Higher bone remodeling biomarkers are related to a higher muscle function in older adults : Effects of acute exercise

Journal article


Smith, Cassandra, Hiam, Danielle, Tacey, Alexander, Lin, Xuzhu, Woessner, Mary, Zarekookandeh, Navabeh, Garnham, Andrew Peter, Chubb, Paul, Lewis, Joshua, Sim, Marc, Herrmann, Markus, Duque, Gustavo and Levinger, Itamar. (2022). Higher bone remodeling biomarkers are related to a higher muscle function in older adults : Effects of acute exercise. Bone. 165, pp. 1-10. https://doi.org/10.1016/j.bone.2022.116545
AuthorsSmith, Cassandra, Hiam, Danielle, Tacey, Alexander, Lin, Xuzhu, Woessner, Mary, Zarekookandeh, Navabeh, Garnham, Andrew Peter, Chubb, Paul, Lewis, Joshua, Sim, Marc, Herrmann, Markus, Duque, Gustavo and Levinger, Itamar
Abstract

Bone and muscle are closely linked mechanically and biochemically. Bone hormones secreted during bone remodeling might be linked to muscle mass and strength maintenance. Exercise elicits high mechanical strain and is essential for bone health. However, the relationship between commonly used bone turnover markers (BTMs) and muscle function in community dwelling older adults remains unclear. It is also unknown how acute exercise with differing mechanical strain may affect BTMs, and whether baseline muscle function alters BTM responses differently. We tested the hypothesis that BTMs are associated with muscle function, and that acute exercise could change the circulating levels of BTMs. Thirty-five older adults (25 females/10 males, 72.8 ± 6.0 years) participated. Baseline assessments included body composition (DXA), handgrip strength and a physical performance test (PPT) (gait speed, timed-up-and-go [TUG], stair ascent/descent). Leg muscle quality (LMQ) and stair climb power (SCP) were calculated. Participants performed (randomized) 30 min aerobic (AE) (cycling 70%HRPeak) and resistance (RE) (leg press 70%RM, jumping) exercise. Serum β-isomerized C-terminal telopeptides (β-CTX), procollagen of type I propeptide (P1NP), total osteocalcin (t)OC and ucOC were assessed at baseline and post-exercise. Data were analyzed using linear mixed models and simple regressions, adjusted for sex. At baseline, higher muscle strength (LMQ, handgrip) was related to higher P1NP, higher SCP was related to higher P1NP and β-CTX, and better physical performance (lower PPT) related to higher P1NP and β-CTX (p < 0.05). Exercise, regardless of mode, decreased β-CTX and tOC (all p < 0.05), while P1NP and ucOC remained unaltered. Higher baseline handgrip strength, SCP and LMQ was associated with lower post-exercise β-CTX responses, and poorer baseline mobility (increased TUG time) was associated with higher post-exercise β-CTX. Independently of exercise mode, acute exercise decreased β-CTX and tOC. Our data suggest that in older adults at baseline, increased BTM levels were linked to better muscle function. Altogether, our data strengthens the evidence for bone-muscle interaction, however, mechanisms behind this specific component of bone-muscle crostalk remain unclear.

KeywordsAging; Biochemical markers of bone turnover; Bone-muscle interactions; Exercise; Skeletal muscle
Year01 Jan 2022
JournalBone
Journal citation165, pp. 1-10
PublisherElsevier Inc.
ISSN8756-3282
Digital Object Identifier (DOI)https://doi.org/10.1016/j.bone.2022.116545
PubMed ID36108920
Web address (URL)https://www.sciencedirect.com/science/article/pii/S8756328222002228
Open accessPublished as non-open access
Research or scholarlyResearch
Page rangeSkeletal muscle
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Controlled
Output statusPublished
Publication dates
Online13 Sep 2022
Publication process dates
Accepted10 Sep 2022
Deposited13 Jan 2023
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Copyright © 2022 Elsevier Inc. All rights reserved.

