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Published in: BMC Gastroenterology 1/2023

Open Access 01-12-2023 | Liver Cirrhosis | Research

Dietary protein intake and mortality among survivors of liver cirrhosis: a prospective cohort study

Authors: Ghazal Daftari, Asal Neshatbini Tehrani, Fereshteh Pashayee-khamene, Sara Karimi, Saleheh Ahmadzadeh, Azita Hekmatdoost, Amin Salehpour, Mahdi Saber-Firoozi, Behzad Hatami, Zahra Yari

Published in: BMC Gastroenterology | Issue 1/2023

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Abstract

Background

Liver cirrhosis is a worldwide burden and is associated with poor clinical outcomes, including increased mortality. The beneficial effects of dietary modifications in reducing morbidity and mortality are inevitable.

Aim

The current study aimed to evaluate the potential association of dietary protein intake with the cirrhosis-related mortality.

Methods

In this cohort study, 121 ambulatory cirrhotic patients with at least 6 months of cirrhosis diagnosis were followed-up for 48 months. A 168-item validated food frequency questionnaire was used for dietary intake assessment. Total dietary protein was classified as dairy, vegetable and animal protein. We estimated crude and multivariable-adjusted hazard ratios (HRs) with 95% confidence intervals (CIs), applying Cox proportional hazard analyses.

Results

After full adjustment for confounders, analyses showed that total (HR = 0.38, 95% CI = 0.2–1.1, p trend = 0.045) and dairy (HR = 0.38, 95% CI = 0.13–1.1, p trend = 0.046) protein intake was associated with a 62% lower risk of cirrhosis-related mortality. While a higher intake of animal protein was associated with a 3.8-fold increase in the risk of mortality in patients (HR = 3.8, 95% CI = 1.7–8.2, p trend = 0.035). Higher intake of vegetable protein was inversely but not significantly associated with mortality risk.

