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Published in: Calcified Tissue International 6/2003

01-06-2003 | Laboratory Investigations

Microstructural Classification of Resorption Lacunae and Perforations in Human Proximal Femora

Authors: C. Gentzsch, G. Delling, E. Kaiser

Published in: Calcified Tissue International | Issue 6/2003

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Abstract

Resorption lacunae and perforation types mirror resorptional activity of osteoclasts and are important for the integrity of bone architecture. In the present study, distinctive microstructural features of cancellous bone dissected from femoral heads of 28 autopsy subjects (14 females and 14 males) were defined and evaluated by light microscopic (LM) histology and scanning electron microscopy (SEM). The work differentiates two types of resorption lacunae in trabecular bone: the longitudinally extended resorption lacunae (LER) and the reticulate patch resorption lacunae (RPR). Further, two types of perforations are distinguished: the lacunar perforation (LP) and the tunneling perforation (TP), which are differentiated from potential blood vessel canals (BC). Evidence is presented that the spatial distribution on rods or plates is highly correlated with the resorption type. The RPR type was more frequently seen and was primarily localized at the nodes of rods, in the middle regions of rods, and in the center region of plates as compared to the LER type. The presented evaluation scheme of resorption and perforation types could prove useful in future studies for systematically investigating potential microstructural changes associated with disturbed bone turnover.
Literature
2.
go back to reference Dubey, A, Koval, KJ, Zuckerman, JD 1999Hip fracture epidemiology: a review.Am J Orthop28497506PubMed Dubey, A, Koval, KJ, Zuckerman, JD 1999Hip fracture epidemiology: a review.Am J Orthop28497506PubMed
3.
go back to reference De Laet, CE, Pols, HA 2000Fractures in the elderly: epidemiology and demography.Baillieres Best Pract Res Clin Endocrinol Metab14171179CrossRefPubMed De Laet, CE, Pols, HA 2000Fractures in the elderly: epidemiology and demography.Baillieres Best Pract Res Clin Endocrinol Metab14171179CrossRefPubMed
4.
go back to reference Wand, JS, Smith, T, Green, JR, Hesp, R, Bradbeer, JN, Reeve, J 1992Whole-body and site-specific bone remodelling in patients with previous femoral fractures: relationships between reduced physical activity, reduced bone mass and increased bone resorption.Clin Sci (Lond)83665675 Wand, JS, Smith, T, Green, JR, Hesp, R, Bradbeer, JN, Reeve, J 1992Whole-body and site-specific bone remodelling in patients with previous femoral fractures: relationships between reduced physical activity, reduced bone mass and increased bone resorption.Clin Sci (Lond)83665675
5.
go back to reference Reeve, J, Zanelli, JM, Garrahan, N, Bradbeer, JN, Wand, JS, Moyes, ST, Roux, JP, Smith, T 1993Bone remodeling in hip fracture.Calcif Tissue Int53S108112PubMed Reeve, J, Zanelli, JM, Garrahan, N, Bradbeer, JN, Wand, JS, Moyes, ST, Roux, JP, Smith, T 1993Bone remodeling in hip fracture.Calcif Tissue Int53S108112PubMed
6.
go back to reference Dresner-Pollak, R, Parker, RA, Poku, M, Thompson, J, Seibel, MJ, Greenspan, SL 1996Biochemical markers of bone turnover reflect femoral bone loss in elderly women.Calcif Tissue Int59328333CrossRefPubMed Dresner-Pollak, R, Parker, RA, Poku, M, Thompson, J, Seibel, MJ, Greenspan, SL 1996Biochemical markers of bone turnover reflect femoral bone loss in elderly women.Calcif Tissue Int59328333CrossRefPubMed
7.
go back to reference Tsai, KS, Pan, WH, Hsu, SH, Cheng, WC, Chen, CK, Chieng, PU, Yang, RS, Twu, ST 1996Sexual differences in bone markers and bone mineral density of normal Chinese.Calcif Tissue Int59454460CrossRefPubMed Tsai, KS, Pan, WH, Hsu, SH, Cheng, WC, Chen, CK, Chieng, PU, Yang, RS, Twu, ST 1996Sexual differences in bone markers and bone mineral density of normal Chinese.Calcif Tissue Int59454460CrossRefPubMed
8.
