An Update on Protein, Leucine, Omega-3 Fatty Acids, and Vitamin D in the Prevention and Treatment of Sarcopenia and Functional Decline

Anne-Julie Tessier, Stéphanie Chevalier, Anne-Julie Tessier, Stéphanie Chevalier

Abstract

Aging is associated with sarcopenia and functional decline, leading to frailty and disability. As a modifiable risk factor, nutrition may represent a target for preventing or postponing the onset of these geriatric conditions. Among nutrients, high-quality protein, leucine, vitamin D, and omega-3 polyunsaturated fatty acids (n-3 PUFA) are of particular interest for their demonstrated effects on skeletal muscle health. This narrative review aims to examine the recent observational and interventional evidence on the associations and the role of these nutrients in the muscle mass, strength, mobility, and physical function of free-living older adults, who are either healthy or at risk of frailty. Recent evidence supports a higher protein intake recommendation of 1.0⁻1.2 g/kg/day in healthy older adults; an evenly distributed mealtime protein intake or minimal protein per meal may be beneficial. In addition, vitamin D supplementation of 800⁻1000 IU, particularly when vitamin D status is low, and doses of ~3 g/day of n-3 PUFA may be favorable for physical function, muscle mass, and strength. Reviewed studies are highly heterogenous, yet the quantity, quality, and timing of intakes should be considered when designing intervention studies. Combined protein, leucine, vitamin D, and n-3 PUFA supplements may convey added benefits and may represent an intervention strategy in the prevention of sarcopenia and functional decline.

Keywords: frailty; leucine; muscle strength; older adults; omega-3 fatty acids; physical performance; protein; sarcopenia; vitamin D.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Potential role of nutrition on the physical health of older adults. Short arrows within boxes: increase or decrease. Long arrows between boxes: may lead to. Double-sided arrows: the relationship may be bidirectional. Arrows passing through boxes: factors in box could be mediators.

References

    1. Cruz-Jentoft A.J., Baeyens J.P., Bauer J.M., Boirie Y., Cederholm T., Landi F., Martin F.C., Michel J.P., Rolland Y., Schneider S.M., et al. Sarcopenia: European consensus on definition and diagnosis: Report of the european working group on sarcopenia in older people. Age Ageing. 2010;39:412–423. doi: 10.1093/ageing/afq034.
    1. Morley J.E., Baumgartner R.N., Roubenoff R., Mayer J., Nair K.S. Sarcopenia. J. Lab. Clin. Med. 2001;137:231–243. doi: 10.1067/mlc.2001.113504.
    1. Woo T., Yu S., Visvanathan R. Systematic literature review on the relationship between biomarkers of sarcopenia and quality of life in older people. J. Frailty Aging. 2016;5:88–99. doi: 10.14283/jfa.2016.93.
    1. Delmonico M.J., Harris T.B., Lee J.S., Visser M., Nevitt M., Kritchevsky S.B., Tylavsky F.A., Newman A.B. Health, Aging and Body Composition Study. Alternative definitions of sarcopenia, lower extremity performance, and functional impairment with aging in older men and women. J. Am. Geriatr. Soc. 2007;55:769–774. doi: 10.1111/j.1532-5415.2007.01140.x.
    1. Morley J.E. Diabetes, sarcopenia, and frailty. Clin. Geriatr. Med. 2008;24:455–469. doi: 10.1016/j.cger.2008.03.004.
    1. Cawthon P.M., Fox K.M., Gandra S.R., Delmonico M.J., Chiou C.F., Anthony M.S., Sewall A., Goodpaster B., Satterfield S., Cummings S.R., et al. Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J. Am. Geriatr. Soc. 2009;57:1411–1419. doi: 10.1111/j.1532-5415.2009.02366.x.
    1. Janssen I., Shepard D.S., Katzmarzyk P.T., Roubenoff R. The healthcare costs of sarcopenia in the united states. J. Am. Geriatr. Soc. 2004;52:80–85. doi: 10.1111/j.1532-5415.2004.52014.x.
    1. Landi F., Cruz-Jentoft A.J., Liperoti R., Russo A., Giovannini S., Tosato M., Capoluongo E., Bernabei R., Onder G. Sarcopenia and mortality risk in frail older persons aged 80 years and older: Results from ilsirente study. Age Ageing. 2013;42:203–209. doi: 10.1093/ageing/afs194.
    1. Bollwein J., Volkert D., Diekmann R., Kaiser M.J., Uter W., Vidal K., Sieber C.C., Bauer J.M. Nutritional status according to the mini nutritional assessment (mna(r)) and frailty in community dwelling older persons: A close relationship. J. Nutr. Health Aging. 2013;17:351–356. doi: 10.1007/s12603-013-0034-7.
    1. Dorner T.E., Luger E., Tschinderle J., Stein K.V., Haider S., Kapan A., Lackinger C., Schindler K.E. Association between nutritional status (mna(r)-sf) and frailty (share-fi) in acute hospitalised elderly patients. J. Nutr. Health Aging. 2014;18:264–269. doi: 10.1007/s12603-013-0406-z.
