Systematic review on intervention with prebiotics/probiotics in patients with obesity-related nonalcoholic fatty liver disease

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Cénit MC, Matzaraki V, Tigchelaar EF, Zhernakova A. Rapidly expanding knowledge on the role of the gut microbiome in health and disease. Biochim. Biophys. Acta 1842(10), 1981–1992 (2014).•• Complete review on the topic.
  Medline CASGoogle Scholar
• 2 Frick JS, Autenrieth IB. The gut microflora and its variety of roles in health and disease. Curr. Top. Microbiol. Immunol. 358, 273–289 (2013).
  Medline CASGoogle Scholar
• 3 Finelli C, Tarantino G. Non-alcoholic fatty liver disease, diet and gut microbiota. EXCLI Journal 13, 461–490 (2014).
  MedlineGoogle Scholar
• 4 Xiao S, Zhao L. Gut microbiota-based translational biomarkers to prevent metabolic syndrome via nutritional modulation. FEMS Microbiol. Ecol. 87(2), 303–314 (2014).
  Medline CASGoogle Scholar
• 5 Sweeney TE, Morton JM. The human gut microbiome: a review of the effect of obesity and surgically induced weight loss. JAMA Surg. 148(6), 563–569 (2013).•• Recent review on the topic.
  Medline CASGoogle Scholar
• 6 Kim JH. The physical activity level in female affects colon transit time. J. Neurogastroenterol. Motil. 18(1), 4–5 (2012).
  MedlineGoogle Scholar
• 7 Cho KO, Jo YJ, Song BK, Oh JW, Kim YS. Colon transit time according to physical activity and characteristics in South Korean adults. World J. Gastroenterol. 19(4), 550–555 (2013).
  MedlineGoogle Scholar
• 8 Valdés-Ramos R, Martínez-Carrillo BE, Aranda-González II et al. Diet, exercise and gut mucosal immunity. Proc. Nutr. Soc. 69(4), 644–650 (2010).
  Medline CASGoogle Scholar
• 9 Clarke SF, Murphy EF, O'Sullivan O et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63(12), 1913–1920 (2014).
  Medline CASGoogle Scholar
• 10 Tarantino G, Finelli C. What about non-alcoholic fatty liver disease as a new criterion to define metabolic syndrome? World J. Gastroenterol. 19(22), 3375–3384 (2013).
  Medline CASGoogle Scholar
• 11 Fierbinteanu-Braticevici C, Negreanu L, Tarantino G. Is fatty liver always benign and should not consequently be treated? J. Physiol. Pharmacol. 64(1), 3–9 (2013).
  Medline CASGoogle Scholar
• 12 Raman M, Allard J. Non alcoholic fatty liver disease: a clinical approach and review. Can. J. Gastroenterol. 20(5), 345–349 (2006).
  MedlineGoogle Scholar
• 13 Pan JJ, Fallon MB. Gender and racial differences in nonalcoholic fatty liver disease. World J. Hepatol. 6(5), 274–283 (2014).
  MedlineGoogle Scholar
• 14 Tarantino G. Gut microbiome, obesity-related comorbidities, and low-grade chronic inflammation. J. Clin. Endocrinol. Metab. 99(7), 2343–2346 (2014).
  Medline CASGoogle Scholar
• 15 Remely M, Aumueller E, Merold C et al. Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in Type 2 diabetes and obesity. Gene 537(1), 85–92 (2014).
  Medline CASGoogle Scholar
• 16 Chen Z, Guo L, Zhang Y et al. Incorporation of therapeutically modified bacteria into gut microbiota inhibits obesity. J. Clin. Invest. 124(8), 3391–3406 (2014).•• Basic research to improve the mechanisms of gut flora modifiers.
  Medline CASGoogle Scholar
• 17 Li M, Gu D, Xu N et al. Gut carbohydrate metabolism instead of fat metabolism regulated by gut microbes mediates high-fat diet-induced obesity. Benef. Microbes 5(3), 335–344 (2014).
  MedlineGoogle Scholar
• 18 Walker A, Pfitzner B, Neschen S et al. Distinct signatures of host-microbial meta-metabolome and gut microbiome in two C57BL/6 strains under high-fat diet. ISME J. 8(12), 2380–2396 (2014).
