The effects of acute exercise on bone turnover markers in middle-aged and older adults:​ a systematic review

Smith, Cassandra<sup>1,2</sup>; Tacey, Alexander<sup>1,2</sup>; Mesinovic, Jakub<sup>3</sup>; Scott, David<sup>2,3,4</sup>; Lin, Xuzhu<sup>3</sup>; Brennan-Speranza, Tara C.<sup>6,7</sup>; Lewis, Joshua R.<sup>8,9,10</sup>; Duque, Gustavo<sup>2,11</sup>; Levinger, Itamar<sup>1,2</sup>

Affiliations

¹Institute for Health and Sport (IHES), Victoria University, Melbourne, VIC, Australia

²Australian Institute for Musculoskeletal Science (AIMSS), University of Melbourne and Western Health, St Albans, VIC, Australia

³School of Clinical Sciences at Monash Health, Monash University, Melbourne, VIC, Australia

⁴Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Burwood, Victoria, Australia

⁵Diabetes & Metabolic Disease Laboratory, St. Vincent’s Institute of Medical Research, Fitzroy, VIC, Australia

⁶Department of Physiology, School of Medical Sciences, Faculty of Medicine and Health, University of Sydney, Sydney, Australia

⁷School of Public Health, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW, Australia

⁸School of Medical and Health Sciences, Edith Cowan University, Perth, WA, Australia

⁹Centre for Kidney Research, Children’s Hospital at Westmead, School of Public Health, Sydney Medical School, The University of Sydney, Sydney, NSW, Australia

¹⁰Medical School, University Western Australia, Perth, WA, Australia

¹¹Department of Medicine-Western Health, Melbourne Medical School, The University of Melbourne, Melbourne, VIC, Australi

Abstract and keywords

Background: Bone turnover is the cellular machinery responsible for bone integrity and strength and, in the clinical setting, it is assessed using bone turnover markers (BTMs). Acute exercise can induce mechanical stress on bone which is needed for bone remodelling, but to date, there are conflicting results in regards to the effects of varying mechanical stimuli on BTMs.

Objectives: This systematic review examines the effects of acute aerobic, resistance and impact exercises on BTMs in middle and older-aged adults and examines whether the responses are determined by the exercise mode, intensity, age and sex.

Methods: We searched PubMed, SCOPUS, Web of Science and EMBASE up to 22nd April 2020. Eligibility criteria included randomised controlled trials (RCTs) and single-arm studies that included middle-aged (50 to 65 years) and older adults (>65 years) and, a single-bout, acute-exercise (aerobic, resistance, impact) intervention with measurement of BTMs. PROSPERO registration number CRD42020145359.

Results: Thirteen studies were included; 8 in middle-aged (n = 275, 212 women/63 men, mean age = 57.9 ± 1.5 years) and 5 in older adults (n = 93, 50 women/43 men, mean age = 68.2 ± 2.2 years). Eleven studies included aerobic exercise (AE, 7 middle-aged/4 older adults), and two included resistance exercise (RE, both middle-aged). AE significantly increased C-terminal telopeptide (CTX), alkaline phosphatase (ALP) and bone-ALP in middle-aged and older adults. AE also significantly increased total osteocalcin (tOC) in middle-aged men and Procollagen I Carboxyterminal Propeptide and Cross-Linked Carboxyterminal Telopeptide of Type I Collagen in older women. RE alone decreased ALP in older adults. In middle-aged adults, RE with impact had no effect on tOC or BALP, but significantly decreased CTX. Impact (jumping) exercise alone increased Procollagen Type 1 N Propeptide and tOC in middle-aged women.

Conclusion: Acute exercise is an effective tool to modify BTMs, however, the response appears to be exercise modality-, intensity-, age- and sex-specific. There is further need for higher quality and larger RCTs in this area.

