Supplementing an energy adequate, higher protein diet with protein does not enhance fat-free mass restoration after short-term severe negative energy balance

Journal of Applied Physiology

Volumn 122, Issue 6, 2017, Pages 1485-1493

  Berryman, C E ^a,b   Sepowitz, J J ^a   McClung, H L ^a   Lieberman, H R ^a   Farina, E K ^a,b   McClung, J P ^a   Ferrando, A A ^c   Pasiakos, S M ^a  

^a U S ARMY RESEARCH INSTITUTE OF ENVIRONMENTAL MEDICINE   (United States)

^b OAK RIDGE INSTITUTE FOR SCIENCE AND EDUCATION   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Casein; Muscle; Negative energy balance; Protein balance; Recovery; Whey

Indexed keywords

ADIPOSE TISSUE; ADULT; BODY MASS; CALORIC INTAKE; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; ENERGY METABOLISM; EPIDEMIOLOGY; EXERCISE; HUMAN; MALE; METABOLISM; PHYSIOLOGY; PROCEDURES; PROTEIN DIET; RANDOMIZED CONTROLLED TRIAL; SOLDIER; UNITED STATES; YOUNG ADULT;

ADIPOSE TISSUE; ADULT; BODY MASS INDEX; DIET, HIGH-PROTEIN; DOUBLE-BLIND METHOD; ENERGY INTAKE; ENERGY METABOLISM; EXERCISE; HUMANS; MALE; MILITARY PERSONNEL; UNITED STATES; YOUNG ADULT;

EID: 85019051452     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01039.2016     Document Type: Article

References (41)

