A novel mechanism for induction of increased cortical porosity in cases of intracapsular hip fracture

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Bell, K. L.¹; Loveridge, N.¹; Jordan, G. R.¹; Power, J.¹; Constant, C. R.²; Reeve, J.¹

A novel mechanism for induction of increased cortical porosity in cases of intracapsular hip fracture

Bone. August 2000;27(2):297-304

©2000 Elsevier Science Inc. All rights reserved.

Affiliations

¹Bone Research Group (MRC), Department of Medicine, University of Cambridge, Cambridge, UK

²Department of Orthopaedics, Addenbrooke’s Hospital, Cambridge, UK
Abstract and keywords

It has been suggested that, in hip fracture, the cortex on the inferoanterior (IA) to superoposterior (SP) axis is thinned and shows increased porosity. This is dependent on the presence of giant canals (i.e., diameter >385 μm), which are related to clusters of remodeling osteons. To investigate further the relationship between remodeling and bone loss, osteonal diameter (On.Dm), wall thickness (W.Th), osteoid width (O.Wi), and extent (OS) were measured in femoral neck biopsies from 12 female intracapsular hip fracture cases and 11 age- and gender-matched controls. Over 83% of giant canals were “composite” osteonal systems in which a single canal was surrounded by multiple packets of osteonal bone. Among smaller canals, over 80% of systems had a canal encircled by a single cement line containing one packet of bone (“simple”). Composites were nearly twice as prevalent in fractures (fracture cases 9.8 ± 0.7/25 mm2, controls 5.3 ± 0.4/25 mm2, p < 0.0001), and were dependent (R² = 0.52) on femoral neck region (p = 0.0008) and the regional distribution of clusters of remodeling osteons (p = 0.0045). Both the inferior (I) and anterior (A) regions had an elevated number of composites (I: 263% of control values, p = 0.0054; A: 202% of control values, p = 0.0092). On.Dm was similar in fracture cases and controls (simple: fracture cases 183 ± 3 μm, controls 191 ± 4 μm; composites: fracture cases 446 ± 13 μm, controls 460 ± 13 μm). W.Th in simples was similar in fracture cases and controls (fracture cases 51 ± 0.8 μm, controls 49 ± 0.7 μm), but composites had significantly (p < 0.0001) thinner walls, with the reduction in fracture cases (31%) being twice that of controls (12%, p < 0.0001). There were no differences in O.Wi. It was unusual for osteoid to fully surround the composite canal surface; OS was 38% lower in composite than simple canals (p < 0.0001). This study indicates that, in the femoral neck cortex, the principal remodeling deficit in hip fracture is specific to composite osteons. Hip fracture cases had zonal increases in composite osteon density with reduced bone formation. The data suggest that generation of composite osteons is a plausible mechanism leading to increasing porosity and trabecularization of the cortex, thus weakening the cortex in regions maximally loaded on fall impact.

Keywords: Cortical remodeling; Femoral neck; Intracapsular hip fracture; Haversian canals; Osteoporosis
Links

DOI: 10.1016/S8756-3282(00)00318-5

PubMed: 10913926

WoS: 000088489000018
History

Received: 2000-01-21

Revised: 2000-04-04

Accepted: 2000-04-04

Cited Works (22)

