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Erschienen in: Osteoporosis International 8/2009

01.08.2009 | Personal View

Thinking inside and outside the envelopes of bone

Dedicated to PDD

verfasst von: P. Szulc, E. Seeman

Erschienen in: Osteoporosis International | Ausgabe 8/2009

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Abstract

Introduction

Bone modeling and remodeling is the final common pathway expressing all genetic and environmental factors that influence the attainment and maintenance of bone’s material and structural strength. Modeling and remodeling require a surface, and during growth this cellular machinery fashions bone’s external size, shape, and internal architecture by depositing bone on, and removing bone from, both its periosteal (external) and endosteal (internal) envelopes. Bone is distributed and redistributed to achieve strength commensurate with its loading requirements.

Methods

Advancing age is associated with: (1) a reduction in the volume of bone resorbed by each basic multicellular unit (BMU); (2) an even greater reduction in the volume of bone formed by each BMU so that each remodeling event, whether adaptive or reparative, removes bone from the bone; (3) increased remodeling (number of BMUs) on the three (endocortical, intracortical, and trabecular) components of its endosteal envelope in midlife in women and late in life in both sexes; and (4) reduced bone formation on the periosteal envelope. The net effect is cortical thinning, increased intracortical porosity, trabecular thinning, and loss of connectivity.

Results

While remodeling intensity on an envelope determines structure (e.g., trabecular perforations), the surface area of the envelope determines remodeling intensity, and, so, structure. High remodeling on trabecular surfaces decreases as trabeculae (with their surface) are lost. Conversely, remodeling on the endocortical and intracortical envelopes increases their surface area, so remodeling intensity increases and bone loss becomes predominantly cortical.

