Dietary Protein, Muscle and Physical Function in the Very Old

Bernhard Franzke, Oliver Neubauer, David Cameron-Smith, Karl-Heinz Wagner, Bernhard Franzke, Oliver Neubauer, David Cameron-Smith, Karl-Heinz Wagner

Abstract

There is an ongoing debate as to the optimal protein intake in older adults. An increasing body of experimental studies on skeletal muscle protein metabolism as well as epidemiological data suggest that protein requirements with ageing might be greater than many current dietary recommendations. Importantly, none of the intervention studies in this context specifically investigated very old individuals. Data on the fastest growing age group of the oldest old (aged 85 years and older) is very limited. In this review, we examine the current evidence on protein intake for preserving muscle mass, strength and function in older individuals, with emphasis on data in the very old. Available observational data suggest beneficial effects of a higher protein intake with physical function in the oldest old. Whilst, studies estimating protein requirements in old and very old individuals based on whole-body measurements, show no differences between these sub-populations of elderly. However, small sample sizes preclude drawing firm conclusions. Experimental studies that compared muscle protein synthetic (MPS) responses to protein ingestion in young and old adults suggest that a higher relative protein intake is required to maximally stimulate skeletal muscle MPS in the aged. Although, data on MPS responses to protein ingestion in the oldest old are currently lacking. Collectively, the data reviewed for this article support the concept that there is a close interaction of physical activity, diet, function and ageing. An attractive hypothesis is that regular physical activity may preserve and even enhance the responsiveness of ageing skeletal muscle to protein intake, until very advanced age. More research involving study participants particularly aged ≥85 years is warranted to better investigate and determine protein requirements in this specific growing population group.

Keywords: ageing; amino acids; anabolic resistance; centenarians; exercise; nonagenarians; octogenarians; protein requirements; skeletal muscle health.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. Janssen I., Heymsfield S.B., Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J. Am. Geriatr. Soc. 2002;50:889–896. doi: 10.1046/j.1532-5415.2002.50216.x.
    1. Mesquita A.F., Silva E.C.D., Eickemberg M., Roriz A.K.C., Barreto-Medeiros J.M., Ramos L.B. Factors associated with sarcopenia in institutionalized elderly. Nutr. Hosp. 2017;34:345–351. doi: 10.20960/nh.427.
    1. Narici M.V., Maffulli N. Sarcopenia. Characteristics, mechanisms and functional significance. Br. Med. Bull. 2010;95:139–159. doi: 10.1093/bmb/ldq008.
    1. Short K.R., Bigelow M.L., Kahl J., Singh R., Coenen-Schimke J., Raghavakaimal S., Nair K.S. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. USA. 2005;102:5618–5623. doi: 10.1073/pnas.0501559102.
    1. Johnston A.P., De Lisio M., Parise G. Resistance training, sarcopenia and the mitochondrial theory of aging. Appl. Physiol. Nutr. Metab. 2008;33:191–199. doi: 10.1139/H07-141.
    1. Christensen K., Doblhammer G., Rau R., Vaupel J.W. Ageing populations: The challenges ahead. Lancet. 2009;374:1196–1208. doi: 10.1016/S0140-6736(09)61460-4.
    1. Global Health and Aging. [(accessed on 15 July 2018)];2011 Available online: .
    1. Barbi E., Lagona F., Marsili M., Vaupel J.W., Wachter K.W. The plateau of human mortality: Demography of longevity pioneers. Science. 2018;360:1459–1461. doi: 10.1126/science.aat3119.
    1. Lee W.S., Cheung W.H., Qin L., Tang N., Leung K.S. Age-associated decrease of type iia/b human skeletal muscle fibres. Clin. Orthop. Relat. Res. 2006;450:231–237. doi: 10.1097/01.blo.0000218757.97063.21.
    1. Janssen I., Heymsfield S.B., Wang Z.M., Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J. Appl. Physiol. (1985) 2000;89:81–88. doi: 10.1152/jappl.2000.89.1.81.
