High-impact exercise stimulated localised adaptation of microarchitecture across distal tibia in postmenopausal women

Du, J.; Hartley, C.; Brooke-Wavell, K.; Paggiosi, M. A.; Walsh, J. S.; Li, S.; Silberschmidt, V. V.

Affiliations

¹Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin, China

²Wolfson School of Mechanical, Electrical and Manufacturing Engineering, Loughborough University, Leicestershire, UK

³School of Sport, Exercise and Health Science, Loughborough University, Leicestershire, UK

⁴Mellanby Centre for Bone Research, University of Sheffield, Sheffield, UK

Abstract and keywords

Summary: We provided evidence that a 6-month regular hopping exercise intervention can increase trabecular number and possibly trabecular volume fraction of the distal tibia. Our novel localised analysis demonstrated region-specific changes, predominantly in the anterior region, in postmenopausal women.

Introduction: The localisation of bone remodelling and microarchitectural adaptation to exercise loading has not been demonstrated previously in vivo in humans. The aim of this study is to assess the feasibility of using 3D image registration and high-resolution peripheral quantitative computed tomography (HR-pQCT) to investigate the effect of high-impact exercise on human trabecular bone variables and remodelling rate across the distal tibia.

Methods: Ten postmenopausal women were recruited for 6-month unilateral hopping exercises, with HR-pQCT scans taken of both exercise leg (EL) and control leg (CL) for each participant before and after the intervention. A 3D image registration was used to ensure measurements were taken at the same region. Short-term reproducibility tests were conducted prior to the assessment using identical setup. The results were assessed comparing CL and EL, and interaction (time × leg) using a two-way repeated measures analysis of variance (RM-ANOVA).

Results: Across the whole tibia, we observed significant increases in trabecular number (Tb.N) (+ 4.4%) and trabecular bone formation rate (tBFR) (3.3%), and a non-significant increase in trabecular bone volume fraction (BV/TV) (+ 1%) in the EL. Regional resorption was higher in the CL than the EL, with this difference being statistically significant at the lateral tibia. In the EL, tBFR was significantly higher in the anterior region than the medial but a trabecular bone resorption rate (tBRR) showed no significant regional variation. Conversely in the CL, both tBFR and tBRR were significantly higher in the anterior and lateral than the medial region.

Conclusion: We demonstrated that it was possible to detect exercise-related bone adaptation with 3D registration of HR-pQCT scan data. Regular hopping exercise increased Tb.N and possibly BV/TV across the whole distal tibia. A novel finding of the study was that tBFR and tBRR responses to loading were localised: changes were achieved by formation rate exceeding resorption rate in the exercise leg, both globally and at the anterior region where turnover was greatest.

Trial registration: clinicaltrials.gov: NCT03225703

Keywords: 3D image registration; Exercise; Finite element analysis; Formation and resorption rates; HR-pQCT; Trabecular bone

Links

DOI: 10.1007/s00198-020-05714-4

PubMed: 33196852

WoS: 000590060500001

History

Received: 2020-06-19

Accepted: 2020-10-23

Online: 2020-11-16

Cited Works (27)

