Skip to main content
Top
Published in: Calcified Tissue International 3/2010

01-03-2010

Region-Specific Sex-Dependent Pattern of Age-Related Changes of Proximal Femoral Cancellous Bone and Its Implications on Differential Bone Fragility

Authors: Marija Djuric, Danijela Djonic, Petar Milovanovic, Slobodan Nikolic, Robert Marshall, Jelena Marinkovic, Michael Hahn

Published in: Calcified Tissue International | Issue 3/2010

Login to get access

Abstract

Despite evident interest in age-related bone changes, data on regional differences within the proximal femur are scarce. To date, there has been no comprehensive study on site-specific age-related changes in the trabecular architecture of three biomechanically important femoral subregions (medial neck, lateral neck, and intertrochanteric region) for both genders. In this study we investigated age-related deterioration in the trabecular architecture of those three subregions of the femoral neck for both genders. The research sample included 52 proximal femora (26 males, 26 females; age range, 26–96 years) from Forensic Department at University of Belgrade. Bone sections from the three regions of interest were scanned by micro-CT at University of Hamburg. The study revealed that proximal femoral microarchitecture cannot be perceived as homogeneous and, more importantly, that the aging process is not uniform. Besides the initial intersite differences, microarchitecture changed differently with increasing age, maintaining significant differences between the regions. In addition, we observed a different aging pattern between genders: deterioration was most significant in the intertrochanteric region in women, while the lateral neck was most affected in men. This finding supports epidemiological data about the differential occurrence of cervical vs. trochanteric fractures in aging males and females. In conclusion, the aging process in the proximal femur cannot be regarded as a simple function of quantitative bone loss but, rather, as an alteration of specific architecture that may degrade bone strength.
Literature
1.
go back to reference Martens M, Van Audekercke R, Delport P, De Meester P, Mulier JC (1983) The mechanical characteristics of cancellous bone at the upper femoral region. J Biomech 16:971–983CrossRefPubMed Martens M, Van Audekercke R, Delport P, De Meester P, Mulier JC (1983) The mechanical characteristics of cancellous bone at the upper femoral region. J Biomech 16:971–983CrossRefPubMed
2.
go back to reference Werner C, Iversen BF, Therkildsen MH (1988) Contribution of the trabecular component to mechanical strength and bone mineral content of the femoral neck. An experimental study on cadaver bones. Scand J Clin Lab Invest 48:457–460CrossRefPubMed Werner C, Iversen BF, Therkildsen MH (1988) Contribution of the trabecular component to mechanical strength and bone mineral content of the femoral neck. An experimental study on cadaver bones. Scand J Clin Lab Invest 48:457–460CrossRefPubMed
3.
go back to reference Delaere O, Dhem A, Bourgois R (1989) Cancellous bone and mechanical strength of the femoral neck. Arch Orthop Trauma Surg 10:72–75CrossRef Delaere O, Dhem A, Bourgois R (1989) Cancellous bone and mechanical strength of the femoral neck. Arch Orthop Trauma Surg 10:72–75CrossRef
4.
go back to reference Passi N, Gefen A (2005) Trabecular bone contributes to strength of the proximal femur under mediolateral impact in the avian. J Biomech Eng 127:198–203CrossRefPubMed Passi N, Gefen A (2005) Trabecular bone contributes to strength of the proximal femur under mediolateral impact in the avian. J Biomech Eng 127:198–203CrossRefPubMed
5.
go back to reference Reich T, Gefen A (2006) Effect of trabecular bone loss on cortical strain rate during impact in an in vitro model of avian femur. BioMed Eng OnLine 5:45–55CrossRefPubMed Reich T, Gefen A (2006) Effect of trabecular bone loss on cortical strain rate during impact in an in vitro model of avian femur. BioMed Eng OnLine 5:45–55CrossRefPubMed
6.
go back to reference Verhulp E, van Rietbergen B, Huiskes R (2008) Load distribution in the healthy and osteoporotic human proximal femur during a fall to the side. Bone 42:30–35CrossRefPubMed Verhulp E, van Rietbergen B, Huiskes R (2008) Load distribution in the healthy and osteoporotic human proximal femur during a fall to the side. Bone 42:30–35CrossRefPubMed
7.
