Exercise and Dietary-Protein as a Countermeasure to Skeletal Muscle Weakness: Liverpool Hope University - Sarcopenia Aging Trial (LHU-SAT)

Ben Kirk, Kate Mooney, Farzad Amirabdollahian, Omid Khaiyat, Ben Kirk, Kate Mooney, Farzad Amirabdollahian, Omid Khaiyat

Abstract

Objective: To investigate the effects of a 16-week concurrent exercise regimen [resistance exercise (RE) + functional exercise (FE)] in combination with, or without, a leucine-enriched whey protein isolate supplement on muscle strength, physical functioning, aerobic capacity, and cardiometabolic health in older adults (≥60 years). Physical activity levels were also evaluated 6 months post-cessation of the intervention.

Methods: Forty-six, community-dwelling, previously untrained males, and females [age: 68 ± 5 years (mean ± SD); BMI: 27.8 ± 6.2 kg/m2] who completed the trial were initially randomized to one of two independent arms [Exercise n = 24 (E); Exercise+Protein n = 22 (EP)]. Both arms completed 16 weeks of RE (performed to fatigue) (2 times/week) with FE (1 time/week) on non-consecutive days. Additionally, EP were administered a leucine-enriched whey protein supplement (3 times/day) for 16 weeks based on individual body-weight (1.5 g/kg/day).

Results: As a result of dietary supplementation, protein intake increased in EP (∼1.2 ± 0.4 to 1.5 ± 0.7 g/kg/day) during the intervention. Maximal strength (1RM) values for leg press (E: +39 ± 7 kg, p = 0.006; EP: +63 ± 7 kg, p < 0.001), chest press (E: +22 ± 4 kg, p < 0.001; EP: +21 ± 6 kg, p < 0.001), and bicep curl (E: +7 ± 0 kg, p = 0.002; EP: +6 ± 1 kg, p = 0.008) significantly increased in E and EP respectively, with no differences between arms (p > 0.05). Physical functioning in the obstacle course (E: -5.1 ± 6.8 s, p < 0.001; EP: -2.8 ± 0.8 s, p < 0.001) and short-physical performance battery scores (E: +0.5 ± 0.5, p = <0.001; EP: +0.4 ± 0.5, p = 0.038), and aerobic capacity in the 6-min walk test (E: +37 ± 24 m, p = 0.014; EP: +36 ± 3 m, p = 0.005) improved in E and EP respectively, with no differences between arms (p > 0.05). No significant change was observed for markers of cardiometabolic health (glycaemic control or blood pressure) (p > 0.05). At follow-up, 86% of older adults reported to performing physical activity ≥1 per week. Of those, 61% were still participating in strength- and cardiovascular- based exercise.

Conclusion: Concurrent exercise (RE + FE) offers a potent method to combat age-related muscle weakness, and our results suggest a high proportion of older adults may continue to exercise unsupervised. However, leucine-enriched whey protein isolate supplementation did not confer any additional benefit in those already consuming ample amounts of dietary protein at trial enrolment. Future trials should utilize a whole-foods approach and investigate the effects in frail and non-frail older adults habitually consuming the RDA of protein, to assess if a higher intake of protein is needed to delay the onset of muscle weakness.

Trial registration: Clinicaltrials.gov Identifier: NCT02912130.

Keywords: aging; dietary-protein; exercise; leucine; muscle weakness.

Figures

FIGURE 1
FIGURE 1
Flow chart of experimental trial.
FIGURE 2
FIGURE 2
Mini obstacle course (25 m).
FIGURE 3
FIGURE 3
Functional exercise circuit.
FIGURE 4
FIGURE 4
1RM values for (A) leg press, (B) chest press, and (C) bicep curl in response to independent treatments (E, black; EP, red). Individual data points are shown with horizontal line indicating the mean and error bars representing the standard deviation. Within-arm time effects were evident post-intervention for leg press, chest press, and bicep curl all (∗p < 0.05). No between-arm effects observed (p > 0.05).
FIGURE 5
FIGURE 5
Physical activity levels 6 months post-trial. Values are presented as pooled responses (%) from survey questions. (A) How many times have you exercised in the past 4-weeks? (B) If you exercised in the past 4-weeks what type of exercise was it? (C) If you exercised in the past 4-weeks how long did each session last?

