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Increased energy and/or protein intake improves anthropometry and muscle strength in chronic obstructive pulmonary disease patients: a systematic review with meta-analysis on randomised controlled clinical trials

Published online by Cambridge University Press:  13 April 2022

Simone Bernardes*
Affiliation:
Post-Graduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil
Igor da Conceição Eckert
Affiliation:
Undergraduate Nutrition Program, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil
Camila Ferri Burgel
Affiliation:
Nutrition Service, Santa Casa de Misericordia of Porto Alegre Hospital Complex, Porto Alegre, Rio Grande do Sul, Brazil
Paulo José Zimermann Teixeira
Affiliation:
Post-Graduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil Undergraduate Medicine Program, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil Pulmologist at Pulmonary Rehabilitation Program, Hospital Pavilhão Pereira Filho, Santa Casa de Misericordia of Porto Alegre Hospital Complex, Porto Alegre, Rio Grande do Sul, Brazil
Flávia Moraes Silva
Affiliation:
Nutrition Department and Postgraduate Program in Nutrition Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Rio Grande do Sul, Brazil
*
* Corresponding author: Simone Bernardes, email simone.bernardes@gmail.com

Abstract

Compromised nutritional status is associated with a poor prognosis in chronic obstructive pulmonary disease (COPD) patients. However, the impact of nutritional support in this group of patients is controversial. The present study systematically reviewed the effect of energy and or protein supplements or food fortification on anthropometry and muscle strength of COPD patients. We searched MEDLINE (PubMed), EMBASE, Cochrane Library and Scopus for all published randomised clinical trials without language restriction up to May 2021. Three reviewers performed study selection and data extraction independently. We judged the risk of bias by RoB 2 and the certainty of evidence by the GRADE approach. We included thirty-two randomised controlled trials and compiled thirty-one of them (1414 participants) in the random-effects model meta-analyses. Interventions were energy and/or protein oral nutritional supplements or food fortification added to the diet for at least one week. Pooled analysis revealed that nutritional interventions increased body weight (muscle circumference (MD) = 1·44 kg, 95 % CI 0·81, 2·08, I2 = 73 %), lean body mass (standardised mean difference (SMD) = 0·37; 95 % CI 0·15, 0·59, I2 = 46 %), midarm muscle circumference (MD = 0·29 mm2, 95 % CI 0·02, 0·57, I2 = 0 %), triceps skinfold (MD = 1·09 mm, 95 % CI 0·01, 2·16, I2 = 0 %) and handgrip strength (SMD = 0·39, 95 % CI 0·07, 0·71, I2 = 62 %) compared with control diets. Certainty of evidence ranged from very low to low, and most studies were judged with some concerns or at high risk of bias. This meta-analysis revealed, with limited evidence, that increased protein and/or energy intake positively impacts anthropometric measures and handgrip strength of COPD patients.

Type
Systematic Review and Meta-Analysis
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Global Initiative for Chronic Obstructive Lung Disease (GOLD) (2022) Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Pulmonary Disease. https://goldcopd.org/2022-gold-reports-2/ (accessed January 2022).Google Scholar
Varmaghani, M, Dehghani, M, Heidari, E, et al. (2019) Global prevalence of chronic obstructive pulmonary disease: systematic review and meta-analysis. East Mediterr Health J 25, 4757.CrossRefGoogle ScholarPubMed
World Health Organization (2020) The Top 10 Causes of Death. https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death (accessed April 2021).Google Scholar
