Non-alcoholic fatty liver disease and obesity: the role of the gut bacteria

1.

World Health Organization (2009) Global health risks: mortality and burden of disease attributable to selected major risks. World Health Organization, Geneva

2.

Clinical Guidelines on the Identification (1998) Evaluation, and treatment of overweight and obesity in adults—the evidence report. Natl Inst Health Obes Res 6(Suppl 2):51S–209S

3.

Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH (2009) The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health 9:88. https://doi.org/10.1186/1471-2458-9-88 CrossRefPubMedPubMedCentral

4.

Pratt LA, Brody DJ (2014) Depression and obesity in the US adult household population, 2005–2010. NCHS Data Brief (167):1–8

5.

Bashiardes S, Shapiro H, Rozin S, Shibolet O, Elinav E (2016) Non-alcoholic fatty liver and the gut microbiota. Mol Metab 5(9):782–794. https://doi.org/10.1016/j.molmet.2016.06.003 CrossRefPubMedPubMedCentral

6.

Lau DC, Douketis JD, Morrison KM, Hramiak IM, Sharma AM, Ur E, Obesity Canada Clinical Practice Guidelines Expert P (2007) 2006 Canadian clinical practice guidelines on the management and prevention of obesity in adults and children [summary]. CMAJ 176 (8):S1-13. https://doi.org/10.1503/cmaj.061409 CrossRefPubMed

7.

Diamant A, Cleghorn MC, Milner J, Sockalingam S, Okrainec A, Jackson TD, Quereshy FA (2015) Patient and operational factors affecting wait times in a bariatric surgery program in Toronto: a retrospective cohort study. CMAJ Open 3(3):E331–E337. https://doi.org/10.9778/cmajo.20150020 CrossRefPubMedPubMedCentral

8.

Canadian Institue for Health Information (2014) Bariatric Surgery in Canada. CIHI, Ottawa

9.

Pitzul KB, Jackson T, Crawford S, Kwong JC, Sockalingam S, Hawa R, Urbach D, Okrainec A (2014) Understanding disposition after referral for bariatric surgery: when and why patients referred do not undergo surgery. Obes Surg 24(1):134–140. https://doi.org/10.1007/s11695-013-1083-z CrossRefPubMed

10.

Courcoulas AP, Christian NJ, Belle SH, Berk PD, Flum DR, Garcia L, Horlick M, Kalarchian MA, King WC, Mitchell JE, Patterson EJ, Pender JR, Pomp A, Pories WJ, Thirlby RC, Yanovski SZ, Wolfe BM, Longitudinal Assessment of Bariatric Surgery C (2013) Weight change and health outcomes at 3 years after bariatric surgery among individuals with severe obesity. JAMA 310(22):2416–2425. https://doi.org/10.1001/jama.2013.280928 CrossRefPubMedPubMedCentral

11.

Chang SH, Stoll CR, Song J, Varela JE, Eagon CJ, Colditz GA (2014) The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surg 149(3):275–287. https://doi.org/10.1001/jamasurg.2013.3654 CrossRefPubMedPubMedCentral

12.

Clark JM, Diehl AM (2002) Hepatic steatosis and type 2 diabetes mellitus. Curr Diabetes Rep 2(3):210–215CrossRef

13.

Bedogni G, Miglioli L, Masutti F, Tiribelli C, Marchesini G, Bellentani S (2005) Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos nutrition and liver study. Hepatology 42(1):44–52. https://doi.org/10.1002/hep.20734 CrossRefPubMed

14.

Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, Hobbs HH (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40(6):1387–1395. https://doi.org/10.1002/hep.20466 CrossRefPubMed

15.

Vernon G, Baranova A, Younossi ZM (2011) Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 34(3):274–285. https://doi.org/10.1111/j.1365-2036.2011.04724.x CrossRefPubMed

16.

Targher G, Bertolini L, Padovani R, Rodella S, Tessari R, Zenari L, Day C, Arcaro G (2007) Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes care 30(5):1212–1218. https://doi.org/10.2337/dc06-2247 CrossRefPubMed

17.

Matteoni CA, Younossi ZM, Gramlich T, Liu NB, McCullough YC AJ (1999) Nonalcoholic FATTY LIVER DISEASE: A SPECTRUM OF CLINICAL AND PATHOLOGICAL SEverity. Gastroenterology 116(6):1413–1419CrossRefPubMed

18.

Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, Natale S, Vanni E, Villanova N, Melchionda N, Rizzetto M (2003) Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37(4):917–923. https://doi.org/10.1053/jhep.2003.50161 CrossRefPubMed

19.

Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr, International Diabetes Federation Task Force on E, Prevention, Hational Heart L, Blood I, American Heart A, World Heart F, International Atherosclerosis S, International Association for the Study of O (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120 (16):1640–1645. https://doi.org/10.1161/CIRCULATIONAHA.109.192644 CrossRefPubMed

20.

