Advertisement

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)

  • René Rizzoli
    Correspondence
    Corresponding author at: Division of Bone Diseases, Department of Internal Medicine Specialties, Geneva University Hospitals and Faculty of Medicine, Rue Gabrielle-Perret-Gentil 4, 1211 Geneva 14, Switzerland. Tel.: +41 22 372 99 50; fax: +41 22 382 99 73.
    Affiliations
    Division of Bone Diseases, Geneva University Hospitals and Faculty of Medicine, Rue Gabrielle-Perret-Gentil 4, 1211 Geneva 14, Switzerland
    Search for articles by this author
  • John C. Stevenson
    Affiliations
    National Heart & Lung Institute, Imperial College London, Royal Brompton & Harefield NHS Foundation Trust, Sydney Street, London SW3 6NP, UK
    Search for articles by this author
  • Jürgen M. Bauer
    Affiliations
    Department of Geriatric Medicine, Klinikum, Carl von Ossietzky University, Ammerländer Heerstrasse 114-118, 26129 Oldenburg, Germany
    Search for articles by this author
  • Luc J.C. van Loon
    Affiliations
    NUTRIM School for Nutrition, Toxicology and Metabolism, Maastricht University, P.O. Box 616, 6200 MD Maastricht, The Netherlands
    Search for articles by this author
  • Stéphane Walrand
    Affiliations
    INRA and Clermont Université, Université d’Auvergne, 49, Boulevard François Mitterrand, CS 60032, 63001 Clermont Ferrand Cedex 1, France
    Search for articles by this author
  • John A. Kanis
    Affiliations
    Centre for Metabolic Bone Diseases, University of Sheffield, Beech Hill Road, Sheffield S10 2RX, South Yorkshire, UK
    Search for articles by this author
  • Cyrus Cooper
    Affiliations
    MRC Lifecourse Epidemiology Unit and NIHR Nutrition Biomedical Research Centre, University of Southampton, Southampton General Hospital, Tremona Road, Southampton SO16 6YD, UK

    NIHR Musculoskeletal Biomedical Research Unit, University of Oxford, Oxford, UK
    Search for articles by this author
  • Maria-Luisa Brandi
    Affiliations
    Department of Surgery and Translational Medicine, University of Florence, Piazza San Marco, 4-50121 Florence, Italy
    Search for articles by this author
  • Adolfo Diez-Perez
    Affiliations
    Department of Internal Medicine, Hospital Del Mar/IMIM, Autonomous University of Barcelona and RETICEF, Instituto Carlos III, Barcelona, Spain
    Search for articles by this author
  • Jean-Yves Reginster
    Affiliations
    Department of Public Health Sciences, University of Liège, Liège, Belgium

    Bone and Cartilage Metabolism Unit, CHU Centre-Ville, University of Liège, Liège, Belgium
    Search for articles by this author
  • for the ESCEO Task Force

      Abstract

      From 50 years of age, postmenopausal women are at an increased risk of developing sarcopenia and osteoporosis as a result of deterioration of musculoskeletal health. Both disorders increase the risk of falls and fractures. The risk of developing sarcopenia and osteoporosis may be attenuated through healthy lifestyle changes, which include adequate dietary protein, calcium and vitamin D intakes, and regular physical activity/exercise, besides hormone replacement therapy when appropriate. Protein intake and physical activity are the main anabolic stimuli for muscle protein synthesis. Exercise training leads to increased muscle mass and strength, and the combination of optimal protein intake and exercise produces a greater degree of muscle protein accretion than either intervention alone. Similarly, adequate dietary protein intake and resistance exercise are important contributors to the maintenance of bone strength. Vitamin D helps to maintain muscle mass and strength as well as bone health. These findings suggest that healthy lifestyle measures in women aged >50 years are essential to allow healthy ageing. The European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) recommends optimal dietary protein intake of 1.0–1.2 g/kg body weight/d with at least 20–25 g of high-quality protein at each main meal, with adequate vitamin D intake at 800 IU/d to maintain serum 25-hydroxyvitamin D levels >50 nmol/L as well as calcium intake of 1000 mg/d, alongside regular physical activity/exercise 3–5 times/week combined with protein intake in close proximity to exercise, in postmenopausal women for prevention of age-related deterioration of musculoskeletal health.