Keywords: Acute exercise; Ageing; Bone turnover markers; Intensity

Links

DOI: 10.1016/j.bone.2020.115766

PubMed: 33227507

WoS: 000604737000003

History

Received: 2020-08-25

Revised: 2020-11-18

Accepted: 2020-11-18

Online: 2020-11-21

Cited Works (28)

Year	Entry
2000	Delmas PD, Eastell R, Garnero P, Seibel MJ, Stepan J; Committee of Scientific Advisors of the International Osteoporosis Foundation. The use of biochemical markers of bone turnover in osteoporosis. Osteoporos Int. December 2000;11(suppl 6):S2-S17.
1995	Forwood MR, Turner CH. Skeletal adaptations to mechanical usage: results from tibial loading studies in rats. Bone. October 1995;17(4)(suppl):197S-205S.
1996	Lanyon LE. Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone. January 1996;18(1)(suppl):37S-43S.
2003	Kontulainen S, Sievänen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res. February 2003;18(2):352-359.
1998	Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW. Pre- and postmenopausal women have different bone mineral density responses to the same high-impact exercise. J Bone Miner Res. December 1998;13(12):1805-1813.
2015	Zhao R, Zhao M, Xu Z. The effects of differing resistance training modes on the preservation of bone mineral density in postmenopausal women: a meta-analysis. Osteoporos Int. May 2015;26(5):1605-1618.
2013	Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S. Mechanosensation and transduction in osteocytes. Bone. June 2013;54(2):182-190.
1999	Turner CH. Toward a mathematical description of bone biology: the principle of cellular accommodation. Calcif Tiss Int. December 1999;65(6):466-471.
2016	Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS. The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. April 2016;27(4):1281-1386.
1987	Frost HM. Bone "mass" and the "mechanostat": a proposal. Anat Rec. September 1987;219(1):1-9.
1996	Garnero P, Sornay‐Rendu E, Chapuy M, Delmas PD. Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. J Bone Miner Res. 1996;11(3):337-349.
1982	Lanyon LE, Goodship AE, Pye CJ, MacFie JH. Mechanically adaptive bone remodelling. J Biomech. 1982;15(3):141-154.
1984	Lanyon LE, Rubin CT. Static vs dynamic loads as an influence on bone remodelling. J Biomech. 1984;17(12):897-905.
1996	Forwood MR, Owan I, Takano Y, Turner CH. Increased bone formation in rat tibiae after a single short period of dynamic loading in vivo. Am J Physiol Endocrinol Metab. March 1996;270(3):E419-E423.
2018	Watson SL, Weeks BK, Weis LJ, Harding AT, Horan SA, Beck BR. High-intensity resistance and impact training improves bone mineral density and physical function in postmenopausal women with osteopenia and osteoporosis: the LIFTMOR randomized controlled trial. J Bone Miner Res. February 2018;33(2):211-220.
1984	Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. March 1984;66A(3):397-402.
1987	Rubin CT, Lanyon LE. Osteoregulatory nature of mechanical stimuli: function as a determinant for adaptive remodeling in bone. J Orthop Res. 1987;5(2):300-310.
2011	Howe TE, Shea B, Dawson LJ, Downie F, Murray A, Ross C, Harbour RT, Caldwell LM, Creed G. Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Sys Rev. July 6, 2011;7:CD000333.
2002	Ehrlich PJ, Lanyon LE. Mechanical strain and bone cell function: a review. Osteoporos Int. September 2002;13(9):688-700.
1994	Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. March 1994;27(3):339-360.
2009	Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. July 21, 2009;6(7):e1000097.
2006	Seeman E, Delmas PD. Bone quality: the material and structural basis of bone strength and fragility. NEJM. May 25, 2006;354(21):2250-2261.
2001	Hsieh Y, Turner CH. Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res. May 2001;16(5):918-924.
2002	Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet. June 1, 2002;359(9321):1929-1936.
1998	Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. November 1998;23(5):399-407.
1982	O'Connor JA, Lanyon LE, MacFie H. The influence of strain rate on adaptive bone remodelling. J Biomech. 1982;15(10):767-781.
1998	Mosley JR, Lanyon LE. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone. October 1998;23(4):313-318.
2002	Robling AG, Hinant FM, Burr DB, Turner CH. Improved bone structure and strength after long‐term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res. August 2002;17(8):1545-1554.

Cited By (1)

Year	Entry
2023	Hilkens L, Boerboom M, van Schijndel N, Bons J, van Loon LJ, van Dijk J-W. Bone turnover following high-impact exercise is not modulated by collagen supplementation in young men: a randomized cross-over trial. Bone. May 2023;170:116705.