Conclusions

Understanding bone structural strength and its decay and the effects of genetic factors, exercise, nutrition, and drug therapy on bone requires thinking outside and inside these envelopes; their absolute and relative movements during growth and aging determine bone structure and its strength.
Literatur
1.
Zurück zum Zitat Currey J (2002) Bones. Structure and mechanics. Princeton UP, Princeton, pp 1–380 Currey J (2002) Bones. Structure and mechanics. Princeton UP, Princeton, pp 1–380
2.
Zurück zum Zitat Parfitt AM (1996) Skeletal heterogeneity and the purposes of bone remodelling: implications for the understanding of osteoporosis. In: Marcus R, Feldman D, Kelsey J (eds) Osteoporosis. Academic, San Diego, pp 315–339 Parfitt AM (1996) Skeletal heterogeneity and the purposes of bone remodelling: implications for the understanding of osteoporosis. In: Marcus R, Feldman D, Kelsey J (eds) Osteoporosis. Academic, San Diego, pp 315–339
3.
Zurück zum Zitat Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I (2000) Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone 27:351–357PubMedCrossRef Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I (2000) Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone 27:351–357PubMedCrossRef
4.
Zurück zum Zitat Murray PDF, Huxley JS (1925) Self differentiation in the grafted limb bud of the chick. J Anat 59:379–384PubMed Murray PDF, Huxley JS (1925) Self differentiation in the grafted limb bud of the chick. J Anat 59:379–384PubMed
5.
Zurück zum Zitat Hattner R, Epker BN, Frost HM (1965) Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling. Nature 206:489–490PubMedCrossRef Hattner R, Epker BN, Frost HM (1965) Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling. Nature 206:489–490PubMedCrossRef
6.
Zurück zum Zitat Rauch F, Neu C, Manz F, Schoenau E (2001) The development of metaphyseal cortex—implications for distal radius fractures during growth. J Bone Miner Res 16:1547–1555PubMedCrossRef Rauch F, Neu C, Manz F, Schoenau E (2001) The development of metaphyseal cortex—implications for distal radius fractures during growth. J Bone Miner Res 16:1547–1555PubMedCrossRef
7.
Zurück zum Zitat Orwoll ES (2003) Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18:949–954PubMedCrossRef Orwoll ES (2003) Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18:949–954PubMedCrossRef
8.
Zurück zum Zitat Parfitt AM (2002) Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone 30:5–7PubMedCrossRef Parfitt AM (2002) Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone 30:5–7PubMedCrossRef
9.
Zurück zum Zitat Mashiba T, Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB (2000) Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. J Bone Miner Res 15:613–620PubMedCrossRef Mashiba T, Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB (2000) Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. J Bone Miner Res 15:613–620PubMedCrossRef
10.
Zurück zum Zitat Odvina CV, Zerwekh JE, Rao DS, Maalouf N, Gottschalk FA, Pak CY (2005) Severely suppressed bone turnover: a potential complication of alendronate therapy. J Clin Endocrinol Metab 90:1294–1301PubMedCrossRef Odvina CV, Zerwekh JE, Rao DS, Maalouf N, Gottschalk FA, Pak CY (2005) Severely suppressed bone turnover: a potential complication of alendronate therapy. J Clin Endocrinol Metab 90:1294–1301PubMedCrossRef
11.
Zurück zum Zitat Parfitt AM (2001) The bone remodeling compartment: a circulatory function for bone lining cells. J Bone Miner Res 16:1583–1585PubMedCrossRef Parfitt AM (2001) The bone remodeling compartment: a circulatory function for bone lining cells. J Bone Miner Res 16:1583–1585PubMedCrossRef
12.
Zurück zum Zitat Hauge EM, Qvesel D, Eriksen EF, Mosekilde L, Melsen F (2001) Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers. J Bone Miner Res 16:1575–1582PubMedCrossRef Hauge EM, Qvesel D, Eriksen EF, Mosekilde L, Melsen F (2001) Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers. J Bone Miner Res 16:1575–1582PubMedCrossRef
13.
Zurück zum Zitat Seeman E, Delmas PD (2006) Bone quality—the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261PubMedCrossRef Seeman E, Delmas PD (2006) Bone quality—the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261PubMedCrossRef