      Abbreviations:

      25(OH)D (25-hydroxyvitamin D), BMD (bone mineral density), DXA (dual-energy X-ray absorptiometry), HRT (hormone replacement therapy), IGF-I (insulin-like growth factor-I), mTOR (mammalian target of rapamycin), QoL (quality of life), RCT (randomized controlled trial), RNI (recommended nutrient intake), VDR (vitamin D receptor)

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Maturitas
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Barry B.K.
        • Carson R.G.
        The consequences of resistance training for movement control in older adults.
        J Gerontol A: Biol Sci Med Sci. 2004; 59: 730-754
        • Keaveny T.M.
        • Kopperdahl D.L.
        • Melton 3rd, L.J.
        • et al.
        Age-dependence of femoral strength in white women and men.
        J Bone Miner Res. 2010; 25: 994-1001
        • Cruz-Jentoft A.J.
        • Baeyens J.P.
        • Bauer J.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
        • Hernlund E.
        • Svedbom A.
        • Ivergard M.
        • et al.
        Osteoporosis in the European Union: Medical Management, Epidemiology and Economic Burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA).
        Arch Osteoporos. 2013; 8: 136https://doi.org/10.1007/s11657-013-0136-1
        • Maltais M.L.
        • Desroches J.
        • Dionne I.J.
        Changes in muscle mass and strength after menopause.
        J Musculoskelet Neuronal Interact. 2009; 9: 186-197
        • Walrand S.
        • Guillet C.
        • Salles J.
        • et al.
        Physiopathological mechanism of sarcopenia.
        Clin Geriatr Med. 2011; 27: 365-385
        • Patel H.P.
        • Syddall H.E.
        • Jameson K.
        • et al.
        Prevalence of sarcopenia in community-dwelling older people in the UK using the European Working Group on Sarcopenia in Older People (EWGSOP) definition: findings from the Hertfordshire Cohort Study (HCS).
        Age Ageing. 2013; 42: 378-384
        • Fielding R.A.
        • Vellas B.
        • Evans W.J.
        • et al.
        Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia.
        J Am Med Dir Assoc. 2011; 12: 249-256
        • Cooper C.
        • Fielding R.
        • Visser M.
        • et al.
        Tools in the assessment of sarcopenia.
        Calcif Tissue Int. 2013; 93: 201-210
        • Muscaritoli M.
        • Anker S.D.
        • Argiles J.
        • et al.
        Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) cachexia-anorexia in chronic wasting diseases and nutrition in geriatrics.
        Clin Nutr. 2010; 29: 154-159
        • Baumgartner R.N.
        • Koehler K.M.
        • Gallagher D.
        • et al.
        Epidemiology of sarcopenia among the elderly in New Mexico.
        Am J Epidemiol. 1998; 147: 755-763
        • Morley J.E.
        • Baumgartner R.N.
        • Roubenoff R.
        • et al.
        Sarcopenia.
        J Lab Clin Med. 2001; 137: 231-243
        • 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
        • 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
        • Stevenson J.C.
        A woman's journey through the reproductive, transitional and postmenopausal periods of life: impact on cardiovascular and musculo-skeletal risk and the role of estrogen replacement.
        Maturitas. 2011; 70: 197-205
        • WHO
        Facts about ageing.
        World Health Organization, 2012
        • Ferrucci L.
        • Baroni M.
        • Ranchelli A.
        • et al.
        Interaction between bone and muscle in older persons with mobility limitations.
        Curr Pharm Des. 2014; 20: 3178-3197
        • Robinson S.
        • Cooper C.
        • Aihie Sayer A.
        Nutrition and sarcopenia: a review of the evidence and implications for preventive strategies.
        J Aging Res. 2012; 2012 ([Epub 15.03.12]): 510801https://doi.org/10.1155/2012/510801
        • Sayer A.A.
        • Robinson S.M.
        • Patel H.P.
        • et al.
        New horizons in the pathogenesis, diagnosis and management of sarcopenia.
