Sex differences in the effect of fish-oil supplementation on the adaptive response to resistance exercise training in older people: a randomized controlled trial

Mariasole Da Boit, Rachael Sibson, Selvaraj Sivasubramaniam, Judith R Meakin, Carolyn A Greig, Richard M Aspden, Frank Thies, Stewart Jeromson, D Lee Hamilton, John R Speakman, Catherine Hambly, Arduino A Mangoni, Thomas Preston, Stuart R Gray, Mariasole Da Boit, Rachael Sibson, Selvaraj Sivasubramaniam, Judith R Meakin, Carolyn A Greig, Richard M Aspden, Frank Thies, Stewart Jeromson, D Lee Hamilton, John R Speakman, Catherine Hambly, Arduino A Mangoni, Thomas Preston, Stuart R Gray

Abstract

Background: Resistance exercise increases muscle mass and function in older adults, but responses are attenuated compared with younger people. Data suggest that long-chain n-3 polyunsaturated fatty acids (PUFAs) may enhance adaptations to resistance exercise in older women. To our knowledge, this possibility has not been investigated in men.

Objective: We sought to determine the effects of long-chain n-3 PUFA supplementation on resistance exercise training-induced increases in muscle mass and function and whether these effects differ between older men and women.

Design: Fifty men and women [men: n = 27, mean ± SD age: 70.6 ± 4.5 y, mean ± SD body mass index (BMI; in kg/m2): 25.6 ± 4.2; women: n = 23, mean ± SD age: 70.7 ± 3.3 y, mean ± SD BMI: 25.3 ± 4.7] were randomly assigned to either long-chain n-3 PUFA (n = 23; 3 g fish oil/d) or placebo (n = 27; 3 g safflower oil/d) and participated in lower-limb resistance exercise training twice weekly for 18 wk. Muscle size, strength, and quality (strength per unit muscle area), functional abilities, and circulating metabolic and inflammatory markers were measured before and after the intervention.

Results: Maximal isometric torque increased after exercise training to a greater (P < 0.05) extent in the long-chain n-3 PUFA group than in the placebo group in women, with no differences (P > 0.05) between groups in men. In both sexes, the effect of exercise training on maximal isokinetic torque at 30, 90, and 240° s-1, 4-m walk time, chair-rise time, muscle anatomic cross-sectional area, and muscle fat did not differ (P > 0.05) between groups. There was a greater (P < 0.05) increase in muscle quality in women after exercise training in the long-chain n-3 PUFA group than in the placebo group, with no such differences in men (P > 0.05). Long-chain n-3 PUFAs resulted in a greater decrease (P < 0.05) than the placebo in plasma triglyceride concentrations in both sexes, with no differences (P > 0.05) in glucose, insulin, or inflammatory markers.

Conclusion: Long-chain n-3 PUFA supplementation augments increases in muscle function and quality in older women but not in older men after resistance exercise training. This trial was registered at clinicaltrials.gov as NCT02843009.

Keywords: aging; exercise; fatty acids; muscle; sarcopenia.

Figures

FIGURE 1
FIGURE 1
Flow diagram illustrating the participant progress through the phases of the study. F, female; LC, long chain.