  Medline CASGoogle Scholar
• 19 Karlsson F, Tremaroli V, Nielsen J, Bäckhed F. Assessing the human gut microbiota in metabolic diseases. Diabetes 62(10), 3341–3349 (2013).
  Medline CASGoogle Scholar
• 20 Tomaro-Duchesneau C, Saha S, Malhotra M et al. Effect of orally administered L. fermentum NCIMB 5221 on markers of metabolic syndrome: an in vivo analysis using ZDF rats. Appl. Microbiol. Biotechnol. 98(1), 115–126 (2014).
  Medline CASGoogle Scholar
• 21 Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int. J. Surg. 8(5), 336–341 (2010).
  MedlineGoogle Scholar
• 22 Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboratio. www.cochrane-handbook.org.
  Google Scholar
• 23 Mykhal'chyshyn HP, Bodnar PM, Kobyliak NM. [Effect of probiotics on proinflammatory cytokines level in patients with Type 2 diabetes and non-alcoholic fatty liver disease]. Lik. Sprava 2, 56–62 (2013).
  MedlineGoogle Scholar
• 24 Wong VW, Won GL, Chim AM et al. Treatment of nonalcoholic steatohepatitis with probiotics. A proof-of-concept study. Ann. Hepatol. 12(2), 256–262 (2013).• Clinical investigation addressing patients with nonalcoholic fatty liver disease.
  Medline CASGoogle Scholar
• 25 Aller R, De Luis DA, Izaola O et al. Effect of a probiotic on liver aminotransferases in nonalcoholic fatty liver disease patients: a double blind randomized clinical trial. Eur. Rev. Med. Pharmacol. Sci. 15(9), 1090–1095 (2011).
  Medline CASGoogle Scholar
• 26 Dewulf EM, Cani PD, Claus SP et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62(8), 1112–1121 (2013).
  Medline CASGoogle Scholar
• 27 de Luis DA, de la Fuente B, Izaola O et al. Double blind randomized clinical trial controlled by placebo with an alpha linoleic acid and prebiotic enriched cookie on risk cardiovascular factor in obese patients. Nutr. Hosp. 26(4), 827–833 (2011).•• Clinical investigation taking into account the cardiovascular disease risk.
  Medline CASGoogle Scholar
• 28 de Luis DA, de la Fuente B, Izaola O et al. Randomized clinical trial with a inulin enriched cookie on risk cardiovascular factor in obese patients. Nutr. Hosp. 25(1), 53–59 (2010).
  Medline CASGoogle Scholar
• 29 Balcázar-Muñoz BR, Martínez-Abundis E, González-Ortiz M. Effect of oral inulin administration on lipid profile and insulin sensitivity in subjects with obesity and dyslipidemia. Rev. Med. Chil. 131(6), 597–604 (2003).
  MedlineGoogle Scholar
• 30 Karlsson Videhult F, Ohlund I, Stenlund H, Hernell O, West CE. Probiotics during weaning: a follow-up study on effects on body composition and metabolic markers at school age. Eur J Nutr. 17 (2014) (Epub ahead of print).
  Google Scholar
• 31 Alisi A, Bedogni G, Baviera G et al. Randomised clinical trial: the beneficial effects of VSL#3 in obese children withnon-alcoholic steatohepatitis. Aliment. Pharmacol. Ther. 39(11), 1276–1285 (2014).
  Medline CASGoogle Scholar
• 32 Sanchez M, Darimont C, Drapeau V et al. Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women. Br. J. Nutr. 111(8), 1507–1519 (2014).•• Clinical investigation with gender differentiation.
  Medline CASGoogle Scholar
• 33 Zarrati M, Salehi E, Mofid V et al. Relationship between probiotic consumption and IL-10 and IL-17 secreted by PBMCs in overweight and obese people. Iran J. Allergy Asthma Immunol. 12(4), 404–406 (2013).
  Medline CASGoogle Scholar
• 34 Kadooka Y, Sato M, Ogawa A et al. Effect of Lactobacillus gasseri SBT2055 in fermented milk on abdominal adiposity in adults in a randomised controlled trial. Br. J. Nutr. 110(9), 1696–1703 (2013).