1. Abdulla H, Smith K, Atherton PJ, Idris I. Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: a systematic review and meta-analysis. Diabetologia 59: 44–55, 2016. doi:10.1007/s00125-015-3751-0.
2. Anonymous. Nutrition and Menu Standards for Human Performance Optimization. Army Regulation 40–25 OPNAVINST 10110.1/MCO 10110.49 AFI 44–141. Washington, DC: Headquarters, Depts. of the Army, Navy, and Air Force, 2017.
3. Areta JL, Burke LM, Camera DM, West DW, Crawshay S, Moore DR, Stellingwerff T, Phillips SM, Hawley JA, Coffey VG. Reduced resting skeletal muscle protein synthesis is rescued by resistance exercise and protein ingestion following short-term energy deficit. Am J Physiol Endocrinol Metab 306: E989–E997, 2014. doi:10.1152/ajpendo.00590. 2013.
4. Bone JL, Ross ML, Tomcik KA, Jeacocke NA, Hopkins WG, Burke LM. Manipulation of muscle creatine and glycogen changes dxa estimates of body composition. Med Sci Sports Exerc 2016 Nov 28. [Epub ahead of print]. doi:10.1249/MSS.0000000000001174.
5. Carbone JW, McClung JP, Pasiakos SM. Skeletal muscle responses to negative energy balance: effects of dietary protein. Adv Nutr 3: 119–126, 2012. doi:10.3945/an.111.001792.
6. Drummond MJ, Rasmussen BB. Leucine-enriched nutrients and the regulation of mammalian target of rapamycin signalling and human skeletal muscle protein synthesis. Curr Opin Clin Nutr Metab Care 11: 222–226, 2008. doi:10.1097/MCO.0b013e3282fa17fb.
7. Fern EB, Garlick PJ, Waterlow JC. Apparent compartmentation of body nitrogen in one human subject: its consequences in measuring the rate of whole-body protein synthesis with 15N. Clin Sci (Lond) 68: 271–282, 1985. doi:10.1042/cs0680271.
8. Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol Endocrinol Metab 270: E627–E633, 1996.
9. Fortes MB, Diment BC, Greeves JP, Casey A, Izard R, Walsh NP. Effects of a daily mixed nutritional supplement on physical performance, body composition, and circulating anabolic hormones during 8 weeks of arduous military training. Appl Physiol Nutr Metab 36: 967–975, 2011. doi:10.1139/h11-124.
10. Groen BB, Res PT, Pennings B, Hertle E, Senden JM, Saris WH, van Loon LJ. Intragastric protein administration stimulates overnight muscle protein synthesis in elderly men. Am J Physiol Endocrinol Metab 302: E52–E60, 2012. doi:10.1152/ajpendo.00321.2011.
11. Hector AJ, Marcotte GR, Churchward-Venne TA, Murphy CH, Breen L, von Allmen M, Baker SK, Phillips SM. Whey protein supplementation preserves postprandial myofibrillar protein synthesis during short-term energy restriction in overweight and obese adults. J Nutr 145: 246–252, 2015. doi:10.3945/jn.114.200832.
12. Henning PC, Park BS, Kim JS. Physiological decrements during sustained military operational stress. Mil Med 176: 991–997, 2011. doi:10. 7205/MILMED-D-11-00053.
13. Hoyt RW, Friedl KE. Field studies of exercise and food deprivation. Curr Opin Clin Nutr Metab Care 9: 685–690, 2006. doi:10.1097/01.mco. 0000247472.72155.7c.
14. Hoyt RW, Jones TE, Stein TP, McAninch GW, Lieberman HR, Askew EW, Cymerman A. Doubly labeled water measurement of human energy expenditure during strenuous exercise. J Appl Physiol (1985) 71: 16–22, 1991.
15. Hoyt RW, Opstad PK, Haugen AH, DeLany JP, Cymerman A, Friedl KE. Negative energy balance in male and female rangers: effects of 7 d of sustained exercise and food deprivation. Am J Clin Nutr 83: 1068–1075, 2006.
16. Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients). Washington, DC: The National Academies Press, 2005.
17. Keys A, Brozek J, Henschel A, Mickelsen O. The Biology of Human Starvation. Minneapolis, MN: Univ of Minnesota Press, 1950.
18. Lieberman HR, Farina EK, Caldwell J, Williams KW, Thompson LA, Niro PJ, Grohmann KA, McClung JP. Cognitive function, stress hormones, heart rate and nutritional status during simulated captivity in military survival training. Physiol Behav 165: 86 –97, 2016. doi:10.1016/ j.physbeh.2016.06.037.
19. Longland TM, Oikawa SY, Mitchell CJ, Devries MC, Phillips SM. Higher compared with lower dietary protein during an energy deficit combined with intense exercise promotes greater lean mass gain and fat mass loss: a randomized trial. Am J Clin Nutr 103: 738–746, 2016. doi:10.3945/ajcn.115.119339.
20. Margolis LM, Murphy NE, Martini S, Gundersen Y, Castellani JW, Karl JP, Carrigan CT, Teien HK, Madslien EH, Montain SJ, Pasiakos SM. Effects of supplemental energy on protein balance during 4-d arctic military training. Med Sci Sports Exerc 48: 1604 –1612, 2016. doi:10. 1249/MSS.0000000000000944.
21. Margolis LM, Murphy NE, Martini S, Spitz MG, Thrane I, McGraw SM, Blatny JM, Castellani JW, Rood JC, Young AJ, Montain SJ, Gundersen Y, Pasiakos SM. Effects of winter military training on energy balance, whole-body protein balance, muscle damage, soreness, and physical performance. Appl Physiol Nutr Metab 39: 1395–1401, 2014. doi:10. 1139/apnm-2014-0212.
