Comparative evaluation of bone microstructure in alveolar cleft repair by cone beam CT: influence of different autologous donor sites and additional application of β-tricalcium phosphate

  • Kazuaki Miyagawa
  • Susumu TanakaEmail author
  • Sachie Hiroishi
  • Yutaka Matsushita
  • Shumei Murakami
  • Mikihiko Kogo
Original Article



This study used cone beam computed tomography (CBCT) images to comparatively evaluate the three-dimensional microstructural features of reconstructed bone bridge based on the bone harvesting site and the presence/absence of artificial bone material, as well as the features of regenerated bone tissue after bone harvesting from mandibular symphysis in secondary alveolar bone grafting (SABG) for patients with cleft lip, with or without cleft palate.

Materials and methods

Thirty-one patients were divided into three groups in which SABG was performed by autologous bone harvesting from iliac crest (IC), mandibular symphysis (MS), or MS combined with β-TCP granules (MS+TCP). The microstructural trabecular bone parameters (TBPs) and bone structure indexes (SIs) were analyzed using datasets of CBCT images taken before and after SABG.


TBPs showed differences between IC and MS groups (P < 0.05), resulting in greater values of bone volume density (P < 0.05) and inferior value of TBPf (P = 0.070) in IC group compared with MS group. Using MS+TCP or filling β-TCP granules into donor site significantly improved reconstructed or regenerated BV/TV and Tb.Th (P < 0.05) compared with group without β-TCP.


Microstructural characteristics of reconstructed bone bridge were dependent on the donor site of bone harvesting; using an absorbable bone conductive material improved bone quality and increased bone volume density.

Clinical relevance

Application of β-TCP granules as a partial alternative with autologous bone from mandibular symphysis could obtain comparable outcomes in the microstructure of bone bridge to SABG with autologous iliac crest.


Alveolar bone grafting Bone microstructure β-TCP Bone regeneration Cleft lip and palate Cone beam computed tomography 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Approval from the Institutional Review Board of the Osaka University Dental Hospital, Osaka University Graduate School of Dentistry, was obtained for this study (H26-E47). All procedures performed in studies involving human participants were in accordance with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from parents of all individual participants included in the study.