  Medline CASGoogle Scholar
• 35 Safavi M, Farajian S, Kelishadi R, Mirlohi M, Hashemipour M. The effects of synbiotic supplementation on some cardio-metabolic risk factors in overweight and obese children: a randomized triple-masked controlled trial. Int. J. Food Sci. Nutr. 64(6), 687–693 (2013).
  Medline CASGoogle Scholar
• 36 Nitert MD, Barrett HL, Foxcroft K et al. SPRING: an RCT study of probiotics in the prevention of gestational diabetes mellitus in overweight and obese women. BMC Pregnancy Childbirth 13, 215158 (2013).
  Google Scholar
• 37 Chorell E, Karlsson Videhult F, Hernell O, Antti H, West CE. Impact of probiotic feeding during weaning on the serum lipid profile and plasma metabolome in infants. Br. J. Nutr. 110(1), 116–126 (2013).
  Medline CASGoogle Scholar
• 38 Leber B, Tripolt NJ, Blattl D et al. The influence of probiotic supplementation on gut permeability in patients with metabolic syndrome: an open label, randomized pilot study. Eur. J. Clin. Nutr. 66(10), 1110–1115 (2012).•• Study addressing the gastrointestinal permeability.
  Medline CASGoogle Scholar
• 39 Gøbel RJ, Larsen N, Jakobsen M, Mølgaard C, Michaelsen KF. Probiotics to adolescents with obesity: effects on inflammation and metabolic syndrome. J. Pediatr. Gastroenterol. Nutr. 55(6), 673–678 (2012).
  MedlineGoogle Scholar
• 40 Mikirova NA, Casciari JJ, Hunninghake RE, Beezley MM. Effect of weight reduction on cardiovascular risk factors and CD34-positive cells in circulation. Int. J. Med. Sci. 8(6), 445–452 (2011).
  Medline CASGoogle Scholar
• 41 Vajro P, Mandato C, Licenziati MR et al. Effects of Lactobacillus rhamnosus strain GG in pediatric obesity-related liver disease. J. Pediatr. Gastroenterol. Nutr. 52(6), 740–743 (2011).•• Clinical investigation made by experts.
  MedlineGoogle Scholar
• 42 Ilmonen J, Isolauri E, Poussa T, Laitinen K. Impact of dietary counselling and probiotic intervention on maternal anthropometric measurements during and after pregnancy: a randomized placebo-controlled trial. Clin. Nutr. 30(2), 156–164 (2011).
  MedlineGoogle Scholar
• 43 Luoto R, Kalliomäki M, Laitinen K, Isolauri E. The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int. J. Obes. (Lond.) 34(10), 1531–1537 (2010).
  CASGoogle Scholar
• 44 Kadooka Y, Sato M, Imaizumi K et al. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur. J. Clin. Nutr. 64(6), 636–643 (2010).
  Medline CASGoogle Scholar
• 45 Luoto R, Laitinen K, Nermes M, Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br. J. Nutr. 103(12), 1792–1799 (2010).
  Medline CASGoogle Scholar
• 46 Woodard GA, Encarnacion B, Downey JR et al. Probiotics improve outcomes after Roux-en-Y gastric bypass surgery: a prospective randomized trial. J. Gastrointest. Surg. 13(7), 1198–1204 (2009).
  MedlineGoogle Scholar
• 47 Agerholm-Larsen L, Raben A, Haulrik N et al. Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur. J. Clin. Nutr. 54(4), 288–297 (2000).
  Medline CASGoogle Scholar
• 48 Amenta M, Cascio MT, Di Fiore P, Venturini I. Diet and chronic constipation. Benefits of oral supplementation with symbiotic zir fos (Bifidobacterium longum W11 + FOS Actilight). Acta Biomed. 77(3), 157–162 (2006).
  MedlineGoogle Scholar
• 49 Huet F, Lachambre E, Beck L, Van Egroo LD, Sznajder M. [Evaluation of a formula with low protein content and supplemented with probiotic agents after breast milk weaning]. Arch. Pediatr. 13(10), 1309–1315 (2006).
  Medline CASGoogle Scholar
• 50 Santacruz A, Marcos A, Wärnberg J et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 17, 1906–1915 (2009).