    1. Chevalier S., Saoud F., Gray-Donald K., Morais J.A. The physical functional capacity of frail elderly persons undergoing ambulatory rehabilitation is related to their nutritional status. J. Nutr. Health Aging. 2008;12:721–726. doi: 10.1007/BF03028620.
    1. Kaiser M.J., Bauer J.M., Ramsch C., Uter W., Guigoz Y., Cederholm T., Thomas D.R., Anthony P.S., Charlton K.E., Maggio M., et al. Frequency of malnutrition in older adults: A multinational perspective using the mini nutritional assessment. J. Am. Geriatr. Soc. 2010;58:1734–1738. doi: 10.1111/j.1532-5415.2010.03016.x.
    1. Wall B.T., Gorissen S.H., Pennings B., Koopman R., Groen B.B., Verdijk L.B., van Loon L.J. Aging is accompanied by a blunted muscle protein synthetic response to protein ingestion. PLoS ONE. 2015;10:e0140903. doi: 10.1371/journal.pone.0140903.
    1. Dodd K.M., Tee A.R. Leucine and mTORC1: A complex relationship. Am. J. Physiol. Endocrinol. Metab. 2012;302:E1329–E1342. doi: 10.1152/ajpendo.00525.2011.
    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. Deutz N.E., Bauer J.M., Barazzoni R., Biolo G., Boirie Y., Bosy-Westphal A., Cederholm T., Cruz-Jentoft A., Krznaric 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. Institute of Medicine . Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. The National Academies Press; Washington, DC, USA: 2005. p. 1358.
    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. Tieland M., Franssen R., Dullemeijer C., van Dronkelaar C., Kyung Kim H., Ispoglou T., Zhu K., Prince R.L., van Loon L.J.C., de Groot L. The impact of dietary protein or amino acid supplementation on muscle mass and strength in elderly people: Individual participant data and meta-analysis of rct’s. J. Nutr. Health Aging. 2017;21:994–1001. doi: 10.1007/s12603-017-0896-1.
    1. Mitchell C.J., Milan A.M., Mitchell S.M., Zeng N., Ramzan F., Sharma P., Knowles S.O., Roy N.C., Sjodin A., Wagner K.H., et al. The effects of dietary protein intake on appendicular lean mass and muscle function in elderly men: A 10-wk randomized controlled trial. Am. J. Clin. Nutr. 2017;106:1375–1383. doi: 10.3945/ajcn.117.160325.
    1. Cawood A.L., Elia M., Stratton R.J. Systematic review and meta-analysis of the effects of high protein oral nutritional supplements. Ageing Res. Rev. 2012;11:278–296. doi: 10.1016/j.arr.2011.12.008.
    1. Neelemaat F., Bosmans J.E., Thijs A., Seidell J.C., van Bokhorst-de van der Schueren M.A. Oral nutritional support in malnourished elderly decreases functional limitations with no extra costs. Clin. Nutr. 2012;31:183–190. doi: 10.1016/j.clnu.2011.10.009.
    1. Kim C.O., Lee K.R. Preventive effect of protein-energy supplementation on the functional decline of frail older adults with low socioeconomic status: A community-based randomized controlled study. J. Gerontol. A Biol. Sci. Med. Sci. 2013;68:309–316. doi: 10.1093/gerona/gls167.
    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. Zhu K., Kerr D.A., Meng X., Devine A., Solah V., Binns C.W., Prince R.L. Two-year whey protein supplementation did not enhance muscle mass and physical function in well-nourished healthy older postmenopausal women. J. Nutr. 2015;145:2520–2526. doi: 10.3945/jn.115.218297.
    1. Paddon-Jones D., Rasmussen B.B. Dietary protein recommendations and the prevention of sarcopenia. Curr. Opin. Clin. Nutr. Metab. Care. 2009;12:86–90. doi: 10.1097/MCO.0b013e32831cef8b.
    1. Dardevet D., Remond D., Peyron M.A., Papet I., Savary-Auzeloux I., Mosoni L. Muscle wasting and resistance of muscle anabolism: The “anabolic threshold concept” for adapted nutritional strategies during sarcopenia. Sci. World J. 2012;2012:269531. doi: 10.1100/2012/269531.
    1. Chevalier S., Gougeon R., Choong N., Lamarche M., Morais J.A. Influence of adiposity in the blunted whole-body protein anabolic response to insulin with aging. J. Gerontol. A Biol. Sci. Med. Sci. 2006;61:156–164. doi: 10.1093/gerona/61.2.156.
    1. Fujita S., Glynn E.L., Timmerman K.L., Rasmussen B.B., Volpi E. Supraphysiological hyperinsulinaemia is necessary to stimulate skeletal muscle protein anabolism in older adults: Evidence of a true age-related insulin resistance of muscle protein metabolism. Diabetologia. 2009;52:1889–1898. doi: 10.1007/s00125-009-1430-8.