References

    1. Arnarson A., Gudny Geirsdottir O., Ramel A., Briem K., Jonsson P. V., Thorsdottir I. (2013). Effects of whey proteins and carbohydrates on the efficacy of resistance training in elderly people: double blind, randomised controlled trial. Eur. J. Clin. Nutr. 67 821–826. 10.1038/ejcn.2013.40
    1. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories Crapo R. O., Casaburi R., Coates A. L., Enright P. L., MacIntyre N. al. (2002). ATS statement: guidelines for the six-minute walk test. Am. J. Respir. Crit. Care Med. 166 111–117. 10.1164/rccm.166/1/111
    1. Baechle T. R., Earle R. W. (2008). Essentials of Strength Training and Conditioning. Champaign, IL: Human Kinetics Publishers. 10.1164/ajrccm.166.1.at1102
    1. Bauer J., Biolo G., Cederholm T., Cesari M., Cruz-Jentoft A. J., Morley J. E., et al. (2013). 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. 14 542–559. 10.1016/J.JAMDA.2013.05.021
    1. Bell K. E., Snijders T., Zulyniak M., Kumbhare D., Parise G., Chabowski A., et al. (2017). A whey protein-based multi-ingredient nutritional supplement stimulates gains in lean body mass and strength in healthy older men: a randomized controlled trial. PLoS One 12:e0181387. 10.1371/journal.pone.0181387
    1. Borg E., Kaijser L. (2006). A comparison between three rating scales for perceived exertion and two different work tests. Scand. J. Med. Sci. Sport 16 57–69. 10.1111/j.1600-0838.2005.00448.x
    1. Brzycki M. (1993). Strength testing—predicting a one-rep max from reps-to-fatigue. J. Phys. Educ. Recreat. Danc. 64 88–90. 10.1080/07303084.1993.10606684
    1. Cawood A. L., Elia M., Stratton R. J. (2012). Systematic review and meta-analysis of the effects of high protein oral nutritional supplements. Ageing Res. Rev. 11 278–296. 10.1016/J.ARR.2011.12.008
    1. Cermak N. M., Res P. T., Groot L. C., De Saris W. H. M., Van Loon L. J. C. (2012). Protein supplementation augments the adaptive response of skeletal muscle to resistance type exercise training a meta analysis.pdf. Am. J. Clin. Nutr. 96 1454–1464. 10.3945/ajcn.112.037556.INTRODUCTION
    1. Charette S. L., McEvoy L., Pyka G., Snow-Harter C., Guido D., Wiswell R. A., et al. (1991). Muscle hypertrophy response to resistance training in older women. J. Appl. Physiol. 70 1912–1916. 10.1152/jappl.1991.70.5.1912
    1. Cimas M., Ayala A., Sanz B., Agulló-Tomás M. S., Escobar A., Forjaz M. J. (2018). Chronic musculoskeletal pain in European older adults: cross-national and gender differences. Eur. J. Pain 22 333–345. 10.1002/ejp.1123
    1. da Silva L. X. N., Teodoro J. L., Menger E., Lopez P., Grazioli R., Farinha J., et al. (2018). Repetitions to failure versus not to failure during concurrent training in healthy elderly men: a randomized clinical trial. Exp. Gerontol. 108 18–27. 10.1016/j.exger.2018.03.017
    1. Dalbo V. J., Czerepusko J. B., Tucker P. S., Kingsley M. I., Moon J. R., Young K., et al. (2015). Not sending the message: a low prevalence of strength-based exercise participation in rural and regional central queensland. Aust. J. Rural Health 23 295–301. 10.1111/ajr.12207
    1. Davis A. G., Fox K. R., Hillsdon M., Sharp D. J., Coulson J. C., Thompson J. L. (2011). Objectively measured physical activity in a diverse sample of older urban UK adults. Med. Sci. Sport Exerc 43 647–654. 10.1249/MSS.0b013e3181f36196
    1. Devries M. C., McGlory C., Bolster D. R., Kamil A., Rahn M., Harkness L., et al. (2018). Leucine, not total protein, content of a supplement is the primary determinant of muscle protein anabolic responses in healthy older women. J. Nutr. 148 1088–1095. 10.1093/jn/nxy091
    1. Faul F., Erdfelder E., Lang A.-G., Buchner A. (2007). G∗Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39 175–191. 10.3758/BF03193146
    1. Fiatarone M. A., Marks E. C., Ryan N. D., Meredith C. N., Lipsitz L. A., Evans W. J. (1990). High-intensity strength training in nonagenarians. JAMA 263:3029 10.1001/jama.1990.03440220053029
    1. Finger D., Goltz F. R., Umpierre D., Meyer E., Rosa L. H. T., Schneider C. D. (2015). Effects of protein supplementation in older adults undergoing resistance training: a systematic review and meta-analysis. Sport Med. 45 245–255. 10.1007/s40279-014-0269-4
