Abstract
Objectives
To investigate the effect of diabetes on the trabecular structure of the mandible in an animal model of spontaneous diabetes mellitus.
Methods
Glucose tolerance tests were performed and the urine glucose level monitored in nine Goto–Kakizaki diabetic rats (DM group) and nine Wistar rats (control group) from their 8th to 81st weeks of life. Mandibular molar bone was resected and evaluated by peripheral quantitative computed tomography to analyze bone mineral density (BMD), cross-sectional morphology, and the bone strength index. Micro-computed tomography was performed to evaluate the three-dimensional structure of bone from the same site, including the alveolar crest level. The morphometric indices, connectivity index, and continuity index were also determined.
Results
The alveolar crest level did not significantly differ between the DM and control groups. Trabecular BMD was significantly decreased in the DM group compared with that in the control group, but there was no significant difference in the cortical BMD. Parameters indicating morphological changes and the Stress/Strain Index, an indication of bone strength, were significantly decreased in the DM group compared with those in the control group. Morphometric indices, the connectivity index, and the continuity index showed a coarser trabecular structure in the DM group than in the control group.
Conclusions
The diabetic condition has a significant effect on the mandibular trabecular structure, which may lead to deterioration in bone quality.
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References
Gunczler P, Lanes R, Paz-Martinez V, Martins R, Esaa S, Colmenares V. Decreased lumbar spine bone mass and low bone turnover in children and adolescents with insulin dependent diabetes mellitus followed longitudinally. J Pediatr Endocrinol Metab. 1998;11:413–9.
Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. Osteopenia in insulin-dependent diabetes mellitus: prevalence and aspects of pathophysiology. J Endocrinol Invest. 2000;23:295–303.
Inaba M, Okuno S, Kumeda Y, Yamakawa T, Ishimura E, Nishizawa Y. Increased incidence of vertebral fracture in older female hemodialyzed patients with type 2 diabetes mellitus. Calcif Tissue Int. 2005;76:256–60.
Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86:32–8.
Rico H, Hernandez ER, Cabranes JA, Gomez-Castresana F. Suggestion of a deficient osteoblastic function in diabetes mellitus: the possible cause of osteopenia in diabetics. Calcif Tissue Int. 1989;45:71–3.
Löe H. Periodontal disease: the six complications of diabetes mellitus. Diabetes Care. 1993;16:329–34.
Shlossman M, William C, Knowler WC, Pettitt DJ, Genco RJ, Saad MF. Type 2 diabetes mellitus and periodontal disease. J Am Dent Assoc. 1990;121:532–6.
Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol. 1991;62:123–31.
Goto Y, Kakizaki M, Masaki N. Production of spontaneous diabetic rats by repetition of selective breeding. Tohoku J Exp Med. 1976;119:85–90.
Goto Y, Kakizaki M, Toyota T, Masaki N, Kitamura A, Yagihashi S. Spontaneous diabetes produced by repeated selective breeding of normal Wistar rats. Excerpta Medica ICS. 1976;413:703–10.
Ferretti JL. Peripheral quantitative computed tomography for evaluating structural and mechanical properties of small bone. In: An YH, Draughn RA, editors. Mechanical testing of bone and the bone-implant interface. Boca Raton: CRC; 2000. p. 390–2.
RATOC System Engineering Co. TRI/3D-BON: basic operation manual. Tokyo: RATOC System Engineering; 2002.
Parfitt AM, Matthews CHE, Villanueva AR, Kleerekoper M, Frame B, Rao DS. Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. J Clin Invest. 1983;72:1396–409.
Odgaard A. Three-dimensional methods fore quantification of cancellous bone architecture. Bone. 1997;20:315–28.
Feldkamp LA, Goldstein SA, Parfitt AM, Jesion G, Kleerekoper M. The direct examination of three-dimensional bone architecture in vitro by computed tomography. J Bone Miner Res. 1989;4:3–11.
Garrahan NJ, Mellish RW, Compston JE. A new method for the two-dimensional analysis of bone structure in human iliac crest biopsies. J Microsc. 1986;142:341–9.
Croucher PI, Garrahan NJ, Compston JE. Assessment of cancellous bone structure: comparison of strut analysis, trabecular bone pattern factor, and marrow space star volume. J Bone Miner Res. 1996;11:955–61.
Ikuta A, Kumasaka S, Kashima I. Quantitative analysis using the star volume method applied to skeleton patterns extracted with a morphological filter. J Bone Miner Metab. 2000;18:271–7.