Year	Entry
2010	Burghardt AJ, Kazakia GJ, Sode M, de Papp AE, Link TM, Majumdar S. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res. December 2010;25(12):2558-2571.
1987	Lorensen WE, Cline HE. Marching cubes: a high resolution 3D surface construction algorithm. Comput Graph. 1987;21(4):163-169.
2001	Crabtree N, Loveridge N, Parker M, Rushton N, Power J, Bell KL, Beck TJ, Reeve J. Intracapsular hip fracture and the region-specific loss of cortical bone: analysis by peripheral quantitative computed tomography. J Bone Miner Res. July 2001;16(7):1318-1328.
2015	Allison SJ, Poole KES, Treece GM, Gee AH, Tonkin C, Rennie WJ, Folland JP, Summers GD, Brooke-Wavell K. The influence of high-impact exercise on cortical and trabecular bone mineral content and 3D distribution across the proximal femur in older men: a randomized controlled unilateral intervention. J Bone Miner Res. 2015;30(9):1709-1716.
2008	Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol. November 2008;3(suppl 3):S131-S139.
2010	Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ. BoneJ: free and extensible bone image analysis in ImageJ. Bone. December 2010;47(6):1076-1079.
2002	Eriksen E, Melsen F, Sod E, Barton I, Chines A. Effects of long-term risedronate on bone quality and bone turnover in women with postmenopausal osteoporosis. Bone. November 2002;31(5):620-625.
2016	Shanbhogue VV, Brixen K, Hansen S. Age- and sex-related changes in bone microarchitecture and estimated strength: a three-year prospective study using HRpQCT. J Bone Miner Res. August 2016;31(8):1541-1549.
2014	Ellouz R, Chapurlat R, van Rietbergen B, Christen P, Pialat J-B, Boutroy S. Challenges in longitudinal measurements with HR-pQCT: evaluation of a 3D registration method to improve bone microarchitecture and strength measurement reproducibility. Bone. June 2014;63:147-157.
2013	Nishiyama KK, Macdonald HM, Hanley DA, Boyd SK. Women with previous fragility fractures can be classified based on bone microarchitecture and finite element analysis measured with HR-pQCT. Osteoporos Int. May 2013;24(5):1733-1740.
2013	Schulte FA, Ruffoni D, Lambers FM, Christen D, Webster DJ, Kuhn G, Müller R. Local mechanical stimuli regulate bone formation and resorption in mice at the tissue level. PLoS One. April 2013;8(4):e62172.
2011	Schulte FA, Lambers FM, Kuhn G, Müller R. In vivo micro-computed tomography allows direct three-dimensional quantification of both bone formation and bone resorption parameters using time-lapsed imaging. Bone. March 2011;48(3):433-442.
2020	Whittier DE, Boyd SK, Burghardt AJ, Paccou J, Ghasem-Zadeh A, Chapurlat R, Engelke K, Bouxsein ML. Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int. September 2020;31(9):1607-1627.
2014	Kawalilak CE, Johnston JD, Olszynski WP, Kontulainen SA. Characterizing microarchitectural changes at the distal radius and tibia in postmenopausal women using HR-pQCT. Osteoporos Int. August 2014;25(8):2057-2066.
2020	Whittier DE, Burt LA, Hanley DA, Boyd SK. Sex‐ and site‐specific reference data for bone microarchitecture in adults measured using second‐generation HR‐pQCT. J Bone Miner Res. November 2020;35(11):2151-2158.
2000	Ding M, Hvid I. Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone. March 2000;26(3):291-295.
2020	Hartley C, Folland JP, Kerslake R, Brooke‐Wavell K. High‐impact exercise increased femoral neck bone density with no adverse effects on imaging markers of knee osteoarthritis in postmenopausal women. J Bone Miner Res. January 2020;35(1):53-63.
1997	Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.
2007	Sornay‐Rendu E, Boutroy S, Munoz F, Delmas PD. Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res. March 2007;22(3):425-433.
2016	Burt LA, Liang Z, Sajobi TT, Hanley DA, Boyd SK. Sex‐ and site‐specific normative data curves for HR‐pQCT. J Bone Miner Res. November 2016;31(11):2041-2047.
2005	Lai YM, Qin L, Yeung HY, Lee KKH, Chan KM. Regional differences in trabecular BMD and micro-architecture of weight-bearing bone under habitual gait loading: a pQCT and microCT study in human cadavers. Bone. 2005;37(2):274-282.
2013	Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R, Brown JP, Ste-Marie L-G, Kremer R, Erlandson MC, Dian L, Burghardt AJ, Boyd SK. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep. June 2013;11(2):136-146.
2013	Chen H, Zhou X, Fujita H, Onozuka M, Kubo K-Y. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. March 18, 2013;2013:213234.
2020	Stuck AK, Schenk D, Zysset P, Bütikofer L, Mathis A, Lippuner K. Reference values and clinical predictors of bone strength for HR-pQCT-based distal radius and tibia strength assessments in women and men. Osteoporos Int. October 2020;31(10):1913-1923.
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.
2010	Sode M, Burghardt AJ, Kazakia GJ, Link TM, Majumdar S. Regional variations of gender-specific and age-related differences in trabecular bone structure of the distal radius and tibia. Bone. June 2010;46(6):1652-1660.
2014	Christen P, Ito K, Ellouz R, Boutroy S, Sornay-Rendu E, Chapurlat RD, van Rietbergen B. Bone remodelling in humans is load-driven but not lazy. Nat Commun. September 2014;5:4855.

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Year	Entry
2023	Monzem S, Valkani D, Evans LAE, Chang Y-M, Pitsillides AA. Regional modular responses in different bone compartments to the anabolic effect of PTH (1-34) and axial loading in mice. Bone. May 2023;170:116720.
2023	Nissen FI, Esser VFC, Bui M, Li S, Hopper JL, Bjørnerem Å, Hansen AK. Is there a causal relationship between physical activity and bone microarchitecture? a study of adult female twin pairs. J Bone Miner Res. July 2023;38(7):951-957.