Application of vibrational spectroscopy to the study of mineralized tissues (review)

Carden, A.<sup>1</sup>; Morris, M. D.<sup>1</sup>

Affiliations

¹Department of Chemistry, University of Michigan, Ann Arbor, Michigan 48109-1055

Abstract and keywords

The infrared and Raman spectroscopy of bone and teeth tissues are reviewed. Characteristic spectra are obtained for both the mineral and protein components of these tissues. Vibrational spectroscopy is used to study the mineralization process, to define the chemical structure changes accompanying bone diseases, and to characterize interactions between prosthetic implants and tissues. Microspectroscopy allows acquisition of spatially resolved spectra, with micron scale resolution. Recently developed imaging modalities allow tissue imaging with chemical composition contrast.

Keywords: Raman; infrared; bone; tooth; collagen; hydroxyapatite

Links

DOI: 10.1117/1.429994

PubMed: 10958610

WoS: 000088707800002

History

Received: 1999-10-12

Revised: 2000-04-21

Accepted: 2000-04-21

Cited Works (13)

Year	Entry
1991	Rey C, Renugopalakrishman V, Collins B, Glimcher MJ. Fourier transform infrared spectroscopic study of the carbonate ions in bone mineral during aging. Calcif Tiss Int. October 1991;49(4):251-258.
1997	Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL. FTIR microspectroscopic analysis of human iliac crest biopsies from untreated osteoporotic bone. Calcif Tiss Int. December 1997;61(6):487-492.
1991	Rey C, Shimizu M, Collins B, Glimcher MJ. Resolution-enhanced fourier transform infrared spectroscopy study of the environment of phosphate ion in the early deposits of a solid phase of calcium phosphate in bone and enamel and their evolution with age, II: investigations in the v₃ PO₄ domain. Calcif Tiss Int. December 1991;49(6):383-388.
1999	Timlin JA, Carden A, Morris MD, Bonadio JF, Hoffler CE II, Kozloff K, Goldstein SA. Spatial distribution of phosphate species in mature and newly generated mammalian bone by hyperspectral Raman imaging. J Biomed Opt. January 1999;4(1):28-34.
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.
1998	Boskey AL, Gadaleta S, Gundberg C, Doty SB, Ducy P, Karsenty G. Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone. September 1998;23(3):187-196.
1989	Rey C, Collins B, Goehl T, Dickson IR, Glimcher MJ. The carbonate environment in bone mineral: a resolution-enhanced fourier transform infrared spectroscopy study. Calcif Tiss Int. September 1989;45(3):157-164.
1996	Paschalis EP, DiCarlo E, Betts F, Sherman P, Mendelsohn R, Boskey AL. FTIR microspectroscopic analysis of human osteonal bone. Calcif Tiss Int. December 1996;59(6):480-487.
1991	Pleshko N, Boskey A, Mendelsohn R. Novel infrared spectroscopic method for the determination of crystallinity of hydroxyapatite minerals. Biophys J. October 1991;60(4):786-793.
1998	Penel G, Leroy G, Rey C, Bres E. MicroRaman spectral study of the PO₄ and CO₃ vibrational modes in synthetic and biological apatites. Calcif Tiss Int. December 1998;63(6):475-481.
1987	Legros R, Balmain N, Bonel G. Age-related changes in mineral of rat and bovine cortical bone. Calcif Tiss Int. September 1987;41(3):137-144.
1997	Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL. FTIR microspectroscopic analysis of normal human cortical and trabecular bone. Calcif Tiss Int. December 1997;61(6):480-486.
1999	Timlin JA, Carden A, Morris MD. Chemical microstructure of cortical bone probed by Raman transects. Appl Spectrosc. November 1999;53(11):1429-1435.

Cited By (54)