go back to reference Singh M, Nagrath AR, Maini PS (1970) Changes in trabecular pattern of the upper end of the femur as an index of osteoporosis. J Bone Joint Surg Am 52(3):457–467PubMed Singh M, Nagrath AR, Maini PS (1970) Changes in trabecular pattern of the upper end of the femur as an index of osteoporosis. J Bone Joint Surg Am 52(3):457–467PubMed
8.
go back to reference Lundeen GA, Vajda EG, Bloebaum RD (2000) Age-related cancellous bone loss in the proximal femur of Caucasian females. Osteoporos Int 11:505–511CrossRefPubMed Lundeen GA, Vajda EG, Bloebaum RD (2000) Age-related cancellous bone loss in the proximal femur of Caucasian females. Osteoporos Int 11:505–511CrossRefPubMed
9.
go back to reference Kawashima T, Uhthoff HK (1991) Pattern of bone loss of the proximal femur: a radiologic, densitometric, and histomorphometric study. J Orthop Res 9:634–640CrossRefPubMed Kawashima T, Uhthoff HK (1991) Pattern of bone loss of the proximal femur: a radiologic, densitometric, and histomorphometric study. J Orthop Res 9:634–640CrossRefPubMed
10.
go back to reference Lai YM, Qin L, Yeung HY, Lee KKH, Chan KM (2005) Regional differences in trabecular BMD and micro-architecture of weight-bearing bone under habitual gait loading—a pQCT and microCT study in human cadavers. Bone 37:274–282CrossRefPubMed Lai YM, Qin L, Yeung HY, Lee KKH, Chan KM (2005) Regional differences in trabecular BMD and micro-architecture of weight-bearing bone under habitual gait loading—a pQCT and microCT study in human cadavers. Bone 37:274–282CrossRefPubMed
11.
go back to reference Meta M, Lu Y, Keyak JH, Lang T (2006) Young-elderly differences in bone density, geometry and strength indices depend on proximal femur sub-region: a cross sectional study in Caucasian-American women. Bone 39(1):152–158CrossRefPubMed Meta M, Lu Y, Keyak JH, Lang T (2006) Young-elderly differences in bone density, geometry and strength indices depend on proximal femur sub-region: a cross sectional study in Caucasian-American women. Bone 39(1):152–158CrossRefPubMed
12.
go back to reference Nazarian A, Muller J, Zurakowski D, Müller R, Snyder BD (2007) Densitometric, morphometric and mechanical distributions in the human proximal femur. J Biomech 40:2573–2579CrossRefPubMed Nazarian A, Muller J, Zurakowski D, Müller R, Snyder BD (2007) Densitometric, morphometric and mechanical distributions in the human proximal femur. J Biomech 40:2573–2579CrossRefPubMed
13.
go back to reference Cui WQ, Won YY, Baek MH, Lee DH, Chung YS, Hur JH, Ma YZ (2008) Age-and region-dependent changes in three-dimensional microstructural properties of proximal femoral trabeculae. Osteoporos Int 19:1579–1587CrossRefPubMed Cui WQ, Won YY, Baek MH, Lee DH, Chung YS, Hur JH, Ma YZ (2008) Age-and region-dependent changes in three-dimensional microstructural properties of proximal femoral trabeculae. Osteoporos Int 19:1579–1587CrossRefPubMed
14.
go back to reference Lochmüller EM, Matsuura M, Bauer J, Hitzl W, Link TM, Müller R, Eckstein F (2008) Site-specific deterioration of trabecular bone architecture in men and women with advancing age. J Bone Miner Res 23(12):1964–1973CrossRefPubMed Lochmüller EM, Matsuura M, Bauer J, Hitzl W, Link TM, Müller R, Eckstein F (2008) Site-specific deterioration of trabecular bone architecture in men and women with advancing age. J Bone Miner Res 23(12):1964–1973CrossRefPubMed
15.
go back to reference Li W, Kornak J, Harris T, Keyak J, Li C, Lu Y, Cheng X, Lang T (2009) Identify fracture-critical regions inside the proximal femur using statistical parametric mapping. Bone 44(4):596–602CrossRefPubMed Li W, Kornak J, Harris T, Keyak J, Li C, Lu Y, Cheng X, Lang T (2009) Identify fracture-critical regions inside the proximal femur using statistical parametric mapping. Bone 44(4):596–602CrossRefPubMed
16.
