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Current Osteoporosis Reports

Erschienen in:

27.04.2023

Fracture Toughness: Bridging the Gap Between Hip Fracture and Fracture Risk Assessment

verfasst von: Daniel Dapaah, Daniel R. Martel, Faezeh Iranmanesh, Corin Seelemann, Andrew C. Laing, Thomas Willett

Erschienen in: Current Osteoporosis Reports | Ausgabe 3/2023

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Abstract

Purpose of Review

This review surveys recent literature related to cortical bone fracture mechanics and its application towards understanding bone fragility and hip fractures.

Recent Findings

Current clinical tools for hip fracture risk assessment have been shown to be insensitive in some cases of elevated fracture risk leading to the question of what other factors account for fracture risk. The emergence of cortical bone fracture mechanics has thrown light on other factors at the tissue level that are important to bone fracture resistance and therefore assessment of fracture risk. Recent cortical bone fracture toughness studies have shown contributions from the microstructure and composition towards cortical bone fracture resistance. A key component currently overlooked in the clinical evaluation of fracture risk is the importance of the organic phase and water to irreversible deformation mechanisms that enhance the fracture resistance of cortical bone. Despite recent findings, there is an incomplete understanding of which mechanisms lead to the diminished contribution of the organic phase and water to the fracture toughness in aging and bone-degrading diseases. Notably, studies of the fracture resistance of cortical bone from the hip (specifically the femoral neck) are few, and those that exist are mostly consistent with studies of bone tissue from the femoral diaphysis.

Summary

Cortical bone fracture mechanics highlights that there are multiple determinants of bone quality and therefore fracture risk and its assessment. There is still much more to learn concerning the tissue-level mechanisms of bone fragility. An improved understanding of these mechanisms will allow for the development of better diagnostic tools and therapeutic measures for bone fragility and fracture.

Wiktorowicz ME, Goeree R, Papaioannou A, Adachi JD, Papadimitropoulos E. Economic implications of hip fracture: health service use, institutional care and cost in Canada. Osteoporos Int. 2001;12(4):271–8.PubMedCrossRef

Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 2006;17:1726–33.PubMedCrossRef

Wu AM, Bisignano C, James SL, Abady GG, Abedi A, Abu-Gharbieh E, et al. Global, regional, and national burden of bone fractures in 204 countries and territories, 1990–2019: a systematic analysis from the Global Burden of Disease Study 2019. Lancet Healthy Longev. 2021;2(9):e580–92.CrossRef

Kanis JA on behalf of the World Health Organization Scientific Group. Assessment of osteoporosis at the primary health care level. Technical Report. World Health Organization Collaborating Centre for Metabolic Bone Diseases, University of Sheffield, UK. 2007

Vestergaard P, Rejnmark L, Mosekilde L. Increased mortality in patients with a hip fracture-effect of pre-morbid conditions and post-fracture complications. Osteoporos Int. 2007;18(12):1583–93.PubMedCrossRef

Schattner A. The burden of hip fractures-why aren’t we better at prevention? QJM. 2018;111(11):765–7.PubMedCrossRef

Nikitovic M, Wodchis WP, Krahn MD, Cadarette SM. Direct health-care costs attributed to hip fractures among seniors: a matched cohort study. Osteoporos Int. 2013;24(2):659–69.PubMedCrossRef

Haentjens PMJ. Meta-analysis : excess mortality after hip fracture among older women and men. Ann Intern Med. 2010;152:380–90.PubMedPubMedCentralCrossRef

Ioannidis G, Papaioannou A, Hopman WM, Akhtar-Danesh N, Anastassiades T, Pickard L, et al. Relation between fractures and mortality: results from the Canadian Multicentre Osteoporosis Study. CMAJ 2009;181(5):265–71.

10.

Jiang HX, Majumdar SR, Dick DA, Moreau M, Raso J, Otto DD, et al. Development and initial validation of a risk score for predicting in-hospital and 1-year mortality in patients with hip fractures. J Bone Miner Res. 2005;20(3):494–500.PubMedCrossRef

11.

Cheng XG, Lowet G, Boonen S, Nicholson PHF, Brys P, Nijs J, et al. Assessment of the strength of proximal femur in vitro: relationship to femoral bone mineral density and femoral geometry. Bone. 1997;20(3):213–8.PubMedCrossRef

12.

Micha K, Aspenberg P, Siev H. Osteoporosis : the emperor has no clothes. J Intern Med. 2015;277:662–73.CrossRef

13.