Year	Entry
2007	Boskey A, Camacho NP. FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials. May 2007;28(15):2465-2478.
2004	Akkus O, Adar F, Schaffler MB. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone. March 2004;34(4):443-453.
2006	McCreadie BR, Morris MD, Chen T-c, Rao DS, Finney WF, Widjaja E, Goldstein SA. Bone tissue compositional differences in women with and without osteoporotic fracture. Bone. December 2006;39(6):1190-1195.
2010	Barth HD, Launey ME, MacDowell AA, Ager JW III, Ritchie RO. On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone. Bone. June 2010;46(6):1475-1485.
2013	Burket JC, Brooks DJ, MacLeay JM, Baker SP, Boskey AL, van der Meulen MCH. Variations in nanomechanical properties and tissue composition within trabeculae from an ovine model of osteoporosis and treatment. Bone. January 2013;52(1):326-336.
2020	Rokidi S, Bravenboer N, Gamsjaeger S, Misof B, Blouin S, Chavassieux P, Klaushofer K, Paschalis E, Papapoulos S, Appelman-Dijkstra N. Impact microindentation assesses subperiosteal bone material properties in humans. Bone. February 2020;131:115110.
2020	Taylor EA, Donnelly E. Raman and Fourier transform infrared imaging for characterization of bone material properties. Bone. October 2020;139:115490.
2021	Vahidi G, Rux C, Sherk VD, Heveran CM. Lacunar-canalicular bone remodeling: impacts on bone quality and tools for assessment. Bone. February 2021;143:115663.
2013	Boskey AL. Bone composition: relationship to bone fragility and antiosteoporotic drug effects. BoneKEy Rep. December 2013;2:447.
2002	Aparicio S, Doty SB, Camacho NP, Paschalis EP, Spevak L, Mendelsohn R, Boskey AL. Optimal methods for processing mineralized tissues for Fourier transform infrared microspectroscopy. Calcif Tiss Int. May 2002;70(5):422-429.
2003	Carden A, Rajachar RM, Morris MD, Kohn DH. Ultrastructural changes accompanying the mechanical deformation of bone tissue: a Raman imaging study. Calcif Tiss Int. February 2003;72(2):166-175.
2011	Donnelly E. Methods for assessing bone quality: a review. Clin Orthop Relat Res. August 2011;469:2128-2138.
2011	Morris MD, Mandair GS. Raman assessment of bone quality. Clin Orthop Relat Res. August 2011;469:2160-2169.
2016	Hunt HB, Donnelly E. Bone quality assessment techniques: geometric, compositional, and mechanical characterization from macroscale to nanoscale. Clin Rev Bone Miner Metab. September 2016;14(3):133-149.
2006	Hofmann T, Heyroth F, Meinhard H, Fränzel W, Raum K. Assessment of composition and anisotropic elastic properties of secondary osteon lamellae. J Biomech. 2006;39(12):2282-2294.
2007	Ramasamy JG, Akkus O. Local variations in the micromechanical properties of mouse femur: the involvement of collagen fiber orientation and mineralization. J Biomech. 2007;40(4):910-918.
2011	Burket J, Gourion-Arsiquaud S, Havill LM, Baker SP, Boskey AL, van der Meulen MCH. Microstructure and nanomechanical properties in osteons relate to tissue and animal age. J Biomech. January 11, 2011;44(2):277-284.
2011	Bi X, Patil CA, Lynch CC, Pharr GM, Mahadevan-Jansen A, Nyman JS. Raman and mechanical properties correlate at whole bone- and tissue-levels in a genetic mouse model. J Biomech. January 11, 2011;44(2):297-303.
2023	Massie C, Knapp E, Awad HA, Berger AJ. Detection of osteoporotic-related bone changes and prediction of distal radius strength using Raman spectra from excised human cadaver finger bones. J Biomech. December 2023;161:111852.
2005	Ager JW III, Nalla RK, Breeden KL, Ritchie RO. Deep-ultraviolet Raman spectroscopy study of the effect of aging on human cortical bone. J Biomed Opt. May–June 2005;10(3):034012.
2010	Farlay D, Panczer G, Rey C, Delmas PD, Boivin G. Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Min Metab. July 2010;28(4):433-445.
2002	Tarnowski CP, Ignelzi MA Jr, Morris MD. Mineralization of developing mouse calvaria as revealed by Raman microspectroscopy. J Bone Miner Res. June 2002;17(6):1118-1126.
2003	Akkus O, Polyakova‐Akkus A, Adar F, Schaffler MB. Aging of microstructural compartments in human compact bone. J Bone Miner Res. June 2003;18(6):1012-1019.
2004	Kozloff KM, Carden A, Bergwitz C, Forlino A, Uveges TE, Morris MD, Marini JC, Goldstein SA. Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J Bone Miner Res. April 2004;19(4):614-622.
2006	Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF. Glucocorticoid‐treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo‐treated or estrogen‐deficient mice. J Bone Miner Res. March 2006;21(3):466-476.
2009	Gourion‐Arsiquaud S, Burket JC, Havill LM, DiCarlo E, Doty SB, Mendelsohn R, van der Meulen MCH, Boskey AL. Spatial variation in osteonal bone properties relative to tissue and animal age. J Bone Miner Res. July 2009;24(7):1271-1281.