go back to reference Issever AS, Vieth V, Lotter A, Meier N, Laib A, Newitt D, Majumdar S, Link TM (2002) Local differences in the trabecular bone structure of the proximal femur depicted with high-spatial resolution MR imaging and multisection CT. Acad Radiol 9:1395–1406CrossRefPubMed Issever AS, Vieth V, Lotter A, Meier N, Laib A, Newitt D, Majumdar S, Link TM (2002) Local differences in the trabecular bone structure of the proximal femur depicted with high-spatial resolution MR imaging and multisection CT. Acad Radiol 9:1395–1406CrossRefPubMed
17.
go back to reference Da Paz LHBC, De Falco V, Teng NC, Dos Reis LM, Pereira RMR, Jorgetti V (2001) Effect of 17ß-estradiol or alendronate on the bone densitometry, bone histomorphometry and bone metabolism of ovariectomized rats. Braz J Med Biol Res 34(8):1015–1022CrossRefPubMed Da Paz LHBC, De Falco V, Teng NC, Dos Reis LM, Pereira RMR, Jorgetti V (2001) Effect of 17ß-estradiol or alendronate on the bone densitometry, bone histomorphometry and bone metabolism of ovariectomized rats. Braz J Med Biol Res 34(8):1015–1022CrossRefPubMed
18.
go back to reference Domrongkitchaiporn S, Sirikulchayanonta V, Angchaisuksiri P, Stitchantrakul W, Kanokkantapong C, Rajatanavin R (2003) Abnormalities in bone mineral density and bone histology in thalassemia. J Bone Miner Res 18(9):1682–1688CrossRefPubMed Domrongkitchaiporn S, Sirikulchayanonta V, Angchaisuksiri P, Stitchantrakul W, Kanokkantapong C, Rajatanavin R (2003) Abnormalities in bone mineral density and bone histology in thalassemia. J Bone Miner Res 18(9):1682–1688CrossRefPubMed
19.
go back to reference Mellibovsky L, Mariñoso ML, Cervantes F, Besses C, Nacher M, Nogués X, Florensa L, Munné A, Diez-Perez A, Serrano S (2004) Relationship among densitometry, bone histomorphometry, and histologic stage in idiopathic myelofibrosis. Bone 34(2):330–335CrossRefPubMed Mellibovsky L, Mariñoso ML, Cervantes F, Besses C, Nacher M, Nogués X, Florensa L, Munné A, Diez-Perez A, Serrano S (2004) Relationship among densitometry, bone histomorphometry, and histologic stage in idiopathic myelofibrosis. Bone 34(2):330–335CrossRefPubMed
20.
go back to reference Tsangari H, Findlay D, Fazzalari N (2007) Structural and remodeling indices in the cancellous bone of the proximal femur across adulthood. Bone 40:211–217CrossRefPubMed Tsangari H, Findlay D, Fazzalari N (2007) Structural and remodeling indices in the cancellous bone of the proximal femur across adulthood. Bone 40:211–217CrossRefPubMed
21.
go back to reference Baudoin C, Fardellone P, Sebert JL (1993) Effect of sex and age on the ratio of cervical to trochanteric hip fracture. A meta-analysis of 16 reports on 36,451 cases. Acta Orthop Scand 64(6):647–653PubMedCrossRef Baudoin C, Fardellone P, Sebert JL (1993) Effect of sex and age on the ratio of cervical to trochanteric hip fracture. A meta-analysis of 16 reports on 36,451 cases. Acta Orthop Scand 64(6):647–653PubMedCrossRef
22.
go back to reference Kannus P, Parkkari J, Sievänen H, Heinonen A, Vuori I, Järvinen M (1996) Epidemiology of hip fractures. Bone 18(Suppl 1):57S–63SCrossRefPubMed Kannus P, Parkkari J, Sievänen H, Heinonen A, Vuori I, Järvinen M (1996) Epidemiology of hip fractures. Bone 18(Suppl 1):57S–63SCrossRefPubMed
23.