Machado, FVC, Spruit, MA, Groenen, MTJ, et al. (2021) Frequency and functional translation of low muscle mass in overweight and obese patients with COPD. Respir Res 22, 18.CrossRefGoogle ScholarPubMed
Schols, AM, Ferreira, IM, Franssen, FM, et al. (2014) Nutritional assessment and therapy in COPD: a European Respiratory Society statement. Eur Respir J 44, 15041520.CrossRefGoogle ScholarPubMed
Alea, C, Mateo, MP & De Guia, T (2013) Correlation of Nutritional Status Using Subjective Global Assessment (SGA) on Pulmonary Function Parameters in Patients With Chronic Obstructive Pulmonary Disease (COPD). Chest 144, 698A.CrossRefGoogle Scholar
Machado, FVC, Schneider, LP, Fonseca, J, et al. (2019) Clinical impact of body composition phenotypes in patients with COPD: a retrospective analysis. Eur J Clin Nutr 73, 15121519.CrossRefGoogle ScholarPubMed
Shoup, R, Dalsky, G, Warner, S, et al. (1997) Body composition and health-related quality of life in patients with obstructive airways disease. Eur Respir J 10, 15761580.CrossRefGoogle ScholarPubMed
Girón, R, Matesanz, C, García-Río, F, et al. (2009) Nutritional state during COPD exacerbation: clinical and prognostic implications. Ann Nutr Metab 54, 5258.CrossRefGoogle ScholarPubMed
Teixeira, P, Kowalski, V, Valduga, K, et al. (2021) Low muscle mass is a predictor of malnutrition and prolonged hospital stay in patients with acute exacerbation of chronic obstructive pulmonary disease: a longitudinal study. J Parenter Enter Nutr 45, 12211230.CrossRefGoogle ScholarPubMed
Attaway, AH, Welch, N, Hatipoğlu, U, et al. (2021) Muscle loss contributes to higher morbidity and mortality in COPD: an analysis of national trends. Respirology 26, 6271.CrossRefGoogle ScholarPubMed
Jerng, J, Tang, C, Cheng, R, et al. (2019) Healthcare utilization, medical costs and mortality associated with malnutrition in patients with chronic obstructive pulmonary disease: a matched cohort study. Curr Med Res Opin 35, 12651273.CrossRefGoogle ScholarPubMed
Schols, A, Slangen, J, Olovics, L, et al. (1998) Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 157, 17911797.CrossRefGoogle ScholarPubMed
Schols, A, Broekhuizen, R, Weling-Scheepers, C, et al. (2005) Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr 82, 5359.CrossRefGoogle ScholarPubMed
Dávalos-Yerovi, V, Marco, E, Sánchez-Rodríguez, D, et al. (2021) Malnutrition according to GLIM criteria is associated with mortality and hospitalizations in rehabilitation patients with stable chronic obstructive pulmonary disease. Nutrients 13, 111.CrossRefGoogle ScholarPubMed
Rawal, G & Yadav, S (2015) Nutrition in chronic obstructive pulmonary disease: a review. J Transl Intern Med 3, 151154.Google ScholarPubMed
Gea, J, Sancho-Muñoz, A & Chalela, R (2018) Nutritional status and muscle dysfunction in chronic respiratory diseases: stable phase v. acute exacerbations. J Thorac Dis 10, S1332S1354.CrossRefGoogle Scholar
Schols, A, Soeters, P, Dingemans, A, et al. (1993) Prevalence and characteristics of nutritional depletion in patients with stable COPD eligible for pulmonary rehabilitation. Am Rev Respir Dis 147, 11511156.CrossRefGoogle ScholarPubMed
Bhakare, M, Godbole, G, Khismatrao, D, et al. (2016) Correlating nutritional status with severity of chronic obstructive pulmonary disease in adult females. Med J DY Patil Univ 9, 570576.CrossRefGoogle Scholar
Chaudhary, S, Rao, P, Sawlani, K, et al. (2017) Assessment of nutritional status in chronic obstructive pulmonary disease patients. Int J Contemp Med Res 4, 268271.Google Scholar
Maltais, F, Decramer, M, Casaburi, R, et al. (2014) An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 189, e15e62.CrossRefGoogle ScholarPubMed