    1. Forkan R., Pumper B., Smyth N., Wirkkala H., Ciol M. A., Shumway-Cook A. (2006). Exercise adherence following physical therapy intervention in older adults with impaired balance. Phys. Ther. 86 401–410. 10.1093/ptj/86.3.401
    1. Fried L. P., Tangen C. M., Walston J., Newman A. B., Hirsch C., Gottdiener J., et al. (2001). Frailty in older adults: evidence for a phenotype. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 56 M146–M157. 10.1093/gerona/56.3.M146
    1. Gade J., Pedersen R. J., Beck A. M. (2018). Effect of protein or essential amino acid supplementation during prolonged resistance exercise training in older adults on body composition, muscle strength, and physical performance parameters: a systematic review. Rehabil. Process Outcome 7:117957271876576 10.1177/1179572718765760
    1. García-Hermoso A., Cavero-Redondo I., Ramírez-Vélez R., Ruiz J. R., Ortega F. B., Lee D.-C., et al. (2018). Muscular strength as a predictor of all-cause mortality in an apparently healthy population: a systematic review and meta-analysis of data from approximately 2 million men and women. Arch. Phys. Med. Rehabil. 99 2100.e5–2113.e5. 10.1016/J.APMR.2018.01.008
    1. Goodpaster B. H., Park S. W., Harris T. B., Kritchevsky S. B., Nevitt M., Schwartz A. V., et al. (2006). The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 61 1059–1064. 10.1093/gerona/61.10.1059
    1. Guralnik J. M., Simonsick E. M., Ferrucci L., Glynn R. J., Berkman L. F., Blazer D. G., et al. (1994). A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J. Gerontol. 49 M85–M94. 10.1093/geronj/49.2.M85
    1. Haub M. D., Wells A. M., Tarnopolsky M. A., Campbell W. W. (2002). Effect of protein source on resistive-training-induced changes in body composition and muscle size in older men. Am. J. Clin. Nutr. 76 511–517. 10.1093/ajcn/76.3.511
    1. Hawley J. A. (2008). Specificity of training adaptation: time for a rethink? J. Physiol. 586 1–2. 10.1113/jphysiol.2007.147397
    1. Holwerda A. M., Overkamp M., Paulussen K. J. M., Smeets J. S. J., van Kranenburg J., Backx E. M. P., et al. (2018). Protein supplementation after exercise and before sleep does not further augment muscle mass and strength gains during resistance exercise training in active older men. J. Nutr. 148 1723–1732. 10.1093/jn/nxy169
    1. Jacob M. E., Travison T. G., Ward R. E., Latham N. K., Leveille S. G., Jette A. M., et al. (2018). Neuromuscular attributes associated with lower extremity mobility among community-dwelling older adults. J. Gerontol. Ser. A 74 544–549. 10.1093/gerona/gly102
    1. Kawada S., Okamoto Y., Ogasahara K., Yanagisawa S., Ohtani M., Kobayashi K. (2013). Resistance exercise combined with essential amino acid supplementation improved walking ability in elderly people. Acta Physiol. Hung. 100 329–339. 10.1556/APhysiol.100.2013.008
    1. Kukuljan S., Nowson C. A., Sanders K., Daly R. M. (2009). Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J. Appl. Physiol. 107 1864–1873. 10.1152/japplphysiol.00392.2009
    1. Latham N. K., Bennett D. A., Stretton C. M., Anderson C. S. (2004). Systematic review of progressive resistance strength training in older adults. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 59 M48–M61. 10.1093/gerona/59.1.M48
    1. Leenders M., Verdijk L. B., Van Der Hoeven L., Van Kranenburg J., Nilwik R., Wodzig W. K. W. H., et al. (2013). Protein supplementation during resistance-type exercise training in the elderly. Med. Sci. Sports Exerc. 45 542–552. 10.1249/MSS.0b013e318272fcdb
    1. Loustalot F., Carlson S. A., Kruger J., Buchner D. M., Fulton J. E. (2013). Muscle-strengthening activities and participation among adults in the United States. Res. Q. Exerc. Sport 84 30–38. 10.1080/02701367.2013.762289
    1. McLean R. R., Mangano K. M., Hannan M. T., Kiel D. P., Sahni S. (2016). Dietary protein intake is protective against loss of grip strength among older adults in the framingham offspring cohort. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 71 356–361. 10.1093/gerona/glv184
