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Published in: Anatomical Science International 3/2011

01-09-2011 | Original Article

The fibrillar organisation of the osteon and cellular aspects of its development

A morphological study using the SEM fractured cortex technique

Authors: Ugo E. Pazzaglia, Terenzio Congiu, Guido Zarattini, Marcella Marchese, Daniela Quacci

Published in: Anatomical Science International | Issue 3/2011

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Abstract

The collagen architecture of secondary osteons was studied with scanning electron microscopy (SEM) employing the fractured cortex technique and osmic maceration. Fibrillar orientation and the change in their direction in sequential lamellae was documented where lamellar formation was ongoing, as well as in resorption pits where osteoclasts had exposed the collagen organisation of the underlying layers. Applying an adaptive stereo matching technique, the mean thickness of matrix layers removed by osteoclasts was 1.36 ± 0.45 μm. It was also documented that osteoclasts do not attack the cellular membrane of the exposed osteocytes. The mean linear osteoblast density in fractured hemicanals was assessed with SEM and no significant differences were observed comparing larger with smaller central canal osteons. These findings suggested a balance between the differentiated osteoblasts that have aligned on the surface of the cutting cone and those that are transformed into osteocytes, because the canal surface is progressively reduced as the lamellar apposition advances.
Literature
go back to reference Ascenzi A, Bonucci E (1965) An electron microscope study of osteon calcification. J Ultrastruct Res 12:287–303PubMedCrossRef Ascenzi A, Bonucci E (1965) An electron microscope study of osteon calcification. J Ultrastruct Res 12:287–303PubMedCrossRef
go back to reference Ascenzi A, Bonucci E (1968) The compressive properties of single osteons. Anat Rec 161(3):377–391PubMedCrossRef Ascenzi A, Bonucci E (1968) The compressive properties of single osteons. Anat Rec 161(3):377–391PubMedCrossRef
go back to reference Ascenzi A, Benvenuti A, Bonucci E (1982) The tensile properties of single osteonic lamellae: technical problems and preliminary results. J Biomech 15:29–37PubMedCrossRef Ascenzi A, Benvenuti A, Bonucci E (1982) The tensile properties of single osteonic lamellae: technical problems and preliminary results. J Biomech 15:29–37PubMedCrossRef
go back to reference Ascenzi A, Bigi A, Ripamonti A, Roveri N (1983) X-ray diffraction analysis of transversal osteonic lamellae. Calcif Tissue Int 35(3):279–283PubMedCrossRef Ascenzi A, Bigi A, Ripamonti A, Roveri N (1983) X-ray diffraction analysis of transversal osteonic lamellae. Calcif Tissue Int 35(3):279–283PubMedCrossRef
go back to reference Bonucci E (2007) Biological calcification: normal and pathological processes in the early stages. Springer, Heidelberg Bonucci E (2007) Biological calcification: normal and pathological processes in the early stages. Springer, Heidelberg
go back to reference Black J, Mattson R, Korostoff E (1974) Haversian osteons: size, distribution, internal structure, and orientation. J Biomed Mater Res 8(5):299–319PubMedCrossRef Black J, Mattson R, Korostoff E (1974) Haversian osteons: size, distribution, internal structure, and orientation. J Biomed Mater Res 8(5):299–319PubMedCrossRef
go back to reference Boyde A, Hordell MH (1969) Scanning electron microscopy of lamellar bone. Z Zellforsch Mikrosk Anat 93(2):213–231PubMedCrossRef Boyde A, Hordell MH (1969) Scanning electron microscopy of lamellar bone. Z Zellforsch Mikrosk Anat 93(2):213–231PubMedCrossRef
go back to reference Chambers TJ, Revell PA, Fuller K, Athanasou NA (1984) Resorption of bone by isolated rabbit osteoclasts. J Cell Sci 66:383–399PubMed Chambers TJ, Revell PA, Fuller K, Athanasou NA (1984) Resorption of bone by isolated rabbit osteoclasts. J Cell Sci 66:383–399PubMed
