Skip to main content
Log in

Development of new criteria for cortical bone histomorphometry in femoral neck: intra- and inter-observer reproducibility

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Schulman RC, Weiss AJ, Mechanick JI (2011) Nutrition, bone, and aging: an integrative physiology approach. Curr Osteoporos Rep 9:184–195

    Article  PubMed  Google Scholar 

  2. 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

    Article  Google Scholar 

  3. Buckwalter JA, Glimcher MJ, Cooper RR, Recker R (1995) Bone biology. J Bone Joint Surg 77:1276–1289

    Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  Google Scholar 

  9. 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

    Article  PubMed  Google Scholar 

  10. 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

    CAS  PubMed  Google Scholar 

  11. Loveridge N, Power J, Reeve J, Boyde A (2004) Bone mineralization density and femoral neck fragility. Bone (NY) 35:929–941

    Article  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. Rauch F, Travers R, Glorieux FH (2007) Intracortical remodeling during human bone development—a histomorphometric study. Bone (NY) 40:274–280

    Article  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    Article  PubMed Central  PubMed  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

    Article  PubMed Central  PubMed  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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

    Article  CAS  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Google Scholar 

  23. 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

    Article  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  PubMed Central  PubMed  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  CAS  Google Scholar 

  31. van Oers RF, Ruimerman R, van Rietbergen B, Hilbers PA, Huiskes R (2008) Relating osteon diameter to strain. Bone (NY) 43:476–482

    Article  Google Scholar 

  32. 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

    Google Scholar 

  33. 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

    Google Scholar 

  34. 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

    Article  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  CAS  PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. 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

    Article  CAS  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Conflict of interest

All authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiao-Yu Tong.

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-014-0562-1

Keywords

Navigation