    1. Chevalier S., Goulet E.D.B., Burgos S.A., Wykes L.J., Morais J.A. Protein anabolic responses to a fed steady state in healthy aging. J. Gerontol. Ser. A. 2011;66A:681–688. doi: 10.1093/gerona/glr036.
    1. Glover E.I., Phillips S.M., Oates B.R., Tang J.E., Tarnopolsky M.A., Selby A., Smith K., Rennie M.J. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J. Physiol. 2008;586:6049–6061. doi: 10.1113/jphysiol.2008.160333.
    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 leglean mass and induces “anabolic resistance” of myofibrillar protein synthesis n healthy elderly. J. Clin. Endocrinol. Metab. 2013;98:2604–2612. doi: 10.1210/jc.2013-1502.
    1. Boirie Y. Fighting sarcopenia in older frail subjects: Protein fuel for strength, exercise for mass. J. Am. Med. Dir. Assoc. 2013;14:140–143. doi: 10.1016/j.jamda.2012.10.017.
    1. Katsanos C.S., Kobayashi H., Sheffield-Moore M., Aarsland A., Wolfe R.R. Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am. J. Clin. Nutr. 2005;82:1065–1073. doi: 10.1093/ajcn/82.5.1065.
    1. Paddon-Jones D., Sheffield-Moore M., Zhang X.J., Volpi E., Wolf S.E., Aarsland A., Ferrando A.A., Wolfe R.R. Amino acid ingestion improves muscle protein synthesis in the young and elderly. Am. J. Physiol. Endocrinol. Metab. 2004;286:E321–E328. doi: 10.1152/ajpendo.00368.2003.
    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. Volpi E., Kobayashi H., Sheffield-Moore M., Mittendorfer B., Wolfe R.R. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am. J. Clin. Nutr. 2003;78:250–258. doi: 10.1093/ajcn/78.2.250.
    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 doi: 10.3945/jn.113.185280.
    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–E28. doi: 10.1152/ajpendo.00382.2014.
    1. Bouillanne O., Curis E., Hamon-Vilcot B., Nicolis I., Chretien P., Schauer N., Vincent J.P., Cynober L., Aussel C. Impact of protein pulse feeding on lean mass in malnourished and at-risk hospitalized elderly patients: A randomized controlled trial. Clin. Nutr. 2013;32:186–192. doi: 10.1016/j.clnu.2012.08.015.
    1. Gaudreau P., Morais J.A., Shatenstein B., Gray-Donald K., Khalil A., Dionne I., Ferland G., Fulop T., Jacques D., Kergoat M.J., et al. Nutrition as a determinant of successful aging: Description of the Quebec longitudinal study nuage and results from cross-sectional pilot studies. Rejuvenation Res. 2007;10:377–386. doi: 10.1089/rej.2007.0596.
    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. ten Haaf D., van Dongen E., Nuijten M., Eijsvogels T., de Groot L., Hopman M. Protein intake and distribution in relation to physical functioning and quality of life in community-dwelling elderly people: Acknowledging the role of physical activity. Nutrients. 2018;10:506. doi: 10.3390/nu10040506.
    1. Gingrich A., Spiegel A., Kob R., Schoene D., Skurk T., Hauner H., Sieber C.C., Volkert D., Kiesswetter E. Amount, distribution, and quality of protein intake are not associated with muscle mass, strength, and power in healthy older adults without functional limitations-an enable study. Nutrients. 2017;9 doi: 10.3390/nu9121358.
    1. Murphy C.H., Oikawa S.Y., Phillips S.M. Dietary protein to maintain muscle mass in aging: A case for per-meal protein recommendations. J. Frailty Aging. 2016;5:49–58. doi: 10.14283/jfa.2016.80.
    1. Mishra S., Goldman J.D., Sahyoun N.R., Moshfegh A.J. Association between dietary protein intake and grip strength among adults aged 51 years and over: What we eat in america, national health and nutrition examination survey 2011-2014. PLoS ONE. 2018;13:e0191368. doi: 10.1371/journal.pone.0191368.
    1. Loenneke J.P., Loprinzi P.D., Murphy C.H., Phillips S.M. Per meal dose and frequency of protein consumption is associated with lean mass and muscle performance. Clin. Nutr. 2016;35:1506–1511. doi: 10.1016/j.clnu.2016.04.002.
    1. Anthony J.C., Yoshizawa F., Anthony T.G., Vary T.C., Jefferson L.S., Kimball S.R. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J. Nutr. 2000;130:2413–2419. doi: 10.1093/jn/130.10.2413.
    1. Crozier S.J., Kimball S.R., Emmert S.W., Anthony J.C., Jefferson L.S. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J. Nutr. 2005;135:376–382. doi: 10.1093/jn/135.3.376.