14.
Zurück zum Zitat SPRA AF (1941) Postmenopausal osteoporosis. J Am Med Assoc 116:2465–2474 SPRA AF (1941) Postmenopausal osteoporosis. J Am Med Assoc 116:2465–2474
15.
Zurück zum Zitat Lips P, Courpron P, Meunier PJ (1978) Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif Tissue Res 26:13–17PubMedCrossRef Lips P, Courpron P, Meunier PJ (1978) Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif Tissue Res 26:13–17PubMedCrossRef
16.
Zurück zum Zitat Vedi S, Compston JE, Webb A, Tighe JR (1982) Histomorphometric analysis of bone biopsies from the iliac crest of normal British subjects. Metab Bone Dis Relat Res 4:231–236PubMedCrossRef Vedi S, Compston JE, Webb A, Tighe JR (1982) Histomorphometric analysis of bone biopsies from the iliac crest of normal British subjects. Metab Bone Dis Relat Res 4:231–236PubMedCrossRef
17.
Zurück zum Zitat Bonyadi M, Waldman SD, Liu D, Aubin JE, Grynpas MD, Stanford WL (2003) Mesenchymal progenitor self-renewal deficiency leads to age-dependent osteoporosis in Sca-1/Ly-6A null mice. Proc Natl Acad Sci U S A 100:5840–5845PubMedCrossRef Bonyadi M, Waldman SD, Liu D, Aubin JE, Grynpas MD, Stanford WL (2003) Mesenchymal progenitor self-renewal deficiency leads to age-dependent osteoporosis in Sca-1/Ly-6A null mice. Proc Natl Acad Sci U S A 100:5840–5845PubMedCrossRef
18.
Zurück zum Zitat Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE (1999) Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J Bone Miner Metab 17:171–177PubMedCrossRef Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE (1999) Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J Bone Miner Metab 17:171–177PubMedCrossRef
19.
Zurück zum Zitat Oreffo RO, Bord S, Triffitt JT (1998) Skeletal progenitor cells and ageing human populations. Clin Sci (Lond) 94:549–555 Oreffo RO, Bord S, Triffitt JT (1998) Skeletal progenitor cells and ageing human populations. Clin Sci (Lond) 94:549–555
20.
Zurück zum Zitat Eriksen EF (1986) Normal and pathological remodeling of human trabecular bone: three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease. Endocr Rev 7:379–408PubMedCrossRef Eriksen EF (1986) Normal and pathological remodeling of human trabecular bone: three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease. Endocr Rev 7:379–408PubMedCrossRef
21.
Zurück zum Zitat Eriksen EF, Langdahl B, Vesterby A, Rungby J, Kassem M (1999) Hormone replacement therapy prevents osteoclastic hyperactivity: a histomorphometric study in early postmenopausal women. J Bone Miner Res 14:1217–1221PubMedCrossRef Eriksen EF, Langdahl B, Vesterby A, Rungby J, Kassem M (1999) Hormone replacement therapy prevents osteoclastic hyperactivity: a histomorphometric study in early postmenopausal women. J Bone Miner Res 14:1217–1221PubMedCrossRef
22.
Zurück zum Zitat Compston JE, Yamaguchi K, Croucher PI, Garrahan NJ, Lindsay PC, Shaw RW (1995) The effects of gonadotrophin-releasing hormone agonists on iliac crest cancellous bone structure in women with endometriosis. Bone 16:261–267PubMedCrossRef Compston JE, Yamaguchi K, Croucher PI, Garrahan NJ, Lindsay PC, Shaw RW (1995) The effects of gonadotrophin-releasing hormone agonists on iliac crest cancellous bone structure in women with endometriosis. Bone 16:261–267PubMedCrossRef
23.
Zurück zum Zitat Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115–137PubMedCrossRef Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115–137PubMedCrossRef
24.
Zurück zum Zitat Eriksen EF, Mosekilde L, Melsen F (1985) Trabecular bone resorption depth decreases with age: differences between normal males and females. Bone 6:141–146PubMedCrossRef Eriksen EF, Mosekilde L, Melsen F (1985) Trabecular bone resorption depth decreases with age: differences between normal males and females. Bone 6:141–146PubMedCrossRef
25.
Zurück zum Zitat Cohen-Solal ME, Shih MS, Lundy MW, Parfitt AM (1991) A new method for measuring cancellous bone erosion depth: application to the cellular mechanisms of bone loss in postmenopausal women. J Bone Miner Res 6:1331–1338PubMedCrossRef Cohen-Solal ME, Shih MS, Lundy MW, Parfitt AM (1991) A new method for measuring cancellous bone erosion depth: application to the cellular mechanisms of bone loss in postmenopausal women. J Bone Miner Res 6:1331–1338PubMedCrossRef
