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Atomic Force Microscopy Characterization of the External Cortical Bone Surface in Young and Elderly Women: Potential Nanostructural Traces of Periosteal Bone Apposition During Aging

Published online by Cambridge University Press:  14 June 2013

Petar Milovanovic ,
Marija Djuric ,
Olivera Neskovic ,
Danijela Djonic ,
Jelena Potocnik ,
Slobodan Nikolic ,
Milovan Stoiljkovic ,
Vladimir Zivkovic  and
Zlatko Rakocevic
Petar Milovanovic
Affiliation:
University of Belgrade, School of Medicine, Institute of Anatomy, Laboratory for Anthropology, 4/2 Dr Subotica, 11 000 Belgrade, Serbia
Marija Djuric*
Affiliation:
University of Belgrade, School of Medicine, Institute of Anatomy, Laboratory for Anthropology, 4/2 Dr Subotica, 11 000 Belgrade, Serbia
Olivera Neskovic
Affiliation:
University of Belgrade, Institute of Nuclear Sciences Vinca, P.O. Box 522, 11 001 Belgrade, Serbia
Danijela Djonic
Affiliation:
University of Belgrade, School of Medicine, Institute of Anatomy, Laboratory for Anthropology, 4/2 Dr Subotica, 11 000 Belgrade, Serbia
Jelena Potocnik
Affiliation:
University of Belgrade, Institute of Nuclear Sciences Vinca, P.O. Box 522, 11 001 Belgrade, Serbia
Slobodan Nikolic
Affiliation:
University of Belgrade, School of Medicine, Institute of Forensic Medicine, 31a Deligradska, 11 000 Belgrade, Serbia
Milovan Stoiljkovic
Affiliation:
University of Belgrade, Institute of Nuclear Sciences Vinca, P.O. Box 522, 11 001 Belgrade, Serbia
Vladimir Zivkovic
Affiliation:
University of Belgrade, School of Medicine, Institute of Forensic Medicine, 31a Deligradska, 11 000 Belgrade, Serbia
Zlatko Rakocevic
Affiliation:
University of Belgrade, Institute of Nuclear Sciences Vinca, P.O. Box 522, 11 001 Belgrade, Serbia
*
*Corresponding author. E-mail: marijadjuric5@gmail.com
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Abstract

On the basis of the suggestion that bone nanostructure bears “tissue age” information and may reflect surface deposition/modification processes, we performed nanoscale characterization of the external cortical bone surface at the femoral neck in women using atomic force microscopy (AFM). The specific aims were to assess age-related differences in bone nanostructure and explore the existence of nanostructural traces of potential bone apposition at this surface. Our findings revealed that the external cortical surface represents a continuous phase composed of densely packed mineral grains. Although the grains varied in size and shape, there was a domination of small grains indicative of freshly deposited bone (mean grain size: young, 35 nm; old, 37 nm; p > 0.05). Advanced quantitative analysis of surface morphological patterns revealed comparable roughness and complexity of the surface, suggesting a similar rate of mineral particle deposition at the surface in both groups. Calcium/phosphorus ratio, a measure of bone tissue age, was within the same range in both groups. In summary, our AFM analyses showed consistent nanostructural and compositional bone features, suggesting existence of new bone at the periosteal bone surface in both young and elderly women. Considering observed age-related increase in the neck diameter, AFM findings may support the theory of continuous bone apposition at the periosteal surface.

