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

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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.

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References

  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 201–212

    Book  Google Scholar 

  2. Fleisch H (2000) Bisphosphonates in bone disease, vol 4. Academic Press, Massachusetts, pp 1–26

    Book  Google Scholar 

  3. Jackson SA, Cartwright AG, Lewis D (1978) The morphology of bone mineral crystals. Calcif Tissue Res 25:217–222

    Article  CAS  PubMed  Google Scholar 

  4. Elliott JC, Wilson RM, Dowker SEP (2002) Apatite structures. Adv X-Ray Anal 45:172–181

    CAS  Google Scholar 

  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 B43:171–174

    Article  Google Scholar 

  6. Katz J, Ukraincik K (1971) On the anisotropic elastic properties of hydroxyapatite. J Biomech 4:221–227

    Article  CAS  PubMed  Google Scholar 

  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 31:479–487

    Article  CAS  PubMed  Google Scholar 

  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 37:134–143

    Article  CAS  PubMed  Google Scholar 

  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 28:1170–1179

    Article  CAS  PubMed  Google Scholar 

  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 52:659–667

    Article  CAS  PubMed  Google Scholar 

  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 512:255–260

    Article  CAS  Google Scholar 

  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 48:337–342

    Article  CAS  Google Scholar 

  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 51:741–747

    Article  PubMed  Google Scholar 

  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 66:2440–2449

    Article  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  16. Buckland-Wright C (2004) Subchondral bone changes in hand and knee osteoarthritis detected by radiography. Osteoarthritis Cartilage 12:S109

    Article  Google Scholar 

  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 65:1812–1821

    Article  PubMed  PubMed Central  Google Scholar 

  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 32:1356–1361

    Article  PubMed  Google Scholar 

  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 59:2449–2458

    Article  CAS  PubMed  Google Scholar 

  20. Arsenault AL (1988) Crystal–collagen relationships in calcified turkey leg tendons visualized by selected-area dark field electron microscopy. Calcif Tissue Int 43:202–212

    Article  CAS  PubMed  Google Scholar 

  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 22:1705–1711

    Article  CAS  PubMed  Google Scholar 

  22. Kellgren JH, Lawrence JS (1957) Radiological assessment of osteoarthritis. Ann Rheum Dis 16:494–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Anderst WJ, Tashman S (2003) A method to estimate in vivo dynamic articular surface interaction. J Biomech 36:1291–1299

    Article  PubMed  Google Scholar 

  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 61:459–467

    Article  PubMed  Google Scholar 

  25. Wong M, Carter DR (2003) Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33:1–13

    Article  CAS  PubMed  Google Scholar 

  26. Wu JZ, Herzog W, Epstein M (2000) Joint contact mechanics in the early stages of osteoarthritis. Med Eng Phys 22:1–12

    Article  CAS  PubMed  Google Scholar 

  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 37:324–332

    Article  PubMed  Google Scholar 

  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 27:1511–1517

    Article  PubMed  Google Scholar 

  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 14:215–223

    Article  CAS  PubMed  Google Scholar 

  30. Burr DB (2012) Bone remodeling in osteoarthritis. Nat Rev Rheumatol 8:665–673

    Article  CAS  PubMed  Google Scholar 

  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 62:1967–1973

    Article  PubMed  Google Scholar 

  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 35:1299–1304

    Article  CAS  PubMed  Google Scholar 

  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 36:1671–1680

    Article  CAS  PubMed  Google Scholar 

  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 179:15–22

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Sasaki N, Sudoh Y (1997) X-ray pole figure analysis of apatite crystals and collagen molecules in bone. Calcif Tissue Int 60:361–367

    Article  CAS  PubMed  Google Scholar 

  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 512:261–264

    Article  Google Scholar 

  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 26:24–33

    Article  CAS  PubMed  Google Scholar 

  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 141:208–217

    Article  CAS  PubMed  Google Scholar 

  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 61:1539–1544

    CAS  Google Scholar 

  40. Radin EL, Rose RM (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 213:34–40

    Google Scholar 

  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 23:363–369

    Article  CAS  PubMed  Google Scholar 

  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 17:1453–1460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 10:66

    Article  PubMed  PubMed Central  Google Scholar 

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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).

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Authors and Affiliations

  1. School of Advanced Materials Engineering, Kookmin University, Seoul, 136-702, Korea

    Jee-Wook Lee

  2. Department of Orthopaedic Surgery, Osaka City University, Graduate School of Medicine, Osaka, 545-8585, Japan

    Akio Kobayashi

  3. Division of Materials and Manufacturing Science, Graduate School of Engineering, Osaka University, Suita, 565-0871, Japan

    Takayoshi Nakano

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Correspondence to Takayoshi Nakano.

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Lee, JW., Kobayashi, A. & Nakano, T. Crystallographic orientation of the c-axis of biological apatite as a new index of the quality of subchondral bone in knee joint osteoarthritis. J Bone Miner Metab 35, 308–314 (2017). https://doi.org/10.1007/s00774-016-0754-y

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  • DOI: https://doi.org/10.1007/s00774-016-0754-y

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