Article

You have full text access to this OnlineOpen article

Cement lines of secondary osteons in human bone are not mineral-deficient: New data in a historical perspective

  1. John G. Skedros1,†,*,
  2. Jennifer L. Holmes1,
  3. Eric G. Vajda1,2,
  4. Roy D. Bloebaum1

Article first published online: 21 JUL 2005

DOI: 10.1002/ar.a.20214

Issue

The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology

The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology

Volume 286A, Issue 1, pages 781–803, September 2005

Additional Information

How to Cite

Skedros, J. G., Holmes, J. L., Vajda, E. G. and Bloebaum, R. D. (2005), Cement lines of secondary osteons in human bone are not mineral-deficient: New data in a historical perspective. Anat. Rec., 286A: 781–803. doi: 10.1002/ar.a.20214

Author Information

  1. 1

    Bone and Joint Research Laboratory, Department of Veterans Affairs Medical Center, Salt Lake City, Utah

  2. 2

    Ligand Pharmaceuticals, Inc., San Diego, California

  1. †

    Fax: 801-713-0609

*Utah Bone and Joint Center, 5323 South Woodrow Street, Suite 202, Salt Lake City, UT 84107

Publication History

  1. Issue published online: 18 AUG 2005
  2. Article first published online: 21 JUL 2005
  3. Manuscript Accepted: 13 DEC 2004
  4. Manuscript Received: 6 NOV 2003

Funded by

  • Office of Research and Development Medical Research Service, Department of Veterans Affairs Salt Lake City Health Care System
  • Department of Orthopedics, University of Utah School of Medicine
  • Utah Bone and Joint Center

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (1079K)

