Abstract
Bone remodeling is a physiological process by which bone constantly adapts its structure to changes in long-term loading manifested by interactions between osteoclasts and osteoblasts. This process can be influenced by many local factors, via effects on bone cells differentiation and proliferation, which are produced by bone cells and act in a paracrine or autocrine way. The aim of the current work is to provide mechanobiological finite elements modeling coupling both cellular activities and mechanical behavior in order to investigate age and gender effects on bone remodeling evolution. A series of computational simulations have been performed on a 2D and 3D human proximal femur. An age- and gender-related impacts on bulk density alteration of trabecular bone have been noticed, and the major actors responsible of this phenomenon have been then discussed.
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Alenghat FJ, Ingber DE (2002) Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Science’s STKE 2002(119): pe6
Barkaoui A (2012) Modélisation multiéchelle du comportement mécano-biologique de l’os humain : de l’ultrastructure au remodelage osseux. Thèse de doctorat Université d’Orléans, Orleans
Baste S, EL Guerjouma R, Gerard G (1989) Mesure de l’endommagement anisotrope d’un composite céramique-céramique par une méthode ultrasonore. Revue de physique appliquée 24(7):721–773
Bilezikian JP, Morishima A, Bell J, Grumbach MM (1998) Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med 339(9):599–603
Bonfoh N, Novinyo E, Lipinski P (2011) Modeling of bone adaptative behavior based on cells activities. Biomech Model Mechanobiol 10:789–798
Boskey A, Camacho PN (2007) FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials 28(15):2465–2478
Boskey AL, Coleman R (2010) Aging and Bone. International & American Associations for Dental Research. J Dent Res 89(12):1333–1348
Carani C, Qin K, Simoni M, Faustini-Fustini M, Serpente S, Boyd J, Korach KS, Simpson ER (1997) Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 337(2):91–95
Carden A, Morris MD (2000) Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt 5(3):259–268
Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB (2009) Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J Bone Miner Res 24(4):597–605
Cerroni AM, Tomlinson GA, Turnquist JE, Grynpas MD (2000) Bone mineral density, osteopenia, and osteoporosis in the rhesus macaques of Cayo Santiago. Am J Phys Anthropol 113(3):389–410
Chaboche JL (1981) Continuous damage mechanics—a tool to describe phenomena before crack initiation. Nucl Eng Des 64(2):233–247
Cho G, Wu Y, Ackerman JL (2003) Detection of hydroxyl ions in bone mineral by solid-state NMR spectroscopy. Science 300(5622):1123–1127
Cui J, Shen Y, Li R (2013) Estrogen synthesis and signaling pathways during ageing: from periphery to brain. Trends Mol Med 19(3):197–209
Currey JD (1969) The relationship between the stiffness and the mineral content of bone. J Biomech 2:477–480
Drummond AE (2006) The role of steroids in follicular growth. Reprod Biol Endocrinol 4, article 16
Findlay JK, Britt K, Kerr JB, O’Donnell L, Jones ME, Drummond AE, Simpson ER (2001) The road to ovulation: the role of estrogens. Reprod Fertil Dev 13(7–8):543–547
Finkelstein JS, Lee H, Burnett-Bowie S-AM, Carl PJ, Yu EW, Borges LF, Jones BF, Barry CV, Wulczyn KE, Thomas BJ, Leder BZ (2013) Gonadal steroids and body composition, strength, and sexual function in men. N Engl J Med 369(11):1011–1022
Fuchs RK, Allen MR, Ruppel ME, Diab T, Phipps RJ, Miller LM, Burr DB (2008) In situ examination of the time-course for secondary mineralization of Haversian bone using synchrotron Fourier transform infrared microspectroscopy. Matrix Biol 27(1):34–41
Gourion-Arsiquaud S, Faibish D, Myers E, Spevak L, Compston J, Hodsman A, Shane E, Recker RR, Boskey ER, Boskey AL (2009) Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res 24:1565–1571
García-Aznar JM, Rüeberg T, Doblaré M (2005) A bone remodelling model coupling microdamage growth and repair by 3D BMU-activity. Biomech Model Mechanobiol 4(2):147–167
Hambli R (2014) Connecting mechanics and bone cell activities in the bone remodeling process: an integrated finite element modeling. Front Bioeng Biotechnol 2:6