go back to reference Fazzalari, NL, Kuliwaba, JS, Atkins, GJ, Forwood, MR, Findlay, DM 2001The ratio of messenger RNA levels of receptor activator of nuclear factor kappaB ligand to osteoprotegerin correlates with bone remodeling indices in normal human cancellous bone but not in osteoarthritis.J Bone Miner Res1610151027PubMed Fazzalari, NL, Kuliwaba, JS, Atkins, GJ, Forwood, MR, Findlay, DM 2001The ratio of messenger RNA levels of receptor activator of nuclear factor kappaB ligand to osteoprotegerin correlates with bone remodeling indices in normal human cancellous bone but not in osteoarthritis.J Bone Miner Res1610151027PubMed
9.
go back to reference Kanis, JA 1994Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group.Osteoporos Int4368381PubMed Kanis, JA 1994Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group.Osteoporos Int4368381PubMed
10.
go back to reference Amling, M, Posl, M, Ritzel, H, Hahn, M, Vogel, M, Wening, VJ, Delling, G 1996Architecture and distribution of cancellous bone yield vertebral fracture clues. A histomorphometric analysis of the complete spinal column from 40 autopsy specimens.Arch Orthop Trauma Surg115262269PubMed Amling, M, Posl, M, Ritzel, H, Hahn, M, Vogel, M, Wening, VJ, Delling, G 1996Architecture and distribution of cancellous bone yield vertebral fracture clues. A histomorphometric analysis of the complete spinal column from 40 autopsy specimens.Arch Orthop Trauma Surg115262269PubMed
11.
go back to reference Delling, G, Amling, M 1995Biomechanical stability of the skeleton—it is not only bone mass, but also bone structure that counts.Nephrol Dial Transplant10601606PubMed Delling, G, Amling, M 1995Biomechanical stability of the skeleton—it is not only bone mass, but also bone structure that counts.Nephrol Dial Transplant10601606PubMed
12.
go back to reference Dempster, DW 2000The contribution of trabecular architecture to cancellous bone quality.J Bone Miner Res152023PubMed Dempster, DW 2000The contribution of trabecular architecture to cancellous bone quality.J Bone Miner Res152023PubMed
14.
go back to reference Legrand, E, Hedde, C, Gallois, Y, Degasne, I, Boux de Casson, F, Mathieu, E, Basle, MF, Chappard, D, Audran, M 2001Osteoporosis in men: a potential role for the sex hormone binding globulin.Bone299095CrossRefPubMed Legrand, E, Hedde, C, Gallois, Y, Degasne, I, Boux de Casson, F, Mathieu, E, Basle, MF, Chappard, D, Audran, M 2001Osteoporosis in men: a potential role for the sex hormone binding globulin.Bone299095CrossRefPubMed
15.
go back to reference Delling, G 1989Neuere Vorstellungen zu Bau und Struktur der menschlichen Spongiosa-Ergebnisse einer kombinierten zwei- und dreidimensionalen Analyse.Z gesamte inn Med44536540PubMed Delling, G 1989Neuere Vorstellungen zu Bau und Struktur der menschlichen Spongiosa-Ergebnisse einer kombinierten zwei- und dreidimensionalen Analyse.Z gesamte inn Med44536540PubMed
16.
go back to reference Parfitt, AM, Mathews, CH, Villanueva, AR, Kleerekoper, M, Frame, B, Rao, DS 1983Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss.J Clin Invest7213961409PubMed Parfitt, AM, Mathews, CH, Villanueva, AR, Kleerekoper, M, Frame, B, Rao, DS 1983Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss.J Clin Invest7213961409PubMed
17.
go back to reference Parfitt, AM 1984Age-related structural changes in trabecular and cortical bone: cellular mechanisms and biomechanical consequences.Calcif Tissue Int36S123128PubMed Parfitt, AM 1984Age-related structural changes in trabecular and cortical bone: cellular mechanisms and biomechanical consequences.Calcif Tissue Int36S123128PubMed
18.
go back to reference Mosekilde, L 1998The effect of modelling and remodelling on human vertebral body architecture.Technol Health Care6287297PubMed Mosekilde, L 1998The effect of modelling and remodelling on human vertebral body architecture.Technol Health Care6287297PubMed
19.