    1. Sancak Y., Peterson T.R., Shaul Y.D., Lindquist R.A., Thoreen C.C., Bar-Peled L., Sabatini D.M. The rag gtpases bind raptor and mediate amino acid signaling to mTORC1. Science. 2008;320:1496–1501. doi: 10.1126/science.1157535.
    1. Jewell J.L., Russell R.C., Guan K.L. Amino acid signalling upstream of mTOR. Nat. Rev. Mol. Cell Biol. 2013;14:133–139. doi: 10.1038/nrm3522.
    1. Wilkinson D.J., Hossain T., Hill D.S., Phillips B.E., Crossland H., Williams J., Loughna P., Churchward-Venne T.A., Breen L., Phillips S.M., et al. Effects of leucine and its metabolite beta-hydroxy-beta-methylbutyrate on human skeletal muscle protein metabolism. J. Physiol. 2013;591:2911–2923. doi: 10.1113/jphysiol.2013.253203.
    1. Katsanos C.S., Aarsland A., Cree M.G., Wolfe R.R. Muscle protein synthesis and balance responsiveness to essential amino acids ingestion in the presence of elevated plasma free fatty acid concentrations. J. Clin. Endocrinol. Metab. 2009;94:2984–2990. doi: 10.1210/jc.2008-2686.
    1. Komar B., Schwingshackl L., Hoffmann G. Effects of leucine-rich protein supplements on anthropometric parameter and muscle strength in the elderly: A systematic review and meta-analysis. J. Nutr. Health Aging. 2015;19:437–446. doi: 10.1007/s12603-014-0559-4.
    1. Xu Z.R., Tan Z.J., Zhang Q., Gui Q.F., Yang Y.M. The effectiveness of leucine on muscle protein synthesis, lean body mass and leg lean mass accretion in older people: A systematic review and meta-analysis. Br. J. Nutr. 2015;113:25–34. doi: 10.1017/S0007114514002475.
    1. Devries M.C., McGlory C., Bolster D.R., Kamil A., Rahn M., Harkness L., Baker S.K., Phillips S.M. Leucine, not total protein, content of a supplement is the primary determinant of muscle protein anabolic responses in healthy older women. J. Nutr. 2018;148:1088–1095. doi: 10.1093/jn/nxy091.
    1. Devries M.C., McGlory C., Bolster D.R., Kamil A., Rahn M., Harkness L., Baker S.K., Phillips S.M. Protein leucine content is a determinant of shorter- and longer-term muscle protein synthetic responses at rest and following resistance exercise in healthy older women: A randomized, controlled trial. Am. J. Clin. Nutr. 2018;107:217–226. doi: 10.1093/ajcn/nqx028.
    1. Murphy C.H., Saddler N.I., Devries M.C., McGlory C., Baker S.K., Phillips S.M. Leucine supplementation enhances integrative myofibrillar protein synthesis in free-living older men consuming lower- and higher-protein diets: A parallel-group crossover study. Am. J. Clin. Nutr. 2016;104:1594–1606. doi: 10.3945/ajcn.116.136424.
    1. Holick M.F. Vitamin D deficiency. N. Engl. J. Med. 2007;357:266–281. doi: 10.1056/NEJMra070553.
    1. Holick M.F. Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease. Am. J. Clin. Nutr. 2004;80:1678S–1688S. doi: 10.1093/ajcn/80.6.1678S.
    1. van Schoor N.M., Lips P. Worldwide vitamin D status. Best Pract. Res. Clin. Endocrinol. Metab. 2011;25:671–680. doi: 10.1016/j.beem.2011.06.007.
    1. Simpson R.U., Thomas G.A., Arnold A.J. Identification of 1,25-dihydroxyvitamin D3 receptors and activities in muscle. J. Biol. Chem. 1985;260:8882–8891.
    1. Dirks-Naylor A.J., Lennon-Edwards S. The effects of vitamin D on skeletal muscle function and cellular signaling. J. Steroid Biochem. Mol. Biol. 2011;125:159–168. doi: 10.1016/j.jsbmb.2011.03.003.
    1. Ross A.C. The 2011 report on dietary reference intakes for calcium and vitamin D. Public Health Nutr. 2011;14:938–939. doi: 10.1017/S1368980011000565.
    1. Houston D.K., Tooze J.A., Davis C.C., Chaves P.H., Hirsch C.H., Robbins J.A., Arnold A.M., Newman A.B., Kritchevsky S.B. Serum 25-hydroxyvitamin D and physical function in older adults: The cardiovascular health study all stars. J. Am. Geriatr. Soc. 2011;59:1793–1801. doi: 10.1111/j.1532-5415.2011.03601.x.
    1. Houston D.K., Cesari M., Ferrucci L., Cherubini A., Maggio D., Bartali B., Johnson M.A., Schwartz G.G., Kritchevsky S.B. Association between vitamin D status and physical performance: The inCHIANTI study. J. Gerontol. A Biol. Sci. Med. Sci. 2007;62:440–446. doi: 10.1093/gerona/62.4.440.