        Age Ageing. 2013; 42: 145-150
        • Kanis J.A.
        • McCloskey E.V.
        • Johansson H.
        • et al.
        European guidance for the diagnosis and management of osteoporosis in postmenopausal women.
        Osteoporos Int. 2013; 24: 23-57
        • Bauer J.
        • Biolo G.
        • Cederholm T.
        • 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
        • Deutz N.E.
        • Bauer J.M.
        • Barazzoni R.
        • et al.
        Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group.
        Clin Nutr. 2014; April (pii:S0261-5614(14)00111-3)https://doi.org/10.1016/j.clnu.2014.04.007
        • Rizzoli R.
        • Boonen S.
        • Brandi M.L.
        • et al.
        Vitamin D supplementation in elderly or postmenopausal women: a 2013 update of the 2008 recommendations from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO).
        Curr Med Res Opin. 2013; 29: 305-313
        • Novak L.P.
        Aging, total body potassium, fat-free mass, and cell mass in males and females between ages 18 and 85 years.
        J Gerontol. 1972; 27: 438-443
        • Kyle U.G.
        • Genton L.
        • Slosman D.O.
        • Pichard C.
        Fat-free and fat mass percentiles in 5225 healthy subjects aged 15–98 years.
        Nutrition. 2001; 17: 534-541
        • Ley C.J.
        • Lees B.
        • Stevenson J.C.
        Sex- and menopause-associated changes in body-fat distribution.
        Am J Clin Nutr. 1992; 55: 950-954
        • Nilwik R.
        • Snijders T.
        • Leenders M.
        • et al.
        The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size.
        Exp Gerontol. 2013; 48: 492-498
        • von Haehling S.
        • Morley J.E.
        • Anker S.D.
        From muscle wasting to sarcopenia and myopenia: update 2012.
        J Cachexia Sarcopenia Muscle. 2012; 3: 213-217
        • Leenders M.
        • Verdijk L.B.
        • van der Hoeven L.
        • et al.
        Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging.
        J Am Med Dir Assoc. 2013; 14: 585-592
        • Koster A.
        • Visser M.
        • Simonsick E.M.
        • et al.
        Association between fitness and changes in body composition and muscle strength.
        J Am Geriatr Soc. 2010; 58: 219-226
        • Janssen I.
        • Baumgartner R.N.
        • Ross R.
        • et al.
        Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women.
        Am J Epidemiol. 2004; 159: 413-421
        • Koopman R.
        • van Loon L.J.
        Aging exercise, and muscle protein metabolism.
        J Appl Physiol (1985). 2009; 106: 2040-2048
        • Ferrucci L.
        • de Cabo R.
        • Knuth N.D.
        • Studenski S.
        Of Greek heroes, wiggling worms, mighty mice, and old body builders.
        J Gerontol A: Biol Sci Med Sci. 2011; 67A: 13-16
        • Manini T.M.
        • Russ D.W.
        • Clark B.C.
        Cruz-Jentoft A.J. Morley J.E. The complex relation between muscle mass and muscle strength. John Wiley & Sons Ltd., Sarcopenia, London2012: 74-103
        • Ko Su Hausdorff J.M.
        • Ferrucci L.
        Age-associated differences in the gait pattern changes of older adults during fast-speed and fatigue conditions: results from the Baltimore longitudinal study of ageing.
        Age Ageing. 2010; 39: 688-694
        • Studenski S.
        • Perera S.
        • Patel K.
        • et al.
        Gait speed and survival in older adults.
        JAMA. 2011; 305: 50-58
        • Stevenson J.C.
        • Lees B.
        • Devenport M.
        • et al.
        Determinants of bone density in normal women: risk factors for future osteoporosis?.
        BMJ. 1989; 298: 924-928
        • Hillard T.C.
        • Whitcroft S.J.
        • Marsh M.S.
        • et al.
        Long-term effects of transdermal and oral hormone replacement therapy on postmenopausal bone loss.
        Osteoporos Int. 1994; 4: 341-348
        • Cauley J.A.
        • Robbins J.
        • Chen Z.
        • et al.
        Effects of estrogen plus progestin on risk of fracture and bone mineral density: the Women's Health Initiative randomized trial.
        JAMA. 2003; 290: 1729-1738
        • de Villiers T.J.
        • Pines A.
        • Panay N.
        • et al.
        Updated 2013 International Menopause Society recommendations on menopausal hormone therapy and preventive strategies for midlife health.
        Climacteric. 2013; 16: 316-337
        • Panay N.
        • Hamoda H.
        • Arya R.
        • Savvas M.
        The 2013 British Menopause Society & Women's Health Concern recommendations on hormone replacement therapy.
        Menopause Int. 2013; 19: 59-68
        • Gompel A.
        • Rozenberg S.
        • Barlow D.H.
        The EMAS 2008 update on clinical recommendations on postmenopausal hormone replacement therapy.
        Maturitas. 2008; 61: 227-232
        • Lowe D.A.
        • Baltgalvis K.A.
        • Greising S.M.
        Mechanisms behind estrogen's beneficial effect on muscle strength in females.
        Exerc Sport Sci Rev. 2010; 38: 61-67
        • Phillips S.K.
        • Rook K.M.
        • Siddle N.C.
        • et al.
        Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy.
        Clin Sci (Lond). 1993; 84: 95-98
        • Ronkainen P.H.
        • Kovanen V.
        • Alen M.
        • et al.
        Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs.
        J Appl Physiol (1985). 2009; 107: 25-33
        • Qaisar R.
        • Renaud G.
        • Hedstrom Y.
        • et al.
        Hormone replacement therapy improves contractile function and myonuclear organization of single muscle fibres from postmenopausal monozygotic female twin pairs.
        J Physiol. 2013; 591: 2333-2344
        • Short K.R.
        • Vittone J.L.
        • Bigelow M.L.
        • et al.
        Age and aerobic exercise training effects on whole body and muscle protein metabolism.
        Am J Physiol Endocrinol Metab. 2004; 286: E92-E101
        • Volpi E.
        • Sheffield-Moore M.
        • Rasmussen B.B.
        • Wolfe R.R.
        Basal muscle amino acid kinetics and protein synthesis in healthy young and older men.
        JAMA. 2001; 286: 1206-1212
        • Moreau K.
        • Walrand S.
        • Boirie Y.
        Protein redistribution from skeletal muscle to splanchnic tissue on fasting and refeeding in young and older healthy individuals.
        J Am Med Dir Assoc. 2013; 14: 696-704
        • Rennie M.J.
        • Edwards R.H.
        • Halliday D.
        • et al.
        Muscle protein synthesis measured by stable isotope techniques in man: the effects of feeding and fasting.
        Clin Sci (Lond). 1982; 63: 519-523
        • Cuthbertson D.
        • Smith K.
        • Babraj J.
        • et al.
        Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle.
        FASEB J. 2005; 19: 422-424
        • 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
        • Pennings B.
        • Groen B.
        • de Lange A.
        • et al.
        Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men.
        Am J Physiol Endocrinol Metab. 2012; 302: E992-E999
        • Pennings B.
        • Boirie Y.
        • Senden J.M.
        • et al.
        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
        • Wall B.T.
        • Hamer H.M.
        • de Lange A.
        • et al.
        Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men.
        Clin Nutr. 2013; 32: 412-419
        • Yang Y.
        • Breen L.
        • Burd N.A.
        • et al.
        Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men.
        Br J Nutr. 2012; 108: 1780-1788
        • Timmerman K.L.
        • Volpi E.
        Amino acid metabolism and regulatory effects in aging.
        Curr Opin Clin Nutr Metab Care. 2008; 11: 45-49
        • Dawson-Hughes B.
        • Harris S.S.
        • Rasmussen H.M.
        • Dallal G.E.
        Comparative effects of oral aromatic and branched-chain amino acids on urine calcium excretion in humans.
        Osteoporos Int. 2007; 18: 955-961
        • Bonjour J.P.
        • Kraenzlin M.
        • Levasseur R.
        • et al.
        Dairy in adulthood: from foods to nutrient interactions on bone and skeletal muscle health.
