Skip to main content

Advertisement

Log in

Influences of carbohydrate plus amino acid supplementation on differing exercise intensity adaptations in older persons: skeletal muscle and endocrine responses

  • Published:
AGE Aims and scope Submit manuscript

Abstract

Losses in physiological function in healthy ageing occur partly as a consequence of reduced protein intake and partly as a consequence of less than 30-min/day of moderate to vigorous physical activity. The current study aimed to compare the effects of two different intensities of resistance training in healthy older adults, whose habitual dietary intake was supplemented with carbohydrate and amino acid preparations. We hypothesised that although intensive exercise with appropriate carbohydrate and amino acid supplementation would result in the most profound impact on in vivo markers of healthy physiologic and endocrine functions in previously sedentary older individuals, the effectiveness of the less intense exercise prescription with supplementation would also result in beneficial adaptations over and above findings of previous studies on low intensity exercise alone. Twenty-nine older adults (out of 32) completed the study after being randomly assigned to low (SUP_LowR, i.e., ∼40% 1RM; n = 16) versus high resistance training (SUP_HighR, i.e., ∼80% 1RM; n = 13) for 12 weeks. A carbohydrate supplement was ingested immediately before and during every exercise session and an amino acid cocktail was ingested post-exercise. Neither intervention significantly impacted upon body composition assessed using: Body mass index, waist/hip ratio and bioelectric impedance. Muscle strength increased similarly in the two groups with the SUP_HighR protocol showing 46 ± 8%, 10.8 ± 4.4% and 26.9 ± 4.9% (P < 0.01) improvements in 1-RM strength, unilateral and bilateral knee extension torque, respectively, compared with 39 ± 2%, 9.4 ± 3.7% and 29.5 ± 8.2% (P < 0.01) increments in the same measures in the SUP_LowR group. Lean muscle thickness however, showed a greater benefit of the SUP_LowR protocol (8.7 ± 3.9% increase, P < 0.05) compared with the SUP_HighR protocol, which elicited no significant change. In terms of functional abilities, only the standing-from-lying (SFL) test exhibited an improvement in rate in the SUP_HighR group (−11.4%, P < 0.05). The SUP_LowR group, on the other hand, showed significant improvements in the get-up-and-go (−8.7 ± 3.6%, P < 0.05), the SFL (−4.7% change, P = 0.05) and the 6-min walk (7.2 ± 2.2% increase in distance covered, P < 0.01) tests. Following overnight fasting, serum levels of glucose changed significantly (−13 ± 4.7% decrease, P < 0.01) in SUP_LowR. Serum levels of insulin (−25 ± 5.3% decrease, P = 0.05), neuropeptide Y (−24 ± 15.3% decrease, P = 0.02), and IGFBP-3 (−11 ± 6.6% decrease, P = 0.03), changed significantly in SUP_HighR. Circulating levels of interleukin-6, tumour necrosis factor-alpha and insulin-like growth factor 1 did not alter significantly in either intervention group. These data suggest that whilst both interventions were beneficial in older persons, the end targets as well as metabolic and hormonal adaptations are different. The supplementation plus low exercise regimen tended to impact on muscle hypertrophy combined with increased habitual function. Supplementation plus high-intensity exercise regimen improved markers of strength, but not to a significantly greater extent than supplementation plus low intensity exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Baba NH, Sawaya S, Torbay N, Habbal Z, Azar S, Hashim SA (1999) High protein vs high carbohydrate hypoenergetic diet for the treatment of obese hyperinsulinemic subjects. Int J Obes Relat Metab Disord 23(11):1202–1206

    Article  CAS  PubMed  Google Scholar 

  • Balagopal P, Rooyackers OE, Adey DB, Ades PA, Nair KS (1997) Effects of aging on in vivo synthesis of skeletal muscle myosin heavy chain and sarcoplasmic protein in humans. Am J Physiol 273(4 Pt 1):E790–E800

    CAS  PubMed  Google Scholar 

  • Blumberg J (1994) Nutrient requirements of the healthy elderly—should there be specific RDAs? Nutr Rev 52(8 Pt 2):S15–S18

    CAS  PubMed  Google Scholar 

  • Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R et al (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3(11):1014–1019

    Article  CAS  PubMed  Google Scholar 

  • Bohe J, Low A, Wolfe RR, Rennie MJ (2003) Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J Physiol 552(Pt 1):315–324

    Article  CAS  PubMed  Google Scholar 

  • Bolster DR, Kubica N, Crozier SJ, Williamson DL, Farrell PA, Kimball SR et al (2003) Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle. J Physiol 553(Pt 1):213–220