  1. 1.
    Boyne PJ, Sands NR (1972) Secondary bone grafting of residual alveolar and palatal clefts. J Oral Surg 30:87–92PubMedGoogle Scholar
  2. 2.
    Mikoya T, Inoue N, Matsuzawa Y, Totsuka Y, Kajii TS, Hirosawa T (2010) Monocortical mandibular bone grafting for reconstruction of alveolar cleft. Cleft Palate Craniofac J 47:454–468CrossRefGoogle Scholar
  3. 3.
    Enemark H, Jensen J, Bosch C (2001) Mandibular bone graft material for reconstruction of alveolar cleft defects: long-term results. Cleft Palate Craniofac J 38:155–163CrossRefGoogle Scholar
  4. 4.
    Koole R, Bosker H, van der Dussen FN (1989) Late secondary autogenous bone grafting in cleft patients comparing mandibular (ectomesenchymal) and iliac crest (mesenchymal) grafts. J Craniomaxillofac Surg 17(suppl 1):28–30CrossRefGoogle Scholar
  5. 5.
    de Ruiter A, Meijer G, Dormaar T et al (2010) Beta-TCP versus autologous bone for repair of alveolar clefts in a goat model. Cleft Palate Craniofac J 48:654–662PubMedGoogle Scholar
  6. 6.
    de Ruiter A, Janssen N, van Es R, Frank M, Meijer G, Koole R, Rosenberg T (2015) Micro-structured beta-tricalcium phosphate for repair of the alveolar cleft in cleft lip and palate patients: pilot study. Cleft Palate Craniofac J 52(3):336–340CrossRefGoogle Scholar
  7. 7.
    Murphy CM, O’Brien FJ, Little DG, Schindeler A (2013) Cell-scaffold interactions in the bone tissue engineering triad. Eur Cell Mater 26:120–132CrossRefGoogle Scholar
  8. 8.
    Janssen NG, de Ruiter AP, van Hout WMMT, van Miegem V, Gawlitta D, Groot FB, Meijer GJ, Rosenberg AJWP, Koole R (2017) Microstructured β-tricalcium phosphate putty versus autologous bone for repair of alveolar clefts in a goat model. Cleft Palate Craniofac J 54(6):699–706CrossRefGoogle Scholar
  9. 9.
    Kindelan JD, Nashed RR, Bromige MR (1997) Radiographic assessment of secondary autogenous alveolar bone grafting in cleft lip and palate patients. Cleft Palate Craniofac J 34(3):195–198CrossRefGoogle Scholar
  10. 10.
    Bergland O, Semb G, Abyholm FE (1986) Elimination of the residual alveolar cleft by secondary bone grafting and subsequent orthodontic treatment. Cleft Palate J 23:175–205PubMedGoogle Scholar
  11. 11.
    Ibrahim N, Parsa A, Hassan B, van der Stelt P, Aartman IH, Wismeijer D (2014) Accuracy of trabecular bone microstructural measurement at planned dental implant sites using cone-beam CT datasets. Clinical oral implants research 25(8):941–945CrossRefGoogle Scholar
  12. 12.
    Hsu JT, Wang SP, Huang HL, Chen YJ, Wu J, Tsai MT (2013) The assessment of trabecular bone parameters and cortical bone strength: a comparison of micro-CT and dental cone-beam CT. Journal of biomechanics 46(15):2611–2618CrossRefGoogle Scholar
  13. 13.
    Oh TS, Park JS, Choi JW, Kwon SM, Koh KS (2016) Risk factor analysis of bone resorption following secondary alveolar bone grafting using three-dimensional computed tomography. J Plast Reconstr Aesthet Surg 69(4):487–492CrossRefGoogle Scholar
  14. 14.
    Ozawa T, Omura S, Fukuyama E, Matsui Y, Torikai K, Fujita K (2007) Factors influencing secondary alveolar bone grafting in cleft lip and palate patients: Prospective analysis using CT image analyzer. Cleft Palate Craniofac J 44:286–291CrossRefGoogle Scholar
  15. 15.
    El Deeb M, Messer LB, Lehnert MW, Hebda TW, Waite DE (1982) Canine eruption into grafted bone in maxillary alveolar cleft defects. Cleft Palate J 19(1):9–16PubMedGoogle Scholar
  16. 16.
    Abyholm FE, Bergland O, Semb G (1981) Secondary bone grafting of alveolar clefts. A surgical/orthodontic treatment enabling a non-prosthodontic rehabilitation in cleft lip and palate patients. Scand J Plast Reconstr Surg 15(2):127–140CrossRefGoogle Scholar
  17. 17.
    Hahn M, Vogel M, Pompesius-Kempa M, Delling G (1992) Trabecular bone pattern factor- a new parameter for simple quantification of bone microarchitecture. Bone 13(4):327–330CrossRefGoogle Scholar
  18. 18.
    Laib A, Kumer JL, Majumdar S, Lane NE (2001) The temporal changes of trabecular architecture in ovariectomized rats assessed by MicroCT. Osteoporos Int 12(11):936–941CrossRefGoogle Scholar
  19. 19.
    Hua Y, Nackaerts O, Duyck J, Maes F, Jacobs R (2009) Bone quality assessment based on cone beam computed tomography imaging. Clin Oral Implants Res 20(8):767–771CrossRefGoogle Scholar
  20. 20.
    Bouxsein ML, Seeman E (2009) Quantifying the material and structural determinants of bone strength. Best Pract Res Clin Rheumatol 23(6):741–753CrossRefGoogle Scholar
  21. 21.
    Bouxsein ML (2008) Technology insight: noninvasive assessment of bone strength in osteoporosis. Nat Clin Pract Rheumatol 4(6):310–318CrossRefGoogle Scholar
  22. 22.
    Verna C, Melsen B, Melsen F (1999) Differences in static cortical bone remodeling parameters in human mandible and iliac crest. Bone 25(5):577–583CrossRefGoogle Scholar
  23. 23.
    von Wowern N, Melsen F (1979) Comparative bone morphometric analysis of mandibles and iliac crests. Scand J Dent Res 87:351–357Google Scholar
  24. 24.
    Podenphant J, Engel U (1987) Regional variations in histomorphometric bone dynamics from the skeleton of an osteoporotic woman. Calcif Tissue Int 40:184–188CrossRefGoogle Scholar
  25. 25.
    Davison N, Yuan H, de Bruijn JD, Barrere-de Groot F (2012) In vivo performance of microstructured calcium phosphate formulated in novel water-free carriers. Acta Biomater 8:2759–2769CrossRefGoogle Scholar
  26. 26.
    Jensen SS, Bornstein MM, Dard M, Bosshardt DD, Buser D (2009) Comparative study of biphasic calcium phosphates with different HA/TCP ratios in mandibular bone defects. A long-term histomorphometric study in minipigs. J Biomed Mater Res B Appl Biomater 90(1):171–181CrossRefGoogle Scholar
  27. 27.
    Weibull L, Widmark G, Ivanoff CJ, Borg E, Rasmusson L (2009) Morbidity after chin bone harvesting—a retrospective long-term follow-up study. Clin Implant Dent Relat Res 11(2):149e157CrossRefGoogle Scholar
  28. 28.
    Booij A, Raghoebar GM, Jansma J, Kalk WW, Vissink A (2005) Morbidity of chin bone transplants used for reconstructing alveolar defects in cleft patients. Cleft Palate Craniofac J 42:533e538CrossRefGoogle Scholar
  29. 29.
    Raghoebar GM, Meijer GJ, Smeele LE (2007) Reconstruction of defects in the oral and maxillofacial region. A review of the various options for treatment. Ned Tijdschr Tandheelkd 114(1):47–53PubMedGoogle Scholar
  30. 30.
    Al-Ani O, Nambiar P, Ha KO, Ngeow WC (2013) Safe zone for bone harvesting from the interforaminal region of the mandible. Clin Oral Implants Res 100:115–121CrossRefGoogle Scholar
  31. 31.
    de Ruiter A, Dik E, van Es R, van der Bilt A, Janssen N, Meijer G, Koole R, Rosenberg A (2014) Micro-structured calcium phosphate ceramic for donor site repair after harvesting chin bone for grafting alveolar clefts in children. J Craniomaxillofac Surg 42(5):460–468CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The 1st Department of Oral and Maxillofacial SurgeryOsaka University Graduate School of DentistryOsakaJapan
  2. 2.Department of Oral and Maxillofacial RadiologyOsaka University Graduate School of DentistryOsakaJapan

Personalised recommendations