Impact of supplementation with amino acids or their metabolites on muscle wasting in patients with critical illness or other muscle wasting illness: A systematic review

Journal of Human Nutrition and Dietetics

Volumn 28, Issue 4, 2015, Pages 313-330

  Wandrag, L ^a   Brett, S J ^b   Frost, G ^a   Hickson, M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

Author keywords

Branched chain amino acid; Critical illness; Essential amino acid supplement; Leucine; Muscle wasting; hydroxy methylbutyrate

Indexed keywords

AMINO ACID; BETA-HYDROXYISOVALERIC ACID; CREATINE; ESSENTIAL AMINO ACID; LEUCINE; VALERIC ACID DERIVATIVE;

AGED; BODY COMPOSITION; CRITICAL ILLNESS; DIET; DIET SUPPLEMENTATION; ENTERIC FEEDING; FEMALE; HUMAN; INTENSIVE CARE UNIT; MALE; MEDLINE; METABOLISM; MUSCULAR ATROPHY; NUTRITIONAL STATUS;

AGED; AMINO ACIDS; AMINO ACIDS, ESSENTIAL; BODY COMPOSITION; CREATINE; CRITICAL ILLNESS; DIET; DIETARY SUPPLEMENTS; ENTERAL NUTRITION; FEMALE; HUMANS; INTENSIVE CARE UNITS; LEUCINE; MALE; MEDLINE; MUSCULAR ATROPHY; NUTRITIONAL STATUS; VALERATES;

EID: 84937570988     PISSN: 09523871     EISSN: 1365277X     Source Type: Journal    
DOI: 10.1111/jhn.12238     Document Type: Article

References (76)

