Abstract
Summary
The microstructure of autologous bone grafts from men over 50 years old and postmenopausal women undergoing spinal fusion were evaluated using micro-CT. We demonstrated postmenopausal women, especially those with osteoporosis (OP) presented more serious microarchitectural deterioration of bone grafts.
Purpose
This study was undertaken to determine microstructural properties of cancellous bone used as autologous bone grafts from osteoporosis patients undergoing lumbar fusion by comparing microstructural indices to controls.
Methods
Cancellous bone specimens from spinous processes were obtained from 41 postmenopausal women (osteoporosis women, n = 19; controls, n = 22) and 26 men over 50 years old (osteoporosis men, n = 8; controls, n = 18) during lumbar fusion surgery. The microstructural parameters were measured using micro-CT.
Results
Significant difference in bone volume fraction (BV/TV), specific bone surface (BS/BV), trabecular thickness (Tb.Th), and structure model index (SMI) value existed between postmenopausal women with OP and controls. Significant difference in trabecular number (Tb.N) existed between men over 50 years old with OP and controls. Postmenopausal women exhibited lower BV/TV, Tb.Th, and higher SMI value than men over 50 years old. Postmenopausal women with OP exhibited lower BV/TV, Tb.Th, and higher BS/BV than men over 50 years old with OP.
Conclusions
Post-menopausal women and older men with OP have worse bone quality in autografts than non-osteoporotic men and women. Postmenopausal women with OP presented serious microarchitectural deterioration in older population
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References
Boden SD (2002) Overview of the biology of lumbar spine fusion and principles for selecting a bone graft substitute. Spine 27(16 Suppl 1):S26–S31. https://doi.org/10.1097/00007632-200208151-00007
Curtis EM, Moon RJ, Dennison EM, Harvey NC, Cooper C (2016) Recent advances in the pathogenesis and treatment of osteoporosis. Clinical medicine 16(4):360–364. https://doi.org/10.7861/clinmedicine.16-4-360
Etebar S, Cahill DW (1999) Risk factors for adjacent-segment failure following lumbar fixation with rigid instrumentation for degenerative instability. J Neurosurg 90(2 Suppl):163–169
Giannoudis PV, Schneider E (2006) Principles of fixation of osteoporotic fractures. The Journal of bone and joint surgery British volume 88(10):1272–1278. https://doi.org/10.1302/0301-620X.88B10.17683
Guzman JZ, Feldman ZM, McAnany S, Hecht AC, Qureshi SA, Cho SK (2016) Osteoporosis in cervical spine surgery. Spine 41(8):662–668. https://doi.org/10.1097/BRS.0000000000001347
Lill CA, Hesseln J, Schlegel U, Eckhardt C, Goldhahn J, Schneider E (2003) Biomechanical evaluation of healing in a non-critical defect in a large animal model of osteoporosis. Journal of orthopaedic research : official publication of the Orthopaedic Research Society 21(5):836–842. https://doi.org/10.1016/S0736-0266(02)00266-8
Pang J, Ye M, Cao Y, Zheng Y, Guo H, Zhao Y, Zhan H, Shi Y (2014) Ovariectomy-induced osteopenia influences the middle and late periods of bone healing in a mouse femoral osteotomy model. Rejuvenation Res:141009011509000. https://doi.org/10.1089/rej.2014.1590
Kim CH, Kim YI, Choi CS, Park JY, Lee MS, Lee SI, Kim GS (2000) Prevalence and risk factors of low quantitative ultrasound values of calcaneus in Korean elderly women. Ultrasound Med Biol 26(1):35–40. https://doi.org/10.1016/S0301-5629(99)00126-X
Vogt MT, Rubin DA, San Valentin R, Palermo L, Kang JD, Donaldson WF 3rd, Nevitt M, Cauley JA (1999) Degenerative lumbar listhesis and bone mineral density in elderly women. The study of osteoporotic fractures. Spine 24(23):2536–2541. https://doi.org/10.1097/00007632-199912010-00016
Chang G, Boone S, Martel D, Rajapakse CS, Hallyburton RS, Valko M, Honig S, Regatte RR (2017) MRI assessment of bone structure and microarchitecture. Journal of magnetic resonance imaging: JMRI 46(2):323–337. https://doi.org/10.1002/jmri.25647
Cauley JA, Fullman RL, Stone KL, Zmuda JM, Bauer DC, Barrett-Connor E, Ensrud K, Lau EM, Orwoll ES, Mr OSRG (2005) Factors associated with the lumbar spine and proximal femur bone mineral density in older men. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 16(12):1525–1537. https://doi.org/10.1007/s00198-005-1866-8
Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359(9319):1761–1767. https://doi.org/10.1016/S0140-6736(02)08657-9
Chin DK, Park JY, Yoon YS, Kuh SU, Jin BH, Kim KS, Cho YE (2007) Prevalence of osteoporosis in patients requiring spine surgery: incidence and significance of osteoporosis in spine disease. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 18(9):1219–1224. https://doi.org/10.1007/s00198-007-0370-8
Chen H, Shoumura S, Emura S, Bunai Y (2008) Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 19(10):1473–1483. https://doi.org/10.1007/s00198-008-0593-3
Marinozzi F, Marinozzi A, Bini F, Zuppante F, Pecci R, Bedini R (2012) Variability of morphometric parameters of human trabecular tissue from coxo-arthritis and osteoporotic samples. Annali dell'Istituto superiore di sanita 48(1):19–25. https://doi.org/10.4415/ann_12_01_04
Banwart JC, Asher MA, Hassanein RS (1995) Iliac crest bone graft harvest donor site morbidity. A statistical evaluation. Spine 20(9):1055–1060. https://doi.org/10.1097/00007632-199505000-00012
Meinel L, Hofmann S, Betz O, Fajardo R, Merkle HP, Langer R, Evans CH, Vunjak-Novakovic G, Kaplan DL (2006) Osteogenesis by human mesenchymal stem cells cultured on silk biomaterials: comparison of adenovirus mediated gene transfer and protein delivery of BMP-2. Biomaterials 27(28):4993–5002. https://doi.org/10.1016/j.biomaterials.2006.05.021
Park SB, Lee YJ, Chung CK (2010) Bone mineral density changes after ovariectomy in rats as an osteopenic model: stepwise description of double dorso-lateral approach. Journal of Korean Neurosurgical Society 48(4):309–312. https://doi.org/10.3340/jkns.2010.48.4.309
Bini G, Bini F, Bedini R, Marinozzi A, Marinozzi F (2017) A topological look at human trabecular bone tissue. Math Biosci 288:159–165. https://doi.org/10.1016/j.mbs.2017.03.009
Chen F, Dai Z, Kang Y, Lv G, Keller ET, Jiang Y (2016) Effects of zoledronic acid on bone fusion in osteoporotic patients after lumbar fusion. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 27(4):1469–1476. https://doi.org/10.1007/s00198-015-3398-1
Li S, Guo H, Liu Y, Wu F, Zhang H, Zhang Z, Xie Z, Sheng Z, Liao E (2015) Relationships of serum lipid profiles and bone mineral density in postmenopausal Chinese women. Clin Endocrinol 82(1):53–58. https://doi.org/10.1111/cen.12616
Park SB, Chung CK (2011) Strategies of spinal fusion on osteoporotic spine. Journal of Korean Neurosurgical Society 49(6):317–322. https://doi.org/10.3340/jkns.2011.49.6.317
Lips P, Courpron P, Meunier PJ (1978) Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif Tissue Res 26(1):13–17. https://doi.org/10.1007/BF02013227
Vedi S, Compston JE, Webb A, Tighe JR (1983) Histomorphometric analysis of dynamic parameters of trabecular bone formation in the iliac crest of normal British subjects. Metabolic bone disease & related research 5(2):69–74. https://doi.org/10.1016/0221-8747(83)90004-8
Gilsanz V, Gibbens DT, Carlson M, Boechat MI, Cann CE, Schulz EE (1988) Peak trabecular vertebral density: a comparison of adolescent and adult females. Calcif Tissue Int 43(4):260–262. https://doi.org/10.1007/BF02555144
Sims NA, Martin TJ (2014) Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit. BoneKEy reports 3:481. https://doi.org/10.1038/bonekey.2013.215
Seeman E (2008) Bone quality: the material and structural basis of bone strength. J Bone Miner Metab 26(1):1–8. https://doi.org/10.1007/s00774-007-0793-5
Cooper C, Aihie A (1994) Osteoporosis: recent advances in pathogenesis and treatment. Q J Med 87(4):203–209
Zhang ZM, Li ZC, Jiang LS, Jiang SD, Dai LY (2010) Micro-CT and mechanical evaluation of subchondral trabecular bone structure between postmenopausal women with osteoarthritis and osteoporosis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 21(8):1383–1390. https://doi.org/10.1007/s00198-009-1071-2
Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK (2011) Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-based HR-pQCT study. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 26(1):50–62. https://doi.org/10.1002/jbmr.171
