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Protein Supplementation Augments Muscle Fiber Hypertrophy but Does Not Modulate Satellite Cell Content During Prolonged Resistance-Type Exercise Training in Frail Elderly

      Abstract

      Objective

      Protein supplementation increases gains in lean body mass following prolonged resistance-type exercise training in frail older adults. We assessed whether the greater increase in lean body mass can be attributed to muscle fiber type specific hypertrophy with concomitant changes in satellite cell (SC) content.

      Design

      A total of 34 frail elderly individuals (77 ± 1 years, n = 12 male adults) participated in this randomized, double-blind, placebo-controlled trial with 2 arms in parallel.

      Intervention

      Participants performed 24 weeks of progressive resistance-type exercise training (2 sessions per week) during which they were supplemented twice-daily with milk protein (2 × 15 g) or a placebo.

      Methods

      Muscle biopsies were taken at baseline, and after 12 and 24 weeks of intervention, to determine type I and type II muscle fiber specific cross-sectional area (CSA), SC content, and myocellular characteristics.

      Results

      In the placebo group, a trend for a 20% ± 11% increase in muscle fiber CSA was observed in type II fibers only (P = .051), with no increase in type I muscle fiber CSA. In the protein group, type I and II muscle fiber CSA increased by 23% ± 7% and 34% ± 10% following 6 months of training, respectively (P < .01). Myonuclear domain size increased over time in both groups and fiber types (P < .001), with no significant differences between groups (P > .05). No changes in myonuclear content and SC contents were observed over time in either group (both P > .05). Regression analysis showed that changes in myonuclear content and domain size are predictive of muscle fiber hypertrophy.

      Conclusions

      Protein supplementation augments muscle fiber hypertrophy following prolonged resistance-type exercise training in frail older people, without changes in myonuclear and SC content.