        J Am Coll Nutr. 2013; 32: 251-263
        • WHO
        Protein and amino acid requirements in human nutrition: report of a joint WHO/FAO/UNU expert consultation. Geneva.
        2007
      1. IoM. Dietary Reference Intakes for energy, carbohydrate, fiber, fat fatty acids, cholesterol, protein, and amino acids (macronutrients). Washington, DC; 2005.

      2. EFSA. Outcome of a public consultation on the draft scientific opinion of the EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA) on dietary reference values for protein. Parma, Italy; 2012.

        • Castaneda C.
        • Gordon P.L.
        • Fielding R.A.
        • et al.
        Marginal protein intake results in reduced plasma IGF-I levels and skeletal muscle fiber atrophy in elderly women.
        J Nutr Health Aging. 2000; 4: 85-90
        • Levine M.E.
        • Suarez J.A.
        • Brandhorst S.
        • et al.
        Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population.
        Cell Metab. 2014; 19: 407-417
        • Fulgoni 3rd, V.L.
        Current protein intake in America: analysis of the National Health and Nutrition Examination Survey, 2003–2004.
        Am J Clin Nutr. 2008; 87: 1554S-1557S
        • Tieland M.
        • Borgonjen-Van den Berg K.J.
        • van Loon L.J.
        • de Groot L.C.
        Dietary protein intake in community-dwelling, frail, and institutionalized elderly people: scope for improvement.
        Eur J Nutr. 2012; 51: 173-179
        • Paddon-Jones D.
        • Rasmussen B.B.
        Dietary protein recommendations and the prevention of sarcopenia.
        Curr Opin Clin Nutr Metab Care. 2009; 12: 86-90
        • Mamerow M.M.
        • Mettler J.A.
        • English K.L.
        • et al.
        Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults.
        J Nutr. 2014; 144: 876-880
        • Bouillanne O.
        • Curis E.
        • Hamon-Vilcot B.
        • et al.
        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
        • Paddon-Jones D.
        • Leidy H.
        Dietary protein and muscle in older persons.
        Curr Opin Clin Nutr Metab Care. 2014; 17: 5-11
        • Houston D.K.
        • Nicklas B.J.
        • Ding J.
        • et al.
        Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study.
        Am J Clin Nutr. 2008; 87: 150-155
        • Meng X.
        • Zhu K.
        • Devine A.
        • et al.
        A 5-year cohort study of the effects of high protein intake on lean mass and BMC in elderly postmenopausal women.
        J Bone Miner Res. 2009; 24: 1827-1834
        • Beasley J.M.
        • Wertheim B.C.
        • LaCroix A.Z.
        • et al.
        Biomarker-calibrated protein intake and physical function in the Women's Health Initiative.
        J Am Geriatr Soc. 2013; 61: 1863-1871
        • Tieland M.
        • van de Rest O.
        • Dirks M.L.
        • et al.
        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
        • Tieland M.
        • Dirks M.L.
        • van der Zwaluw N.
        • et al.
        Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: a randomized, double-blind, placebo-controlled trial.
        J Am Med Dir Assoc. 2012; 13: 713-719
        • 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
        • Schurch M.A.
        • Rizzoli R.
        • Slosman D.
        • et al.
        Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial.
        Ann Intern Med. 1998; 128: 801-809
        • Mangano K.M.
        • Sahni S.
        • Kerstetter J.E.
        Dietary protein is beneficial to bone health under conditions of adequate calcium intake: an update on clinical research.
        Curr Opin Clin Nutr Metab Care. 2014; 17: 69-74
        • Macdonald H.M.
        • New S.A.
        • Fraser W.D.
        • et al.
        Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women.
        Am J Clin Nutr. 2005; 81: 923-933
        • Dawson-Hughes B.
        • Harris S.S.
        • Rasmussen H.
        • et al.
        Effect of dietary protein supplements on calcium excretion in healthy older men and women.
        J Clin Endocrinol Metab. 2004; 89: 1169-1173
        • Kerstetter J.E.
        • Kenny A.M.
        • Insogna K.L.
        Dietary protein and skeletal health: a review of recent human research.
        Curr Opin Lipidol. 2011; 22: 16-20
        • Ammann P.