    1. Moore D. R., Churchward-Venne T. A., Witard O., Breen L., Burd N. A., Tipton K. D., et al. (2015). Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 70 57–62. 10.1093/gerona/glu103
    1. Morton R. W., Murphy K. T., McKellar S. R., Schoenfeld B. J., Henselmans M., Helms E., et al. (2017). A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br. J. Sports Med. 52 376–384. 10.1136/bjsports-2017-097608
    1. Morton R. W., Oikawa S. Y., Wavell C. G., Mazara N., McGlory C., Quadrilatero J., et al. (2016). Neither load nor systemic hormones determine resistance training-mediated hypertrophy or strength gains in resistance-trained young men. J. Appl. Physiol. 121 129–138. 10.1152/japplphysiol.00154.2016
    1. Mustafa J., Ellison R. C., Singer M. R., Bradlee M. L., Kalesan B., Holick M. F., et al. (2018). Dietary protein and preservation of physical functioning among middle-aged and older adults in the framingham offspring study. Am. J. Epidemiol. 187 1411–1419. 10.1093/aje/kwy014
    1. Nelson M., Rejeski W., Blair S., Duncan P., Judge J., King A., et al. (2007). Physical activity and public health in older adults: recommendation from the american college of sports medicine and the american heart association. Circulation 116 1094–1105. 10.1161/circulationaha.107.185650
    1. Niccoli T., Partridge L. (2012). Ageing as a risk factor for disease. Curr. Biol. 22 R741–R752. 10.1016/j.cub.2012.07.024
    1. Nilwik R., Snijders T., Leenders M., Groen B. B. L., van Kranenburg J., Verdijk L. B., et al. (2013). The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp. Gerontol. 48 492–498. 10.1016/J.EXGER.2013.02.012
    1. Norton C., Toomey C., McCormack W. G., Francis P., Saunders J., Kerin E., et al. (2016). Protein supplementation at breakfast and lunch for 24 weeks beyond habitual intakes increases whole-body lean tissue mass in healthy older adults. J. Nutr. 146 65–69. 10.3945/jn.115.219022
    1. Oesen S., Halper B., Hofmann M., Jandrasits W., Franzke B., Strasser E.-M. M., et al. (2015). Effects of elastic band resistance training and nutritional supplementation on physical performance of institutionalised elderly - A randomized controlled trial. Exp. Gerontol. 72 99–108. 10.1016/j.exger.2015.08.013
    1. Paddon-Jones D., Rasmussen B. B. (2009). Dietary protein recommendations and the prevention of sarcopenia. Curr. Opin. Clin. Nutr. Metab. Care 12 86–90. 10.1097/MCO.0b013e32831cef8b
    1. Pavasini R., Guralnik J., Brown J. C., di Bari M., Cesari M., Landi F., et al. (2016). Short physical performance Battery and all-cause mortality: systematic review and meta-analysis. BMC Med. 14:215. 10.1186/s12916-016-0763-7
    1. Pendergast D. R., Fisher N. M., Calkins E. (1993). Cardiovascular, neuromuscular, and metabolic alterations with age leading to frailty. J. Gerontol. 48 61–67. 10.1093/geronj/48.special_issue.61
    1. Pinedo-Villanueva R., Westbury L. D., Syddall H. E., Sanchez-Santos M. T., Dennison E. M., Robinson S. M., et al. (2018). Health care costs associated with muscle weakness: a UK population-based estimate. Calcif. Tissue Int. 104 137–144. 10.1007/s00223-018-0478-1
    1. Pollock R. D., Duggal N. A., Lazarus N. R., Lord J. M., Harridge S. D. R. (2018). Cardiorespiratory fitness not sedentary time or physical activity is associated with cardiometabolic risk in active older adults. Scand. J. Med. Sci. Sports 28 1653–1660. 10.1111/sms.13071
    1. Rantanen T., Avlund K., Suominen H., Schroll M., Frändin K., Pertti E. (2002). Muscle strength as a predictor of onset of ADL dependence in people aged 75 years. Aging Clin. Exp. Res. 14 10–15.
    1. Reilly T., Morris T., Whyte G. (2009). The specificity of training prescription and physiological assessment: a review. J. Sports Sci. 27 575–589. 10.1080/02640410902729741
    1. Rosendahl E., Gustafson Y., Nordin E., Lundin-Olsson L., Nyberg L. (2008). A randomized controlled trial of fall prevention by a high-intensity functional exercise program for older people living in residential care facilities. Aging Clin. Exp. Res. 20 67–75. 10.1007/BF03324750