go back to reference Memon A, Pospula WM, Tantawy AY, Abdul-Ghafar S, Suresh A, Al-Rowaih A (1998) Incidence of hip fracture in Kuwait. Int J Epidemiol 27:860–865CrossRefPubMed Memon A, Pospula WM, Tantawy AY, Abdul-Ghafar S, Suresh A, Al-Rowaih A (1998) Incidence of hip fracture in Kuwait. Int J Epidemiol 27:860–865CrossRefPubMed
24.
go back to reference Löfman O, Berglund K, Larsson L, Toss G (2002) Changes in hip fracture epidemiology: redistribution between ages, genders and fracture types. Osteoporosis Int 13(1):18–25CrossRef Löfman O, Berglund K, Larsson L, Toss G (2002) Changes in hip fracture epidemiology: redistribution between ages, genders and fracture types. Osteoporosis Int 13(1):18–25CrossRef
25.
go back to reference Morosano M, Masoni A, Sánchez A (2005) Incidence of hip fractures in the city of Rosario, Argentina. Osteoporos Int 16(11):1339–1344CrossRefPubMed Morosano M, Masoni A, Sánchez A (2005) Incidence of hip fractures in the city of Rosario, Argentina. Osteoporos Int 16(11):1339–1344CrossRefPubMed
26.
go back to reference Lönnroos E, Kautiainen H, Karppi P, Huusko T, Hartikainen S, Kiviranta I, Sulkava R (2006) Increased incidence of hip fractures. A population based-study in Finland. Bone 39:623–627CrossRefPubMed Lönnroos E, Kautiainen H, Karppi P, Huusko T, Hartikainen S, Kiviranta I, Sulkava R (2006) Increased incidence of hip fractures. A population based-study in Finland. Bone 39:623–627CrossRefPubMed
27.
go back to reference Truong LH, Kuliwaba JS, Tsangari H, Fazzalari NL (2006) Differential gene expression of bone anabolic factors and trabecular bone architectural changes in the proximal femoral shaft of primary hip osteoarthritis patients. Arth Res Ther 8(6):R188CrossRef Truong LH, Kuliwaba JS, Tsangari H, Fazzalari NL (2006) Differential gene expression of bone anabolic factors and trabecular bone architectural changes in the proximal femoral shaft of primary hip osteoarthritis patients. Arth Res Ther 8(6):R188CrossRef
28.
go back to reference Thomsen JS, Ebbesen EN, Mosekilde L (2000) A new method of comprehensive static histomorphometry applied on human lumbar vertebral cancellous bone. Bone 27:129–138CrossRefPubMed Thomsen JS, Ebbesen EN, Mosekilde L (2000) A new method of comprehensive static histomorphometry applied on human lumbar vertebral cancellous bone. Bone 27:129–138CrossRefPubMed
29.
go back to reference Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA (2000) Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res 15:32–40CrossRefPubMed Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA (2000) Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res 15:32–40CrossRefPubMed
30.
go back to reference Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle MF, Audran M (2000) Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res 15:13–19CrossRefPubMed Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle MF, Audran M (2000) Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res 15:13–19CrossRefPubMed
32.
go back to reference Ding M, Odgaard A, Danielsen CC, Hvid I (2002) Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J Bone Joint Surg Br 84-B(6):900–907CrossRef Ding M, Odgaard A, Danielsen CC, Hvid I (2002) Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J Bone Joint Surg Br 84-B(6):900–907CrossRef
33.
go back to reference Whitehouse WJ, Dyson ED (1974) Scanning electron microscope studies of trabecular bone in the proximal end of the human femur. J Anat 118(Pt 3):417–444PubMed Whitehouse WJ, Dyson ED (1974) Scanning electron microscope studies of trabecular bone in the proximal end of the human femur. J Anat 118(Pt 3):417–444PubMed
34.
go back to reference Lotz JC, Cheal EJ, Hayes WC (1995) Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporosis Int 5:252–261CrossRef Lotz JC, Cheal EJ, Hayes WC (1995) Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporosis Int 5:252–261CrossRef
35.
go back to reference Rudman KE, Aspden RM, Meakin JR (2006) Compression or tension? The stress distribution in the proximal femur. BioMed Eng OnLine 5:12–19CrossRefPubMed Rudman KE, Aspden RM, Meakin JR (2006) Compression or tension? The stress distribution in the proximal femur. BioMed Eng OnLine 5:12–19CrossRefPubMed
36.