go back to reference Elmardi AS, Katchburian MV, Katchburian E (1990) Electron microscopy of developing calvaria reveals images that suggest that osteoclasts engulf and destroy osteocytes during bone resorption. Calcif Tissue Int 46:239–245PubMedCrossRef Elmardi AS, Katchburian MV, Katchburian E (1990) Electron microscopy of developing calvaria reveals images that suggest that osteoclasts engulf and destroy osteocytes during bone resorption. Calcif Tissue Int 46:239–245PubMedCrossRef
go back to reference Frank R, Frank P, Klein M, Fontaine R (1955) Electronic microscopy of normal human compact bone. Arch Anat Pathol (Paris) 44(2):191–206 Frank R, Frank P, Klein M, Fontaine R (1955) Electronic microscopy of normal human compact bone. Arch Anat Pathol (Paris) 44(2):191–206
go back to reference Frasca P, Harper RA, Katz JL (1977) Collagen fiber orientations in human secondary osteons. Acta Anat (Basel) 98(1):1–13CrossRef Frasca P, Harper RA, Katz JL (1977) Collagen fiber orientations in human secondary osteons. Acta Anat (Basel) 98(1):1–13CrossRef
go back to reference Frost HM (1962) Interlamellar thickness in human bone. Clin Orthop Relat Res 24:198–205 Frost HM (1962) Interlamellar thickness in human bone. Clin Orthop Relat Res 24:198–205
go back to reference Fuller K, Thong JT, Breton BC, Chambers TJ (1994) Automated three-dimensional characterization of the osteoclastic resorption lacunae by stereoscopic scanning electron microscopy. J Bone Miner Res 9(1):17–23PubMedCrossRef Fuller K, Thong JT, Breton BC, Chambers TJ (1994) Automated three-dimensional characterization of the osteoclastic resorption lacunae by stereoscopic scanning electron microscopy. J Bone Miner Res 9(1):17–23PubMedCrossRef
go back to reference Gebhardt W (1906) Uber funktionelle wichtige Anordungsweisen der feineren und groβeren Bauelemente des Wirbeltierknochens, II. Spezieller Teil. Der Bau der Haver’schen Lamellen-systeme und seine funktionelle Bedeutung. Archiv für Entwicklungmechanik der Organismen 20:187–322CrossRef Gebhardt W (1906) Uber funktionelle wichtige Anordungsweisen der feineren und groβeren Bauelemente des Wirbeltierknochens, II. Spezieller Teil. Der Bau der Haver’schen Lamellen-systeme und seine funktionelle Bedeutung. Archiv für Entwicklungmechanik der Organismen 20:187–322CrossRef
go back to reference Giraud-Guille MM (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42(3):167–180PubMedCrossRef Giraud-Guille MM (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42(3):167–180PubMedCrossRef
go back to reference Kragstrub J, Nelsen F, Mosekilde L (1983) Thickness of lamellae in normal human iliac trabecular bone. Metab Bone Dis Relat Res 4:291–295CrossRef Kragstrub J, Nelsen F, Mosekilde L (1983) Thickness of lamellae in normal human iliac trabecular bone. Metab Bone Dis Relat Res 4:291–295CrossRef
go back to reference Manelli A, Sangiorgi S, Binaghi E, Raspanti M (2007) 3D analysis of SEM images of corrosion casting using adaptive stereo matching. Microsc Res Tech 70(4):350–354PubMedCrossRef Manelli A, Sangiorgi S, Binaghi E, Raspanti M (2007) 3D analysis of SEM images of corrosion casting using adaptive stereo matching. Microsc Res Tech 70(4):350–354PubMedCrossRef
go back to reference Marotti G (1973) Decrement in volume of osteoblasts during osteon formation and its effect on the size of the corresponding osteocytes. In: Meunier PJ (ed) Bone histomorphometry. Armour Montagu, Levallois, 1976, pp 385–397 Marotti G (1973) Decrement in volume of osteoblasts during osteon formation and its effect on the size of the corresponding osteocytes. In: Meunier PJ (ed) Bone histomorphometry. Armour Montagu, Levallois, 1976, pp 385–397
go back to reference Marotti G (1993) A new theory of bone lamellation. Calcif Tissue Int 53(S1):47–55CrossRef Marotti G (1993) A new theory of bone lamellation. Calcif Tissue Int 53(S1):47–55CrossRef