26.
Zurück zum Zitat Birkenhäger-Frenkel DH, Nigg AL, Hens CJJ, Birkenhäger JC (1993) Changes of interstitial bone thickness with age in men and women. Bone 14:211–216PubMedCrossRef Birkenhäger-Frenkel DH, Nigg AL, Hens CJJ, Birkenhäger JC (1993) Changes of interstitial bone thickness with age in men and women. Bone 14:211–216PubMedCrossRef
27.
Zurück zum Zitat Croucher PI, Mellish RWE, Vedi S, Garrahan NJ, Compston JE (1989) The relationship between resorption depth and mean interstitial bone thickness: age-related changes in man. Calcif Tissue Int 45:15–19PubMedCrossRef Croucher PI, Mellish RWE, Vedi S, Garrahan NJ, Compston JE (1989) The relationship between resorption depth and mean interstitial bone thickness: age-related changes in man. Calcif Tissue Int 45:15–19PubMedCrossRef
28.
Zurück zum Zitat Balena R, Shih MS, Parfitt AM (1992) Bone resorption and formation on the periosteal envelope of the ilium: a histomorphometric study in healthy women. J Bone Miner Res 7:1475–1482PubMedCrossRef Balena R, Shih MS, Parfitt AM (1992) Bone resorption and formation on the periosteal envelope of the ilium: a histomorphometric study in healthy women. J Bone Miner Res 7:1475–1482PubMedCrossRef
29.
Zurück zum Zitat Riggs BL, Melton LJ III, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S (2004) Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 19:1945–1954PubMedCrossRef Riggs BL, Melton LJ III, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S (2004) Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 19:1945–1954PubMedCrossRef
30.
Zurück zum Zitat Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S (2008) A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res 23:205–214PubMedCrossRef Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S (2008) A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res 23:205–214PubMedCrossRef
31.
Zurück zum Zitat Riggs BL, Wahner HW, Melton LJ 3rd, Richelson LS, Judd HL, Offord KP (1986) Rates of bone loss in the appendicular and axial skeletons of women. Evidence of substantial vertebral bone loss before menopause. J Clin Invest 77:1487–1491PubMedCrossRef Riggs BL, Wahner HW, Melton LJ 3rd, Richelson LS, Judd HL, Offord KP (1986) Rates of bone loss in the appendicular and axial skeletons of women. Evidence of substantial vertebral bone loss before menopause. J Clin Invest 77:1487–1491PubMedCrossRef
32.
Zurück zum Zitat Gilsanz V, Gibbens DT, Carlson M, Boechat MI, Cann CE, Schulz EE (1988) Peak trabecular vertebral density: a comparison of adolescent and adult females. Calcif Tissue Int 43:260–262PubMedCrossRef Gilsanz V, Gibbens DT, Carlson M, Boechat MI, Cann CE, Schulz EE (1988) Peak trabecular vertebral density: a comparison of adolescent and adult females. Calcif Tissue Int 43:260–262PubMedCrossRef
33.
Zurück zum Zitat van der Linden JC, Homminga J, Verhaar JA, Weinans H (2001) Mechanical consequences of bone loss in cancellous bone. J Bone Miner Res 16:457–465PubMedCrossRef van der Linden JC, Homminga J, Verhaar JA, Weinans H (2001) Mechanical consequences of bone loss in cancellous bone. J Bone Miner Res 16:457–465PubMedCrossRef
34.
Zurück zum Zitat Seeman E (2003) Periosteal bone formation—a neglected determinant of bone strength. N Engl J Med 349:320–323PubMedCrossRef Seeman E (2003) Periosteal bone formation—a neglected determinant of bone strength. N Engl J Med 349:320–323PubMedCrossRef
35.
Zurück zum Zitat Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD (2006) Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21:1856–1863PubMedCrossRef Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD (2006) Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21:1856–1863PubMedCrossRef
36.
Zurück zum Zitat Parfitt A (1980) Morphological basis of bone mineral measurements: transient and steady state effects of treatment in osteoporosis. Miner Electrolyte Metab 4:273–287 Parfitt A (1980) Morphological basis of bone mineral measurements: transient and steady state effects of treatment in osteoporosis. Miner Electrolyte Metab 4:273–287
37.