Machado M, Marques-Vidal P, Cortez-Pinto H (2006) Hepatic histology in obese patients undergoing bariatric surgery. J Hepatol 45(4):600–606. https://doi.org/10.1016/j.jhep.2006.06.013 CrossRefPubMed

21.

McGarry JD, Foster DW (1980) Regulation of hepatic fatty acid oxidation and ketone body production. Ann Rev Biochem 49:395–420. https://doi.org/10.1146/annurev.bi.49.070180.002143 CrossRefPubMed

22.

Bugianesi E, Marchesini G, Gentilcore E, Cua IH, Vanni E, Rizzetto M, George J (2006) Fibrosis in genotype 3 chronic hepatitis C and nonalcoholic fatty liver disease: role of insulin resistance and hepatic steatosis. Hepatology 44(6):1648–1655. https://doi.org/10.1002/hep.21429 CrossRefPubMed

23.

Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ (2005) Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 115(5):1343–1351. https://doi.org/10.1172/jci200523621 CrossRefPubMedPubMedCentral

24.

Schreuder TC, Verwer BJ, van Nieuwkerk CM, Mulder CJ (2008) Nonalcoholic fatty liver disease: an overview of current insights in pathogenesis, diagnosis and treatment. World J Gastroenterol WJG 14(16):2474–2486CrossRefPubMed

25.

Petta S, Muratore C, Craxi A (2009) Non-alcoholic fatty liver disease pathogenesis: the present and the future. Dig Liver Dis (9):615–625. https://doi.org/10.1016/j.dld.2009.01.004

26.

Jacobs RL, Lingrell S, Zhao Y, Francis GA, Vance DE (2008) Hepatic CTP: phosphocholine cytidylyltransferase-alpha is a critical predictor of plasma high density lipoprotein and very low density lipoprotein. J Biol Chem 283(4):2147–2155. https://doi.org/10.1074/jbc.M706628200 CrossRefPubMed

27.

Dowman JK, Tomlinson JW, Newsome PN (2010) Pathogenesis of non-alcoholic fatty liver disease. QJM Mon J Assoc Physicians 103(2):71–83. https://doi.org/10.1093/qjmed/hcp158 CrossRef

28.

Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444(7121):860–867. https://doi.org/10.1038/nature05485 CrossRefPubMed

29.

Ribeiro PS, Cortez-Pinto H, Sola S, Castro RE, Ramalho RM, Baptista A, Moura MC, Camilo ME, Rodrigues CM (2004) Hepatocyte apoptosis, expression of death receptors, and activation of NF-kappaB in the liver of nonalcoholic and alcoholic steatohepatitis patients. Am J Gastroenterol 99(9):1708–1717. https://doi.org/10.1111/j.1572-0241.2004.40009.x CrossRefPubMed

30.

Cortez-Pinto H, de Moura MC, Day CP (2006) Non-alcoholic steatohepatitis: from cell biology to clinical practice. J Hepatol 44(1):197–208. https://doi.org/10.1016/j.jhep.2005.09.002 CrossRefPubMed

31.

Klover PJ, Zimmers TA, Koniaris LG, Mooney RA (2003) Chronic exposure to interleukin-6 causes hepatic insulin resistance in mice. Diabetes 52(11):2784–2789CrossRefPubMed

32.

Crespo J, Cayon A, Fernandez-Gil P, Hernandez-Guerra M, Mayorga M, Dominguez-Diez A, Fernandez-Escalante JC, Pons-Romero F (2001) Gene expression of tumor necrosis factor alpha and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients. Hepatology 34(6):1158–1163. https://doi.org/10.1053/jhep.2001.29628 CrossRefPubMed

33.

Gregor MF, Hotamisligil GS (2007) Thematic review series: adipocyte biology. adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48(9):1905–1914. https://doi.org/10.1194/jlr.R700007-JLR200 CrossRefPubMed

34.

Mancuso P (2016) The role of adipokinesis in chronic inflammation. Immuno Targets Ther 5:47–56. https://doi.org/10.2147/ITT.S73223 CrossRef

35.

Berg AH, Combs TP, Scherer PE (2002) ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Meta 13(2):84–89CrossRef

36.

Widhalm K, Ghods E (2010) Nonalcoholic fatty liver disease: a challenge for pediatricians. Int J Obesity 34(10):1451–1467. https://doi.org/10.1038/ijo.2010.185 CrossRef

37.

Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, Faga E, Silli B, Pagano G (2003) Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology 37(4):909–916. https://doi.org/10.1053/jhep.2003.50132 CrossRefPubMed

38.

da Silva DD, Silva E, Carvalho F, Carmo H (2014) Mixtures of 3,4-methylenedioxymethamphetamine (ecstasy) and its major human metabolites act additively to induce significant toxicity to liver cells when combined at low, non-cytotoxic concentrations. J Appl Toxicol 34(6):618–627. https://doi.org/10.1002/jat.2885 CrossRefPubMed

39.