    Article  CAS  PubMed  Google Scholar 

  • Bonnefoy M, Cornu C, Normand S, Boutitie F, Bugnard F, Rahmani A et al (2003) The effects of exercise and protein-energy supplements on body composition and muscle function in frail elderly individuals: a long-term controlled randomised study. Br J Nutr 89(5):731–739

    Article  CAS  PubMed  Google Scholar 

  • Borsheim E, Aarsland A, Wolfe RR (2004) Effect of an amino acid, protein, and carbohydrate mixture on net muscle protein balance after resistance exercise. Int J Sport Nutr Exerc Metab 14(3):255–271

    CAS  PubMed  Google Scholar 

  • Borsheim E, Bui QU, Tissier S, Kobayashi H, Ferrando AA, Wolfe RR (2008) Effect of amino acid supplementation on muscle mass, strength and physical function in elderly. Clin Nutr 27(2):189–195

    Article  CAS  PubMed  Google Scholar 

  • Campbell WW, Crim MC, Young VR, Joseph LJ, Evans WJ (1995) Effects of resistance training and dietary protein intake on protein metabolism in older adults. Am J Physiol 268(6 Pt 1):E1143–E1153

    CAS  PubMed  Google Scholar 

  • Campbell WW, Trappe TA, Wolfe RR, Evans WJ (2001) The recommended dietary allowance for protein may not be adequate for older people to maintain skeletal muscle. J Gerontol A Biol Sci Med Sci 56(6):M373–M380

    CAS  PubMed  Google Scholar 

  • Castaneda C, Charnley JM, Evans WJ, Crim MC (1995) Elderly women accommodate to a low-protein diet with losses of body cell mass, muscle function, and immune response. Am J Clin Nutr 62(1):30–39

    CAS  PubMed  Google Scholar 

  • Chandler JM, Duncan PW, Kochersberger G, Studenski S (1998) Is lower extremity strength gain associated with improvement in physical performance and disability in frail, community-dwelling elders? Arch Phys Med Rehabil 79(1):24–30

    Article  CAS  PubMed  Google Scholar 

  • Chernoff R (2004) Protein and older adults. J Am Coll Nutr 23(6 Suppl):627S–630S

    CAS  PubMed  Google Scholar 

  • Chevalier S, Gougeon R, Nayar K, Morais JA (2003) Frailty amplifies the effects of aging on protein metabolism: role of protein intake. Am J Clin Nutr 78:422–429

    CAS  PubMed  Google Scholar 

  • Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P et al (2005) Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19(3):422–424

    CAS  PubMed  Google Scholar 

  • Dreyer HC, Drummond MJ, Pennings B, Fujita S, Glynn EL, Chinkes DL et al (2008) Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am J Physiol Endocrinol Metab 294(2):E392–E400

    Article  CAS  PubMed  Google Scholar 

  • Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M (2001) Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol 535(Pt 1):301–311

    Article  CAS  PubMed  Google Scholar 

  • Fiatarone MA, O’Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME et al (1994) Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med 330(25):1769–1775

    Article  CAS  PubMed  Google Scholar 

  • Fiatarone Singh MA, Bernstein MA, Ryan AD, O’Neill EF, Clements KM, Evans WJ (2000) The effect of oral nutritional supplements on habitual dietary quality and quantity in frail elders. J Nutr Health Aging 4(1):5–12

    CAS  PubMed  Google Scholar 

  • Frontera WR, Meredith CN, O’Reilly KP, Knuttgen HG, Evans WJ (1988) Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 64(3):1038–1044

    CAS  PubMed  Google Scholar 

  • Guigoz Y (2006) The Mini Nutritional Assessment (MNA) review of the literature—what does it tell us? J Nutr Health Aging 10(6):466–485, Discussion 485-7

    CAS  PubMed  Google Scholar 

  • Gray-Donald K, Payette H, Boutier V (1995) Randomized clinical trial of nutritional supplementation shows little effect on functional status among free-living frail elderly. J Nutr 125(12):2965–2971

    CAS  PubMed  Google Scholar 

  • Jensen MB, Hessov I (1997) Dietary supplementation at home improves the regain of lean body mass after surgery. Nutrition 13(5):422–430

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen JO, Vahl N, Hansen TB, Thuesen L, Hagen C, Christiansen JS (1996) Growth hormone versus placebo treatment for one year in growth hormone deficient adults: increase in exercise capacity and normalization of body composition. Clin Endocrinol (Oxf) 45(6):681–688