Conclusion

A comprehensive evaluation of the associations of dietary protein intake with cirrhosis-related mortality indicated that a higher intakes of total and dairy protein and a lower intakes of animal protein are associated with a reduced risk of mortality in cirrhotic patients.
Literature
1.
3.
go back to reference Yao CK, Fung J, Chu NHS, Tan VPY. Dietary interventions in liver cirrhosis. J Clin Gastroenterol. 2018;52(8):663–73.CrossRefPubMed Yao CK, Fung J, Chu NHS, Tan VPY. Dietary interventions in liver cirrhosis. J Clin Gastroenterol. 2018;52(8):663–73.CrossRefPubMed
4.
go back to reference Dawood RM, El-Meguid MA, Salum GM, El Awady MK. Key Players of Hepatic Fibrosis. J Interferon Cytokine Res. 2020;40(10):472–89.CrossRefPubMed Dawood RM, El-Meguid MA, Salum GM, El Awady MK. Key Players of Hepatic Fibrosis. J Interferon Cytokine Res. 2020;40(10):472–89.CrossRefPubMed
5.
go back to reference Garcia-Tsao G, Friedman S, Iredale J, Pinzani M. Now there are many (stages) where before there was one: In search of a pathophysiological classification of cirrhosis. Hepatology (Baltimore, MD). 2010;51(4):1445.CrossRefPubMed Garcia-Tsao G, Friedman S, Iredale J, Pinzani M. Now there are many (stages) where before there was one: In search of a pathophysiological classification of cirrhosis. Hepatology (Baltimore, MD). 2010;51(4):1445.CrossRefPubMed
6.
go back to reference Juakiem W, Torres DM, Harrison SA. Nutrition in cirrhosis and chronic liver disease. Clin Liver Dis. 2014;18(1):179–90.CrossRefPubMed Juakiem W, Torres DM, Harrison SA. Nutrition in cirrhosis and chronic liver disease. Clin Liver Dis. 2014;18(1):179–90.CrossRefPubMed
7.
go back to reference Ishikawa T, Imai M, Ko M, Sato H, Nozawa Y, Sano T, et al. Evaluation of the branched-chain amino acid-to-tyrosine ratio prior to treatment as a prognostic predictor in patients with liver cirrhosis. Oncotarget. 2017;8(45):79480.CrossRefPubMedPubMedCentral Ishikawa T, Imai M, Ko M, Sato H, Nozawa Y, Sano T, et al. Evaluation of the branched-chain amino acid-to-tyrosine ratio prior to treatment as a prognostic predictor in patients with liver cirrhosis. Oncotarget. 2017;8(45):79480.CrossRefPubMedPubMedCentral
8.
go back to reference Urata Y, Okita K, Korenaga K, Uchida K, Yamasaki T, Sakaida I. The effect of supplementation with branched-chain amino acids in patients with liver cirrhosis. Hepatol Res. 2007;37(7):510–6.CrossRef Urata Y, Okita K, Korenaga K, Uchida K, Yamasaki T, Sakaida I. The effect of supplementation with branched-chain amino acids in patients with liver cirrhosis. Hepatol Res. 2007;37(7):510–6.CrossRef
9.
go back to reference Plauth M, Merli M, Kondrup J, Weimann A, Ferenci P, Müller M, et al. ESPEN guidelines for nutrition in liver disease and transplantation. Clin Nutr. 1997;16(2):43–55.CrossRefPubMed Plauth M, Merli M, Kondrup J, Weimann A, Ferenci P, Müller M, et al. ESPEN guidelines for nutrition in liver disease and transplantation. Clin Nutr. 1997;16(2):43–55.CrossRefPubMed
10.
go back to reference Moriwaki H, Miwa Y, Tajika M, Kato M, Fukushima H, Shiraki M. Branched-chain amino acids as a protein-and energy-source in liver cirrhosis. Biochem Biophys Res Commun. 2004;313(2):405–9.CrossRefPubMed Moriwaki H, Miwa Y, Tajika M, Kato M, Fukushima H, Shiraki M. Branched-chain amino acids as a protein-and energy-source in liver cirrhosis. Biochem Biophys Res Commun. 2004;313(2):405–9.CrossRefPubMed
11.
go back to reference Holeček M. Branched-chain amino acid supplementation in treatment of liver cirrhosis: updated views on how to attenuate their harmful effects on cataplerosis and ammonia formation. Nutrition. 2017;41:80–5.CrossRefPubMed Holeček M. Branched-chain amino acid supplementation in treatment of liver cirrhosis: updated views on how to attenuate their harmful effects on cataplerosis and ammonia formation. Nutrition. 2017;41:80–5.CrossRefPubMed