Kovarik, M, Joskova, V, Patkova, A, et al. (2017) Hand grip endurance test relates to clinical state and prognosis in COPD patients better than 6-minute walk test distance. Int J Chron Obstruct Pulmon Dis 12, 34293435.CrossRefGoogle ScholarPubMed
Samarghandi, A, Ioachimescu, O & Qayyum, R (2020) Association between peak inspiratory flow rate and hand grip muscle strength in hospitalized patients with acute exacerbation of chronic obstructive pulmonary disease. PLOS ONE 15, e0227737.CrossRefGoogle ScholarPubMed
Anker, SD, Laviano, A, Filippatos, G, et al. (2009) ESPEN Guidelines on parenteral nutrition: on cardiology and pneumology. Clin Nutr 28, 455460.CrossRefGoogle ScholarPubMed
Bauer, J, Biolo, G, Cederholm, T, et al. (2013) Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the prot-age study group. J Am Med Dir Assoc 14, 542559.CrossRefGoogle ScholarPubMed
Ferreira, IM, Brooks, D, Lacasse, Y, et al. (2000) Nutritional support for individuals with COPD: a meta-analysis. Chest 117, 672678.CrossRefGoogle ScholarPubMed
Collins, P, Stratton, R & Elia, M (2012) Nutritional support in chronic obstructive pulmonary disease: a systematic review and meta-analysis. Am J Clin Nutr 95, 13851395.CrossRefGoogle ScholarPubMed
Collins, PF, Elia, M &Stratton, RJ (2013) Nutritional support and functional capacity in chronic obstructive pulmonary disease: a systematic review and meta-analysis. Respirology 18, 616629.CrossRefGoogle ScholarPubMed
Ferreira, IM, Brooks, D, White, J, et al. (2012) Nutritional supplementation for stable chronic obstructive pulmonary disease. Cochrane Database Syst Rev 12, CD000998.Google ScholarPubMed
Aldhahir, AM, Rajeh, AMA, Aldabayan, YS, et al. (2020) Nutritional supplementation during pulmonary rehabilitation in COPD: a systematic review. Chron Respir Dis 17, 121.CrossRefGoogle ScholarPubMed
Higgins, J, Thomas, J, Chandler, J, et al. (2020) Cochrane Handbook for Systematic Reviews of Interventions Version 6.1 (Updated September 2020). http://www.training.cochrane.org/handbook (accessed October 2020).Google Scholar
Page, M, McKenzie, J, Bossuyt, P, et al. (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372, n71.CrossRefGoogle ScholarPubMed
Sterne, J, Savović, J, Page, M, et al. (2019) RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 366, I4898.CrossRefGoogle ScholarPubMed
Schünemann, H, Brożek, J, Guyatt, G, et al (2013) GRADE Handbook for Grading Quality of Evidence and Strength of Recommendations. The GRADE Working Group. http://guidelinedevelopment.org/handbook (accessed October 2013).Google Scholar
Follmann, D, Elliott, P, Suh, I, et al. (1992) Variance imputation for overviews of clinical trials with continuous response. J Clin Epidemiol 45, 769773.CrossRefGoogle ScholarPubMed
Hedges, L & Vevea, J (1998) Fixed- and random-effects models in meta-analysis. Psychol Methods 3, 486504.CrossRefGoogle Scholar
IntHout, J, Ioannidis, J & Borm, G (2014) The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method. BMC Med Res Methodol 18, 25.CrossRefGoogle Scholar
Cohen, J (1977) Statistical Power Analysis for the Behavioral Sciences, 1st ed. San Diego: Academic Press.Google Scholar
Lewis, M, Belman, M & Dorr-Uyemura, L (1987) Nutritional supplementation in ambulatory patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 135, 10621068.Google ScholarPubMed
Efthimiou, J, Fleming, J, Gomes, C, et al. (1998) The effect of supplementary oral nutrition in poorly nourished patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 137, 10751082.CrossRefGoogle Scholar
Goris, AHC, Vermeeren, MAP, Wouters, EFM, et al. (2003) Energy balance in depleted ambulatory patients with chronic obstructive pulmonary disease: the effect of physical activity and oral nutritional supplementation. Br J Nutr 89, 725729.CrossRefGoogle ScholarPubMed