go back to reference Mosekilde, L 2000Age-related changes in bone mass, structure, and strength—effects of loading.Z Rheumatol5919CrossRef Mosekilde, L 2000Age-related changes in bone mass, structure, and strength—effects of loading.Z Rheumatol5919CrossRef
20.
go back to reference Melsen, F, Steiniche, T, Eriksen, E, Mosekilde, L, Vesterby, A 1996Bone remodeling and bone structure in osteoporosis.Broell, HDambacher, M eds. Osteoporosis: a guide to diagnosis and treatment.RheumatolgyKrager, Basel2838 Melsen, F, Steiniche, T, Eriksen, E, Mosekilde, L, Vesterby, A 1996Bone remodeling and bone structure in osteoporosis.Broell, HDambacher, M eds. Osteoporosis: a guide to diagnosis and treatment.RheumatolgyKrager, Basel2838
21.
go back to reference Krempien, B 1979Bone modelling processes at the endosteal surface of human femora. Scanning electron microscopical studies in normal bone and in renal osteodystrophy.Virchows Arch A Pathol Anat Histol3827388PubMed Krempien, B 1979Bone modelling processes at the endosteal surface of human femora. Scanning electron microscopical studies in normal bone and in renal osteodystrophy.Virchows Arch A Pathol Anat Histol3827388PubMed
22.
go back to reference Eriksen, E, Mosekilde, L, Melsen, F 1985Trabecular bone resorption depth increases with age: differences between normal males and females.Bone6141146PubMed Eriksen, E, Mosekilde, L, Melsen, F 1985Trabecular bone resorption depth increases with age: differences between normal males and females.Bone6141146PubMed
23.
go back to reference Parfitt, AM 1987Trabecular bone architecture in the pathogenesis and prevention of fracture.Am J Med826872 Parfitt, AM 1987Trabecular bone architecture in the pathogenesis and prevention of fracture.Am J Med826872
24.
go back to reference Kukita, A, Chenu, C, McManus, LM, Mundy, GR, Roodman, GD 1990Atypical multinucleated cells form in long-term marrow cultures from patients with Paget’s disease.J Clin Invest8512801286PubMed Kukita, A, Chenu, C, McManus, LM, Mundy, GR, Roodman, GD 1990Atypical multinucleated cells form in long-term marrow cultures from patients with Paget’s disease.J Clin Invest8512801286PubMed
25.
go back to reference Marks Jr, SC, Cielinski, MJ, Sundquist, KT 1996Bone surface morphology reflects local skeletal metabolism.Microsc Res Tech33121127CrossRefPubMed Marks Jr, SC, Cielinski, MJ, Sundquist, KT 1996Bone surface morphology reflects local skeletal metabolism.Microsc Res Tech33121127CrossRefPubMed
26.
go back to reference Kameda, T, Mano, H, Yuasa, T, Mori, Y, Miyazawa, K, Shiokawa, M, Nakamaru, Y, Hiroi, E, Hiura, K, Kameda, A, Yang, NN, Hakeda, Y, Kumegawa, M 1997Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts.J Exp Med186489495PubMed Kameda, T, Mano, H, Yuasa, T, Mori, Y, Miyazawa, K, Shiokawa, M, Nakamaru, Y, Hiroi, E, Hiura, K, Kameda, A, Yang, NN, Hakeda, Y, Kumegawa, M 1997Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts.J Exp Med186489495PubMed
27.
go back to reference Delling, G, Vogel, M, Wieland, U, Pompesius-Kempa, M, Hahn, M 1988Trabecular bone structure in the human spine: results of a new 2- and 3-dimensional analysis.Takahashi, H eds. Bone morphometry.Nishimura Co., Ltd.Niigata, Japan256259 Delling, G, Vogel, M, Wieland, U, Pompesius-Kempa, M, Hahn, M 1988Trabecular bone structure in the human spine: results of a new 2- and 3-dimensional analysis.Takahashi, H eds. Bone morphometry.Nishimura Co., Ltd.Niigata, Japan256259
28.
