Feeding critically ill patients the right ‘whey’: thinking outside of the box. A personal view

Annals of Intensive Care

Volumn 5, Issue 1, 2015, Pages

  Marik, Paul E ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

Autophagy; Continuous feeding; Incretin; Insulin; Intermittent feeding; Metabolic function; MTOR; Muscle atrophy; Muscle mass; Nutrition; Ubiquitin proteasome complex; Whey

Indexed keywords

LEUCINE; MUSCLE PROTEIN;

ACUTE DISEASE; AMINO ACID SYNTHESIS; CRITICALLY ILL PATIENT; ENTERIC FEEDING; FEEDING; HUMAN; NUTRITIONAL SUPPORT; PARENTERAL NUTRITION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DIET; PROTEIN INTAKE; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TRANSLATION INITIATION; WHEY;

EID: 84930934362     PISSN: None     EISSN: 21105820     Source Type: Journal    
DOI: 10.1186/s13613-015-0051-2     Document Type: Review

References (95)

1. Batt J, dos Santos CC, Herridge MS. Muscle injury during critical illness. JAMA. 2013;310:1569–70.
2. Kress JP, Hall JB. ICU-acquired weakness and recovery from critical illness. N Engl J Med. 2014;370:1626–35.
3. Fan E, Cheek F, Chlan L, Gosselink R, Hart N, Herridge MS, et al. An Official American Thoracic Society Clinical Practice Guideline: the diagnosis of intensive care unit-acquired weakness in adults. Am J Respir Crit Care Med. 2014;190:1437–46.
4. Wollersheim T, Woehlecke J, Krebs M, Hamati J, Lodka D, Luther-Schroeder A, et al. Dynamics of myosin degradation in intensive care unit-acquired weakness during severe critical illness. Intensive Care Med. 2014;40:528–38.
5. Stevens RD, Dowdy DW, Michaels RK, Mendez-Tellez PA, Pronovost PJ, Needham DM. Neuromuscular dysfunction acquired in critical illness: a systematic review. Intensive Care Med. 2007;33:1876–91.
6. Herridge MS, Cheung AM, Tansey CM, Matte-Martyn A, Diaz-Granados N, Al-Saidi F, et al. One-year outcomes in survivors of the acute respiratory distress syndrome. N Engl J Med. 2003;348:683–93.
7. Herridge MS, Tansey CM, Matte A, Tomlionson G, Diaz-Granados N, Cooper A, et al. Functional disability 5 years after acute respiratory distress syndrome. N Engl J Med. 2011;364:1293–304.
8. Phillips BE, Hill DS, Atherton PJ. Regulation of muscle protein synthesis in humans. Curr Opin Clin Nutr Metab Care. 2012;15:58–63.
9. Rennie MJ, Wackerhage H, Spangenburg EE, Booth FW. Control of the size of the human muscle mass. Annu Rev Physiol. 2004;66:799–828.
10. Atherton PJ, Etheridge T, Watt PW, Wilkinson D, Selby A, Rankin D, et al. Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am J Clin Nutr. 2010;92:1080–8.
11. Mitchell WK, Phillips BE, Williams JP, Rankin D, Lund JN, Smith K, et al. A dose- rather than delivery profile-dependent mechanism regulates the "muscle-full" effect in response to oral essential amino acid intake in young men. J Nutr. 2015;145:207–14.
12. Staples AW, Burd NA, West DW, Currie KD, Atherton PJ, Moore DR, et al. Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Med Sci Sports Exerc. 2011;43:1154–61.
13. Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310:1591–600.
14. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 2004;18:39–51.
15. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA. 2001;98:14440–5.
16. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science. 2001;294:1704–8.
17. Klaude M, Mori M, Tjader I, Gustafsson T, Wernerman J, Rooyackers O. Protein metabolism and gene expression in skeletal muscle of critically ill patients with sepsis. Clin Sci. 2012;122:133–42.
18. Lecker SH, Lecker SH. Ubiquitin-protein ligases in muscle wasting: multiple parallel pathways? Curr Opin Clin Nutr Metab Care. 2003;6:271–5.
