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Journal of Bone and Mineral Metabolism

, Volume 35, Issue 3, pp 308–314 | Cite as

Crystallographic orientation of the c-axis of biological apatite as a new index of the quality of subchondral bone in knee joint osteoarthritis

  • Jee-Wook Lee
  • Akio Kobayashi
  • Takayoshi NakanoEmail author
Original Article

Abstract

The aim of the present study was to investigate the preferred orientation of biological apatite (BAp) as a new index of the quality of subchondral bone (SB) in knee joint osteoarthritis (OA). Ten OA and five normal knee joints were obtained. Thickness, quantity and bone mineral density (BMD) of SB were analyzed at the medial condyle of the femur in dry conditions by peripheral quantitative computed tomography. In addition, the preferred crystallographic orientation of the c-axis of BAp was evaluated as bone quality parameter using a microbeam X-ray diffractometer technique. BMD and thickness of SB were significantly increased in OA specimens compared to normal knee specimens (P < 0.01), and the preferred orientation of the c-axis of BAp along the normal direction of SB surface was significantly higher in OA specimens (P < 0.01), reflecting the change in stress of concentration in the pathological portion without cartilage. SB sclerosis in OA results in both proliferation of bone tissues and enhanced degree of preferential alignment of the c-axis of BAp. Our findings could have major implications for the diagnosis of clinical studies, including pathologic elucidation in OA.

Keywords

Osteoarthritis (OA) Apatite orientation Bone quality Microbeam X-ray diffractometer (μXRD) 

Notes

Acknowledgments

The authors would like to thank Prof. Yuji Nakajima and Prof. Hiroshi Kiyama, Osaka City University for providing the bone specimens. We wish to thank the family of the donor for the generosity in the face of the bereavement. This work was supported by Grants-in-Aid for Scientific Research (S) from the Japan Society for Promotion of Science (Grant No. 25220912) and basic science research program through the National Research Foundation of Korea (NRF) (2009-0093814).

Compliance with ethical standards

Conflict of interest

None of the authors has competing interests to declare.

Supplementary material

774_2016_754_MOESM1_ESM.pdf (212 kb)
Supplementary material 1 (PDF 212 kb)