Schuit SCE, Van Der Klift M, Weel AEAM, De Laet CEDH, Burger H, Seeman E, et al. Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam study. Bone. 2004;34(1):195–202.PubMedCrossRef

14.

Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes - a meta-analysis. Osteoporos Int. 2007;18(4):427–44.PubMedCrossRef

15.

Holzer G, Von Skrbensky G, Holzer LA, Pichl W. Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Mineral Res. 2009;24:468–74.CrossRef

16.

Hart NH, Nimphius S, Rantalainen T, Ireland A, Siafarikas A, Newton RU. Mechanical basis of bone strength: influence of bone material, bone structure and muscle action. J Musculoskelet Neuronal Interact. 2017;17(3):114.PubMedPubMedCentral

17.

Wolinsky FD, Bentler SE, Liu L, Obrizan M, Cook EA, Wright KB, et al. Recent hospitalization and the risk of hip fracture among older Americans. J Gerontol - Ser Biol Sci Med Sci. 2009;64(2):249–55.CrossRef

18.

Robinovitch SN, Hayes WC, McMahon TA. Prediction of femoral impact forces in falls on the hip. J Biomech Eng. 1991;113:366–74.PubMedCrossRef

19.

Pinilla TP, Boardman KC, Bouxsein ML, Myers ER, Hayes WC. Impact direction from a fall influences the failure load of the proximal femur as much as age-related bone loss. Calcif Tissue Int. 1996;58(4):231–5.PubMedCrossRef

20.

Masud T, Morris RO. Epidemiology of falls. Age Ageing. 2001;30(S4):3–7.PubMedCrossRef

21.

Nevitt MC, Cummings SR. Type of fall and risk of hip and wrist fractures: the study of osteoporotic fractures. J Am Geriatr Soc. 1993;41(11):1226–34.PubMedCrossRef

22.

Jean S, O’Donnell S, Lagacé C, Walsh P, Bancej C, Brown JP, et al. Trends in hip fracture rates in Canada: an age-period-cohort analysis. J Bone Mineral Res. 2013;28(6):1283–9.CrossRef

23.

Hendrickx G, Boudin E, Van Hul W. A look behind the scenes: the risk and pathogenesis of primary osteoporosis. Nat Rev Rheumatol 2015;11(8):462–74.

24.

Santos L, Elliott-Sale KJ, Sale C. Exercise and bone health across the lifespan. Biogerontol. 2017;18(6):931–46.CrossRef

25.

Caillet P, Klemm S, Ducher M, Aussem A, Schott AM. Hip fracture in the elderly: a re-analysis of the EPIDOS study with causal Bayesian networks. PLoS ONE. 2015;10(3):1–12.CrossRef

26.

Kanis JA, McCloskey E, Johansson H, Oden A, Leslie WD. FRAX® with and without bone mineral density. Calcif Tissue Int. 2012;90(1):1–13.PubMedCrossRef

27.

Aspray TJ. Fragility fracture: Recent developments in risk assessment. Ther Adv Musculoskelet Dis. 2015;7:17–25.PubMedPubMedCentralCrossRef

28.

Dagan N, Cohen-Stavi C, Leventer-Roberts M, Balicer RD. External validation and comparison of three prediction tools for risk of osteoporotic fractures using data from population based electronic health records: tetrospective cohort study. BMJ 2017;356.

29.

Bolland MJ, Siu AT, Mason BH, Horne AM, Ames RW, Grey AB, et al. Evaluation of the FRAX and Garvan fracture risk calculators in older women. J Bone Miner Res. 2011;26(2):420–7.PubMedCrossRef

30.

Fraser LA, Langsetmo L, Berger C, Ioannidis G, Goltzman D, Adachi JD, et al. Fracture prediction and calibration of a Canadian FRAX® tool: a population-based report from CaMos. Osteoporos Int. 2011;22(3):829–37.PubMedCrossRef

31.

Giangregorio LM, Leslie WD, Lix LM, Johansson H, Oden A, McCloskey E, et al. FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res. 2012;27(2):301–8.PubMedCrossRef

32.

Järvinen TLN, Michaëlsson K, Aspenberg P, Sievänen H. Osteoporosis: the emperor has no clothes. J Intern Med. 2015;277(6):662–73.PubMedPubMedCentralCrossRef

33.

Courtney AC, Wachtel EF, Myers ER, Hayes WC. Effects of loading rate on strength of the proximal femur. Calcif Tissue Int. 1994;55(1):53–8.PubMedCrossRef

34.