12.
go back to reference Muto Y, Sato S, Watanabe A, Moriwaki H, Suzuki K, Kato A, et al. Effects of oral branched-chain amino acid granules on event-free survival in patients with liver cirrhosis. Clin Gastroenterol Hepatol. 2005;3(7):705–13.CrossRefPubMed Muto Y, Sato S, Watanabe A, Moriwaki H, Suzuki K, Kato A, et al. Effects of oral branched-chain amino acid granules on event-free survival in patients with liver cirrhosis. Clin Gastroenterol Hepatol. 2005;3(7):705–13.CrossRefPubMed
13.
go back to reference Shinaberger CS, Kilpatrick RD, Regidor DL, McAllister CJ, Greenland S, Kopple JD, et al. Longitudinal associations between dietary protein intake and survival in hemodialysis patients. Am J Kidney Dis. 2006;48(1):37–49.CrossRefPubMed Shinaberger CS, Kilpatrick RD, Regidor DL, McAllister CJ, Greenland S, Kopple JD, et al. Longitudinal associations between dietary protein intake and survival in hemodialysis patients. Am J Kidney Dis. 2006;48(1):37–49.CrossRefPubMed
14.
15.
go back to reference Song M, Fung TT, Hu FB, Willett WC, Longo VD, Chan AT, et al. Association of animal and plant protein intake with all-cause and cause-specific mortality. JAMA Intern Med. 2016;176(10):1453–63.CrossRefPubMedPubMedCentral Song M, Fung TT, Hu FB, Willett WC, Longo VD, Chan AT, et al. Association of animal and plant protein intake with all-cause and cause-specific mortality. JAMA Intern Med. 2016;176(10):1453–63.CrossRefPubMedPubMedCentral
16.
go back to reference Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M, Azizi F. Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public Health Nutr. 2010;13(5):654–62.CrossRefPubMed Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M, Azizi F. Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public Health Nutr. 2010;13(5):654–62.CrossRefPubMed
17.
go back to reference Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, Ter Borg PC. A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology. 2000;31(4):864–71.CrossRefPubMed Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, Ter Borg PC. A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology. 2000;31(4):864–71.CrossRefPubMed
18.
go back to reference Yang Y, Zhao L-G, Wu Q-J, Ma X, Xiang Y-B. Association between dietary fiber and lower risk of all-cause mortality: a meta-analysis of cohort studies. Am J Epidemiol. 2015;181(2):83–91.CrossRefPubMed Yang Y, Zhao L-G, Wu Q-J, Ma X, Xiang Y-B. Association between dietary fiber and lower risk of all-cause mortality: a meta-analysis of cohort studies. Am J Epidemiol. 2015;181(2):83–91.CrossRefPubMed
19.
go back to reference Detsky AS, Baker J, Johnston N, Whittaker S, Mendelson R, Jeejeebhoy K. What is subjective global assessment of nutritional status? J Parenter Enter Nutr. 1987;11(1):8–13.CrossRef Detsky AS, Baker J, Johnston N, Whittaker S, Mendelson R, Jeejeebhoy K. What is subjective global assessment of nutritional status? J Parenter Enter Nutr. 1987;11(1):8–13.CrossRef
20.
go back to reference Chen LK, Liu LK, Woo J, Assantachai P, Auyeung T-W, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15(2):95–101.CrossRefPubMed Chen LK, Liu LK, Woo J, Assantachai P, Auyeung T-W, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15(2):95–101.CrossRefPubMed
22.
go back to reference Tharrey M, Mariotti F, Mashchak A, Barbillon P, Delattre M, Fraser GE. Patterns of plant and animal protein intake are strongly associated with cardiovascular mortality: the Adventist Health Study-2 cohort. Int J Epidemiol. 2018;47(5):1603–12.CrossRefPubMedPubMedCentral Tharrey M, Mariotti F, Mashchak A, Barbillon P, Delattre M, Fraser GE. Patterns of plant and animal protein intake are strongly associated with cardiovascular mortality: the Adventist Health Study-2 cohort. Int J Epidemiol. 2018;47(5):1603–12.CrossRefPubMedPubMedCentral