Zurück zum Zitat Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB (2003) Aging of microstructural compartments in human compact bone. J Bone Miner Res 18:1012–1019PubMedCrossRef Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB (2003) Aging of microstructural compartments in human compact bone. J Bone Miner Res 18:1012–1019PubMedCrossRef
38.
Zurück zum Zitat 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(Suppl 1):S37–S45PubMedCrossRef 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(Suppl 1):S37–S45PubMedCrossRef
39.
Zurück zum Zitat Brown JP, Delmas PD, Arlot M, Meunier PJ (1987) Active bone turnover of the cortico-endosteal envelope in postmenopausal osteoporosis. J Clin Endocrinol Metab 6:954–959CrossRef Brown JP, Delmas PD, Arlot M, Meunier PJ (1987) Active bone turnover of the cortico-endosteal envelope in postmenopausal osteoporosis. J Clin Endocrinol Metab 6:954–959CrossRef
40.
Zurück zum Zitat Arlot ME, Delmas PD, Chappard D, Meunier PJ (1990) Trabecular and endocortical bone remodeling in postmenopausal osteoporosis: comparison with normal postmenopausal women. Osteoporos Int 1:41–49PubMedCrossRef Arlot ME, Delmas PD, Chappard D, Meunier PJ (1990) Trabecular and endocortical bone remodeling in postmenopausal osteoporosis: comparison with normal postmenopausal women. Osteoporos Int 1:41–49PubMedCrossRef
41.
Zurück zum Zitat Foldes J, Parfitt AM, Shih MS, Rao DS, Kleerekoper M (1991) Structural and geometric changes in iliac bone: relationship to normal aging and osteoporosis. J Bone Miner Res 6:759–766PubMed Foldes J, Parfitt AM, Shih MS, Rao DS, Kleerekoper M (1991) Structural and geometric changes in iliac bone: relationship to normal aging and osteoporosis. J Bone Miner Res 6:759–766PubMed
42.
Zurück zum Zitat Martin RB (1984) Porosity and specific surface of bone. Crit Rev Biomed Eng 10:179–222PubMed Martin RB (1984) Porosity and specific surface of bone. Crit Rev Biomed Eng 10:179–222PubMed
43.
Zurück zum Zitat Brockstedt H, Kassem M, Eriksen EF, Mosekilde L, Melsen F (1993) Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone 14:681–691PubMedCrossRef Brockstedt H, Kassem M, Eriksen EF, Mosekilde L, Melsen F (1993) Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone 14:681–691PubMedCrossRef
44.
Zurück zum Zitat Yeni YN, Brown CU, Wang Z, Norman TL (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21:453–459PubMedCrossRef Yeni YN, Brown CU, Wang Z, Norman TL (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21:453–459PubMedCrossRef
45.
Zurück zum Zitat Hernandez CJ, Gupta A, Keaveny TM (2006) A biomechanical analysis of the effects of resorption cavities on cancellous bone strength. J Bone Miner Res 21:1248–1255PubMedCrossRef Hernandez CJ, Gupta A, Keaveny TM (2006) A biomechanical analysis of the effects of resorption cavities on cancellous bone strength. J Bone Miner Res 21:1248–1255PubMedCrossRef
46.
Zurück zum Zitat Boivin G, Lips P, Ott SM, Harper KD, Sarkar S, Pinette KV, Meunier PJ (2003) Contribution of raloxifene and calcium and vitamin D3 supplementation to the increase of the degree of mineralization of bone in postmenopausal women. J Clin Endocrinol Metab 88:4199–4205PubMedCrossRef Boivin G, Lips P, Ott SM, Harper KD, Sarkar S, Pinette KV, Meunier PJ (2003) Contribution of raloxifene and calcium and vitamin D3 supplementation to the increase of the degree of mineralization of bone in postmenopausal women. J Clin Endocrinol Metab 88:4199–4205PubMedCrossRef
47.
Zurück zum Zitat Boivin G, Meunier PJ (2002) Changes in bone remodeling rate influence the degree of mineralization of bone. Connect Tissue Res 43:535–537PubMedCrossRef Boivin G, Meunier PJ (2002) Changes in bone remodeling rate influence the degree of mineralization of bone. Connect Tissue Res 43:535–537PubMedCrossRef
48.
Zurück zum Zitat Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336PubMedCrossRef Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336PubMedCrossRef
49.
Zurück zum Zitat Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, Christiansen C, Delmas PD (2006) Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 38:300–309PubMedCrossRef Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, Christiansen C, Delmas PD (2006) Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 38:300–309PubMedCrossRef
