Shorter, more frequent mechanical loading sessions enhance bone mass

wbldb

Robling, Alexander G.¹; Hinant, Felicia M.¹; Burr, David B.¹; Turner, Charles H.¹

Shorter, more frequent mechanical loading sessions enhance bone mass

Med Sci Sports Exer. February 2002;34(2):196-202

©2002 American College of Sports Medicine

Affiliations

¹Department of Anatomy and Cell Biology; Department of Orthopaedic Surgery; Biomechanics and Biomaterials Research Center; Indiana University School of Medicine, Indianapolis, IN
Abstract and keywords

Purpose: The beneficial effects of exercise on bone mass and strength can be attributed to the sensitivity of bone cells to mechanical stimuli. However, bone cells lose mechanosensitivity soon after they are stimulated. We investigated whether the osteogenic response to a simulated high-impact exercise program lasting 4 months could be enhanced by dividing the daily protocol into brief sessions of loading, separated by recovery periods.

Methods: The right forelimbs of adult rats were subjected to 360 load cycles·d⁻¹, 3 d·wk⁻¹, for 16 wk. On each loading day, one group received all 360 cycles in a single, uninterrupted bout (360 × 1); the other group received 4 bouts of 90 cycles/bout (90 × 4), with each bout separated by 3 h. After sacrifice, bone mineral content (BMC), and areal bone mineral density (aBMD) were measured in the loaded (right) and nonloaded control (left) ulnae using DXA. Volumetric BMD (vBMD) and cross-sectional area (CSA) were measured at midshaft and the olecranon by using pQCT. Maximum and minimum second moments of area (I_MAX and I_{_MIN}) were measured from the midshaft tomographs.

Results: After 16 wk of loading, BMC, aBMD, vBMD, midshaft CSA, I_MAX, and I_{_MIN} were significantly greater in right (loaded) ulnae compared with left (nonloaded) ulnae in the two loaded groups. When the daily loading regimen was broken into four sessions per day (90×4), BMC, aBMD, midshaft CSA, and I_{_MIN} improved significantly over the loading schedule that applied the daily stimulus in a single, uninterrupted session (360×1).

Conclusion: Human exercise programs aimed at maintaining or improving bone mass might achieve greater success if the daily exercise regime is broken down into smaller sessions separated by recovery periods.

Keywords: MECHANICAL LOADING; BONE ADAPTATION; RECOVERY; EXERCISE; OSTEOPOROSIS; BMD
Links

DOI: 10.1097/00005768-200202000-00003

PubMed: 11828225

WoS: 000173739100003
History

Received: 2001-02

Accepted: 2002-05

Cited Works (15)

Year	Entry
1998	Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. November 1998;23(5):399-407.
1992	Akhter MP, Raab DM, Turner CH, Kimmel DB, Recker RR. Characterization of in vivo strain in the rat tibia during external application of a four-point bending load. J Biomech. October 1992;25(10):1241-1246.
1997	Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S. Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res. September 1997;12(10):1480-1485.
1994	Torrance AG, Mosley JR, Suswillo RFL, Lanyon LE. Noninvasive loading of the rat ulna in vivo induces a strain-related modeling response uncomplicated by trauma or periostal pressure. Calcif Tiss Int. March 1994;54(3):241-247.
1995	Kannus P, Haapasalo H, Sankelo M, Sievanen H, Pasanen M, Heinonen A, Oja P, Vuori I. Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med. July 1995;123(1):27-31.
2000	Robling AG, Burr DB, Turner CH. Partitioning a daily mechanical stimulus into discrete loading bouts improves the osteogenic response to loading. J Bone Miner Res. August 2000;15(8):1596-1602.
1996	Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, Hoshaw S, Saiag E, Simkin A. In vivo measurement of human tibial strains during vigorous activity. Bone. May 1996;18(5):405-410.
1990	Frost HM. Skeletal structural adaptations to mechanical usage (SATMU), I: redefining Wolff's law: the bone modeling problem. Anat Rec. 1990;226(4):403-413.
1990	Frost HM. Skeletal structural adaptations to mechanical usage (SATMU), II: redefining Wolff's Law: the remodeling problem. Anat Rec. April 1990;226(4):414-422.
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.
1984	Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. March 1984;66A(3):397-402.
2001	Robling AG, Burr DB, Turner CH. Recovery periods restore mechanosensitivity to dynamically loaded bone. J Exp Biol. 2001;204(19):3389-3399.
1994	Bassey EJ, Ramsdale SJ. Increase in femoral bone density in young women following high-impact exercise. Osteoporos Int. March 1994;4(2):72-75.
2001	Robling AG, Duijvelaar KM, Geevers JV, Ohashi N, Turner CH. Modulation of appositional and longitudinal bone growth in the rat ulna by applied static and dynamic force. Bone. August 2001;29(2):105-113.
1987	Frost HM. Bone "mass" and the "mechanostat": a proposal. Anat Rec. September 1987;219(1):1-9.