LITERATURE CITED

  • Advani SH, Lee T-S, Martin RB. 1987. Analysis of crack arrest by cement lines in osteonal bone. In: ErdmanAG, editor. Advances in bioengineering BED, vol. 3. New York: American Society of Mechanical Engineers. p 57–58.
  • Åkesson K, Grynpas MD, Hancock RG, Odselius R, Obrant KJ. 1994. 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.
  • Amprino R, Engström A. 1952. Studies on X-ray absorption and diffraction of bone tissue. Acta Anat 15: 1–22.
  • Ascenzi A, Ascenzi MG, Benvenuti A, Mango F. 1997. Pinching in longitudinal and alternate osteons during cyclic loading. J Biomech 30: 689–695.
  • Bachus KN, Bloebaum RD. 1992. Projection effect errors in biomaterials and bone research. Cells Mater 2: 347–355.
  • Bain SD, Impeduglia TM, Rubin CT. 1990. Cement line staining in undecalcified thin sections of cortical bone. Stain Technol 65: 1–5.
  • Baron R, Vignery A, Horowitz M. 1984. Lymphocytes, macrophages and the regulation of bone remodeling. In: PeckWA, editor. Bone and mineral research, annual 2. Amsterdam: Elsevier. p 175–243.
  • Behiri JC, Bonfield W. 1980. Crack velocity dependence of longitudinal fracture in bone. J Mater Sci 15: 1841–1849.
  • Bloebaum RD, Bachus KN, Boyce TM. 1990. Backscattered electron imaging: the role in calcified tissue and implant analysis. J Biomater Appl 5: 56–85.
  • Bloebaum RD, Lauritzen RS, Skedros JG, Smith EF, Thomas KA, Bennett JT, Hofmann AA. 1993. Roentgenographic procedure for selecting proximal femur allograft for use in revision arthroplasty. J Arthroplasty 8: 347–360.
  • Bloebaum RD, Skedros JG, Vajda EG, Bachus KN, Constantz BR. 1997. Determining mineral content variations in bone using backscattered electron imaging. Bone 20: 485–490.
  • Boivin G, Meunier PJ. 2002. The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif Tissue Int 70: 503–511.
  • Bonfield W. 1987. Advances in the fracture mechanics of cortical bone. J Biomech 20: 1071–1081.
  • Bosshardt DD, Zalzal S, McKee MD, Nanci A. 1998. Developmental appearance and distribution of bone sialoprotein and osteopontin in human and rat cementum. Anat Rec 250: 13–33.
    Direct Link:
  • Boyce TM, Fyhrie DP, Glotkowski MC, Radin EL, Schaffler MB. 1998. Damage type and strain mode associations in human compact bone bending fatigue. J Orthop Res 16: 322–329.
    Direct Link:
  • Boyde A, Maconnachie, Reid SA, Delling G, Mundy GR. 1986. Scanning electron microscopy in bone pathology: review of methods, potential and applications. Scanning Electr Microsc 4: 1537–1554.
  • Boyde A, Jones S. 1987. Early scanning electron microscopic studies of hard tissue resorption: their relation to current concepts reviewed. Scanning Microsc 1: 369–381.
  • Boyde A, Hendel P, Hendel R, Maconnachie E, Jones SJ. 1990. Human cranial bone structure and the healing of cranial bone grafts: a study using backscattered electron imaging and confocal microscopy. Anat Embryol 181: 235–251.
  • Boyde A, Jones SJ. 1996. Scanning electron microscopy of bone: instrument, specimen, and issues. Microsc Res Tech 33: 92–120.
    Direct Link:
  • Boyde A, Kingsmill VJ. 1998. Mineralisation density of human mandibular bone: quantitative backscattered electron image analysis. J Anat 192: 245–256.
    Direct Link:
  • Braidotti P, Branca FP, Stagni L. 1997. Scanning electron microscopy of human cortical bone failure surfaces. J Biomech 30: 155–162.
  • Broz JJ, Simske SJ, Greenberg AR. 1995. Material and compositional properties of selectively demineralized cortical bone. J Biomech 28: 13457–1368.
  • Brunski JB, Puleo DA, Nanci A. 2000. Biomaterials and biomechanics of oral and maxillofacial implants: Current status and future developments. Int J Oral Maxillofac Implants 15: 15–46.
  • Bumrerraj S, Katz JL. 2001. Scanning acoustic microscopy study of human cortical and trabecular bone. Ann Biomed Eng 29: 1034–1042.
  • Burr DB, Martin RB, Schaffler MB, Radin EL. 1985. Bone remodeling in response to in vivo fatigue microdamage. J Biomech 18: 189–200.
  • Burr DB, Schaffler MB, Frederickson RG. 1988. Composition of the cement line and its possible mechanical role as a local interface in human compact bone. J Biomech 21: 939–945.
  • Carter DR, Hayes WC. 1977. Compact bone fatigue damage: a microscopic examination. Clin Orthop 127: 265–274.
  • Castanet J. 1981. Nouvelles donnees sur les lignes cimentates de l'os. Arch Biol (Bruxelles) 92: 1–24.
  • Choi K, Goldstein SA. 1992. A comparison of the fatigue behavior of human trabecular and cortical bone tissue. J Biomech 25: 1371–1381.