22. Margolis LM, Pasiakos SM, Karl JP, Rood JC, Cable SJ, Williams KW, Young AJ, McClung JP. Differential effects of military training on fat-free mass and plasma amino acid adaptations in men and women. Nutrients 4: 2035–2046, 2012. doi:10.3390/nu4122035.
23. Margolis LM, Rivas DA, Berrone M, Ezzyat Y, Young AJ, McClung JP, Fielding RA, Pasiakos SM. Prolonged calorie restriction downregu-lates skeletal muscle mTORC1 signaling independent of dietary protein intake and associated microRNA expression. Front Physiol 7: 445, 2016. doi:10.3389/fphys.2016.00445.
24. Margolis LM, Rood J, Champagne C, Young AJ, Castellani JW. Energy balance and body composition during US Army special forces training. Appl Physiol Nutr Metab 38: 396 –400, 2013. doi:10.1139/apnm-2012-0323.
25. Morgan CA III, Hazlett G, Southwick S, Rasmusson A, Lieberman HR. Effect of carbohydrate administration on recovery from stress-induced deficits in cognitive function: a double-blind, placebo-controlled study of soldiers exposed to survival school stress. Mil Med 174: 132–138, 2009. doi:10.7205/MILMED-D-58-7808.
26. Murphy CH, Churchward-Venne TA, Mitchell CJ, Kolar NM, Kassis A, Karagounis LG, Burke LM, Hawley JA, Phillips SM. Hypoenergetic diet-induced reductions in myofibrillar protein synthesis are restored with resistance training and balanced daily protein ingestion in older men. Am J Physiol Endocrinol Metab 308: E734 –E743, 2015. doi:10.1152/ajpendo. 00550.2014.
27. Nindl BC, Barnes BR, Alemany JA, Frykman PN, Shippee RL, Friedl KE. Physiological consequences of U.S. Army Ranger training. Med Sci Sports Exerc 39: 1380 –1387, 2007. doi:10.1249/MSS.0b013e318067e2f7.
28. Nindl BC, Leone CD, Tharion WJ, Johnson RF, Castellani JW, Patton JF, Montain SJ. Physical performance responses during 72 h of military operational stress. Med Sci Sports Exerc 34: 1814–1822, 2002. doi:10.1097/00005768-200211000-00019.
29. Pasiakos SM, Austin KG, Lieberman HR, Askew EW. Efficacy and safety of protein supplements for U.S. Armed Forces personnel: consensus statement. J Nutr 143: 1811S–1814S, 2013. doi:10.3945/jn.113.176859.
30. Pasiakos SM, Cao JJ, Margolis LM, Sauter ER, Whigham LD, McClung JP, Rood JC, Carbone JW, Combs GF Jr, Young AJ. Effects of high-protein diets on fat-free mass and muscle protein synthesis following weight loss: a randomized controlled trial. FASEB J 27: 3837–3847, 2013. doi:10.1096/fj.13-230227.
31. Pasiakos SM, McClung HL, McClung JP, Margolis LM, Andersen NE, Cloutier GJ, Pikosky MA, Rood JC, Fielding RA, Young AJ. Leucine-enriched essential amino acid supplementation during moderate steady state exercise enhances postexercise muscle protein synthesis. Am J Clin Nutr 94: 809–818, 2011. doi:10.3945/ajcn.111.017061.
32. Pasiakos SM, Vislocky LM, Carbone JW, Altieri N, Konopelski K, Freake HC, Anderson JM, Ferrando AA, Wolfe RR, Rodriguez NR. Acute energy deprivation affects skeletal muscle protein synthesis and associated intracellular signaling proteins in physically active adults. J Nutr 140: 745–751, 2010. doi:10.3945/jn.109.118372.
33. Res PT, Groen B, Pennings B, Beelen M, Wallis GA, Gijsen AP, Senden JM, VAN Loon LJ. Protein ingestion before sleep improves postexercise overnight recovery. Med Sci Sports Exerc 44: 1560–1569, 2012. doi:10.1249/MSS.0b013e31824cc363.
34. Siri WE. The gross composition of the body. Adv Biol Med Phys 4: 239–280, 1956. doi:10.1016/B978-1-4832-3110-5.50011-X.
35. Stein TP, Rumpler WV, Leskiw MJ, Schluter MD, Staples R, Bodwell CE. Effect of reduced dietary intake on energy expenditure, protein turnover, and glucose cycling in man. Metabolism 40: 478–483, 1991. doi:10.1016/0026-0495(91)90228-O.
36. Subar AF, Freedman LS, Tooze JA, Kirkpatrick SI, Boushey C, Neuhouser ML, Thompson FE, Potischman N, Guenther PM, Tara-suk V, Reedy J, Krebs-Smith SM. Addressing current criticism regarding the value of self-report dietary data. J Nutr 145: 2639–2645, 2015. doi:10.3945/jn.115.219634.
37. Taves DR. Minimization: a new method of assigning patients to treatment and control groups. Clin Pharmacol Ther 15: 443–453, 1974. doi:10.1002/ cpt1974155443.
38. Tharion WJ, Lieberman HR, Montain SJ, Young AJ, Baker-Fulco CJ, Delany JP, Hoyt RW. Energy requirements of military personnel. Appetite 44: 47–65, 2005. doi:10.1016/j.appet.2003.11.010.
39. Thomas DT, Erdman KA, Burke LM. American College of Sports Medicine joint position statement. Nutrition and athletic performance. Med Sci Sports Exerc 48: 543–568, 2016. doi:10.1249/MSS. 0000000000000852.
40. Welsh TT, Alemany JA, Montain SJ, Frykman PN, Tuckow AP, Young AJ, Nindl BC. Effects of intensified military field training on jumping performance. Int J Sports Med 29: 45–52, 2008. doi:10.1055/s-2007-964970.
41. West DW, Burd NA, Coffey VG, Baker SK, Burke LM, Hawley JA, Moore DR, Stellingwerff T, Phillips SM. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am J Clin Nutr 94: 795–803, 2011. doi:10.3945/ajcn.111.013722.