References

    1. Rosenberg IH. Sarcopenia: origins and clinical relevance. J Nutr 1997;127(5 Suppl):990S–1S.
    1. Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 2012;3:260.
    1. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 2006;61:1059–64.
    1. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, et al. . Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 2009;90:1579–85.
    1. Greig CA, Gray C, Rankin D, Young A, Mann V, Noble B, Atherton PJ. Blunting of adaptive responses to resistance exercise training in women over 75y. Exp Gerontol 2011;46:884–90.
    1. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 1990;263:3029–34.
    1. Leenders M, Verdijk LB, van der Hoeven L, van Kranenburg J, Nilwik R, van Loon LJC. Elderly men and women benefit equally from prolonged resistance-type exercise training. J Gerontol A Biol Sci Med Sci 2013;68:769–79.
    1. Da Boit M, Sibson R, Meakin JR, Aspden RM, Thies F, Mangoni AA, Gray SR. Sex differences in the response to resistance exercise training in older people. Physiol Rep 2016;4:e12834.
    1. Forbes SC, Little JP, Candow DG. Exercise and nutritional interventions for improving aging muscle health. Endocrine 2012;42:29–38.
    1. Gray S, Da Boit M. Marine n-3 polyunsaturated fatty acids: a potential role in the treatment of sarcopenia. Clin Lipidol 2013;8:187–94.
    1. Bergeron K, Julien P, Davis TA, Myre A, Thivierge MC. Long-chain n-3 fatty acids enhance neonatal insulin-regulated protein metabolism in piglets by differentially altering muscle lipid composition. J Lipid Res 2007;48:2396–410.
    1. Gingras AA, White PJ, Chouinard PY, Julien P, Davis TA, Dombrowski L, Couture Y, Dubreuil P, Myre A, Bergeron K, et al. . Long-chain omega-3 fatty acids regulate bovine whole-body protein metabolism by promoting muscle insulin signalling to the Akt-mTOR-S6K1 pathway and insulin sensitivity. J Physiol 2007;579:269–84.
    1. Kamolrat T, Gray SR, Carole TM. Fish oil positively regulates anabolic signalling alongside an increase in whole-body gluconeogenesis in ageing skeletal muscle. Eur J Nutr 2013;52:647–57.
    1. Kamolrat T, Gray SR. The effect of eicosapentaenoic and docosahexaenoic acid on protein synthesis and breakdown in murine C2C12 myotubes. Biochem Biophys Res Commun 2013;432:593–8.
    1. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, Mittendorfer B. Omega 3 polyunsaturated fatty acids augment the muscle protein anabolic response to hyperaminoacidemia-hyperinsulinemia in healthy young and middle aged men and women. Clin Sci 2011;121:267–78.
    1. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, Mittendorfer B. Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am J Clin Nutr 2011;93:402–12.
    1. Smith GI, Julliand S, Reeds DN, Sinacore DR, 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;102:115–22.
    1. Rodacki CLN, Rodacki ALF, Pereira G, Naliwaiko K, Coelho I, Pequito D, Fernandes LC. Fish-oil supplementation enhances the effects of strength training in elderly women. Am J Clin Nutr 2012;95:428–36.
    1. Rawdon T, Sharp R, Shelley M, Thomas J. Meta-analysis of the placebo effect in nutritional supplement studies of muscular performance. Kinesiology Rev 2012;1:137–48.
    1. Robinson SM, Jameson KA, Batelaan SF, Martin HJ, Syddall HE, Dennison EM, Cooper C, Sayer AA. 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.
    1. Greig CA, Young A, Skelton DA, Pippet E, Butler FMM, Mahmud SM. Exercise studies with elderly volunteers. Age Ageing 1994;23:185–9.
    1. Guralnik JM, Ferrucci L, Pieper CF, Leveille SG, Markides KS, Ostir GV, Studenski S, Berkman LF, Wallace RB. Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. J Gerontol A Biol Sci Med Sci 2000;55:M221–31.
    1. Mackay I, Ford I, Thies F, Fielding S, Bachoo P, Brittenden J. Effect of omega-3 fatty acid supplementation on markers of platelet and endothelial function in patients with peripheral arterial disease. Atherosclerosis 2012;221:514–20.
    1. Damas F, Phillips SM, Libardi CA, Vechin FC, Lixandrao ME, Jannig PR, Costa LA, Bacurau AV, Snijders T, Parise G, et al. . Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J Physiol 2016;594:5209–22.
    1. McGlory C, White A, Treins C, Drust B, Close GL, Maclaren DP, Campbell IT, Philp A, Schenk S, Morton JP, et al. . Application of the [γ-32P] ATP kinase assay to study anabolic signaling in human skeletal muscle. J Appl Physiol (1985) 2014;116:504–13.