    Article  CAS  Google Scholar 

  • Kaiser FE, Morley JE (1994) Idiopathic CD4+ T lymphopenia in older persons. J Am Geriatr Soc 42(12):1291–1294

    CAS  PubMed  Google Scholar 

  • Kimball SR, Jefferson LS (1994) Mechanisms of translational control in liver and skeletal muscle. Biochimie 76(8):729–736

    Article  CAS  PubMed  Google Scholar 

  • Klitgaard H, Mantoni M, Schiaffino S, Ausoni S, Gorza L, Laurent-Winter C et al (1990) Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol Scand 140(1):41–54

    Article  CAS  PubMed  Google Scholar 

  • Lauque S, Arnaud-Battandier F, Mansourian R, Guigoz Y, Paintin M, Nourhashemi F et al (2000) Protein-energy oral supplementation in malnourished nursing home residents. A controlled trial. Age Ageing 29(1):51–56

    Article  CAS  PubMed  Google Scholar 

  • Levenhagen DK, Carr C, Carlson MG, Maron DJ, Borel MJ, Flakoll PJ (2002) Post-exercise protein intake enhances whole body and leg protein accretion in humans. Med Sci Sports Exerc 34(5):828–837

    Article  CAS  PubMed  Google Scholar 

  • Lintsi M, Kaarma H, Kull I (2004) Comparison of hand-to-hand bioimpedance and anthropometry equations versus dual-energy X-ray absorptiometry for the assessment of body fat percentage in 17-18-year-old conscripts. Clin Physiol Funct Imaging 24(2):85–90

    Article  PubMed  Google Scholar 

  • Lucas M, Heiss CJ (2005) Protein needs of older adults engaged in resistance training: a review. J Aging Phys Act 13(2):223–236

    PubMed  Google Scholar 

  • Meredith CN, Frontera WR, O’Reilly KP, Evans WJ (1992) Body composition in elderly men: effect of dietary modification during strength training. J Am Geriatr Soc 40(2):155–162

    CAS  PubMed  Google Scholar 

  • Onambélé GL, Maganaris CN, Mian OS, Tam E, Rejc E, McEwan IM et al (2008) Inertial vs. isotonic training in old age: neuromuscular and balance effects. J Biomechanics 41(15):3133–3138

    Article  Google Scholar 

  • Onambele GN, Bruce SA, Woledge RC (2006) Oestrogen status in relation to the early training responses in human thumb adductor muscles. Acta Physiol (Oxf) 188(1):41–52

    Article  CAS  Google Scholar 

  • Paddon-Jones D, Sheffield-Moore M, Aarsland A, Wolfe RR, Ferrando AA (2005) Exogenous amino acids stimulate human muscle anabolism without interfering with the response to mixed meal ingestion. Am J Physiol Endocrinol Metab 288(4):E761–E767

    Article  CAS  PubMed  Google Scholar 

  • Paddon-Jones D, Sheffield-Moore M, Katsanos CS, Zhang XJ, Wolfe RR (2006) Differential stimulation of muscle protein synthesis in elderly humans following isocaloric ingestion of amino acids or whey protein. Exp Gerontol 41(2):215–219

    Article  CAS  PubMed  Google Scholar 

  • Payette H, Boutier V, Coulombe C, Gray-Donald K (2002) Benefits of nutritional supplementation in free-living, frail, undernourished elderly people: a prospective randomized community trial. J Am Diet Assoc 102(8):1088–1095

    PubMed  Google Scholar 

  • Pearson SJ, Onambele GN (2005) Acute changes in knee-extensors torque, fiber pennation, and tendon characteristics. Chronobiol Int 22(6):1013–1027

    Article  PubMed  Google Scholar 

  • Pearson SJ, Onambele GN (2006) Influence of time of day on tendon compliance and estimations of voluntary activation levels. Muscle Nerve 33(6):792–800

    Article  PubMed  Google Scholar 

  • Prior BM, Cureton KJ, Modlesky CM, Evans EM, Sloniger MA, Saunders M et al (1997) In vivo validation of whole body composition estimates from dual-energy X-ray absorptiometry. J Appl Physiol 83(2):623–630

    CAS  PubMed  Google Scholar 

  • Rea IM, Alexander HD, Crockard AD, Morris TC (1996) CD4 lymphopenia in very elderly people. Lancet 347(8997):328–329

    CAS  PubMed  Google Scholar 

  • Roberts RG, Redfern CP, Goodship TH (2003) Effect of insulin upon protein degradation in cultured human myocytes. Eur J Clin Invest 33(10):861–867

