Abstract
Histomorphometry is commonly applied to study bone remodeling. Histological definitions of cortical bone boundaries have not been consistent. In this study, new criteria for specific definition of the transitional zone between the cortical and cancellous bone in the femoral neck were developed. The intra- and inter-observer reproducibility of this method was determined by quantitative histomorphometry and areal overlapping analysis. The undecalcified histological sections of femoral neck specimens (n = 6; from men aged 17–59 years) were processed and scanned to acquire histological images of complete bone sections. Specific criteria were applied to define histological boundaries. “Absolute cortex area” consisted of pure cortical bone tissue only, and was defined mainly based on the size of composite canals and their distance to an additional “guide” boundary (so-called “preliminary cortex boundary,” the clear demarcation line of density between compact cortex and sparse trabeculae). Endocortical bone area was defined by recognizing characteristic endocortical structures adjacent to the preliminary cortical boundary. The present results suggested moderate to high reproducibility for low-magnification parameters (e.g., cortical bone area). The coefficient of variation (CV %) ranged from 0.02 to 5.61 in the intra-observer study and from 0.09 to 16.41 in the inter-observer study. However, the intra-observer reproducibility of some high-magnification parameters (e.g., osteoid perimeter/endocortical perimeter) was lower (CV %, 0.33–87.9). The overlapping of three histological areas in repeated analyses revealed highest intra- and inter-observer reproducibility for the absolute cortex area. This study provides specific criteria for the definition of histological boundaries for femoral neck bone specimens, which may aid more precise cortical bone histomorphometry.
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References
Schulman RC, Weiss AJ, Mechanick JI (2011) Nutrition, bone, and aging: an integrative physiology approach. Curr Osteoporos Rep 9:184–195
Diab T, Condon KW, Burr DB, Vashishth D (2006) Age-related change in the damage morphology of human cortical bone and its role in bone fragility. Bone (NY) 38:427–431
Buckwalter JA, Glimcher MJ, Cooper RR, Recker R (1995) Bone biology. J Bone Joint Surg 77:1276–1289
O’Brien FJ, Brennan O, Kennedy OD, Lee TC (2005) Microcracks in cortical bone: how do they affect bone biology? Curr Osteoporos Rep 3:39–45
Bell KL, Loveridge N, Power J, Rushton N, Reeve J (1999) Intracapsular hip fracture: increased cortical remodeling in the thinned and porous anterior region of the femoral neck. Osteoporos Int 10:248–257
Bell KL, Loveridge N, Jordan GR, Power J, Constant CR, Reeve J (2000) A novel mechanism for induction of increased cortical porosity in cases of intracapsular hip fracture. Bone (NY) 27:297–304
Crabtree N, Loveridge N, Parker M, Rushton N, Power J, Bell KL, Beck TJ, Reeve J (2001) Intracapsular hip fracture and the region-specific loss of cortical bone: analysis by peripheral quantitative computed tomography. J Bone Miner Res 16:1318–1328
Jordan GR, Loveridge N, Bell KL, Power J, Dickson GR, Vedi S, Rushton N, Clarke MT, Reeve J (2003) Increased femoral neck cancellous bone and connectivity in coxarthrosis (hip osteoarthritis). Bone (NY) 32:86–95
Thomas CD, Mayhew PM, Power J, Poole KE, Loveridge N, Clement JG, Burgoyne CJ, Reeve J (2009) Femoral neck trabecular bone: loss with aging and role in preventing fracture. J Bone Miner Res 24:1808–1818
Skala-Rosenbaum J, Cech O, Dzupa V (2012) Arthroplasty for intracapsular fractures of the femoral neck. Current concept review. Acta Chir Orthop Traumatol Cech 79:484–492
Loveridge N, Power J, Reeve J, Boyde A (2004) Bone mineralization density and femoral neck fragility. Bone (NY) 35:929–941
Power J, Loveridge N, Lyon A, Rushton N, Parker M, Reeve J (2003) Bone remodeling at the endocortical surface of the human femoral neck: a mechanism for regional cortical thinning in cases of hip fracture. J Bone Miner Res 18:1775–1780
Rauch F, Travers R, Glorieux FH (2006) Cellular activity on the seven surfaces of iliac bone: a histomorphometric study in children and adolescents. J Bone Miner Res 21:513–519
Rauch F, Travers R, Glorieux FH (2007) Intracortical remodeling during human bone development—a histomorphometric study. Bone (NY) 40:274–280
Ostertag A, Cohen-Solal M, Audran M, Legrand E, Marty C, de Chappard D, Vernejoul M-C (2009) Vertebral fractures are associated with increased cortical porosity in iliac crest bone biopsy of men with idiopathic osteoporosis. Bone (NY) 44:413–417
Vedi S, Kaptoge S, Compston JE (2011) Age-related changes in iliac crest cortical width and porosity: a histomorphometric study. J Anat 218:510–516
Power J, Doube M, van Bezooijen RL, Loveridge N, Reeve J (2012) Osteocyte recruitment declines as the osteon fills in: interacting effects of osteocytic sclerostin and previous hip fracture on the size of cortical canals in the femoral neck. Bone (NY) 50:1107–1114
Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:2–17
Poole KES, Vedi S, Debiram I, Rose C, Power J, Loveridge N, Warburton EA, Reeve J, Compston J (2009) Bone structure and remodelling in stroke patients: early effects of zoledronate. Bone (NY) 44:629–633
Recker RR, Bare SP, Smith SY, Varela A, Miller MA, Morris SA, Fox J (2009) Cancellous and cortical bone architecture and turnover at the iliac crest of postmenopausal osteoporotic women treated with parathyroid hormone 1–84. Bone (NY) 44:113–119
Arlot ME, Jiang Y, Genant HK, Zhao J, Burt-Pichat B, Roux J-P, Delmas PD, Meunier PJ (2007) Histomorphometric and μCT analysis of bone biopsies from postmenopausal osteoporotic women treated with strontium ranelate. J Bone Miner Res 23:215–222
Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S (2010) Age and gender related differences in the geometric properties and biomechanical significance of intra-cortical porosity in the distal radius and tibia. J Bone Miner Res 25:983–993
Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK (2007) Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone (NY) 41:505–515
Yeni YN, Brown CU, Wang Z, Norman TL (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone (NY) 21:453–459
Power J, Loveridge N, Lyon A, Rushton N, Parker M, Reeve J (2005) Osteoclastic cortical erosion as a determinant of subperiosteal osteoblastic bone formation in the femoral neck’s response to BMU imbalance. Effects of stance-related loading and hip fracture. Osteoporos Int 16:1049–1056
Goldenstein J, Kazakia G, Majumdar S (2010) In vivo evaluation of the presence of bone marrow in cortical porosity in postmenopausal osteopenic women. Ann Biomed Eng 38:235–246
Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J (2000) Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone (NY) 26:305–313
Bell KL, Loveridge N, Reeve J, Thomas CD, Feik SA, Clement JG (2001) Super-osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec 264:378–386
Lakshmanan S, Bodi A, Raum K (2007) Assessment of anisotropic tissue elasticity of cortical bone from high-resolution, angular acoustic measurements. IEEE Trans Ultrason Ferroelectr Freq Cont 54:1560–1570
Malo MK, Rohrbach D, Isaksson H, Toyras J, Jurvelin JS, Tamminen IS, Kroger H, Raum K (2013) Longitudinal elastic properties and porosity of cortical bone tissue vary with age in human proximal femur. Bone (NY) 53:451–458
van Oers RF, Ruimerman R, van Rietbergen B, Hilbers PA, Huiskes R (2008) Relating osteon diameter to strain. Bone (NY) 43:476–482
Bernhard A, Milovanovic P, Zimmermann EA, Hahn M, Djonic D, Krause M, Breer S, Puschel K, Djuric M, Amling M, Busse B (2013) Micro-morphological properties of osteons reveal changes in cortical bone stability during aging, osteoporosis, and bisphosphonate treatment in women. Osteoporos Int 30:30
Chappard C, Bensalah S, Olivier C, Gouttenoire PJ, Marchadier A, Benhamou C, Peyrin F (2013) 3D characterization of pores in the cortical bone of human femur in the elderly at different locations as determined by synchrotron micro-computed tomography images. Osteoporos Int 24:1023–1033
Cooper DML, Thomas CDL, Clement JG, Turinsky AL, Sensen CW, Hallgrímsson B (2007) Age-dependent change in the 3D structure of cortical porosity at the human femoral midshaft. Bone (NY) 40:957–965
Brown JP, Delmas PD, Arlot M, Meunier PJ (1987) Active bone turnover of the cortico-endosteal envelope in postmenopausal osteoporosis. J Clin Endocrinol Metab 64:954–959
Arlot ME, Delmas PD, Chappard D, Meunier PJ (1990) Trabecular and endocortical bone remodeling in postmenopausal osteoporosis: comparison with normal postmenopausal women. Osteoporos Int 1:41–49
Garrahan NJ, Mellish RW, Compston JE (1986) A new method for the two-dimensional analysis of bone structure in human iliac crest biopsies. J Microsc 142:341–349
Schnitzler CM, Mesquita JM, Pettifor JM (2009) Cortical bone development in black and white South African children: iliac crest histomorphometry. Bone (NY) 44:603–611
Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610
Acknowledgments
The authors acknowledge Ms. Ritva Sormunen and Mr. Arto Koistinen for their assistance in sample preparation. We also acknowledge the financial support from the China Scholarship Council (CSC), Sigrid Juselius Foundation, and the Strategic Funding of the University of Eastern Finland.
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All authors declare that they have no conflict of interest.
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Tong, XY., Malo, M., Tamminen, I.S. et al. Development of new criteria for cortical bone histomorphometry in femoral neck: intra- and inter-observer reproducibility. J Bone Miner Metab 33, 109–118 (2015). https://doi.org/10.1007/s00774-014-0562-1
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DOI: https://doi.org/10.1007/s00774-014-0562-1