go back to reference Roux W (1881) Der zuchtende Kampf der Teile, oder die “Teilau- slese” im Organismus (Theorie der “funktionellen Anpassung”). Wilhelm Engelmann, Leipzig, Germany Roux W (1881) Der zuchtende Kampf der Teile, oder die “Teilau- slese” im Organismus (Theorie der “funktionellen Anpassung”). Wilhelm Engelmann, Leipzig, Germany
37.
go back to reference Wolff J (1892) Das Gesetz der Transformation der Knochen [The law of bone remodelling]. Springer, Berlin Wolff J (1892) Das Gesetz der Transformation der Knochen [The law of bone remodelling]. Springer, Berlin
38.
go back to reference Hert J (1994) A new attempt at the interpretation of the functional architecture of the cancellous bone. J Biomech 27(2):239–242CrossRefPubMed Hert J (1994) A new attempt at the interpretation of the functional architecture of the cancellous bone. J Biomech 27(2):239–242CrossRefPubMed
39.
go back to reference Skedros JG, Baucom SL (2007) Mathematical analysis of trabecular ‘trajectories’ in apparent trajectorial structures: the unfortunate historical emphasis on the human proximal femur. J Theor Biol 244:15–45CrossRefPubMed Skedros JG, Baucom SL (2007) Mathematical analysis of trabecular ‘trajectories’ in apparent trajectorial structures: the unfortunate historical emphasis on the human proximal femur. J Theor Biol 244:15–45CrossRefPubMed
40.
go back to reference Lovejoy CO (2005) The natural history of human gait and posture. Part 2. Hip and thigh. Gait Posture 21(1):113–124CrossRefPubMed Lovejoy CO (2005) The natural history of human gait and posture. Part 2. Hip and thigh. Gait Posture 21(1):113–124CrossRefPubMed
41.
go back to reference Pauwels F (1980) Biomechanics of the locomotor apparatus. Springer-Verlag, Berlin Pauwels F (1980) Biomechanics of the locomotor apparatus. Springer-Verlag, Berlin
42.
go back to reference Kalmey JK, Lovejoy CO (2002) Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading? Bone 31(2):327–332CrossRefPubMed Kalmey JK, Lovejoy CO (2002) Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading? Bone 31(2):327–332CrossRefPubMed
43.
go back to reference Westerlind KC, Wronski TJ, Ritman EL, Luo ZP, An KN, Bell NH, Turner RT (1997) Estrogen regulates the rate of bone turnover but bone balance in ovariectomized rats is modulated by prevailing mechanical strain. Proc Natl Acad Sci USA 94:4199–4204CrossRefPubMed Westerlind KC, Wronski TJ, Ritman EL, Luo ZP, An KN, Bell NH, Turner RT (1997) Estrogen regulates the rate of bone turnover but bone balance in ovariectomized rats is modulated by prevailing mechanical strain. Proc Natl Acad Sci USA 94:4199–4204CrossRefPubMed
44.
go back to reference Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J (2005) Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 366:129–135CrossRefPubMed Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J (2005) Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 366:129–135CrossRefPubMed
45.
46.
go back to reference Judex S, Garman R, Squire M, Donahue LR, Rubin C (2004) Genetically based influences on the site-specific regulation of trabecular and cortical bone morphology. J Bone Miner Res 19:600–606CrossRefPubMed Judex S, Garman R, Squire M, Donahue LR, Rubin C (2004) Genetically based influences on the site-specific regulation of trabecular and cortical bone morphology. J Bone Miner Res 19:600–606CrossRefPubMed
47.
go back to reference Zhang L, Cheng A, Bai Z, Lu Y, Endo N, Dohmae Y, Takahashi HE (2000) Epidemiology of cervical and trochanteric fractures of the proximal femur in 1994 in Tangshan, China. J Bone Miner Metab 18(2):84–88CrossRefPubMed Zhang L, Cheng A, Bai Z, Lu Y, Endo N, Dohmae Y, Takahashi HE (2000) Epidemiology of cervical and trochanteric fractures of the proximal femur in 1994 in Tangshan, China. J Bone Miner Metab 18(2):84–88CrossRefPubMed
48.