Year	Entry
1990	Parfitt AM. Bone-forming cells in clinical conditions. In: Hall BK, ed. Bone. Volume 1: The Osteoblast and Osteocyte. Caldwell, NJ: Inc., The Telford Press; 1990:351-429.
1996	Lanyon LE. Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone. January 1996;18(1)(suppl):37S-43S.
1993	Mosekilde L. Vertebral structure and strength in vivo and in vitro. Calcif Tiss Int. February 1993;53(suppl 1):S121-S126.
1993	Mori S, Burr DB. Increased intracortical remodeling following fatigue damage. Bone. March–April 1993;14(2):103-109.
1993	Brockstedt H, Kassem M, Eriksen EF, Mosekilde L, Melsen F. Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone. July–August 1993;14(4):681-691.
1986	Mosekilde L, Mosekilde L. Normal vertebral body size and compressive strength: relations to age and to vertebral and iliac trabecular bone compressive strength. Bone. 1986;7(3):207-212.
1995	Gross TS, Rubin CT. Uniformity of resorptive bone loss induced by disuse. J Orthop Res. September 1995;13(5):708-714.
1990	Eriksen EF, Hodgson SF, Eastell R, Cedel SL, O'Fallon WM, Riggs BL. Cancellous bone remodeling in type I (postmenopausal) osteoporosis: quantitative assessment of rates of formation, resorption, and bone loss at tissue and cellular levels. J Bone Miner Res. April 1990;5(4):311-319.
1989	Mosekilde L. Sex differences in age-related loss of vertebral trabecular bone mass and structure—biomechanical consequences. Bone. 1989;10(6):425-432.
1999	Bell KL, Loveridge N, Power J, Garrahan N, Meggitt BF, Reeve J. Regional differences in cortical porosity in the fractured femoral neck. Bone. January 1999;24(1):57-64.
1983	Parfitt AM, Mathews CH, Villanueva AR, Kleerekoper M, Frame B, Rao DS. Relationships 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 Invest. October 1983;72(4):1396-1409.
1991	Cohen‐Solal ME, Shih M, Lundy MW, Parfitt AM. A new method for measuring cancellous bone erosion depth: application to the cellular mechanisms of bone loss in postmenopausal osteoporosis. J Bone Miner Res. December 1991;6(12):1331-1338.
1995	Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int. July 1995;5(3):252-261.
1983	Parfitt AM. The physiologic and clinical significance of bone histomorphometric data. In: Recker RR, ed. Bone Histomorphometry: Techniques and Interpretation. Boca Raton, FL: Inc., CRC Press; 1983:143-223.
1985	Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tiss Int. 1985;37(4):411-417.
1999	Bell KL, Loveridge N, Power J, Garrahan N, Stanton M, Lunt M, Meggitt BF, Reeve J. Structure of the femoral neck in hip fracture: cortical bone loss in the inferoanterior to superoposterior axis. J Bone Miner Res. January 1999;14(1):111-119.
1980	Thompson DD. Age changes in bone mineralization, cortical thickness, and Haversian canal area. Calcif Tiss Int. December 1980;31(1):5-11.
1986	Eriksen EF. Normal and pathological remodeling of human trabecular bone: three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease. Endocr Rev. November 1986;7(4):379-408.
1958	Cohen J, Harris WH. The three-dimensional anatomy of Haversian systems. J Bone Joint Surg. April 1958;40A(2):419-434.
1978	Lips P, Courpron P, Meunier PJ. Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif Tiss Res. 1978;26(1):13-17.
2000	Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J. Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone. March 2000;26(3):305-313.
1960	Jowsey J. Age changes in human bone. Clin Orthop. 1960;17:210-218.