Kumasaka S, Kiyohara S, Takahashi T, Asai H, Kashima I. Morphologically extracted trabecular skeleton superimposed upon digital radiograph structure. J Bone Miner Metab. 2000;18:208–11.
Vesterby A, Gunndersen HJG, Melsen F. Star volume of marrow space and trabeculae of the first lumber vertebra: sampling efficiency and biological variation. Bone. 1989;10:7–13.
Nakamura K, Matsubara M, Asai H, Koyama A, Fujikawa T, Kashima I. Mathematical morphology for extraction of bone trabecular pattern: preliminary investigation of quantitative analysis using the star volume. J Jpn Soc Bone Morphom. 1999;9:45–51.
Albright F, Reinfenstein EC. Parathyroid glands and metabolic bone disease. In: Selected studies. Baltimore: Williams & Wilkins; 1948. p. 150.
Tuominen JT, Impivaara O, Puukka P, Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999;22:1196–200.
McNair P. Bone mineral metabolism in human type 1 (insulin dependent) diabetes mellitus. Dan Med Bull. 1988;35:109–21.
Isaia G, Bodrato L, Carlevatto V, Mussetta M, Salamano G, Molinatti GM. Osteoporosis in type II diabetes. Acta Diabetol Lat. 1987;24:305–10.
Gregorio F, Cristallini S, Santeusanio F, Filipponi P, Fumelli P. Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract. 1994;23:43–54.
Kwon DJ, Kim JH, Chung KW, Kim JH, Lee JW, Kim SP. Bone mineral density of the spine using dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. J Obstet Gynaecol Res. 1996;22:157–62.
Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T. Bone mineral density measured by dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. Bone. 1993;14:29–33.
Sosa M, Dominguez M, Navarro MC, Segarra MC, Hernández D, de Pablos P. Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complicat. 1996;10:201–5.
Van Daele PL, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A. Bone density in non-insulin-dependent diabetes mellitus: the Rotterdam study. Ann Intern Med. 1995;122:409–14.
Rishaug U, Birkeland KI, Falch JA, Vaaler S. Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest. 1995;55:257–62.
Stolk RP, Van Daele PL, Pols HA, Burger H, Hofman A, Birkenhäger JC. Hyperinsulinemia and bone mineral density in an elderly population: the Rotterdam study. Bone. 1996;18:545–9.
Anderson BG, Smith AH, Arnim SS, Orten A. Changes in molar teeth and their supporting structures of rats following extraction on the upper right first and second molars. Yale J Biol Med. 1936;9:189–93.
Cimasoni G, Becks H. Growth study of the rat mandible as related to function. Angle Orthod. 1963;33:27–34.
Taguchi A, Tanimoto K, Suei Y, Otani K, Wada T. Oral signs as indicators of possible osteoporosis in elderly women. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1995;80:612–6.
Bollen AM, Taguchi A, Hujoel PP, Hollender LG. Case-control study on self- reported osteoporotic fractures and mandibular cortical bone. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000;90:518–24.
Jowitt N, MacFalkane T, Devlin H, Klemetti E, Horner K. The reproducibility of the mandibular cortical index. Dentomaxillofac Radiol. 1999;28:141–4.
Asai H, Kozai Y, Matsumoto Y, Kawamata R, Kumasaka S, Kashima I. Radiological morphometric analysis of the mandibular bone structure after ovariectomy in mature cynomolgus monkeys. Oral Sci Int. 2005;2:54–63.
NIH Consensus Development Panel. Osteoporosis prevention, diagnosis, and therapy. JAMA. 2001;285:785–95.
Shimamoto M, Kozai Y, Matsumoto Y, Kawamata R, Sakurai T, Kashima I. Radiological morphometric analysis for the trabecular bone structure of mandibular condyle after ovariectomy in mature cynomolgus monkeys. Oral Sci Int. 2007;4:86–96.
Nicodemus KK, Folsom AR. Iowa Women’s Health Study. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24:1192–7.
Brown SA, Sharpless JL. Osteoporosis: an under-appreciated complication of diabetes. Clin Diabetes. 2004;22:10–20.
Heath H 3rd, Melton LJ 3rd, Chu CP. Diabetes mellitus and risk of skeletal fracture. N Engl J Med. 1980;303:567.
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Onoyama, K., Kawamata, R., Kozai, Y. et al. Comparison of mandibular trabecular structures between normal and diabetic rats: evaluation of spontaneous type 2 diabetes in a rat model. Oral Radiol 27, 35–42 (2011). https://doi.org/10.1007/s11282-011-0065-x
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DOI: https://doi.org/10.1007/s11282-011-0065-x