      Keywords

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      References

        • Abellan van Kan G.
        • Rolland Y.
        • Bergman H.
        • et al.
        The I.A.N.A Task Force on frailty assessment of older people in clinical practice.
        J Nutr Health Aging. 2008; 12: 29-37
        • Fried L.P.
        • Tangen C.M.
        • Walston J.
        • et al.
        Frailty in older adults: Evidence for a phenotype.
        J Gerontol A Biol Sci Med Sci. 2001; 56: M146-M156
        • Evans W.J.
        • Paolisso G.
        • Abbatecola A.M.
        • et al.
        Frailty and muscle metabolism dysregulation in the elderly.
        Biogerontology. 2010; 11: 527-536
        • Evans W.J.
        What is sarcopenia?.
        J Gerontol A Biol Sci Med Sci. 1995; 50: 5-8
        • 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
        • Morley J.E.
        • Anker S.D.
        • von Haehling S.
        Prevalence, incidence, and clinical impact of sarcopenia: Facts, numbers, and epidemiology-update 2014.
        J Cachexia Sarcopenia Muscle. 2014; 5: 253-259
        • Phillips S.M.
        • Tipton K.D.
        • Aarsland A.
        • et al.
        Mixed muscle protein synthesis and breakdown after resistance exercise in humans.
        Am J Physiol. 1997; 273: E99-E107
        • Tipton K.D.
        • Ferrando A.A.
        • Phillips S.M.
        • et al.
        Postexercise net protein synthesis in human muscle from orally administered amino acids.
        Am J Physiol. 1999; 276: E628-E634
        • 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
        • Tieland M.
        • Borgonjen-Van den Berg K.J.
        • van Loon L.J.
        • et al.
        Dietary protein intake in community-dwelling, frail, and institutionalized elderly people: Scope for improvement.
        Eur J Nutr. 2012; 51: 173-179
        • 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
        • Fosbol M.O.
        • Zerahn B.
        Contemporary methods of body composition measurement.
        Clin Physiol Funct Imaging. 2015; 35: 81-97
        • Cheek D.B.
        The control of cell mass and replication. The DNA unit–a personal 20-year study.
        Early Hum Dev. 1985; 12: 211-239
        • Moss F.P.
        • Leblond C.P.
        Nature of dividing nuclei in skeletal muscle of growing rats.
        J Cell Biol. 1970; 44: 459-462
        • Schiaffino S.
        • Bormioli S.P.
        • Aloisi M.
        The fate of newly formed satellite cells during compensatory muscle hypertrophy.
        Virchows Arch B Cell Pathol. 1976; 21: 113-118
        • Fry C.S.
        • Lee J.D.
        • Jackson J.R.
        • et al.
        Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy.
        FASEB J. 2014; 28: 1654-1665
        • Snijders T.
        • Verdijk L.B.
        • van Loon L.J.
        The impact of sarcopenia and exercise training on skeletal muscle satellite cells.
        Ageing Res Rev. 2009; 8: 328-338
        • Hawke T.J.
        • Garry D.J.
        Myogenic satellite cells: Physiology to molecular biology.
        J Appl Physiol. 2001; 91: 534-551
        • Kryger A.I.
        • Andersen J.L.
        Resistance training in the oldest old: Consequences for muscle strength, fiber types, fiber size, and MHC isoforms.
        Scand J Med Sci Sports. 2007; 17: 422-430
        • Levey A.S.
        • Coresh J.
        • Greene T.
        • et al.
        Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate.
        Ann Intern Med. 2006; 145: 247-254
        • Mayhew J.L.
        • Prinster J.L.
        • Ware J.S.
        • et al.
        Muscular endurance repetitions to predict bench press strength in men of different training levels.
        J Sports Med Phys Fitness. 1995; 35: 108-113
        • Bergstrom J.
        Percutaneous needle biopsy of skeletal muscle in physiological and clinical research.
        Scand J Clin Lab Invest. 1975; 35: 609-616
        • Verdijk L.B.
        • Koopman R.
        • Schaart G.
        • et al.
        Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly.
        Am J Physiol Endocrinol Metab. 2007; 292: E151-E157
        • Dirks M.L.
        • Hansen D.
        • Van Assche A.
        • et al.
        Neuromuscular electrical stimulation prevents muscle wasting in critically ill comatose patients.
        Clin Sci (Lond). 2015; 128: 357-365
        • Mackey A.L.
        • Andersen L.L.
        • Frandsen U.
        • et al.
        Distribution of myogenic progenitor cells and myonuclei is altered in women with vs those without chronically painful trapezius muscle.
        J Appl Physiol. 2010; 109: 1920-1929
        • Edelstein A.D.
        • Tsuchida M.A.
        • Amodaj N.
        • et al.
        Advanced methods of microscope control using muManager software.
        J Biol Methods. 2014; 1: e10
        • Strandberg S.
        • Wretling M.L.
        • Wredmark T.
        • et al.
        Reliability of computed tomography measurements in assessment of thigh muscle cross-sectional area and attenuation.
        BMC Med Imaging. 2010; 10: 18
        • Kosek D.J.
        • Kim J.S.
        • Petrella J.K.
        • et al.
        Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults.
        J Appl Physiol. 2006; 101: 531-544
        • 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
        • Verdijk L.B.
        • Snijders T.
        • Beelen M.
        • et al.
        Characteristics of muscle fiber type are predictive of skeletal muscle mass and strength in elderly men.
        J Am Geriatr Soc. 2010; 58: 2069-2075
        • Lexell J.
        • Taylor C.C.
        • Sjostrom M.
        What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men.
        J Neurol Sci. 1988; 84: 275-294
        • 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
        • Andersen J.L.
        • Aagaard P.
        Effects of strength training on muscle fiber types and size; consequences for athletes training for high-intensity sport.
        Scand J Med Sci Sports. 2010; 20: 32-38
        • Verdijk L.B.
        • Gleeson B.G.
        • Jonkers R.A.
        • et al.
        Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men.
        J Gerontol A Biol Sci Med Sci. 2009; 64: 332-339
        • Leenders M.
        • Verdijk L.B.
        • Van der Hoeven L.
        • et al.
        Protein supplementation during resistance-type exercise training in the elderly.
        Med Sci Sports Exerc. 2013; 45: 542-552
        • Verdijk L.B.
        • Snijders T.
        • Drost M.
        • et al.
        Satellite cells in human skeletal muscle; from birth to old age.
        Age (Dordr). 2014; 36: 545-547
        • Fiatarone M.A.
        • Marks E.C.
        • Ryan N.D.
        • et al.
        High-intensity strength training in nonagenarians. Effects on skeletal muscle.
        JAMA. 1990; 263: 3029-3034
        • Fiatarone M.A.
        • O'Neill E.F.
        • Ryan N.D.
        • et al.
        Exercise training and nutritional supplementation for physical frailty in very elderly people.
        N Engl J Med. 1994; 330: 1769-1775
        • Petrella J.K.
        • Kim J.S.
        • Cross J.M.
        • et al.
        Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women.
        Am J Physiol Endocrinol Metab. 2006; 291: E937-E946
        • Petrella J.K.
        • Kim J.S.
        • Mayhew D.L.
        • et al.
        Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: A cluster analysis.
        J Appl Physiol (1985). 2008; 104: 1736-1742
        • Verney J.
        • Kadi F.
        • Charifi N.
        • et al.
        Effects of combined lower body endurance and upper body resistance training on the satellite cell pool in elderly subjects.
        Muscle Nerve. 2008; 38: 1147-1154
        • Hikida R.S.
        • Walsh S.
        • Barylski N.
        • et al.
        Is hypertrophy limited in elderly muscle fibers? A comparison of elderly and young strength-trained men.
        BAM. 1998; 8: 419-427
        • Snijders T.
        • Smeets J.S.
        • van Kranenburg J.
        • et al.
        Changes in myonuclear domain size do not precede muscle hypertrophy during prolonged resistance-type exercise training.
        Acta Physiol (Oxf). 2016; 216: 231-239