References

  1. 1.
    Boskey AL (2006) Mineralization, structure and function of bone. Dynamics of bone and cartilage metabolism: principles and clinical applications, vol 2. Academic Press, Massachusetts, pp 201–212CrossRefGoogle Scholar
  2. 2.
    Fleisch H (2000) Bisphosphonates in bone disease, vol 4. Academic Press, Massachusetts, pp 1–26CrossRefGoogle Scholar
  3. 3.
    Jackson SA, Cartwright AG, Lewis D (1978) The morphology of bone mineral crystals. Calcif Tissue Res 25:217–222CrossRefPubMedGoogle Scholar
  4. 4.
    Elliott JC, Wilson RM, Dowker SEP (2002) Apatite structures. Adv X-Ray Anal 45:172–181Google Scholar
  5. 5.
    Brès EF, Waddington WG, Hutchison JL, Cohen S, Mayer I, Voegel JC (1987) Detection of non-hexagonal symmetry in an apatite-structure-related mineral (Nasonite). Acta Crystallogr B43:171–174CrossRefGoogle Scholar
  6. 6.
    Katz J, Ukraincik K (1971) On the anisotropic elastic properties of hydroxyapatite. J Biomech 4:221–227CrossRefPubMedGoogle Scholar
  7. 7.
    Nakano T, Kaibara K, Tabata Y, Nagata N, Enomoto S, Marukawa E, Umakoshi Y (2002) Unique alignment and texture of biological apatite crystallites in typical calcified tissues analyzed by microbeam X-ray diffractometer system. Bone 31:479–487CrossRefPubMedGoogle Scholar
  8. 8.
    Matsugaki A, Aramoto G, Ninomiya T, Sawada H, Hata S, Nakano T (2015) Abnormal arrangement of a collagen/apatite extracellular matrix orthogonal to osteoblast alignment is constructed by a nanoscale periodic surface structure. Biomaterials 37:134–143CrossRefPubMedGoogle Scholar
  9. 9.
    Ishimoto T, Nakano T, Umakoshi Y, Yamamoto M, Tabata Y (2013) Degree of biological apatite c-axis orientation rather than bone mineral density controls mechanical function in bone regenerated using recombinant bone morphogenetic protein-2. J Bone Miner Res 28:1170–1179CrossRefPubMedGoogle Scholar
  10. 10.
    Noyama Y, Nakano T, Ishimoto T, Yoshikawa H (2013) Design and optimization of the oriented groove on the hip implant surface to promote bone microstructure integrity. Bone 52:659–667CrossRefPubMedGoogle Scholar
  11. 11.
    Nakano T, Ishimoto T, Lee JW, Umakoshi Y, Yamamoto M, Tabata Y, Kobayashi A, Iwaki H, Takaoka K, Kawai M, Yamamoto T (2006) Crystallographic approach to regenerated and pathological hard tissues. Mater Sci Forum 512:255–260CrossRefGoogle Scholar
  12. 12.
    Lee JW, Nakano T, Toyosawa S, Tabata Y, Umakoshi Y (2007) Areal distribution of preferential alignment of biological apatite (BAp) crystallite on cross-section of center of femoral diaphysis in osteopetrotic (op/op) mouse. Mater Trans 48:337–342CrossRefGoogle Scholar
  13. 13.
    Nakano T, Kaibara K, Ishimoto T, Tabata Y, Umakoshi Y (2012) Biological apatite (BAp) crystallographic orientation and texture as a new index for assessing the microstructure and function of bone regenerated by tissue engineering. Bone 51:741–747CrossRefPubMedGoogle Scholar
  14. 14.
    Huebner JL, Bay-Jensen AC, Huffman KM, He Y, Leeming DJ, McDaniel GE, Karsdal MA, Kraus VB (2014) Alpha C-telopeptide of type I collagen is associated with subchondral bone turnover and predicts progression of joint space narrowing and osteophytes in osteoarthritis. Arthritis Rheum 66:2440–2449CrossRefGoogle Scholar
  15. 15.
    Yusup A, Kaneko H, Liu L, Ning L, Sadatsuki R, Hada S, Kamagata K, Kinoshita M, Futami I, Shimura Y, Tsuchiya M, Saita Y, Takazawa Y, Ikeda H, Aoki S, Kaneko K, Ishijima M (2015) Bone marrow lesions, subchondral bone cysts and subchondral bone attrition are associated with histological synovitis in patients with end-stage knee osteoarthritis: a cross-sectional study. Osteoarthritis Cartilage. doi: 10.1016/j.joca.2015.05.017 PubMedGoogle Scholar
  16. 16.
    Buckland-Wright C (2004) Subchondral bone changes in hand and knee osteoarthritis detected by radiography. Osteoarthritis Cartilage 12:S109CrossRefGoogle Scholar
  17. 17.
    Kraus VB, Feng S, Wang S, White S, Ainslie M, Graverand MP, Brett A, Eckstein F, Hunter DJ, Lane NE, Taljanovic MS, Schnitzer T, Charles HC (2013) Subchondral bone trabecular integrity predicts and changes concurrently with radiographic and magnetic resonance imaging-determined knee osteoarthritis progression. Arthritis Rheum 65:1812–1821CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Egloff C, Paul J, Pagenstert G, Vavken P, Hintermann B, Valderrabo V, Müller-Gerbl M (2014) Changes of density distribution of the subchondral bone plate after supramalleolar osteotomy for valgus ankle osteoarthritis. J Orthop Res 32:1356–1361CrossRefPubMedGoogle Scholar
  19. 19.
    Zerfass P, Lowitz T, Museyko O, Bousson V, Laouisset L, Kalender WA, Laredo JD, Engelke K (2012) An integrated segmentation and analysis approach for QCT of the knee to determine subchondral bone mineral density and texture. IEEE Trans Biomed Eng 59:2449–2458CrossRefPubMedGoogle Scholar
  20. 20.
    Arsenault AL (1988) Crystal–collagen relationships in calcified turkey leg tendons visualized by selected-area dark field electron microscopy. Calcif Tissue Int 43:202–212CrossRefPubMedGoogle Scholar
  21. 21.
    Kikuchi M, Itoh S, Ichinose S, Shinoyama K, Tanaka J (2001) Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 22:1705–1711CrossRefPubMedGoogle Scholar
  22. 22.
    Kellgren JH, Lawrence JS (1957) Radiological assessment of osteoarthritis. Ann Rheum Dis 16:494–502CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Anderst WJ, Tashman S (2003) A method to estimate in vivo dynamic articular surface interaction. J Biomech 36:1291–1299CrossRefPubMedGoogle Scholar