Roberts BJ, Thrall E, Muller JA, Bouxsein ML. Comparison of hip fracture risk prediction by femoral aBMD to experimentally measured factor of risk. Bone. 2010;46(3):742–6.PubMedCrossRef

35.

Bachmann KN, Fazeli PK, Lawson EA, Russell BM, Riccio AD, Meenaghan E, et al. Comparison of hip geometry, strength, and estimated fracture risk in women with anorexia nervosa and overweight/obese women. J Clin Endocrinol Metab. 2014;99(12):4664–73.PubMedPubMedCentralCrossRef

36.

Hansen S, Jensen JEB, Ahrberg F, Hauge EM, Brixen K. The combination of structural parameters and areal bone mineral density improves relation to proximal femur strength: an in vitro study with high-resolution peripheral quantitative computed tomography. Calcif Tissue Int. 2011;89(4):335–46.PubMedCrossRef

37.

Bouxsein ML, Seeman E. Quantifying the material and structural determinants of bone strength. Best Pract Res Clin Rheumatol. 2009;23(6):741–53. https://doi.org/10.1016/j.berh.2009.09.008.CrossRefPubMed

38.

Dinçel VE, Şengelen M, Sepici V, Çavuşoǧlu T, Sepici B. The association of proximal femur geometry with hip fracture risk. Clin Anat. 2008;21(6):575–80.PubMedCrossRef

39.

Chappard C, Bousson V, Bergot C, Mitton D, Marchadier A, Moser T, et al. Prediction of femoral fracture load: cross-sectional study of texture analysis and geometric measurements on plain radiographs versus bone mineral density. Radiol. 2010;255(2):536–43.CrossRef

40.

Elbuken F, Baykara M, Ozturk C. Standardisation of the neck-shaft angle and measurement of age-, gender- and BMI-related changes in the femoral neck using DXA. Singapore Med J. 2012;53(9):587–90.PubMed

41.

Maeda Y, Sugano N, Saito M, Yonenobu K. Comparison of femoral morphology and bone mineral density between femoral neck fractures and trochanteric fractures. Clin Orthop Relat Res. 2011;469(3):884–9.PubMedCrossRef

42.

Partanen J, Jämsä T, Jalovaara P. Influence of the upper femur and pelvic geometry on the risk and type of hip fractures. J Bone Miner Res. 2001;16(8):1540–6.PubMedCrossRef

43.

Dufour AB, Roberts B, Broe KE, Kiel DP, Bouxsein ML, Hannan MT. The factor-of-risk biomechanical approach predicts hip fracture in men and women: the Framingham study. Osteoporos Int. 2012;23(2):513–20.PubMedCrossRef

44.

• Martel DR, Lysy M, Laing AC. Predicting population level hip fracture risk: a novel hierarchical model incorporating probabilistic approaches and factor of risk principles. Comput Methods Biomech Biomed Engin. 2020;23(15):1201–14. https://doi.org/10.1080/10255842.2020.1793331. (A recent study that used a hierarchical probabilistic model to predict population-level hip fracture risk based on factor of risk (FOR) principles.•)CrossRefPubMed

45.

Le Corroller T, Halgrin J, Pithioux M, Guenoun D, Chabrand P, Champsaur P. Combination of texture analysis and bone mineral density improves the prediction of fracture load in human femurs. Osteoporos Int. 2012;23(1):163–9.PubMedCrossRef

46.

Luo Y, Sarvi MN, Sun P, Leslie WD, Ouyang J. Prediction of impact force in sideways fall by image-based subject-specific dynamics model. Int Biomech. 2014;1(1):1–14. https://doi.org/10.1080/23310472.2014.975745.CrossRef

47.

• Luo Y. On challenges in clinical assessment of hip fracture risk using image-based biomechanical modelling: a critical review. J Bone Miner Metab. 2021;39(4):523–33. https://doi.org/10.1007/s00774-020-01198-8. (A critical review of image-based biomechanical modeling to assess hip fracture risk that points to the importance of bone quality assessment.•)CrossRefPubMed

48.

C. Cowin, JJ Telega. Bone mechanics handbook, 2nd edition. Applied Mechanics Reviews. 2003;56:61–63

49.

Boskey AL, Coleman R. Aging and bone. J Dent Res. 2010;89(12):1333–48.PubMedPubMedCentralCrossRef

50.

Burr DB. Changes in bone matrix properties with aging. Bone. 2019; 85–93. https://doi.org/10.1016/j.bone.2018.10.010

51.

Zioupos P, Currey JD. Changes in the stiffness, strength, and toughness of human cortical bone with age. 1998;22(1):57–66.

