Low-load resistance training during step-reduction attenuates declines in muscle mass and strength and enhances anabolic sensitivity in older men

Physiological Reports

Volumn 3, Issue 8, 2015, Pages

  Devries, Michaela C ^a   Breen, Leigh ^a,b   Von Allmen, Mark ^a   MacDonald, Maureen J ^a   Moore, Daniel R ^c   Offord, Elizabeth A ^d   Horcajada, Marie Noëlle ^d   Breuillé, Denis ^d   Phillips, Stuart M ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF TORONTO   (Canada)

^d NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

Anabolic resistance; Resistance training; Sarcopenia; Step reduction

Indexed keywords

AMINO ACID; GLUCOSE; INSULIN;

AGED; ANABOLIC SENSITIVITY; ARTICLE; BLOOD ANALYSIS; BODY COMPOSITION; CONTROLLED STUDY; DIETARY INTAKE; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; EXERCISE TEST; FEMALE; GAS CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MASS SPECTROMETRY; MUSCLE BIOPSY; MUSCLE ISOMETRIC CONTRACTION; MUSCLE MASS; MUSCLE STRENGTH; NORMAL HUMAN; PEDOMETRY; PHYSICAL ACTIVITY; POSTPRANDIAL STATE; RANDOMIZED CONTROLLED TRIAL; RESISTANCE TRAINING; STEP REDUCTION TEST;

EID: 84973281009     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12493     Document Type: Article

References (50)