Keywords

atomic force microscopy (AFM)bonenanostructureperiosteal surfaceagingfemoral neck
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 5 , October 2013 , pp. 1341 - 1349
Copyright
Copyright © Microscopy Society of America 2013 

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References

Akkus, O., Polyakova-Akkus, A., Adar, F. & Schaffler, M.B. (2003). Aging of microstructural compartments in human compact bone. J Bone Miner Res 18(6), 1012–1019.Google Scholar
Allen, M.R. & Burr, D.B. (2005). Human femoral neck has less cellular periosteum, and more mineralized periosteum, than femoral diaphyseal bone. Bone 36(2), 311–316.Google Scholar
Anczykowski, B., Gotsmann, B., Fuchs, H., Cleveland, J.P. & Elings, V.B. (1999). How to measure energy dissipation in dynamic mode atomic force microscopy. Appl Surf Sci 140(3-4), 376–382.Google Scholar
Bar, G., Delineau, L., Brandsch, R., Bruch, M. & Whangbo, M.H. (1999). Importance of the indentation depth in tapping-mode atomic force microscopy study of compliant materials. Appl Phys Lett 75(26), 4198–4200.CrossRefGoogle Scholar
Beck, T.J., Looker, A.C., Ruff, C.B., Sievanen, H. & Wahner, H.W. (2000). Structural trends in the aging femoral neck and proximal shaft: Analysis of the Third National Health and Nutrition Examination Survey dual-energy X-ray absorptiometry data. J Bone Miner Res 15(12), 2297–2304.Google Scholar
Bliziotes, M., Sibonga, J.D., Turner, R.T. & Orwoll, E. (2006). Periosteal remodeling at the femoral neck in nonhuman primates. J Bone Miner Res 21(7), 1060–1067.Google Scholar
Bose, S., Dasgupta, S., Tarafder, S. & Bandyopadhyay, A. (2010). Microwave-processed nanocrystalline hydroxyapatite: Simultaneous enhancement of mechanical and biological properties. Acta Biomater 6(9), 3782–3790.Google Scholar
Boskey, A.L. (2001). Bone mineralization. In Bone Mechanics Handbook, Cowin, S.C. (Ed.), pp. 5/1–5/33. Boca Raton, FL: CRC Press.Google Scholar
Bozec, L., De Groot, J., Odlyha, M., Nicholls, B. & Horton, M.A. (2005). Mineralised tissues as nanomaterials: Analysis by atomic force microscopy. IEE Proc Nanobiotechnol 152(5), 183–186.Google Scholar
Busse, B., Djonic, D., Milovanovic, P., Hahn, M., Püschel, K., Ritchie, R.O., Djuric, M. & Amling, M. (2010a). Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9(6), 1065–1075.Google Scholar
Busse, B., Hahn, M., Schinke, T., Püschel, K., Duda, G.N. & Amling, M. (2010b). Reorganization of the femoral cortex due to age-, sex-, and endoprosthetic-related effects emphasized by osteonal dimensions and remodeling. J Biomed Mater Res A 92A(4), 1440–1451.Google Scholar
Busse, B., Hahn, M., Soltau, M., Zustin, J., Püschel, K., Duda, G.N. & Amling, M. (2009). Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: Mineralization, morphology and biomechanics of human single trabeculae. Bone 45(6), 1034–1043.Google Scholar
Cullinane, D. & Einhorn, T. (2002). Biomechanics of bone. In Principles of Bone Biology, Bilezikian, J., Raisz, L. & Rodan, G. (Eds.), pp. 17–32. San Diego, CA: Academic Press.Google Scholar
Currey, J.D. (2002). Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press.Google Scholar
Demajo, M.A., Neskovic, O.M., Pavlovic, M.S., Veljkovic, M.V., Savovic, J.J. & Stoiljkovic, M.M. (2002). Biomonitoring of freshwater quality with Gammarus pulex. In Proceedings of the 6th International Conference on Fundamental and Applied Aspects of Physical Chemistry, pp. 347–349, Belgrade, Yugoslavia.Google Scholar
Diez-Perez, A., Güerri, R., Nogues, X., Cáceres, E., Peña, M.J., Mellibovsky, L., Randall, C., Bridges, D., Weaver, J.C., Proctor, A., Brimer, D., Koester, K.J., Ritchie, R.O. & Hansma, P.K. (2010). Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J Bone Miner Res 25(8), 1877–1885.Google Scholar