52.

Vinz H. Change in the mechanical properties of human compact bone tissue upon aging. Polymer Mechanics. 1975;11(4):568–71.CrossRef

53.

Evans GP, Behiri JC, Vaughan LC, Bonfield W. The response of equine cortical bone to loading at strain rates experienced in vivo by the galloping horse. Equine Vet J. 1992;24(2):125–8.PubMedCrossRef

54.

• Zioupos P, Kirchner HOK, Peterlik H. Ageing bone fractures: The case of a ductile to brittle transition that shifts with age. Bone. 2020;131:115176. https://doi.org/10.1016/j.bone.2019.115176. ( An interesting study which shows how older bone’s ductile to brittle transition occurs at physiological relevant rates as opposed to the younger bone which is most fracture resistant at these rates. Combined with the reduced capacity of older bone to plastically deformed this might further explain why older bone is brittle.)CrossRefPubMed

55.

Hansen U, Zioupos P, Simpson R, Currey JD, Hynd D. The effect of strain rate on the mechanical properties of human cortical bone. J Biomech Eng. 2008;130(1):1–8.CrossRef

56.

Katzenberger MJ, Albert DL, Agnew AM, Kemper AR. Effects of sex, age, and two loading rates on the tensile material properties of human rib cortical bone. J Mech Behav Biomed Mater. 2020;102:103410.PubMedCrossRef

57.

McCalden RW, McGeough JA, Barker MB. Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity mineralization and microstructure. J Bone Joint Surg Am. 1993;75(8):1193–205.PubMedCrossRef

58.

Burstein AH, Reilly DT, Martens M. Aging of bone tissue: mechanical properties. J Bone Joint Surg Am. 1976;58(1):82–6.PubMedCrossRef

59.

Ritchie RO. Toughening materials: Enhancing resistance to fracture. Phil Trans Royal Soc A. 2021;379(2203).

60.

Hernandez CJ, van der Meulen MCH. Understanding bone strength is not enough. J Bone Miner Res. 2017;32(6):1157–62.PubMedCrossRef

61.

Anderson TL. Fracture mechanics: fundamentals and applications. Boca Raton: CRC Press LLC; 2005.CrossRef

62.

Pruitt LA, Chakravartula AM. Mechanics of biomaterials: fundamental principles for implant design. New York: Cambridg University Press; 2011.CrossRef

63.

Bonfield W, Datta PK. Fracture toughness of compact bone. J Biomech. 1976;9(3):131–132.

64.

Behiri JC, Bonfield W. Orientation dependence of the fracture mechanics of cortical bone. J Biomech 1989;22(8/9):863–72.

65.

Yeni YN, Brown CU, Wang Z, Norman TL. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone. 1997;21(5):453–9.PubMedCrossRef

66.

Yeni YN, Norman TL. Fracture toughness of human femoral neck: effect of microstructure, composition, and age. Bone. 2000;26(5):499–504.PubMedCrossRef

67.

Feng Z, Rho J, Han S, Ziv I. Orientation and loading condition dependence of fracture toughness in cortical bone. Mater Sci Eng, C. 2000;11:41–6.CrossRef

68.

Lucksanasombool P, Higgs WAJ, Higgs RJED, Swain MV. Fracture toughness of bovine bone: Influence of orientation and storage media. Biomater. 2001;22(23):3127–32.CrossRef

69.

Yang QD, Cox BN, Nalla RK, Ritchie RO. Re-evaluating the toughness of human cortical bone. Bone. 2006;38(6):878–87.PubMedCrossRef

70.

Launey ME, Buehler MJ, Ritchie RO. On the mechanistic origins of toughness in bone. Annu Rev Mater Res. 2010;40(1):25–53. https://doi.org/10.1146/annurev-matsci-070909-104427.CrossRef

71.

ASTM Standard E1820-18. Standard test method for measurement of fracture toughness. ASTM Book of Standards. 2013;1–54

72.

Granke M, Makowski AJ, Uppuganti S, Does MD, Nyman JS. Identifying novel clinical surrogates to assess human bone fracture toughness. journal of bone and mineral research. 2015;30(7):1290–300.

73.

• Willett TL, Dapaah DY, Uppuganti S, Granke M, Nyman JS. Bone collagen network integrity and transverse fracture toughness of human cortical bone. Bone. 2019;1(120):187–93. (This study demonstrates that collagen network connectivity degradation is an important determinant in reduced cortical bone fracture toughness, highlighting the need to better understand mechanisms of collagen network connectivity degradation for better fragility assessment.)CrossRef

74.

