adipoR2, LXR-α and PPAR-γ ↓ Hepatic glycogen ↑ Intestinal bile acids |
Bejar et al. [41] | Lactobacillus plantarum | Rats; Diabetes mellitus | Alloxan-induced diabetic rats treated with L. plantarum | Uncharacterized | ↓ serum levels of plasma glucose, triglyceride, LDL cholesterol, LDL/HDL ratio, creatinine, urea and transaminases. ↑ HDL cholesterol ↓ hepatic total cholesterol and triglycerides ↓ pancreatic and plasmatic lipase activities ↓ pancreatic β-cell, renal and hepatic injuries |
Park et al. [42] and Sakai et al. [40] | Lactobacillus plantarum | Mice; obesity | Mice were fed a high-fat diet and administered 1 × 107 or 1 × 109 CFU/mouse of L. plantarum or L. rhamnosus daily for 12 weeks | Uncharacterized | ↓ Serum levels of TG, insulin and leptin ↓ levels of glucose and non-esterified fatty acids ↓ mRNA expression of adipose tissue IL-1β ↓ levels of back and epididymal fat ↓ triglyceride, insulin and leptin ↑ hepatic mRNA expression of PPARα and CPT-I ↓ hepatic mRNA expression of ACC, SREBP-1 and LXRα ↓ Epididymal adipose tissue PPARγ expression |
Kim et al. [45] | Lactobacillus rhamnosus | Mice; obesity | Mice were fed a high-fat diet and administered 1 × 109 CFU/mouse of L. plantarum or L. rhamnosus daily for 13 weeks | Uncharacterized | ↓ weight gain ↑ insulin sensitivity and adiponectin secretion ↑ Adiponectin production ↑ Expression of hepatic fatty acid oxidative genes ↓ Expression of gluconeogenic genes ↑ mRNA expression of skeletal GLUT4 |
Kang et al. [44] | Lactobacillus gasseri | Mice; obesity | Mice fed high-sucrose diet and L. gasseri (1 × 109 or 1010 CFU/mouse) for 10 weeks | Uncharacterized | ↓ body weight and white adipose tissue weight ↓ serum levels of insulin and leptin ↑ mRNA levels of GLUT4 and fatty acid oxidation-related genes (ACO, CPT1, PPARα and PPARδ) ↓ mRNA levels of fatty acid synthesis-related genes (SREBP-1c and ACC) |
Reference | Rodent/metabolic model | Study design (including treatment, type of prebiotics, dosage and duration) | Effects on gut microbiota | Effects on metabolic derangements or abnormalities |
---|---|---|---|---|
Dewulf et al. and Neyrinck et al. [62,63] | Mice; Obesity | Mice fed high-fat diet and provided with inulin-type fructans (0.2 g/day per mouse) or arabinoxylans (10% w/w) for 4 weeks | ↑ Abundance of Bifidobacteria and Bacteroides-Prevotella species ↓ Number of Clostridium and Roseburia species | ↓ Body weight gain ↓ Serum and hepatic cholesterol levels ↓ Insulin resistance ↓ Adipocyte size and adiposity ↓ PPAR-γ-activated differentiation factors ↑ adipose tissue GPR43 expression ↑ Gut barrier function ↓ Inflammatory markers ↓ Expression of genes involved in fatty acid uptake, differentiation, fatty acid oxidation and inflammation ↓ Lipogenic enzyme activity |
Everard et al. [60] | Mice; Obesity and diabetes mellitus | Genetic or diet-induced obese and diabetic mice fed with prebiotic-enriched diet (oligofructose, 0.3 g/mouse/day) for 8 weeks | ↑ Bacteroidetes phylum ↓ Firmicutes phylum | ↓ Glucose intolerance and plasma glucose ↑ L-cell number and plasma GLP-1 ↑ Leptin sensitivity ↑ LPL and proglucagon mRNA levels ↓ Plasma TG and adipose tissue weight ↓ Muscle TG and lipid content ↓ Adipose tissue oxidative stress ↓ Low grade inflammation |
Parnell and Reimer [61] | Rats; Obesity | Obese rats fed 10% and 20% fibre (inulin: oligofructose) diets for 10 weeks | ↑ Number of Bacteroidetes group ↓ Number of Firmicutes and Clostridium coccoides group ↑ Bifidobacterium and Lactobacillus species | ↓ Energy intake ↓ Glucagon ↑ GLP-1 secretion ↓ Ghrelin response ↑ mRNA levels of caecal peptide YY and proglucagon ↓ Ghrelin O-acyltransferase mRNA levels |
Erejuwa et al. and Nemoseck et al. [67,87–89] | Rats; Diabetes mellitus | Rats fed honey or sucrose as well as STZ-induced diabetic rats fed honey for 33 days | Uncharacterized | ↓ Body weight gain in honey fed vs. sucrose fed rats ↑ Body weight in honey-treated STZ vs. STZ control rats ↓ Epididymal fat weight ↓ Serum levels of glucose and fructosamine ↓ Serum levels of TG, VLDL-C, leptin and bilirubin ↑ Serum albumin, insulin and HDL-C |