go back to reference Marotti G, Muglia MA (1988) A scanning electron microscope study of human bony lamellae. Proposal for a new model of collagen lamellar organization. Arch Ital Anat Embriol 93(3):163–175PubMed Marotti G, Muglia MA (1988) A scanning electron microscope study of human bony lamellae. Proposal for a new model of collagen lamellar organization. Arch Ital Anat Embriol 93(3):163–175PubMed
go back to reference Marotti G, Ferretti M, Muglia MA, Palumbo C, Palazzini S (1992) A quantitative evaluation of osteoblast–osteocyte relationships on growing endosteal surface of rabbit tibiae. Bone 13(5):363–368PubMedCrossRef Marotti G, Ferretti M, Muglia MA, Palumbo C, Palazzini S (1992) A quantitative evaluation of osteoblast–osteocyte relationships on growing endosteal surface of rabbit tibiae. Bone 13(5):363–368PubMedCrossRef
go back to reference Palumbo C (1986) A three-dimensional ultrastructural study of osteoid-osteocytes in the tibia of chick embryos. Cell Tissue Res 246(1):125–131PubMedCrossRef Palumbo C (1986) A three-dimensional ultrastructural study of osteoid-osteocytes in the tibia of chick embryos. Cell Tissue Res 246(1):125–131PubMedCrossRef
go back to reference Palumbo C, Palazzini S, Zaffe D, Marotti G (1990) Osteocyte differentiation in the tibia of newborn rabbits: an ultrastructural study of the formation of cytoplasmic processes. Acta Anat (Basel) 137(4):350–358CrossRef Palumbo C, Palazzini S, Zaffe D, Marotti G (1990) Osteocyte differentiation in the tibia of newborn rabbits: an ultrastructural study of the formation of cytoplasmic processes. Acta Anat (Basel) 137(4):350–358CrossRef
go back to reference Pazzaglia UE, Andrini L, Di Nucci A (1997) The reaction to nailing or cementing of the femur in rats. A microangiographic and fluorescence study. Int Orthop 21(4):267–273PubMedCrossRef Pazzaglia UE, Andrini L, Di Nucci A (1997) The reaction to nailing or cementing of the femur in rats. A microangiographic and fluorescence study. Int Orthop 21(4):267–273PubMedCrossRef
go back to reference Pazzaglia UE, Congiu T, Raspanti M, Ranchetti F, Quacci D (2009a) Anatomy of the intracortical canal system: scanning electron microscopy study in rabbit femur. Clin Orthop Relat Res 467:2449–2456CrossRef Pazzaglia UE, Congiu T, Raspanti M, Ranchetti F, Quacci D (2009a) Anatomy of the intracortical canal system: scanning electron microscopy study in rabbit femur. Clin Orthop Relat Res 467:2449–2456CrossRef
go back to reference Pazzaglia UE, Congiu T, Ranchetti F, Salari M, Dell’Orbo C (2009b) Scanning electron microscopy study of bone intracortical vessels using an injection and fractured surfaces technique. Anat Sci Int 85:31–27. doi:10.1007/s12565-009-0049-7 Pazzaglia UE, Congiu T, Ranchetti F, Salari M, Dell’Orbo C (2009b) Scanning electron microscopy study of bone intracortical vessels using an injection and fractured surfaces technique. Anat Sci Int 85:31–27. doi:10.​1007/​s12565-009-0049-7
go back to reference Pazzaglia UE, Congiu T, Marchese M, Dell’Orbo C (2010) The shape modulation of osteoblast–osteocyte transformation and its correlation with fibrillar organization in secondary osteons. A SEM study employing the graded osmic maceration technique. Cell Tissue Res 340:533–540PubMedCrossRef Pazzaglia UE, Congiu T, Marchese M, Dell’Orbo C (2010) The shape modulation of osteoblast–osteocyte transformation and its correlation with fibrillar organization in secondary osteons. A SEM study employing the graded osmic maceration technique. Cell Tissue Res 340:533–540PubMedCrossRef
go back to reference Raspanti M, Guizzardi S, De Pasquale V, Martini D, Ruggeri A (1994) Ultrastructure of heat-deproteinated compact bone. Biomaterials 15(6):433–437PubMedCrossRef Raspanti M, Guizzardi S, De Pasquale V, Martini D, Ruggeri A (1994) Ultrastructure of heat-deproteinated compact bone. Biomaterials 15(6):433–437PubMedCrossRef
go back to reference Raspanti M, Guizzardi S, Strocchi R, Ruggeri A (1996) Collagen fibril patterns in compact bone: preliminary ultrastructural observations. Acta Anat (Basel) 155(4):249–256CrossRef Raspanti M, Guizzardi S, Strocchi R, Ruggeri A (1996) Collagen fibril patterns in compact bone: preliminary ultrastructural observations. Acta Anat (Basel) 155(4):249–256CrossRef