    1. Bischoff-Ferrari H.A., Dietrich T., Orav E.J., Hu F.B., Zhang Y., Karlson E.W., Dawson-Hughes B. Higher 25-hydroxyvitamin D concentrations are associated with better lower-extremity function in both active and inactive persons aged > or =60 y. Am. J. Clin. Nutr. 2004;80:752–758. doi: 10.1093/ajcn/80.3.752.
    1. Houston D.K., Tooze J.A., Neiberg R.H., Hausman D.B., Johnson M.A., Cauley J.A., Bauer D.C., Cawthon P.M., Shea M.K., Schwartz G.G., et al. 25-hydroxyvitamin D status and change in physical performance and strength in older adults: The health, aging, and body composition study. Am. J. Epidemiol. 2012;176:1025–1034. doi: 10.1093/aje/kws147.
    1. Toffanello E.D., Perissinotto E., Sergi G., Zambon S., Musacchio E., Maggi S., Coin A., Sartori L., Corti M.C., Baggio G., et al. Vitamin D and physical performance in elderly subjects: The pro.V.A study. PLoS ONE. 2012;7:e34950. doi: 10.1371/journal.pone.0034950.
    1. Dam T.-T.L., von Mühlen D., Barrett-Connor E.L. Sex specific association of serum 25-hydroxyvitamin D levels with physical function in older adults. Osteoporos. Int. 2009;20:751–760. doi: 10.1007/s00198-008-0749-1.
    1. Mowe M., Haug E., Bohmer T. Low serum calcidiol concentration in older adults with reduced muscular function. J. Am. Geriatr. Soc. 1999;47:220–226. doi: 10.1111/j.1532-5415.1999.tb04581.x.
    1. Zamboni M., Zoico E., Tosoni P., Zivelonghi A., Bortolani A., Maggi S., Di Francesco V., Bosello O. Relation between vitamin D, physical performance, and disability in elderly persons. J. Gerontol. A Biol. Sci. Med. Sci. 2002;57:M7-11. doi: 10.1093/gerona/57.1.M7.
    1. Annweiler C., Beauchet O., Berrut G., Fantino B., Bonnefoy M., Herrmann F.R., Schott A.M. Is there an association between serum 25-hydroxyvitamin D concentration and muscle strength among older women? Results from baseline assessment of the epidos study. J. Nutr. Health Aging. 2009;13:90–95. doi: 10.1007/s12603-009-0013-1.
    1. Annweiler C., Henni S., Walrand S., Montero-Odasso M., Duque G., Duval G.T. Vitamin D and walking speed in older adults: Systematic review and meta-analysis. Maturitas. 2017;106:8–25. doi: 10.1016/j.maturitas.2017.07.012.
    1. Vaes A.M.M., Brouwer-Brolsma E.M., Toussaint N., de Regt M., Tieland M., van Loon L.J.C., de Groot L. The association between 25-hydroxyvitamin D concentration, physical performance and frailty status in older adults. Eur. J. Nutr. 2018 doi: 10.1007/s00394-018-1634-0.
    1. Zhou J., Huang P., Liu P., Hao Q., Chen S., Dong B., Wang J. Association of vitamin D deficiency and frailty: A systematic review and meta-analysis. Maturitas. 2016;94:70–76. doi: 10.1016/j.maturitas.2016.09.003.
    1. Sohl E., de Jongh R.T., Heijboer A.C., Swart K.M., Brouwer-Brolsma E.M., Enneman A.W., de Groot C.P., van der Velde N., Dhonukshe-Rutten R.A., Lips P., et al. Vitamin D status is associated with physical performance: The results of three independent cohorts. Osteoporos. Int. 2013;24:187–196. doi: 10.1007/s00198-012-2124-5.
    1. Houston D.K., Neiberg R.H., Tooze J.A., Hausman D.B., Johnson M.A., Cauley J.A., Bauer D.C., Shea M.K., Schwartz G.G., Williamson J.D., et al. Low 25-hydroxyvitamin D predicts the onset of mobility limitation and disability in community-dwelling older adults: The health abc study. J. Gerontol. A Biol. Sci. Med. Sci. 2013;68:181–187. doi: 10.1093/gerona/gls136.
    1. Wicherts I.S., van Schoor N.M., Boeke A.J., Visser M., Deeg D.J., Smit J., Knol D.L., Lips P. Vitamin D status predicts physical performance and its decline in older persons. J. Clin. Endocrinol. Metab. 2007;92:2058–2065. doi: 10.1210/jc.2006-1525.
    1. Visser M., Deeg D.J., Lips P., Longitudinal Aging Study A. Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): The longitudinal aging study amsterdam. J. Clin. Endocrinol. Metab. 2003;88:5766–5772. doi: 10.1210/jc.2003-030604.