  • Clark J, Stechschulte DJ Jr. 1998. The interface between bone and tendon at an insertion site: a study of the quadriceps tendon insertion. J Anat 193: 605–616.
    Direct Link:
  • Cool SM, Forwood MR, Campbell P, Bennett MB. 2002. Comparisons between bone and cementum compositions and the possible basis for their layered appearances. Bone 30: 386–392.
  • Corondan G, Haworth WL. 1986. A fractographic study of human long bone. J Biomech 19: 207–218.
  • Courtney AC, Hayes WC, Gibson LJ. 1996. Age-related differences in post-yield damage in human cortical bone. Experiment and model. J Biomech 29: 1463–1471.
  • Currey JD. 1984. The mechanical adaptations of bones. Princeton, NJ: Princeton University Press.
  • Currey JD. 2002. Bones: structure and mechanics. Princeton, NJ: Princeton University Press.
  • Davies JE. 1996. In vitro modeling of the bone/implant interface. Anat Rec 245: 426–445.
    Direct Link:
  • Dempster WT, Coleman RF. 1961. Tensile strength of bone along and across the grain. J Appl Physiol 16: 355–360.
  • de Ricqlès A, Meunier FJ, Castanet J, Francillon-Vieillot H. 1991. Comparative microstructure of bone. In: HallBK, editor. Bone, vol. 3. Boca Raton, FL: CRC Press. p 1–78.
  • Denhardt DT, Guo X. 1993. Osteopontin: a protein with diverse functions. FASEB J 7: 1475–1482.
  • de Ricqlès A, Meunier FJ, Castanet J, Francillon-Vieillot H. 1991. Comparative microstructure of bone. In: HallBK, editor. Bone, vol. 3. Boca Raton, FL: CRC Press. p 1–78.
  • Dhem A. 1980. Etude histologique et microradiographique des manifestations biologiques propres au tissu osseux compact. Bull Mem Acad R Med Belg 135: 368–381.
  • Dhem A, Robert V. 1986. Morphology of bone tissue aging. In: UthoffHK, StahlE, editors. Current concept of bone fragility. Berlin: Springer-Verlag. p 363–370.
  • Donahue SW, Sharkey NA, Modanlou KA, Sequeira LN, Martin RB. 2000. Bone strain and microcracks at stress fracture sites in human metatarsals. Bone 27: 827–833.
  • Dong XN, Guo XE. 2004. Geometric determinants to cement line debonding and osteonal lamellae failure in osteon pullout tests. J Biomechanical Eng 126: 387–390.
  • Dorlot J-M, L'Esperance G, Meunier A. 1986. Characterization of single osteons: microhardness and mineral content. Trans 32nd Orthop Res Soc 11: 330.
  • Edie JW, Glick PL. 1979. Irradiation effects in the electron microprobe quantitation of mineralized tissues. J Microsc 117: 285–296.
  • Emmanual J, Hornbeck C, Bloebaum RD. 1987. A polymethyl methacrylate method for large specimens of mineralized bone with implants. Stain Technol 62: 401–410.
  • Evans FG, Bang S. 1966. Physical and histological differences between human fibular and femoral compact bone. In: EvansFG, editor. Studies on the anatomy and function of bone and joints. New York: Springer. p 142–155.
  • Everts V, Delaissé, Korper W, Jansen DC, Tigchelaar-Gutter W, Saftig P, Beertsen W. 2002. The bone lining cell: its role in cleaning Howship's lacunae and initiating bone formation. J Bone Min Res 17: 77–90.
    Direct Link:
  • Fawcett DW. 1994. Bloom and Fawcett: a textbook of histology, 12th ed. New York: Chapman and Hall. p 224.
  • Fawns HT, Landells JW. 1953. Histochemical studies of rheumatic conditions: I, observations on the fine structures of the matrix of normal bone and cartilage. Ann Rheum Dis 12: 105–113.
  • Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire JY, Zylberberg L, de Ricqlès A. 1990. Microstructure and mineralization of vertebrate skeletal tissues, In: CarterJG, editor. Skeletal biomineralization: patterns, processes and evolutionary trends, vol. 1. New York: Van Nostrand Reinhold. p 471–530.
  • Frank JD, Ryan M, Kalscheur VL, Ruaux-Mason CP, Hozak RR, Muir P. 2002. Aging and accumulation of microdamage in canine bone. Bone 30: 201–206.
  • Frasca P. 1981. Scanning-electron microscopy studies of “ground substance” in the cement lines, resting lines, hypercalcified rings and reversal lines of human cortical bone. Acta Anat 109: 115–121.
  • Frasca P, Harper R, Katz JL. 1981a. Strain and frequency dependence of shear storage modulus for human single osteons and cortical bone microsamples: size and hydration effects. J Biomech 14: 679–690.
  • Frasca P, Harper RA, Katz JL. 1981b. Scanning electron microscopy studies of collagen, mineral and ground substance in human cortical bone. Scanning Electr Microsc 3: 338–346.
  • Fratzl P, Schreiber S, Roschger P, Lafage M-H, Rodan G, Kalushofer K. 1996. 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 11: 248–253.