    Article  CAS  PubMed  Google Scholar 

  • Rosendahl E, Lindelof N, Littbrand H, Yifter-Lindgren E, Lundin-Olsson L, Haglin L et al (2006) High-intensity functional exercise program and protein-enriched energy supplement for older persons dependent in activities of daily living: a randomised controlled trial. Aust J Physiother 52(2):105–113

    PubMed  Google Scholar 

  • Shizgal HM, Martin MF, Gimmon Z (1992) The effect of age on the caloric requirement of malnourished individuals. Am J Clin Nutr 55(4):783–789

    CAS  PubMed  Google Scholar 

  • Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS (2004) Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol Endocrinol Metab 286(1):E92–E101

    Article  CAS  PubMed  Google Scholar 

  • Skelton DA, Young A, Greig CA, Malbut KE (1995) Effects of resistance training on strength, power, and selected functional abilities of women aged 75 and older. J Am Geriatr Soc 43(10):1081–1087

    CAS  PubMed  Google Scholar 

  • Solerte SB, Gazzaruso C, Schifino N, Locatelli E, Destro T, Ceresini G et al (2004) Metabolic effects of orally administered amino acid mixture in elderly subjects with poorly controlled type 2 diabetes mellitus. Am J Cardiol 93(8A):23A–29A

    Article  CAS  PubMed  Google Scholar 

  • Tidball JG (2005) Mechanical signal transduction in skeletal muscle growth and adaptation. J Appl Physiol 98(5):1900–1908

    Article  CAS  PubMed  Google Scholar 

  • Tipton KD, Elliott TA, Cree MG, Aarsland AA, Sanford AP, Wolfe RR (2007) Stimulation of net muscle protein synthesis by whey rotein ingestion before and after exercise. Am J Physiol Endocrinol Metab 292:E71–E76

    Article  CAS  PubMed  Google Scholar 

  • Tobin J, Spector D (1986) Dietary protein has no effect on future creatinine clearance. Gerontologist 26:59A

    Google Scholar 

  • Tonino RP (1989) Effect of physical training on the insulin resistance of aging. Am J Physiol 256(3 Pt 1):E352–E356

    CAS  PubMed  Google Scholar 

  • Vellas BJ, Hunt WC, Romero LJ, Koehler KM, Baumgartner RN, Garry PJ (1997) Changes in nutritional status and patterns of morbidity among free-living elderly persons: a 10-year longitudinal study. Nutrition 13(6):515–519

    Article  CAS  PubMed  Google Scholar 

  • Ventadour S, Attaix D (2006) Mechanisms of skeletal muscle atrophy. Curr Opin Rheumatol 18(6):631–635

    Article  CAS  PubMed  Google Scholar 

  • Volkert D, Kruse W, Oster P, Schlierf G (1992) Malnutrition in geriatric patients: diagnostic and prognostic significance of nutritional parameters. Ann Nutr Metab 36(2):97–112

    Article  CAS  PubMed  Google Scholar 

  • Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR (2003) Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am J Clin Nutr 78(2):250–258

    CAS  PubMed  Google Scholar 

  • Volpi E, Mittendorfer B, Rasmussen BB, Wolfe RR (2000) The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. J Clin Endocrinol Metab 85(12):4481–4490

    Article  CAS  PubMed  Google Scholar 

  • Volpi E, Mittendorfer B, Wolf SE, Wolfe RR (1999) Oral amino acids stimulate muscle protein anabolism in the elderly despite higher first-pass splanchnic extraction. Am J Physiol 277(3 Pt 1):E513–E520

    CAS  PubMed  Google Scholar 

  • Wagenmakers AJ (1999) Tracers to investigate protein and amino acid metabolism in human subjects. Proc Nutr Soc 58(4):987–1000

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Barbaro MF, Baraban SC (2006) A role for the mTOR pathway in surface expression of AMPA receptors. Neurosci Lett 401(1–2):35–39

    Article  CAS  PubMed  Google Scholar 

  • Welle S, Thornton CA (1998) High-protein meals do not enhance myofibrillar synthesis after resistance exercise in 62- to 75-yr-old men and women. Am J Physiol 274(4 Pt 1):E677–E683

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gladys Leopoldine Onambélé-Pearson.

About this article

Cite this article

Onambélé-Pearson, G.L., Breen, L. & Stewart, C.E. Influences of carbohydrate plus amino acid supplementation on differing exercise intensity adaptations in older persons: skeletal muscle and endocrine responses. AGE 32, 125–138 (2010). https://doi.org/10.1007/s11357-009-9129-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-009-9129-9

Keywords

Navigation