    1. Rogers M.A., Evans W.J. Changes in skeletal muscle with aging: Effects of exercise training. Exerc. Sport Sci. Rev. 1993;21:65–102. doi: 10.1249/00003677-199301000-00003.
    1. Wagner K.H., Cameron-Smith D., Wessner B., Franzke B. Biomarkers of aging: From function to molecular biology. Nutrients. 2016;8:338. doi: 10.3390/nu8060338.
    1. Song Z., von Figura G., Liu Y., Kraus J.M., Torrice C., Dillon P., Rudolph-Watabe M., Ju Z., Kestler H.A., Sanoff H., et al. Lifestyle impacts on the aging-associated expression of biomarkers of DNA damage and telomere dysfunction in human blood. Aging Cell. 2010;9:607–615. doi: 10.1111/j.1474-9726.2010.00583.x.
    1. Ornish D., Lin J., Daubenmier J., Weidner G., Epel E., Kemp C., Magbanua M.J., Marlin R., Yglecias L., Carroll P.R., et al. Increased telomerase activity and comprehensive lifestyle changes: A pilot study. Lancet Oncol. 2008;9:1048–1057. doi: 10.1016/S1470-2045(08)70234-1.
    1. Seals D.R., Justice J.N., LaRocca T.J. Physiological geroscience: Targeting function to increase healthspan and achieve optimal longevity. J. Physiol. 2016;594:2001–2024. doi: 10.1113/jphysiol.2014.282665.
    1. Smoliner C., Norman K., Wagner K.H., Hartig W., Lochs H., Pirlich M. Malnutrition and depression in the institutionalised elderly. Br. J. Nutr. 2009;102:1663–1667. doi: 10.1017/S0007114509990900.
    1. Phillips S.M., Chevalier S., Leidy H.J. Protein “requirements” beyond the RDA: Implications for optimizing health. Appl. Physiol. Nutr. Metab. 2016;41:565–572. doi: 10.1139/apnm-2015-0550.
    1. Lonnie M., Hooker E., Brunstrom J.M., Corfe B.M., Green M.A., Watson A.W., Williams E.A., Stevenson E.J., Penson S., Johnstone A.M. Protein for life: Review of optimal protein intake, sustainable dietary sources and the effect on appetite in ageing adults. Nutrients. 2018;10:360. doi: 10.3390/nu10030360.
    1. Traylor D.A., Gorissen S.H.M., Phillips S.M. Perspective: Protein requirements and optimal intakes in aging: Are we ready to recommend more than the recommended daily allowance? Adv. Nutr. 2018;9:171–182. doi: 10.1093/advances/nmy003.
    1. Deutz N.E., Bauer J.M., Barazzoni R., Biolo G., Boirie Y., Bosy-Westphal A., Cederholm T., Cruz-Jentoft A., Krznariç Z., Nair K.S., et al. Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group. Clin. Nutr. 2014;33:929–936. doi: 10.1016/j.clnu.2014.04.007.
    1. Mitchell C.J., Milan A.M., Mitchell S.M., Zeng N., Ramzan F., Sharma P., Knowles S., Roy N., Sjödin A., Wagner K.-H., et al. The effects of dietary protein intake on appendicular lean mass and muscle function in elderly men: A 10 week randomized controlled trial. Am. J. Clin. Nutr. 2017;106:1375–1383. doi: 10.3945/ajcn.117.160325.
    1. World Health Organization . Protein and Amino Acid Requirements in Human Nutrition. 935th ed. World Health Organization; Geneva, Switzerland: 2007.
    1. Elango R., Ball R.O., Pencharz P.B. Recent advances in determining protein and amino acid requirements in humans. Br. J. Nutr. 2012;108(Suppl. 2):S22–S30. doi: 10.1017/S0007114512002504.
    1. Nowson C., O’Connell S. Protein requirements and recommendations for older people: A review. Nutrients. 2015;7:6874–6899. doi: 10.3390/nu7085311.