        • Laib A.
        • Bonjour J.P.
        • et al.
        Dietary essential amino acid supplements increase bone strength by influencing bone mass and bone microarchitecture in ovariectomized adult rats fed an isocaloric low-protein diet.
        J Bone Miner Res. 2002; 17: 1264-1272
        • Hannan M.T.
        • Tucker K.L.
        • Dawson-Hughes B.
        • et al.
        Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study.
        J Bone Miner Res. 2000; 15: 2504-2512
        • Darling A.L.
        • Millward D.J.
        • Torgerson D.J.
        • et al.
        Dietary protein and bone health: a systematic review and meta-analysis.
        Am J Clin Nutr. 2009; 90: 1674-1692
        • Radavelli-Bagatini S.
        • Zhu K.
        • Lewis J.R.
        • Prince R.L.
        Dairy food intake, peripheral bone structure and muscle mass in elderly ambulatory women.
        J Bone Miner Res. 2014; ([Epub 20.01.14])https://doi.org/10.1002/jbmr.2181
        • Tang M.
        • O’Connor L.E.
        • Campbell W.W.
        Diet-induced weight loss: the effect of dietary protein on bone.
        J Acad Nutr Diet. 2014; 114: 72-85
        • Beasley J.M.
        • Lacroix A.Z.
        • Larson J.C.
        • et al.
        Biomarker-calibrated protein intake and bone health in the Women's Health Initiative clinical trials and observational study.
        Am J Clin Nutr. 2014; 99: 934-940
        • Sahni S.
        • Cupples L.A.
        • McLean R.R.
        • et al.
        Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham offspring cohort.
        J Bone Miner Res. 2010; 25: 2770-2776
        • Dawson-Hughes B.
        • Castaneda-Sceppa C.
        • Harris S.S.
        • et al.
        Impact of supplementation with bicarbonate on lower-extremity muscle performance in older men and women.
        Osteoporos Int. 2010; 21: 1171-1179
        • Jehle S.
        • Hulter H.N.
        • Krapf R.
        Effect of potassium citrate on bone density, microarchitecture, and fracture risk in healthy older adults without osteoporosis: a randomized controlled trial.
        J Clin Endocrinol Metab. 2013; 98: 207-217
        • Buclin T.
        • Cosma M.
        • Appenzeller M.
        • et al.
        Diet acids and alkalis influence calcium retention in bone.
        Osteoporos Int. 2001; 12: 493-499
        • Fenton T.R.
        • Tough S.C.
        • Lyon A.W.
        • et al.
        Causal assessment of dietary acid load and bone disease: a systematic review & meta-analysis applying Hill's epidemiologic criteria for causality.
        Nutr J. 2011; 10: 41
        • Schoenau E.
        • Fricke O.
        Mechanical influences on bone development in children.
        Eur J Endocrinol. 2008; 159: S27-S31
        • Leenders M.
        • Verdijk L.B.
        • van der Hoeven L.
        • et al.
        Elderly men and women benefit equally from prolonged resistance-type exercise training.
        J Gerontol A: Biol Sci Med Sci. 2013; 68: 769-779
        • Nelson M.E.
        • Rejeski W.J.
        • Blair S.N.
        • et al.
        Physical activity and public health in older adults: recommendation from the American College of Sports Medicine and the American Heart Association.
        Circulation. 2007; 116: 1094-1105
        • Chodzko-Zajko W.J.
        • Proctor D.N.
        • Fiatarone Singh M.A.
        • et al.
        American College of Sports Medicine position stand. Exercise and physical activity for older adults.
        Med Sci Sports Exerc. 2009; 41: 1510-1530
        • Gianoudis J.
        • Bailey C.A.
        • Sanders K.M.
        • et al.
        Osteo-cise: Strong Bones for Life: protocol for a community-based randomised controlled trial of a multi-modal exercise and osteoporosis education program for older adults at risk of falls and fractures.
        BMC Musculoskelet Disord. 2012; 13: 78
        • Gianoudis J.
        • Bailey C.A.
        • Ebeling P.R.
        • et al.
