Skip to main content Accessibility help
×
Home

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

  • Petar Milovanovic (a1), Marija Djuric (a1), Olivera Neskovic (a2), Danijela Djonic (a1), Jelena Potocnik (a2), Slobodan Nikolic (a3), Milovan Stoiljkovic (a2), Vladimir Zivkovic (a3) and Zlatko Rakocevic (a2)...

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.

Copyright

Corresponding author

* Corresponding author. E-mail: marijadjuric5@gmail.com

References

Hide All
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), 10121019.
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), 311316.
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), 376382.
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), 41984200.
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), 22972304.
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), 10601067.
Bose, S., Dasgupta, S., Tarafder, S. & Bandyopadhyay, A. (2010). Microwave-processed nanocrystalline hydroxyapatite: Simultaneous enhancement of mechanical and biological properties. Acta Biomater 6(9), 37823790.
Boskey, A.L. (2001). Bone mineralization. In Bone Mechanics Handbook, Cowin, S.C. (Ed.), pp. 5/15/33. Boca Raton, FL: CRC Press.
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), 183186.
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), 10651075.
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), 14401451.
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), 10341043.
Cullinane, D. & Einhorn, T. (2002). Biomechanics of bone. In Principles of Bone Biology, Bilezikian, J., Raisz, L. & Rodan, G. (Eds.), pp. 1732. San Diego, CA: Academic Press.
Currey, J.D. (2002). Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press.
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. 347349, Belgrade, Yugoslavia.
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), 18771885.
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), 449457.
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), 369380.
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), 10271034.
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), 335343.
García, R., Magerle, R. & Perez, R. (2007). Nanoscale compositional mapping with gentle forces. Nat Mater 6(6), 405411.
Grynpas, M. (1993). Age and disease-related changes in the mineral of bone. Calcif Tissue Int 53, S57S64.
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), 162168.
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), 410.
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), 10871094.
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), 681687.
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, 1217.
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), 013705013708.
Huja, S., Beck, F. & Thurman, D. (2006). Indentation properties of young and old osteons. Calcif Tissue Int 78(6), 392397.
Jandt, K.D. (2001). Atomic force microscopy of biomaterials surfaces and interfaces. Surf Sci 491(3), 303332.
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), 7685.
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, 5965.
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.
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), 146154.
Legros, R., Balmain, N. & Bonel, G. (1987). Age-related changes in mineral of rat and bovine cortical bone. Calcif Tissue Int 41(3), 137144.
Lin, Y. & Xu, S. (2011). AFM analysis of the lacunar-canalicular network in demineralized compact bone. J Microsc 241(3), 291302.
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), 76927699.
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), 11901195.
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), 427433.
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), 154159.
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), 34463451.
Mitchell, M.W. & Bonnell, D.A. (1990). Quantitative topographic analysis of fractal surfaces by scanning tunneling microscopy. J Mat Res 5(10), 22442254.
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), 42424248.
Orwoll, E.S. (2003). Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18(6), 949954.
Parfitt, A.M. (2002). Parathyroid hormone and periosteal bone expansion. J Bone Miner Res 17(10), 17411743.
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), 480486.
Pfeifer, P. (1984). Fractal dimension as working tool for surface-roughness problems. Appl Surf Sci 18(1-2), 146164.
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), 141145.
Rauch, F. (2007). Bone accrual in children: Adding substance to surfaces. Pediatrics 119(Suppl 2), S137S140.
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), 10741081.
Roschger, P., Paschalis, E.P., Fratzl, P. & Klaushofer, K. (2008). Bone mineralization density distribution in health and disease. Bone 42(3), 456466.
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), 8595.
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), 333337.
Seeman, E. (2003). Periosteal bone formation—A neglected determinant of bone strength. N Engl J Med 349(4), 320323.
Seeman, E. (2007). The periosteum—A surface for all seasons. Osteoporos Int 18(2), 123128.
Seeman, E. (2008). Bone quality: The material and structural basis of bone strength. J Bone Miner Metab 26(1), 18.
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), 6571.
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), 5764.
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), 38953899.
Su, X., Sun, K., Cui, F.Z. & Landis, W.J. (2003). Organization of apatite crystals in human woven bone. Bone 32(2), 150162.
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), 18561863.
Thurner, P.J. (2009). Atomic force microscopy and indentation force measurement of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol 1(6), 624649.
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. 515526.
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. 3748. Badajoz, Spain: Formatex.
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), 592598.
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), 109115.
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), 1630.
Wallace, J.M. (2012). Applications of atomic force microscopy for the assessment of nanoscale morphological and mechanical properties of bone. Bone 50(1), 420427.
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), 13491354.

Keywords

Related content

Powered by UNSILO

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

  • Petar Milovanovic (a1), Marija Djuric (a1), Olivera Neskovic (a2), Danijela Djonic (a1), Jelena Potocnik (a2), Slobodan Nikolic (a3), Milovan Stoiljkovic (a2), Vladimir Zivkovic (a3) and Zlatko Rakocevic (a2)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.