1. Bode-Böger, S. M., R. H. Böger, A. Galland, D. Tsikas, and J. C. Frölich. 1998. L-arginine-induced vasodilation in healthy humans:pharmacokinetic–pharmacodynamic relationship. Br. J. Clin. Pharmacol. 46:489–497.
2. Bovetto, L, C. Schmitt, F. Robin, and M. Pouzot. 2008. Whey protein micelles. In: https://wwwgooglecom/patents/US8399043. USA: Nestec S.A.
3. Breen, L., K. Stokes, T. Churchward-Venne, D. Moore, S. Baker, K. Smith, et al. 2013. Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly. J. Clin. Endocrinol. Metab. 98:2604–2612.
4. Brooks, N., G. Cloutier, S. Cadena, J. Layne, C. Nelsen, A. Freed, et al. 2008. Resistance training and timed essential amino acids protect against the loss of muscle mass and strength during 28 days of bed rest and energy deficit. J. Appl. Physiol. 105:241–248.
5. Burd, N., D. West, A. Staples, P. Atherton, J. Baker, D. Moore, et al. 2010. Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS ONE 5:e12033.
6. Burd, N. A., D. West, T. Rerecich, T. Prior, S. Baker, and S. Phillips. 2011a. Validation of a single biopsy approach and bolus protein feeding to determine myofibrillar protein synthesis in stable isotope tracer studies in humans. Nutr. Metab. (Lond) 8:15.
7. Burd, N. A., D. W. D. West, D. R. Moore, P. J. Atherton, A. W. Staples, T. Prior, et al. 2011b. Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men. J. Nutr. 141:568–573.
8. Carroll, T. J., R. D. Herbert, J. Munn, M. Lee, and S. C. Gandevia. 2006. Contralateral effects of unilateral strength training: evidence and possible mechanisms. J. Appl. Physiol. 101:1514–1522.
9. Casey, D. P., B. G. Walker, S. M. Ranadive, J. L. Taylor, and M. J. Joyner. 2013. Contribution of nitric oxide in the contraction-induced rapid vasodilation in young and older adults. J. Appl. Physiol. 115:446–455.
10. Chadderdon, S. M., J. T. Belcik, E. Smith, L. Pranger, P. Kievit, K. L. Grove, et al. 2012. Activity restriction, impaired capillary function, and the development of insulin resistance in lean primates. Am. J. Physiol. Endocrinol. Metab. 303: E607–E613.
11. Churchward-Venne, T., L. Cotie, M. MacDonald, C. J. Mitchell, T. Prior, S. Baker, et al. 2014. Citrulline does not enhance blood flow, microvascular circulation, or myofibrillar protein synthesis in elderly men at rest or following exercise. Am. J. Physiol. Endocrinol. Metab. 307: E71–E83.
12. Dai, Z., Z. Wu, Y. Yang, J. Wang, M. C. Satterfield, C. J. Meininger, et al. 2013. Nitric oxide and energy metabolism in mammals. BioFactors 39:383–391.
13. Di Donato, D. M., D. W. D. West, T. A. Churchward-Venne, L. Breen, S. K. Baker, and S. M. Phillips. 2014. Influence of aerobic exercise intensity on myofibrillar and mitochondrial protein synthesis in young men during early and late postexercise recovery. Am. J. Physiol. Endocrinol. Metab. 306:E1025–E1032.
14. Donato, A., L. Gano, I. Eskurza, A. Silver, P. Gates, K. Jablonski, et al. 2009. Vascular endothelial dysfunction with aging: endothelin-I and endothelial nitric oxide synthase. Am. J. Physiol. Heart Circ. Physiol. 297:H425–H432.
15. Farthing, J. P., and E. P. Zehr. 2014. Restoring symmetry: clinical applications of cross-education. Exerc. Sport Sci. Rev. 42:70–75.
16. Farthing, J., J. Krentz, and C. Magnus. 2009. Strength training the free limb attenuated strength loss during unilateral immobilization. J. Appl. Physiol. 106:830–836.
17. Farthing, J., J. Krentz, C. Magnus, T. Barss, J. Lanovaz, J. Cummine, et al. 2011. Changes in functional magnetic resonance imaging cortical activation with cross education to an immobilized limb. Med. Sci. Sports Exerc. 43:1394–1405.
18. Ferrando, A., K. Tipton, M. Bamman, and R. R. Wolfe. 1997. Resistance exercise maintains skeletal muscle protein synthesis during bed rest. J. Appl. Physiol. 82:807–810.
19. Gibson, J., D. Halliday, W. Morrison, P. Stoward, G. Hornsby, P. Watt, et al. 1987. Decrease in human quadriceps muscle protein turnover consequent upon leg immobilisation. Clin. Sci. 72:503–509.
20. Gibson, J. N. A., K. Smith, and M. J. Rennie. 1988. Prevention of disuse muscle atrophy by means of electrical stimulation: maintenance of protein synthesis. Lancet 332:767–770.
21. Glover, E. I., and S. M. Phillips. 2010. Resistance exercise and appropriate nutrition to counteract muscle wasting and promote muscle hypertrophy. Curr. Opin. Clin. Nutr. Metab. Care 13:630–634.
22. Glover, E., S. Phillips, B. Oates, J. Tang, M. Tarnopolsky, A. Selby, et al. 2008. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J. Physiol. 586:6049-6061.
23. Hvid, L., P. Aagaard, L. Justesen, M. L. Bayer, J. L. Andersen, N. Ørtenblad, et al. 2010. Effects of aging on muscle mechanical function and muscle fiber morphology during short-term immobilization and subsequent retraining. J. Appl. Physiol. (1985). 109:1628–1634.
24. Hvid, L. G., C. Suetta, J. H. Nielsen, M. M. Jensen, U. Frandsen, N. Ørtenblad, et al. 2014. Aging impairs the recovery in mechanical muscle function following 4 days of disuse. Exp Gerontol. 52:1–8.
25. Jourdan, M., K. S. Nair, R. E. Carter, J. Schimke, G. C. Ford, J. Marc, et al. 2014. Citrulline stimulates muscle protein synthesis in the post-absorptive state in healthy people fed a low-protein diet -A pilot study. Clin. Nutr. 34:449–456.
26. Kawakami, Y., H. Akima, K. Kubo, Y. Muraoko, H. Hasegawa, M. Kouzaki, et al. 2001. Changes in muscle size, architecture, and neural activation after 20 days of bed rest with and without resistance exercise. Eur. J. Appl. Physiol. 84:7–12.