    1. MacDonald AJ, Small AC, Greig CA, Husi H, Ross JA, Stephens NA, Fearon KCH, Preston T. A novel oral tracer procedure for measurement of habitual myofibrillar protein synthesis. Rapid Commun Mass Spectrom 2013;27:1769–77.
    1. Burd NA, West DW, Rerecich T, Prior T, Baker SK, Phillips SM. 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) 2011;8:15.
    1. Symons TB, Vandervoort AA, Rice CL, Overend TJ, Marsh GD. Effects of maximal isometric and isokinetic resistance training on strength and functional mobility in older adults. J Gerontol A Biol Sci Med Sci 2005;60:777–81.
    1. Calder PC. Omega-3 fatty acids and inflammatory processes. Nutrients 2010;2:355–74.
    1. Ferrucci L, Penninx BW, Volpato S, Harris TB, Bandeen-Roche K, Balfour J, Leveille SG, Fried LP, Md JM. Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels. J Am Geriatr Soc 2002;50:1947–54.
    1. Reinders I, Song X, Visser M, Eiriksdottir G, Gudnason V, Sigurdsson S, Aspelund T, Siggeirsdottir K, Brouwer IA, Harris TB, 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;145:105–12.
    1. Burke RE, Levine DN, Zajac FE 3rd. Mammalian motor units: physiological-histochemical correlation in three types in cat gastrocnemius. Science 1971;174:709–12.
    1. Larsson L, Sjodin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22–65 years. Acta Physiol Scand 1978;103:31–9.
    1. Deschenes MR. Motor unit and neuromuscular junction remodeling with aging. Curr Aging Sci 2011;4:209–20.
    1. Power GA, Dalton BH, Rice CL. Human neuromuscular structure and function in old age: a brief review. J Sport Health Sci 2013;2:215–26.
    1. Campbell MJ, McComas AJ, Petito F. Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry 1973;36:174–82.
    1. Doherty TJ, Vandervoort AA, Taylor AW, Brown WF. Effects of motor unit losses on strength in older men and women. J Appl Physiol 1993;74:868–74.
    1. Lewis EJH, Radonic PW, Wolever TMS, Wells GD. 21 days of mammalian omega-3 fatty acid supplementation improves aspects of neuromuscular function and performance in male athletes compared to olive oil placebo. J Int Soc Sports Nutr 2015;12:28.
    1. Lauritzen L, Hansen HS, Jørgensen MH, Michaelsen KF. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 2001;40:1–94.
    1. Salem N Jr, Litman B, Kim HY, Gawrisch K. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 2001;36:945–59.
    1. Schultz AB, Ashton-Miller JA, Alexander NB. What leads to age and gender differences in balance maintenance and recovery? Muscle Nerve Suppl 1997;5:S60–4.
    1. Lamboley CR, Wyckelsma VL, Dutka TL, McKenna MJ, Murphy RM, Lamb GD. Contractile properties and sarcoplasmic reticulum calcium content in type I and type II skeletal muscle fibres in active aged humans. J Physiol 2015;593:2499–514.
    1. Ponsard B, Durot I, Fournier A, Oudot F, Athias P, Grynberg A. Long-chain polyunsaturated fatty acids influence both β- and α-adrenergic function of rat cardiomyocytes. J Am Oil Chem Soc 1998;75:247–54.
    1. Vargiu R, Littarru GP, Fraschini M, Perinu A, Tiano L, Capra A, Mancinelli R. Enhancement of shortening velocity, power, and acto-myosin crossbridge (CB) kinetics following long-term treatment with propionyl-L-carnitine, coenzyme Q10, and omega-3 fatty acids in BIO TO-2 cardiomyopathic Syrian hamsters papillary muscle. Biofactors 2010;36:229–39.
    1. Supinski GS, Vanags J, Callahan L. Eicosapentaenoic acid preserves diaphragm force generation following endotoxin administration. Crit Care 2010;14:R35.
    1. Caslake MJ, Miles EA, Kofler BM, Lietz G, Curtis P, Armah CK, Kimber AC, Grew JP, Farrell L, Stannard J, et al. . Effect of sex and genotype on cardiovascular biomarker response to fish oils: the FINGEN Study. Am J Clin Nutr 2008;88:618–29.
    1. Pirillo A, Catapano AL. Omega-3 polyunsaturated fatty acids in the treatment of hypertriglyceridaemia. Int J Cardiol 2013;170(2 Suppl 1):S16–20.
    1. Akinkuolie AO, Ngwa JS, Meigs JB, Djoussé L. Omega-3 polyunsaturated fatty acid and insulin sensitivity: a meta-analysis of randomized controlled trials. Clin Nutr 2011;30:702–7.
    1. Evans WJ. Exercise strategies should be designed to increase muscle power. J Gerontol A Biol Sci Med Sci 2000;55:M309–10.
    1. Degens H, McPhee JS. Muscle wasting, dysfunction, and inflammaging. In: Bagchi IR, editor. Inflammation, advancing age and nutrition. San Diego (CA): Academic Press; 2014: p. 247–54.

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa