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Bone Architecture: Collagen Structure and Calcium/Phosphorus Maps

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Abstract

Bone collagen structure in normal and pathological tissues is presented using techniques of thin section transmission electron microscopy and morphometry. In pathological tissue, deviations from normal fine structure are reflected in abnormal arrangements of collagen fibrils and abnormalities in fibril diameter. The relationships between these bone structural changes and the skeletal calcium/phosphorus ratio are discussed. Calcium/phosphorus ratio is measured by X-ray absorptiometry and computed microtomography.

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References

  1. Kaplan, F.S., Hayes, W.C., Keaveny, T.M., Boskey, A., Einhorn, J.P., Iannotti, J.P.: Form and function of bone. In: Simon, S.R., (ed.) Orthopaedic Basic Science, pp. 127–184. American Academy of Orthopaedic Surgeons, Rosemont, IL (1994)

    Google Scholar 

  2. Rubin, M.A., Rubin, J., Jasiuk, I.: SEM and TEM study of the hierarchical structure of C57BL/6J and C3H/HeJ mice trabecular bone. Bone 35, 1–20 (2004). doi:10.1016/j.bone.2004.02.008

    Article  Google Scholar 

  3. Kjaer, M.: Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84, 649–698 (2004). doi:10.1152/physrev.00031.2003

    Article  Google Scholar 

  4. Dahl, T., Veis, A.: Electrostatic interactions lead to the formation of asymmetric collagen–phosphophoryn aggregates. Connect. Tissue Res. 44(Suppl 1), 206–213 (2003). doi:10.1080/713713589

    Article  Google Scholar 

  5. Paschalis, E.P., Recker, R., Dicarlo, E., Doty, S.B., Atti, E., Boskey, A.L.: Distribution of collagen cross-links in normal human trabecular bone. J. Bone Miner. Res. 18, 1942–1946 (2003). doi:10.1359/jbmr.2003.18.11.1942

    Article  Google Scholar 

  6. Wu, T.J., Huang, H.H., Lan, C.W., Lin, C.H., Hsu, F.Y., Wang, Y.J.: Studies on the microspheres comprised of reconstituted collagen and hydroxyapatite. Biomaterials 25, 651–658 (2004). doi:10.1016/S0142-9612(03)00576-3

    Article  Google Scholar 

  7. Midura, R.J., Vasanji, A., Su, X., Wang, A., Midura, S.B., Gorski, J.P.: Calcospherulites isolated from the mineralization front of bone induce the mineralization of type I collagen. Bone 41, 1005–1016 (2007). doi:10.1016/j.bone.2007.08.036

    Article  Google Scholar 

  8. Tzaphlidou, M.: The role of collagen in bone structure: an image processing approach. Micron 36, 593–601 (2005). doi:10.1016/j.micron.2005.05.009

    Article  Google Scholar 

  9. Dalle Carbonare, L., Giannini, S.: Bone microarchitecture as an important determination of bone strength. J. Endocrinol. Invest. 27, 99–105 (2004)

    Google Scholar 

  10. Mosekilde, L.: Age-related changes in bone mass, structure, and strength—effects of loading. Z. Rheumatol. 59(Suppl 1), 1–9 (2000). doi:10.1007/s003930070031

    Article  Google Scholar 

  11. Akesson, K., Grynpas, M.D., Hancock, R.G.V., Odelius, R., Obrant, K.J.: Energy-dispersive X-ray microanalysis of the bone mineral content in human trabecular bone: a comparison with ICPES and neutron activation analysis. Calcif. Tissue Int. 55, 236–239 (1994). doi:10.1007/BF00425881

    Article  Google Scholar 

  12. Bailey, A.J., Wotton, S.F., Sims, T.J., Thompson, P.W.: Post-translational modifications in the collagen of human osteoporotic femoral head. Biochem. Biophys. Res. Commun. 185, 801–805 (1992). doi:10.1016/0006-291X(92)91697-O

    Article  Google Scholar 

  13. Kafantari, H., Kounadi, E., Fatouros, M., Milonakis, M., Tzaphlidou, M.: Structural alterations in rat skin and bone collagen fibrils induced by ovariectomy. Bone 26, 349–353 (2000). doi:10.1016/S8756-3282(99)00279-3

    Article  Google Scholar 

  14. Pace, J.M., Atkinson, M., Willing, M.C., Wallis, G., Byers, P.H.: Deletions and duplications of Gly-Xaa-Yaa triplet repeats in the triple helical domains of type I collagen chains disrupt helix formation and result in several types of osteogenesis imperfecta. Hum. Mutat. 18, 319–326 (2001). doi:10.1002/humu.1193

    Article  Google Scholar 

  15. Batge, B., Diebold, J., Stein, H., Bodo, M., Muller, P.K.: Compositional analysis of the collagenous bone matrix-a study on adult normal and osteopenic bone tissue. Eur. J. Clin. Invest. 22, 805–812 (1992). doi:10.1111/j.1365-2362.1992.tb01450.x

    Article  Google Scholar 

  16. Bank, R.A., Tekopelle, J.M., Janus, G.J., Wassen, M.H., Pruijs, H.E., Van der Sluijs, H.A., Sakkers, R.J.: Pyridinium cross-links in bone of patients with osteogenesis imperfecta: evidence of a normal intrafibrillar collagen packing. J. Bone Miner. Res. 15, 1330–1336 (2000). doi:10.1359/jbmr.2000.15.7.1330

    Article  Google Scholar 

  17. Prockop, D.J., Constantinou, C.D., Dombrowski, K.E., Hojima, Y., Kadler, K.E., Kuivaniemi, H., Tromp, G., Vogel, B.E.: Type I procollagen: the gene–protein system that harbors most of the mutations causing osteogenesis imperfecta and probably more common heritable disorders of connective tissue. Am. J. Med. Genet. 34, 60–67 (1989). doi:10.1002/ajmg.1320340112

    Article  Google Scholar 

  18. Rubin, M.A., Jasiuk, I., Taylor, J., Rubin, J., Ganey, T., Apkarian, R.P.: TEM analysis of the nanostructure of normal and osteoporotic human trabecular bone. Bone 33, 270–282 (2003). doi:10.1016/S8756-3282(03)00194-7

    Article  Google Scholar 

  19. Adachi, E., Hopkinson, I., Hayashi, T.: Basement–membrane stromal relationships: interactions between collagen fibrils and the lamina densa. Int. Rev. Cytol. 173, 73–156 (1997). doi:10.1016/S0074-7696(08)62476-6

    Article  Google Scholar 

  20. Kounadi, E., Fountos, G., Tzaphlidou, M.: The influence of inflammation-mediated osteopenia (IMO) on the structure of rabbit bone and skin collagen fibrils. Connect. Tissue Res. 37, 69–76 (1998). doi:10.3109/03008209809028901

    Article  Google Scholar 

  21. Tzaphlidou, M., Kounadi, E., Kafantari, H.: Influence of lithium on mouse bone collagen fibrils. J. Trace Microprobe Tech. 18, 321–326 (2000)

    Google Scholar 

  22. Diebold, J., Batge, B., Stein, H., Muller-Esch, G., Muller, P.K., Lohrs, U.: Osteoporosis in longstanding acromegaly: characteristic changes of vertebral trabecular architecture and bone matrix composition. Virchows Arch., A Pathol. Anat. Histopathol. 419, 209–215 (1991). doi:10.1007/BF01626350

    Article  Google Scholar 

  23. Fountos, G., Kounadi, E., Tzaphlidou, M., Yasumura, S., Glaros, D.: The effects of inflammation-mediated osteoporosis (IMO) on the skeletal Ca/P ratio and on the structure of rabbit bone and skin collagen. Appl. Radiat. Isotopes 49, 657–659 (1998). doi:10.1016/S0969-8043(97)00086-9

    Article  Google Scholar 

  24. Parry, D.A., Barnes, G.R., Craig, A.S.: A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc. R. Soc. Lond. B 203, 305–321 (1978)

    Article  ADS  Google Scholar 

  25. Baek, G.H., Carlin, G.J., Vogrin, T.M., Woo, S.L., Harner, C.D.: Quantitative analysis of collagen fibrils of human cruciate and meniscofemoral ligaments. Clin. Orthop. Relat. Res. 357, 205–211 (1998). doi:10.1097/00003086-199812000-00026

    Article  Google Scholar 

  26. Ottani, V., Franchi, M., De Pasquale, V., Leonardi, L., Morocutti, M., Ruggeri, A.: Collagen fibril arrangement and size distribution in monkey oral mucosa. J. Anat. 192, 321–328 (1998). doi:10.1046/j.1469-7580.1998.19230321.x

    Article  Google Scholar 

  27. Berillis, P., Emfietzoglou, D., Tzaphlidou, M.: Collagen fibril diameter in relation to bone site and to calcium/phosphorus ratio. Sci. World J. 6, 1109–1113 (2006). doi:10.100/isw.2006.212 doi:10.1100/tsw.2006.212

    Google Scholar 

  28. Chapman, J.A.: Molecular organisation in the collagen fibril. In: Hukins, D.W.L. (ed.) Connective Tissue Matrix, pp. 89–132. Verlag Chemie (1984)

  29. Robey, P.G., Fedarko, N.S., Hefferan, T.E., Bianco, P., Vetter, U.K., Grzesik, W., Friedenstein, A., Van Der Pluijm, G., Mintz, K.P., Young, M.F., Kerr, J.M., Ibaraki, K., Heegard, A.M.: Structure and molecular of bone matrix proteins. J. Bone Miner. Res. 8, 483–487 (1993)

    Article  Google Scholar 

  30. Aerssens, J., Dequeker, J., Mbuyi-Muamba, J.M.: Bone tissue composition: biochemical anatomy of bone. Clin. Rheumatol. 13, 54–62 (1994). doi:10.1007/BF02229866

    Article  Google Scholar 

  31. Ferris, B.D., Klenerman, L., Dodds, R.A., Bitensky, L., Chayen, J.: Altered organization of non-collagenous bone matrix in osteoporosis. Bone 8, 285–288 (1987). doi:10.1016/8756-3282(87)90003-2

    Article  Google Scholar 

  32. Kent, G.N., Dodds, R.A., Bitensky, L., Klenerman, L., Watts, R.W.E., Chayen, J.: Changes in crystal size and orientation of acidic glycosaminoglycans at the fracture site in fractured necks of femur. J. Bone Jt. Surg. 65-B, 189–194 (1983)

    Google Scholar 

  33. Suarez, K.N., Romanello, M., Bettica, P., Moro, L.: Collagen type I of rat cortical and trabecular bone differs in the extent of posttranslational modifications. Calcif. Tissue Int. 58, 65–69 (1996). doi:10.1007/BF02509548

    Article  Google Scholar 

  34. Stein, I.D., Granik, G.: Rib structure and bending strength: an autopsy study. Calcif. Tissue Res. 20, 61–73 (1976). doi:10.1007/BF02546398

    Article  Google Scholar 

  35. Stenstrom, M., Olander, B., Lehto-Axtelius, D., Madsen, J.E., Nordsletten, L., Carlsson, G.A.: Bone mineral density and bone structure parameters as predictors of bone strength: an analysis using computerized microtomography and gastrectomy-induced osteopenia in the rat. J. Biomech. 33, 289–297 (2000). doi:10.1016/S0021-9290(99)00181-5

    Article  Google Scholar 

  36. Werner, C., Iversen, B.F., Therkildsen, M.H.: Contribution of the trabecular component to mechanical strength and bone mineral content of the femoral neck. An experimental study on cadaver bones. Scand. J. Clin. Lab. Invest. 48, 457–460 (1988). doi:10.3109/00365518809085757

    Article  Google Scholar 

  37. Lotz, J.C., Cheal, E.J., Hayes, W.C.: Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos. Int. 5, 252–261 (1995). doi:10.1007/BF01774015

    Article  Google Scholar 

  38. Fountos, G., Yasumura, S., Glaros, D.: The skeletal calcium/phosphorus ratio: a new in vivo method of determination. Med. Phys. 24, 1303–1310 (1997). doi:10.1118/1.598152

    Article  Google Scholar 

  39. Fountos, G., Tzaphlidou, M., Kounadi, E., Glaros, D.: In vivo measurement of radius calcium/phosphorus ratio by X-ray absorptiometry. Appl. Radiat. Isotopes 51, 273–278 (1999). doi:10.1016/S0969-8043(99)00056-1

    Article  Google Scholar 

  40. Tzaphlidou, M., Zaichick, V.: Neutron activation analysis of calcium/phosphorus ratio in rib bone of healthy humans. Appl. Radiat. Isotopes 57, 779–783 (2002). doi:10.1016/S0969-8043(02)00171-9

    Article  Google Scholar 

  41. Tzaphlidou, M., Zaichick, V.: Calcium, phosphorus, calcium–phosphorus ratio in rib bone of healthy humans. Biol. Trace Elem. Res. 93, 63–74 (2003). doi:10.1385/BTER:93:1-3:63

    Article  Google Scholar 

  42. Zaichick, V., Tzaphlidou, M.: Determination of calcium, phosphorus, and the calcium/phosphorus ratio in cortical bone from the human femoral neck by neutron activation analysis. Appl. Radiat. Isotopes 56, 781–786 (2002). doi:10.1016/S0969-8043(02)00066-0

    Article  Google Scholar 

  43. Zaichick, V., Tzaphlidou, M.: Calcium and phosphorus concentrations and the calcium/phosphorus ratio in trabecular bone from the femoral neck of healthy humans as determined by neutron activation analysis. Appl. Radiat. Isotopes 58, 623–627 (2003). doi:10.1016/S0969-8043(03)00092-7

    Article  Google Scholar 

  44. Bolotin, H.H., Sievanen, H.: Inaccuracies inherent in dual-energy X-ray absorptiometry in vivo bone mineral density can seriously mislead diagnostic/prognostic interpretations of patient-specific bone fragility. J. Bone Miner. Res. 16, 799–805 (2001). doi:10.1359/jbmr.2001.16.5.799

    Article  Google Scholar 

  45. Peyrin, F., Salome, M., Nuzzo, S., Cloetens, P., Laval-Jeantet, A.M., Baruchel, J.: Perspectives in three-dimensional analysis of bone samples using synchrotron radiation microtomography. Cell. Mol. Biol. 46, 1089–1102 (2000)

    Google Scholar 

  46. Nuzzo, S., Peyrin, F., Cloetens, P., Baruchel, J., Boivin, G.: Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography. Med. Phys. 29, 2672–2681 (2002). doi:10.1118/1.1513161

    Article  Google Scholar 

  47. Postnov, A.A., Vinogradov, A.V., Van Dyck, D., Saveliev, S.V., De Clerck, N.M.: Quantitative analysis of bone mineral content by X-ray microtomography. Physiol. Meas. 24, 165–178 (2003). doi:10.1088/0967-3334/24/1/312

    Article  Google Scholar 

  48. Salome, M., Peyrin, F., Cloetens, P., Odet, C., Laval-Jeante, A.M., Baruchel, J., Spanne, P.: A synchrotron radiation microtomography system for the analysis of trabecular bone samples. Med. Phys. 26, 2194–2204 (1999). doi:10.1118/1.598736

    Article  Google Scholar 

  49. Davis, G.R., Wong, F.S.: X-ray microtomography of bones and teeth. Physiol. Meas. 17, 121–146 (1996). doi:10.1088/0967-3334/17/3/001

    Article  Google Scholar 

  50. Kinney, J.H., Haupt, D.L., Balooch, M., Ladd, A.J., Lane, N.E.: Three-dimensional morphometry of the L6 vertebra in the ovariectomized rat model of osteoporosis: biomechanical implications. J. Bone Miner. Res. 15, 1981–1991 (2000). doi:10.1359/jbmr.2000.15.10.1981

    Article  Google Scholar 

  51. Tzaphlidou, M., Speller, R., Royle, G., Griffiths, J., Olivo, A., Pani, S., Longo, R.: High resolution Ca/P maps of bone architecture in 3D synchrotron radiation microtomographic images. Appl. Radiat. Isotopes 62, 569–575 (2005). doi:10.1016/j.apradiso.2004.10.003

    Article  Google Scholar 

  52. Nuzzo, S., Lafage-Proust, M.H., Martin-Badosa, E., Boivin, G., Thomas, T., Alexandre, C., Peyrin, F.: Synchrotron radiation microtomography allows the analysis three-dimensional microarchitecture and degree of mineralization of human iliac crest biopsy specimens: effects etidronate treatment. J. Bone Miner. Res. 17, 1372–1382 (2002). doi:10.1359/jbmr.2002.17.8.1372

    Article  Google Scholar 

  53. Nuzzo, S., Meneghini, C., Braillon, P., Bouvier, R., Mobilio, S., Peyri, F.: Microarchitectural and physical changes during fetal growth in human vertebral bone. J. Bone Miner. Res. 18, 760–768 (2003). doi:10.1359/jbmr.2003.18.4.760

    Article  Google Scholar 

  54. Bousson, V., Peyrin, F., Bergot, C., Hausard, M., Sautet, A., Laredo, J.D.: Cortical bone in the human femoral neck: three-dimensional appearance and porosity using synchrotron radiation. J. Bone Miner. Res. 19, 794–802 (2004). doi:10.1359/JBMR.040124

    Article  Google Scholar 

  55. Stenstrom, M., Olander, B., Carlsson, C.A., Carlsson, G.A., Lehto-Axtelius, D., Hakanson, R.: The use of computed microtomography to monitor morphological changes in small animals. Appl. Radiat. Isotopes 49, 565–570 (1998). doi:10.1016/S0969-8043(97)00189-9

    Article  Google Scholar 

  56. Barbier, A., Martel, C., de Vernejoul, M.C., Tirode, F., Nys, M., Mocaer, G., Morieux, C., Murakami, H., Lacheretz, F.: The visualization and evaluation of bone architecture in the rat using three-dimensional X-ray microcomputed tomography. J. Bone Miner. Metab. 17, 37–44 (1999). doi:10.1007/s007740050061

    Article  Google Scholar 

  57. Laib, A., Barou, O., Vico, L., Lafage-Proust, M.H., Alexandre, C., Ruegsegger, P.: 3D micro-computed tomography of trabecular and cortical bone architecture with application to a rat model of immobilisation osteoporosis. Med. Biol. Eng. Comput. 38, 326–332 (2000). doi:10.1007/BF02347054

    Article  Google Scholar 

  58. Martin-Badosa, E., Elmoutaouakkil, A., Nuzzo, S., Amblard, D., Vico, L., Peyrin, F.: A method for the automatic characterization of bone architecture in 3D mice microtomographic images. Comput. Med. Imaging Graph. 27, 447–458 (2003). doi:10.1016/S0895-6111(03)00031-4

    Article  Google Scholar 

  59. Speller, R., Pani, S., Tzaphlidou, M., Horrocks, J.: MicroCT analysis of calcium/phosphorus ratio maps at different bone sites. Phys. Res. A 548, 269–273 (2005)

    Google Scholar 

  60. Tzaphlidou, M., Speller, R., Royle, G., Griffiths, J.: Preliminary estimates of the calcium/phosphorus ratio at different cortical bone sites using synchrotron microCT. Phys. Med. Biol. 51, 1849–1855 (2006). doi:10.1088/0031-9155/51/7/015

    Article  Google Scholar 

  61. Tzaphlidou, M., Kafantari, H.: Influence of nutritional factors on bone collagen fibrils in ovariectomized rats. Bone 27, 635–638 (2000). doi:10.1016/S8756-3282(00)00382-3

    Article  Google Scholar 

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  1. Department of Medical Physics, Medical School, Ioannina University, 45110, Ioannina, Greece

    Margaret Tzaphlidou

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Tzaphlidou, M. Bone Architecture: Collagen Structure and Calcium/Phosphorus Maps. J Biol Phys 34, 39–49 (2008). https://doi.org/10.1007/s10867-008-9115-y

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