Substitution of One Meat-Based Meal With Vegetarian and Vegan Alternatives Generates Lower Ammonia and Alters Metabolites in Cirrhosis: A Randomized Clinical Trial.
Journal
Clinical and translational gastroenterology
ISSN: 2155-384X
Titre abrégé: Clin Transl Gastroenterol
Pays: United States
ID NLM: 101532142
Informations de publication
Date de publication:
01 Jun 2024
01 Jun 2024
Historique:
received:
07
02
2024
accepted:
22
04
2024
medline:
11
7
2024
pubmed:
11
7
2024
entrez:
10
7
2024
Statut:
epublish
Résumé
Diet can affect ammoniagenesis in cirrhosis and hepatic encephalopathy (HE), but the impact of dietary preferences on metabolomics in cirrhosis is unclear. As most Western populations follow meat-based diets, we aimed to determine the impact of substituting a single meat-based meal with an equal protein-containing vegan/vegetarian alternative on ammonia and metabolomics in outpatients with cirrhosis on a meat-based diet. Outpatients with cirrhosis with and without prior HE on a stable Western meat-based diet were randomized 1:1:1 into 3 groups. Patients were given a burger with 20 g protein of meat, vegan, or vegetarian. Blood for metabolomics via liquid chromatography-mass spectrometry and ammonia was drawn at baseline and hourly for 3 hours after meal while patients under observation. Stool microbiome characteristics, changes in ammonia, and metabolomics were compared between/within groups. Stool microbiome composition was similar at baseline. Serum ammonia increased from baseline in the meat group but not the vegetarian or vegan group. Metabolites of branched chain and acylcarnitines decreased in the meat group compared with the non-meat groups. Alterations in lipid profile (higher sphingomyelins and lower lysophospholipids) were noted in the meat group when compared with the vegan and vegetarian groups. Substitution of a single meat-based meal with a non-meat alternatives results in lower ammoniagenesis and altered serum metabolomics centered on branched-chain amino acids, acylcarnitines, lysophospholipids, and sphingomyelins in patients with cirrhosis regardless of HE or stool microbiome. Intermittent meat substitution with vegan or vegetarian alternatives could be helpful in reducing ammonia generation in cirrhosis.
Identifiants
pubmed: 38986526
doi: 10.14309/ctg.0000000000000707
pii: 01720094-202406000-00006
doi:
Substances chimiques
Ammonia
7664-41-7
acylcarnitine
0
Carnitine
S7UI8SM58A
Amino Acids, Branched-Chain
0
Types de publication
Journal Article
Randomized Controlled Trial
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1Subventions
Organisme : U.S. Department of Veterans Affairs, American College of Gastroenterology
ID : 1I01CX002472, 2I01CX001076
Informations de copyright
Copyright © 2024 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of The American College of Gastroenterology.
Références
Bustamante J, Rimola A, Ventura PJ, et al. Prognostic significance of hepatic encephalopathy in patients with cirrhosis. J Hepatol 1999;30:890–5.
Tapper EB, Halbert B, Mellinger J. Rates of and reasons for hospital readmissions in patients with cirrhosis: A multistate population-based cohort study. Clin Gastroenterol Hepatol 2016;14(8):1181–8.e2.
Kang DJ, Betrapally NS, Ghosh SA, et al. Gut microbiota drive the development of neuroinflammatory response in cirrhosis in mice. Hepatology 2016;64(4):1232–48.
Shawcross DL, Thabut D, Amodio P. Ammonia–an enduring foe–What evaluating whole body ammonia metabolism can teach us about cirrhosis and therapies treating hepatic encephalopathy. J Hepatol 2023;79(2):266–8.
Eriksen PL, Djernes L, Vilstrup H, et al. Clearance and production of ammonia quantified in humans by constant ammonia infusion–the effects of cirrhosis and ammonia-targeting treatments. J Hepatol 2023;79(2):340–8.
Ballester MP, Tranah TH, Balcar L, et al. Development and validation of the AMMON-OHE model to predict risk of overt hepatic encephalopathy occurrence in outpatients with cirrhosis. J Hepatol 2023;79(4):967–76.
Tranah TH, Ballester MP, Carbonell-Asins JA, et al. Plasma ammonia levels predict hospitalisation with liver-related complications and mortality in clinically stable outpatients with cirrhosis. J Hepatol 2022;77(6):1554–63.
Kachaamy T, Bajaj JS. Diet and cognition in chronic liver disease. Curr Opin Gastroenterol 2011;27(2):174–9.
Amodio P, Bemeur C, Butterworth R, et al. The nutritional management of hepatic encephalopathy in patients with cirrhosis: International society for hepatic encephalopathy and nitrogen metabolism consensus. Hepatology 2013;58(1):325–36.
Bianchi GP, Marchesini G, Fabbri A, et al. Vegetable versus animal protein diet in cirrhotic patients with chronic encephalopathy. A randomized cross-over comparison. J Intern Med 1993;233(5):385–92.
Ashton LM, Sharkey T, Whatnall MC, et al. Effectiveness of interventions and behaviour change techniques for improving dietary intake in young adults: A systematic review and meta-analysis of RCTs. Nutrients 2019;11(4):825.
Bajaj JS, Bloom PP, Chung RT, et al. Variability and lability of ammonia levels in healthy volunteers and patients with cirrhosis: Implications for trial design and clinical practice. Am J Gastroenterol 2020;115(5):783–5.
Bajaj JS, Betrapally NS, Hylemon PB, et al. Salivary microbiota reflects changes in gut microbiota in cirrhosis with hepatic encephalopathy. Hepatology 2015;62(4):1260–71.