Solga S, Alkhuraishe AR, Clark JM, Torbenson M, Greenwald A, Diehl AM, Magnuson T (2004) Dietary composition and nonalcoholic fatty liver disease. Dig Dis Sci 49(10):1578–1583CrossRefPubMed

40.

Vos MB, Lavine JE (2013) Dietary fructose in nonalcoholic fatty liver disease. Hepatology 57(6):2525–2531. https://doi.org/10.1002/hep.26299 CrossRefPubMed

41.

Pollock NK, Bundy V, Kanto W, Davis CL, Bernard PJ, Zhu H, Gutin B, Dong Y (2012) Greater fructose consumption is associated with cardiometabolic risk markers and visceral adiposity in adolescents. J Nutr 142(2):251–257. https://doi.org/10.3945/jn.111.150219 CrossRefPubMed

42.

Le KA, Faeh D, Stettler R, Ith M, Kreis R, Vermathen P, Boesch C, Ravussin E, Tappy L (2006) A 4-week high-fructose diet alters lipid metabolism without affecting insulin sensitivity or ectopic lipids in healthy humans. Am J Clin Nutr 84(6):1374–1379CrossRefPubMed

43.

Kalliomaki M, Collado MC, Salminen S, Isolauri E (2008) Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr 87(3):534–538CrossRefPubMed

44.

Conterno L, Fava F, Viola R, Tuohy KM (2011) Obesity and the gut microbiota: does up-regulating colonic fermentation protect against obesity and metabolic disease? Genes Nutr 6(3):241–260. https://doi.org/10.1007/s12263-011-0230-1 CrossRefPubMedPubMedCentral

45.

Cani PD, Delzenne NM (2009) The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Design 15(13):1546–1558CrossRef

46.

Duseja A, Chawla YK (2014) Obesity and NAFLD: the role of bacteria and microbiota. Clin Liver Dis 18(1):59–71. https://doi.org/10.1016/j.cld.2013.09.002 CrossRefPubMed

47.

Dore J, Simren M, Buttle L, Guarner F (2013) Hot topics in gut microbiota. United Eur Gastroenterol J 1(5):311–318. https://doi.org/10.1177/2050640613502477 CrossRef

48.

Simren M, Barbara G, Flint HJ, Spiegel BM, Spiller RC, Vanner S, Verdu EF, Whorwell PJ, Zoetendal EG, Rome Foundation C (2013) Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut 62(1):159–176. https://doi.org/10.1136/gutjnl-2012-302167 CrossRefPubMed

49.

Mai V, Draganov PV (2009) Recent advances and remaining gaps in our knowledge of associations between gut microbiota and human health. World J Gastroenterol 15(1):81–85CrossRefPubMedPubMedCentral

50.

Bosscher D, Breynaert A, Pieters L, Hermans N (2009) Food-based strategies to modulate the composition of the intestinal microbiota and their associated health effects. J Physiol Pharmacol 60 Suppl 6:5–11PubMed

51.

Othman M, Aguero R, Lin HC (2008) Alterations in intestinal microbial flora and human disease. Curr Opin Gastroenterol 24(1):11–16. https://doi.org/10.1097/MOG.0b013e3282f2b0d7 CrossRefPubMed

52.

Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1241214. https://doi.org/10.1126/science.1241214 CrossRefPubMed

53.

Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM (2013) Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Trans Med 5(178):178ra141. https://doi.org/10.1126/scitranslmed.3005687 CrossRef

54.

Gao R, Zhu C, Li H, Yin M, Pan C, Huang L, Kong C, Wang X, Zhang Y, Qu S, Qin H (2018) Dysbiosis signatures of gut microbiota along the sequence from healthy, young patients to those with overweight and obesity. Obesity 26(2):351–361. https://doi.org/10.1002/oby.22088 CrossRefPubMed

55.

Liu R, Hong J, Xu X, Feng Q, Zhang D, Gu Y, Shi J, Zhao S, Liu W, Wang X, Xia H, Liu Z, Cui B, Liang P, Xi L, Jin J, Ying X, Wang X, Zhao X, Li W, Jia H, Lan Z, Li F, Wang R, Sun Y, Yang M, Shen Y, Jie Z, Li J, Chen X, Zhong H, Xie H, Zhang Y, Gu W, Deng X, Shen B, Xu X, Yang H, Xu G, Bi Y, Lai S, Wang J, Qi L, Madsen L, Wang J, Ning G, Kristiansen K, Wang W (2017) Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nature medicine 23(7):859–868. https://doi.org/10.1038/nm.4358 CrossRefPubMed

56.

Armougom F, Henry M, Vialettes B, Raccah D, Raoult D (2009) Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PloS one 4(9):e7125. https://doi.org/10.1371/journal.pone.0007125 CrossRefPubMedPubMedCentral

57.

Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023. https://doi.org/10.1038/4441022a CrossRefPubMed

58.

Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, Hardt PD (2010) Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18(1):190–195. https://doi.org/10.1038/oby.2009.167 CrossRefPubMed

59.