    Direct Link:
  • Frost HM. 1963. Bone remodeling dynamics. Springfield, IL: Charles C.
  • Frost HM. 1973. Bone modeling and skeletal modeling errors. Springfield, IL: Charles C.
  • Frost HM. 1990. Skeletal structural adaptations to mechanical usage (SATMU): 2, redefining Wolff's law: the remodeling problem. Anat Rec 226: 414–422.
    Direct Link:
  • Gerstenfeld LC. 1999. Osteopontin in skeletal tissue homeostasis: an emerging picture of the autocrine/paracrine functions of the extracellular matrix. J Bone Miner Res 14: 850–855.
    Direct Link:
  • Goldstein JI, Newbury DE, Echlin P, Joy DC, Romig AD Jr, Lyman CE, Fiori C, Lifshin E. 1992. Electron-specimen interactions. In: Scanning electron microscopy and x-ray microanalysis: a text for biologists, material scientists, and geologists. New York: Plenum Press. p 69–147.
  • Glowacki J, Rey C, Glimcher MJ, Cox KA, Lian J. 1991. A role for osteocalcin in osteoclast differentiation. J Cell Biochem 45: 292–302.
    Direct Link:
  • Gottesman T, Hashin Z. 1980. Analysis of viscoelastic behavior of bones on the basis of microstructure. J Biomech 13: 89–96.
  • Grynpas MD, Holmyard DP, Pritzker KPH. 1994. Bone mineralization and histomorphometry in biopsies of osteoporotic patients treated with fluoride. Cells Mater 4: 287–297.
  • Guo XE, Liang LC, Goldstein SA. 1998. Micromechanics of osteonal cortical bone fracture. Trans ASME J Biomech Eng 120: 112–117.
  • Guo XE. 2001. Mechanical properties of cortical bone and cancellous bone tissue. In: CowinSC, editor. Bone mechanics handbook, 2nd ed. Boca Raton, FL: CRC Press. p 10.1–10.23.
  • Ham AW, Cormack DH. 1979. Histophysiology of cartilage, bone, and joints. Philadelphia: J.B. Lippincott. p 367–485.
  • Hauschka PV, Maviakos AD, Iafrati MD, Doleman SE, Klagsbrun M. 1986. Growth factors in bone matrix. J Biol Chem 261: 2665–2674.
  • Heuck F. 1971. Investigations of high density areas in metabolic bone diseases. Isr J Med Sci 7: 477–480.
  • Heuck FW. 1993. Comparative histological and microradiographic investigations of human bone. In: GrupeG, GarlandAN, editors. Histology of ancient human bone: methods and diagnosis. Berlin: Springer-Verlag. p 125–136.
  • Hiller LP, Stover SM, Gibson VA, Gibeling JC, Prater CS, Hazelwood SJ, Yeh OC, Martin RB. 2003. Osteon pullout in the equine third metacarpal bone: Effects of ex vivo fatigue. J Orthop Res 21: 481–488.
    Direct Link:
  • Hofmann A, Konrad L, Gotzen L, Printz H, Ramaswamy A, Hofmann C. 2003. Bioengineering human bone tissue using autogenous osteoblasts cultured on different biomatrices. J Biomed Mater Res 67: 191–199.
    Direct Link:
  • Hogan HA. 1992. Micromechanics modeling of Haversian cortical bone properties. J Biomech 25: 549–556.
  • Hosseini MM, Sodek J, Franke R-P, Davies JE. 2000. The structure and composition of the bone-implant interface. In: DaviesJE, editor. Bone engineering. Toronto: Em Squared. p 295–304.
  • Holmes JL, Bachus KN, Bloebaum RD. 2000. Thermal effects of the electron beam and implications of surface damage in the analysis of bone tissue. Scanning 22: 243–248.
    Direct Link:
  • Howell PG, Boyde A. 1994. Monte Carlo simulations of electron scattering in bone. Bone 15: 285–291.
  • Howell PG, Boyde A. 1999. Surface roughness of preparations for back scattered-electron scanning electron microscopy: The image differences and their Monte Carlo simulation. Scanning 21: 361–367.
    Direct Link:
  • Hunter GK, Goldberg HA. 1993. Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci USA 90: 8562–8565.
  • Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA. 1996. Nucleation and inhibition of hydroxyapatite by mineralized tissue proteins. Biochem J 317: 59–64.
  • Ingram RT, Clarke BL, Fisher LW, Fitzpatrick LA. 1993. Distribution of noncollagenous proteins in the matrix of adult human bone: evidence of anatomic and functional heterogeneity. J Bone Miner Res 8: 1019–1029.
    Direct Link:
  • Jaffe HL. 1972. Metabolic, degenerative, and inflammatory diseases of bones and joints. Philadelphia: Lea and Febiger. p 52–68
  • Jee WSS. 1983. The skeletal tissues. In: WeissL, editor. Histology: cell and tissue biology, 5th ed. New York: Elsevier Biomedical. p 200–255.
  • Jepsen KJ, Davy DT, Krzypow DJ. 1999. The role of the lamellar interface during torsional yielding of human cortical bone. J Biomech 32: 303–310.
  • Jowsey J. 1960. Age changes in human bone. Clin Orthop 17: 210–217.
  • Jowsey J. 1964. Variations in bone mineralization with age and disease. In: FrostHM, editor. Bone biodynamics. Boston: Little, Brown. p 461–479.