  MedlineGoogle Scholar
• 51 Osto M, Abegg K, Bueter M, le Roux CW, Cani PD, Lutz TA. Roux-en-Y gastric bypass surgery in rats alters gut microbiota profile along the intestine. Physiol. Behav. 119, 92–96 (2013).
  Medline CASGoogle Scholar
• 52 Hermes GD, Zoetendal EG, Smidt H. Molecular ecological tools to decipher the role of our microbial mass in obesity. Benef. Microbes 6(1), 61–81 (2014).
  Google Scholar
• 53 Martinez-Gonzalez MA, Sayon-Orea C, Ruiz-Canela M, de la Fuente C, Gea A, Bes-Rastrollo M. Yogurt consumption, weight change and risk of overweight/obesity: The SUN cohort study. Nutr. Metab. Cardiovasc. Dis. 24(11), 1189–1196 (2014).
  Medline CASGoogle Scholar
• 54 Jacques PF, Wang H. Yogurt and weight management. Am. J. Clin. Nutr. 99(5), 1229–1234 (2014).
  Google Scholar
• 55 Prentice AM, Jebb SA. Beyond body mass index. Obes. Rev. 2(3), 141–147 (2001).
  Medline CASGoogle Scholar
• 56 Sun Q, van Dam RM, Spiegelman D, Heymsfield SB, Willett WC, Hu FB. Comparison of dual-energy x-ray absorptiometric and anthropometric measures of adiposity in relation to adiposity-related biologic factors. Am. J. Epidemiol. 172(12), 1442–1454 (2010).
  MedlineGoogle Scholar
• 57 Hamdy O, Porramatikul S, Al-Ozairi E. Metabolic obesity: the paradox between visceral and subcutaneous fat. Curr. Diabetes Rev. 2(4), 367–373 (2006).
  MedlineGoogle Scholar
• 58 Pischon T, Boeing H, Hoffmann K et al. General and abdominal adiposity and risk of death in Europe. N. Engl. J. Med. 359(20), 2105–2120 (2008).
  Medline CASGoogle Scholar
• 59 Cerhan JR, Moore SC, Jacobs EJ et al. A pooled analysis of waist circumference and mortality in 650,000 adults. Mayo Clin Proc. 89(3), 335–345 (2014).
  MedlineGoogle Scholar
• 60 Gomes AC, Bueno AA, de Souza RG, Mota JF. Gut microbiota, probiotics and diabetes. Nutr. J. 13, 215158 (2014).
  Google Scholar
• 61 Bolnick DI, Snowberg LK, Hirsch PE et al. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat. Commun. 5, 215158 (2014).
  Google Scholar
• 62 Stenman LK, Waget A, Garret C, Klopp P, Burcelin R, Lahtinen S. Potential probiotic Bifidobacterium animalis ssp. lactis 420 prevents weight gain and glucose intolerance in diet-induced obese mice. Benef. Microbes 1, 215158 (2014).
  Google Scholar
• 63 Hanage WP. Microbiology: microbiome science needs a healthy dose of scepticism. Nature 512(7514), 247–248 (2014).
  Medline CASGoogle Scholar
• 64 Shanahan F. The microbiota in inflammatory bowel disease: friend, bystander, and sometime-villain. Nutr. Rev. 70(1), 31–37 (2012).
  Google Scholar
• 65 Iacono A, Raso GM, Canani RB, Calignano A, Meli R. Probiotics as an emerging therapeutic strategy to treat NAFLD: focus on molecular and biochemical mechanisms. J. Nutr. Biochem. 22(8), 699–711 (2011).
  Medline CASGoogle Scholar
• 66 Eslamparast T, Eghtesad S, Hekmatdoost A, Poustchi H. Probiotics and nonalcoholic fatty liver disease. Middle East J. Dig. Dis. 5(3), m129–m136 (2013).
  MedlineGoogle Scholar
• 67 Tuohy KM, Probert HM, Smejkal CW, Gibson GR. Using probiotics and prebiotico to improve gut health. Drug Discov. Today 8(15), 692–700 (2003).
  MedlineGoogle Scholar
• 68 Sánchez de Medina F, Romero-Calvo I, Mascaraque C, Martínez-Augustin O. Intestinal inflammation and mucosal barrier function. Inflamm. Bowel Dis. 20(12), 2394–2404 (2014).
  MedlineGoogle Scholar