Skip to main content

Advertisement

SpringerLink
Log in

Age-Related Three-Dimensional Microarchitectural Adaptations of Subchondral Bone Tissues in Guinea Pig Primary Osteoarthrosis

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

We explored potential mechanisms of the microarchitectural adaptations of subchondral bone tissues in a guinea pig primary osteoarthrosis (OA) model. We harvested proximal tibiae of male Dunkin-Hartley (Charles River strain) guinea pigs at 3, 6, 9, 12, and 24 months of age (10 in each group). These proximal tibiae were scanned by micro-computed tomography to quantify the three-dimensional microarchitecture of the subchondral plate, cancellous bone, and cortical bone. Subsequently, the bones were compression-tested to determine their mechanical properties. Furthermore, bone collagen, bone mineral, and bone density were determined. Mankin’s score corresponded to OA grading from absent or minimal cartilage degeneration in 3-month-old to severe degeneration in 24-month-old guinea pigs. In young guinea pigs, the volume fraction and thickness of the subchondral plate markedly increased from 3 to 6 months, whereas the volume fraction of the subchondral cancellous bone displayed an initial decline followed by an increase. With age, the trabeculae increased in thickness, changed from rod-like to plate-like, and became more axially oriented. An increasing ratio of bone collagen to mineral in subchondral bone indicated undermineralized bone tissues. In subchondral cancellous bone, Young’s modulus was maximal at 6 months of age, whereas ultimate stress and failure energy showed a gradual increase with age. The findings show pronounced alterations of the microarchitecture and bone matrix composition of the subchondral bone. These alterations did not appear to follow the same pattern as in normal aging and may have different influences on the resulting mechanical properties.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Carlson CS, Loeser RF, Purser CB, Gardin JF, Jerome CP (1996) Osteoarthritis in cynomolgus macaques. III: Effects of age, gender, and subchondral bone thickness on the severity of disease. J Bone Miner Res 11:1209–1217

    CAS  PubMed  Google Scholar 

  2. Bendele AM, Hulman JF (1988) Spontaneous cartilage degeneration in guinea pigs. Arthritis Rheum 31:561–565

    CAS  PubMed  Google Scholar 

  3. Walton M (1977) Degenerative joint disease in the mouse knee; radiological and morphological observations. J Pathol 123:97–107

    CAS  PubMed  Google Scholar 

  4. Watson PJ, Hall LD, Malcolm A, Tyler JA (1996) Degenerative joint disease in the guinea pig. Use of magnetic resonance imaging to monitor progression of bone pathology. Arthritis Rheum 39:1327–1337

    CAS  PubMed  Google Scholar 

  5. Bendele AM, White SL, Hulman JF (1989) Osteoarthrosis in guinea pigs: histopathologic and scanning electron microscopic features. Lab Anim Sci 39:115–121

    CAS  PubMed  Google Scholar 

  6. Jimenez PA, Glasson SS, Trubetskoy OV, Haimes HB (1997) Spontaneous osteoarthritis in Dunkin Hartley guinea pigs: histologic, radiologic, and biochemical changes. Lab Anim Sci 47:598–601

    CAS  PubMed  Google Scholar 

  7. de-Bri E, Reinholt FP, Svensson O (1995) Primary osteoarthrosis in guinea pigs: a stereological study. J Orthop Res 13:769–776

    CAS  PubMed  Google Scholar 

  8. Radin EL, Rose RM (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop 34–40

    PubMed  Google Scholar 

  9. Mansell JP, Bailey AJ (1998) Abnormal cancellous bone collagen metabolism in osteoarthritis. J Clin Invest 101:1596–1603

    Article  CAS  PubMed  Google Scholar 

  10. Boivin G, Meunier PJ (2003) The mineralization of bone tissue: a forgotten dimension in osteoporosis research. Osteoporos Int 14(suppl 3):19–24

    Google Scholar 

  11. Ding M, Dalstra M, Linde F, Hvid I (1998) Changes in the stiffness of the human tibial cartilage-bone complex in early-stage osteoarthrosis. Acta Orthop Scand 69:358–362