  • Jowsey J. 1966. Quantitative microradiography: a new approach in the evaluation of metabolic bone disease. Am J Med 40: 485–491.
  • Kagayama M, Sasano Y, Akita H. 1993. Lectin binding in bone matrix of adult rats with special reference to cement lines. Tohoku J Exp Med 170: 81–91.
  • Kanaya K, Okayama S. 1972. Penetration and energy-loss theory of electrons in solid targets. J Phys D Appl Phys 5: 43–58.
  • Kato Y, Boskey A, Spevak L, Dallas M, Hori M, Bonewald LF. 2001. Establishment of an osteoid preosteocyte-like cell MLO-A5 that spontaneously mineralizes in culture. J Bone Miner Res 16: 1622–1633.
    Direct Link:
  • Katz JL. 1980. Anisotropy of Young's modulus of bone. Nature 283: 106–107.
  • Katz JL. 1981. Composite material models for cortical bone. In: CowinSC, editor. Mechanical properties of bone. New York: American Society of Mechanical Engineers. p 171–184.
  • Katz JL, Meunier A. 1993. Scanning acoustic microscope studies of the elastic properties of osteons and osteon lamellae. ASME Trans J Biomech Eng 115: 543–548.
  • Kornblum SS, Kelly PJ. 1964. The lacunae and Haversian canals in tibial cortical bone from ischemic and non-ischemic limbs: a comparative microradiographic study. J Bone Joint Surg 46A: 797–810.
  • Lacroix P. 1971. The internal remodeling of bones. In: BourneGH, editor. The biochemistry and physiology of bone, vol. 3. New York: Academic Press. p 119–144.
  • Lakes RS, Katz JL. 1974. Interrelationships among the viscoelastic functions for anisotropic solids: application to calcified tissues and related systems. J Biomech 7: 259–270.
  • Lakes RS, Katz JL. 1979. Viscoelastic properties of wet cortical bone: II, relaxation mechanisms. J Biomech 12: 679–687.
  • Lakes RS, Saha S. 1979. Cement line motion in bone. Science 204: 501–503.
  • Lakes R. 1995. On the torsional properties of single osteons. J Biomech 28: 1409–1410.
  • Lakes R. 2001. Viscoelastic properties of cortical bone. In: CowinSC, editor. Bone mechanics handbook, 2nd ed. Boca Raton, FL: CRC Press. p 11.1–11.15.
  • Landis WJ, Glimcher MJ. 1978. Electron diffraction and electron probe microanalysis of the mineral phase of bone tissue prepared by anhydrous techniques. J Ultrastructural Res 63: 188–233.
  • Les CM, Spence CA, Vance JL, Christopherson GT, Patel B, Turner AS, Divine GW, Fyhrie DP. 2004. Determinants of ovine compact bone viscoelastic properties: effects of architecture, mineralization, and remodeling. Bone 35: 729–738.
  • Mabrey JD, Fitch RD. 1989. Plastic deformation in pediatric fractures: mechanism and treatment. J Pediatr Orthop 9: 310–314.
  • Maj G, Toajari E. 1937. Osservazioni sperimentali sul meccanismo di resistenza del tessuto osseo lamellare compatto alle azioni meccaniche. Chir Org Mov 22: 541–557.
  • Marotti G. 1996. The structure of bone tissues and the cellular control of their deposition. Ital J Anat Embryol 101: 25–79.
  • Martin RB, Burr DB. 1982. A hypothetical mechanism for the stimulation of osteonal remodeling by fatigue damage. J Biomech 15: 137–139.
  • Martin RB, Burr DB. 1989. Structure, function, and adaptation of compact bone. New York: Raven Press.
  • Martin RB, Burr DB, Sharkey NA. 1998. Skeletal Tissue Mechanics. New York: Springer.
  • Martin RB. 1993. A finite element model for mineral transport into newly-formed bone. Trans 39th Orthop Res Soc 18: 80.
  • Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffin LV. 1996. Osteonal structure in the equine third metacarpus. Bone 19: 165–171.
  • Mason MW, Skedros JG, Bloebaum RD. 1995. Evidence of strain-mode-related cortical adaptation in the diaphysis of the horse radius. Bone 17: 229–237.
  • McKee MD, Nanci A. 1995. Osteopontin and the bone remodeling sequence: colloidal-gold immunocytochemistry of an interfacial extracellular matrix protein. Ann NY Acad Sci 760: 177–189.
    Direct Link:
  • McKee MD, Nanci A. 1996a. Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc Res Tech 33: 141–164.
    Direct Link:
  • McKee MD, Nanci A. 1996b. Osteopontin: an interfacial extracellular matrix protein in mineralized tissues. Connect Tissue Res 35: 197–205.
  • Mellors RC. 1964. Electron probe microanalysis: 1, calcium and phosphorous in normal human cortical bone. Lab Invest 13: 183–195.
  • Meunier PJ, Boivin G. 1997. Bone mineral density reflects bone mass but also the degree of mineralization of bone: therapeutic implications. Bone 21: 373–377.
