Abstract
Summary
This HR-pQCT study was conducted to examine bone properties of the distal tibia post-stroke and to identify clinical outcomes that were associated with these properties at this site. It was found that spasticity and gait speed were independently associated with estimated failure load in individuals with chronic stroke.
Purpose
(1) To examine the influence of stroke on distal tibia bone properties and (2) the association between these properties and clinical outcomes in people with chronic stroke.
Methods
Sixty-four people with stroke (age, 60.8 ± 7.7 years; time since stroke, 5.7 ± 3.9 years) and 64 controls (age: 59.4 ± 7.8 years) participated in this study. High-resolution peripheral quantitative computed tomography (HR-pQCT) was used to scan the bilateral distal tibia, and estimated failure load was calculated by automated finite element analysis. Echo intensity of the medial gastrocnemius muscle and blood flow of the popliteal artery were assessed with ultrasound. The 10-m walk test (10MWT), Fugl-Meyer Motor Assessment (FMA), and Composite Spasticity Scale (CSS) were also administered.
Results
The percent side-to-side difference (%SSD) in estimated failure load, cortical area, thickness, and volumetric bone mineral density (vBMD), and trabecular and total vBMD were significantly greater in the stroke group than their control counterparts (Cohen’s d = 0.48–1.51). Isometric peak torque and echo intensity also showed significant within- and between-groups differences (p ≤ 0.01). Among HR-pQCT variables, the %SSD in estimated failure load was empirically chosen as one example of the strong discriminators between the stroke group and control group, after accounting for other relevant factors. The 10MWT and CSS subscale for ankle clonus remained significantly associated with the %SSD in estimated failure load after adjusting for other relevant factors (p ≤ 0.05).
Conclusion
The paretic distal tibia showed more compromised vBMD, cortical area, cortical thickness, and estimated failure load than the non-paretic tibia. Gait speed and spasticity were independently associated with estimated failure load. As treatment programs focusing on these potentially modifiable stroke-related impairments are feasible to administer, future studies are needed to determine the efficacy of such intervention strategies for improving bone strength in individuals with chronic stroke.
Similar content being viewed by others
Data availability
The authors agree to deposit the project data on a community-recognized data repository.
Code availability
Post-processing of B-mode ultrasound images involved the use of a custom program written in MATLAB (version R2018a, MathWorks, Natick, MA, USA) for estimating muscle echo intensity (impixel function). MATLAB and SPSS (version 26, IBM Corp., Armonk, NY, USA) are commercially available software.
References
Eng JJ (2008) Balance, falls, and bone health: Role of exercise in reducing fracture risk after stroke. J Rehabil Res Dev 45:297–314
Poole KES, Reeve J, Warburton EA (2002) Falls, fractures, and osteoporosis after stroke. Time to think about protection? Stroke 33:1432–1436
Dennis MS, Lo KM, McDowall M, West T (2002) Fractures after stroke Frequency, Types, and Associations. Stroke 33:728–734
Ramnemark A, Nyberg L, Borssén B, Olsson T, Gustafson Y (1998) Fractures after stroke. Osteoporos Int 8:92–95
Pang MY, Ashe MC, Eng JJ (2008) Tibial bone geometry in chronic stroke patients: influence of sex, cardiovascular health, and muscle mass. J Bone Miner Res 23:1023–1030
Pang MYC, Lau RWK (2010) The effects of treadmill exercise training on hip bone density and tibial bone geometry in stroke survivors: a pilot study. Neurorehabil Neural Repair 24:368–376
Pang MY, Ashe MC, Eng JJ (2010) Compromised bone strength index in the hemiparetic distal tibia epiphysis among chronic stroke patients: the association with cardiovascular function, muscle atrophy, mobility, and spasticity. Osteoporos Int 21:997–1007
Lam FM, Bui M, Yang FZ, Pang MY (2016) Chronic effects of stroke on hip bone density and tibial morphology: a longitudinal study. Osteoporos Int 27:591–603
Pang MYC, Ashe MC, Eng JJ, McKay HA, Dawson AS (2006) A 19-week exercise program for people with chronic stroke enhances bone geometry at the tibia: a peripheral quantitative computed tomography study. Osteoporos Int 17:1615–1625
Yang FZ, Pang MY (2015) Influence of chronic stroke impairments on bone strength index of the tibial distal epiphysis and diaphysis. Osteoporos Int 26:469–480
Talla R, Galea M, Lythgo N, Eser T, Talla P, Angeli P, Eser P, Lythgo P (2011) Contralateral comparison of bone geometry, BMD and muscle function in the lower leg and forearm after stroke. J Musculoskeletal Neuronal Interact 11:306–313
