Characterizing microarchitectural changes at the distal radius and tibia in postmenopausal women using HR-pQCT

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Kawalilak, C. E.¹; Johnston, J. D.²; Olszynski, W. P.³; Kontulainen, S. A.¹

Characterizing microarchitectural changes at the distal radius and tibia in postmenopausal women using HR-pQCT

Osteoporos Int. August 2014;25(8):2057-2066

©2014 International Osteoporosis Foundation and National Osteoporosis Foundation

Affiliations

¹College of Kinesiology, University of Saskatchewan, 87 Campus Drive, Saskatoon, SK S7N 5B2, Canada

²Department of Mechanical Engineering, College of Engineering, University of Saskatchewan, Saskatoon, Canada

³College of Medicine, University of Saskatchewan, Saskatoon, Canada
Abstract and keywords

Summary: Limited prospective evidence exists regarding bone microarchitectural deterioration. We report annual changes in trabecular and cortical bone microarchitecture at the distal radius and tibia in postmenopausal women. Lost trabeculae with corresponding increase in trabecular thickness at the radius and thinning tibial cortex indicated trabecularization of the cortex at both sites.

Introduction: Osteoporosis is characterized by low bone mass and the deterioration of bone microarchitecture. However, limited prospective evidence exists regarding bone microarchitectural changes in postmenopausal women: a population prone to sustaining osteoporotic fractures. Our primary objective was to characterize the annual change in bone area, density, and microarchitecture at the distal radius and distal tibia in postmenopausal women.

Methods: Distal radius and tibia were measured using high-resolution peripheral quantitative computed tomography (HR-pQCT) at baseline and 1 year later in 51 women (mean age ± SD, 77 ± 7 years) randomly sampled from the Saskatoon cohort of the Canadian Multicentre Osteoporosis Study (CaMos). We used repeated measures analysis of variance (ANOVA) with Bonferroni adjustment for multiple comparisons to characterize the mean annual change in total density, cortical perimeter, trabecular and cortical bone area, density, content, and microarchitecture. Significant changes were accepted at P < 0.05.

Results: At the distal radius in women without bone-altering drugs, total density (−1.7 %) and trabecular number (−6.4 %) decreased, while trabecular thickness (+6.0 %), separation (+8.6 %), and heterogeneity (+12.1 %) increased. At their distal tibia, cortical area (−4.5 %), density (−1.9 %), content (−6.3 %), and thickness (−4.4 %) decreased, while trabecular area (+0.4 %) increased.

Conclusions: The observed loss of trabeculae with concomitant increase in trabecular size at the distal radius and the declined cortical thickness, density, and content at the distal tibia indicated a site-specific trabecularization of the cortical bone in postmenopausal women.

Keywords: Distal radius and tibia; HR-pQCT; Microarchitecture; One-year change
Links

DOI: 10.1007/s00198-014-2719-0

PubMed: 24781379

WoS: 000339895100008
History

Received: 2013-12-12

Accepted: 2014-04-11

Online: 2014-04-30

Cited Works (26)