1. Agusti, A.G., Sauleda, J., Miralles, C., Gomez, C., Togores, B., Sala, E., Batle, S. & Busquets, X. (2002) Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 166, 485-489.
2. Agusti, A., Morla, M., Sauleda, J., Saus, C. & Busquets, X. (2004) NF-kappaB activation and iNOS upregulation in skeletal muscle of patients with COPD and low body weight. Thorax 59, 483-487.
3. Ali, N.A., O'Brien, J.M. Jr, Hoffmann, S.P., Phillips, G., Garland, A., Finley, J.C., Almoosa, K., Hejal, R., Wolf, K.M., Lemeshow, S., Connors, A.F. Jr & Marsh, C.B. (2008) Acquired weakness, handgrip strength, and mortality in critically ill patients. Am. J. Respir. Crit. Care Med. 178, 261-268.
4. Anthony, J.C., Anthony, T.G., Kimball, S.R. & Jefferson, L.S. (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131, 856S-860S.
5. Anzueto, A. (1999) Muscle dysfunction in the intensive care unit. Clin. Chest Med. 20, 435-452.
6. Aquilani, R., Opasich, C., Gualco, A., Verri, M., Testa, A., Pasini, E., Viglio, S., Iadarola, P., Pastoris, O., Dossena, M. & Boschi, F. (2008) Adequate energy-protein intake is not enough to improve nutritional and metabolic status in muscle-depleted patients with chronic heart failure. Eur. J. Heart Fail. 10, 1127-1135.
7. Atkins, D., Best, D., Briss, P.A., Eccles, M., Falck-Ytter, Y., Flottorp, S., Guyatt, G.H., Harbour, R.T., Haugh, M.C., Henry, D., Hill, S., Jaeschke, R., Leng, G., Liberati, A., Magrini, N., Mason, J., Middleton, P., Mrukowicz, J., O'Connell, D., Oxman, A.D., Phillips, B., Schunemann, H.J., Edejer, T.T., Varonen, H., Vist, G.E., Williams, J.W. Jr & Zaza, S. (2004) Grading quality of evidence and strength of recommendations. BMJ. 328, 1490.
8. Attaix, D., Mosoni, L., Dardevet, D., Combaret, L., Mirand, P.P. & Grizard, J. (2005) Altered responses in skeletal muscle protein turnover during aging in anabolic and catabolic periods. Int. J. Biochem. Cell Biol. 37, 1962-1973.
9. Bienvenu, O.J., Colantuoni, E., Mendez-Tellez, P.A., Dinglas, V.D., Shanholtz, C., Husain, N., Dennison, C.R., Herridge, M.S., Pronovost, P.J. & Needham, D.M. (2012) Depressive symptoms and impaired physical function after acute lung injury: a 2-year longitudinal study. Am. J. Respir. Crit. Care Med. 185, 517-524.
10. Borsheim, E., Bui, Q.U., Tissier, S., Kobayashi, H., Ferrando, A.A. & Wolfe, R.R. (2008) Effect of amino acid supplementation on muscle mass, strength and physical function in elderly. Clin. Nutr. 27, 189-195.
11. Breen, L. & Phillips, S.M. (2011) Skeletal muscle protein metabolism in the elderly: interventions to counteract the 'anabolic resistance' of ageing. Nutr. Metab. (Lond.) 8, 68.
12. Breuille, D., Bechereau, F., Buffiere, C., Denis, P., Pouyet, C. & Obled, C. (2006) Beneficial effect of amino acid supplementation, especially cysteine, on body nitrogen economy in septic rats. Clin. Nutr. 25, 634-642.
13. Brooks, N., Cloutier, G.J., Cadena, S.M., Layne, J.E., Nelsen, C.A., Freed, A.M., Roubenoff, R. & Castaneda-Sceppa, C. (2008) Resistance training and timed essential amino acids protect against the loss of muscle mass and strength during 28 days of bed rest and energy deficit. J. Appl. Physiol. 105, 241-248.
14. Callahan, L.A. & Supinski, G.S. (2009) Sepsis-induced myopathy. Crit. Care Med. 37(10 Suppl.), S354-S367.
15. Carmeli, E., Coleman, R. & Reznick, A.Z. (2002) The biochemistry of aging muscle. Exp. Gerontol. 37, 477-489.
16. Casperson, S.L., Sheffield-Moore, M., Hewlings, S.J. & Paddon-Jones, D. (2012) Leucine supplementation chronically improves muscle protein synthesis in older adults consuming the RDA for protein. Clin. Nutr. 31, 512-519.
17. Clark, R.H., Feleke, G., Din, M., Yasmin, T., Singh, G., Khan, F.A. & Rathmacher, J.A. (2000) Nutritional treatment for acquired immunodeficiency virus-associated wasting using beta-hydroxy beta-methylbutyrate, glutamine, and arginine: a randomized, double-blind, placebo-controlled study. JPEN J.Parenter.Enteral Nutr. 24, 133-139.
18. Crozier, S.J., Kimball, S.R., Emmert, S.W., Anthony, J.C. & Jefferson, L.S. (2005) Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J. Nutr. 135, 376-382.