Henao-Mejia J, Elinav E, Thaiss CA, Flavell RA (2013) The intestinal microbiota in chronic liver disease. Adv Immunol 117:73–97. https://doi.org/10.1016/B978-0-12-410524-9.00003-7 CrossRefPubMed

60.

Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal WZ, Strowig T, Thaiss CA, Kau AL, Eisenbarth SC, Jurczak MJ, Camporez JP, Shulman GI, Gordon JI, Hoffman HM, Flavell RA (2012) Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482(7384):179–185. https://doi.org/10.1038/nature10809 CrossRefPubMedPubMedCentral

61.

Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A, Perlemuter G, Cassard-Doulcier AM, Gerard P (2013) Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62(12):1787–1794. https://doi.org/10.1136/gutjnl-2012-303816 CrossRefPubMed

62.

Rabot S, Membrez M, Bruneau A, Gerard P, Harach T, Moser M, Raymond F, Mansourian R, Chou CJ (2010) Germ-free C57BL/6J mice are resistant to high-fat-diet-induced insulin resistance and have altered cholesterol metabolism. FASEB J 24(12):4948–4959. https://doi.org/10.1096/fj.10-164921 CrossRefPubMed

63.

Spencer MD, Hamp TJ, Reid RW, Fischer LM, Zeisel SH, Fodor AA (2011) Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology 140(3):976–986. https://doi.org/10.1053/j.gastro.2010.11.049 CrossRefPubMed

64.

Raman M, Ahmed I, Gillevet PM, Probert CS, Ratcliffe NM, Smith S, Greenwood R, Sikaroodi M, Lam V, Crotty P, Bailey J, Myers RP, Rioux KP (2013) Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 11(7):868–875 e861–863. https://doi.org/10.1016/j.cgh.2013.02.015 CrossRefPubMed

65.

Mouzaki M, Comelli EM, Arendt BM, Bonengel J, Fung SK, Fischer SE, McGilvray ID, Allard JP (2013) Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology 58(1):120–127. https://doi.org/10.1002/hep.26319 CrossRefPubMed

66.

Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, Baker RD, Gill SR (2013) Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57(2):601–609. https://doi.org/10.1002/hep.26093 CrossRefPubMed

67.

Michail S, Lin M, Frey MR, Fanter R, Paliy O, Hilbush B, Reo NV (2015) Altered gut microbial energy and metabolism in children with non-alcoholic fatty liver disease. FEMS Microbiol Ecol 91(2):1–9. https://doi.org/10.1093/femsec/fiu002 CrossRefPubMed

68.

Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, Guy CD, Seed PC, Rawls JF, David LA, Hunault G, Oberti F, Cales P, Diehl AM (2016) The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 63(3):764–775. https://doi.org/10.1002/hep.28356 CrossRefPubMed

69.

Da Silva HE, Teterina A, Comelli EM, Taibi A, Arendt BM, Fischer SE, Lou W, Allard JP (2018) Nonalcoholic fatty liver disease is associated with dysbiosis independent of body mass index and insulin resistance. Sci Rep 8(1):1466. https://doi.org/10.1038/s41598-018-19753-9 CrossRefPubMedPubMedCentral

70.

Duarte SMB, Stefano JT, Miele L, Ponziani FR, Souza-Basqueira M, Okada L, de Barros Costa FG, Toda K, Mazo DFC, Sabino EC, Carrilho FJ, Gasbarrini A, Oliveira CP (2018) Gut microbiome composition in lean patients with NASH is associated with liver damage independent of caloric intake: a prospective pilot study. Nutr Metab Cardiovasc Dis 28(4):369–384. https://doi.org/10.1016/j.numecd.2017.10.014 CrossRefPubMed

71.

Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101(44):15718–15723. https://doi.org/10.1073/pnas.0407076101 CrossRefPubMedPubMedCentral

72.

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031. https://doi.org/10.1038/nature05414 CrossRefPubMed

73.

Backhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104(3):979–984. https://doi.org/10.1073/pnas.0605374104 CrossRefPubMedPubMedCentral

74.

Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27(2):104–119. https://doi.org/10.1111/j.1365-2036.2007.03562.x CrossRefPubMed

75.

De Vuyst L, Leroy F (2011) Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifdobacterial competitiveness, butyrate production, and gas production. Int J Food Microbiol 149(1):73–80. https://doi.org/10.1016/j.ijfoodmicro.2011.03.003 CrossRefPubMed

76.

Lin HV, Frassetto A, Kowalik EJ Jr, Nawrocki AR, Lu MM, Kosinski JR, Hubert JA, Szeto D, Yao X, Forrest G, Marsh DJ (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PloS One 7(4):e35240. https://doi.org/10.1371/journal.pone.0035240 CrossRefPubMedPubMedCentral

77.

Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, Masciana R, Forgione A, Gabrieli ML, Perotti G, Vecchio FM, Rapaccini G, Gasbarrini G, Day CP, Grieco A (2009) Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 49(6):1877–1887. https://doi.org/10.1002/hep.22848 CrossRefPubMed

78.

Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, Sonnenburg JL (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502(7469):96–99. https://doi.org/10.1038/nature12503 CrossRefPubMedPubMedCentral

79.

Kudo H, Takahara T, Yata Y, Kawai K, Zhang W, Sugiyama T (2009) Lipopolysaccharide triggered TNF-alpha-induced hepatocyte apoptosis in a murine non-alcoholic steatohepatitis model. Journal of hepatology 51(1):168–175. https://doi.org/10.1016/j.jhep.2009.02.032 CrossRefPubMed

80.

Guo S, Al-Sadi R, Said HM, Ma TY (2013) Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am J Pathol 182(2):375–387. https://doi.org/10.1016/j.ajpath.2012.10.014 CrossRefPubMedPubMedCentral

81.

Hatayama H, Iwashita J, Kuwajima A, Abe T (2007) The short chain fatty acid, butyrate, stimulates MUC2 mucin production in the human colon cancer cell line, LS174T. Biochem Biophys Res Commun 356 (3):599–603. https://doi.org/10.1016/j.bbrc.2007.03.025 CrossRefPubMed

82.

Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58(8):1091–1103. https://doi.org/10.1136/gut.2008.165886 CrossRefPubMed

83.

Krueger S, Hundertmark T, Kuester D, Kalinski T, Peitz U, Roessner A (2007) Helicobacter pylori alters the distribution of ZO-1 and p120ctn in primary human gastric epithelial cells. Pathol Res Pract 203(6):433–444. https://doi.org/10.1016/j.prp.2007.04.003 CrossRefPubMed

84.

Gaudier E, Rival M, Buisine MP, Robineau I, Hoebler C (2009) Butyrate enemas upregulate Muc genes expression but decrease adherent mucus thickness in mice colon. Physiol Res Acad Sci Bohemoslovaca 58(1):111–119

85.

Wang HB, Wang PY, Wang X, Wan YL, Liu YC (2012) Butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein Claudin-1 transcription. Dig Dis Sci 57(12):3126–3135. https://doi.org/10.1007/s10620-012-2259-4 CrossRefPubMed

86.

Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, Weir TL, Ehrentraut SF, Pickel C, Kuhn KA, Lanis JM, Nguyen V, Taylor CT, Colgan SP (2015) Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe 17(5):662–671. https://doi.org/10.1016/j.chom.2015.03.005 CrossRefPubMedPubMedCentral

87.

Bomhof MR, Saha DC, Reid DT, Paul HA, Reimer RA (2014) Combined effects of oligofructose and Bifidobacterium animalis on gut microbiota and glycemia in obese rats. Obesity 22(3):763–771. https://doi.org/10.1002/oby.20632 CrossRefPubMed

88.

Brun P, Castagliuolo I, Di Leo V, Buda A, Pinzani M, Palu G, Martines D (2007) Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 292(2):G518–G525. https://doi.org/10.1152/ajpgi.00024.2006 CrossRefPubMed

89.

Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56(7):1761–1772. https://doi.org/10.2337/db06-1491 CrossRefPubMed

90.

Song MJ, Kim KH, Yoon JM, Kim JB (2006) Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Biochem Biophys Res Commun 346(3):739–745. https://doi.org/10.1016/j.bbrc.2006.05.170 CrossRefPubMed

91.

Harte AL, da Silva NF, Creely SJ, McGee KC, Billyard T, Youssef-Elabd EM, Tripathi G, Ashour E, Abdalla MS, Sharada HM, Amin AI, Burt AD, Kumar S, Day CP, McTernan PG (2010) Elevated endotoxin levels in non-alcoholic fatty liver disease. J Inflamm 7:15. https://doi.org/10.1186/1476-9255-7-15 CrossRef

92.

Thuy S, Ladurner R, Volynets V, Wagner S, Strahl S, Konigsrainer A, Maier KP, Bischoff SC, Bergheim I (2008) Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr 138(8):1452–1455CrossRefPubMed

93.

Volynets V, Kuper MA, Strahl S, Maier IB, Spruss A, Wagnerberger S, Konigsrainer A, Bischoff SC, Bergheim I (2012) Nutrition, intestinal permeability, and blood ethanol levels are altered in patients with nonalcoholic fatty liver disease (NAFLD). Dig Dis Sci 57(7):1932–1941. https://doi.org/10.1007/s10620-012-2112-9 CrossRefPubMed

94.

Alisi A, Manco M, Devito R, Piemonte F, Nobili V (2010) Endotoxin and plasminogen activator inhibitor-1 serum levels associated with nonalcoholic steatohepatitis in children. J Pediatric Gastroenterol Nutr 50(6):645–649. https://doi.org/10.1097/MPG.0b013e3181c7bdf1 CrossRef

95.

Chen X, Zhang C, Zhao M, Shi CE, Zhu RM, Wang H, Zhao H, Wei W, Li JB, Xu DX (2011) Melatonin alleviates lipopolysaccharide-induced hepatic SREBP-1c activation and lipid accumulation in mice. J Pineal Res 51(4):416–425. https://doi.org/10.1111/j.1600-079X.2011.00905.x CrossRefPubMed

96.