  • Meunier A, Katz JL, Christel P, Sedel L. 1998. A reflection scanning acoustic microscope for bone and bone-biomaterials interface studies. J Orthop Res 6: 770–775.
    Direct Link:
  • Moyle DD, Bowden RW. 1984. Fracture of human femoral bone. J Biomech 17: 203–213.
  • Muir P, Ruaux-Mason CP. 2000. Microcrack density and length in the proximal and distal metaphyses of the humerus and radius in dogs. Am J Vet Res 61: 6–8.
  • Mulari MT, Qu Q, Harkonen PL, Vaananen HK. 2004. Osteoblast-like cells complete osteoclastic bone resorption and form new mineralized bone matrix in vitro. Calcif Tissue Int 75: 253–261.
  • Mundy GR, Rodan SB, Majeska RJ, DeMartino S, Trimmier C, Martin TJ, Rodan GA. 1982. Unidirectional migration of osteosarcoma cells with osteoblast characteristics in response to products of bone resorption. Calcif Tissue Int 34: 542–546.
  • Murata K. 1974. Spatial distribution of backscattered electrons in the scanning electron microscope and electron microbe. J Appl Physiol 45: 4110–4117.
  • Nanci A. 1999. Content and distribution of noncollagenous matrix proteins in bone and cementum: relationship to speed of formation and collagen packing density. J Struct Biol 126: 256–259.
  • Nesbitt SA, Horton MA. 1997. Trafficking of matrix collagens through bone-resorbing osteoclasts. Science 276: 266–269.
  • Nicholson WAP, Ashton BA, Hohling HJ, Quint P, Schreiber J. 1977. Electron microprobe investigations into the process of hard tissue formation. Cell Tissue Res 177: 331–345.
  • Nicholson WAP, Dempster DW. 1980. Aspects of microprobe analysis of mineralized tissues. Scanning Electr Microsc Pt 2: 517–533.
  • Nicolella DP, Nicholls AE, Lankford J, Davy DT. 2001. Machine vision photogrammetry: a technique for measurement of microstructural strain in cortical bone. J Biomech 34: 135–139.
  • Norman TL, Vashishth D, Burr DB. 1995. Fracture toughness of human bone under tension. J Biomech 28: 309–320.
  • Norman TL, Wang Z. 1997. Microdamage of human cortical bone: incidence and morphology in long bones. Bone 20: 375–379.
  • Nyssen-Behets C, Arnould V, Dhem A. 1994. Hypermineralized lamellae below the bone surface: a quantitative microradiographic study. Bone 15: 685–689.
  • O'Brien FJ, Taylor D, Lee TC. 2003. Microcrack accumulation at different intervals during fatigue testing of compact bone. J Biomech 36: 973–980.
  • Ortner DJ, von Endt DW. 1971. Microscopic and electron microprobe characterization of the sclerotic lamellae in human osteons. Isr J Med Sci 7: 480–482.
  • Pampena DA, Roberson KA, Litvinova O, Lajoie G, Goldberg HA. 2004. Inhibition of hydroxyapatite formation by osteopontin phosphopeptides. Biochem J 378: 1083–1087.
  • Pankovich AM, Simmons DJ, Kulkarni VV. 1974. Zonal osteons in cortical bone. Clin Orthop 100: 356–363.
  • Parfitt AM. 1983. The physiologic and clinical significance of bone histomorphometric data. In: ReckerRR, editor. Bone histomorphometry: techniques and interpretation. Boca Raton, FL: CRC Press. p 143–223.
  • Parfitt AM. 1984. The cellular basis of bone remodeling: the quantum concept reexamined in light of recent advances in the cell biology of bone. Calcif Tissue Int 36: S37–S45.
  • Parfitt AM. 1994. Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. J Cell Biochem 55: 273–286.
    Direct Link:
  • Park HC, Lakes RS. 1986. Cosserat micromechanics of human bone: strain redistribution by a hydration sensitive constituent. J Biomech 19: 385–397.
  • Payne CM, Cromey DW. 1990. Limitations of ZAF correction factors in the determination of calcium/phosphorus ratios: important forensic science considerations relevant to the analysis of bone fragments using scanning electron microscopy and energy-dispersive X-ray microanalysis. J Forens Sci 35: 560–568.
  • Phelps JB, Hubbard GB, Wang X, Agrawal CM. 2000. Microstructural heterogeneity and the fracture toughness of bone. J Biomed Mater Res 51: 735–741.
    Direct Link:
  • Philipson B. 1965. Composition of cement lines in bone. J Histochem Cytochem 13: 270–281.
  • Piekarski K. 1970. Fracture of bone. J Appl Physiol 41: 215–223.
  • Piekarski K. 1984. Fractography of bone. In: HastingsGW, DucheyneP, editors. Natural living biomaterials. Boca Raton, FL: CRC Press. p 99–117.
  • Prendergast PJ, Huiskes R. 1996. Microdamage and osteocyte lacuna strain in bone: a microstructural finite element analysis. ASME Trans J Biomech Eng 118: 240–246.
  • Pritchard JJ. 1972. General histology of bone. In: BourneGH, editor. The biochemistry and physiology of bone, 2nd ed., vol. 1. New York: Academic Press. p 1–20.