    1. Sherrington C., Fairhall N. J., Wallbank G. K., Tiedemann A., Michaleff Z. A., Howard K., et al. (2019). Exercise for preventing falls in older people living in the community. Coch. Database Syst. Rev. 1:CD012424. 10.1002/14651858.CD012424.pub2
    1. Silva R. G., da Silva D. R. P., da Pina F. L. C., Nascimento M. A., do Ribeiro A. S., Cyrino E. S., et al. (2017). Effect of two different weekly resistance training frequencies on muscle strength and blood pressure in normotensive older women. Rev. Bras. Cineantropometria Desempenho Hum. 19 118–127. 10.5007/1980-0037.2017v19n1p118
    1. Stec M. J., Thalacker-Mercer A., Mayhew D. L., Kelly N. A., Tuggle C. S., Merritt E. K., et al. (2017). Randomized, four-arm, dose-response clinical trial to optimize resistance exercise training for older adults with age-related muscle atrophy. Exp. Gerontol. 99 98–109. 10.1016/j.exger.2017.09.018
    1. Steele J., Raubold K., Kemmler W., Fisher J., Gentil P., Giessing J. (2017). The effects of 6 months of progressive high effort resistance training methods upon strength, body composition, function, and wellbeing of elderly adults. Biomed. Res. Int. 2017:2541090. 10.1155/2017/2541090
    1. Stragier S., Baudry S., Poortmans J., Duchateau J., Carpentier A. (2016). Leucine-enriched protein supplementation does not influence neuromuscular adaptations in response to a 6-month strength training programme in older adults. Exp. Gerontol. 82 58–66. 10.1016/j.exger.2016.06.002
    1. Sun F., Norman I. J., While A. E. (2013). Physical activity in older people: a systematic review. BMC Publ. Health 13:449. 10.1186/1471-2458-13-449
    1. Thompson P. D., Arena R., Riebe D., Pescatello L. S. (2013). ACSM’s new preparticipation health screening recommendations from ACSM’s guidelines for exercise testing and prescription, ninth edition. Curr. Sports Med. Rep. 12 215–217. 10.1249/JSR.0b013e31829a68cf
    1. Tieland M., van der Zwaluw N., Verdijk L. B., van de Rest O., de Groot L. C. P. G. M., van Loon L. J. C. (2012). 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. 13 713–719. 10.1016/j.jamda.2012.05.020
    1. Tieland M., Verdijk L. B., de Groot L. C. P. G. M., van Loon L. J. C. (2015). Handgrip strength does not represent an appropriate measure to evaluate changes in muscle strength during an exercise intervention program in frail older people. Int. J. Sport Nutr. Exerc. Metab. 25 27–36. 10.1123/ijsnem.2013-0123
    1. Van Holle V., Van Cauwenberg J., Van Dyck D., Deforche B., Van de Weghe N., De Bourdeaudhuij I. (2014). Relationship between neighborhood walkability and older adults’ physical activity: results from the Belgian environmental physical activity study in seniors (BEPAS Seniors). Int. J. Behav. Nutr. Phys. Act. 11:110. 10.1186/s12966-014-0110-3
    1. Vellas B., Fielding R. A., Bens C., Bernabei R., Cawthon P. M., Cederholm T., et al. (2018). Implications of ICD-10 for sarcopenia clinical practice and clinical trials: report by the international conference on frailty and sarcopenia research task force. J. Frail. Aging 7 2–9. 10.14283/jfa.2017.30
    1. Verdijk L., Jonkers R. A., Gleeson B. G., Beelen M., Meijer K., Savelberg H. H., et al. (2009). Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am. J. Clin. Nutr. 89 608–616. 10.3945/ajcn.2008.26626
    1. Whitehurst M. A., Johnson B. L., Parker C. M., Brown L. E., Ford A. M. (2005). The benefits of a functional exercise circuit for older adults. J. Strength Cond. Res. 19 647–651.
    1. Wood T. M., Maddalozzo G. F., Harter R. A. (2002). Accuracy of seven equations for predicting 1-RM performance of apparently healthy, sedentary older adults. Meas. Phys. Educ. Exerc. Sci. 6 67–94. 10.1207/S15327841MPEE0602_1
    1. Wright C., Zhou J., Sayer R., Kim J., Campbell W., Wright C. S., et al. (2018). Effects of a high-protein diet including whole eggs on muscle composition and indices of cardiometabolic health and systemic inflammation in older adults with overweight or obesity: a randomized controlled trial. Nutrients 10:946. 10.3390/nu10070946

Source: PubMed

3
Abonnieren