• Gauthier R, Follet H, Langer M, Meille S, Chevalier J, Rongiéras F, et al. Strain rate influence on human cortical bone toughness: a comparative study of four paired anatomical sites. J Mech Behav Biomed Mater. 2017;71:223–30. (One of the few studies to measure the fracture toughness of cortical bone tissue from the femoral neck at quasi-static and fall-related loading rates.)

75.

• Dapaah D, Martel DR, Laing AC, Willett TL. The impact of fall-related loading rate on the formation of micro-damage in human cortical bone fracture. J Biomech. 2022;1:142. (A recent study of the effects of loading rate on the formation of the microdamage process zone during cortical bone fracture.)

76.

• Dapaah D, Willett T. A critical evaluation of cortical bone fracture toughness testing methods. J Mech Behav Biomed Mater. 2022;1:134. (A recent methodology study that examined the effects of how the crack extension is measured during SENB fracture toughness tests of cortical bone.)

77.

Yan J, Mecholsky JJ, Clifton KB. How tough is bone ? Application of elastic – plastic fracture mechanics to bone. Bone. 2007;40:479–84.PubMedCrossRef

78.

An B, Liu Y, Arola D, Zhang D. Fracture toughening mechanism of cortical bone : an experimental and numerical approach. J Mech Behav Biomed Mater. 2011;4(7):983–92. https://doi.org/10.1016/j.jmbbm.2011.02.012.CrossRefPubMed

79.

Willett TL, Burton B, Woodside M, Wang Z, Gaspar A, Attia T. γ-Irradiation sterilized bone strengthened and toughened by ribose pre-treatment. J Mech Behav Biomed Mater. 2015;44:147–55. https://doi.org/10.1016/j.jmbbm.2015.01.003.CrossRefPubMed

80.

Woodside M, Willett TL. Elastic – plastic fracture toughness and rising J R -curve behavior of cortical bone is partially protected from irradiation – sterilization-induced degradation by ribose protectant. J Mech Behav Biomed Mater. 2016;64:53–64.PubMedCrossRef

81.

Singh J, Sharma NK, Sarker MD, Naghieh S, Sehgal SS, Chen DXB. Assessment of elastic-plastic fracture behavior of cortical bone using a small punch testing technique. J Biomech Eng. 2020;142(1):1–9.CrossRef

82.

Yadav RN, Uniyal P, Sihota P, Kumar S, Dhiman V, Goni VG, et al. Effect of ageing on microstructure and fracture behavior of cortical bone as determined by experiment and extended finite element method (XFEM). Med Eng Phys. 2021;93:100–12. https://doi.org/10.1016/j.medengphy.2021.05.021.CrossRefPubMed

83.

Li JZ, Wang X, He LT, Yan FX, Zhang N, Ren CX, et al. Strength–fracture toughness synergy strategy in ostrich tibia’s compact bone: hierarchical and gradient. J Mech Behav Biomed Mater. 2022;131:105262

84.

Koester KJ, Ager JW, Ritchie RO. The true toughness of human cortical bone measured with realistically short cracks. Nat Mater. 2008;7(8):672–7.PubMedCrossRef

85.

Zimmermann EA, Gludovatz B, Schaible E, Busse B, Ritchie RO. Fracture resistance of human cortical bone across multiple length-scales at physiological strain rates. Biomater. 2014;35(21):5472–81. https://doi.org/10.1016/j.biomaterials.2014.03.066.CrossRef

86.

Shin M, Zhang M, vom Scheidt A, Pelletier MH, Walsh WR, Martens PJ, et al. Impact of test environment on the fracture resistance of cortical bone. J Mech Behav Biomed Mater. 2022;129:105155.

87.

Maghsoudi-Ganjeh M, Wang X, Zeng X. Computational investigation of the effect of water on the nanomechanical behavior of bone. J Mech Behav Biomed Mater. 2020;1:101.

88.

Nyman JS, Gorochow LE, Adam Horch R, Uppuganti S, Zein-Sabatto A, Manhard MK, et al. Partial removal of pore and loosely bound water by low-energy drying decreases cortical bone toughness in young and old donors. J Mech Behav Biomed Mater. 2013;22:136–45. https://doi.org/10.1016/j.jmbbm.2012.08.013.CrossRefPubMed

89.

Wasserman N, Brydges B, Searles S, Akkus O. In vivo linear microcracks of human femoral cortical bone remain parallel to osteons during aging. Bone. 2008;43(5):856–61.PubMedCrossRef

90.