  • Reid SA, Boyde A. 1987. Changes in the mineral density distribution in human bone with age: image analysis using backscattered electrons in the SEM. J Bone Miner Res 2: 13–22.
    Direct Link:
  • Rho JY, Zioupos P, Currey JD, Pharr GM. 1999. Variations in the individual thick lamellar properties within osteons by nanoindentation. Bone 25: 295–300.
  • Rosenberg AE. 1994. Skeletal system and soft tissue tumors. In: CotranRS, KumarV, RobbinsSL, SchoenFJ, editors. Robbins pathologic basis of disease, 5th ed. Philadelphia: W.B. Saunders. p 1213–1271.
  • Roschger P, Eschberger J, Plenk H Jr. 1993. Formation of ultracracks in methacrylate-embedded undecalcified bone samples by exposure to aqueous solutions. Cells Mater 3: 361–365.
  • Roschger P, Plenk H Jr, Klaushofer K, Eschberger J. 1995. A new scanning electron microscopy approach to the quantification of bone mineral distribution: backscattered electron image grey-levels correlated to calcium Kα-line intensities. Scanning Microsc 9: 75–88.
  • Roschger P, Fratzl P, Klaushofer K, Rodan G. 1997. Mineralization of cancellous bone after alendronate and sodium fluoride treatment: a quantitative backscattered electron imaging study on minipig ribs. Bone 20: 393–397.
  • Ruff CB, Hayes WC. 1983. Cross-sectional geometry of Pecos Pueblo femora and tibiae: a biomechanical investigation—method and general patterns of variation. Am J Phys Anthropol 60: 359–381.
    Direct Link:
  • Saha S. 1977. Longitudinal shear properties of human compact bone and its constituents and the associated failure mechanisms. J Mater Sci 12: 1798–1806.
  • Salo J, Lehenkari P, Mulari M, Metsikko K, Vaananen HK. 1997. Removal of osteoclast bone resorption products by transcytosis. Science 276: 270–273.
  • Schaffler MB, Burr DB, Frederickson RG. 1987. Morphology of the osteonal cement line in human bone. Anat Rec 217: 223–228.
    Direct Link:
  • Schaffler MB, Choi K, Milgrom C. 1995. Aging and matrix microdamage accumulation in human compact bone. Bone 17: 521–525.
  • Schmidt WJ. 1959. Grenzscheiden der lakunen und kittlinien des knochengewebes: polarisationsoptische analyse kollagenfreier kongorrotgefarbter schliffe. Z Zellforsch 50: 275–296.
  • Simmons DJ. 1985. Options for bone aging with the microscope. Yearbook Phys Anthropol 28: 249–263.
    Direct Link:
  • Simmons ED Jr, Pritzker KPH, Grynpas MD. 1991. Age-related changes in the human femoral cortex. J Orthop Res 9: 155–167.
    Direct Link:
  • Sissons HA, Jowsey J, Stewart L. 1960. The microradiographic appearance of normal bone at various ages. In: EngströmA, CoslettV, PatteeH, editors. X-ray microscopy and X-ray microanalysis: proceedings of the Second International Symposium. New York: Elsevier. p 206–215.
  • Sissons HA. 1962. Age changes in the structure and mineralization of bone tissue in man. In: McLeanFC, LaCroixP, BudyAM, editors. Radioisotopes and bone. London: Blackwell Scientific Publications. p 443–465.
  • Sit S, Bizios R, Vashishth D. 2003. Is bone resorption in human cortical bone limited by cement lines? Trans 49th Orthop Res Soc 28: 384.
  • Skedros JG, Bloebaum RD, Bachus KN, Boyce TM. 1993a. The meaning of gray levels in backscattered electron images of bone. J Biomed Mater Res 27: 47–56.
    Direct Link:
  • Skedros JG, Bloebaum RD, Bachus KN, Boyce TM, Constantz B. 1993b. Influence of mineral content and composition on gray levels in backscattered electron images of bone. J Biomed Mater Res 27: 57–64.
    Direct Link:
  • Skedros JG, Mason MW, Bloebaum RD. 1994. Differences in osteonal micromorphologies between tensile and compressive cortices of a bending skeletal system: indications of potential strain-specific differences in bone microstructure. Anat Rec 239: 47–63.
    Direct Link:
  • Skedros JG, Durand P, Bloebaum RD. 1995. Hypermineralized peripheral lamellae in primary osteons of deer antler: potential functional analogues of cement lines in mammalian secondary bone. J Bone Miner Res 10(Suppl 1): S441.
  • Skedros JG, Mason MW, Nelson MC, Bloebaum RD. 1996. Evidence of structural and material adaptation to specific strain features in cortical bone. Anat Rec 246: 47–63.
    Direct Link:
  • Skedros JG, Hunt KJ, Bloebaum RD. 2004. Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus. J Morphol 259: 281–307.
    Direct Link:
  • Smith JW. 1963. Age changes in the organic fraction of bone. J Bone Joint Surg 45B: 761–769.
  • Sobelman OS, Gibeling JC, Stover SM, Hazelwood SJ, Yeh OC, Shelton DR, Martin RB. 2004. Do microcracks decrease or increase fatigue resistance in cortical bone? J Biomech 27: 1295–1303.