Hambli R (2016) Prediction of denosumab effects on bone remodeling: a combined pharmacokinetics and finite element modeling. J Mech Behav Biomed Mater 60:492–504
Hambli R, Soulat D, Gasser A, Benhamou CL (2009) Strain—damage coupled algorithm for cancellous bone mechano-regulation with spatial function influence. Comput Methods Appl Mech Eng 198(33):2673–2682
Hanschin RG, Stern WB (1995) X-ray diffraction studies on the lattice perfection of human bone apatite (Crista iliaca). Bone 16(4 Suppl):355S–363S
Hernandez CJ, Beaupré GS, Carter DR (2003) A theoretical analysis of the changes in basic multicellular unit activity at menopause. Bone 32(4):357–363
Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR (2001) Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore longitudinal study of aging. J Clin Endocrinol Metab 86(2):724–731
Henriksen K, Leeming DJ, Byrjalsen I, Nielsen RH, Sorensen MG, Dziegiel MH et al (2007) Osteoclasts prefer aged bone. Osteoporos Int 18(6):751–759
Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala B, Slooff TJ (1987) Adaptive bone-remodeling theory applied to prosthetic-design analysis. J Biomech 20(11–12):1135–1150
Hwee DT, Bodine SC (2009) Age-related deficit in load-induced skeletal muscle growth. J Gerontol A Biol Sci Med Sci 64(6):618–628
Ingber DE (2003) Mechanobiology and diseases of mechanotransduction. Ann Med 35(8):564–577
Jacob CR, Simo JC, Beaupre GS, Carter DR (1997) Adaptive bone remodeling incorporating simultaneous density and anisotropy considerations. J biomechanics 30(6):603–613
Jiang Y, Mishima H, Sakai S, Liu YK, Ohyabu Y, Uemura T (2008) Gene expression analysis of major lineage-defining factors in human bone marrow cells: effect of aging, gender, and age-related disorders. J Orthop Res 26:910–917
Jilka RL, Weinstein RS, Parfitt AM, Manolagas SC (2007) Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J Bone Miner Res 22:1492–1501
Kaufman JM, Vermeulen A (1997) Declining gonadal function in elderly men. Baillière’s Clin Endocrinol Metab 11(2):289–309
Komarova SV, Smith RJ, Dixon SJ, Sims SM, Wahl LM (2003) Mathematical model predicts a critical role for osteoclast autocrine regulation in the control of bone remodeling. Bone 33(2):206–215
Komarova SV (2005) Mathematical model of paracrine interactions between osteoclasts and osteoblasts predicts anabolic action of parathyroid hormone on bone. Endocrinology 146(8):3589–3595
Lee CC, Fletcher MD, Tarantal AF (2005) Effect of age on the frequency, cell cycle, and lineage maturation of rhesus monkey (Macacamulatta) CD34+ and hematopoietic progenitor cells. Pediatr Res 58:315–322
Lemaire V, Tobin FL, Greller LD, Cho CR, Suva LJ (2004) Modeling the interactions between osteoblast and osteoclast activities in bone remodeling. J Theor Biol 229(3):293–309
Lindeberg M (2008) Molecular and morphological studies of folliculogenesis, oocyte maturation and embryogenesis in humans. Doctoral degree Ph.D. KarolinskaInstitutet, Stockholm, Sweden
Liu PY, Beilin J, Meier C, Nguyen TV, Center JR, Leedman PJ, Seibel MJ, Eisman JA, Handelsman DJ (2007) Age-related changes in serum testosterone and sex hormone binding globulin in Australian men: longitudinal analyses of two geographically separate regional cohorts. J Clin Endocrinol Metab 92(9):3599–3603
Maldonado S, Borchers S, Findeisen R, Allgöwer F (2006) Mathematical modeling and analysis of force induced bone growth. Proceedings of 28th internationalk conference of IEEE-EMBC, New York, pp 3154–3160
Manolagas SC, Parfitt AM (2010) What old means to bone. Trends Endocrinol Metab 21:369–374
Martin GM, Sprague CA, Epstein CJ (1970) Replicative life-span of cultivated human cells. Effects of donor’s age, tissue, and genotype. Lab Invest 23:86–92
Martin BR (1992) A theory of fatigue damage accumulation and repair in cortical bone. J Orthop Res 10(6):818–825
Martin RB, Burr DB, Sharkey NA (1998) Skeletal tissue mechanics. Springer, New York
Martin RB (2003) Fatigue damage, remodeling, and the minimization of skeletal weight. J Theor Biol 220(2):271–276
Martin MJ, Buckland-Wright JC (2004) Sensitivity analysis of a novel mathematical model identifies factors determining bone resorption rates. Bone 35(4):918–928
Masood DN, Roach EC, Beauregard KG, Khalil RA (2010) Impact of sex hormone metabolism on the vascular effects of menopausal hormone therapy in cardiovascular disease. Curr Drug Metab 11(8):693–714
McLachlan R (2015) Androgen (testosterone) deficiency. Andrology Australia. https://www.andrologyaustralia.org
Meneghini C, Dalconi MC, Nuzzo S, Mobilio S, Wenk RH (2003) Rietveld refinement on x-ray diffraction patterns of bioapatite in human fetal bones. Biophys J 84(3):2021–2029
Morishima A, Grumbach MM, Simpson ER, Fisher C, Qin K (1995) Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab 80(12):3689–3698
Moroz A, Crane MC, Smith G, Wimpenny DI (2006) Phenomenological model of bone remodeling cycle containing osteocyte regulation loop. Biosystems 84(3):183–190
Nagaraja S, Couse TL, Guldberg RE (2005) Trabecular bone microdamage and microstructural stresses under uniaxial compression. J Biomech 38(4):707–716
Nardozza Júnior A, SzelbracikowskiSdos S, Nardi AC, Almeida JC (2011) Age-related testosterone decline in a Brazilian cohort of healthy military men. Int Braz J Urol 37(5):591–597
Ober C, Loisel DA, Gilad Y (2008) Sex-specific genetic architecture of human disease. Nat Rev Genet 9:911–922
Otsuka F, Moore RK, Wang X, Sharma S, Miyoshi T, Shimasaki S (2005) Essential role of the oocyte in estrogen amplification of follicle-stimulating hormone signaling in granulosa cells. Endocrinology 146(8):3362–3367
Pardo PS, Lopez MA, Boriek AM (2008) FOXO transcription factors are mechanosensitive and their regulation is altered with aging in the respiratory pump. Am J Physiol Cell Physiol 294(4):C1056–C1066
Patel SH, Murphy KP (2006) Fractures of the proximal femur: correlates of radiological evidence of osteoporosis. Skeletal Radiol 35(4):202–211
Pattin CA, Caler WE, Carter DR (1996) Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech 29(1):69–79
Pivonka P, Zimak J, Smith DW, Gardiner BS, Dunstan CR, Sims NA, Martin TJ, Mundy GR (2008) Model structure and control of bone remodeling: a theoretical study. Bone 43(2):249–263
Popat VB, Prodanov T, Calis KA, Nelson LM (2008) The menstrual cycle a biological marker of general health in adolescents. Ann N Y Acad Sci 1135:43–51
Rice KM, Desai DH, Preston DL, Wehner PS, Blough ER (2007) Uniaxial stretch-induced regulation of mitogen-activated protein kinase, Akt and p70 S6 kinase in the ageing Fischer 344 x Brown Norway rat aorta. Exp Physiol 92(5):963–970
Rieger R (2011) Modélisation mécano-biologique par éléments finis de l’os trabéculaire. Des activités cellulaires au remodelage osseux. Thèse de doctorat Uiversité d’Orléans, France
Rodriguez-Tolrà J, Torremadé J, di Gregorio S, Del Rio L, Franco E (2013) Effects of testosterone treatment on bone mineral density in men with testosterone deficiency syndrome. Andrology 1(4):570–575
Simpson ER (2003) Sources of estrogen and their importance. J Steroid Biochem Mol Biol 86(3–5):225–230
Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 331(16):1056–1061
Tosi LL, Boyan BD, Boskey AL (2005) Does sex matter in musculoskeletal health? The influence of sex and gender on musculoskeletal health. J Bone Jt Surg 87(7):1631–1647
Van Rietbergen B, Huiskes R, Eckstein F, Rüegsegger P (2003) Trabecular bone tissue strains in the healthy and osteoporotic human femur. J Bone Miner Res 18(10):1781–1788
Walker WH (2011) Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis 1(2):116–120
Wimpenny D, Moroz A (2007) On allosteric control model of bone turnover cycle containing osteocyte regulation loop. Biosystems 90(2):295–308
Wu M, Fannin J, Rice KM, Wang B, Blough ER (2011) Effect of aging on cellular mechanotransduction. Ageing Res Rev 10(1):1–15
Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS et al (2008) Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 7:335–343
Zioupos P, Casinos A (1998) Cumulative damage and the response of human bone in two-step loading fatigue. J Biomech 31(9):825–833
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Barkaoui, A., Ben Kahla, R., Merzouki, T. et al. Age and gender effects on bone mass density variation: finite elements simulation. Biomech Model Mechanobiol 16, 521–535 (2017). https://doi.org/10.1007/s10237-016-0834-x
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DOI: https://doi.org/10.1007/s10237-016-0834-x