Bone mineralization as studied by small-angle x-ray scattering

Fratzl, P.; Schreiber, S.; Klaushofer, K.

Affiliations

¹Materials Physics Institute, University of Vienna, Strudlhofgasse 4, A- 1090 Wien, Austria

²Ludwig Boltzmunn Institute for Osteology, 4th Med. Dept., Hanusch Hospitul, A-1 140 Wien, Austria

³Present address: Institut fur Materialphysik der Universität Wien, Strudlhofgasse 4, A-1090 Wien, Austria

Abstract and keywords

Small-angle x-ray scattering (SAXS) can provide information on mean size, predominant orientation and typical shape of mineral crystals in bone. In this paper, recent developments of this technique for application in bone research are reviewed. Then the structure of the collagen/mineral composite in bone, as determined by SAXS, is compared for a number of species. The thickness of the mineral crystals was found to increase with age up to a value around 3 to 4 nanometers in adult animals, depending on the species. The SAXS results also suggest the existence of needle-shaped mineral crystals in mouse or rat bone and more plate-shaped crystals in other tissues like adult human bone or mineralized turkey leg tendon.

Keywords: Collagen; hydroxyapatite; biomineralization; calcified tissue; diffraction

Links

DOI: 10.3109/03008209609005268

PubMed: 9084633

History

Received: 1995-11-11

Revised: 1995-11-25

Accepted: 1996-02-06

Cited Works (7)

Year	Entry
1993	Landis WJ, Song MJ, Leith A, McEwen L, McEwen BF. Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high-voltage electron microscopic tomography and graphic image reconstruction. J Struct Biol. January 1993;110(1):39-54.
1996	Fratzl P, Schreiber S, Roschger P, Lafage M, Rodan G, Klaushofer K. Effects of sodium fluoride and alendronate on the bone mineral in minipigs: a small‐angle X‐ray scattering and backscattered electron imaging study. J Bone Miner Res. February 1996;11(2):248-253.
1991	Fratzl P, Fratzl-Zelman N, Klaushofer K, Vogl G, Koller K. Nucleation and growth of mineral crystals in bone studied by small-angle X-ray scattering. Calcif Tiss Int. June 1991;48(6):407-413.
1992	Wagner HD, Weiner S. On the relationship between the microstructure of bone and its mechanical stiffness. J Biomech. November 1992;25(11):1311-1320.
1994	Fratzl P, Roschger P, Eschberger J, Abendroth B, Klaushofer K. Abnormal bone mineralization after fluoride treatment in osteoporosis: a small‐angle x‐ray‐scattering study. J Bone Miner Res. October 1994;9(10):1541-1549.
1992	Fratzl P, Groschner M, Vogl G, Plenk H Jr, Eschberger J, Fratzl-Zelman N, Koller K, Klaushofer K. Mineral crystals in calcified tissues: a comparative study by SAXS. J Bone Miner Res. March 1992;7(3):329-334.
1989	Traub W, Arad T, Weiner S. Three-dimensional ordered distribution of crystals in turkey tendon collagen fibers. Proc Natl Acad Sci USA. December 1989;86(24):9822-9826.

Cited By (41)