19. Cynober, L. & Harris, R.A. (2006) Symposium on branched-chain amino acids: conference summary. J. Nutr. 136(1 Suppl.), 333S-336S.
20. Dal Negro, R.W., Aquilani, R., Bertacco, S., Boschi, F., Micheletto, C. & Tognella, S. (2010) Comprehensive effects of supplemented essential amino acids in patients with severe COPD and sarcopenia. Monaldi Arch. Chest Dis. 73, 25-33.
21. Dickinson, J.M., Fry, C.S., Drummond, M.J., Gundermann, D.M., Walker, D.K., Glynn, E.L., Timmerman, K.L., Dhanani, S., Volpi, E. & Rasmussen, B.B. (2011) Mammalian target of rapamycin complex 1 activation is required for the stimulation of human skeletal muscle protein synthesis by essential amino acids. J. Nutr. 141, 856-862.
22. Dillon, E.L., Sheffield-Moore, M., Paddon-Jones, D., Gilkison, C., Sanford, A.P., Casperson, S.L., Jiang, J., Chinkes, D.L. & Urban, R.J. (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, 1630-1637.
23. Dodd, S.L., Gagnon, B.J., Senf, S.M., Hain, B.A. & Judge, A.R. (2010) Ros-mediated activation of NF-kappaB and Foxo during muscle disuse. Muscle Nerve 41, 110-113.
24. Engelen, M.P., Rutten, E.P., De Castro, C.L., Wouters, E.F., Schols, A.M. & Deutz, N.E. (2007) Supplementation of soy protein with branched-chain amino acids alters protein metabolism in healthy elderly and even more in patients with chronic obstructive pulmonary disease. Am. J. Clin. Nutr. 85, 431-439.
25. Ershler, W.B. & Keller, E.T. (2000) Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu. Rev. Med. 51, 245-270.
26. Ferrando, A.A., Paddon-Jones, D. & Wolfe, R.R. (2006) Bed rest and myopathies. Curr. Opin. Clin. Nutr. Metab. Care 9, 410-415.
27. Ferrando, A.A., Paddon-Jones, D., Hays, N.P., Kortebein, P., Ronsen, O., Williams, R.H., McComb, A., Symons, T.B., Wolfe, R.R. & Evans, W. (2010) EAA supplementation to increase nitrogen intake improves muscle function during bed rest in the elderly. Clin. Nutr. 29, 18-23.
28. Freyssenet, D., Berthon, P., Denis, C., Barthelemy, J.C., Guezennec, C.Y. & Chatard, J.C. (1996) Effect of a 6-week endurance training programme and branched-chain amino acid supplementation on histomorphometric characteristics of aged human muscle. Arch. Physiol. Biochem. 104, 157-162.
29. Fuld, J.P., Kilduff, L.P., Neder, J.A., Pitsiladis, Y., Lean, M.E., Ward, S.A. & Cotton, M.M. (2005) Creatine supplementation during pulmonary rehabilitation in chronic obstructive pulmonary disease. Thorax 60, 531-537.
30. Gamrin, L., Andersson, K., Hultman, E., Nilsson, E., Essen, P. & Wernerman, J. (1997) Longitudinal changes of biochemical parameters in muscle during critical illness. Metabolism 46, 756-762.
31. Gerovasili, V., Stefanidis, K., Vitzilaios, K., Karatzanos, E., Politis, P., Koroneos, A., Chatzimichail, A., Routsi, C., Roussos, C. & Nanas, S. (2009) Electrical muscle stimulation preserves the muscle mass of critically ill patients: a randomized study. Crit. Care 13, R161.
32. Glynn, E.L., Fry, C.S., Drummond, M.J., Timmerman, K.L., Dhanani, S., Volpi, E. & Rasmussen, B.B. (2010) Excess leucine intake enhances muscle anabolic signaling but not net protein anabolism in young men and women. J. Nutr. 140, 1970-1976.
33. Gosker, H.R., Kubat, B., Schaart, G., van der Vusse, G.J., Wouters, E.F. & Schols, A.M. (2003) Myopathological features in skeletal muscle of patients with chronic obstructive pulmonary disease. Eur. Respir. J. 22, 280-285.
34. Griffiths, R.D. & Hall, J.B. (2010) Intensive care unit-acquired weakness. Crit. Care Med. 38, 779-787.
35. Herndon, D.N., Hart, D.W., Wolf, S.E., Chinkes, D.L. & Wolfe, R.R. (2001) Reversal of catabolism by beta-blockade after severe burns. N. Engl. J. Med. 345, 1223-1229.
36. Herndon, D.N., Rodriguez, N.A., Diaz, E.C., Hegde, S., Jennings, K., Mlcak, R.P., Suri, J.S., Lee, J.O., Williams, F.N., Meyer, W., Suman, O.E., Barrow, R.E., Jeschke, M.G. & Finnerty, C.C. (2012) Long-term propranolol use in severely burned pediatric patients: a randomized controlled study. Ann. Surg. 256, 402-411.
37. Herridge, M.S., Tansey, C.M., Matte, A., Tomlinson, G., Diaz-Granados, N., Cooper, A., Guest, C.B., Mazer, C.D., Mehta, S., Stewart, T.E., Kudlow, P., Cook, D., Slutsky, A.S. & Cheung, A.M. (2011) Functional disability 5 years after acute respiratory distress syndrome. N. Engl. J. Med. 364, 1293-1304.