    1. Nordic Nutrition Recommendations 2012: Integrating Nutrition and Physical Activity. 5th ed. Nordic Council of Ministers; Copenhagen, Denmark: 2014. [(accessed on 15 July 2018)]. Available online: .
    1. D-A-CH Referenzwerte für die Nährstoffzufuhr. Volume 2. Deutsche Gesellschaft für Ernährung, Österreichische Gesellschaft für Ernährung, Schweizerische Gesellschaft für Ernährung; Bonn, Germany: 2017.
    1. Morley J.E., Argiles J.M., Evans W.J., Bhasin S., Cella D., Deutz N.E., Doehner W., Fearon K.C., Ferrucci L., Hellerstein M.K., et al. Nutritional recommendations for the management of sarcopenia. J. Am. Med. Dir. Assoc. 2010;11:391–396. doi: 10.1016/j.jamda.2010.04.014.
    1. Bauer J., Biolo G., Cederholm T., Cesari M., Cruz-Jentoft A.J., Morley J.E., Phillips S., Sieber C., Stehle P., Teta D., et al. 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. 2013;14:542–559. doi: 10.1016/j.jamda.2013.05.021.
    1. Rizzoli R., Stevenson J.C., Bauer J.M., van Loon L.J., Walrand S., Kanis J.A., Cooper C., Brandi M.L., Diez-Perez A., Reginster J.Y., et al. The role of dietary protein and vitamin d in maintaining musculoskeletal health in postmenopausal women: A consensus statement from the European society for clinical and economic aspects of osteoporosis and osteoarthritis (ESCEO) Maturitas. 2014;79:122–132. doi: 10.1016/j.maturitas.2014.07.005.
    1. Tang M., McCabe G.P., Elango R., Pencharz P.B., Ball R.O., Campbell W.W. Assessment of protein requirement in octogenarian women with use of the indicator amino acid oxidation technique. Am. J. Clin. Nutr. 2014;99:891–898. doi: 10.3945/ajcn.112.042325.
    1. Okada T., Ikebe K., Kagawa R., Inomata C., Takeshita H., Gondo Y., Ishioka Y., Okubo H., Kamide K., Masui Y., et al. Lower protein intake mediates association between lower occlusal force and slower walking speed: From the septuagenarians, octogenarians, nonagenarians investigation with centenarians study. J. Am. Geriatr. Soc. 2015;63:2382–2387. doi: 10.1111/jgs.13784.
    1. Ozaki A., Uchiyama M., Tagaya H., Ohida T., Ogihara R. The japanese centenarian study: Autonomy was associated with health practices as well as physical status. J. Am. Geriatr. Soc. 2007;55:95–101. doi: 10.1111/j.1532-5415.2006.01019.x.
    1. An R., Xiang X., Liu J., Guan C. Diet and self-rated health among oldest-old Chinese. Arch. Gerontol. Geriatr. 2018;76:125–132. doi: 10.1016/j.archger.2018.02.011.
    1. Granic A., Mendonça N., Sayer A.A., Hill T.R., Davies K., Adamson A., Siervo M., Mathers J.C., Jagger C. Low protein intake, muscle strength and physical performance in the very old: The Newcastle 85+ study. Clin. Nutr. 2017 doi: 10.1016/j.clnu.2017.11.005.
    1. Mendonça N., Hill T.R., Granic A., Davies K., Collerton J., Mathers J.C., Siervo M., Wrieden W.L., Seal C.J., Kirkwood T.B., et al. Macronutrient intake and food sources in the very old: Analysis of the Newcastle 85+ study. Br. J. Nutr. 2016;115:2170–2180. doi: 10.1017/S0007114516001379.
    1. Shi Z., Zhang T., Byles J., Martin S., Avery J.C., Taylor A.W. Food habits, lifestyle factors and mortality among oldest old Chinese: The Chinese longitudinal healthy longevity survey (CLHLS) Nutrients. 2015;7:7562–7579. doi: 10.3390/nu7095353.
    1. Granic A., Mendonça N., Hill T.R., Jagger C., Stevenson E.J., Mathers J.C., Sayer A.A. Nutrition in the very old. Nutrients. 2018;10:269. doi: 10.3390/nu10030269.