Reference | Antibiotics administered | Rodent/metabolic model | Study design (including treatment, dosage and duration) | Effects on gut microbiota | Effects on metabolic derangements |
---|---|---|---|---|---|
Membrez et al. [80] | Norfloxacin and ampicillin | Mice; Insulin resistance and obesity | Genetically obese, diet-induced obese and insulin-resistant mice treated with norfloxacin and ampicillin (1 g/L each) for 14 or 17 days | Uncharacterized | ↓ Blood glucose and glucose intolerance ↓ Plasma insulin and insulin resistance ↓ Plasma LPS ↓ Hepatic TG ↑ Adiponectin ↑ Hepatic glycogen storage |
Carvalho et al., Bergheim et al. and Cho et al. [81–83] | Aampicillin, neomycin and metronidazole | Mice; Fatty liver, adiposity | Mice fed HFD with ampicillin, neomycin and metronidazole, each at 1 g/L) or polymyxin B (92 mg) and neomycin (216 mg) for 8 weeks | ↓ Total bacterial count ↓ Bacteroidetes and Firmicutes | ↓ Food intake and body weight gain ↓ Plasma glucose and insulin ↑ Glucose and insulin tolerance ↓ LPS, TNF-α and IL-6 ↓ TLR4, JNK, IKKbeta ↑ Colonic levels of SCFAs and GIP ↑ Phosphorylation of IR, IRS-1 and Akt ↑ Circulating acetate ↑ AMPK phosphorylation |
Murphy et al. and Bech-Nielsen et al. [84,85] | Vancomycin, ampicillin | Mice; Obesity | Mice fed a low-fat or high-fat diet with/without vancomycin (2 mg/day) for 8 weeks | ↑ Proteobacteria ↓ Bacteroidetes and Firmicutes | ↓ Body weight gain ↑ Glucose tolerance ↓ Blood glucose ↓ Plasma TG and TNF-α |
Hansen et al. [86] | Vancomycin | Mice; Diabetes mellitus | NOD mice treated with vancomycin (83 mg/kg/day) until development of diabetes or weaning (28 days) | ↓ Bacteroidetes and Firmicutes | ↓ Blood glucose ↓ Insulitis score |
Reference | Intervention/modulation | Metabolic disorder | Study design | Effects on gut microbiota and metabolic derangements including other alterations |
---|---|---|---|---|
Andreasen et al. and Asemi et al. [47,48] | Probiotic (L. acidophilus and B. animalis) | Insulin resistance; Diabetes mellitus | Randomized, double-blind, controlled studies. 45 males with type 2 diabetes, impaired or normal glucose tolerance treated with/without L. acidophilus for 4 weeks and controlled clinical trial; 70 pregnant women given a probiotic yoghurt containing L. acidophilus and B. animalis (200 g/day) for 9 weeks | ↑ L. acidophilus ↑ Insulin sensitivity in probiotic group ↓ insulin resistance |
Ejtahed et al. [49,50] | Probiotic (L. acidophilus and B. lactis) | Diabetes mellitus | Randomized, double-blind, controlled trials. 60–64 patients with type 2 diabetes mellitus consumed probiotic/non-prebiotic yogurt containing L. acidophilus and B. lactis (300 g/day) for 6 weeks | Gut microbiota: Uncharacterized ↓ Blood glucose and HbA1c ↓ TC and LDL-C in probiotic group ↓ Atherogenic indices (TC:HDL-C ratio and LDL-C:HDL-C ratio) ↑ Erythrocyte TAS, SOD and GPx activities ↓ Serum MDA |
Kadooka et al. and Jung et al. [52,53] | Probiotic (L. gasseri) | Overweight and Obesity | Randomized, multicenter, double-blind, placebo-controlled trial. 57 or 87 obese subjects received fermented milk containing L. gasseri or without (200 g/day) for 12 weeks | ↓ Body weight ↓ BMI ↓ Abdominal visceral, subcutaneous and total fat areas in prebiotic group ↓ Waist and hip circumferences ↓ Waist-to-hip ratio |
Asemi et al. [51] | Probiotic and prebiotic. Probiotic (L. acidophilus, L. casei, L. rhamnosus, L. bulgaricus, B. breve, B. longum, S. thermophilus) Prebiotic (fructo-oligosaccharide) | Diabetes mellitus | Randomized, double-blind, placebo-controlled clinical trial. 54 diabetic patients ingested a multispecies probiotic/non-prebiotic supplement (consisting of L. acidophilus, L. casei, L. rhamnosus, L. bulgaricus, B. breve, B. longum, S. thermophilus and fructo-oligosaccharide) for 8 weeks | Gut microbiota: Uncharacterized ↓ Blood glucose increments ↓ Insulin resistance ↓ Serum hs-CRP ↑ Plasma GSH levels |