2016	Paschalis EP, Gamsjaeger S, Fratzl-Zelman N, Roschger P, Masic A, Brozek W, Hassler N, Glorieux FH, Rauch F, Klaushofer K, Fratzl P. Evidence for a role for nanoporosity and pyridinoline content in human mild osteogenesis imperfecta. J Bone Miner Res. May 2016;31(5):1050-1059.
2010	Boskey AL, Coleman R. Aging and bone. J Dent Res. December 2010;89(2):1333-1348.
2006	Ager JW III, Balooch G, Ritchie RO. Fracture, aging, and disease in bone. J Mater Res. August 2006;21(8):1878-1892.
2012	Pathak S, Vachhani SJ, Jepsen KJ, Goldman HM, Kalidindi SR. Assessment of lamellar level properties in mouse bone utilizing a novel spherical nanoindentation data analysis method. J Mech Behav Biomed Mater. September 2012;13:102-117.
2006	Nalla RK, Kruzic JJ, Kinney JH, Balooch M, Ager JW III, Ritchie RO. Role of microstructure in the aging-related deterioration of the toughness of human cortical bone. Mater Sci Eng C Mater Biol Appl. September 2006;26(8):1251-1260.
2017	Unal M. Classification of Bound Water and Collagen Denaturation Status of Cortical Bone by Raman Spectroscopy [PhD thesis]. Cleveland, OH: Case Western Reserve University; January 2017.
2020	Mehraban Alvandi L. Diffuse Damage Repair Mechanism in Bone [PhD thesis]. New York, NY: The City College of New York; 2020.
2010	Campbell SE. Nanoindentation of Bio- and Geo-Mineralized Composites: Contribution of Microstructure and Composition [PhD thesis]. University of Colorado; 2010.
2017	Heveran CM. Bone Tissue Material Properties Are Altered in Chronic Kidney Disease to Lower Fracture Resistance Determining Bone Quality [PhD thesis]. University of Colorado; 2017.
2013	Burket JC. Alterations in Tissue Composition and Nanomechanical Properties With Ageing, Osteoporosis, and Treatment [PhD thesis]. Ithaca, NY: Cornell University; January 2013.
2013	Kim G. The Effects of Mineralization and Crystallinity on the Mechanical Behavior of Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2013.
2018	Hunt HB. Characterization of Material Properties, Microarchitecture, and Mechanics of Bone from Subjects With Type 2 Diabetes Mellitus [PhD thesis]. Ithaca, NY: Cornell University; December 2018.
2020	Taylor EA. Validation and Implementation of Vibrational Spectroscopic Measures of Bone Composition [PhD thesis]. Ithaca, NY: Cornell University; December 2020.
2009	Massey CJ. Finite Element Analysis and Materials Characterization of Changes Due to Aging and Degeneration of the Human Intervertebral Disc [PhD thesis]. Drexel University; September 2009.
2014	Carretta R. Post-Yield Mechanics and Material Composition of Single Trabeculae: A Combined Experimental and Modelling Approach [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2014.
2010	Feng L. Multi-Scale Characterization of Swine Femoral Cortical Bone and Long Bone Defect Repair by Regeneration [PhD thesis]. University of Illinois at Urbana-Champaign; 2010.
2020	O’Sullivan LM. Time-Sequence of Biomechanical Adaption in Trabecular Tissue During Estrogen Deficiency [PhD thesis]. National University of Ireland Galway; March 2020.
2013	Maher JR. Transcutaneous Raman Spectroscopy of Bone [PhD thesis]. University of Rochester; 2013.
2006	Diab T. The Role of Damage Morphology in Age-Related Increase in Bone Fragility [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; 2006.
2012	Brennan MA. Close to the Bone: Investigations Into Bone Tissue Mineralisation and Mechanobiology of Osteoporosis [PhD thesis]. University of Southampton; January 2012.
2003	Rajachar RM. Effects of Age -Related Ultra-Structural Level Changes in Bone on Microdamage Mechanisms [PhD thesis]. University of Michigan; 2003.
2005	Kozloff KM. Influence of a Collagen Mutation of the Mechanical Nature of Bone: Governing Factors in a Disease Model for Osteogenesis Imperfecta Type IV [PhD thesis]. University of Michigan; 2005.
2009	Sahar ND. Investigating the Effects of Age and Exercise on Bone Composition and the Impact of Composition on Mechanical Integrity. [PhD thesis]. University of Michigan; 2009.
2011	Raghavan M. Investigation of Mineral and Collagen Organization in Bone Using Raman Spectroscopy [PhD thesis]. University of Michigan; 2011.
2012	McElderry J-DP. Dynamics of Mineralization During Bone Development [PhD thesis]. University of Michigan; 2012.
2010	Wynnyckyj C. The Consequences of Collagen Degradation on Bone Mechanical Properties [PhD thesis]. University of Toronto; 2010.
2015	Ng AH-M. A Mouse Model of Adynamic Bone Disease (ABD) and Its Consequences on Bone Quality With Age [PhD thesis]. University of Toronto; 2015.
2014	Makowski AJ. Evaluation of Raman Spectroscopy for Fracture Resistance Assessment [PhD thesis]. Nashville, TN: Vanderbilt University; December 2014.