    1. Verreault R., Semba R.D., Volpato S., Ferrucci L., Fried L.P., Guralnik J.M. Low serum vitamin D does not predict new disability or loss of muscle strength in older women. J. Am. Geriatr. Soc. 2002;50:912–917. doi: 10.1046/j.1532-5415.2002.50219.x.
    1. Granic A., Hill T.R., Davies K., Jagger C., Adamson A., Siervo M., Kirkwood T.B., Mathers J.C., Sayer A.A. Vitamin D status, muscle strength and physical performance decline in very old adults: A prospective study. Nutrients. 2017;9:379. doi: 10.3390/nu9040379.
    1. Annweiler C., Schott A.M., Berrut G., Fantino B., Beauchet O. Vitamin D-related changes in physical performance: A systematic review. J. Nutr. Health Aging. 2009;13:893–898. doi: 10.1007/s12603-009-0248-x.
    1. Muir S.W., Montero-Odasso M. Effect of vitamin D supplementation on muscle strength, gait and balance in older adults: A systematic review and meta-analysis. J. Am. Geriatr. Soc. 2011;59:2291–2300. doi: 10.1111/j.1532-5415.2011.03733.x.
    1. Rosendahl-Riise H., Spielau U., Ranhoff A.H., Gudbrandsen O.A., Dierkes J. Vitamin D supplementation and its influence on muscle strength and mobility in community-dwelling older persons: A systematic review and meta-analysis. J. Hum. Nutr. Diet. 2017;30:3–15. doi: 10.1111/jhn.12394.
    1. Beaudart C., Buckinx F., Rabenda V., Gillain S., Cavalier E., Slomian J., Petermans J., Reginster J.Y., Bruyere O. The effects of vitamin D on skeletal muscle strength, muscle mass, and muscle power: A systematic review and meta-analysis of randomized controlled trials. J. Clin. Endocrinol. Metab. 2014;99:4336–4345. doi: 10.1210/jc.2014-1742.
    1. Glendenning P., Zhu K., Inderjeeth C., Howat P., Lewis J.R., Prince R.L. Effects of three-monthly oral 150,000 iu cholecalciferol supplementation on falls, mobility, and muscle strength in older postmenopausal women: A randomized controlled trial. J. Bone Miner. Res. 2012;27:170–176. doi: 10.1002/jbmr.524.
    1. Pirotta S., Kidgell D.J., Daly R.M. Effects of vitamin D supplementation on neuroplasticity in older adults: A double-blinded, placebo-controlled randomised trial. Osteoporos. Int. 2015;26:131–140. doi: 10.1007/s00198-014-2855-6.
    1. Bischoff-Ferrari H.A., Dawson-Hughes B., Orav E., Staehelin H.B., Meyer O.W., Theiler R., Dick W., Willett W.C., Egli A. Monthly high-dose vitamin D treatment for the prevention of functional decline: A randomized clinical trial. JAMA Intern. Med. 2016;176:175–183. doi: 10.1001/jamainternmed.2015.7148.
    1. Centers for Disease Control and Prevention 10 Leading Causes of Injury Deaths by Age Group Highlighting Unintentional Injury Deaths, United States—2016. [(accessed on 8 August 2018)]; Available online: .
    1. Deandrea S., Lucenteforte E., Bravi F., Foschi R., La Vecchia C., Negri E. Risk factors for falls in community-dwelling older people: A systematic review and meta-analysis. Epidemiology. 2010;21:658–668. doi: 10.1097/EDE.0b013e3181e89905.
    1. Bolland M.J., Grey A., Reid I.R. Differences in overlapping meta-analyses of vitamin D supplements and falls. J. Clin. Endocrinol. Metab. 2014;99:4265–4272. doi: 10.1210/jc.2014-2562.
    1. Bolland M.J., Grey A., Reid I.R. Vitamin D supplements and the risk of falls. JAMA Intern. Med. 2015;175:1723–1724. doi: 10.1001/jamainternmed.2015.3962.
    1. Bolland M.J., Grey A., Gamble G.D., Reid I.R. Vitamin D supplementation and falls: A trial sequential meta-analysis. Lancet Diabetes Endocrinol. 2014;2:573–580. doi: 10.1016/S2213-8587(14)70068-3.
    1. Guirguis-Blake J.M., Michael Y.L., Perdue L.A., Coppola E.L., Beil T.L. Interventions to prevent falls in older adults: Updated evidence report and systematic review for the us preventive services task force. JAMA. 2018;319:1705–1716. doi: 10.1001/jama.2017.21962.
    1. Sanders K.M., Stuart A.L., Williamson E.J., Simpson J.A., Kotowicz M.A., Young D., Nicholson G.C. Annual high-dose oral vitamin D and falls and fractures in older women: A randomized controlled trial. JAMA. 2010;303:1815–1822. doi: 10.1001/jama.2010.594.
    1. U.S. Preventive Services Task Force Interventions to prevent falls in community-dwelling older adults: Us preventive services task force recommendation statement. JAMA. 2018;319:1696–1704. doi: 10.1001/jama.2018.3097.
