Gut microbiome composition in lean patients with NASH is associated with liver damage independent of caloric intake: A prospective pilot study

Nutrition, Metabolism and Cardiovascular Diseases

Volumn 28, Issue 4, 2018, Pages 369-384

  Duarte, S M B ^a   Stefano, J T ^a   Miele, L ^b   Ponziani, F R ^b   Souza Basqueira, M ^a   Okada, L S R R ^a   de Barros Costa, F G ^a   Toda, K ^a   Mazo, D F C ^a   Sabino, E C ^a   Carrilho, F J ^a   Gasbarrini, A ^b   Oliveira, C P ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b CATHOLIC UNIVERSITY   (Italy)

Author keywords

Gut microbiome; Lean; NASH; Obese; Overweight

Indexed keywords

LIPOPOLYSACCHARIDE; RNA 16S;

ADULT; ALCOHOL CONSUMPTION; ARTICLE; BIFIDOBACTERIUM; BIOPSY; CALORIC INTAKE; CROSS-SECTIONAL STUDY; DNA EXTRACTION; DRUG DEPENDENCE; FAECALIBACTERIUM; FECES ANALYSIS; FEMALE; FOOD INTAKE; GENE AMPLIFICATION; HEMOCHROMATOSIS; HEPATITIS B; HEPATITIS C; HUMAN; HUMAN TISSUE; INTESTINE FLORA; LABORATORY TEST; LACTOBACILLUS; LEAN BODY WEIGHT; LIPID DIET; LIVER FIBROSIS; LIVER INJURY; MACRONUTRIENT; MAJOR CLINICAL STUDY; MALE; MICROBIOME; NONALCOHOLIC FATTY LIVER; NORMAL HUMAN; OBESITY; PHYSICAL EXAMINATION; PILOT STUDY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; PYROSEQUENCING; QUESTIONNAIRE; RUMINOCOCCUS; SCHISTOSOMIASIS; BACTERIUM; BODY MASS; CASE CONTROL STUDY; CLASSIFICATION; COMPARATIVE STUDY; DYSBIOSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; LIVER CIRRHOSIS; MICROBIOLOGY; MIDDLE AGED; PATHOLOGY; PRELIMINARY DATA; RIBOTYPING; RISK FACTOR; YOUNG ADULT;

ADULT; BACTERIA; BIOPSY; BODY MASS INDEX; CASE-CONTROL STUDIES; DYSBIOSIS; ENERGY INTAKE; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; LIVER; LIVER CIRRHOSIS; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; PILOT PROJECTS; PRELIMINARY DATA; PROSPECTIVE STUDIES; RIBOTYPING; RISK FACTORS; YOUNG ADULT;

EID: 85042355265     PISSN: 09394753     EISSN: 15903729     Source Type: Journal    
DOI: 10.1016/j.numecd.2017.10.014     Document Type: Article

References (44)