Steiner, MC, Barton, RL, Singh, SJ, et al. (2003) Nutritional enhancement of exercise performance in chronic obstructive pulmonary disease: a randomised controlled trial. Thorax 58, 745751.CrossRefGoogle ScholarPubMed
Vermeeren, MAP, Wouters, EFM, Geraerts-Keeris, AJW, et al. (2004) Nutritional support in patients with chronic obstructive pulmonary disease during hospitalization for an acute exacerbation; a randomized controlled feasibility trial. Clin Nutr 23, 11841192.CrossRefGoogle ScholarPubMed
Fuld, J, Kilduff, L, Neder, JA, et al. (2005) Creatine supplementation during pulmonary rehabilitation in chronic obstructive pulmonary disease. Thorax 60, 531537.CrossRefGoogle ScholarPubMed
Faager, G, Söderlund, K, Sköld, CM, et al. (2006) Creatine supplementation and physical training in patients with COPD: a double blind, placebo-controlled study. Int J Chron Obstruct Pulmon Dis 1, 445453.Google ScholarPubMed
Deacon, SJ, Vincent, EE, Greenhaff, PL, et al. (2008) Randomized controlled trial of dietary creatine as an adjunct therapy to physical training in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 178, 233239.CrossRefGoogle ScholarPubMed
Weekes, CE, Emery, PW & Elia, M (2009) Dietary counselling and food fortification in stable copd: a randomised trial. Thorax 64, 326331.CrossRefGoogle ScholarPubMed
Baldi, S, Aquilani, R, Pinna, GD, et al. (2010) Fat-free mass change after nutritional rehabilitation in weight losing COPD: role of insulin, C-reactive protein and tissue hypoxia. Int J COPD 5, 2939.CrossRefGoogle ScholarPubMed
Dal Negro, RW, Aquilani, R, Bertacco, S, et al. (2010) Comprehensive effects of supplemented essential amino acids in patients with severe COPD and sarcopenia. Monaldi Arch Chest Dis 73, 2533.Google ScholarPubMed
Sugawara, K, Takahashi, H, Kasai, C, et al. (2010) Effects of nutritional supplementation combined with low-intensity exercise in malnourished patients with COPD. Respir Med 104, 18831889.CrossRefGoogle ScholarPubMed
Knowles, JB, Fairbarn, MS, Wiggs, BJ, et al. (1988) Dietary supplementation and respiratory muscle performance in patients with COPD. Chest 93, 977983.CrossRefGoogle ScholarPubMed
Dal Negro, RW, Testa, A, Aquilani, R, et al. (2012) Essential amino acid supplementation in patients with severe COPD: a step towards home rehabilitation. Monaldi Arch Chest Dis 77, 6775.Google ScholarPubMed
Sugawara, K, Takahashi, H, Kashiwagura, T, et al. (2012) Effect of anti-inflammatory supplementation with whey peptide and exercise therapy in patients with COPD. Respir Med 106, 15261534.Google ScholarPubMed
Constantin, D, Menon, MK, Houchen-Wolloff, L, et al. (2013) Skeletal muscle molecular responses to resistance training and dietary supplementation in COPD. Thorax 68, 625633.CrossRefGoogle ScholarPubMed
Gurgun, A, Deniz, S, Argin, M, et al. (2013) Effects of nutritional supplementation combined with conventional pulmonary rehabilitation in muscle-wasted chronic obstructive pulmonary disease: a prospective, randomized and controlled study. Respirology 18, 495500.CrossRefGoogle ScholarPubMed
Marinari, S, Manigrasso, MR & De Benedetto, F (2013) Effects of nutraceutical diet integration, with coenzyme Q10 (Q-Ter multicomposite) and creatine, on dyspnea, exercise tolerance, and quality of life in COPD patients with chronic respiratory failure. Multidiscip Respir Med 8, 40.CrossRefGoogle ScholarPubMed
Ahnfeldt-Mollerup, P, Hey, H, Johansen, C, et al. (2015) The effect of protein supplementation on quality of life, physical function, and muscle strength in patients with chronic obstructive pulmonary disease. Eur J Phys Rehabil Med. 51, 447456.Google ScholarPubMed