Year	Entry
2001	Boskey AL. Bone mineralization. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:5-1–5-33.
2022	Micheletti C, Hurley A, Gourrier A, Palmquist A, Tang T, Shah FA, Grandfield K. Bone mineral organization at the mesoscale: a review of mineral ellipsoids in bone and at bone interfaces. Acta Biomater. April 1, 2022;142:1-13.
2010	Hamed E, Lee Y, Jasiuk I. Multiscale modeling of elastic properties of cortical bone. Acta Mech. August 2010;213(1):131-154.
2004	Hellmich C, Ulm F-J, Dormieux L. Can the diverse elastic properties of trabecular and cortical bone be attributed to only a few tissue-independent phase properties and their interactions? arguments from a multiscale approach. Biomech Model Mechanobiol. June 2004;2(4):219-238.
2008	Yoon YJ, Cowin SC. The estimated elastic constants for a single bone osteonal lamella. Biomech Model Mechanobiol. February 2008;7(1):1-11.
2000	Jäger I, Fratzl P. Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys J. October 2000;79(4):1737-1746.
1999	Camacho NP, Rinnerthaler S, Paschalis EP, Mendelsohn R, Boskey AL, Fratzl P. Complementary information on bone ultrastructure from scanning small angle X-ray scattering and Fourier-transform infrared microspectroscopy. Bone. September 1999;25(3):287-293.
2001	Roschger P, Rinnerthaler S, Yates J, Rodan GA, Fratzl P, Klaushofer K. Alendronate increases degree and uniformity of mineralization in cancellous bone and decreases the porosity in cortical bone of osteoporotic women. Bone. August 2001;29(2):185-191.
2001	Grabner B, Landis WJ, Roschger P, Rinnerthaler S, Peterlik H, Klaushofer K, Fratzl P. Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone. November 2001;29(5):453-457.
2008	Roschger P, Paschalis EP, Fratzl P, Klaushofer K. Bone mineralization density distribution in health and disease. Bone. March 2008;42(3):456-466.
2010	Gamsjaeger S, Masic A, Roschger P, Kazanci M, Dunlop JWC, Klaushofer K, Paschalis EP, Fratzl P. Cortical bone composition and orientation as a function of animal and tissue age in mice by raman spectroscopy. Bone. August 2010;47(2):392-399.
2020	Ascenzi M-G. Theoretical mathematics, polarized light microscopy and computational models in healthy and pathological bone. Bone. May 2020;134:115295.
2020	Xi L, Song Y, Wu W, Qu Z, Wen J, Liao B, Tao R, Ge J, Fang D. Investigation of bone matrix composition, architecture and mechanical properties reflect structure-function relationship of cortical bone in glucocorticoid induced osteoporosis. Bone. July 2020;136:115334.
1999	Rinnerthaler S, Roschger P, Jakob HF, Nader A, Klaushofer K, Fratzl P. Scanning small angle X-ray scattering analysis of human bone sections. Calcif Tiss Int. May 1999;64(5):422-429.
2002	Boivin G, Meunier PJ. The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif Tiss Int. June 2002;70(6):503-511.
2004	Hellmich C, Barthélémy J-F, Dormieux L. Mineral–collagen interactions in elasticity of bone ultrastructure: a continuum micromechanics approach. Eur J Mech – A/Solids. September–October 2004;23(5):783-810.
2002	Hellmich C, Ulm F-J. Are mineralized tissues open crystal foams reinforced by crosslinked collagen? some energy arguments. J Biomech. September 2002;35(9):1199-1212.
2020	Törnquist E, Isaksson H, Turunen MJ. Mineralization of cortical bone during maturation and growth in rabbits. J Bone Min Metab. May 2020;38(3):289-298.
2003	Misof BM, Roschger P, Cosman F, Kurland ES, Tesch W, Messmer P, Dempster DW, Nieves J, Shane E, Fratzl P, Klaushofer K, Bilezikian J, Lindsay R. Effects of intermittent parathyroid hormone administration on bone mineralization density in iliac crest biopsies from patients with osteoporosis: a paired study before and after treatment. J Clin Endocrinol Metab. January 2003;88(3):1150-1156.