Djonic, D., Milovanovic, P., Nikolic, S., Ivovic, M., Marinkovic, J., Beck, T. & Djuric, M. (2011). Inter-sex differences in structural properties of aging femora: Implications on differential bone fragility: A cadaver study. J Bone Miner Metab 29(4), 449–457.CrossRefGoogle ScholarPubMed
Dougherty, G. & Henebry, G.M. (2001). Fractal signature and lacunarity in the measurement of the texture of trabecular bone in clinical CT images. Med Eng Phys 23(6), 369–380.CrossRefGoogle ScholarPubMed
Eppell, S.J., Tong, W., Lawrence Katz, J., Kuhn, L. & Glimcher, M.J. (2001). Shape and size of isolated bone mineralites measured using atomic force microscopy. J Orthop Res 19(6), 1027–1034.Google Scholar
Fratzl-Zelman, N., Roschger, P., Gourrier, A., Weber, M., Misof, B., Loveridge, N., Reeve, J., Klaushofer, K. & Fratzl, P. (2009). Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility. Calcif Tissue Int 85(4), 335–343.CrossRefGoogle ScholarPubMed
García, R., Magerle, R. & Perez, R. (2007). Nanoscale compositional mapping with gentle forces. Nat Mater 6(6), 405–411.Google Scholar
Grynpas, M. (1993). Age and disease-related changes in the mineral of bone. Calcif Tissue Int 53, S57–S64.CrossRefGoogle ScholarPubMed
Güerri-Fernández, R.C., Nogués, X., Quesada Gómez, J.M., Torres del Pliego, E., Puig, L., García-Giralt, N., Yoskovitz, G., Mellibovsky, L., Hansma, P.K. & Díez-Pérez, A. (2013). Microindentation for in vivo measurement of bone tissue material properties in atypical femoral fracture patients and controls. J Bone Miner Res 28(1), 162–168.CrossRefGoogle ScholarPubMed
Hassenkam, T., Fantner, G.E., Cutroni, J.A., Weaver, J.C., Morse, D.E. & Hansma, P.K. (2004). High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35(1), 4–10.Google Scholar
Hassenkam, T., Jørgensen, H.L. & Lauritzen, J.B. (2006). Mapping the imprint of bone remodeling by atomic force microscopy. Anat Rec A Discov Mol Cell Evol Biol 288(10), 1087–1094.CrossRefGoogle ScholarPubMed
Hassenkam, T., Jørgensen, H.L., Pedersen, M.B., Kourakis, A.H., Simonsen, L. & Lauritzen, J.B. (2005). Atomic force microscopy on human trabecular bone from an old woman with osteoporotic fractures. Micron 36(7-8), 681–687.Google Scholar
Hengsberger, S., Kulik, A. & Zysset, P. (2001). A combined atomic force microscopy and nanoindentation technique to investigate the elastic properties of bone structural units. Eur Cell Mater 1, 12–17.Google Scholar
Horcas, I., Fernandez, R., Gomez-Rodriguez, J.M., Colchero, J., Gomez-Herrero, J. & Baro, A.M. (2007). WSXM: A software for scanning probe microscopy and a tool for nanotechnology. Rev Sci Instrum 78(1), 013705–013708.Google Scholar
Huja, S., Beck, F. & Thurman, D. (2006). Indentation properties of young and old osteons. Calcif Tissue Int 78(6), 392–397.Google Scholar
Jandt, K.D. (2001). Atomic force microscopy of biomaterials surfaces and interfaces. Surf Sci 491(3), 303–332.Google Scholar
Jiang, T., Hall, N., Ho, A. & Morin, S. (2005). Quantitative analysis of electrodeposited tin film morphologies by atomic force microscopy. Thin Solid Films 471(1-2), 76–85.CrossRefGoogle Scholar
Kindt, J.H., Fantner, G.E., Thurner, P.J., Schitter, G. & Hansma, P.K. (2005). A new technique for imaging mineralized fibrils on bovine trabecular bone fracture surfaces by atomic force microscopy. Mater Res Soc Symp Proc 874, 59–65.Google Scholar
Kindt, J.H., Thurner, P.J., Lauer, M.E., Bosma, B.L., Schitter, G., Fantner, G.E., Izumi, M., Weaver, J.C., Morse, D.E. & Hansma, P.K. (2007). In situ observation of fluoride-ion-induced hydroxyapatite–collagen detachment on bone fracture surfaces by atomic force microscopy. Nanotechnology 18(13), 135102. Google Scholar