    CAS  PubMed  Google Scholar 

  12. Ding M, Danielsen CC, Hvid I (2001) Bone density does not reflect mechanical properties in early-stage arthrosis. Acta Orthop Scand 72:181–185

    Article  CAS  PubMed  Google Scholar 

  13. Ding M, Odgaard A, Hvid I (2003) Changes in the three-dimensional microstructure of human tibial cancellous bone in early osteoarthritis. J Bone Joint Surg Br 85:906–912

    CAS  PubMed  Google Scholar 

  14. Li B, Aspden RM (1997) Composition and mechanical properties of cancellous bone from the femoral head of patients with osteoporosis or osteoarthritis. J Bone Miner Res 12:641–651

    CAS  PubMed  Google Scholar 

  15. Li B, Aspden RM (1997) Material properties of bone from the femoral neck and calcar femorale of patients with osteoporosis or osteoarthritis. Osteoporos Int 7:450–456

    Article  CAS  PubMed  Google Scholar 

  16. Li B, Aspden RM (1997) Mechanical and material properties of the subchondral bone plate from the femoral head of patients with osteoarthritis or osteoporosis. Ann Rheum Dis 56:247–254

    Article  CAS  PubMed  Google Scholar 

  17. Ding M, Odgaard A, Hvid I (1999) Accuracy of cancellous bone volume fraction measured by micro-CT scanning. J Biomech 32:323–326

    Article  CAS  PubMed  Google Scholar 

  18. Ding M, Dalstra M, Danielsen CC, Kabel J, Hvid I, Linde F (1997) Age variations in the properties of human tibial trabecular bone. J Bone Joint Surg Br 79:995–1002

    Article  CAS  PubMed  Google Scholar 

  19. Ding M, Danielsen CC, Hvid I (2005) Effects of hyaluronan on three-dimensional microarchitecture of subchondral bone tissues in guinea pig primary osteoarthrosis. Bone 36:489–501

    Article  CAS  PubMed  Google Scholar 

  20. Hildebrand T, Rüegsegger P (1997) A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc 185:67–75

    Article  Google Scholar 

  21. Hildebrand T, Rüegsegger P (1997) Quantification of bone microarchitecture with the structure model index. CMBBE 1:15–23

    PubMed  Google Scholar 

  22. Goulet RW, Goldstein SA, Ciarelli MJ, Kuhn JL, Brown MB, Feldkamp LA (1994) The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech 27:375–389

    CAS  PubMed  Google Scholar 

  23. Odgaard A, Gundersen HJ (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14:173–182

    Article  CAS  PubMed  Google Scholar 

  24. Odgaard A (1997) Three-dimensional methods for quantification of cancellous bone architecture. Bone 20:315–328

    Article  CAS  PubMed  Google Scholar 

  25. Mankin HJ, Dorfman H, Lippiello L, Zarins A (1971) Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 53:523–537

    CAS  PubMed  Google Scholar 

  26. Hogan HA, Ruhmann SP, Sampson HW (2000) The mechanical properties of cancellous bone in the proximal tibia of ovariectomized rats. J Bone Miner Res 15:284–292

    CAS  PubMed  Google Scholar 

  27. Ding M, Odgaard A, Linde F, Hvid I (2002) Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res 20:615–621

    Article  PubMed  Google Scholar 

  28. Ding M, Hvid I (2000) Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone 26:291–295

    Article  CAS  PubMed  Google Scholar 

  29. 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 84:900–907

    Article  PubMed  Google Scholar 

  30. Nafei A, Kabel J, Odgaard A, Linde F, Hvid I (2000) Properties of growing trabecular ovine bone. Part II: Architectural and mechanical properties. J Bone Joint Surg Br 82:921–927

    CAS  PubMed  Google Scholar 

  31. Tanck E, Homminga J, van Lenthe GH, Huiskes R (2001) Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone 28:650–654