Khan, NA, Kumar, N & Daga, MK (2016) Effect of dietary supplementation on body composition, pulmonary function and health-related quality of life in patients with stable COPD. Tanaffos 15, 225235.Google ScholarPubMed
van de Bool, C, Rutten, EPA, van Helvoort, A, et al. (2017) A randomized clinical trial investigating the efficacy of targeted nutrition as adjunct to exercise training in COPD. J Cachexia Sarcopenia Muscle 8, 748758.CrossRefGoogle ScholarPubMed
De Benedetto, F, Pastorelli, R, Ferrario, M, et al. (2018) Supplementation with Qter® and Creatine improves functional performance in COPD patients on long term oxygen therapy. Respir Med 142, 8693.CrossRefGoogle ScholarPubMed
Degirmenci, D, Şahin, H & Soylu, M (2018) The effect of enteral nutrition support on muscle function capacity and pulmonary functions in malnourished patients with Chronic Obstructive Pulmonary Disease. Prog Nutr 20, 120127.Google Scholar
Otte, KE, Ahlburg, P, D’Amore, F, et al. (1989) Nutritional repletion in malnourished patients with emphysema. J Parenter Enter Nutr 13, 152156.Google ScholarPubMed
van Beers, M, Rutten-van Mölken, M, van de Bool, C, et al. (2020) Clinical outcome and cost-effectiveness of a 1-year nutritional intervention programme in COPD patients with low muscle mass: the randomized controlled NUTRAIN trial. Clin Nutr 39, 405413.CrossRefGoogle ScholarPubMed
Ahmadi, A, Eftekhari, MH, Mazloom, Z, et al. (2020) Fortified whey beverage for improving muscle mass in chronic obstructive pulmonary disease: a single-blind, randomized clinical trial. Respir Res 21, 111.Google ScholarPubMed
Fuenzalida, CE, Petty, TL, Jones, ML, et al. (1990) The immune response to short-term nutritional intervention in advanced chronic obstructive pulmonary disease. Am Rev Respir Dis 142, 4956.CrossRefGoogle ScholarPubMed
Entrenas Costa, L, Domínguez Platas, T, Checa Pinilla, J, et al. (1991) Is nutritional support useful in chronic obstructive pulmonary disease (COPD)? Neumosur Rev la Asoc neumólogos del sur 3, 4149.Google Scholar
Rogers, R, Donahoe, M & Costantino, J (1992) Physiologic effects of oral supplemental feeding in malnourished patients with chronic obstructive pulmonary disease: a randomized control study. Am Rev Respir Dis 146, 15111517.Google ScholarPubMed
Ganzoni, A, Heilig, P, Schönenberger, K, et al. (1994) Hochkalorische Ernährung bei chronischer obstruktiver Lungenkrankheit (High-caloric nutrition in chronic obstructive lung disease). Schweiz Rundsch Med Prax 83, 1316.Google ScholarPubMed
Schols, A, Soeters, P, Mostert, R, et al. (1995) Physiologic effects of nutritional support and anabolic steroids in patients with chronic obstructive pulmonary disease. A placebo-controlled randomized trial. Am J Respir Crit Care Med 152, 12681274.CrossRefGoogle ScholarPubMed
Saudny-Unterberger, H, Martin, JG & Gray-Donald, K (1997) Impact of nutritional support on functional status during an acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 156, 794799.CrossRefGoogle ScholarPubMed
Angelillo, VA, Bedi, S, Durfee, D, et al. (1985) Effects of low and high carbohydrate feedings in ambulatory patients with chronic obstructive pulmonary disease and chronic hypercapnia. Ann Intern Med 103, 883885.CrossRefGoogle ScholarPubMed
Benito Martínez, M, La Serna Infantes, J, Guarro Riba, M, et al. (2017) Estado nutricional y funcional en pacientes con enfermedad pulmonar obstructiva crónica: efectos de la suplementación nutricional oral (estudio OFOS) (Nutritional and functional state of patients with chronic obstructive pulmonary disease: effects of oral). Nutr Hosp 34, 776783.Google Scholar
Cai, B, Zhu, Y, Ma, Y, et al. (2003) Effect of supplementing a high-fat, low-carbohydrate enteral formula in COPD patients. Nutrition 19, 229232.CrossRefGoogle ScholarPubMed