1997	Misof K, Landis WJ, Klaushofer K, Fratzl P. Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. J Clin Invest. July 1997;100(1):40-45.
2004	Ji B, Gao H. Mechanical properties of nanostructure of biological materials. J Mech Phys Solids. September 2004;52(9):1963-1990.
2016	Georgiadis M, Müller R, Schneider P. Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils. J R Soc Interface. June 1, 2016;13(119):20160088.
2001	Roschger P, Grabner BM, Rinnerthaler S, Tesch W, Kneissel M, Berzlanovich A, Klaushofer K, Fratzl P. Structural development of the mineralized tissue in the human L4 vertebral body. J Struct Biol. November 2001;136(2):126-136.
2003	Ascenzi M-G, Ascenzi A, Benvenuti A, Burghammer M, Panzavolta S, Bigid A. Structural differences between “dark” and “bright” isolated human osteonic lamellae. J Struct Biol. January 2003;141(1):22-33.
2005	Almer JD, Stock SR. Internal strains and stresses measured in cortical bone via high-energy X-ray diffraction. J Struct Biol. October 2005;152(1):14-27.
2016	Turunen MJ, Kaspersen JD, Olsson U, Guizar-Sicairos M, Bech M, Schaff F, Tägil M, Jurvelin JS, Isaksson H. Bone mineral crystal size and organization vary across mature rat bone cortex. J Struct Biol. September 2016;195(3):337-344.
2007	Fritsch A, Hellmich C. “Universal” microstructural patterns in bone: micromechanics-based prediction of anisotropic material behavior. J Theo Biol. February 21, 2007;244(4):597-620.
2009	Fritsch A, Hellmich C, Dormieux L. Ductile sliding between mineral crystals followed by rupture of collagen crosslinks: experimentally supported micromechanical explanation of bone strength. J Theo Biol. September 21, 2009;260(2):230-252.
2020	Mehraban Alvandi L. Diffuse Damage Repair Mechanism in Bone [PhD thesis]. New York, NY: The City College of New York; 2020.
2023	Micheletti C. Multimodal and Multiscale Characterization of Bone and Bone Interfaces in Health and Disease [PhD thesis]. University of Gothenburg; 2023.
2019	Groetsch A. Micro- and Nanomechanics of Mineralised Collagen Fibre Elasto-Plasticity [PhD thesis]. Ebinburgh, Scotland: Heriot-Watt University; November 2019.
2010	Deuerling JM. Effects of Ultrastructural Organization on the Mechanical Properties and Anisotropy of Human Cortical Bone [PhD thesis]. University of Notre Dame; December 2010.
2022	Gupta SD. Mineralized Tissues At the Osteochondral Junction in Healthy and Osteoarthritic Joints: Advanced Microimaging and Mechanical Studies [PhD thesis]. University of Oulu; 2022.
2022	Tice MJL. Loss and Modulation of Bone Matrix and Fragility During Diabetes Mellitus [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; May 2022.
2012	Acerbo AS. Local Chemical and Nanostructural Properties of Rat Cortical Bone Are Altered by Osteoporosis and Pharmaceutical Treatments [PhD thesis]. Stony Brook, NY: Stony Brook University; August 2012.
2006	Gleeson JP. Composition and Mechanical Properties of Osteoarthritic Subchondral Trabecular Tibial Bone [PhD thesis]. Trinity College Dublin; November 2006.
2018	Tang T. Fracture Mechanisms and Structural Fragility of Human Femoral Cortical Bone [PhD thesis]. Vancouver, BC: University of British Columbia; April 2018.
2013	Wang Y-K. Multi-Level Micromechanical Modeling of Bone Tissues [PhD thesis]. Los Angeles, CA: Los Angeles, University of California; 2013.
2003	Rajachar RM. Effects of Age -Related Ultra-Structural Level Changes in Bone on Microdamage Mechanisms [PhD thesis]. University of Michigan; 2003.
2018	Burke MV. Quantification of Changes in Vertebral Bone Quality in the Presence of Metastases [PhD thesis]. University of Toronto; 2018.
2018	Samuel J. Nanomechanics of Human Bone: In Situ Deformation Characterization Using Synchrotron X-Ray Scattering and Pole Figure Inversion Techniques [PhD thesis]. San Antionio, TX: University of Texas at San Antonio; December 2018.