Fukunishi S, Sujishi T, Takeshita A, Ohama H, Tsuchimoto Y, Asai A, Tsuda Y, Higuchi K (2014) Lipopolysaccharides accelerate hepatic steatosis in the development of nonalcoholic fatty liver disease in Zucker rats. J Clin Biochem Nutr 54(1):39–44. https://doi.org/10.3164/jcbn.13-49 CrossRefPubMed

97.

Ganz M, Szabo G (2013) Immune and inflammatory pathways in NASH. Hepatol Int 7(Suppl 2):771–781. https://doi.org/10.1007/s12072-013-9468-6 CrossRefPubMed

98.

Aron-Wisnewsky J, Gaborit B, Dutour A, Clement K (2013) Gut microbiota and non-alcoholic fatty liver disease: new insights. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases 19 (4):338–348. https://doi.org/10.1111/1469-0691.12140

99.

Zhang G, Ghosh S (2000) Molecular mechanisms of NF-kappaB activation induced by bacterial lipopolysaccharide through Toll-like receptors. J Endotoxin Res 6(6):453–457CrossRefPubMed

100.

Cani PD, Delzenne NM, Amar J, Burcelin R (2008) Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol Biol 56(5):305–309. https://doi.org/10.1016/j.patbio.2007.09.008 CrossRefPubMed

101.

Ye D, Li FY, Lam KS, Li H, Jia W, Wang Y, Man K, Lo CM, Li X, Xu A (2012) Toll-like receptor-4 mediates obesity-induced non-alcoholic steatohepatitis through activation of X-box binding protein-1 in mice. Gut 61(7):1058–1067. https://doi.org/10.1136/gutjnl-2011-300269 CrossRefPubMed

102.

Poggi M, Bastelica D, Gual P, Iglesias MA, Gremeaux T, Knauf C, Peiretti F, Verdier M, Juhan-Vague I, Tanti JF, Burcelin R, Alessi MC (2007) C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50(6):1267–1276. https://doi.org/10.1007/s00125-007-0654-8 CrossRefPubMed

103.

Saberi M, Woods NB, de Luca C, Schenk S, Lu JC, Bandyopadhyay G, Verma IM, Olefsky JM (2009) Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab 10(5):419–429. https://doi.org/10.1016/j.cmet.2009.09.006 CrossRefPubMedPubMedCentral

104.

Aoyama T, Paik YH, Seki E (2010) Toll-like receptor signaling and liver fibrosis. Gastroenterol Res Pract. https://doi.org/10.1155/2010/192543 CrossRefPubMedPubMedCentral

105.

Paik YH, Schwabe RF, Bataller R, Russo MP, Jobin C, Brenner DA (2003) Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 37(5):1043–1055. https://doi.org/10.1053/jhep.2003.50182 CrossRefPubMed

106.

Sutterwala FS, Ogura Y, Flavell RA (2007) The inflammasome in pathogen recognition and inflammation. J Leukoc Biol 82(2):259–264. https://doi.org/10.1189/jlb.1206755 CrossRefPubMed

107.

Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10(2):417–426CrossRefPubMed

108.

Dixon LJ, Berk M, Thapaliya S, Papouchado BG, Feldstein AE (2012) Caspase-1-mediated regulation of fibrogenesis in diet-induced steatohepatitis. Lab Invest 92(5):713–723. https://doi.org/10.1038/labinvest.2012.45 CrossRefPubMedPubMedCentral

109.

O’Sullivan TA, Oddy WH, Bremner AP, Sherriff JL, Ayonrinde OT, Olynyk JK, Beilin LJ, Mori TA, Adams LA (2014) Lower fructose intake may help protect against development of nonalcoholic fatty liver in adolescents with obesity. J Pediatr Gastroenterol Nutr 58(5):624–631. https://doi.org/10.1097/MPG.0000000000000267 CrossRefPubMed

110.

Moore JB, Gunn PJ, Fielding BA (2014) The role of dietary sugars and de novo lipogenesis in non-alcoholic fatty liver disease. Nutrients 6(12):5679–5703. https://doi.org/10.3390/nu6125679 CrossRefPubMedPubMedCentral

111.

Jin R, Willment A, Patel SS, Sun X, Song M, Mannery YO, Kosters A, McClain CJ, Vos MB (2014) Fructose induced endotoxemia in pediatric nonalcoholic Fatty liver disease. Int J Hepatol 2014:560620. https://doi.org/10.1155/2014/560620 CrossRefPubMedPubMedCentral

112.

Jegatheesan P, Beutheu S, Ventura G, Sarfati G, Nubret E, Kapel N, Waligora-Dupriet AJ, Bergheim I, Cynober L, De-Bandt JP (2016) Effect of specific amino acids on hepatic lipid metabolism in fructose-induced non-alcoholic fatty liver disease. Clin Nutr 35(1):175–182. https://doi.org/10.1016/j.clnu.2015.01.021 CrossRefPubMed

113.