23.
go back to reference Huang J, Liao LM, Weinstein SJ, Sinha R, Graubard BI, Albanes D. Association between plant and animal protein intake and overall and cause-specific mortality. JAMA Intern Med. 2020;180(9):1173–84.CrossRefPubMed Huang J, Liao LM, Weinstein SJ, Sinha R, Graubard BI, Albanes D. Association between plant and animal protein intake and overall and cause-specific mortality. JAMA Intern Med. 2020;180(9):1173–84.CrossRefPubMed
24.
go back to reference Chalvon-Demersay T, Azzout-Marniche D, Arfsten J, Egli L, Gaudichon C, Karagounis LG, et al. A systematic review of the effects of plant compared with animal protein sources on features of metabolic syndrome. J Nutr. 2017;147(3):281–92.PubMed Chalvon-Demersay T, Azzout-Marniche D, Arfsten J, Egli L, Gaudichon C, Karagounis LG, et al. A systematic review of the effects of plant compared with animal protein sources on features of metabolic syndrome. J Nutr. 2017;147(3):281–92.PubMed
25.
go back to reference Holmes MD, Pollak MN, Willett WC, Hankinson SE. Dietary correlates of plasma insulin-like growth factor I and insulin-like growth factor binding protein 3 concentrations. Cancer Epidemiol Biomarkers Prev. 2002;11(9):852–61.PubMed Holmes MD, Pollak MN, Willett WC, Hankinson SE. Dietary correlates of plasma insulin-like growth factor I and insulin-like growth factor binding protein 3 concentrations. Cancer Epidemiol Biomarkers Prev. 2002;11(9):852–61.PubMed
26.
go back to reference Allen NE, Appleby PN, Davey GK, Kaaks R, Rinaldi S, Key TJ. The associations of diet with serum insulin-like growth factor I and its main binding proteins in 292 women meat-eaters, vegetarians, and vegans. Cancer Epidemiol Biomarkers Prev. 2002;11(11):1441–8.PubMed Allen NE, Appleby PN, Davey GK, Kaaks R, Rinaldi S, Key TJ. The associations of diet with serum insulin-like growth factor I and its main binding proteins in 292 women meat-eaters, vegetarians, and vegans. Cancer Epidemiol Biomarkers Prev. 2002;11(11):1441–8.PubMed
27.
go back to reference Ney M, Abraldes JG, Ma M, Belland D, Harvey A, Robbins S, et al. Insufficient protein intake is associated with increased mortality in 630 patients with cirrhosis awaiting liver transplantation. Nutr Clin Pract. 2015;30(4):530–6.CrossRefPubMed Ney M, Abraldes JG, Ma M, Belland D, Harvey A, Robbins S, et al. Insufficient protein intake is associated with increased mortality in 630 patients with cirrhosis awaiting liver transplantation. Nutr Clin Pract. 2015;30(4):530–6.CrossRefPubMed
28.
go back to reference Sam J, Nguyen GC. Protein-calorie malnutrition as a prognostic indicator of mortality among patients hospitalized with cirrhosis and portal hypertension. Liver Int. 2009;29(9):1396–402.CrossRefPubMed Sam J, Nguyen GC. Protein-calorie malnutrition as a prognostic indicator of mortality among patients hospitalized with cirrhosis and portal hypertension. Liver Int. 2009;29(9):1396–402.CrossRefPubMed
29.
go back to reference Córdoba J, López-Hellín J, Planas M, Sabín P, Sanpedro F, Castro F, et al. Normal protein diet for episodic hepatic encephalopathy: results of a randomized study. J Hepatol. 2004;41(1):38–43.CrossRefPubMed Córdoba J, López-Hellín J, Planas M, Sabín P, Sanpedro F, Castro F, et al. Normal protein diet for episodic hepatic encephalopathy: results of a randomized study. J Hepatol. 2004;41(1):38–43.CrossRefPubMed
30.
go back to reference Charlton MR. Protein metabolism and liver disease. Baillieres Clin Endocrinol Metab. 1996;10(4):617–35.CrossRefPubMed Charlton MR. Protein metabolism and liver disease. Baillieres Clin Endocrinol Metab. 1996;10(4):617–35.CrossRefPubMed
31.