        Effects of a targeted multimodal exercise program incorporating high-speed power training on falls and fracture risk factors in older adults: a community-based randomized controlled trial.
        J Bone Miner Res. 2014; 29: 182-191
        • Holm L.
        • Olesen J.L.
        • Matsumoto K.
        • et al.
        Protein-containing nutrient supplementation following strength training enhances the effect on muscle mass, strength, and bone formation in postmenopausal women.
        J Appl Physiol (1985). 2008; 105: 274-281
        • Nikander R.
        • Sievanen H.
        • Heinonen A.
        • et al.
        Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life.
        BMC Med. 2010; 8: 47
        • Biolo G.
        • Maggi S.P.
        • Williams B.D.
        • et al.
        Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans.
        Am J Physiol. 1995; 268: E514-E520
        • Mithal A.
        • Bonjour J.P.
        • Boonen S.
        • et al.
        Impact of nutrition on muscle mass, strength, and performance in older adults.
        Osteoporos Int. 2013; 24: 1555-1566
        • Tang J.E.
        • Manolakos J.J.
        • Kujbida G.W.
        • et al.
        Minimal whey protein with carbohydrate stimulates muscle protein synthesis following resistance exercise in trained young men.
        Appl Physiol Nutr Metab. 2007; 32: 1132-1138
        • Biolo G.
        • Tipton K.D.
        • Klein S.
        • Wolfe R.R.
        An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein.
        Am J Physiol. 1997; 273: E122-E129
        • Moore D.R.
        • Tang J.E.
        • Burd N.A.
        • et al.
        Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise.
        J Physiol. 2009; 587: 897-904
        • Pennings B.
        • Koopman R.
        • Beelen M.
        • et al.
        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
        • Drummond M.J.
        • Dreyer H.C.
        • Pennings B.
        • et al.
        Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging.
        J Appl Physiol (1985). 2008; 104: 1452-1461
        • Reitelseder S.
        • Agergaard J.
        • Doessing S.
        • et al.
        Positive muscle protein net balance and differential regulation of atrogene expression after resistance exercise and milk protein supplementation.
        Eur J Nutr. 2014; 53: 321-333
        • Cermak N.M.
        • Res P.T.
        • de Groot L.C.
        • et al.
        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
        • Josse A.R.
        • Tang J.E.
        • Tarnopolsky M.A.
        • Phillips S.M.
        Body composition and strength changes in women with milk and resistance exercise.
        Med Sci Sports Exerc. 2010; 42: 1122-1130
        • Josse A.R.
        • Phillips S.M.
        Impact of milk consumption and resistance training on body composition of female athletes.
        Med Sport Sci. 2012; 59: 94-103
        • Rolland Y.
        • Dupuy C.
        • van Kan Abellan G.
        • et al.
        Treatment strategies for sarcopenia and frailty.
        Med Clin North Am. 2011; 95 (ix): 427-438
        • Morelli S.
        • de Boland A.R.
        • Boland R.L.
        Generation of inositol phosphates, diacylglycerol and calcium fluxes in myoblasts treated with 1,25-dihydroxyvitamin D3.
        Biochem J. 1993; 289: 675-679
        • Pfeifer M.
        • Begerow B.
        • Minne H.W.
        Vitamin D and muscle function.
        Osteoporos Int. 2002; 13: 187-194
        • Salles J.
        • Chanet A.
        • Giraudet C.
        • et al.
        1,25(OH)2-vitamin D3 enhances the stimulating effect of leucine and insulin on protein synthesis rate through Akt/PKB and mTOR mediated pathways in murine C2C12 skeletal myotubes.
        Mol Nutr Food Res. 2013; 57: 2137-2146
        • 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
        • Bischoff H.A.
        • Borchers M.
        • Gudat F.
        • et al.
        In situ detection of 1,25-dihydroxyvitamin D3 receptor in human skeletal muscle tissue.
        Histochem J. 2001; 33: 19-24
        • Bischoff-Ferrari H.A.
        • Borchers M.
        • Gudat F.
        • et al.
        Vitamin D receptor expression in human muscle tissue decreases with age.
        J Bone Miner Res. 2004; 19: 265-269
        • Bischoff-Ferrari H.A.