Cited By (29)

Year	Entry
2005	Fritton JC, Myers ER, Wright TM, van der Meulen MCH. Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia. Bone. June 2005;36(6):1030-1038.
2006	Bonewald LF. Mechanosensation and transduction in osteocytes. BoneKEy Osteovision. October 2006;3(10):7-15.
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.
2006	Sawakami K, Robling AG, Ai M, Pitner ND, Liu D, Warden SJ, Li J, Maye P, Rowe DW, Duncan RL, Warman ML, Turner CH. The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem. August 18, 2006;281(33):23698-23711.
2005	Schriefer JL, Warden SJ, Saxon LK, Robling AG, Turner CH. Cellular accommodation and the response of bone to mechanical loading. J Biomech. September 2005;38(9):1838-1845.
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.
2011	Bonewald LF. The amazing osteocyte. J Bone Miner Res. 2011;26(2):229-238.
2021	Ng C, Scott D, Seibel MJ, Cumming RG, Naganathan V, Blyth FM, Le Couteur DG, Waite LM, Handelsman DJ, Hirani V. Higher‐impact physical activity is associated with maintenance of bone mineral density but not reduced incident falls or fractures in older men: the Concord Health and Aging in Men Project. J Bone Miner Res. April 2021;36(4):662-672.
2008	Weeks BK, Beck BR. The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos Int. November 2008;19(11):1567-1577.
2021	Ng C-A, McMillan LB, Humbert L, Ebeling PR, Scott D. Feasibility, safety and effectiveness of a pilot 16-week home-based, impact exercise intervention in postmenopausal women with low bone mineral density. Osteoporos Int. May 2021;32(5):893-905.
2017	Lewis KJ. Osteocyte Calcium Signaling Responses to Mechanical Load in Vivo: A Novel Experimental Approach [PhD thesis]. New York, NY: The City College of New York; 2017.
2006	Fritton JC. Mechanical Loading Induced Adaptation of the Mouse Tibia [PhD thesis]. Ithaca, NY: Cornell University; January 2006.
2010	Lynch ME. Cancellous Bone Adaptation to Non-Invasive Mechanical Loading in the Murine Tibia [PhD thesis]. Ithaca, NY: Cornell University; August 2010.
2004	Duty AO. Controlled in Vivo Mechanical Stimulation of Bone Repair Constructs [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; April 2004.
2007	Young CM. Do in-Line Dance, Progressively Loaded Squats and Foot Stomping Affect the Parameters of Fracture Risk in Postmenopausal Women? [Master's thesis]. Brisbane, Australia: Griffith University; 2007.
2008	Weeks BK. Improving Bone Health With Physical Activity: The Power PE Study and Development of the Bone-Specific Physical Activity Questionnaire (BPAQ) [PhD thesis]. Brisbane, Australia: Griffith University; January 2008.
2009	Edwards WB. Internal Structural Loading of the Lower Extremity During Running: Implications for Skeletal Injury [PhD thesis]. Iowa State University; 2009.
2005	Zumwalt AC. The Effect of Endurance Exercise on the Morphology of Muscle Attachment Sites: An Experimental Study in Sheep (Ovis Aries) [PhD thesis]. Johns Hopkins University; March 2005.
2004	Giangregorio L. Musculoskeletal Changes After Spinal Cord Injury: Effects of Body Weight Supported Treadmill Training [PhD thesis]. Hamilton, ON: McMaster University; November 2004.
2013	Antolić A. Mitochondrial Contributions to Bone Health, an Investigation Using Two Different Animal Models of Mitochondrial Capacity [PhD thesis]. Hamilton, ON: McMaster University; September 2013.
2015	Ireland AD. Bone Mechanoadaptation and the Influence of Muscular Action on Bone Across the Lifespan [PhD thesis]. Manchester Metropolitan University; 2015.
2022	Ng CATT. Getting the Jump on Healthy Bones: The Skeletal Effects of Impact Physical Activity Across the Lifespan [PhD thesis]. Monash University; 2022.
2006	Bauer JJ. Defining Intensity of Skeletal Loading in Children [PhD thesis]. Corvalis, OR: Oregon State University; June 2006.
2012	Kaupp JA. Simulated Joint Loading Enhances the Expression of of Superficial Zone Markers in Tissue Engineered Cartilage Constructs [PhD thesis]. Queen's University; February 2012.
2006	Hannay G. Mechanical and Electrical Environments to Stimulate Bone Cell Development [PhD thesis]. Queensland University of Technology; August 2006.
2006	Macdonald HM. Effectiveness of a School-Based Physical Activity Intervention for Increasing Bone Strength in Children: Action Schools! British Columbia [PhD thesis]. Vancouver, BC: University of British Columbia; July 2006.
2015	Tan VPS. Effects of a School-Based Physical Activity Intervention on Adolescent Bone Strength, Structure and Density: The Health Promoting Secondary Schools (HPSS) Bone Health Study [PhD thesis]. Vancouver, BC: University of British Columbia; June 2015.
2020	Pei S. Osteocyte Mechanosensing: Interstitial Fluid Flow, Cellular Response, and Turnover of Pericellular Matrix [PhD thesis]. University of Delaware; 2020.
2007	Wallace JM III. Investigating the Inbred Strain-Specific Response to Biglycan-Deficiency and Exercise: A Study in Genetically-Mediated Skeletal Adaptation [PhD thesis]. University of Michigan; 2007.