Kuhn, L., Grynpas, M., Rey, C., Wu, Y., Ackerman, J. & Glimcher, M. (2008). A comparison of the physical and chemical differences between cancellous and cortical bovine bone mineral at two ages. Calcif Tissue Int 83(2), 146–154.CrossRefGoogle ScholarPubMed
Legros, R., Balmain, N. & Bonel, G. (1987). Age-related changes in mineral of rat and bovine cortical bone. Calcif Tissue Int 41(3), 137–144.Google Scholar
Lin, Y. & Xu, S. (2011). AFM analysis of the lacunar-canalicular network in demineralized compact bone. J Microsc 241(3), 291–302.Google Scholar
Lita, A.E. & Sanchez, J.E. Jr. (2000). Effects of grain growth on dynamic surface scaling during the deposition of Al polycrystalline thin films. Phys Rev B 61(11), 7692–7699.CrossRefGoogle Scholar
McCreadie, B.R., Morris, M.D., Chen, T.-c., Sudhaker Rao, D., Finney, W.F., Widjaja, E. & Goldstein, S.A. (2006). Bone tissue compositional differences in women with and without osteoporotic fracture. Bone 39(6), 1190–1195.Google Scholar
Milovanovic, P., Djuric, M. & Rakocevic, Z. (2012a). Age-dependence of power spectral density and fractal dimension of bone mineralized matrix in atomic force microscope topography images: Potential correlates of bone tissue age and bone fragility in female femoral neck trabeculae. J Anat 221(5), 427–433.CrossRefGoogle ScholarPubMed
Milovanovic, P., Potocnik, J., Djonic, D., Nikolic, S., Zivkovic, V., Djuric, M. & Rakocevic, Z. (2012b). Age-related deterioration in trabecular bone mechanical properties at material level: Nanoindentation study of the femoral neck in women by using AFM. Exp Gerontol 47(2), 154–159.Google Scholar
Milovanovic, P., Potocnik, J., Stoiljkovic, M., Djonic, D., Nikolic, S., Neskovic, O., Djuric, M. & Rakocevic, Z. (2011). Nanostructure and mineral composition of trabecular bone in the lateral femoral neck: Implications for bone fragility in elderly women. Acta Biomater 7(9), 3446–3451.Google Scholar
Mitchell, M.W. & Bonnell, D.A. (1990). Quantitative topographic analysis of fractal surfaces by scanning tunneling microscopy. J Mat Res 5(10), 2244–2254.Google Scholar
Nenadović, M., Potočnik, J., Ristić, M., Štrbac, S. & Rakočević, Z. (2012). Surface modification of polyethylene by Ag+ and Au+ ion implantation observed by phase imaging atomic force microscopy. Surf Coat Technol 206(19-20), 4242–4248.Google Scholar
Orwoll, E.S. (2003). Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18(6), 949–954.Google Scholar
Parfitt, A.M. (2002). Parathyroid hormone and periosteal bone expansion. J Bone Miner Res 17(10), 1741–1743.Google Scholar
Paschalis, E.P., Betts, F., DiCarlo, E., Mendelsohn, R. & Boskey, A.L. (1997). FTIR microspectroscopic analysis of normal human cortical and trabecular bone. Calcif Tissue Int 61(6), 480–486.Google Scholar
Pfeifer, P. (1984). Fractal dimension as working tool for surface-roughness problems. Appl Surf Sci 18(1-2), 146–164.Google Scholar
Power, J., Loveridge, N., Rushton, N., Parker, M. & Reeve, J. (2003). Evidence for bone formation on the external “periosteal” surface of the femoral neck: A comparison of intracapsular hip fracture cases and controls. Osteoporos Int 14(2), 141–145.Google Scholar
Rauch, F. (2007). Bone accrual in children: Adding substance to surfaces. Pediatrics 119(Suppl 2), S137–S140.Google Scholar
Reilly, G.C., Knapp, H.F., Stemmer, A., Niederer, P. & Knothe Tate, M.L. (2001). Investigation of the morphology of the lacunocanalicular system of cortical bone using atomic force microscopy. Ann Biomed Eng 29(12), 1074–1081.Google Scholar
Roschger, P., Paschalis, E.P., Fratzl, P. & Klaushofer, K. (2008). Bone mineralization density distribution in health and disease. Bone 42(3), 456–466.Google Scholar