Year	Entry
2012	Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S. Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone. January 2012;50(1):111-118.
1995	Riggs BL, Melton LJ III. The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone. November 1995;17(5)(suppl 1):S505-S511.
1988	Schaffler MB, Burr DB. Stiffness of compact bone: effects of porosity and density. J Biomech. 1988;21(1):13-16.
2009	Mueller TL, van Lenthe GH, Stauber M, Gratzke C, Eckstein F, Müller R. Regional, age and gender differences in architectural measures of bone quality and their correlation to bone mechanical competence in the human radius of an elderly population. Bone. November 2009;45(5):882-891.
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.
1999	Kreiger N, Tenenhouse A, Joseph L, Mackenzie T, Poliquin S, Brown JP, Prior JC, Rittmaster RS. The Canadian Multicentre Osteoporosis study (CaMos): background, rationale, methods. Can J Aging. 1999;18(3):376-387.
2010	Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S. Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res. May 2010;25(5):983-993.
1998	Laib A, Häuselmann HJ, Rüegsegger P. In vivo high resolution 3D-QCT of the human forearm. Technol Health Care. 1998;6(5-6):329-337.
1997	Laib A, Hildebrand T, Häuselmann HJ, Rüegsegger P. Ridge number density: a new parameter for in vivo bone structure analysis. Bone. December 1997;21(6):541-546.
2005	Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. December 2005;90(12):6508-6515.
2008	Kanis JA, McCloskey EV, Johansson H, Oden A, Melton LJ III, Khaltaev N. A reference standard for the description of osteoporosis. Bone. March 2008;42(3):467-475.
2009	Dalzell N, Kaptoge S, Morris N, Berthier A, Koller B, Braak L, van Rietbergen B, Reeve J. Bone micro-architecture and determinants of strength in the radius and tibia: age-related changes in a population-based study of normal adults measured with high-resolution pQCT. Osteoporos Int. October 2009;20(10):1683-1694.
2009	Holzer G, von Skrbensky G, Holzer LA, Pichl W. Hip fractures and the contribution of cortical versustrabecular bone to femoral neck strength. J Bone Miner Res. March 2009;24(3):468-474.
2011	Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK. Age‐related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population‐based HT‐pQCT study. J Bone Miner Res. January 2011;26(1):50-62.
2001	Siris ES, Miller PD, Barrett-Connor E, Faulkner KG, Wehren LE, Abbott TA, Berger ML, Santora AC, Sherwood LM. Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: results from the national osteoporosis risk assessment. JAMA. December 12, 2001;286(22):2815-2822.
1999	Cuddihy M-T, Gabriel SE, Crowson CS, O’Fallon WM, Melton LJ III. Forearm fractures as predictors of subsequent osteoporotic fractures. Osteoporos Int. June 1999;9(6):469-475.
2010	Liu XS, Cohen A, Shane E, Yin PT, Stein EM, Rogers H, Kokolus SL, McMahon DJ, Lappe JM, Recker RR, Lang T, Guo XE. Bone density, geometry, microstructure, and stiffness: relationships between peripheral and central skeletal sites assessed by DXA, HR‐pQCT, and cQCT in premenopausal women. J Bone Miner Res. October 2010;25(10):2229-2238.
2010	Zebaze RMD, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. May 15, 2010;375(9727):1729-1736.
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.
2006	Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. December 2006;17(12):1726-1733.
2005	Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J. Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet. July 9, 2005;366(9480):129-135.
2002	Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet. June 1, 2002;359(9321):1929-1936.
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.
1999	Laib A, Rüegsegger P. Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-μm-resolution microcomputed tomography. Bone. January 1999;24(1):35-39.
2010	Papaioannou A, Morin S, Cheung AM, Atkinson S, Brown JP, Feldman S, Hanley DA, Hodsman A, Jamal SA, Kaiser SM, Kvern B, Siminoski K, Leslie WD; Scientific Advisory Council of Osteoporosis Canada. 2010 clinical practice guidelines for the diagnosis and management of osteoporosis in Canada: summary. Can Med Assoc J. November 23, 2010;182(17):1864-1873.