1. Miquel, S., Leclerc, M., Martin, R., Chain, F., Lenoir, M., Raguideau, S., et al. Identification of metabolic signatures linked to anti-inflammatory effects of Faecalibacterium prausnitzii. MBio, 6, 2015.
2. Loomba, R., Sanyal, A.J., The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol 10 (2013), 686–690.
3. Wong, R.J., Cheung, R., Ahmed, A., Nonalcoholic steatohepatitis is the most rapidly growing indication for liver transplantation in patients with hepatocellular carcinoma in the U.S. Hepatology 59 (2014), 2188–2195.
4. Manti, S., Romano, C., Chirico, V., Filippelli, M., Cuppari, C., Loddo, I., et al. Nonalcoholic Fatty liver disease/non-alcoholic steatohepatitis in childhood: endocrine-metabolic “mal-programming. Hepat Mon, 14, 2014, e17641.
5. Basaranoglu, M., Basaranoglu, G., Sentürk, H., From fatty liver to fibrosis: a tale of “second hit. World J Gastroenterol 19 (2013), 1158–1165.
6. Mosca, A., Nobili, V., De Vito, R., Crudele, A., Scorletti, E., Villani, A., et al. Serum uric acid concentrations and fructose consumption are independently associated with NASH in children and adolescents. J Hepatol 66:5 (2017), 1031–1036.
7. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., et al. A core gut microbiome in obese and lean twins. Nature 457 (2009), 480–484.
8. Turnbaugh, P., Ley, R., Mahowald, M., Magrini, V., Mardis, E., Gordon, J., An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1031.
9. Murphy, E.F., Cotter, P.D., Hogan, A., O'Sullivan, O., Joyce, A., Fouhy, F., et al. Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity. Gut 62 (2013), 220–226.
10. Vrieze, A., Van Nood, E., Holleman, F., Salojärvi, J., Kootte, R.S., Bartelsman, J.F., et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology, 143, 2012 913–916.e917.
11. Larsen, N., Vogensen, F.K., van den Berg, F.W., Nielsen, D.S., Andreasen, A.S., Pedersen, B.K., et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One, 5, 2010, e9085.
12. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
13. Schnabl, B., Brenner, D.A., Interactions between the intestinal microbiome and liver diseases. Gastroenterology 146 (2014), 1513–1524.
14. Boursier, J., Diehl, A.M., Nonalcoholic fatty liver disease and the gut microbiome. Clin Liver Dis 20 (2016), 263–275.
15. Zhu, L., Baker, S.S., Gill, C., Liu, W., Alkhouri, R., Baker, R.D., et al. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57 (2013), 601–609.
16. Betrapally, N.S., Gillevet, P.M., Bajaj, J.S., Changes in the intestinal microbiome and alcoholic and nonalcoholic liver diseases: causes or effects?. Gastroenterology, 150, 2016 1745–1755.e1743.
17. Machado, M.V., Cortez-Pinto, H., Diet, microbiota, obesity, and NAFLD: a dangerous quartet. Int J Mol Sci, 17, 2016, 481.
18. Boursier, J., Mueller, O., Barret, M., Machado, M., Fizanne, L., Araujo-Perez, F., et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 63 (2016), 764–775.
19. Sreenivasa Baba, C., Alexander, G., Kalyani, B., Pandey, R., Rastogi, S., Pandey, A., et al. Effect of exercise and dietary modification on serum aminotransferase levels in patients with nonalcoholic steatohepatitis. J Gastroenterol Hepatol 21 (2006), 191–198.
20. Margariti, E., Deutsch, M., Manolakopoulos, S., Papatheodoridis, G.V., Non-alcoholic fatty liver disease may develop in individuals with normal body mass index. Ann Gastroenterol 25 (2012), 45–51.
21. Neuschwander-Tetri, B.A., Caldwell, S.H., Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology 37 (2003), 1202–1219.
22. Bellentani, S., Dalle Grave, R., Suppini, A., Marchesini, G., Network, F.L.I., Behavior therapy for nonalcoholic fatty liver disease: the need for a multidisciplinary approach. Hepatology 47 (2008), 746–754.
23. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (2010), 335–336.
24. Raman, M., Ahmed, I., Gillevet, P.M., Probert, C.S., Ratcliffe, N.M., Smith, S., et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol, 11, 2013 868–875.e861-863.
25. Wong, V.W., Tse, C.H., Lam, T.T., Wong, G.L., Chim, A.M., Chu, W.C., et al. Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis–a longitudinal study. PLoS One, 8, 2013, e62885.
26. Jiang, W., Wu, N., Wang, X., Chi, Y., Zhang, Y., Qiu, X., et al. Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease. Sci Rep, 5, 2015, 8096.
27. Scott, K.P., Martin, J.C., Duncan, S.H., Flint, H.J., Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol Ecol 87 (2014), 30–40.
28. Prorok-Hamon, M., Friswell, M.K., Alswied, A., Roberts, C.L., Song, F., Flanagan, P.K., et al. Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut 63 (2014), 761–770.
29. Al-Jashamy, K., Murad, A., Zeehaida, M., Rohaini, M., Hasnan, J., Prevalence of colorectal cancer associated with Streptococcus bovis among inflammatory bowel and chronic gastrointestinal tract disease patients. Asian Pac J Cancer Prev 11 (2010), 1765–1768.
30. Leung, C., Rivera, L., Furness, J.B., Angus, P.W., The role of the gut microbiota in NAFLD. Nat Rev Gastroenterol Hepatol 13 (2016), 412–425.
31. Brahe, L.K., Astrup, A., Larsen, L.H., Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases?. Obes Rev 14 (2013), 950–959.
32. Duncan, S.H., Louis, P., Thomson, J.M., Flint, H.J., The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol 11 (2009), 2112–2122.
33. Jumpertz, R., Le, D.S., Turnbaugh, P.J., Trinidad, C., Bogardus, C., Gordon, J.I., et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr 94 (2011), 58–65.
34. Sheng, L., Jena, P.K., Liu, H.X., Kalanetra, K.M., Gonzalez, F.J., French, S.W., et al. Gender differences in bile acids and microbiota in relationship with gender dissimilarity in steatosis induced by diet and FXR inactivation. Sci Rep, 7, 2017, 1748.
35. Trottier, J., Caron, P., Straka, R.J., Barbier, O., Profile of serum bile acids in noncholestatic volunteers: gender-related differences in response to fenofibrate. Clin Pharmacol Ther 90 (2011), 279–286.
36. Org, E., Mehrabian, M., Parks, B.W., Shipkova, P., Liu, X., Drake, T.A., et al. Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes 7 (2016), 313–322.
37. Del Chierico, F., Nobili, V., Vernocchi, P., Russo, A., De Stefanis, C., Gnani, D., et al. Gut microbiota profiling of pediatric NAFLD and obese patients unveiled by an integrated meta-omics based approach. Hepatology 65:2 (2017), 451–464.
38. Savard, C., Tartaglione, E.V., Kuver, R., Haigh, W.G., Farrell, G.C., Subramanian, S., et al. Synergistic interaction of dietary cholesterol and dietary fat in inducing experimental steatohepatitis. Hepatology 57 (2013), 81–92.
39. de Wit, N., Derrien, M., Bosch-Vermeulen, H., Oosterink, E., Keshtkar, S., Duval, C., et al. Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine. Am J Physiol Gastrointest Liver Physiol 303 (2012), G589–G599.
40. Lin, H., An, Y., Hao, F., Wang, Y., Tang, H., Correlations of fecal metabonomic and microbiomic changes induced by high-fat diet in the pre-obesity state. Sci Rep, 6, 2016, 21618.
41. Cani, P.D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A.M., Delzenne, N.M., et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57 (2008), 1470–1481.
42. Wiseman, M., The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc 67 (2008), 253–256.
43. 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 444 (2006), 1027–1031.
44. Macfarlane, G.T., Macfarlane, S., Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. J Clin Gastroenterol, 45, 2011 Suppl:S120-127.