Wagnerberger S, Spruss A, Kanuri G, Volynets V, Stahl C, Bischoff SC, Bergheim I (2012) Toll-like receptors 1–9 are elevated in livers with fructose-induced hepatic steatosis. Br J Nutr 107(12):1727–1738. https://doi.org/10.1017/S0007114511004983 CrossRefPubMed

114.

Arab JP, Candia R, Zapata R, Munoz C, Arancibia JP, Poniachik J, Soza A, Fuster F, Brahm J, Sanhueza E, Contreras J, Cuellar MC, Arrese M, Riquelme A (2014) Management of nonalcoholic fatty liver disease: an evidence-based clinical practice review. World J Gastroenterol 20(34):12182–12201. https://doi.org/10.3748/wjg.v20.i34.12182 CrossRefPubMedPubMedCentral

115.

Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, Harrison SA, Brunt EM, Sanyal AJ (2017) The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the american association for the study of liver diseases. Hepatology. https://doi.org/10.1002/hep.29367 CrossRefPubMed

116.

Nostedt JJ, Switzer NJ, Gill RS, Dang J, Birch DW, de Gara C, Bailey RJ, Karmali S (2016) The effect of bariatric surgery on the spectrum of fatty liver disease. Can J Gastroenterol Hepatol 2016:2059245. https://doi.org/10.1155/2016/2059245

117.

De Ridder RJ, Schoon EJ, Smulders JF, van Hout GC, Stockbrugger RW, Koek GH (2007) Review article: non-alcoholic fatty liver disease in morbidly obese patients and the effect of bariatric surgery. Aliment Pharmacol Ther 26(Suppl 2):195–201. https://doi.org/10.1111/j.1365-2036.2007.03483.x CrossRefPubMed

118.

Hafeez S, Ahmed MH (2013) Bariatric surgery as potential treatment for nonalcoholic fatty liver disease: a future treatment by choice or by chance? J Obes 2013:839275. https://doi.org/10.1155/2013/839275

119.

Lee YM, Low HC, Lim LG, Dan YY, Aung MO, Cheng CL, Wee A, Lim SG, Ho KY (2012) Intragastric balloon significantly improves nonalcoholic fatty liver disease activity score in obese patients with nonalcoholic steatohepatitis: a pilot study. Gastrointest Endosc 76(4):756–760. https://doi.org/10.1016/j.gie.2012.05.023 CrossRefPubMed

120.

Stephen S, Baranova A, Younossi ZM (2012) Nonalcoholic fatty liver disease and bariatric surgery. Expert Rev Gastroenterol Hepatol 6(2):163–171. https://doi.org/10.1586/egh.11.97 CrossRefPubMed

121.

Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106(7):2365–2370. https://doi.org/10.1073/pnas.0812600106 CrossRefPubMedPubMedCentral

122.

Prachand VN, Alverdy JC (2009) The role of malabsorption in bariatric surgery. World J Surg 33(10):1989–1994. https://doi.org/10.1007/s00268-009-0101-8 CrossRefPubMed

123.

Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Dore J, Henegar C, Rizkalla S, Clement K (2010) Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59(12):3049–3057. https://doi.org/10.2337/db10-0253 CrossRefPubMedPubMedCentral

124.

Chavez-Tapia NC, Tellez-Avila FI, Barrientos-Gutierrez T, Mendez-Sanchez N, Lizardi-Cervera J, Uribe M (2010) Bariatric surgery for non-alcoholic steatohepatitis in obese patients. Cochrane Database Syst Rev.1:CD007340. https://doi.org/10.1002/14651858.CD007340.pub2 CrossRef

125.

Albenberg LG, Wu GD (2014) Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 146(6):1564–1572. https://doi.org/10.1053/j.gastro.2014.01.058 CrossRefPubMed

126.

Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, Delzenne NM, Schrenzel J, Francois P, Cani PD (2014) Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J 8(10):2116–2130. https://doi.org/10.1038/ismej.2014.45 CrossRefPubMedPubMedCentral

127.

Barengolts E (2016) Gut microbiota, prebiotics, probiotics, and synbiotics in management of obesity and prediabetes: review of randomized controlled trials. Endocr Pract 22(10):1224–1234. https://doi.org/10.4158/EP151157.RA CrossRefPubMed

128.

Kobyliak N, Abenavoli L, Mykhalchyshyn G, Kononenko L, Boccuto L, Kyriienko D, Dynnyk O (2018) A multi-strain probiotic reduces the fatty liver index, cytokines and aminotransferase levels in nafld patients: evidence from a randomized clinical trial. J Gastrointestin Liver Dis 27(1):41–49. https://doi.org/10.15403/jgld.2014.1121.271.kby CrossRefPubMed

129.