go back to reference Reid SA (1986) A study of lamellar organisation in juvenile and adult human bone. Anat Embryol (Berlin) 174(3):329–338CrossRef Reid SA (1986) A study of lamellar organisation in juvenile and adult human bone. Anat Embryol (Berlin) 174(3):329–338CrossRef
go back to reference Riggs CM, Lanyon LE, Boyde A (1993a) Functional associations between collagen fibres orientation and locomotor strain direction in cortical bone of the equine radius. Anat Embryol (Berlin) 187(3):231–238 Riggs CM, Lanyon LE, Boyde A (1993a) Functional associations between collagen fibres orientation and locomotor strain direction in cortical bone of the equine radius. Anat Embryol (Berlin) 187(3):231–238
go back to reference Riggs CM, Vaughan LC, Evans GP, Lanyon LE, Boyde A (1993b) Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anat Embryol (Berlin) 187(3):239–248 Riggs CM, Vaughan LC, Evans GP, Lanyon LE, Boyde A (1993b) Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anat Embryol (Berlin) 187(3):239–248
go back to reference Rouiller C, Huber L, Kellenberger E, Rutishauser E (1952) The lamellar structure of the osteon. Acta Anat (Basel) 14(1–2):9–22CrossRef Rouiller C, Huber L, Kellenberger E, Rutishauser E (1952) The lamellar structure of the osteon. Acta Anat (Basel) 14(1–2):9–22CrossRef
go back to reference Ruth EB (1953) Bone studies. II. An experimental study of the Haversian-type vascular channels. Am J Anat 93(3):429–455PubMedCrossRef Ruth EB (1953) Bone studies. II. An experimental study of the Haversian-type vascular channels. Am J Anat 93(3):429–455PubMedCrossRef
go back to reference Smith JW (1960) The arrangement of collagen fibres in human secondary osteones. J Bone Joint Surg Br 42-B:588–605PubMed Smith JW (1960) The arrangement of collagen fibres in human secondary osteones. J Bone Joint Surg Br 42-B:588–605PubMed
go back to reference Smith JW (1963) Age changes in the organic fraction of bone. J Bone Joint Surg Br 45:761–769PubMed Smith JW (1963) Age changes in the organic fraction of bone. J Bone Joint Surg Br 45:761–769PubMed
go back to reference Wagermaier W, Gupta HS, Gourrier A, Burghammer M, Roschger P, Fratzi P (2006) Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1(1):1PubMedCrossRef Wagermaier W, Gupta HS, Gourrier A, Burghammer M, Roschger P, Fratzi P (2006) Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1(1):1PubMedCrossRef
go back to reference Weidenreich F (1923) Knochenstudien 1. Über Aufbau und Entwicklung des Knochens und der Chowauter des Knochengewebes. Z Anat Entwickl Gesch 69:382–466CrossRef Weidenreich F (1923) Knochenstudien 1. Über Aufbau und Entwicklung des Knochens und der Chowauter des Knochengewebes. Z Anat Entwickl Gesch 69:382–466CrossRef
go back to reference Weiner S, Traub W, Wagner HD (1999) Lamellar bone: structure–function relations. J Struct Biol 126:241–255PubMedCrossRef Weiner S, Traub W, Wagner HD (1999) Lamellar bone: structure–function relations. J Struct Biol 126:241–255PubMedCrossRef
go back to reference Ziegler O (1906) Studien über die feinere Struktur des Rőhrenknochens und dessen Polarisation. Dtsch Z Chir 85:248–263CrossRef Ziegler O (1906) Studien über die feinere Struktur des Rőhrenknochens und dessen Polarisation. Dtsch Z Chir 85:248–263CrossRef
Metadata
Title
The fibrillar organisation of the osteon and cellular aspects of its development
A morphological study using the SEM fractured cortex technique
Authors
Ugo E. Pazzaglia
Terenzio Congiu
Guido Zarattini
Marcella Marchese
Daniela Quacci
Publication date
01-09-2011
Publisher
Springer Japan
Published in
Anatomical Science International / Issue 3/2011
Print ISSN: 1447-6959
Electronic ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-010-0099-x

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