Ruff CB, Hayes WC (1988) Sex differences in age-related remodeling of the femur and tibia. Journal of orthopaedic research: official publication of the Orthopaedic Research Society 6(6):886–896. https://doi.org/10.1002/jor.1100060613
Duan Y, Wang XF, Evans A, Seeman E (2005) Structural and biomechanical basis of racial and sex differences in vertebral fragility in Chinese and Caucasians. Bone 36(6):987–998. https://doi.org/10.1016/j.bone.2004.11.016
Ding M, Hvid I (2000) Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone 26(3):291–295. https://doi.org/10.1016/S8756-3282(99)00281-1
Li J, Liu X, Zuo B, Zhang L (2016) The role of bone marrow microenvironment in governing the balance between Osteoblastogenesis and Adipogenesis. Aging and disease 7(4):514–525. https://doi.org/10.14336/AD.2015.1206
Chen H, Zhou X, Shoumura S, Emura S, Bunai Y (2010) Age- and gender-dependent changes in three-dimensional microstructure of cortical and trabecular bone at the human femoral neck. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 21(4):627–636. https://doi.org/10.1007/s00198-009-0993-z
Siu WS, Qin L, Cheung WH, Leung KS (2004) A study of trabecular bones in ovariectomized goats with micro-computed tomography and peripheral quantitative computed tomography. Bone 35(1):21–26. https://doi.org/10.1016/j.bone.2004.03.014
Stauber M, Muller R (2006) Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 17(4):616–626. https://doi.org/10.1007/s00198-005-0025-6
Ito M, Nishida A, Aoyagi K, Uetani M, Hayashi K, Kawase M (2005) Effects of risedronate on trabecular microstructure and biomechanical properties in ovariectomized rat tibia. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 16(9):1042–1048. https://doi.org/10.1007/s00198-004-1802-3
Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 25(7):1468–1486. https://doi.org/10.1002/jbmr.141
Eckstein F, Matsuura M, Kuhn V, Priemel M, Muller R, Link TM, Lochmuller EM (2007) Sex differences of human trabecular bone microstructure in aging are site-dependent. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 22(6):817–824. https://doi.org/10.1359/jbmr.070301
Lochmuller EM, Matsuura M, Bauer J, Hitzl W, Link TM, Muller R, Eckstein F (2008) Site-specific deterioration of trabecular bone architecture in men and women with advancing age. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 23(12):1964–1973. https://doi.org/10.1359/jbmr.080709
Boyce RW, Wronski TJ, Ebert DC, Stevens ML, Paddock CL, Youngs TA, Gundersen HJ (1995) Direct stereological estimation of three-dimensional connectivity in rat vertebrae: effect of estrogen, etidronate and risedronate following ovariectomy. Bone 16(2):209–213. https://doi.org/10.1016/8756-3282(94)00031-T
Odgaard A, Gundersen HJ (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14(2):173–182. https://doi.org/10.1016/8756-3282(93)90245-6
Brandi ML (2009) Microarchitecture, the key to bone quality. Rheumatology 48(Suppl 4):iv3–iv8. https://doi.org/10.1093/rheumatology/kep273
Stenderup K, Justesen J, Eriksen EF, Rattan SI, Kassem M (2001) Number and proliferative capacity of osteogenic stem cells are maintained during aging and in patients with osteoporosis. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 16(6):1120–1129. https://doi.org/10.1359/jbmr.2001.16.6.1120
Acknowledgements
This study was supported by grants from National Natural Science Foundation of China (81670804) and National Development and Reform Commission Foundation of Hunan Province (20131199).
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This study was approved by the medical ethics committee of the Second Xiangya Hospital of Central South University in China. All patients were informed and written consents of donating their bone samples were obtained.
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Xie, F., Zhou, B., Wang, J. et al. Microstructural properties of trabecular bone autografts: comparison of men and women with and without osteoporosis. Arch Osteoporos 13, 18 (2018). https://doi.org/10.1007/s11657-018-0422-z
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DOI: https://doi.org/10.1007/s11657-018-0422-z