go back to reference Thomsen, JS, Mosekilde, L, Boyce, RW, Mosekilde, E 1994Stochastic simulation of vertebral trabecular bone remodeling.Bone15655666PubMed Thomsen, JS, Mosekilde, L, Boyce, RW, Mosekilde, E 1994Stochastic simulation of vertebral trabecular bone remodeling.Bone15655666PubMed
29.
go back to reference Van Der Linden, JC, Verhaar, JA, Weinans, H 2001A three-dimensional simulation of age-related remodeling in trabecular bone.J Bone Miner Res16688696PubMed Van Der Linden, JC, Verhaar, JA, Weinans, H 2001A three-dimensional simulation of age-related remodeling in trabecular bone.J Bone Miner Res16688696PubMed
30.
go back to reference Thomsen, JS, Ebbesen, EN, Mosekilde, L 2000A new method of comprehensive static histomorphometry applied on human lumbar vertebral cancellous bone.Bone27129138CrossRefPubMed Thomsen, JS, Ebbesen, EN, Mosekilde, L 2000A new method of comprehensive static histomorphometry applied on human lumbar vertebral cancellous bone.Bone27129138CrossRefPubMed
31.
go back to reference Sugita, H, Oka, M, Toguchida, J, Nakamura, T, Ueo, T, Hayami, T 1999Anisotropy of osteoporotic cancellous bone.Bone24513516CrossRefPubMed Sugita, H, Oka, M, Toguchida, J, Nakamura, T, Ueo, T, Hayami, T 1999Anisotropy of osteoporotic cancellous bone.Bone24513516CrossRefPubMed
32.
go back to reference Fazzalari, NL, Parkinson, IH 1998Fractal properties of cancellous bone of the iliac crest in vertebral crush fracture.Bone235357CrossRefPubMed Fazzalari, NL, Parkinson, IH 1998Fractal properties of cancellous bone of the iliac crest in vertebral crush fracture.Bone235357CrossRefPubMed
33.
go back to reference Andresen, R, Radmer, S, Banzer, D 1998Bone mineral density and spongiosa architecture in correlation to vertebral body insufficiency fractures.Acta Radiol39538542PubMed Andresen, R, Radmer, S, Banzer, D 1998Bone mineral density and spongiosa architecture in correlation to vertebral body insufficiency fractures.Acta Radiol39538542PubMed
34.
go back to reference Currey, J 1959Differences in the tensile strength of bone of different histological types.J Anat938795PubMed Currey, J 1959Differences in the tensile strength of bone of different histological types.J Anat938795PubMed
35.
go back to reference Mori, S, Harruff, R, Ambrosius, W, Burr, DB 1997Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures.Bone21521526CrossRefPubMed Mori, S, Harruff, R, Ambrosius, W, Burr, DB 1997Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures.Bone21521526CrossRefPubMed
36.
go back to reference Jones, SJ, Boyde, A 1993Histomorphometry of Howship’s lacunae formed in vivo and in vitro: depths and volumes measured by scanning electron and confocal microscopy.Bone14455460PubMed Jones, SJ, Boyde, A 1993Histomorphometry of Howship’s lacunae formed in vivo and in vitro: depths and volumes measured by scanning electron and confocal microscopy.Bone14455460PubMed
37.
go back to reference Jones, SJ, Boyde, A, Ali, N, Maconnachie, E 1985A review of bone cell and substratum interactions.Scanning7524 Jones, SJ, Boyde, A, Ali, N, Maconnachie, E 1985A review of bone cell and substratum interactions.Scanning7524
38.
go back to reference Jones, SJ, Boyde, A, Ali, NN 1984The resorption of biological and non-biological substrates by cultured avian and mammalian osteoclasts.Anat Embryol170247256PubMed Jones, SJ, Boyde, A, Ali, NN 1984The resorption of biological and non-biological substrates by cultured avian and mammalian osteoclasts.Anat Embryol170247256PubMed
39.
go back to reference Reid, SA 1986Effect of mineral content of human bone on in vitro resorption.Anat Embryol174225234PubMed Reid, SA 1986Effect of mineral content of human bone on in vitro resorption.Anat Embryol174225234PubMed
40.