    Article  CAS  PubMed  Google Scholar 

  32. Kamibayashi L, Wyss UP, Cooke TD, Zee B (1995) Changes in mean trabecular orientation in the medial condyle of the proximal tibia in osteoarthritis. Calcif Tissue Int 57:69–73

    Article  CAS  PubMed  Google Scholar 

  33. Boyd SK, Muller R, Zernicke RF (2002) Mechanical and architectural bone adaptation in early stage experimental osteoarthritis. J Bone Miner Res 17:687–694

    PubMed  Google Scholar 

  34. Bailey AJ, Mansell JP (1997) Do subchondral bone changes exacerbate or precede articular cartilage destruction in osteoarthritis of the elderly? Gerontology 43:296–304

    Article  CAS  PubMed  Google Scholar 

  35. McCalden RW, McGeough JA, Barker MB, Court BC (1993) Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg Am 75:1193–1205

    CAS  PubMed  Google Scholar 

  36. Burr DB (2002) The contribution of the organic matrix to bone’s material properties. Bone 31:8–11

    Article  CAS  PubMed  Google Scholar 

  37. Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7

    Article  PubMed  Google Scholar 

  38. Danielsen CC, Mosekilde L, Svenstrup B (1993) Cortical bone mass, composition, and mechanical properties in female rats in relation to age, long-term ovariectomy, and estrogen substitution. Calcif Tissue Int 52:26–33

    Article  CAS  PubMed  Google Scholar 

  39. Mansell JP, Tarlton JF, Bailey AJ (1997) Biochemical evidence for altered subchondral bone collagen metabolism in osteoarthritis of the hip. Br J Rheumatol 36:16–19

    Article  CAS  PubMed  Google Scholar 

  40. Lane NE, Nevitt MC (1994) Osteoarthritis and bone mass. J Rheumatol 21:1393–1396

    CAS  PubMed  Google Scholar 

  41. Kirwan JR, Silman AJ (1987) Epidemiological, sociological and environmental aspects of rheumatoid arthritis and osteoarthrosis. Baillieres Clin Rheumatol 1:467–489

    CAS  PubMed  Google Scholar 

  42. Nelson DA, Jacobsen G, Barondess DA, Parfitt AM (1995) Ethnic differences in regional bone density, hip axis length, and lifestyle variables among healthy black and white men. J Bone Miner Res 10:782–787

    Article  CAS  PubMed  Google Scholar 

  43. Huebner JL, Hanes MA, Beekman B, TeKoppele JM, Kraus VB (2002) A comparative analysis of bone and cartilage metabolism in two strains of guinea-pig with varying degrees of naturally occurring osteoarthritis. Osteoarthritis Cartilage 10:758–767

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Danish Rheumatism Association (Gigtforeningen, grant 233-949-11.07.00), Hørslev-fonden, and Helga og Peter Kornings Fond. We thank Jane Pauli, Anette Milton, and Eva Mikkelsen for skillful technical assistance and Ulla Dansberg and Hilmar Hald for animal care.

Author information

Authors and Affiliations

  1. Orthopedic Research Laboratory, Department of Orthopedics, Aarhus University Hospital, Aarhus C, Denmark

    M. Ding & I. Hvid

  2. Orthopedic Research Laboratory, Department of Orthopedics and Laboratory for Molecular Endocrinology, Odense University Hospital, Odense C, Denmark

    M. Ding

  3. Department of Connective Tissue Biology, Institute of Anatomy, University of Aarhus, Aarhus C, Denmark

    C. C. Danielsen

Authors
  1. M. Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. C. Danielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Hvid
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Ding.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ding, M., Danielsen, C.C. & Hvid, I. Age-Related Three-Dimensional Microarchitectural Adaptations of Subchondral Bone Tissues in Guinea Pig Primary Osteoarthrosis. Calcif Tissue Int 78, 113–122 (2006). https://doi.org/10.1007/s00223-005-0028-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-005-0028-5

Keywords

Search

Navigation