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Year	Entry
2015	Manske SL, Zhu Y, Sandino C, Boyd SK. Human trabecular bone microarchitecture can be assessed independently of density with second generation HR-pQCT. Bone. October 2015;79:213-221.
2020	Jin Y, Zhang T, Cheung JPY, Wong TM, Feng X, Sun T, Zu H, Sze KY, Lu WW. A novel mechanical parameter to quantify the microarchitecture effect on apparent modulus of trabecular bone: a computational analysis of ineffective bone mass. Bone. June 2020;135:115314.
2020	Liu C, Pang Q, Jiang Y, Xia Y, Fang L, Wang O, Li M, Xing X, Gong Y, Xia W. Defective O-glycosylation of novel FGF23 mutations in a Chinese family with hyperphosphatemic familial tumoral calcinosis. Bone. August 2020;137:115401.
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.
2017	Burt LA, Hanley DA, Boyd SK. Cross-sectional versus longitudinal change in a prospective HR-pQCT study. J Bone Miner Res. July 2017;32(7):1505-1513.
2017	Manske SL, Davison EM, Burt LA, Raymond DA, Boyd SK. The estimation of second-generation HR-pQCT from first-generation -pQCT using in vivo cross-calibration. J Bone Miner Res. July 2017;32(7):1514-1524.
2020	Yu F, Xu Y, Hou Y, Lin Y, Jiajue R, Jiang Y, Wang O, Li M, Xing X, Zhang L, Qin L, Hsieh E, Xia W. Age‐, site‐, and sex‐specific normative centile curves for HR‐pQCT‐derived microarchitectural and bone strength parameters in a Chinese mainland population. J Bone Miner Res. November 2020;35(11):2159-2170.
2020	Burt LA, Billington EO, Rose MS, Kremer R, Hanley DA, Boyd SK. Adverse effects of high‐dose vitamin D supplementation on volumetric bone density are greater in females than males. J Bone Miner Res. December 2020;35(12):2404-2414.
2022	Johannesdottir F, Putman MS, Burnett-Bowie S-AM, Finkelstein JS, Yu EW, Bouxsein ML. Age-related changes in bone density, microarchitecture, and strength in postmenopausal black and white women: the SWAN longitudinal HR-pQCT study. J Bone Miner Res. January 2022;37(1):41-51.
2023	Agarwal S, Shiau S, Kamanda-Kosseh M, Bucovsky M, Kil N, Lappe JM, Stubby J, Recker RR, Guo XE, Shane E, Cohen A. Teriparatide followed by denosumab in premenopausal idiopathic osteoporosis: bone microstructure and strength by HR-pQCT. J Bone Miner Res. January 2023;38(1):35-47.
2023	Sadoughi S, Subramanian A, Ramil G, Burghardt AJ, Kazakia GJ. A Laplace–Hamming binarization approach for second-generation HR-pQCT rescues fine feature segmentation. J Bone Miner Res. July 2023;38(7):1006-1014.
2021	Jiang H, Robinson DL, Lee PVS, Krejany EO, Yates CJ, Hickey M, Wark JD. Loss of bone density and bone strength following premenopausal risk–reducing bilateral salpingo-oophorectomy: a prospective controlled study (WHAM Study). Osteoporos Int. January 2021;32(1):101-112.
2021	Rønn SH, Harsløf T, Oei L, Pedersen SB, Langdahl BL. The effect of vitamin MK-7 on bone mineral density and microarchitecture in postmenopausal women with osteopenia, a 3-year randomized, placebo-controlled clinical trial. Osteoporos Int. January 2021;32(1):185-191.
2021	Du J, Hartley C, Brooke-Wavell K, Paggiosi MA, Walsh JS, Li S, Silberschmidt VV. High-impact exercise stimulated localised adaptation of microarchitecture across distal tibia in postmenopausal women. Osteoporos Int. May 2021;32(5):907-919.
2017	Hemmatian H. Does the Osteocyte Lacuna Affect Bone Adaptive Response in Aging? [PhD thesis]. Katholieke Universiteit Leuven; December 2017.
2019	Du J. Mechanical Adaptation of Human Trabecular Bone: Experimental and Computational Study [PhD thesis]. Loughborough University; 2019.
2016	Hildebrandt EM. Effect of Increased 25(OH)D on Bone Health, a High Resolution Peripheral Computed Tomography Study [Master's thesis]. Calgary, AB: University of Calgary; April 2016.
2023	Kaketsis D. Investigating Bone Remodelling in Knee Osteoarthritis Using HR-PQCT Imaging [Master's thesis]. Calgary, AB: University of Calgary; May 2023.
2018	Hosseinitabatabaei S. High-Resolution Peripheral Quantitative Computed Tomography Based Finite Element Modelling of Distal Radius Strength: Assessing Effect of Heterogeneous Material Properties and Scan Site [Master's thesis]. University of Saskatchewan; October 2018.
2020	Bunyamin ATO. Predicting Off-Axis Bone Strength of the Distal Radius Using High-Resolution Peripheral Quantitative Computed Tomography Based Finite Element Modeling [Master's thesis]. University of Saskatchewan; March 2020.