go back to reference Fuller, K, Thong, JT, Breton, BC, Chambers, TJ 1994Automated three-dimensional characterization of osteoclastic resorption lacunae by stereoscopic scanning electron microscopy.J Bone Miner Res91723PubMed Fuller, K, Thong, JT, Breton, BC, Chambers, TJ 1994Automated three-dimensional characterization of osteoclastic resorption lacunae by stereoscopic scanning electron microscopy.J Bone Miner Res91723PubMed
41.
go back to reference Boyde, A, Jones, SJ 1991Pitfalls in pit measurement.Calcif Tissue Int496570PubMed Boyde, A, Jones, SJ 1991Pitfalls in pit measurement.Calcif Tissue Int496570PubMed
42.
go back to reference Boyde, A, Ali, NN, Jones, SJ 1985Optical and scanning electron microscopy in the single osteoclast resorption assay.Scan Electron Microsc 12591271 Boyde, A, Ali, NN, Jones, SJ 1985Optical and scanning electron microscopy in the single osteoclast resorption assay.Scan Electron Microsc 12591271
43.
go back to reference Boyde, A, Ali, NN, Jones, SJ 1984Resorption of dentine by isolated osteoclasts in vitro.Br Dent J156216220PubMed Boyde, A, Ali, NN, Jones, SJ 1984Resorption of dentine by isolated osteoclasts in vitro.Br Dent J156216220PubMed
44.
go back to reference Boyde, A, Elliott, JC, Jones, SJ 1993Stereology and histogram analysis of backscattered electron images: age changes in bone.Bone14205210PubMed Boyde, A, Elliott, JC, Jones, SJ 1993Stereology and histogram analysis of backscattered electron images: age changes in bone.Bone14205210PubMed
45.
go back to reference Jones, SJ, Piper, K, Vesely, P, Gray, C, Boyde, A 1994The significance of the size of an osteoclast.Davidovitch, Z eds. The biological mechanisms of tooth eruption, resorption and replacement by implants.Harvard Society for the Advancement of OrthodonticsBoston, MA5571 Jones, SJ, Piper, K, Vesely, P, Gray, C, Boyde, A 1994The significance of the size of an osteoclast.Davidovitch, Z eds. The biological mechanisms of tooth eruption, resorption and replacement by implants.Harvard Society for the Advancement of OrthodonticsBoston, MA5571
46.
go back to reference Boyde, A, Jones, SJ 1998Aspects of anatomy and development of bone: the nm, um, and mm hierarchy.Advances in organ biology.JAI Press Inc.344 Boyde, A, Jones, SJ 1998Aspects of anatomy and development of bone: the nm, um, and mm hierarchy.Advances in organ biology.JAI Press Inc.344
47.
go back to reference Boyde, A, Jones, SJ 1996Scanning electron microscopy of bone: instrument, specimen, and issues.Microsc Res Tech3392120CrossRefPubMed Boyde, A, Jones, SJ 1996Scanning electron microscopy of bone: instrument, specimen, and issues.Microsc Res Tech3392120CrossRefPubMed
48.
go back to reference Jayasinghe, JA, Jones, SJ, Boyde, A 1993Scanning electron microscopy of human lumbar vertebral trabecular bone surfaces.Virchows Arch A Pathol Anat Histopathol4222534PubMed Jayasinghe, JA, Jones, SJ, Boyde, A 1993Scanning electron microscopy of human lumbar vertebral trabecular bone surfaces.Virchows Arch A Pathol Anat Histopathol4222534PubMed
49.
go back to reference Jones, SJ, Boyde, A 1994aQuestions of quality and quantity—a morphological view of bone biology.Kaibogaku Zasshi69229243 Jones, SJ, Boyde, A 1994aQuestions of quality and quantity—a morphological view of bone biology.Kaibogaku Zasshi69229243
50.
go back to reference Kingsmill, VJ, Boyde, A 2001Collagen fiber orientation affects osteoclastic resorption.J Dent Res8020852088PubMed Kingsmill, VJ, Boyde, A 2001Collagen fiber orientation affects osteoclastic resorption.J Dent Res8020852088PubMed
51.
go back to reference Babo, Hv, Heuck, F 1974Hormonal bedingte Knochenveränderungen bei der renalen Osteopathie.Radiologe14225231PubMed Babo, Hv, Heuck, F 1974Hormonal bedingte Knochenveränderungen bei der renalen Osteopathie.Radiologe14225231PubMed
52.