go back to reference Ling P-R, Bistrian BR. Comparison of the effects of food versus protein restriction on selected nutritional and inflammatory markers in rats. Metabolism. 2009;58(6):835–42.CrossRefPubMedPubMedCentral Ling P-R, Bistrian BR. Comparison of the effects of food versus protein restriction on selected nutritional and inflammatory markers in rats. Metabolism. 2009;58(6):835–42.CrossRefPubMedPubMedCentral
32.
go back to reference Tsiaousi ET, Hatzitolios AI, Trygonis SK, Savopoulos CG. Malnutrition in end stage liver disease: recommendations and nutritional support. J Gastroenterol Hepatol. 2008;23(4):527–33.CrossRefPubMed Tsiaousi ET, Hatzitolios AI, Trygonis SK, Savopoulos CG. Malnutrition in end stage liver disease: recommendations and nutritional support. J Gastroenterol Hepatol. 2008;23(4):527–33.CrossRefPubMed
33.
go back to reference Pashayee-Khamene F, Kord-Varkaneh H, Saber-Firoozi M, Hatami B, Rashidkhani B, Hekmatdoost A. Dietary protein sources and disease severity, malnutrition and anthropometric measurements in cirrhotic patients. Gastroenterol Hepatol Bed Bench. 2019;12(2):143.PubMedPubMedCentral Pashayee-Khamene F, Kord-Varkaneh H, Saber-Firoozi M, Hatami B, Rashidkhani B, Hekmatdoost A. Dietary protein sources and disease severity, malnutrition and anthropometric measurements in cirrhotic patients. Gastroenterol Hepatol Bed Bench. 2019;12(2):143.PubMedPubMedCentral
34.
go back to reference Bianchi GP, Marchesini G, Fabbri A, Rondelli A, Bugianesi E, Zoli M, 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.CrossRefPubMed Bianchi GP, Marchesini G, Fabbri A, Rondelli A, Bugianesi E, Zoli M, 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.CrossRefPubMed
35.
go back to reference Amodio P, Caregaro L, Pettenó E, Marcon M, DelPiccolo F, Gatta A. Vegetarian diets in hepatic encephalopathy: facts or fantasies? Dig Liver Dis. 2001;33(6):492–500.CrossRefPubMed Amodio P, Caregaro L, Pettenó E, Marcon M, DelPiccolo F, Gatta A. Vegetarian diets in hepatic encephalopathy: facts or fantasies? Dig Liver Dis. 2001;33(6):492–500.CrossRefPubMed
36.
go back to reference Ooi P, Gilmour S, Yap J, Mager D. Effects of branched chain amino acid supplementation on patient care outcomes in adults and children with liver cirrhosis: a systematic review. Clin Nutr ESPEN. 2018;28:41–51.CrossRefPubMed Ooi P, Gilmour S, Yap J, Mager D. Effects of branched chain amino acid supplementation on patient care outcomes in adults and children with liver cirrhosis: a systematic review. Clin Nutr ESPEN. 2018;28:41–51.CrossRefPubMed
37.
go back to reference Ruiz-Margáin A, Macías-Rodríguez R, Ríos-Torres S, Román-Calleja B, Méndez-Guerrero O, Rodríguez-Córdova P, et al. Effect of a high-protein, high-fiber diet plus supplementation with branched-chain amino acids on the nutritional status of patients with cirrhosis. Revista de Gastroenterol Méx (English Edition). 2018;83(1):9–15.CrossRef Ruiz-Margáin A, Macías-Rodríguez R, Ríos-Torres S, Román-Calleja B, Méndez-Guerrero O, Rodríguez-Córdova P, et al. Effect of a high-protein, high-fiber diet plus supplementation with branched-chain amino acids on the nutritional status of patients with cirrhosis. Revista de Gastroenterol Méx (English Edition). 2018;83(1):9–15.CrossRef
Metadata
Title
Dietary protein intake and mortality among survivors of liver cirrhosis: a prospective cohort study
Authors
Ghazal Daftari
Asal Neshatbini Tehrani
Fereshteh Pashayee-khamene
Sara Karimi
Saleheh Ahmadzadeh
Azita Hekmatdoost
Amin Salehpour
Mahdi Saber-Firoozi
Behzad Hatami
Zahra Yari
Publication date
01-12-2023
Publisher
BioMed Central
Keyword
Liver Cirrhosis
Published in
BMC Gastroenterology / Issue 1/2023
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/s12876-023-02832-1

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