  • Sokoloff L. 1973. A note on the histology of cement lines. In: KenediRM, editor. Perspectives in biomedical engineering. Baltimore, MD: University Park Press. p 135–138.
  • Stout S, Simmons DJ. 1979. Use of histology in ancient bone research. Yearbook Phys Anthropol 22: 228–249.
  • Sumner DR, Bryan JM, Urban RM, Kuszak JR. 1990. Measuring the volume fraction of bone ingrowth: a comparison of three techniques. J Orthop Res 8: 448–452.
    Direct Link:
  • Terai K, Takano-Yamamoto T, Ohba Y, Hiura K, Sugimoto M, Sato M, Kawahata H, Inaguma N, Kitamura Y, Nomura S. 1999. Role of osteopontin in bone remodeling caused by mechanical stress. J Bone Miner Res 14: 839–849.
    Direct Link:
  • Tran Van P, Vignery A, Baron R. 1982. An electron microscopic study of the bone remodeling sequence in the rat. Cell Tissue Res 225: 283–292.
  • Trotter M, Hixon BB. 1974. Sequential changes in weight, density, and percentage ash weight of human skeletons from an early fetal period through old age. Anat Rec 179: 1–18.
    Direct Link:
  • Tye CE, Rattray KR, Warner KJ, Gordon JAR, Sodek J, Hunter GK, Goldberg HA. 2003. Delineation of the hydroxyapatite-nucleating domains of bone sialoprotein. J Biol Chem 278: 7949–7955.
  • Vajda EG, Skedros JG, Bloebaum RD. 1995. Consistency in calibrated backscattered electron images of calcified tissues and minerals analyzed in multiple imaging sessions. Scanning Microsc 9: 741–755.
  • Vajda EG, Bloebaum RD, Skedros JG. 1996. Validation of energy dispersive X-ray spectrometry as a method to standardize backscattered electron images of bone. Cells Mater 6: 79–92.
  • Vajda EG, Bloebaum RD, Skedros JG. 1998. Errors in backscattered electron analysis of bone standardized by energy-dispersive X-ray spectrometry. Scanning 20: 527–535.
    Direct Link:
  • Vajda EG, Humphrey S, Skedros JG, Bloebaum RD. 1999. Influence of topography and specimen preparation on backscattered electron images of bone. Scanning 21: 379–386.
    Direct Link:
  • Von Ebner V. 1875 Uber den feineren bau der knochensubstanz. Sitzungsberichte Deutsch Akad Wissenschaften Berlin 72: 49–138.
  • Villanueva AR, Sypitkowski C, Parfitt AM. 1986. A new method for identification of cement lines in undecalcified, plastic embedded sections of bone. Stain Technol 61: 83–88.
  • Vose GP, Baylink DJ. 1970. Effect of fibrillar structure of pericanalicular and intercanalicular bone on X-ray absorption. Anat Rec 166: 239–246.
    Direct Link:
  • Wang Z, Norman TL. 1996. In vivo microdamage of human cortical bone supports the hypothesis that cement lines “trap” cracks. Trans 42nd Orthop Res Soc 21: 594.
  • Weidenreich F. 1930. Das knochengewebe. In: von MollendorffW, editor. Mollendorff Handbuch der mikroskopischen Anatomie des Menschen, vol. 2, pt. 2. Berlin: Verlag Julius Springer. p 391–520.
  • Weinmann JP, Sicher H. 1955. Bone tissue. In: Bone and bones. fundamentals of bone biology, 2nd ed. St. Louis, MO: C.V. Mosby. p 18–46.
  • Wong FL, Elliott JC. 1997. Theoretical explanation of the relationship between backscattered electron and X-ray linear attenuation coefficients in calcified tissues. Scanning 19: 541–546.
    Direct Link:
  • Xiao Y, Haase H, Young WG, Bartold PM. 2004. Development and transplantation of a mineralized matrix formed by osteoblasts in vitro for bone regeneration. Cell Transplant 12: 15–25.
  • Yeager JA. 1971. Bone morphology and mineral homeostasis, In: MoyersRE, KrogmanWM, editors. Cranio-facial growth in man: part II, the biology of bone. New York: Pergamon Press. p 27–32.
  • Yeni YN, Brown CU, Wang Z, Norman TL. 1997. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21: 453–459.
  • Yeni YN, Norman TL. 2000. Calculation of porosity and osteon cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth. J Biomed Mat Res 51: 504–509.
    Direct Link:
  • Zagba-Mongalima G, Goret-Nicaise M, Dhem A. 1988. Age change in human bone: a microradiographic and histological study of subperiosteal and periosteal calcifications. Gerontology 34: 264–276.
  • Zhou H, Chernecky R, Davies JE. 1994. Deposition of cement at reversal lines in rat femoral bone. J Bone Miner Res 9: 367–374.
    Direct Link:
  • Zhu X-L, Ganss B, Goldberg HA, Sodek J. 2001. Synthesis and processing of bone sialoproteins during de novo bone formation in vitro. Biochem Cell Biol 79: 737–746.
  • Zioupos P, Currey JD. 1994. The extent of microcracking and the morphology of microcracks in damaged bone. J Mater Sci 29: 978–986.
View Full Article (HTML) Get PDF (1079K)