go back to reference Cohen-Solal, ME, Graulet, AM, Gueris, J, Denne, MA, Bergot, C, Morieux, C, Sedel, L, Kuntz, D, De Vernejoul, MC 1995Bone resorption at the femoral neck is dependent on local factors in nonosteoporotic late postmenopausal women: an in vitro-in vivo study.J Bone Miner Res10307314PubMed Cohen-Solal, ME, Graulet, AM, Gueris, J, Denne, MA, Bergot, C, Morieux, C, Sedel, L, Kuntz, D, De Vernejoul, MC 1995Bone resorption at the femoral neck is dependent on local factors in nonosteoporotic late postmenopausal women: an in vitro-in vivo study.J Bone Miner Res10307314PubMed
53.
go back to reference Gentzsch, C, Jung, M, Pueschel, ., Delling, G, Kaiser, E 2002Scanning electron microscopy: New approach for evaluating the amount of resorption lacunae in cancellous bone..in pressMATH Gentzsch, C, Jung, M, Pueschel, ., Delling, G, Kaiser, E 2002Scanning electron microscopy: New approach for evaluating the amount of resorption lacunae in cancellous bone..in pressMATH
54.
go back to reference Horikoshi, T, Endo, N, Uchiyama, T, Tanizawa, T, Takahashi, HE 1999Peripheral quantitative computed tomography of the femoral neck in 60 Japanese women.Calcif Tissue Int65447453CrossRefPubMed Horikoshi, T, Endo, N, Uchiyama, T, Tanizawa, T, Takahashi, HE 1999Peripheral quantitative computed tomography of the femoral neck in 60 Japanese women.Calcif Tissue Int65447453CrossRefPubMed
55.
go back to reference Fazzalari, NL, Moore, RJ, Manthey, BA, Vernon-Roberts, B 1989Comparative study of iliac crest and proximal femur histomorphometry in normal patients.J Clin Pathol42745748PubMed Fazzalari, NL, Moore, RJ, Manthey, BA, Vernon-Roberts, B 1989Comparative study of iliac crest and proximal femur histomorphometry in normal patients.J Clin Pathol42745748PubMed
56.
go back to reference Dempster, DW, Shane, E, Horbert, W, Lindsay, R 1986A simple method for correlative light and scanning electron microscopy of human iliac crest bone biopsies: qualitative observations in normal and osteoporotic subjects.J Bone Miner Res11521PubMed Dempster, DW, Shane, E, Horbert, W, Lindsay, R 1986A simple method for correlative light and scanning electron microscopy of human iliac crest bone biopsies: qualitative observations in normal and osteoporotic subjects.J Bone Miner Res11521PubMed
57.
go back to reference Amling, M, Herden, S, Posl, M, Hahn, M, Ritzel, H, Delling, G 1996Heterogeneity of the skeleton: comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus.J Bone Miner Res113645PubMed Amling, M, Herden, S, Posl, M, Hahn, M, Ritzel, H, Delling, G 1996Heterogeneity of the skeleton: comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus.J Bone Miner Res113645PubMed
58.
go back to reference Chai, B, Tang, X, Zhou, W, Li, H 1996A scanning electron microscopic study of trabeculae in osteoporotic femoral head.Chin Med J (Engl)109399403 Chai, B, Tang, X, Zhou, W, Li, H 1996A scanning electron microscopic study of trabeculae in osteoporotic femoral head.Chin Med J (Engl)109399403
60.
go back to reference Hahn, M, Vogel, M, Amling, M, Ritzel, H, Delling, G 1995Microcallus formations of the cancellous bone: a quantitative analysis of the human spine.J Bone Miner Res1014101416PubMed Hahn, M, Vogel, M, Amling, M, Ritzel, H, Delling, G 1995Microcallus formations of the cancellous bone: a quantitative analysis of the human spine.J Bone Miner Res1014101416PubMed
61.
go back to reference Amling, M, Grote, HJ, Vogel, M, Hahn, M, Delling, G 1994Three-dimensional analysis of the spine in autopsy cases with renal osteodystrophy.Kidney Int46733743PubMed Amling, M, Grote, HJ, Vogel, M, Hahn, M, Delling, G 1994Three-dimensional analysis of the spine in autopsy cases with renal osteodystrophy.Kidney Int46733743PubMed
62.
