Log in

Spatial Distribution of Microcracks in Osteoarthritic Femoral Neck: Influence of Osteophytes on Microcrack Formation

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Osteophytes have been suggested to influence the bone mechanical properties. The aim of this study was to compare the microcrack density in osteophytes with that in the other parts of the osteoarthritic femoral neck (FN). The presence of microcracks was investigated in the ultra-distal FN and in the osteophytes in samples obtained during hip arthroplasty in 24 postmenopausal women aged 67 ± 10 years. Furthermore, the 3D microarchitecture and the collagen crosslinks contents were assessed by high-resolution peripheral quantitative computed tomography and high-performance liquid chromatography, respectively. Osteophytes were present in the 24 FN, mainly at the level of the inferior quadrant. Microcracks were present in all FN with an average of 2.8 per sample. All observed microcracks were linear. The microcrack density (Cr.N/BV; #/mm2) was significantly higher in cancellous than in cortical bone (p = 0.004), whereas the microcrack length (Cr.Le, µm) was significantly greater in cortical bone (p = 0.04). The collagen crosslinks ratio pyridinoline/deoxypyridinoline was significantly and negatively correlated with Cr.N/BV in the posterior (r′ = − 0.68, p = 0.01) and inferior (r′ = − 0.53, p = 0.05) quadrants. Microcracks were observed in seven osteophytes in seven patients. When microcracks were present in the osteophyte area, Cr.N/BV was also significantly higher in the whole FN and in the quadrant of the osteophyte compared to the cases without microcrack in the osteophyte (p < 0.03). In conclusion, in FN from hip osteoarthritis microcracks are present in all FNs but in only 23% of the osteophytes. The microcrack formation was greater and their progression was smaller in the cancellous bone than in the cortex. The spatial distribution of microcracks varied according to the proximity of the osteophyte, and suggests that osteophyte may influence microcrack formation related to changes in local bone quality.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Gelse K, Söder S, Eger W, Diemtar T, Aigner T (2003) Osteophyte development—molecular characterization of differentiation stages. Osteoarthr Cartil 11:141–118. https://doi.org/10.1053/joca.2002.0873

    Article  Google Scholar 

  2. van der Kraan PM, van den Berg WB (2007) Osteophytes: relevance and biology. Osteoarthr Cartil 15:237–244. https://doi.org/10.1016/j.joca.2006.11.006

    Article  PubMed  Google Scholar 

  3. Saha PK, Liang G, Elkins JM, Coimbra A, Duong LT, Williams DS, Sonka M (2011) A new osteophyte segmentation algorithm using partial shape model and its applications to rabbit femur anterior cruciate ligament transection via micro-CT imaging. IEEE Trans Biomed Eng. https://doi.org/10.1109/TBME.2011.2129519

    Article  PubMed  PubMed Central  Google Scholar 

  4. Blain H, Chavassieux P, Portero-Muzy N, Bonnel F, Canovas F, Chammas M, Maury P, Delmas PD (2008) Cortical and trabecular bone distribution in the femoral neck in osteoporosis and osteoarthritis. Bone 43:862–868. https://doi.org/10.1016/j.bone.2008.07.236

    Article  CAS  PubMed  Google Scholar 

  5. Boutroy S, Vilayphiou N, Roux JP, Delmas PD, Blain H, Chapurlat RD, Chavassieux P (2011) Comparison of 2D and 3D bone microarchitecture evaluation at the femoral neck, among postmenopausal women with hip fracture or hip osteoarthritis. Bone 49:1055–1061. https://doi.org/10.1016/j.bone.2011.07.037

    Article  PubMed  Google Scholar 

  6. Rabelo GD, Roux JP, Portero-Muzy N, Gineyts E, Chapurlat R, Chavassieux P (2018) Cortical fractal analysis and collagen crosslinks content in femoral neck after osteoporotic fracture in postmenopausal women: comparison with osteoarthritis. Calcif Tissue Int 102:644-650. https://doi.org/10.1007/s00223-017-0378-9

    Article  PubMed  Google Scholar 

  7. Al-Rawahi M, Luo J, Pollintine P, Dolan P, Adams MA (2011) Mechanical function of vertebral body osteophytes, as revealed by experiments on cadaveric spines. Spine (Phila Pa 1976) 36:770–777. https://doi.org/10.1097/BRS.0b013e3181df1a70