Cani et al. and Parnell and Reimer [70,71] | Prebiotic (oligofructose or a mixture of glucosyl- (fructosyl)n-fructose and (fructosyl)mfructose extracted from chicory roots) | Healthy, overweight and obesity | Randomized, double-blind, parallel, placebo-controlled trial 10 healthy adults given 16 g of prebiotics/day | ↑ Marker of gut microbiota fermentation (breath-hydrogen excretion) ↓ Body weight ↓ Caloric intake ↓ Plasma glucose and postprandial glucose responses ↓ Insulin levels ↑ Levels of GLP-1 and peptide YY ↓ Ghrelin levels |
Sasaki et al. [72] | Prebiotic (transglucosidase) | Healthy and Diabetes mellitus | Randomized, double-blind, parallel, placebo-controlled study. 60 diabetic patients received 300 or 900 mg/day of transglucosidase for 12 weeks. | ↑ Bacteroidetes-to-Firmicutes ratio ↓ Body weight ↓ Blood glucose |
Jernberg et al. and O’Sullivan et al. [90,91] | Antibiotics (Clindamycin) | Healthy adults | 42 elderly subjects were treated with one antibiotic within 1 month | ↓ Bacteroides ↓ Bifidobacterium spp. Metabolic derangements: Unevaluated |
Zhang et al. And Kong et al. [25,92] | Gastric bypass | Obesity | Comparison of the structures of microbes in individuals with normal weight, morbid obesity and post-gastric-bypass surgery | ↓ Firmicutes ↑ Proteobacteria ↑ Alterations of WAT genes ↑ Associations between gut microbiota composition and WAT gene expression Metabolic derangements: Unevaluated |
Kashyap et al. [93–95] | Bariatric surgery | Obesity and Diabetes mellitus | Randomized, prospective, controlled and nonrandomized, controlled observational trials Type 2 diabetic subjects with moderate obesity received bariatric surgery Changes of gut microbial composition 3 months before and after RYGB in morbidly obese patients with type 2 diabetes mellitus | ↑ Proteobacteria ↓ Firmicutes and Bacteroidetes ↑ Weight loss ↓ Blood glucose ↓ HbA1c ↑ Pancreatic β-cell function ↑ Insulin sensitivity ↓ Adiposity ↑ GLP-1 and peptide YY levels ↓ Ghrelin levels |
Duncan et al. [96,97] | Weight loss/Caloric restriction | Obesity | Obese and non-obese individuals under conditions of weight maintenance, and undergoing weight loss on reduced carbohydrate diets for 4 weeks | ↓ Total fecal SCFAs ↓ Abundance of butyrate-producing bacteria such as Firmicutes, Bifidobacteria, Eubacterium rectale and Roseburia spp. Metabolic derangements: Unevaluated |
Kim et al. [98] | Weight loss/Caloric restriction/Vegetarian diet | Obesity and Diabetes mellitus | Obese individuals with type 2 diabetes and/or hypertension assigned to a vegetarian diet for 1 month | ↓ Firmicutes-to-Bacteroidetes ratio ↓ Body weight ↓ Fasting and postprandial glucose ↓ HbA1c ↓ TC, LDL-C and TG |
Santacruz et al. and Nadal et al. [99,100] | Weight loss, caloric restriction or increased physical activity | Obesity | Longitudinal intervention study Overweight and obese individuals placed on a calorie-restricted diet and increased physical activity program for 10 weeks | ↑ Weight loss ↓ BMI and BMI z-score ↑ Total bacteria, Bacteroides-Prevotella group and Lactobacillus group counts ↓ Clostridium coccoides group, Bifidobacterium longum, and Bifidobacterium adolescentis counts Reduced body weight and BMI z-score correlated with reduction of certain gut microbes |
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Erejuwa, O.O.; Sulaiman, S.A.; Wahab, M.S.A. Modulation of Gut Microbiota in the Management of Metabolic Disorders: The Prospects and Challenges. Int. J. Mol. Sci. 2014, 15, 4158-4188. https://doi.org/10.3390/ijms15034158
Erejuwa OO, Sulaiman SA, Wahab MSA. Modulation of Gut Microbiota in the Management of Metabolic Disorders: The Prospects and Challenges. International Journal of Molecular Sciences. 2014; 15(3):4158-4188. https://doi.org/10.3390/ijms15034158
Chicago/Turabian StyleErejuwa, Omotayo O., Siti A. Sulaiman, and Mohd S. Ab Wahab. 2014. "Modulation of Gut Microbiota in the Management of Metabolic Disorders: The Prospects and Challenges" International Journal of Molecular Sciences 15, no. 3: 4158-4188. https://doi.org/10.3390/ijms15034158