    1. Burdge G.C., Jones A.E., Wootton S.A. Eicosapentaenoic and docosapentaenoic acids are the principal products of alpha-linolenic acid metabolism in young men*. Br. J. Nutr. 2002;88:355–363. doi: 10.1079/BJN2002662.
    1. Burdge G.C., Wootton S.A. Conversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br. J. Nutr. 2002;88:411–420. doi: 10.1079/BJN2002689.
    1. Simopoulos A.P. Omega-3 fatty acids in inflammation and autoimmune diseases. J. Am. Coll. Nutr. 2002;21:495–505. doi: 10.1080/07315724.2002.10719248.
    1. Crupi R., Marino A., Cuzzocrea S. N-3 fatty acids: Role in neurogenesis and neuroplasticity. Curr. Med. Chem. 2013;20:2953–2963. doi: 10.2174/09298673113209990140.
    1. Tan A., Sullenbarger B., Prakash R., McDaniel J.C. Supplementation with eicosapentaenoic acid and docosahexaenoic acid reduces high levels of circulating proinflammatory cytokines in aging adults: A randomized, controlled study. Prostaglandins Leukot. Essent. Fatty Acids. 2018;132:23–29. doi: 10.1016/j.plefa.2018.03.010.
    1. Mozaffarian D., Lemaitre R.N., King I.B., Song X., Huang H., Sacks F.M., Rimm E.B., Wang M., Siscovick D.S. Plasma phospholipid long-chain omega-3 fatty acids and total and cause-specific mortality in older adults: A cohort study. Ann. Intern. Med. 2013;158:515–525. doi: 10.7326/0003-4819-158-7-201304020-00003.
    1. Vannice G., Rasmussen H. Position of the academy of nutrition and dietetics: Dietary fatty acids for healthy adults. J. Acad. Nutr. Diet. 2014;114:136–153. doi: 10.1016/j.jand.2013.11.001.
    1. Papanikolaou Y., Brooks J., Reider C., Fulgoni V.L., III U.S. Adults are not meeting recommended levels for fish and omega-3 fatty acid intake: Results of an analysis using observational data from nhanes 2003–2008. Nutr. J. 2014;13:31. doi: 10.1186/1475-2891-13-31.
    1. Ewaschuk J.B., Almasud A., Mazurak V.C. Role of n-3 fatty acids in muscle loss and myosteatosis. Appl. Physiol. Nutr. Metab. 2014;39:654–662. doi: 10.1139/apnm-2013-0423.
    1. Gray S.R., Mittendorfer B. Fish oil-derived n-3 polyunsaturated fatty acids for the prevention and treatment of sarcopenia. Curr. Opin. Clin. Nutr. Metab. Care. 2018;21:104–109. doi: 10.1097/MCO.0000000000000441.
    1. Lalia A.Z., Dasari S., Robinson M.M., Abid H., Morse D.M., Klaus K.A., Lanza I.R. Influence of omega-3 fatty acids on skeletal muscle protein metabolism and mitochondrial bioenergetics in older adults. Aging. 2017;9:1096–1129. doi: 10.18632/aging.101210.
    1. Robinson S.M., Jameson K.A., Batelaan S.F., Martin H.J., Syddall H.E., Dennison E.M., Cooper C., Sayer A.A., Hertfordshire Cohort Study G. Diet and its relationship with grip strength in community-dwelling older men and women: The hertfordshire cohort study. J. Am. Geriatr. Soc. 2008;56:84–90. doi: 10.1111/j.1532-5415.2007.01478.x.
    1. Rousseau J.H., Kleppinger A., Kenny A.M. Self-reported dietary intake of omega-3 fatty acids and association with bone and lower extremity function. J. Am. Geriatr. Soc. 2009;57:1781–1788. doi: 10.1111/j.1532-5415.2008.01870.x.
    1. Brenna J.T., Plourde M., Stark K.D., Jones P.J., Lin Y.H. Best practices for the design, laboratory analysis, and reporting of trials involving fatty acids. Am. J. Clin. Nutr. 2018 doi: 10.1093/ajcn/nqy089.
    1. Abbatecola A.M., Cherubini A., Guralnik J.M., Andres Lacueva C., Ruggiero C., Maggio M., Bandinelli S., Paolisso G., Ferrucci L. Plasma polyunsaturated fatty acids and age-related physical performance decline. Rejuvenation Res. 2009;12:25–32. doi: 10.1089/rej.2008.0799.
    1. Frison E., Boirie Y., Peuchant E., Tabue-Teguo M., Barberger-Gateau P., Feart C. Plasma fatty acid biomarkers are associated with gait speed in community-dwelling older adults: The three-city-bordeaux study. Clin. Nutr. 2015 doi: 10.1016/j.clnu.2015.12.008.