  24. 24.
    Tanamas S, Hanna FS, Cicuttini FM, Wluka AE, Berry P, Urquhart DM (2009) Does knee malalignment increase the risk of development and progression of knee osteoarthritis? A systematic review. Arthritis Rheum 61:459–467CrossRefPubMedGoogle Scholar
  25. 25.
    Wong M, Carter DR (2003) Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33:1–13CrossRefPubMedGoogle Scholar
  26. 26.
    Wu JZ, Herzog W, Epstein M (2000) Joint contact mechanics in the early stages of osteoarthritis. Med Eng Phys 22:1–12CrossRefPubMedGoogle Scholar
  27. 27.
    Oegema TR, Carpenter RJ, Hofmeister F, Thompson RC (1997) The interaction of the zone of calcified cartilage and subchondral bone in osteoarthritis. Microsc Res Tech 37:324–332CrossRefPubMedGoogle Scholar
  28. 28.
    Chiba K, Nango N, Kubota S, Okazaki N, Taguchi K, Osaki M, Ito M (2012) Relationship between microstructure and degree of mineralization in subchondral bone of osteoarthritis: a synchrotron radiation μCT study. J Bone Miner Res 27:1511–1517CrossRefPubMedGoogle Scholar
  29. 29.
    Chappard C, Peyrin F, Bonnassie A, Lemineur G, Brunet-lmbault B, Lespessailles E, Benhamou C-L (2006) Subchondral bone micro-architectural alterations in osteoarthritis: a synchrotron micro-computed tomography study. Osteoarthritis Cartilage 14:215–223CrossRefPubMedGoogle Scholar
  30. 30.
    Burr DB (2012) Bone remodeling in osteoarthritis. Nat Rev Rheumatol 8:665–673CrossRefPubMedGoogle Scholar
  31. 31.
    Doré D, Quinn S, Ding C, Winzenberg T, Cicuttini F, Jones G (2010) Subchondral bone and cartilage damage: a prospective study in older adults. Arthritis Rheum 62:1967–1973CrossRefPubMedGoogle Scholar
  32. 32.
    Arden NK, Griffiths GO, Hart DJ, Doyle DV, Spector TD (1996) The association between osteoarthritis and osteoporotic fracture: the Chingford study. Br J Rheumatol 35:1299–1304CrossRefPubMedGoogle Scholar
  33. 33.
    Hannan MT, Anderson JJ, Zhang Y, Levy D, Felson DT (1993) Bone mineral density and knee osteoarthritis in elderly men and women. The Framingham Study. Arthritis Rheum 36:1671–1680CrossRefPubMedGoogle Scholar
  34. 34.
    Bacon GE, Goodship AE (1991) The orientation of the mineral crystals in the radius and tibia of the sheep, and its variation with age. J Anat 179:15–22PubMedPubMedCentralGoogle Scholar
  35. 35.
    Sasaki N, Sudoh Y (1997) X-ray pole figure analysis of apatite crystals and collagen molecules in bone. Calcif Tissue Int 60:361–367CrossRefPubMedGoogle Scholar
  36. 36.
    Ishimoto T, Nakano T, Umakoshi Y, Yamamoto M, Tabata Y (2006) Role of stress distribution on healing process of preferential alignment of biological apatite in long bone. Mat Sci Forum 512:261–264CrossRefGoogle Scholar
  37. 37.
    Kashii M, Hashimoto J, Nakano T, Umakoshi Y, Yoshikawa H (2008) Alendronate treatment promotes bone formation with a less anisotropic microstructure during intramembranous ossification in rats. J Bone Miner Metab 26:24–33CrossRefPubMedGoogle Scholar
  38. 38.
    Zizak I, Roschger P, Paris O, Misof BM, Berzlanovich A, Bernstorff S, Amenitsch H, Klaushofer K, Fratzl P (2003) Characteristics of mineral particles in the human bone/cartilage interface. J Struct Biol 141:208–217CrossRefPubMedGoogle Scholar
  39. 39.
    Neogi T, Felson D, Niu J, Lynch J, Nevitt M, Guermazi A, Roemer F, Lewis CE, Wallace B, Zhang Y (2009) Cartilage loss occurs in the same subregions as subchondral bone attrition: a within-knee subregion-matched approach from the Multicenter Osteoarthritis Study. Ann Rheum Dis 61:1539–1544Google Scholar
  40. 40.
    Radin EL, Rose RM (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 213:34–40Google Scholar
  41. 41.
    Holzer N, Salvo D, Marijnissen ACA, Vincken KL, Ahmad AC, Serra E, Hoffmeyer P, Stern R, Lübbeke A, Assal M (2015) Radiographic evaluation of posttraumatic osteoarthritis of the ankle: the Kellgren–Lawrence scale is reliable and correlates with clinical symptoms. Osteoarthritis Cartilage 23:363–369CrossRefPubMedGoogle Scholar
  42. 42.
    Wong AKO, Beattie KA, Emond PD, Inglis D, Duryea J, Doan A, Ioannidis G, Webber CE, O’Neill J, de Beer J, Adachi JD, Papaioannou A (2009) Quantitative analysis of subchondral sclerosis of the tibia by bone texture parameters in knee radiographs: site-specific relationships with joint space width. Osteoarthritis Cartilage 17:1453–1460CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Shiraishi A, Miyabe S, Nakano T, Umakoshi Y, Ito M, Mihara M (2009) The combination therapy with alfacalcidol and risedronate improves the mechanical property in lumbar spine by affecting the material properties in an ovariectomized rat model of osteoporosis. BMC Musculoskelet Disord 10:66CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Japanese Society for Bone and Mineral Research and Springer Japan 2016

Authors and Affiliations

  • Jee-Wook Lee
    • 1
  • Akio Kobayashi
    • 2
  • Takayoshi Nakano
    • 3
    Email author
  1. 1.School of Advanced Materials EngineeringKookmin UniversitySeoulKorea
  2. 2.Department of Orthopaedic SurgeryOsaka City University, Graduate School of MedicineOsakaJapan
  3. 3.Division of Materials and Manufacturing Science, Graduate School of EngineeringOsaka UniversitySuitaJapan

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