Diab T, Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone. 2007;40(3):612–8.PubMedCrossRef

91.

• Gauthier R, Langer M, Follet H, Olivier C, Gouttenoire PJ, Helfen L, et al. Influence of loading condition and anatomical location on human cortical bone linear micro-cracks. J Biomech. 2019;6(85):59–66. (Another study by Gauthier et al. that examined the fracture behavior of bone tissue from the human femoral neck. They showed that fall-like loading rates resulted in reduced accumulation of linear micro-cracks as compared to quasi-static loading rates for the femoral neck.)CrossRef

92.

Diab T, Condon KW, Burr DB, Vashishth D. Age-related change in the damage morphology of human cortical bone and its role in bone fragility. Bone. 2006;38(3):427–31.PubMedCrossRef

93.

Willett T, Josey D, Xing R, Lu Z, Minhas G, Montesano J. The micro-damage process zone during transverse cortical bone fracture : no ears at crack growth initiation. J Mech Behav Biomed Mater. 2017;74:371–82. https://doi.org/10.1016/j.jmbbm.2017.06.029.CrossRefPubMed

94.

Dapaah D, Badaoui R, Bahmani A, Montesano J, Willett T. Modelling the micro-damage process zone during cortical bone fracture. Eng Fract Mech. 2019;2020(224):106811.

95.

Dapaah D, Montesano J, Willett T. The importance of rate-dependent effects in modelling the micro-damage process zone in cortical bone fracture. Eng Fract Mech. 2021;264:108351. https://doi.org/10.1016/j.engfracmech.2022.108351.CrossRef

96.

97.

Currey JD, Brear K, Zioupos P. Strain rate dependence of work of fracture tests on bone and similar tissues: Reflections on testing methods and mineral content effects. Bone. 2019;128:115038.PubMedCrossRef

98.

Nalla RK, Kinney JH, Ritchie RO. Mechanistic fracture criteria for the failure of human cortical bone. Nat Mater. 2003;2:164–8.

99.

Nalla RK, Kruzic JJ, Ritchie RO. On the origin of the toughness of mineralized tissue : microcracking or crack bridging ? Bone. 2004;34:790–8.PubMedCrossRef

100.

Vashishth D. Rising crack-growth-resistance behavior in cortical bone: Implications for toughness measurements. J Biomech. 2004;37(6):943–6.PubMedCrossRef

101.

• Seelemann CA, Willett TL. Empirical evidence that bone collagen molecules denature as a result of bone fracture. J Mech Behav Biomed Mater. 2022;131:105220. https://doi.org/10.1016/j.jmbbm.2022.105220. (This study presents the first empirical evidence that bone collage molecules unravel or denature as a result of bone fracture and suggests a potentially important toughening mechanism that may be degraded in aging and disease. Certainly, a hypothesis requiring more investigation.•)CrossRefPubMed

102.

Granke M, Makowski AJ, Uppuganti S, Nyman JS. Prevalent role of porosity and osteonal area over mineralization heterogeneity in the fracture toughness of human cortical bone. J Biomech. 2016;49(13):2748–55. https://doi.org/10.1016/j.jbiomech.2016.06.009.CrossRefPubMedPubMedCentral

103.

Gauthier R, Follet H, Langer M, Gineyts E, Rongiéras F, Peyrin F, et al. Relationships between human cortical bone toughness and collagen cross-links on paired anatomical locations. Bone. 2018;112:202–11. https://doi.org/10.1016/j.bone.2018.04.024.CrossRefPubMed

104.

Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195–214.PubMedCrossRef

105.

Poundarik AA, Wu PC, Evis Z, Sroga GE, Ural A, Rubin M, et al. A direct role of collagen glycation in bone fracture. J Mech Behav Biomed Mater. 2015;52:120–30.PubMedPubMedCentralCrossRef

106.

Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. 2001;28(2):195–201.PubMedCrossRef

107.

Willett TL, Sutty S, Gaspar A, Avery N, Grynpas M. In vitro non-enzymatic ribation reduces post-yield strain accommodation in cortical bone. Bone. 2013;52(2):611–22. https://doi.org/10.1016/j.bone.2012.11.014.CrossRefPubMed

108.

Zioupos P, Currey JD, Hamer AJ. The role of collagen in the declining mechanical properties of aging human cortical bone. J Biomed Mater Res. 1999;45(2):108–16.PubMedCrossRef

109.

Wang X, Bank RA, TeKoppele JM, Mauli AC. The role of collagen in determining bone mechanical properties. J Orthop Res. 2001;19(6):1021–6.PubMedCrossRef

110.

Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone. 2002;31(1):1–7.PubMed

111.

• Thomas CJ, Cleland TP, Sroga GE, Vashishth D. Accumulation of carboxymethyl-lysine (CML) in human cortical bone. Bone. 2018;110:128–33. (The first study demonstrating a negative relationship between AGE adduct content and fracture toughness of human cortical bone.)PubMedPubMedCentralCrossRef

112.

•• Arakawa S, Suzuki R, Kurosaka D, Ikeda R, Hayashi H, Kayama T, et al. Mass spectrometric quantitation of AGEs and enzymatic crosslinks in human cancellous bone. Sci Rep. 2020;10(1):18774. https://doi.org/10.1038/s41598-020-75923-8. (This study highlights the abundance of non-crosslinking AGEs (AGE adducts) as compared to crosslinking AGEs albeit for cancellous bone. This raises the concern for a better understanding of the impact of AGE adducts on the structure and function of the collagen network specifically in relation to skeletal fragility.••)CrossRefPubMedPubMedCentral

113.

• Willett TL, Dapaah DY, Tupy J, Uppuganti S, Nyman JS. N-ε-(carboxymethyl)lysine correlates with the degradation of human cortical bone fracture resistance. Proceedings from the Annual Meeting of the Orthopaedic Research Society 2022: Paper no. 435. (A second study demonstrating a negative relationship between CML, an AGE adduct, and cortical bone fracture toughness.)

114.

•• Willett TL, Voziyan P, Nyman JS. Causative or associative: a critical review of the role of advanced glycation end-products in bone fragility. Bone. 2022;163:116485. (A timely critical review of the evidence for and against a role for AGEs in bone fragility that highlights the many gaps and unanswered questions and concerns.)

115.

Icer MA, Gezmen-Karadag M. The multiple functions and mechanisms of osteopontin. Clin Biochem. 2018;1(59):17–24.CrossRef

116.

Cavelier S, Dastjerdi AK, Mckee MD, Barthelat F. Bone toughness at the molecular scale: a model for fracture toughness using crosslinked osteopontin on synthetic and biogenic mineral substrates. Bone. 2018;110:304–11. https://doi.org/10.1016/j.bone.2018.02.022.CrossRefPubMed

117.

Poundarik AA, Diab T, Sroga GE, Ural A, Boskey AL, Gundberg CM, et al. Dilatational band formation in bone. Proc Natl Acad Sci. 2012;109(47):19178–83. https://doi.org/10.1073/pnas.1201513109.CrossRefPubMedPubMedCentral

118.

Morgan S, Poundarik AA, Vashishth D. Do non-collagenous proteins affect skeletal mechanical properties? Calcif Tissue Int. 2015;97(3):281–91. https://doi.org/10.1007/s00223-015-0016-3.CrossRefPubMedPubMedCentral

119.

Sroga GE, Vashishth D. Effects of bone matrix proteins on fracture and fragility in osteoporosis. Curr Osteoporos Rep. 2012;10(2):141–50. https://doi.org/10.1007/s11914-012-0103-6.CrossRefPubMedPubMedCentral

120.

Nikel O, Poundarik AA, Bailey S, Vashishth D. Structural role of osteocalcin and osteopontin in energy dissipation in bone. J Biomech. 2018;80:45–52.

121.

Karim L, Kwaczala A, Vashishth D, Judex S. Dose-dependent effects of pharmaceutical treatments on bone matrix properties in ovariectomized rats. Bone Rep 2021;15:101137

122.

Wang Z, Vashishth D, Picu RC. Bone toughening through stress-induced non-collagenous protein denaturation. Biomech Model Mechanobiol. 2018;17(4):1093–106. https://doi.org/10.1007/s10237-018-1016-9.CrossRefPubMed

123.

Tavakol M, Vaughan TJ. Energy dissipation of osteopontin at a HAp mineral interface: Implications for bone biomechanics. Biophys J. 2022;121(2):228–36.PubMedCrossRef

124.

• Thomas CJ, Cleland TP, Zhang S, Gundberg CM, Vashishth D. Identification and characterization of glycation adducts on osteocalcin. Anal Biochem. 2017;15(525):46–53. (A fascinating in vitro study that suggests how non-collagenous proteins may be modified by glycation. This could alter the fracture resistance of bone.)CrossRef

125.