Place of publicationUnited States
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The effects of knee injury on skeletal muscle function, Na+-ATPase content, and isoform abundance
Perry, Ben D., Levinger, P, Morris, Hayden G., Petersen, Aaron C., Garnham, Andrew, Levinger, Itamar and McKenna, Michael J.. (2015). The effects of knee injury on skeletal muscle function, Na+-ATPase content, and isoform abundance. Physiological Reports. 3(2), pp. 1 - 14. https://doi.org/10.14814/phy2.12294
The effects of beta-alanine supplementation on physical working capacity at heart rate threshold
Smith-Ryan, Abbie E., Woessner, Mary N., Melvin, Malia N., Wingfield, Hailee L. and Hackney, Anthony C.. (2014). The effects of beta-alanine supplementation on physical working capacity at heart rate threshold. Clinical Physiology and Functional Imaging. 34(5), pp. 397-404. https://doi.org/10.1111/cpf.12111
Reproducibility and validity of a-mode ultrasound for body composition measurement and classification in overweight and obese men and women
Smith-Ryan, Abbie E., Fultz, Sarah N., Melvin, Malia N., Wingfield, Hailee L. and Woessner, Mary N.. (2014). Reproducibility and validity of a-mode ultrasound for body composition measurement and classification in overweight and obese men and women. PLoS ONE. 9(3), pp. 1-8. https://doi.org/10.1371/journal.pone.0091750
Body composition assessment in overweight women : Validation of air displacement plethysmography
Wingfield, Hailee L., Smith-Ryan, Abbie E., Woessner, Mary N., Melvin, Malia N., Fultz, Sarah N. and Graff, Rachel M.. (2014). Body composition assessment in overweight women : Validation of air displacement plethysmography. Clinical Physiology and Functional Imaging. 34(1), pp. 72-76. https://doi.org/10.1111/cpf.12067
Identification of MicroRNAs linked to regulators of muscle protein synthesis and regeneration in young and old skeletal muscle
Zacharewicz, Evelyn, Della Gatta, P. A., Reynolds, John, Garnham, Andrew, Crowley, Tamsyn, Russell, Andrew and Lamon, Séverine. (2014). Identification of MicroRNAs linked to regulators of muscle protein synthesis and regeneration in young and old skeletal muscle. PLoS ONE. 9(12), pp. 1 - 25. https://doi.org/10.1371/journal.pone.0114009
Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise
Stefanetti, Renae J., Zacharewicz, Evelyn, Della Gatta, Paul A., Garnham, Andrew, Russell, Aaron P. and Lamon, Séverine. (2014). Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Frontiers in Physiology. 5, pp. 1 - 10. https://doi.org/10.3389/fphys.2014.00030
Effect of exercise training on skeletal muscle cytokine expression in the elderly
Della Gatta, Paul A., Garnham, Andrew P., Peake, Jonathan M. and Cameron-Smith, David. (2014). Effect of exercise training on skeletal muscle cytokine expression in the elderly. Brain, Behavior, and Immunity. 39, pp. 80 - 86. https://doi.org/10.1016/j.bbi.2014.01.006
Effect of exercise on the skeletal muscle proteome in patients with type 2 diabetes
Hussey, Sophie E., Sharoff, Carrie G., Garnham, Andrew, Yi, Zhengping, Bowen, Benjamin P., Mandarino, Lawrence J. and Hargreaves, Mark. (2013). Effect of exercise on the skeletal muscle proteome in patients with type 2 diabetes. Medicine and Science in Sports and Exercise. 45(6), pp. 1069 - 1076. https://doi.org/10.1249/MSS.0b013e3182814917
Preexercise aminoacidemia and muscle protein synthesis after resistance exercise
Burke, Louise, Hawley, John, Ross, M, Moore, Daniel, Phillips, S, Slater, G, Stellingwerff, T, Tipton, K, Garnham, A and Coffey, Vernon. (2012). Preexercise aminoacidemia and muscle protein synthesis after resistance exercise. Medicine and Science in Sports and Exercise. 44(10), pp. 1968 - 1977. https://doi.org/10.1249/MSS.0b013e31825d28fa
Early inflammatory and myogenic responses to resistance exercise in the elderly
Mathers, Jessica L., Farnfield, Michelle M., Garnham, Andrew P., Caldow, Marissa K., Cameron-Smith, David and Peake, Jonathan M.. (2012). Early inflammatory and myogenic responses to resistance exercise in the elderly. Muscle & Nerve. 46(3), pp. 407 - 412. https://doi.org/10.1002/mus.23317
Evaluation of the MAIIA dipstick test to detect recombinant human erythropoietin in plasma
Ashenden, Michael, Sharpe, Ken, Garnham, Andrew and Gore, Christopher J.. (2012). Evaluation of the MAIIA dipstick test to detect recombinant human erythropoietin in plasma. Journal of Pharmaceutical and Biomedical Analysis. 67-68, pp. 123 - 128. https://doi.org/10.1016/j.jpba.2012.04.025
Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion
Farnfield, Michelle M., Breen, Leigh, Carey, Kate A., Garnham, Andrew and Cameron-Smith, David. (2012). Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion. Applied Physiology, Nutrition and Metabolism. 37(1), pp. 21 - 30. https://doi.org/10.1139/H11-132