27. Krogh-Madsen, R., J. P. Thyfault, C. Broholm, O. H. Mortensen, R. H. Olsen, R. Mounier, et al. 2010. A 2-wk reduction of ambulatory activity attenuates peripheral insulin sensitivity. J. Appl. Physiol. 108:1034–1040.
28. Leenders, M., L. Verdijk, L. van der Hoeven, J. van Kranenburg, R. Nilwik, and L. Van Loon. 2013. Elderly men and women benefit equally from prolonged resistance-type exercise training. J. Gerontol. A Biol. Sci. Med. Sci. 68:769-779.
29. Magnus, C., T. Barss, J. Lanovaz, and J. Farthing. 2010. Effects of cross-education on the muscle after a period of unilateral limb immobilization using a should sling and swathe. J. Appl. Physiol. 109:1887–1894.
30. Mitchell, C. J., T. Churchward-Venne, D. W. D. West, N. A. Burd, L. Breen, S. Baker, et al. 2012. Resistance exercise load does not determine training-mediated hypertrophic gains in young men. J. Appl. Physiol. 113:71–77.
31. Mitchell, W., B. Phillips, J. Williams, D. Rankin, K. Smith, J. Lund, et al. 2013. Development of a new Sonovue TM contrast-enhanced ultrasound approach reveals temporal and age-related features of muscle microvascular responses to feeding. Physiol Rep 1:e00119.
32. Moinard, C., I. Nicolis, N. Neveux, S. Darquy, S. Benazeth, and L. Cynober. 2008. Dose-ranging effects of citrulline administration on plasma amino acids and hormonal patterns in healthy subjects: the Citrudose pharmacokinetic study. Br. J. Nutr. 99:855–862.
33. Moore, D., M. Robinson, J. Fry, J. Tang, E. Glover, S. Wilkinson, et al. 2009. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am. J. Clin. Nutr. 89:161–168.
34. Moore, D., T. Churchward-Venne, O. Witard, L. Breen, N. Burd, K. Tipton, et al. 2015. 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. 70:57–62.
35. Oates, B. R., E. I. Glover, D. W. West, J. L. Fry, M. A. Tarnopolsky, and S. M. Phillips. 2010. Low-volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve 42:539–546.
36. Osowska, S., T. Duchemann, S. Walrand, A. Paillard, Y. Boirie, L. Cynober, et al. 2006. Citrulline modulates muscle protein metabolism in old malnourished rats. Am. J. Physiol. Endocrinol. Metab. 291:E582–E586.
37. Phillips, S. 2009. Physiologic and molecular bases of muscle hypertrophy and atrophy: impact of resistance exercise on human skeletal muscle (protein and exercise dose effects). Appl. Physiol. Nutr. Metab. 34:403–410.
38. Phillips, B., J. Williams, P. Atherton, K. Smith, W. Hildebrandt, D. Rankin, et al. 2012. Resistance exercise training improves age-related declines in leg vascular conductance and rejuvenates acute leg blood flow responses to feeding and exercise. J. Appl. Physiol. 112:347–353.
39. Phillips, B., P. Atherton, K. Varadhan, D. Wilkinson, M. Limb, A. Selby, et al. 2014. Pharmacological enhancement of leg and muscle microvascular blood flow does not augment anabolic responses in skeletal muscle of young men under fed conditions. Am. J. Physiol. Endocrinol. Metab. 306: E168–E176.
40. Phillips, B., P. Atherton, K. Varadhan, M. Limb, D. Wilkinson, K. Sjoberg, et al. 2015. The effects of resistance exercise training on macro- and micro-circulatory responses to feeding and skeletal muscle protein anabolism in older men. J. Physiol. doi: 10.1113/JP270343.
41. Schmitt, C., C. Bovay, M. Rouvet, S. Shojaei-Rami, and E. Kolodziejczyk. 2007. Whey protein soluble aggregates from heating with NaCl: physicochemical, interfacial, and foaming properties. Langmuir 23:4155–4166.
42. Shih, R., Z. Wang, M. Heo, W. Wang, and S. Heymsfield. 2000. Lower limb skeletal muscle mass: development of dual-energy x-ray absorptiometry prediction model. J. Appl. Physiol. 89:1380–1386.
43. Suetta, C., J. Andersen, U. Dalgas, J. Berget, S. Koskinen, P. Aagaard, et al. 2008. Resistance training induced qualitative changes in muscle morphology, muscle architecture, and muscle function in elderly postoperative patients. J. Appl. Physiol. 105:180–186.
44. Suetta, C., L. Hvid, L. Justesen, U. Christensen, K. Neergaard, L. Simonsen, et al. 2009. Effects of aging on human skeletal muscle after immobilization and retraining. J. Appl. Physiol. 107:1172–1180.
45. Timmerman, K. L., J. L. Lee, S. Fujita, S. Dhanani, H. C. Dreyer, C. S. Fry, et al. 2010. Pharmacological vasodilation improves insulin-stimulated muscle protein anabolism but not glucose utilization in older adults. Diabetes 59:2764-2771.
46. Timmerman, K. L., S. Dhanani, E. L. Glynn, C. S. Fry, M. J. Drummond, K. Jennings, et al. 2012. A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am. J. Clin. Nutr. 95:1403–1412.
47. Ventura, G., P. Noirez, D. Breuillé, J. P. Godin, S. Pinaud, M. Cleroux, et al. 2013. Effect of citrulline on muscle functions during moderate dietary restriction in healthy adult rats. Amino Acids 45:1123–1131.
48. Wall, B., T. Snijders, J. Senden, C. Ottenbros, A. Gijsen, L. Verdijk, et al. 2013. Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men. J. Clin. Endocrinol. Metab. 98:4872–4881.
49. West, D., N. Burd, T. Churchward-Venne, D. Camera, C. Mitchell, S. Baker, et al. 2012. Sex-based comparisons of myofibrillar protein synthesis after resistance exercise in the fed state. J. Appl. Physiol. 112:1805–1813.
50. Wilkinson, S., M. Tarnopolsky, M. Macdonald, J. Macdonald, D. Armstrong, and S. Phillips. 2007. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am. J. Clin. Nutr. 85:1031–1040. ª 2015