Calder, PC, Laviano, A, Lonnqvist, F, et al. (2018) Targeted medical nutrition for cachexia in chronic obstructive pulmonary disease: a randomized, controlled trial. J Cachexia Sarcopenia Muscle 9, 2840.Google ScholarPubMed
Camere, MA, Benito, P, Camere, DM, et al. (2016) MON-P093: an oral nutritional supplement reduces malnutrition in chronic obstructive pulmonary disease patients. Clin Nutr 35, S187S188.CrossRefGoogle Scholar
Collins, PF, Stratton, RJ & Elia, M (2014) PP122-SUN: outstanding abstract: nutritional support in Chronic Obstructive Pulmonary Disease (COPD): a randomised trial. Clin Nutr 33, S65.CrossRefGoogle Scholar
Gurgun, A, Deniz, S, Argın, M, et al. (2011) The effects of nutritional supplementation added to pulmonary rehabilitation in muscle wasted chronic obstructive pulmonary disease: a randomised, controlled, prospective study. Am J Respir Crit Care Med. 183, A3972.Google Scholar
Ingadottir, AR, Bjorgvinsdottir, EB, Beck, AM, et al. (2020) Effect of two different nutritional supplements on postprandial glucose response and energy- and protein intake in hospitalised patients with COPD: a randomised cross-over study. Clin Nutr 39, 10851091.CrossRefGoogle ScholarPubMed
Laviolette, L, Lands, L, Dauletbaev, N, et al. (2010) Combined effect of dietary supplementation with pressurized whey and exercise training in chronic obstructive pulmonary disease: a randomized, controlled, double-blind pilot study. J Med Food 13, 589598.Google ScholarPubMed
Matsuyama, W, Mitsuyama, H, Watanabe, M, et al. (2005) Effects of n-3 polyunsaturated fatty acids on inflammatory markers in COPD. Chest 128, 38173827.CrossRefGoogle ScholarPubMed
Ogasawara, T, Marui, S, Miura, E, et al. (2018) Effect of eicosapentaenoic acid on prevention of lean body mass depletion in patients with exacerbation of chronic obstructive pulmonary disease: a prospective randomized controlled trial. Clin Nutr ESPEN 28, 6773.Google ScholarPubMed
Planas, M, Álvarez, J, García-Peris, PA, et al. (2005) Nutritional support and quality of life in stable chronic obstructive pulmonary disease (COPD) patients. Clin Nutr 24, 433441.CrossRefGoogle ScholarPubMed
Raizada, N, Daga, MK, Kumar, N, et al. (2014) Nutritional intervention in stable COPD patients and its effect on anthropometry, pulmonary function, and health-related quality of life (HRQL). J Indian Acad Clin Med 15, 100105.Google Scholar
Sugawara, K, Takanobu, S, Masahiro, S, et al. (2011) Anti-inflammatory nutritional support enhances exercise performance and QOL in patients with stable COPD. Eur Respir J 38, 1893.Google Scholar
Tümer, G, Mercanligil, SM, Uzun, O, et al. (2009) The effects of a high-fat, low-carbohydrate diet on the prognosis of patients with an acute attack of chronic obstructive pulmonary disease. Turkiye Klin J Med Sci 29, 895904.Google Scholar
Zongxing, O (2005) Analysis of the therapeutic effect of glutamine on COPD patients with malnutrition. China Trop Med 5, 12851287.Google Scholar
Sakkas, G, Schambelan, M & Mulligan, K (2009) Can the use of creatine supplementation attenuate muscle loss in cachexia and wasting? Curr Opin Clin Nutr Metab Care 12, 623627.CrossRefGoogle ScholarPubMed
Brose, A, Parise, G & Tarnopolsky, M (2003) Creatine supplementation enhances isometric strength and body composition improvements following strength exercise training in older adults. J Gerontol A Biol Sci Med Sci 58,1119.CrossRefGoogle ScholarPubMed
Dillon, E, Sheffield-Moore, M, Paddon-Jones, D, et al. (2009) Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women. J Clin Endocrinol Metab 94, 16301637.Google ScholarPubMed
Yan, G (2008) Glutamine supplementation therapy in elderly patients during the COPD acute exacerbation stage. Chinese J Clin Healthc 11, 113115.Google Scholar
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