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2025	Cole ME. Visualization and interpretation of cortical porosity. In: Stout SD, Crowder C, eds. Bone Histology: A Biological Anthropological Perspective. 2nd ed. Boca Raton, FL: CRC Press; 2025:442-470.
2001	Bell KL, Loveridge N, Reeve J, Thomas CDL, Feik SA, Clement JG. Super‐osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec. December 1, 2001;264(4):378-386.
2018	Andreasen CM, Delaisse J-M, van der Eerden BCJ, van Leeuwen JPTM, Ding M, Andersen TL. Understanding age-induced cortical porosity in women: is a negative BMU balance in quiescent osteons a major contributor? Bone. December 2018;117:70-82.
2020	Andreasen CM, Bakalova LP, Brüel A, Hauge EM, Kiil BJ, Delaisse J-M, Kersh ME, Thomsen JS, Andersen TL. The generation of enlarged eroded pores upon existing intracortical canals is a major contributor to endocortical trabecularization. Bone. January 2020;130:115127.
2011	Burghardt AJ, Link TM, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res. August 2011;469:2179-2193.
2005	Felsenberg D, Boonen S. The bone quality framework: determinants of bone strength and their interrelationships, and implications for osteoporosis management. Clin Ther. January 2005;27(1):1-11.
2016	Granke M, Makowski AJ, Uppuganti S, Nyman JS. Prevalent role of porosity and osteonal area over mineralization heterogeneity in the fracture toughness of human cortical bone. J Biomech. September 6, 2016;49(13):2748-2755.
2018	Andreasen CM, Delaisse J, van der Eerden BCJ, van Leeuwen JPTM, Ding M, Andersen TL. Understanding age-induced cortical porosity in women: the accumulation and coalescence of eroded cavities upon existing intracortical canals is the main contributor. J Bone Miner Res. April 2018;33(4):606-620.
2018	Bakalova LP, Andreasen CM, Thomsen JS, Brüel A, Hauge E-M, Kiil BJ, Delaisse J-M, Andersen TL, Kersh ME. Intracortical bone mechanics are related to pore morphology and remodeling in human bone. J Bone Miner Res. December 2018;33(12):2177-2185.
2005	Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J. Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet. July 9, 2005;366(9480):129-135.
2008	Techawiboonwong A, Song HK, Leonard MB, Wehrli FW. Cortical bone water: in vivo quantification with ultrashort echo-time MR imaging. Radiology. September 2008;248(3):824-833.
2007	Clark EM. An Investigation Into the Role of Bone Mass and Other Factors in Determining Fracture Risk in Children [PhD thesis]. Bristol, UK: University of Bristol; 2007.
2006	Poole KES. The Effects of Stroke on the Skeleton [PhD thesis]. Cambridge, UK: University of Cambridge; 2006.
2003	Winwood K. An Experimental Investigation Into the Effects of Cyclic Fatigue on Ageing Human Cortical Bone [PhD thesis]. Cranfield University; September 2003.
2018	Wang M. Effect of Osteonal Microstructure on Crack Propagation: A Computational Study [PhD thesis]. Loughborough University; October 2018.
2019	Nobakhti S. Multiscale Characteristics of Bone Toughness [PhD thesis]. Northeastern University; July 2019.
2019	Piet J. Restoring Mechano-Adaptation in Aged Murine Bone [PhD thesis]. Northeastern University; March 2019.
2015	Hunter RL. Variation in Cortical Osteocyte Lacunar Density and Distribution: Implications for Bone Quality Assessment [PhD thesis]. The Ohio State University; 2015.
2008	Kennedy OD. The Effect of Bone Turnover on Bone Quality and Material Properties [PhD thesis]. Trinity College Dublin; 2008.
2011	Ebacher V. Experimental Study of Deformation and Microcracking in Human Cortical Bone [PhD thesis]. Vancouver, BC: University of British Columbia; May 2011.
2018	Alousaimi H. A Study of Bone Quality in Femoral Neck of Osteoarthritis [Master's thesis]. Vancouver, BC: University of British Columbia; August 2018.
2018	Tang T. Fracture Mechanisms and Structural Fragility of Human Femoral Cortical Bone [PhD thesis]. Vancouver, BC: University of British Columbia; April 2018.
2005	Cooper DML. 3D Micro-CT Imaging of Human Cortical Bone Porosity: A Novel Method for Estimating Age At Death [PhD thesis]. Calgary, AB: University of Calgary; December 2005.
2012	Nishiyama KKS. In Vivo Assessment of Bone Microarchitecture and Estimated Bone Strength [PhD thesis]. Calgary, AB: University of Calgary; October 2012.
2019	Surowiec R. Novel Models to Image and Quantify Bone Drug Efficacy and Disease Progression in Vivo: Addressing the Fragility Phenotype [PhD thesis]. University of Michigan; 2019.