    1. Paddon-Jones D., Campbell W.W., Jacques P.F., Kritchevsky S.B., Moore L.L., Rodriguez N.R., van Loon L.J. Protein and healthy aging. Am. J. Clin. Nutr. 2015 doi: 10.3945/ajcn.114.084061.
    1. Burd N.A., Gorissen S.H., van Loon L.J. Anabolic resistance of muscle protein synthesis with aging. Exerc. Sport Sci. Rev. 2013;41:169–173. doi: 10.1097/JES.0b013e318292f3d5.
    1. Moore D.R., Churchward-Venne T.A., Witard O., Breen L., Burd N.A., Tipton K.D., Phillips S.M. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J. Gerontol. A Biol. Sci. Med. Sci. 2015;70:57–62. doi: 10.1093/gerona/glu103.
    1. Shad B.J., Thompson J.L., Breen L. Does the muscle protein synthetic response to exercise and amino acid-based nutrition diminish with advancing age? A systematic review. Am. J. Physiol. Endocrinol. Metab. 2016;311:E803–E817. doi: 10.1152/ajpendo.00213.2016.
    1. Moore D.R., Robinson M.J., Fry J.L., Tang J.E., Glover E.I., Wilkinson S.B., Prior T., Tarnopolsky M.A., Phillips S.M. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am. J. Clin. Nutr. 2009;89:161–168. doi: 10.3945/ajcn.2008.26401.
    1. Witard O.C., Jackman S.R., Breen L., Smith K., Selby A., Tipton K.D. 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. doi: 10.3945/ajcn.112.055517.
    1. Rafii M., Chapman K., Owens J., Elango R., Campbell W.W., Ball R.O., Pencharz P.B., Courtney-Martin G. Dietary protein requirement of female adults >65 years determined by the indicator amino acid oxidation technique is higher than current recommendations. J. Nutr. 2015;145:18–24. doi: 10.3945/jn.114.197517.
    1. Rafii M., Chapman K., Elango R., Campbell W.W., Ball R.O., Pencharz P.B., Courtney-Martin G. Dietary protein requirement of men >65 years old determined by the indicator amino acid oxidation technique is higher than the current estimated average requirement. J. Nutr. 2016;46 doi: 10.3945/jn.115.225631.
    1. Pennings B., Koopman R., Beelen M., Senden J.M., Saris W.H., van Loon L.J. Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men. Am. J. Clin. Nutr. 2011;93:322–331. doi: 10.3945/ajcn.2010.29649.
    1. Burd N.A., Tang J.E., Moore D.R., Phillips S.M. Exercise training and protein metabolism: Influences of contraction, protein intake and sex-based differences. J. Appl. Physiol. (1985) 2009;106:1692–1701. doi: 10.1152/japplphysiol.91351.2008.
    1. Timmerman K.L., Dhanani S., Glynn E.L., Fry C.S., Drummond M.J., Jennings K., Rasmussen B.B., Volpi E. A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am. J. Clin. Nutr. 2012;95:1403–1412. doi: 10.3945/ajcn.111.020800.
    1. Drummond M.J., Miyazaki M., Dreyer H.C., Pennings B., Dhanani S., Volpi E., Esser K.A., Rasmussen B.B. Expression of growth-related genes in young and older human skeletal muscle following an acute stimulation of protein synthesis. J. Appl. Physiol. (1985) 2009;106:1403–1411. doi: 10.1152/japplphysiol.90842.2008.
    1. Drummond M.J., McCarthy J.J., Fry C.S., Esser K.A., Rasmussen B.B. Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am. J. Physiol. Endocrinol. Metab. 2008;295:E1333–1340. doi: 10.1152/ajpendo.90562.2008.
    1. Cermak N.M., Res P.T., de Groot L.C., Saris W.H., van Loon L.J. Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: A meta-analysis. Am. J. Clin. Nutr. 2012;96:1454–1464. doi: 10.3945/ajcn.112.037556.