Sahoo, N.K., Thakur, S. & Tokas, R.B. (2006). Fractals and superstructures in gadolinia thin film morphology: Influence of process variables on their characteristic parameters. Thin Solid Films 503(1-2), 85–95.Google Scholar
Sasaki, N., Tagami, A., Goto, T., Taniguchi, M., Nakata, M. & Hikichi, K. (2002). Atomic force microscopic studies on the structure of bovine femoral cortical bone at the collagen fibril-mineral level. J Mater Sci Mater Med 13(3), 333–337.Google Scholar
Seeman, E. (2003). Periosteal bone formation—A neglected determinant of bone strength. N Engl J Med 349(4), 320–323.Google Scholar
Seeman, E. (2007). The periosteum—A surface for all seasons. Osteoporos Int 18(2), 123–128.CrossRefGoogle ScholarPubMed
Seeman, E. (2008). Bone quality: The material and structural basis of bone strength. J Bone Miner Metab 26(1), 1–8.Google Scholar
Silk, T., Hong, Q., Tamm, J. & Compton, R.G. (1998). AFM studies of polypyrrole film surface morphology II. Roughness characterization by the fractal dimension analysis. Synth Met 93(1), 65–71.Google Scholar
Skedros, J.G., Bloebaum, R.D., Bachus, K.N., Boyce, T.M. & Constantz, B. (1993). Influence of mineral content and composition on graylevels in backscattered electron images of bone. J Biomed Mater Res 27(1), 57–64.Google Scholar
Strbac, S., Nenadovic, M., Rajakovic, L. & Rakocevic, Z. (2010). Chemical surface composition of the polyethylene implanted by Ag+ ions studied by phase imaging atomic force microscopy. Appl Surf Sci 256(12), 3895–3899.Google Scholar
Su, X., Sun, K., Cui, F.Z. & Landis, W.J. (2003). Organization of apatite crystals in human woven bone. Bone 32(2), 150–162.Google Scholar
Szulc, P., Seeman, E., Duboeuf, F., Sornay-Rendu, E. & Delmas, P.D. (2006). Bone fragility: Failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21(12), 1856–1863.Google Scholar
Thurner, P.J. (2009). Atomic force microscopy and indentation force measurement of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol 1(6), 624–649.Google Scholar
Thurner, P.J., Müller, R., Kindt, J.H., Schitter, G., Fantner, G.E., Wyss, P., Sennhauser, U. & Hansma, P.K. (2005). Novel techniques for high-resolution functional imaging of trabecular bone. In Proceedings of the SPIE, San Diego, CA, February 12, 2005, pp. 515–526.Google Scholar
Thurner, P.J., Oroudjev, E., Jungmann, R., Kreutz, C., Kindt, J.H., Schitter, G., Okouneva, T.O., Lauer, M.E., Fantner, G.E., Hansma, H.G. & Hansma, P.K. (2007). Imaging of bone ultrastructure using atomic force microscopy. In Modern Research and Educational Topics in Microscopy, Méndez-Vilas, A. and Díaz, J. (Eds.), pp. 37–48. Badajoz, Spain: Formatex.Google Scholar
Tong, W., Glimcher, M.J., Katz, J.L., Kuhn, L. & Eppell, S.J. (2003). Size and shape of mineralites in young bovine bone measured by atomic force microscopy. Calcif Tissue Int 72(5), 592–598.Google Scholar
Ulmeanu, M., Serghei, A., Mihailescu, I.N., Budau, P. & Enachescu, M. (2000). C–Ni amorphous multilayers studied by atomic force microscopy. Appl Surf Sci 165(2-3), 109–115.Google Scholar
Wagoner Johnson, A.J. & Herschler, B.A. (2011). A review of the mechanical behavior of CaP and CaP/polymer composites for applications in bone replacement and repair. Acta Biomater 7(1), 16–30.CrossRefGoogle ScholarPubMed
Wallace, J.M. (2012). Applications of atomic force microscopy for the assessment of nanoscale morphological and mechanical properties of bone. Bone 50(1), 420–427.Google Scholar
Wallace, J.M., Erickson, B., Les, C.M., Orr, B.G. & Banaszak Holl, M.M. (2010). Distribution of type I collagen morphologies in bone: Relation to estrogen depletion. Bone 46(5), 1349–1354.Google Scholar