Low muscle glycogen concentration does not suppress the anabolic response to resistance exercise
Camera, Donny, West, D, Burd, N, Phillips, S, Garnham, A, Hawley, John and Coffey, Vernon. (2012). Low muscle glycogen concentration does not suppress the anabolic response to resistance exercise. Journal of Applied Physiology. 113(2), pp. 206 - 214. https://doi.org/10.1152/japplphysiol.00395.2012
Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints
Coffey, Vernon, Moore, Daniel, Burd, N, Rerecich, T, Stellingwerff, T, Garnham, A, Phillips, S and Hawley, John. (2011). Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints. European Journal of Applied Physiology. 111(7), pp. 1473 - 1483. https://doi.org/10.1007/s00421-010-1768-0
Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men
Trenerry, Marissa K., Della Gatta, Paul A., Larsen, Amy E., Garnham, Andrew P. and Cameron-Smith, David. (2011). Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men. Muscle & Nerve. 43(3), pp. 385 - 392. https://doi.org/10.1002/mus.21875
Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men
Trenerry, Melissa K., Della Gatta, Paul A., Larson, Amy E. and Garnham, Andrew P.. (2011). Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men. Muscle & Nerve. 43(3), pp. 385 - 392. https://doi.org/10.1002/mus.21875
Vitamin D status and musculoskeletal health in adolescent male ballet dancers a pilot study
Ducher, Gaele, Kukuljan, Sonja, Hill, B., Garnham, Andrew P., Nowson, Carol A., Kimlin, M. G. and Cook, Jill. (2011). Vitamin D status and musculoskeletal health in adolescent male ballet dancers a pilot study. Journal of Dance Medicine and Science. 15(3), pp. 99 - 107.
Current markers of the Athlete Blood Passport do not flag microdose EPO doping
Ashenden, Michael, Gough, Clare E., Garnham, Andrew, Gore, Christopher J. and Sharpe, Ken. (2011). Current markers of the Athlete Blood Passport do not flag microdose EPO doping. European Journal of Applied Physiology. 111(9), pp. 2307 - 2314. https://doi.org/10.1007/s00421-011-1867-6
Exercise training increases adipose tissue GLUT4 expression in patients with type 2 diabetes
Hussey, Sophie E., McGee, S. L., Garnham, Andrew, Wentworth, John M., Jeukendrup, A. E. and Hargreaves, M.. (2011). Exercise training increases adipose tissue GLUT4 expression in patients with type 2 diabetes. Diabetes, Obesity and Metabolism. 13(10), pp. 959 - 962. https://doi.org/10.1111/j.1463-1326.2011.01426.x
Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen : Experimental Physiology-Research Paper
Yeo, W, McGee, S, Carey, A, Paton, C, Garnham, A, Hargreaves, M and Hawley, John. (2010). Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen : Experimental Physiology-Research Paper. Experimental Physiology. 95(2), pp. 351 - 358. https://doi.org/10.1113/expphysiol.2009.049353
Cytokine responses to carbohydrate ingestion during recovery from exercise-induced muscle injury
Ross, M, Halson, Shona, Suzuki, K, Garnham, A, Hawley, John, Cameron-Smith, David and Peake, J. (2010). Cytokine responses to carbohydrate ingestion during recovery from exercise-induced muscle injury. Journal of Interferon and Cytokine Research. 30(5), pp. 329 - 337. https://doi.org/10.1089/jir.2009.0079
Effect of consecutive repeated sprint and resistance exercise bouts on acute adaptive responses in human skeletal muscle
Coffey, Vernon Glenn, Jemiolo, Bozena, Edge, Johann, Garnham, Andrew P., Trappe, Scott W. and Hawley, John Alan. (2009). Effect of consecutive repeated sprint and resistance exercise bouts on acute adaptive responses in human skeletal muscle. American Journal of Physiology - Regulatory Integrative and Comparative Physiology. 297(5), pp. 1441 - 1451. https://doi.org/10.1152/ajpregu.00351.2009
Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle
Coffey, Vernon Glenn, Pilegaard, Henriette, Garnham, Andrew P., O'Brien, Brendan J. and Hawley, John Alan. (2009). Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle. Journal of Applied Physiology. 106(4), pp. 1187 - 1197. https://doi.org/10.1152/japplphysiol.91221.2008
Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens
Yeo, Wee Kian, Paton, Carl D., Garnham, Andrew P., Burke, Louise M., Carey, Andrew L. and Hawley, John Alan. (2008). Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. Journal of Applied Physiology. 105(5), pp. 1462 - 1470. https://doi.org/10.1152/japplphysiol.90882.2008
Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans
Yeo, Wee Kian, Lessard, Sarah J., Chen, Zhi-Ping, Garnham, Andrew P., Burke, Louise, Rivas, Donato A., Kemp, Bruce Ernest and Hawley, John Alan. (2008). Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans. Journal of Applied Physiology. 105(5), pp. 1519 - 1526. https://doi.org/10.1152/japplphysiol.90540.2008