19. Levine S, Biswas C, Dierov J, Barsotti R, Shrager JB, Nguyen T, et al. Increased proteolysis, myosin depletion, and atrophic AKT-FOXO signaling in human diaphragm disuse. Am J Respir Crit Care Med. 2011;183:483–90.
20. Smith IJ, Alamdari N, O'Neal P, Gonnella P, Aversa Z, Hasselgren PO. Sepsis increases the expression and activity of the transcription factor Forkhead Box O 1 (FOXO1) in skeletal muscle by a glucocorticoid-dependent mechanism. Int J Biochem Cell Biol. 2010;42:701–11.
21. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 2004;117:399–412.
22. Constantin D, McCullough J, Mahajan RP, Greenhaff PL, Constantin D, McCullough J, et al. Novel events in the molecular regulation of muscle mass in critically ill patients. J Physiol. 2011;589:3883–95.
23. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, et al. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem. 2005;280:2737–44.
24. Zhao X, Gan L, Pan H, Kan D, Majeski M, Adam SA, et al. Multiple elements regulate nuclear/cytoplasmic shuttling of FOXO1: characterization of phosphorylation- and 14-3-3-dependent and -independent mechanisms. Biochem J. 2004;378:839–49.
25. Dickinson JM, Fry CS, Drummond MJ, Gundermann DM, Walker DK, Glynn EL, et al. Mammalian target of rapamycin complex 1 activation is required for the stimulation of human skeletal muscle protein synthesis by essential amino acids. J Nutr. 2011;141:856–62.
26. Farnfield MM, Carey KA, Gran P, Trenerry MK, Cameron-Smith D. Whey protein ingestion activates mTOR-dependent signalling after resistance exercise in young men: a double-blinded randomized controlled trial. Nutrients. 2009;1:263–75.
27. Burd NA, Yang Y, Moore DR, Tang JE, Tarnopolsky MA, Phillips SM. Greater stimulation of myofibrillar protein synthesis with ingestion of whey protein isolate v. micellar casein at rest and after resistance exercise in elderly men. Br J Nutr. 2012;108:958–62.
28. Karlsson HK, Nilsson PA, Nilsson J, Chibalin AV, Zierath JR, Blomstrand E. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab. 2004;287:E1–7.
29. Blomstrand E, Eliasson J, Karlsson HK, Kohnke R. Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. J Nutr. 2006;136:269S–73.
30. Anthony JC, Anthony TG, Kimball SR, Jefferson LS. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr. 2001;131:856S–60.
31. Reynolds TH, Bodine SC, Lawrence Jr JC. Control of Ser2448 phosphorylation in the mammalian target of rapamycin by insulin and skeletal muscle load. J Biol Chem. 2002;277:17657–62.
32. Timmerman KL, Lee JL, Dreyer HC, Dhanani S, Glynn EL, Fry CS, et al. Insulin stimulates human skeletal muscle protein synthesis via an indirect mechanism involving endothelial-dependent vasodilation and mammalian target of rapamycin complex 1 signaling. J Clin Endocrinol Metab. 2010;95:3848–57.
33. Jakubowicz D, Froy O. Biochemical and metabolic mechanisms by which dietary whey protein may combat obesity and Type 2 diabetes. J Nutr Biochem. 2013;24:1–5.
34. Norton LE, Layman DK, Bunpo P, Anthony TG, Brana DV, Garlick PJ. The leucine content of a complete meal directs peak activation but not duration of skeletal muscle protein synthesis and mammalian target of rapamycin signaling in rats. J Nutr. 2009;139:1103–9.
35. Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, van Loon LJ. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr. 2011;93:997–1005.
36. Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J Appl Physiol. 2009;107:987–92.
37. Verreijen AM, Verlaan S, Engberink MF, Swinkels S, deVogel-van den Bosch J, Weijs PJ. A high whey protein-, leucine-, and vitamin D-enriched supplement preserves muscle mass during intentional weight loss in obese older adults: a double=blind randomized controlled trial. Am J Clin Nutr. 2015;101:279–86.