    1. Tieland M., van de Rest O., Dirks M.L., van der Zwaluw N., Mensink M., van Loon L.J., de Groot L.C. Protein supplementation improves physical performance in frail elderly people: A randomized, double-blind, placebo-controlled trial. J. Am. Med. Dir. Assoc. 2012;13:720–726. doi: 10.1016/j.jamda.2012.07.005.
    1. Breen L., Stokes K.A., Churchward-Venne T.A., Moore D.R., Baker S.K., Smith K., Atherton P.J., Phillips S.M. 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;98:2604–2612. doi: 10.1210/jc.2013-1502.
    1. Drummond M.J., Dickinson J.M., Fry C.S., Walker D.K., Gundermann D.M., Reidy P.T., Timmerman K.L., Markofski M.M., Paddon-Jones D., Rasmussen B.B., et al. Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling and protein synthesis in response to essential amino acids in older adults. Am. J. Physiol. Endocrinol. Metab. 2012;302:E1113–1122. doi: 10.1152/ajpendo.00603.2011.
    1. Nyberg M., Hellsten Y. Reduced blood flow to contracting skeletal muscle in ageing humans: Is it all an effect of sand through the hourglass? J. Physiol. 2016;594:2297–2305. doi: 10.1113/JP270594.
    1. Trappe S., Hayes E., Galpin A., Kaminsky L., Jemiolo B., Fink W., Trappe T., Jansson A., Gustafsson T., Tesch P. New records in aerobic power among octogenarian lifelong endurance athletes. J. Appl. Physiol. 2013;114:3–10. doi: 10.1152/japplphysiol.01107.2012.
    1. Harridge S.D., Lazarus N.R. Physical activity, aging and physiological function. Physiology. 2017;32:152–161. doi: 10.1152/physiol.00029.2016.
    1. Cartee G.D., Hepple R.T., Bamman M.M., Zierath J.R. Exercise promotes healthy aging of skeletal muscle. Cell Metab. 2016;23:1034–1047. doi: 10.1016/j.cmet.2016.05.007.
    1. Raue U., Slivka D., Minchev K., Trappe S. Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. J. Appl. Physiol. (1985) 2009;106:1611–1617. doi: 10.1152/japplphysiol.91587.2008.
    1. Slivka D., Raue U., Hollon C., Minchev K., Trappe S. Single muscle fiber adaptations to resistance training in old (>80 yr) men: Evidence for limited skeletal muscle plasticity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008;295:R273–R280. doi: 10.1152/ajpregu.00093.2008.
    1. Grosicki G.J., Standley R.A., Murach K.A., Raue U., Minchev K., Coen P.M., Newman A.B., Cummings S., Harris T., Kritchevsky S., et al. Improved single muscle fiber quality in the oldest-old. J. Appl. Physiol. (1985) 2016;121:878–884. doi: 10.1152/japplphysiol.00479.2016.
    1. Tang J.E., Moore D.R., Kujbida G.W., Tarnopolsky M.A., Phillips S.M. 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. (1985) 2009;107:987–992. doi: 10.1152/japplphysiol.00076.2009.
    1. Van Loon L.J. Leucine as a pharmaconutrient in health and disease. Curr. Opin. Clin. Nutr. Metab. Care. 2012;15:71–77. doi: 10.1097/MCO.0b013e32834d617a.
    1. Pennings B., Groen B.B., van Dijk J.W., de Lange A., Kiskini A., Kuklinski M., Senden J.M., van Loon L.J. Minced beef is more rapidly digested and absorbed than beef steak, resulting in greater postprandial protein retention in older men. Am. J. Clin. Nutr. 2013;98:121–128. doi: 10.3945/ajcn.112.051201.
    1. Conley T.B., Apolzan J.W., Leidy H.J., Greaves K.A., Lim E., Campbell W.W. Effect of food form on postprandial plasma amino acid concentrations in older adults. Br. J. Nutr. 2011;106:203–207. doi: 10.1017/S0007114511000419.