• Du JY, Flanagan CD, Bensusan JS, Knusel KD, Akkus O, Rimnac CM. Raman biomarkers are associated with cyclic fatigue life of human allograft cortical bone. J Bone Joint Surg. 2019;101(17):e85. (One of a series of papers that demonstrate how Raman methods can detect changes in the organic phase of bone that correlate with fracture resistance.)PubMedCrossRef

126.

• Unal M, Jung H, Akkus O. Novel raman spectroscopic biomarkers indicate that postyield damage denatures bone’s collagen. J Bone Miner Res. 2016;31(5):1015–25. (One of a series of papers that demonstrate how Raman methods can detect changes in the organic phase of bone that correlate with fracture resistance.)PubMedCrossRef

127.

Unal M, Uppuganti S, Timur S, Mahadevan-Jansen A, Akkus O, Nyman JS. Assessing matrix quality by Raman spectroscopy helps predict fracture toughness of human cortical bone. Sci Rep. 2019;9(1):1–13. https://doi.org/10.1038/s41598-019-43542-7.CrossRef

128.

• Unal M. Raman spectroscopic determination of bone matrix quantity and quality augments prediction of human cortical bone mechanical properties. J Biomech. 2021;15(119):110342. (One of a series of papers that demonstrate how Raman methods can detect changes in the organic phase of bone that correlate with fracture resistance.)CrossRef

129.

• Makowski AJ, Granke M, Ayala OD, Uppuganti S, Mahadevan-Jansen A, Nyman JS. Applying full spectrum analysis to a raman spectroscopic assessment of fracture toughness of human cortical bone. Appl Spectrosc. 2017;71(10):2385–94. (One of a series of papers that demonstrate how Raman methods can detect changes in the organic phase of bone that correlate with fracture resistance.)PubMedPubMedCentralCrossRef

130.

Inzana JA, Maher JR, Takahata M, Schwarz EM, Berger AJ, Awad HA. Bone fragility beyond strength and mineral density: Raman spectroscopy predicts femoral fracture toughness in a murine model of rheumatoid arthritis. J Biomech. 2013;46(4):723–30. https://doi.org/10.1016/j.jbiomech.2012.11.039.CrossRefPubMed

131.

Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res. 2007;22(3):465–75.PubMedCrossRef

132.

Brown CU, Yeni YN, Norman TL. Fracture toughness is dependent on bone location--a study of the femoral neck, femoral shaft, and the tibial shaft. J Biomed Mater Res. 2000;49(3):380–9.

133.

Yeni TL, Norman YN. Fracture toughness of human femoral neck cortical bone is reduced with age and with increased osteon eccentricity. Eng Comp Sci Facult Present. 104

134.

Gauthier R, Langer M, Follet H, Olivier C, Gouttenoire PJ, Helfen L, et al. 3D micro structural analysis of human cortical bone in paired femoral diaphysis, femoral neck and radial diaphysis. J Struct Biol. 2018;204(2):182–90.PubMedCrossRef

135.

Jenkins T, Katsamenis OL, Andriotis OG, Coutts LV, Carter B, Dunlop DG, et al. The inferomedial femoral neck is compromised by age but not disease: fracture toughness and the multifactorial mechanisms comprising reference point microindentation. J Mech Behav Biomed Mater. 2017;1(75):399–412.CrossRef

136.

Osima M, Kral R, Borgen TT, Høgestøl IK, Joakimsen RM, Eriksen EF, et al. Women with type 2 diabetes mellitus have lower cortical porosity of the proximal femoral shaft using low-resolution CT than nondiabetic women, and increasing glucose is associated with reduced cortical porosity. Bone. 2017;1(97):252–60.CrossRef

137.

• Acevedo C, Stadelmann VA, Pioletti DP, Alliston T, Ritchie RO. Fatigue as the missing link between bone fragility and fracture. Nat Biomed Eng. 2018;2(2):62–71. https://doi.org/10.1038/s41551-017-0183-9. (This article makes a strong case for why fatigue resistance is relevant to understanding bone fragility and assessing fracture risk as a whole.•)CrossRefPubMed

Titel: Fracture Toughness: Bridging the Gap Between Hip Fracture and Fracture Risk Assessment
verfasst von: Daniel Dapaah
Daniel R. Martel
Faezeh Iranmanesh
Corin Seelemann
Andrew C. Laing
Thomas Willett
Publikationsdatum: 27.04.2023
Verlag: Springer US
Erschienen in: Current Osteoporosis Reports / Ausgabe 3/2023
Print ISSN: 1544-1873
Elektronische ISSN: 1544-2241
DOI: https://doi.org/10.1007/s11914-023-00789-4

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