38. Katsanos CS, Chinkes DL, Paddon-Jones D, Zhang XJ, Aarsland A, Wolfe RR. Whey protein ingestion in elderly persons results in greater muscle protein accrual than ingestion of its constituent essential amino acid content. Nutr Res. 2008;28:651–8.
39. Nilsson M, Stenberg M, Frid AH, Holst JJ, Bjorck IM. Glycemia and insulinemia in healthy subjects after lactose-equivalent meals of milk and other food proteins: the role of plasma amino acids and incretins. Am J Clin Nutr. 2004;80:1246–53.
40. Nilsson M, Holst JJ, Bjorck IM. Metabolic effects of amino acid mixtures and whey protein in healthy subjects: studies using glucose-equivalent drinks. Am J Clin Nutr. 2007;85:996–1004.
41. Blagosklonny MV. Hypoxia, MTOR and autophagy: converging on senescence or quiescence. Autophagy. 2013;9:260–2.
42. Tsutsumi R, Horikawa Y, Kume K, Tanaka K, Kasai A, Kadota T, Tsutsumi Y. Whey-protein based formulas are protective in LPS mediated sepsis. JPEN. 2014; ePub.
43. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, et al. Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am J Clin Nutr. 2011;93:402–12.
44. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, et al. Omega-3 polyunsaturated fatty acids augment the muscle protein anabolic response to hyperinsulinaemia-hyperaminoacidaemia in healthy young and middle-aged men and women. Clin Sci. 2011;121:267–78.
45. Suryawan A, O'Connor PM, Bush JA, Nguyen HV, Davis TA. Differential regulation of protein synthesis by amino acids and insulin in peripheral and visceral tissues of neonatal pigs. Amino Acids. 2009;37:97–104.
46. O'Connor PM, Bush JA, Suryawan A, Nguyen HV, Davis TA. Insulin and amino acids independently stimulate skeletal muscle protein synthesis in neonatal pigs. Am J Physiol Endocrinol Metab. 2003;284:E110–9.
47. Wilson FA, Suryawan A, Orellana RA, Kimball SR, Gazzaneo MC, Nguyen HV, et al. Feeding rapidly stimulates protein synthesis in skeletal muscle of neonatal pigs by enhancing translation initiation. J Nutr. 2009;139:1873–80.
48. Bohe J, Low JF, Wolfe RR, Rennie MJ. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. J Physiol. 2001;532:575–9.
49. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, et al. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr. 2009;89:161–8.
50. West DW, Burd NA, Coffey VG, Baker SK, Burke LM, Hawley JA, et al. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am J Clin Nutr. 2011;94:795–803.
51. Gazzaneo MC, Suryawan A, Orellana RA, Torrazza RM, El-Kadi SW, Wilson FA, et al. Intermittent bolus feeding has a greater stimulatory effect on protein synthesis in skeletal muscle than continuous feeding in neonatal pigs. J Nutr. 2011;141:2152–8.
52. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, et al. Age-related differences in the dose–response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol. 2009;587:211–7.
53. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, et al. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005;19:422–4.
54. Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD. Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am J Clin Nutr. 2014;99:86–95.
55. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, et al. Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr. 2012;108:1780–8.
56. Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of 10 days of bed rest on skeletal muscle in healthy older adults. JAMA. 2007;297:1772–4.
57. Breen L, Stokes KA, Churchward-Venne TA, Moore DR, Baker SK, Smith K, et al. Two weeks of reduced activity decreases leg lean mass and induces "anabolic resistance" of myofibrillar protein synthesis in healthy elderly. J Clin Endocrinol Metab. 2013;98:2604–12.
58. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, et al. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol. 2008;586:6049–61.
59. Lang CH, Frost RA, Nairn AC, MacLean DA, Vary TC. TNF-alpha impairs heart and skeletal muscle protein synthesis by altering translation initiation. Am J Physiol Endocrinol Metab. 2002;282:E336–47.
60. Lang CH, Frost RA. Sepsis-induced suppression of skeletal muscle translation initiation mediated by tumor necrosis factor alpha. Metabolism. 2007;56:49–57.
61. Lang CH, Frost RA. Endotoxin disrupts the leucine-signaling pathway involving phosphorylation of mTOR, 4E-BP1, and S6K1 in skeletal muscle. J Cell Physiol. 2005;203:144–55.
62. Balage M, Averous J, Remond D, Bos C, Pujos-Guillot E, Papet I, et al. Presence of low-grade inflammation impaired postprandial stimulation of muscle protein synthesis in old rats. J Nutr Biochem. 2010;21:325–31.
63. Vary TC. Acute oral leucine administration stimulates protein synthesis during chronic sepsis through enhanced association of eukaryotic initiation factor 4G with eukaryotic initiation factor 4E in rats. J Nutr. 2007;137:2074–9.
64. Atherton PJ. Is there an optimal time for warfighters to supplement with protein? J Nutr. 2013;143:1848S–51.
65. Initial trophic vs full enteral feeding in patients with acute lung injury. The EDEN randomized trial. JAMA. 2012; 307:795–803.
66. Arabi YM, Tamim HM, Dhar GS, Al-Dawood A, Al-Sultan M, Sakkijha MH, et al. Permissive underfeeding and intensive insulin therapy in critically ill patients: a randomized controlled trial. Am J Clin Nutr. 2011;93:569–77.
67. Heyland DK, Murch L, Cahill N, McCall M, Muscedere J, Stelfox HT, et al. Enhanced protein-energy provision via the enteral route feeding protocol in critically ill patients: Results of a cluster randomized trial. Crit Care Med. 2013;41:2743–53.
68. Charles EJ, Petroze RT, Metzger R, Hranjec T, Rosenberger LH, Riccio LM, et al. Hypocaloric compared with eucaloric nutritional support and its effect on infection rates in a surgical intensive care unit: a randomized controlled trial. Am J Clin Nutr. 2014;100:1337–43.
69. Needham DM, Dinglas VD, Bienvenu OJ, Colantuoni E, Wozniak AW, Rice TW, et al. One year outcomes in patients with acute lung injury randomised to initial trophic or full enteral feeding: prospective follow-up of EDEN randomised trial. BMJ. 2013;346:f1532.
70. Needham DM, Dinglas VD, Morris PE, Jackson JC, Hough CL, Mendez-Tellez PA, et al. Physical and cognitive performance of acute lung injury patients one year after initial trophic vs full enteral feeding: EDEN trial follow-up. Am J Respir Crit Care Med. 2013;188:567–76.
71. Casaer MP, Mesotten D, Hermans G, Wouters PJ, Schetz M, Meyfroidt G, et al. Early versus late parenteral nutrition in critically ill adults. N Engl J Med. 2011;365:506–17.
72. Casaer MP, Wilmer A, Hermans G, Wouters PJ, Mesotten D, van den Berghe G. Role of disease and macronutrient dose in the randomized controlled EPaNIC trial. A Post Hoc Analysis Am J Respir Crit Care Med. 2013;187:247–55.
73. McClave SA, Martindale RG, Vanek VW, McCarthy M, Roberts P, Taylor B, et al. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: Society of Critical Care Medicine (SCCM) and American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.). JPEN. 2009;33:277–316.
74. MacLeod JB, Lefton J, Houghton D, Roland C, Doherty J, Cohn SM, et al. Prospective randomized control trial of intermittent versus continuous gastric feeds for critically ill trauma patients. J Trauma. 2007;63:57–61.
75. Drucker DJ. Enhancing the action of incretin hormones: a new whey forward? Endocrinology. 2006;147:3171–2.