    1. Fougere B., de Souto Barreto P., Goisser S., Soriano G., Guyonnet S., Andrieu S., Vellas B., Group M.S. Red blood cell membrane omega-3 fatty acid levels and physical performance: Cross-sectional data from the mapt study. Clin. Nutr. 2018;37:1141–1144. doi: 10.1016/j.clnu.2017.04.005.
    1. Reinders I., Song X., Visser M., Eiriksdottir G., Gudnason V., Sigurdsson S., Aspelund T., Siggeirsdottir K., Brouwer I.A., Harris T.B., et al. Plasma phospholipid pufas are associated with greater muscle and knee extension strength but not with changes in muscle parameters in older adults. J. Nutr. 2015;145:105–112. doi: 10.3945/jn.114.200337.
    1. Reinders I., Murphy R.A., Song X., Visser M., Cotch M.F., Lang T.F., Garcia M.E., Launer L.J., Siggeirsdottir K., Eiriksdottir G., et al. Polyunsaturated fatty acids in relation to incident mobility disability and decline in gait speed; the age, gene/environment susceptibility-reykjavik study. Eur. J. Clin. Nutr. 2015;69:489–493. doi: 10.1038/ejcn.2014.277.
    1. Fougere B., Goisser S., Cantet C., Soriano G., Guyonnet S., De Souto Barreto P., Cesari M., Andrieu S., Vellas B., Group M.S. Omega-3 fatty acid levels in red blood cell membranes and physical decline over 3 years: Longitudinal data from the mapt study. Geroscience. 2017 doi: 10.1007/s11357-017-9990-x.
    1. Hutchins-Wiese H.L., Kleppinger A., Annis K., Liva E., Lammi-Keefe C.J., Durham H.A., Kenny A.M. The impact of supplemental n-3 long chain polyunsaturated fatty acids and dietary antioxidants on physical performance in postmenopausal women. J. Nutr. Health Aging. 2013;17:76–80. doi: 10.1007/s12603-012-0415-3.
    1. Smith G.I., Julliand S., Reeds D.N., Sinacore D.R., Klein S., Mittendorfer B. Fish oil-derived n-3 pufa therapy increases muscle mass and function in healthy older adults. Am. J. Clin. Nutr. 2015;102:115–122. doi: 10.3945/ajcn.114.105833.
    1. Logan S.L., Spriet L.L. Omega-3 fatty acid supplementation for 12 weeks increases resting and exercise metabolic rate in healthy community-dwelling older females. PLoS ONE. 2015;10:e0144828. doi: 10.1371/journal.pone.0144828.
    1. Krzyminska-Siemaszko R., Czepulis N., Lewandowicz M., Zasadzka E., Suwalska A., Witowski J., Wieczorowska-Tobis K. The effect of a 12-week omega-3 supplementation on body composition, muscle strength and physical performance in elderly individuals with decreased muscle mass. Int J. Environ. Res. Public Health. 2015;12:10558–10574. doi: 10.3390/ijerph120910558.
    1. Bo Y., Liu C., Ji Z., Yang R., An Q., Zhang X., You J., Duan D., Sun Y., Zhu Y., et al. A high whey protein, vitamin D and e supplement preserves muscle mass, strength, and quality of life in sarcopenic older adults: A double-blind randomized controlled trial. Clin. Nutr. 2018 doi: 10.1016/j.clnu.2017.12.020.
    1. Chanet A., Verlaan S., Salles J., Giraudet C., Patrac V., Pidou V., Pouyet C., Hafnaoui N., Blot A., Cano N., et al. Supplementing breakfast with a vitamin D and leucine-enriched whey protein medical nutrition drink enhances postprandial muscle protein synthesis and muscle mass in healthy older men. J. Nutr. 2017;147:2262–2271. doi: 10.3945/jn.117.252510.
    1. Bell K.E., Snijders T., Zulyniak M., Kumbhare D., Parise G., Chabowski A., Phillips S.M. A whey protein-based multi-ingredient nutritional supplement stimulates gains in lean body mass and strength in healthy older men: A randomized controlled trial. PLoS ONE. 2017;12:e0181387. doi: 10.1371/journal.pone.0181387.
    1. Bauer J.M., Verlaan S., Bautmans I., Brandt K., Donini L.M., Maggio M., McMurdo M.E., Mets T., Seal C., Wijers S.L., et al. Effects of a vitamin D and leucine-enriched whey protein nutritional supplement on measures of sarcopenia in older adults, the provide study: A randomized, double-blind, placebo-controlled trial. J. Am. Med. Dir. Assoc. 2015;16:740–747. doi: 10.1016/j.jamda.2015.05.021.
    1. Hangartner T.N., Warner S., Braillon P., Jankowski L., Shepherd J. The official positions of the international society for clinical densitometry: Acquisition of dual-energy X-ray absorptiometry body composition and considerations regarding analysis and repeatability of measures. J. Clin. Densitom. 2013;16:520–536. doi: 10.1016/j.jocd.2013.08.007.

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