38. Hsieh, L.C., Chien, S.L., Huang, M.S., Tseng, H.F. & Chang, C.K. (2006) Anti-inflammatory and anticatabolic effects of short-term beta-hydroxy-beta-methylbutyrate supplementation on chronic obstructive pulmonary disease patients in intensive care unit. Asia Pac. J. Clin. Nutr. 15, 544-550.
39. Jagoe, R.T. & Engelen, M.P. (2003) Muscle wasting and changes in muscle protein metabolism in chronic obstructive pulmonary disease. Eur. Respir. J. Suppl. 46, 52s-63s.
40. Jensen, G.L., Miller, R.H., Talabiska, D.G., Fish, J. & Gianferante, L. (1996) A double-blind, prospective, randomized study of glutamine-enriched compared with standard peptide-based feeding in critically ill patients. Am. J. Clin. Nutr. 64, 615-621.
41. Jeschke, M.G., Finnerty, C.C., Suman, O.E., Kulp, G., Mlcak, R.P. & Herndon, D.N. (2007) The effect of oxandrolone on the endocrinologic, inflammatory, and hypermetabolic responses during the acute phase postburn. Ann. Surg. 246, 351-360.
42. Jespersen, J.G., Nedergaard, A., Reitelseder, S., Mikkelsen, U.R., Dideriksen, K.J., Agergaard, J., Kreiner, F., Pott, F.C., Schjerling, P. & Kjaer, M. (2011) Activated protein synthesis and suppressed protein breakdown signaling in skeletal muscle of critically ill patients. PLoS One 6, e18090.
43. Kamel, H.K. (2003) Sarcopenia and aging. Nutr. Rev. 61, 157-167.
44. Katsanos, C.S., Kobayashi, H., Sheffield-Moore, M., Aarsland, A. & Wolfe, R.R. (2005) Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am. J. Clin. Nutr. 82, 1065-1073.
45. Katsanos, C.S., Kobayashi, H., Sheffield-Moore, M., Aarsland, A. & Wolfe, R.R. (2006) A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am. J. Physiol. Endocrinol. Metab 291, E381-E387.
46. Kazi, A.A., Pruznak, A.M., Frost, R.A. & Lang, C.H. (2011) Sepsis-induced alterations in protein-protein interactions within mTOR complex 1 and the modulating effect of leucine on muscle protein synthesis. Shock 35, 117-125.
47. Kress, J.P. (2009) Clinical trials of early mobilization of critically ill patients. Crit. Care Med. 37(10 Suppl.), S442-S447.
48. Kuhls, D.A., Rathmacher, J.A., Musngi, M.D., Frisch, D.A., Nielson, J., Barber, A., MacIntyre, A.D., Coates, J.E. & Fildes, J.J. (2007) Beta-hydroxy-beta-methylbutyrate supplementation in critically ill trauma patients. J. Trauma 62, 125-131.
49. Ladner, K.J., Caligiuri, M.A. & Guttridge, D.C. (2003) Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products. J. Biol. Chem. 278, 2294-2303.
50. Mansoor, O., Breuille, D., Bechereau, F., Buffiere, C., Pouyet, C., Beaufrere, B., Vuichoud, J., Van't-Of, M. & Obled, C. (2007) Effect of an enteral diet supplemented with a specific blend of amino acid on plasma and muscle protein synthesis in ICU patients. Clin. Nutr. 26, 30-40.
51. May, P.E., Barber, A., D'Olimpio, J.T., Hourihane, A. & Abumrad, N.N. (2002) Reversal of cancer-related wasting using oral supplementation with a combination of beta-hydroxy-beta-methylbutyrate, arginine, and glutamine. Am. J. Surg. 183, 471-479.
52. McCarthy, J.J. & Esser, K.A. (2010) Anabolic and catabolic pathways regulating skeletal muscle mass. Curr. Opin. Clin. Nutr. Metab Care 13, 230-235.
53. Moher, D., Liberati, A., Tetzlaff, J. & Altman, D.G.; The PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6, e1000097.
54. Morley, J.E. & Baumgartner, R.N. (2004) Cytokine-related aging process. J. Gerontol. A Biol. Sci. Med. Sci. 59, M924-M929.
55. National Institute for Health and Care Excellence (NICE). (2009) Rehabilitation after Critical Illness, (CG83). Available at: http://guidance.nice.org.uk/CG83 (accessed on March 2009).
56. Oudijk, E.J., Lammers, J.W. & Koenderman, L. (2003) Systemic inflammation in chronic obstructive pulmonary disease. Eur. Respir. J. Suppl. 46, 5s-13s.
57. Paddon-Jones, D., Sheffield-Moore, M., Creson, D.L., Sanford, A.P., Wolf, S.E., Wolfe, R.R. & Ferrando, A.A. (2003) Hypercortisolemia alters muscle protein anabolism following ingestion of essential amino acids. Am. J. Physiol. Endocrinol. Metab 284, E946-E953.