    1. Vliet S.V., Beals J.W., Martinez I.G., Skinner S.K., Burd N.A. Achieving optimal post-exercise muscle protein remodeling in physically active adults through whole food consumption. Nutrients. 2018;10:224. doi: 10.3390/nu10020224.
    1. Van Vliet S., Burd N.A., van Loon L.J. The skeletal muscle anabolic response to plant- versus animal-based protein consumption. J. Nutr. 2015;145:1981–1991. doi: 10.3945/jn.114.204305.
    1. Mamerow M.M., Mettler J.A., English K.L., Casperson S.L., Arentson-Lantz E., Sheffield-Moore M., Layman D.K., Paddon-Jones D. Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. J. Nutr. 2014;144:876–880. doi: 10.3945/jn.113.185280.
    1. Farsijani S., Morais J.A., Payette H., Gaudreau P., Shatenstein B., Gray-Donald K., Chevalier S. Relation between mealtime distribution of protein intake and lean mass loss in free-living older adults of the NuAge study. Am. J. Clin. Nutr. 2016;104:694–703. doi: 10.3945/ajcn.116.130716.
    1. Farsijani S., Payette H., Morais J.A., Shatenstein B., Gaudreau P., Chevalier S. Even mealtime distribution of protein intake is associated with greater muscle strength but not with 3-y physical function decline, in free-living older adults: The Quebec longitudinal study on Nutrition as a Determinant of Successful Aging (NuAge study) Am. J. Clin. Nutr. 2017;106:113–124. doi: 10.3945/ajcn.116.146555.
    1. Kim I.Y., Schutzler S., Schrader A., Spencer H., Kortebein P., Deutz N.E., Wolfe R.R., Ferrando A.A. Quantity of dietary protein intake but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. Am. J. Physiol. Endocrinol. Metab. 2015;308:E21–28. doi: 10.1152/ajpendo.00382.2014.
    1. Areta J.L., Burke L.M., Ross M.L., Camera D.M., West D.W., Broad E.M., Jeacocke N.A., Moore D.R., Stellingwerff T., Phillips S.M., et al. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J. Physiol. 2013;591:2319–2331. doi: 10.1113/jphysiol.2012.244897.
    1. Close G.L., Hamilton D.L., Philp A., Burke L.M., Morton J.P. New strategies in sport nutrition to increase exercise performance. Free. Radic. Biol. Med. 2016;98:144–158. doi: 10.1016/j.freeradbiomed.2016.01.016.
    1. Phillips S.M. A brief review of higher dietary protein diets in weight loss: A focus on athletes. Sports Med. 2014;44(Suppl. 2):S149–S153. doi: 10.1007/s40279-014-0254-y.
    1. McGlory C., Devries M.C., Phillips S.M. Skeletal muscle and resistance exercise training; the role of protein synthesis in recovery and remodeling. J. Appl. Physiol. (1985) 2017;122:541–548. doi: 10.1152/japplphysiol.00613.2016.
    1. Agarwal E., Miller M., Yaxley A., Isenring E. Malnutrition in the elderly: A narrative review. Maturitas. 2013;76:296–302. doi: 10.1016/j.maturitas.2013.07.013.
    1. Rydwik E., Welmer A.K., Kåreholt I., Angleman S., Fratiglioni L., Wang H.X. Adherence to physical exercise recommendations in people over 65—the SNAC-Kungsholmen study. Eur. J. Public. Health. 2013;23:799–804. doi: 10.1093/eurpub/cks150.
    1. Calvez J., Poupin N., Chesneau C., Lassale C., Tomé D. Protein intake, calcium balance and health consequences. Eur. J. Clin. Nutr. 2012;66:281–295. doi: 10.1038/ejcn.2011.196.
    1. Aragon A.A., Schoenfeld B.J., Wildman R., Kleiner S., VanDusseldorp T., Taylor L., Earnest C.P., Arciero P.J., Wilborn C., Kalman D.S., et al. International society of sports nutrition position stand: Diets and body composition. J. Int. Soc. Sports Nutr. 2017;14:16. doi: 10.1186/s12970-017-0174-y.

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