Lazoura O, Groumas N, Antoniadou E, Papadaki PJ, Papadimitriou A, Thriskos P, Fezoulidis I, Vlychou M (2008) Bone mineral density alterations in upper and lower extremities 12 months after stroke measured by peripheral quantitative computed tomography and DXA. J Clin Densitom 11:511–517
Ramnemark A, Nyberg L, Lorentzon R, Englund U, Gustafson Y (1999) Progressive hemiosteoporosis on the paretic side and increased bone mineral density in the nonparetic arm the first year after severe stroke. Osteoporos Int 9:269–275
Souzanchi MF, Palacio-Mancheno P, Borisov YA, Cardoso L, Cowin SC (2012) Microarchitecture and bone quality in the human calcaneus: local variations of fabric anisotropy. J Bone Miner Res 27:2562–2572
Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515
Burt LA, Manske SL, Hanley DA, Boyd SK (2018) Lower bone density, impaired microarchitecture, and strength predict future fragility fracture in postmenopausal women: 5-year follow-up of the Calgary CaMos Cohort. J Bone Miner Res 33:589–597
Sornay-Rendu E, Boutroy S, Duboeuf F, Chapurlat RD (2017) Bone microarchitecture assessed by HR-pQCT as predictor of fracture risk in postmenopausal women: the OFELY study. J Bone Miner Res 32:1243–1251
Szulc P, Boutroy S, Chapurlat R (2018) Prediction of fractures in men using bone microarchitectural parameters assessed by high-resolution peripheral quantitative computed tomography-the prospective STRAMBO Study. J Bone Miner Res 33:1470–1479
Langsetmo L, Peters KW, Burghardt AJ et al (2018) Volumetric bone mineral density and failure load of distal limbs predict incident clinical fracture independent of FRAX and clinical risk factors among older men. J Bone Miner Res 33:1302–1311
Fink HA, Langsetmo L, Vo TN, Orwoll ES, Schousboe JT, Ensrud KE, Osteoporotic Fractures in Men Study G (2018) Association of high-resolution peripheral quantitative computed tomography (HR-pQCT) bone microarchitectural parameters with previous clinical fracture in older men: the Osteoporotic Fractures in Men (MrOS) study. Bone 113:49–56
Samelson EJ, Broe KE, Xu H et al (2019) Cortical and trabecular bone microarchitecture as an independent predictor of incident fracture risk in older women and men in the Bone Microarchitecture International Consortium (BoMIC): a prospective study. Lancet Diabetes Endocrinol 7:34–43
Borschmann K, Iuliano S, Ghasem-Zadeh A, Churilov L, Pang MYC, Bernhardt J (2018) Upright activity and higher motor function may preserve bone mineral density within 6 months of stroke: a longitudinal study. Arch Osteoporos 13:5
Miller T, Ying MTC, Hung VWY, Tsang CSL, Ouyang H, Chung RCK, Qin L, Pang MYC (2020) Determinants of estimated failure load in the distal radius after stroke: An HR-pQCT study. Bone 144:115831
Whittier DE, Boyd SK, Burghardt AJ, Paccou J, Ghasem-Zadeh A, Chapurlat R, Engelke K, Bouxsein ML (2020) Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int 31(9):1607–1627
Portney LG (2015) Foundations of clinical research : applications to practice. F.A. Davis Company, Philadelphia
Pang MY, Cheng AQ, Warburton DE, Jones AY (2012) Relative impact of neuromuscular and cardiovascular factors on bone strength index of the hemiparetic distal radius epiphysis among individuals with chronic stroke. Osteoporos Int 23:2369–2379
Blanca MJ, Alarcon R, Arnau J, Bono R, Bendayan R (2017) Non-normal data: is ANOVA still a valid option? Psicothema 29:552–557
Eriksen EF (2010) Cellular mechanisms of bone remodeling. Rev Endocr Metab Disord 11:219–227
Zhou B, Zhang Z, Hu Y, Wang J, Yu YE, Nawathe S, Nishiyama KK, Keaveny TM, Shane E, Guo XE (2019) Regional variations of HR-pQCT morphological and biomechanical measurements of the distal radius and tibia and their associations with whole bone mechanical properties. J Biomech Eng 141(9):0910081–0910087
Barry DW, Kohrt WM (2008) Exercise and the preservation of bone health. J Cardiopulm Rehabil Prev 28:153–162
Worthen LC, Kim CM, Kautz SA, Lew HL, Kiratli BJ, Beaupre GS (2005) Key characteristics of walking correlate with bone density in individuals with chronic stroke. J Rehabil Res Dev 42:761–768
Fulk GD, He Y, Boyne P, Dunning K (2017) Predicting home and community walking activity poststroke. Stroke 48:406–411
Raja B, Neptune RR, Kautz SA (2012) Quantifiable patterns of limb loading and unloading during hemiparetic gait: relation to kinetic and kinematic parameters. J Rehabil Res Dev 49:1293–1304
Jørgensen L, Crabtree NJ, Reeve J, Jacobsen BK (2000) Ambulatory level and asymmetrical weight bearing after stroke affects bone loss in the upper and lower part of the femoral neck differently: bone adaptation after decreased mechanical loading. Bone 27:701–707