go back to reference El Maghraoui A, Koumba BA, Jroundi I, Achemlal L, Bezza A, Tazi MA (2005) Epidemiology of hip fractures in 2002 in Rabat, Morocco. Osteoporos Int 16(6):597–602CrossRefPubMed El Maghraoui A, Koumba BA, Jroundi I, Achemlal L, Bezza A, Tazi MA (2005) Epidemiology of hip fractures in 2002 in Rabat, Morocco. Osteoporos Int 16(6):597–602CrossRefPubMed
49.
go back to reference Lesić A, Jarebinski M, Pekmezović T, Bumbasirević M, Spasovski D, Atkinson HD (2007) Epidemiology of hip fractures in Belgrade, Serbia Montenegro, 1990–2000. Arch Orthop Trauma Surg 127(3):179–183CrossRefPubMed Lesić A, Jarebinski M, Pekmezović T, Bumbasirević M, Spasovski D, Atkinson HD (2007) Epidemiology of hip fractures in Belgrade, Serbia Montenegro, 1990–2000. Arch Orthop Trauma Surg 127(3):179–183CrossRefPubMed
50.
go back to reference Hedlund R, Ahlbom A, Lindgren U (1986) Hip fracture incidence in Stockholm 1972–1981. Acta Orthopaed 57:30–34CrossRef Hedlund R, Ahlbom A, Lindgren U (1986) Hip fracture incidence in Stockholm 1972–1981. Acta Orthopaed 57:30–34CrossRef
51.
go back to reference Ito M, Nishida A, Koga A, Ikeda S, Shiraishi A, Uetani M, Hayashi K, Nakamura T (2002) Contribution of trabecular and cortical components to the mechanical properties of bone and their regulating parameters. Bone 31(3):351–358CrossRefPubMed Ito M, Nishida A, Koga A, Ikeda S, Shiraishi A, Uetani M, Hayashi K, Nakamura T (2002) Contribution of trabecular and cortical components to the mechanical properties of bone and their regulating parameters. Bone 31(3):351–358CrossRefPubMed
52.
go back to reference Holzer G, Von Skrbensky G, Holzer LA, Pichl W (2009) Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res 24:468–474CrossRefPubMed Holzer G, Von Skrbensky G, Holzer LA, Pichl W (2009) Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res 24:468–474CrossRefPubMed
53.
go back to reference Manske SL, Liu-Ambrose T, Cooper DML, Kontulainen S, Guy P, Forster BB, McKay HA (2009) Cortical and trabecular bone in the femoral neck both contribute to proximal femur failure load prediction. Osteoporos Int 20:445–453CrossRefPubMed Manske SL, Liu-Ambrose T, Cooper DML, Kontulainen S, Guy P, Forster BB, McKay HA (2009) Cortical and trabecular bone in the femoral neck both contribute to proximal femur failure load prediction. Osteoporos Int 20:445–453CrossRefPubMed
54.
go back to reference Yates LB, Karasik D, Beck TJ, Cupples LA, Kiel DP (2007) Hip structural geometry in old and old-old age: similarities and differences between men and women. Bone 41(4):722–732CrossRefPubMed Yates LB, Karasik D, Beck TJ, Cupples LA, Kiel DP (2007) Hip structural geometry in old and old-old age: similarities and differences between men and women. Bone 41(4):722–732CrossRefPubMed
55.
go back to reference Looker AC, Beck TJ, Orwoll ES (2001) Does body size account for gender differences in femur bone density and geometry? J Bone Miner Res 16(7):1291–1299CrossRefPubMed Looker AC, Beck TJ, Orwoll ES (2001) Does body size account for gender differences in femur bone density and geometry? J Bone Miner Res 16(7):1291–1299CrossRefPubMed
Metadata
Title
Region-Specific Sex-Dependent Pattern of Age-Related Changes of Proximal Femoral Cancellous Bone and Its Implications on Differential Bone Fragility
Authors
Marija Djuric
Danijela Djonic
Petar Milovanovic
Slobodan Nikolic
Robert Marshall
Jelena Marinkovic
Michael Hahn
Publication date
01-03-2010
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 3/2010
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-009-9325-8

Other articles of this Issue 3/2010

Calcified Tissue International 3/2010 Go to the issue