go back to reference Parfitt, A 1979Bone remodeling: relationship to the amount of structure of bone, and the pathogenesis and prevention of fractures.Riggs, LMelton, L eds. Osteoporosis: etiology, diagnosis and management.Raven PressNew York4593 Parfitt, A 1979Bone remodeling: relationship to the amount of structure of bone, and the pathogenesis and prevention of fractures.Riggs, LMelton, L eds. Osteoporosis: etiology, diagnosis and management.Raven PressNew York4593
63.
go back to reference Ascenzi, MG 1999A first estimation of prestress in so-called circularly fibered osteonic lamellae.J Biomech32935942PubMed Ascenzi, MG 1999A first estimation of prestress in so-called circularly fibered osteonic lamellae.J Biomech32935942PubMed
64.
go back to reference Vincentelli, R 1978Relation between collagen fiber orientation and age of osteon formation in human tibial compact bone.Acta Anat100120128 Vincentelli, R 1978Relation between collagen fiber orientation and age of osteon formation in human tibial compact bone.Acta Anat100120128
65.
go back to reference Kanehisa, J, Heersche, JN 1988Osteoclastic bone resorption: in vitro analysis of the rate of resorption and migration of individual osteoclasts.Bone97379PubMed Kanehisa, J, Heersche, JN 1988Osteoclastic bone resorption: in vitro analysis of the rate of resorption and migration of individual osteoclasts.Bone97379PubMed
66.
go back to reference Jones, SJ, Boyde, A, Ali, NN 1986The interface of cells and their matrices in mineralized tissues: a review.Scan Electron Microsc15551569 Jones, SJ, Boyde, A, Ali, NN 1986The interface of cells and their matrices in mineralized tissues: a review.Scan Electron Microsc15551569
67.
go back to reference Fuller, K, Owens, JM, Chambers, TJ 1995Macrophage inflammatory protein-1 alpha and IL-8 stimulate the motility but suppress the resorption of isolated rat osteoclasts.J Immunol15460656072PubMed Fuller, K, Owens, JM, Chambers, TJ 1995Macrophage inflammatory protein-1 alpha and IL-8 stimulate the motility but suppress the resorption of isolated rat osteoclasts.J Immunol15460656072PubMed
68.
go back to reference Ali, NN, Boyde, A, Jones, SJ 1984Motility and resorption: osteoclastic activity in vitro.Anat Embryol1705156PubMed Ali, NN, Boyde, A, Jones, SJ 1984Motility and resorption: osteoclastic activity in vitro.Anat Embryol1705156PubMed
69.
go back to reference Zaidi, M, Adebanjo, OA, Moonga, BS, Sun, L, Huang, CL 1999Emerging insights into the role of calcium ions in osteoclast regulation.J Bone Miner Res14669674PubMed Zaidi, M, Adebanjo, OA, Moonga, BS, Sun, L, Huang, CL 1999Emerging insights into the role of calcium ions in osteoclast regulation.J Bone Miner Res14669674PubMed
70.
go back to reference Zaidi, M, Moonga, BS, Adebanjo, OA 1999Novel mechanisms of calcium handling by the osteoclast: a review-hypothesis.Proc Assoc Am Physicians111319327PubMed Zaidi, M, Moonga, BS, Adebanjo, OA 1999Novel mechanisms of calcium handling by the osteoclast: a review-hypothesis.Proc Assoc Am Physicians111319327PubMed
71.
go back to reference Reid, SA, Boyde, A 1987Changes in the mineral density distribution in human bone with age: image analysis using backscattered electrons in the SEM.J Bone Miner Res21322PubMed Reid, SA, Boyde, A 1987Changes in the mineral density distribution in human bone with age: image analysis using backscattered electrons in the SEM.J Bone Miner Res21322PubMed
72.
go back to reference Lanyon, L, Skerry, T 2001Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis.J Bone Miner Res1619371947PubMed Lanyon, L, Skerry, T 2001Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis.J Bone Miner Res1619371947PubMed
73.