Vajro P, Mandato C, Licenziati MR, Franzese A, Vitale DF, Lenta S, Caropreso M, Vallone G, Meli R (2011) Effects of Lactobacillus rhamnosus strain GG in pediatric obesity-related liver disease. J Pediatr Gastroenterol Nutr 52(6):740–743. https://doi.org/10.1097/MPG.0b013e31821f9b85 CrossRefPubMed

130.

Alisi A, Bedogni G, Baviera G, Giorgio V, Porro E, Paris C, Giammaria P, Reali L, Anania F, Nobili V (2014) Randomised clinical trial: The beneficial effects of VSL#3 in obese children with non-alcoholic steatohepatitis. Aliment Pharmacol Ther 39(11):1276–1285. https://doi.org/10.1111/apt.12758 CrossRefPubMedPubMedCentral

131.

Mofidi F, Poustchi H, Yari Z, Nourinayyer B, Merat S, Sharafkhah M, Malekzadeh R, Hekmatdoost A (2017) Synbiotic supplementation in lean patients with non-alcoholic fatty liver disease: a pilot, randomised, double-blind, placebo-controlled, clinical trial. Br J Nutr 117(5):662–668. https://doi.org/10.1017/S0007114517000204 CrossRefPubMed

132.

Nilsson A, Johansson E, Ekstrom L, Bjorck I (2013) Effects of a brown beans evening meal on metabolic risk markers and appetite regulating hormones at a subsequent standardized breakfast: a randomized cross-over study. PLoS One 8(4):e59985. https://doi.org/10.1371/journal.pone.0059985 CrossRefPubMedPubMedCentral

133.

Smith TJ, Anderson D, Margolis LM, Sikes A, Young AJ (2011) Persistence of Lactobacillus reuteri DSM17938 in the human intestinal tract: response to consecutive and alternate-day supplementation. J Am Coll Nutr 30(4):259–264CrossRefPubMed

134.

Mattner J, Schmidt F, Siegmund B (2016) Faecal microbiota transplantation—a clinical view. Int J Med Microbiol 306(5):310–315. https://doi.org/10.1016/j.ijmm.2016.02.003 CrossRefPubMed

135.

Khanna S (2018) Microbiota replacement therapies: innovation in gastrointestinal care. Clin Pharmacol Ther 103(1):102–111. https://doi.org/10.1002/cpt.923 CrossRefPubMed

136.

Khoruts A, Dicksved J, Jansson JK, Sadowsky MJ (2010) Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea. J Clin Gastroenterol 44(5):354–360. https://doi.org/10.1097/MCG.0b013e3181c87e02 CrossRefPubMed

137.

Colman RJ, Rubin DT (2014) Fecal microbiota transplantation as therapy for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis 8(12):1569–1581. https://doi.org/10.1016/j.crohns.2014.08.006 CrossRefPubMed

138.

Paramsothy S, Paramsothy R, Rubin DT, Kamm MA, Kaakoush NO, Mitchell HM, Castano-Rodriguez N (2017) faecal microbiota transplantation for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis 11(10):1180–1199. https://doi.org/10.1093/ecco-jcc/jjx063 CrossRefPubMed

139.

Halkjaer SI, Boolsen AW, Gunther S, Christensen AH, Petersen AM (2017) Can fecal microbiota transplantation cure irritable bowel syndrome? World J Gastroenterol 23(22):4112–4120. https://doi.org/10.3748/wjg.v23.i22.4112 CrossRefPubMedPubMedCentral

140.

Pinn DM, Aroniadis OC, Brandt LJ (2015) Is fecal microbiota transplantation (FMT) an effective treatment for patients with functional gastrointestinal disorders (FGID)? Neurogastroenterol Motil 27(1):19–29. https://doi.org/10.1111/nmo.12479 CrossRefPubMed

141.

Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, Kheradman R, Heuman D, Wang J, Gurry T, Williams R, Sikaroodi M, Fuchs M, Alm E, John B, Thacker LR, Riva A, Smith M, Taylor-Robinson SD, Gillevet PM (2017) Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology 66(6):1727–1738. https://doi.org/10.1002/hep.29306 CrossRefPubMed

142.

Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143(4):913–916 e917. https://doi.org/10.1053/j.gastro.2012.06.031 CrossRefPubMed

143.

Abdul-Hai A, Abdallah A, Malnick SD (2015) Influence of gut bacteria on development and progression of non-alcoholic fatty liver disease. World J Hepatol 7(12):1679–1684. https://doi.org/10.4254/wjh.v7.i12.1679 CrossRefPubMedPubMedCentral

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Non-alcoholic fatty liver disease and obesity: the role of the gut bacteria

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2019

Еffects of fortified milk on cognitive abilities in school-aged children: results from a randomized-controlled trial

Median urinary iodine concentration reflected sufficient iodine supply in neonates from Northeast Germany in 2005–2006

Association of sugar sweetened beverages consumption with non-alcoholic fatty liver disease: a systematic review and meta-analysis

Individual characteristics associated with changes in the contribution of plant foods to dietary intake in a French prospective cohort