Chang K-H, Liou T-H, Sung J-Y, Wang C-Y, Genant HK, Chan WP (2014) Femoral neck bone mineral density change is associated with shift in standing weight in hemiparetic stroke patients. Am J Phys Med Rehabil 93:477–485
Sherk KA, Sherk VD, Anderson MA, Bemben DA, Bemben MG (2013) Differences in tibia morphology between the sound and affected sides in ankle-foot orthosis-using survivors of stroke. Arch Phys Med Rehabil 94:510–515
Eng JJ (2010) Fitness and Mobility Exercise (FAME) Program for stroke. Top Geriatr Rehabil 26:310–323
Pang MYC, Eng JJ, Dawson AS, McKay HA, Harris JE (2005) A community-based fitness and mobility exercise program for older adults with chronic stroke: a randomized, controlled trial. J Am Geriatr Soc 53:1667–1674
Pang MY, Ashe MC, Eng JJ (2007) Muscle weakness, spasticity and disuse contribute to demineralization and geometric changes in the radius following chronic stroke. Osteoporos Int 18:1243–1252
Pang MY, Eng JJ (2005) Muscle strength is a determinant of bone mineral content in the hemiparetic upper extremity: implications for stroke rehabilitation. Bone 37:103–111
Marcolino MAZ, Hauck M, Stein C, Schardong J, Pagnussat AdS, Plentz RDM (2020) Effects of transcutaneous electrical nerve stimulation alone or as additional therapy on chronic post-stroke spasticity: systematic review and meta-analysis of randomized controlled trials. Disabil Rehabil 42:623–635
Lin S, Sun Q, Wang H, Xie G (2018) Influence of transcutaneous electrical nerve stimulation on spasticity, balance, and walking speed in stroke patients: a systematic review and meta-analysis. J Rehabil Med 50:3–7
Macneil JA, Boyd SK (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213
Turner CH, Rho J, Takano Y, Tsui TY, Pharr GM (1999) The elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques. J Biomech 32:437–441
van Rietbergen B, Ito K (2015) A survey of micro-finite element analysis for clinical assessment of bone strength: the first decade. J Biomech 48:832–841
Varga P, Dall’Ara E, Pahr DH, Pretterklieber M, Zysset PK (2011) Validation of an HR-pQCT-based homogenized finite element approach using mechanical testing of ultra-distal radius sections. Biomech Model Mechanobiol 10:431–444
Mikolajewicz N, Bishop N, Burghardt AJ et al (2019) HR-pQCT measures of bone microarchitecture predict fracture: systematic review and meta-analysis. J Bone Miner Res 35(3):446–459
Zhou B, Wang J, Yu YE, Zhang Z, Nawathe S, Nishiyama KK, Rosete FR, Keaveny TM, Shane E, Guo XE (2016) High-resolution peripheral quantitative computed tomography (HR-pQCT) can assess microstructural and biomechanical properties of both human distal radius and tibia: ex vivo computational and experimental validations. Bone 86:58–67
Ellouz R, Chapurlat R, van Rietbergen B, Christen P, Pialat J-B, Boutroy S (2014) Challenges in longitudinal measurements with HR-pQCT: evaluation of a 3D registration method to improve bone microarchitecture and strength measurement reproducibility. Bone 63:147–157
Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM (2013) Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res 28:313–324
Zhu TY, Hung VW, Cheung WH, Cheng JC, Qin L, Leung KS (2016) Value of measuring bone microarchitecture in fracture discrimination in older women with recent hip fracture: a case-control study with HR-pQCT. Sci Rep 6:34185
Acknowledgements
The authors would like to thank the participants and Sik Cheung Siu for his support and technical assistance during this study.
Funding
Tiev Miller and Charlotte San Lau Tsang were funded by post-graduate research studentships through the Department of Rehabilitation Sciences at The Hong Kong Polytechnic University (Grants RL27, RUNV). This study was substantially supported by a research grant provided to Marco Y. C. Pang by the Research Grants Council (General Research Fund: 151031/18 M).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
Ethical approval was obtained from the Human Research Ethics Review Committee of the University. All of the experimental procedures were conducted in accordance with the Helsinki Declaration for human experiments.
Consent to participate
The details of the study were explained to the participants before informed written consent was obtained.
Consent for publication
Consent to use information and data collected during the course of the study for educational and knowledge dissemination purposes was granted by the participants.
Conflicts of interest
None.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Miller, T., Qin, L., Hung, V.W.Y. et al. Gait speed and spasticity are independently associated with estimated failure load in the distal tibia after stroke: an HR-pQCT study. Osteoporos Int 33, 713–724 (2022). https://doi.org/10.1007/s00198-021-06191-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-021-06191-z