50.
Zurück zum Zitat Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L (1999) Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int 65:203–210PubMedCrossRef Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L (1999) Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int 65:203–210PubMedCrossRef
51.
Zurück zum Zitat Banse X, Sims TJ, Bailey AJ (2002) Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 17:1621–1628PubMedCrossRef Banse X, Sims TJ, Bailey AJ (2002) Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 17:1621–1628PubMedCrossRef
52.
Zurück zum Zitat Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO (2004) Effect of aging on the toughness of human cortical bone: evaluation by R-curves. Bone 35:1240–1246PubMedCrossRef Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO (2004) Effect of aging on the toughness of human cortical bone: evaluation by R-curves. Bone 35:1240–1246PubMedCrossRef
53.
Zurück zum Zitat Qiu S, Rao DS, Fyhrie DP, Palnitkar S, Parfitt AM (2005) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37:10–15PubMedCrossRef Qiu S, Rao DS, Fyhrie DP, Palnitkar S, Parfitt AM (2005) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37:10–15PubMedCrossRef
54.
Zurück zum Zitat Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003) Bone loss and bone size after menopause. N Engl J Med 349:327–334PubMedCrossRef Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003) Bone loss and bone size after menopause. N Engl J Med 349:327–334PubMedCrossRef
55.
Zurück zum Zitat Aaron JE, Makins NB, Sagreiya K (1987) The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop Relat Res 215:260–271PubMed Aaron JE, Makins NB, Sagreiya K (1987) The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop Relat Res 215:260–271PubMed
56.
Zurück zum Zitat Duan Y, Beck TJ, Wang XF, Seeman E (2003) Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res 18(10):1766–1774PubMedCrossRef Duan Y, Beck TJ, Wang XF, Seeman E (2003) Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res 18(10):1766–1774PubMedCrossRef
57.
Zurück zum Zitat Duan Y, Turner CH, Kim BT, Seeman E (2001) Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res 16:2267–2275PubMedCrossRef Duan Y, Turner CH, Kim BT, Seeman E (2001) Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res 16:2267–2275PubMedCrossRef
58.
Zurück zum Zitat Duan Y, Wang XF, Evans A, Seeman E (2005) Structural and biomechanical basis of racial and sex differences in vertebral fragility in Chinese and Caucasians. Bone 36:987–998PubMedCrossRef Duan Y, Wang XF, Evans A, Seeman E (2005) Structural and biomechanical basis of racial and sex differences in vertebral fragility in Chinese and Caucasians. Bone 36:987–998PubMedCrossRef
59.
Zurück zum Zitat Wang XF, Duan Y, Beck TJ, Seeman E (2005) Varying contributions of growth and ageing to racial and sex differences in femoral neck structure and strength in old age. Bone 36:978–986PubMedCrossRef Wang XF, Duan Y, Beck TJ, Seeman E (2005) Varying contributions of growth and ageing to racial and sex differences in femoral neck structure and strength in old age. Bone 36:978–986PubMedCrossRef
60.
Zurück zum Zitat Seeman E, Duan Y, Fong C, Edmonds J (2001) Fracture site-specific deficits in bone size and volumetric density in men with spine or hip fractures. J Bone Miner Res 16:120–127PubMedCrossRef Seeman E, Duan Y, Fong C, Edmonds J (2001) Fracture site-specific deficits in bone size and volumetric density in men with spine or hip fractures. J Bone Miner Res 16:120–127PubMedCrossRef
Metadaten
Titel
Thinking inside and outside the envelopes of bone
Dedicated to PDD
verfasst von
P. Szulc
E. Seeman
Publikationsdatum
01.08.2009
Verlag
Springer-Verlag
Erschienen in
Osteoporosis International / Ausgabe 8/2009
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-009-0994-y

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Sie sei „ethisch geboten“, meint Gesundheitsminister Karl Lauterbach: mehr Transparenz über die Qualität von Klinikbehandlungen. Um sie abzubilden, lässt er gegen den Widerstand vieler Länder einen virtuellen Klinik-Atlas freischalten.

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