58. Paddon-Jones, D., Sheffield-Moore, M., Urban, R.J., Sanford, A.P., Aarsland, A., Wolfe, R.R. & Ferrando, A.A. (2004) Essential amino acid and carbohydrate supplementation ameliorates muscle protein loss in humans during 28 days bedrest. J. Clin. Endocrinol. Metab. 89, 4351-4358.
59. Paddon-Jones, D., Sheffield-Moore, M., Urban, R.J., Aarsland, A., Wolfe, R.R. & Ferrando, A.A. (2005) The catabolic effects of prolonged inactivity and acute hypercortisolemia are offset by dietary supplementation. J. Clin. Endocrinol. Metab. 90, 1453-1459.
60. Parry, S.M., Berney, S., Granger, C.L., Koopman, R., El-Ansary, D. & Denehy, L. (2013) Electrical muscle stimulation in the intensive care setting: a systematic review. Crit. Care Med. 41, 2406-2418.
61. Plank, L.D. & Hill, G.L. (2000) Similarity of changes in body composition in intensive care patients following severe sepsis or major blunt injury. Ann. N. Y. Acad. Sci. 904, 592-602.
62. Puthucheary, Z.A., Rawal, J., McPhail, M., Connolly, B., Ratnayake, G., Chan, P., Hopkinson, N.S., Padhke, R., Dew, T., Sidhu, P.S., Velloso, C., Seymour, J., Agley, C.C., Selby, A., Limb, M., Edwards, L.M., Smith, K., Rowlerson, A., Rennie, M.J., Moxham, J., Harridge, S.D., Hart, N. & Montgomery, H.E. (2013) Acute skeletal muscle wasting in critical illness. JAMA. 310, 1591-1600.
63. Reid, C.L., Campbell, I.T. & Little, R.A. (2004) Muscle wasting and energy balance in critical illness. Clin. Nutr. 23, 273-280.
64. Rennie, M.J., Bohe, J., Smith, K., Wackerhage, H. & Greenhaff, P. (2006) Branched-chain amino acids as fuels and anabolic signals in human muscle. J. Nutr. 136(1 Suppl.), 264S-268S.
65. Rieu, I., Balage, M., Sornet, C., Giraudet, C., Pujos, E., Grizard, J., Mosoni, L. & Dardevet, D. (2006) Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia. J. Physiol. 575, 305-315.
66. Rondanelli, M., Opizzi, A., Antoniello, N., Boschi, F., Iadarola, P., Pasini, E., Aquilani, R. & Dioguardi, F.S. (2011) Effect of essential amino acid supplementation on quality of life, amino acid profile and strength in institutionalized elderly patients. Clin. Nutr. 30, 571-577.
67. Roubenoff, R. & Hughes, V.A. (2000) Sarcopenia: current concepts. J. Gerontol. A Biol. Sci. Med. Sci. 55, M716-M724.
68. Soeters, P.B. & Grimble, R.F. (2009) Dangers, and benefits of the cytokine mediated response to injury and infection. Clin. Nutr. 28, 583-596.
69. Stein, T.P., Schluter, M.D., Leskiw, M.J. & Boden, G. (1999) Attenuation of the protein wasting associated with bed rest by branched-chain amino acids. Nutrition 15, 656-660.
70. Takala, J., Ruokonen, E., Webster, N.R., Nielsen, M.S., Zandstra, D.F., Vundelinckx, G. & Hinds, C.J. (1999) Increased mortality associated with growth hormone treatment in critically ill adults. N. Engl. J. Med. 341, 785-792.
71. de Theije, C., Costes, F., Langen, R.C., Pison, C. & Gosker, H.R. (2011) Hypoxia and muscle maintenance regulation: implications for chronic respiratory disease. Curr. Opin. Clin. Nutr. Metab. Care 14, 548-553.
72. Verhoeven, S., Vanschoonbeek, K., Verdijk, L.B., Koopman, R., Wodzig, W.K., Dendale, P. & van Loon, L.J. (2009) Long-term leucine supplementation does not increase muscle mass or strength in healthy elderly men. Am. J. Clin. Nutr. 89, 1468-1475.
73. Vescovo, G., Serafini, F., Facchin, L., Tenderini, P., Carraro, U., Dalla, L.L., Catani, C. & Ambrosio, G.B. (1996) Specific changes in skeletal muscle myosin heavy chain composition in cardiac failure: differences compared with disuse atrophy as assessed on microbiopsies by high resolution electrophoresis. Heart 76, 337-343.
74. Volpi, E., Kobayashi, H., Sheffield-Moore, M., Mittendorfer, B. & Wolfe, R.R. (2003) Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am. J. Clin. Nutr. 78, 250-258.
75. Winkelman, C. (2010) The role of inflammation in ICU-acquired weakness. Crit. Care 14, 186.
76. Yende, S., Waterer, G.W., Tolley, E.A., Newman, A.B., Bauer, D.C., Taaffe, D.R., Jensen, R., Crapo, R., Rubin, S., Nevitt, M., Simonsick, E.M., Satterfield, S., Harris, T. & Kritchevsky, S.B. (2006) Inflammatory markers are associated with ventilatory limitation and muscle dysfunction in obstructive lung disease in well functioning elderly subjects. Thorax 61, 10-16.