go back to reference Smit, TH, Burger, EH 2000Is BMU-coupling a strain-regulated phenomenon? A finite element analysis.J Bone Miner Res15301307PubMed Smit, TH, Burger, EH 2000Is BMU-coupling a strain-regulated phenomenon? A finite element analysis.J Bone Miner Res15301307PubMed
74.
go back to reference Evans, FG 1976Mechanical properties and histology of cortical bone from younger and older men.Anat Rec185111PubMed Evans, FG 1976Mechanical properties and histology of cortical bone from younger and older men.Anat Rec185111PubMed
75.
go back to reference Takano, Y, Turner, CH, Owan, I, Martin, RB, Lau, ST, Forwood, MR, Burr, DB 1999Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution.J Orthop Res175966PubMed Takano, Y, Turner, CH, Owan, I, Martin, RB, Lau, ST, Forwood, MR, Burr, DB 1999Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution.J Orthop Res175966PubMed
76.
go back to reference Turner, CH, Chandran, A, Pidaparti, RM 1995The anisotropy of osteonal bone and its ultrastructural implications.Bone178589PubMed Turner, CH, Chandran, A, Pidaparti, RM 1995The anisotropy of osteonal bone and its ultrastructural implications.Bone178589PubMed
77.
go back to reference Suda, K, Abe, K, Kaneda, K 1999Changes in the orientation of collagen fibers on the superficial layer of the mouse tibial bone after denervation: scanning electron microscopic observations.Arch Histol Cytol62231235PubMed Suda, K, Abe, K, Kaneda, K 1999Changes in the orientation of collagen fibers on the superficial layer of the mouse tibial bone after denervation: scanning electron microscopic observations.Arch Histol Cytol62231235PubMed
78.
go back to reference Wolff, J 1892Das Gesaetz der Tranformation der Knochen.Berlin Wolff, J 1892Das Gesaetz der Tranformation der Knochen.Berlin
79.
go back to reference Mori, S, Burr, DB 1993Increased intracortical remodeling following fatigue damage.Bone14103109PubMed Mori, S, Burr, DB 1993Increased intracortical remodeling following fatigue damage.Bone14103109PubMed
81.
go back to reference Burr, DB, Turner, CH, Naick, P, Forwood, MR, Ambrosius, W, Hasan, MS, Pidaparti, R 1998Does microdamage accumulation affect the mechanical properties of bone?J Biomech31337345CrossRefPubMed Burr, DB, Turner, CH, Naick, P, Forwood, MR, Ambrosius, W, Hasan, MS, Pidaparti, R 1998Does microdamage accumulation affect the mechanical properties of bone?J Biomech31337345CrossRefPubMed
82.
go back to reference Kopperdahl, DL, Roberts, AD, Keaveny, TM 1999Localized damage in vertebral bone is most detrimental in regions of high strain energy density.J Biomech Eng121622628PubMed Kopperdahl, DL, Roberts, AD, Keaveny, TM 1999Localized damage in vertebral bone is most detrimental in regions of high strain energy density.J Biomech Eng121622628PubMed
83.
go back to reference Vashishth, D, Koontz, J, Qiu, SJ, Lundin-Cannon, D, Yeni, YN, Schaffler, MB, Fyhrie, DP 2000In vivo diffuse damage in human vertebral trabecular bone.Bone26147152CrossRefPubMed Vashishth, D, Koontz, J, Qiu, SJ, Lundin-Cannon, D, Yeni, YN, Schaffler, MB, Fyhrie, DP 2000In vivo diffuse damage in human vertebral trabecular bone.Bone26147152CrossRefPubMed
84.
go back to reference Yeh, OC, Keaveny, TM 2001Relative roles of microdamage and microfracture in the mechanical behavior of trabecular bone.J Orthop Res1910011007CrossRefPubMed Yeh, OC, Keaveny, TM 2001Relative roles of microdamage and microfracture in the mechanical behavior of trabecular bone.J Orthop Res1910011007CrossRefPubMed
Metadata
Title
Microstructural Classification of Resorption Lacunae and Perforations in Human Proximal Femora
Authors
C. Gentzsch
G. Delling
E. Kaiser
Publication date
01-06-2003
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 6/2003
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-002-2020-7

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