76. Phillips LK, Prins JB. Update on incretin hormones. Ann New York Acad Sci. 2011;1243:E55–74.
77. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. 2007;87:1409–39.
78. Stoll B, Puiman PJ, Cui L, Chang X, Benight NM, Bauchart-Thevret C, et al. Continuous parenteral and enteral nutrition induces metabolic dysfunction in neonatal pigs. JPEN. 2012;36:538–50.
79. Shulman RJ, Redel CA, Stathos TH. Bolus versus continuous feedings stimulate small-intestinal growth and development in the newborn pig. J Pediat Gastroenterol Nutr. 1994;18:350–4.
80. Chowdhury AH, Murray K, Hoad CL, Costigan C, Marciani L, MacDonald IA, et al. Effects of bolus and continuous nasogastric feeding on gastric emptying, small bowel water content, superior mesenteric artery blood flow, and plasma hormone concentrations in heathy adults. A randomized crossover study. Ann Surg. 2015; ePub.
81. Subaran SC, Sauder MA, Chai W, Jahn LA, Fowler DE, Aylor KW, et al. GLP-1 at physiological concentrations recruits skeletal and cardiac muscle microvasculature in healthy humans. Clin Sci. 2014;127:163–70.
82. Chai W, Dong Z, Wang N, Wang W, Tao L, Cao W, et al. Glucagon-like peptide 1 recruits microvasculature and increases glucose use in muscle via a nitric oxide-dependent mechanism. Diabetes. 2012;61:888–96.
83. Cho YM, Fujita Y, Kieffer TJ. Glucagon-like peptide-1: glucose homeostasis and beyond. Annu Rev Plant Physiol Plant Mol Biol. 2014;76:535–59.
84. Yabe D, Seino Y. Incretin actions beyond the pancreas: lessons from knockout mice. Curr Opin Pharmacol. 2013;13:946–53.
85. Mashako MN, Bernard C, Cezard JP, Chayvialle JA, Navarro J. Effect of total parenteral nutrition, constant rate enteral nutrition, and discontinuous oral feeding on plasma cholecystokinin immunoreactivity in children. J Pediatr Gastroenterol Nutr. 1987;6:948–52.
86. Jawaheer G, Shaw NJ, Pierro A, Jawaheer G, Shaw NJ, Pierro A. Continuous enteral feeding impairs gallbladder emptying in infants. J Pediatr. 2001;138:822–5.
87. Barie PS, Eachempati SR. Acute acalculous cholecystitis. Gastroenterol Clin North Am. 2010;39:343–57.
88. Serpa LF, Kimura M, Faintuch J, Cecenella I. Effects of continuous versus bolus infusion of enteral nutrition in critical patients. Rev Hosp Clin Fac Med S Paulo. 2003;58:9–14.
89. Maurya I, Pawar M, Garg R, Kaur M, Sood R. Comparison of respiratory quotient and resting energy expenditure in two regimens of enteral feeding - continuous vs. intermittent in head-injured critically ill patients. Saudi J Anaesth. 2011;5:195–201.
90. Ochala J, Gustafson AM, Diez ML, Renaud G, Li M, Aare S, et al. Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: underlying mechanisms. J Physiol. 2011;589:2007–26.
91. Renaud G, Llano-Diez M, Ravara B, Gorza L, Feng HZ, Jin JP, et al. Sparing of muscle mass and function by passive loading in an experimental intensive care unit model. J Physiol. 2013;591:1385–402.
92. Llano-Diez M, Renaud G, Andersson M, Marrero HG, Cacciani N, Engquist H, et al. Mechanisms underlying ICU muscle wasting and effects of passive mechanical loading. Crit Care. 2012;16:R209.
93. Bailey P, Thomsen GE, Spuhler VJ, Blair R, Jewkes J, Bezdjian L, et al. Early activity is feasible and safe in respiratory failure patients. Crit Care Med. 2007;35:139–45.
94. Morris PE, Goad A, Thompson C, Taylor K, Harry B, Passmore L, et al. Early intensive care unit mobility therapy in the treatment of acute respiratory failure. Crit Care Med. 2008;36:2238–43.
95. Kayambu G, Boots R, Paratz J. Physical therapy for the critically ill in the ICU: a systematic review and meta-analysis. Crit Care Med. 2013;41:1543–54.