    Article  Google Scholar 

  8. Castaño-Betancourt MC, Rivadeneira F, Bierma-Zeinstra S, Kerkhof HJ, Hofman A, Uitterlinden AG, van Meurs JB (2013) Bone parameters across different types of hip osteoarthritis and their relationship to osteoporotic fracture risk. Arthritis Rheum 65:693–700. https://doi.org/10.1002/art.37792

    Article  CAS  PubMed  Google Scholar 

  9. Chavassieux P, Seeman E, Delmas PD (2007) Insights into material and structural basis of bone fragility from diseases associated with fractures: how determinants of the biomechanical properties of bone are compromised by disease. Endocr Rev 28:151–164. https://doi.org/10.1210/er.2006-0029

    Article  CAS  PubMed  Google Scholar 

  10. Qiu S, Rao DS, Fyhrie DP, Palnitkar S, Parfitt AM (2013) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37:10–15. https://doi.org/10.1016/j.bone.2005.01.023

    Article  Google Scholar 

  11. Mori S, Burr DB (1993) Increased intracortical remodeling following fatigue damage. Bone 14:103–109. https://doi.org/10.1016/8756-3282(93)90235-3

    Article  CAS  PubMed  Google Scholar 

  12. Vashishth D, Behiri JC, Bonfield W. Crack growth resistance in cortical bone: concept of microcrack toughening. J Biomech 30:763–769. https://doi.org/10.1016/S0021-9290(97)00029-8

    Article  CAS  Google Scholar 

  13. Chapurlat RD, Delmas PD (2009) Bone microcrack: a clinical perspective. Osteoporos Int 20:1299–1308. https://doi.org/10.1007/s00198-009-0899-9

    Article  CAS  PubMed  Google Scholar 

  14. Portero-Muzy NR, Chavassieux PM, Arlot ME, Chapurlat RD (2011) Staining procedure for the detection of microcracks: application to ewe bone. Bone 49:917–919. https://doi.org/10.1016/j.bone.2011.07.001

    Article  CAS  PubMed  Google Scholar 

  15. Chappard D, Legrand E, Haettich B, Chales G, Auvinet B, Eschard JP, Hamelin JP, Basle MF, Audran M (2001) Fractal dimension of trabecular bone: comparison of three histomorphometric computed techniques for measuring the architectural two-dimensional complexity. J Pathol 195:515–521. https://doi.org/10.1002/path.970

    Article  CAS  PubMed  Google Scholar 

  16. Viguet-Carrin S, Gineyts E, Bertholon C, Delmas PD (2009) Simple and sensitive method for quantification of fluorescent enzymatic mature and senescent crosslinks of collagen in bone hydrolysate using single-column high performance liquid chromatography. J Chromatogr B 877:1–7. https://doi.org/10.1016/j.jchromb.2008.10.043

    Article  CAS  Google Scholar 

  17. Seeman E, Delmas PD (2006) Bone quality—the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261. https://doi.org/10.1056/NEJMra053077

    Article  CAS  Google Scholar 

  18. Burr DB, Turner CH, Naick P, Forwood MR, Ambrosius W, Hasan MS, Pidaparti R (1998) Does microdamage accumulation affect the mechanical properties of bone? J Biomech 31:337–345. https://doi.org/10.1016/S0021-9290(98)00016-5

    Article  CAS  PubMed  Google Scholar 

  19. Tang T, Cripton PA, Guy P, McKay HA, Wang R (2018) Clinical hip fracture is accompanied by compression induced failure in the superior cortex of the femoral neck. Bone 108:121–131. https://doi.org/10.1016/j.bone.2017.12.020

    Article  PubMed  Google Scholar 

  20. Lotz JC, Cheal EJ, Hayes WC (1995) Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int 5:252–261

    Article  CAS  Google Scholar 

  21. 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 38:427–431. https://doi.org/10.1016/j.bone.2005.09.002

    Article  PubMed  Google Scholar 

  22. Nyman JS, Reyes M, Wang X (2005) Effect of ultrastructural changes on the toughness of bone. Micron 36:566–582. https://doi.org/10.1016/j.micron.2005.07.004

    Article  CAS  PubMed  Google Scholar 

  23. Courtney AC, Hayes WC, Gibson LJ (1996) Age-related differences in post-yield damage in human cortical bone. Exp Model J Biomech 29:1463–1471

    Article  CAS  Google Scholar 

  24. Diab T, Vashishth D (2007) Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone 40:612–618. https://doi.org/10.1016/j.bone.2006.09.027