Gedgaudas R, Bajaj JS, Skieceviciene J, et al. Circulating microbiome in patients with portal hypertension. Gut Microbes 2022;14(1):2029674.
Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12(6):R60.
Bajaj JS, Tandon P, O'Leary JG, et al. Admission serum metabolites and thyroxine predict advanced hepatic encephalopathy in a multi-center inpatient cirrhosis cohort. Clin Gastroenterol Hepatol 2022.
Uribe M, Marquez MA, Garcia Ramos G, et al. Treatment of chronic portal-systemic encephalopathy with vegetable and animal protein diets. A controlled crossover study. Dig Dis Sci. 1982;27(12):1109–16.
de Bruijn KM, Blendis LM, Zilm DH, et al. Effect of dietary protein manipulation in subclinical portal-systemic encephalopathy. Gut 1983;24(1):53–60.
Daftari G, Tehrani AN, Pashayee-Khamene F, et al. Dietary protein intake and mortality among survivors of liver cirrhosis: A prospective cohort study. BMC Gastroenterol 2023;23(1):227.
Gluud LL, Dam G, Borre M, et al. Oral branched-chain amino acids have a beneficial effect on manifestations of hepatic encephalopathy in a systematic review with meta-analyses of randomized controlled trials. J Nutr 2013;143:1263–8.
Kroupina K, Bemeur C, Rose CF. Amino acids, ammonia, and hepatic encephalopathy. Anal Biochem 2022;649:114696.
Konstantis G, Pourzitaki C, Chourdakis M, et al. Efficacy of branched chain amino acids supplementation in liver cirrhosis: A systematic review and meta-analysis. Clin Nutr 2022;41(6):1171–90.
Gorissen SHM, Crombag JJR, Senden JMG, et al. Protein content and amino acid composition of commercially available plant-based protein isolates. Amino Acids 2018;50(12):1685–95.
Cutroneo S, Prandi B, Faccini A, et al. Comparison of protein quality and digestibility between plant-based and meat-based burgers. Food Res Int 2023;172:113183.
Fountoulakis M, Lahm HW. Hydrolysis and amino acid composition of proteins. J Chromatogr A 1998;826(2):109–34.
Ravindranath A, Sarma MS. Mitochondrial hepatopathy: Anticipated difficulties in management of fatty acid oxidation defects and urea cycle defects. World J Hepatol 2022;14(1):180–94.
Chinen Y, Nakamura S, Tamashiro K, et al. Isovaleric acidemia: Therapeutic response to supplementation with glycine, l-carnitine, or both in combination and a 10-year follow-up case study. Mol Genet Metab Rep 2017;11:2–5.
Lheureux PE, Hantson P. Carnitine in the treatment of valproic acid-induced toxicity. Clin Toxicol (Phila) 2009;47(2):101–11.
Claria J, Curto A, Moreau R, et al. Untargeted lipidomics uncovers lipid signatures that distinguish severe from moderate forms of acutely decompensated cirrhosis. J Hepatol 2021;75(5):1116–27.
Chiappini F, Coilly A, Kadar H, et al. Metabolism dysregulation induces a specific lipid signature of nonalcoholic steatohepatitis in patients. Sci Rep 2017;7:46658.
Puri P, Baillie RA, Wiest MM, et al. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 2007;46(4):1081–90.
Puri P, Wiest MM, Cheung O, et al. The plasma lipidomic signature of nonalcoholic steatohepatitis. Hepatology 2009;50(6):1827–38.
Rubio T, Felipo V, Tarazona S, et al. Multi-omic analysis unveils biological pathways in peripheral immune system associated to minimal hepatic encephalopathy appearance in cirrhotic patients. Sci Rep 2021;11(1):1907.
Musso G, Cassader M, Paschetta E, et al. Bioactive lipid species and metabolic pathways in progression and resolution of nonalcoholic steatohepatitis. Gastroenterology 2018;155(2):282–302.e8.
Meijer AJ, Lamers WH, Chamuleau RA. Nitrogen metabolism and ornithine cycle function. Physiol Rev 1990;70(3):701–48.
Cheng HS, Tan SP, Wong DMK, et al. The blood microbiome and health: Current evidence, controversies, and challenges. Int J Mol Sci 2023;24(6):5633.
Kumar A, Davuluri G, Silva RNE, et al. Ammonia lowering reverses sarcopenia of cirrhosis by restoring skeletal muscle proteostasis. Hepatology 2017;65(6):2045–58.
Medawar E, Beyer F, Thieleking R, et al. Prebiotic diet changes neural correlates of food decision-making in overweight adults: A randomised controlled within-subject cross-over trial. Gut 2024;73(2):298–310.
Peng L, Li ZR, Green RS, et al. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 2009;139(9):1619–25.
Lee C, Lee J, Eor JY, et al. Effect of consumption of animal products on the gut microbiome composition and gut health. Food Sci Anim Resour 2023;43(5):723–50.
Romero-Gomez M, Grande L, Camacho I, et al. Altered response to oral glutamine challenge as prognostic factor for overt episodes in patients with minimal hepatic encephalopathy. J Hepatol 2002;37(6):781–7.
Ampuero J, Gil A, Viloria MDM, et al. Oral glutamine challenge is a marker of altered ammonia metabolism and predicts the risk of hepatic encephalopathy. Liver Int 2020;40(4):921–30.
Gheorghe L, Iacob R, Vadan R, et al. Improvement of hepatic encephalopathy using a modified high-calorie high-protein diet. Rom J Gastroenterol 2005;14(3):231–8.
Dasarathy S, Merli M. Sarcopenia from mechanism to diagnosis and treatment in liver disease. J Hepatol 2016;65(6):1232–44.