        • Dietrich T.
        • Orav E.J.
        • et al.
        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
        • Visser M.
        • Deeg D.J.
        • Lips P.
        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
        • Wicherts I.S.
        • van Schoor N.M.
        • Boeke A.J.
        • et al.
        Vitamin D status predicts physical performance and its decline in older persons.
        J Clin Endocrinol Metab. 2007; 92: 2058-2065
        • Houston D.K.
        • Tooze J.A.
        • Neiberg R.H.
        • 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
        • Faulkner K.A.
        • Cauley J.A.
        • Zmuda J.M.
        • et al.
        Higher 1,25-dihydroxyvitamin D3 concentrations associated with lower fall rates in older community-dwelling women.
        Osteoporos Int. 2006; 17: 1318-1328
        • Snijder M.B.
        • van Schoor N.M.
        • Pluijm S.M.
        • et al.
        Vitamin D status in relation to one-year risk of recurrent falling in older men and women.
        J Clin Endocrinol Metab. 2006; 91: 2980-2985
        • Sato Y.
        • Iwamoto J.
        • Kanoko T.
        • Satoh K.
        Low-dose vitamin D prevents muscular atrophy and reduces falls and hip fractures in women after stroke: a randomized controlled trial.
        Cerebrovasc Dis. 2005; 20: 187-192
        • Ceglia L.
        • Niramitmahapanya S.
        • da Silva Morais M.
        • et al.
        A randomized study on the effect of vitamin D3 supplementation on skeletal muscle morphology and vitamin D receptor concentration in older women.
        J Clin Endocrinol Metab. 2013; 98: E1927-E1935
        • Glerup H.
        • Mikkelsen K.
        • Poulsen L.
        • et al.
        Hypovitaminosis D myopathy without biochemical signs of osteomalacic bone involvement.
        Calcif Tissue Int. 2000; 66: 419-424
        • 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
        • Stockton K.A.
        • Mengersen K.
        • Paratz J.D.
        • et al.
        Effect of vitamin D supplementation on muscle strength: a systematic review and meta-analysis.
        Osteoporos Int. 2011; 22: 859-871
        • Michael Y.L.
        • Whitlock E.P.
        • Lin J.S.
        • et al.
        Primary care-relevant interventions to prevent falling in older adults: a systematic evidence review for the U.S. Preventive Services Task Force.
        Ann Intern Med. 2010; 153: 815-825
        • Murad M.H.
        • Elamin K.B.
        • Abu Elnour N.O.
        • et al.
        Clinical review: the effect of vitamin D on falls: a systematic review and meta-analysis.
        J Clin Endocrinol Metab. 2011; 96: 2997-3006
        • Bischoff-Ferrari H.A.
        • Dawson-Hughes B.
        • Staehelin H.B.
        • et al.
        Fall prevention with supplemental and active forms of vitamin D: a meta-analysis of randomised controlled trials.
        BMJ. 2009; 339: b3692
        • Ross A.C.
        • Manson J.E.
        • Abrams S.A.
        • et al.
        The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know.
        J Clin Endocrinol Metab. 2011; 96: 53-58
        • Gillespie L.D.
        • Robertson M.C.
        • Gillespie W.J.
        • et al.
        Interventions for preventing falls in older people living in the community.
        Cochrane Database Syst Rev. 2009; : CD007146
        • Katsanos C.S.
        • Kobayashi H.
        • Sheffield-Moore M.
        • et al.
        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. 2006; 291: E381-E387
        • Phillips S.M.
        • Tang J.E.
        • Moore D.R.
        The role of milk- and soy-based protein in support of muscle protein synthesis and muscle protein accretion in young and elderly persons.
        J Am Coll Nutr. 2009; 28: 343-354
        • Caroli A.
        • Poli A.
        • Ricotta D.
        • et al.
        Invited review: dairy intake and bone health: a viewpoint from the state of the art.
        J Dairy Sci. 2011; 94: 5249-5262
        • Rizzoli R.
        Dairy products, yogurts, and bone health.
        Am J Clin Nutr. 2014; 99: 1256S-1262S

      Linked Article