    Article  PubMed  Google Scholar 

  25. Green JO, Wang J, Diab T, Vidakovic B, Guldberg RE (2011) Age-related differences in the morphology of microdamage propagation in trabecular bone. J Biomech 44:2659–2666. https://doi.org/10.1016/j.jbiomech.2011.08.006

    Article  PubMed  PubMed Central  Google Scholar 

  26. Fazzalari NL, Forwood MR, Smith K, Manthey BA, Herreen P (1998) Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone 22:381–388. https://doi.org/10.1016/S8756-3282(97)00298-6

    Article  CAS  PubMed  Google Scholar 

  27. Karim L, Vashishth D (2011) Role of trabecular microarchitecture in the formation, accumulation, and morphology of microdamage in human cancellous bone. J Orthop Res 29:1739–1744. https://doi.org/10.1002/jor.21448

    Article  PubMed  PubMed Central  Google Scholar 

  28. Chapurlat RD, Arlot M, Burt-Pichat B, Chavassieux P, Roux JP, Portero-Muzy N, Delmas PD (2007) Microcrack frequency and bone remodeling in postmenopausal osteoporotic women on long-term bisphosphonates: a bone biopsy study. J Bone Miner Res 22:1502–1509. https://doi.org/10.1359/jbmr.070609

    Article  CAS  PubMed  Google Scholar 

  29. Follet H, Farlay D, Bala Y, Viguet-Carrin S, Gineyts E, Burt-Pichat B, Wegrzyn J, Delmas P, Boivin G, Chapurlat R (2013) Determinants of microdamage in elderly human vertebral trabecular bone. PLoS ONE 8:e55232. https://doi.org/10.1371/journal.pone.0055232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mohsin S, O’Brien FJ, Lee TC (2006) Osteonal crack barriers in ovine compact bone. J Anat 208:81–89. https://doi.org/10.1111/j.1469-7580.2006.00509.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bernhard A, Milovanovic P, Zimmermann EA, Hahn M, Djonic D, Krause M, Breer S, Püschel 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 24:2671–2680. https://doi.org/10.1007/s00198-013-2374-x

    Article  CAS  PubMed  Google Scholar 

  32. Dooley C, Tisbo P, Lee TC, Taylor D (2012) Rupture of osteocyte processes across microcracks: the effect of crack length and stress. Biomech Model Mechanobiol 11:759–766. https://doi.org/10.1007/s10237-011-0349-4

    Article  PubMed  Google Scholar 

  33. Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336. https://doi.org/10.1007/s00198-005-2035-9

    Article  CAS  PubMed  Google Scholar 

  34. Banse X, Sims TJ, Bailey AJ (2002) Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 17:1621–1628. https://doi.org/10.1359/jbmr.2002.17.9.1621

    Article  CAS  PubMed  Google Scholar 

  35. Oni OO, Morrison CJ (1998) The mechanical ‘quality’ of osteophytes. Injury 29:31–33. https://doi.org/10.1016/S0020-1383(97)00122-8

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author Gustavo Davi Rabelo thanks “Ciência sem Fronteiras—Conselho Nacional de Desenvolvimento Científico e Tecnológico/Brasil” (Processos: 245336/2012-5 e 301588/2014-7) for the scholarship.

Author information

Authors and Affiliations

Authors

Contributions

PC and RC designed the study. GDR and PC were evolved in all phases of the study and in writing the manuscript. NPM, EG, and JPR contributed to the experimental work and drafting the results. PC and RC are guarantors of the data. All authors revised and approved the final version of the manuscript and the decision to submit the manuscript for publication.

Corresponding author

Correspondence to Pascale Chavassieux.

Ethics declarations

Conflict of interest

Gustavo Davi Rabelo, Nathalie Portero-Muzy, Evelyne Gineyts, Jean-Paul Roux, Roland Chapurlat, and Pascale Chavassieux declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

All procedures performed in studies involving human participants were in accordance with the ethical standard of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the research ethics committee, and written informed consent to participation in the study was obtained for all women.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rabelo, G.D., Portero-Muzy, N., Gineyts, E. et al. Spatial Distribution of Microcracks in Osteoarthritic Femoral Neck: Influence of Osteophytes on Microcrack Formation. Calcif Tissue Int 103, 617–624 (2018). https://doi.org/10.1007/s00223-018-0456-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-018-0456-7

Keywords

Navigation