Abstract
Estrogen deficiency-induced postmenopausal osteoporosis has become a worldwide problem, inducing low bone mass and microarchitectural deterioration of the bone scaffolding in the vertebrae and long bones. With the prevalence of such osteoporosis on the increase, the influence of this estrogen deficiency on the jaw bones has drawn the attention of researchers and clinicians in the field of dentistry. The aim of this article is therefore to review the microstructural changes occurring after ovariectomy in the jaw bones of animal subjects. Induced estrogen deficiency clearly led to structural changes in the jaw bones and alveolar bone of animal subjects (rats and monkeys). Severe bone loss in the rat alveolar bone was principally caused by high bone resorptive activity. This activity accelerated greatly immediately after ovariectomy, and was then followed by more moderate resorptive activity, which continued over an extended period. Additionally, occlusal hypofunction further greatly accelerated the fragility of the alveolar bone structure in ovariectomized rats. Microstructural damage also seen in the alveolar bone of ovariectomized monkeys was found to be directly connected to their systemic osteoporosis. Recent investigations of the relationship in humans between systemic osteoporosis and jaw bone loss have also suggested that a connection may exist between these two. However, more research is required to confirm this connection in humans as well.
Similar content being viewed by others
References
Johnell O, Kanis, JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733
Reginster JY, Burlet N (2006) Osteoporosis: a still increasing prevalence. Bone (NY) 38:S4–S9
Dervis E (2005) Oral implications of osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 100:349–356
Lerner UH (2006) Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis. J Dent Res 85:596–607
Krall EA, Garcia RI, Dawson-Hughes B (1996) Increased risk of tooth loss is related to bone loss at the whole body, hip, and spine. Calcif Tissue Int 59:433–437
Taguchi A, Suei Y, Ohtsuka M, Otani K, Tanimoto K, Hollender LG (1999) Relationship between bone mineral density and tooth loss in elderly Japanese women. Dentomaxillofac Radiol 28: 219–223
Inagaki K, Kurosu Y, Yoshinari N, Noguchi T, Krall EA, Garcia RI (2005) Efficacy of periodontal disease and tooth loss to screen for low bone mineral density in Japanese women. Calcif Tissue Int 77:9–14
Yoshihara A, Seida Y, Hanada N, Nakashima K, Miyazaki H (2005) The relationship between bone mineral density and the number of remaining teeth in community-dwelling older adults. J Oral Rehabil 32:735–740
Kribbs PJ (1990) Comparison of mandibular bone in normal and osteoporotic women. J Prosthet Dent 63:218–222
Kribbs PJ, Chesnut CH III, Ott SM, Kilcoyne RF (1989) Relationships between mandibular and skeletal bone in an osteoporotic population. J Prosthet Dent 62:703–707
Horner K, Devlin H, Alsop CW, Hodgkinson IM, Adams JE (1996) Mandibular bone mineral density as a predictor of skeletal osteoporosis. Br J Radiol 69:1019–1025
Jeffcoat MK (1998) Osteoporosis: a possible modifying factor in oral bone loss. Ann Periodontol 3:312–321
Lee BD, White SC (2005) Age and trabecular features of alveolar bone associated with osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 100:92–98
Takaishi Y, Okamoto Y, Ikeo T, Morii H, Takeda M, Hide K, Arai T, Nonaka K (2005) Correlations between periodontitis and loss of mandibular bone in relation to systemic bone changes in postmenopausal Japanese women. Osteoporos Int 16:1875–1882
Devlin H, Horner K (2002) Mandibular radiomorphometric indices in the diagnosis of reduced skeletal bone mineral density. Osteoporos Int 13:373–378
Nakamoto T, Taguchi A, Ohtsuka M, Suei Y, Fujita M, Tanimoto K, Tsuda M, Sanada M, Ohama K, Takahashi J, Rohlin M (2003) Dental panoramic radiograph as a tool to detect postmenopausal women with low bone mineral density: untrained general dental practitioners’ diagnostic performance. Osteoporos Int 14:659–664
Taguchi A, Suei Y, Sanada M, Ohtsuka M, Nakamoto T, Sumida H, Ohama K, Tanimoto K (2004) Validation of dental panoramic radiography measures for identifying postmenopausal women with spinal osteoporosis. AJR Am J Roentgenol 183:1755–1760
Halling A, Persson GR, Berglund J, Johansson O, Renvert S (2005) Comparison between the Klemetti index and heel DXA BMD measurements in the diagnosis of reduced skeletal bone mineral density in the elderly. Osteoporos Int 16:999–1003
White SC, Taguchi A, Kao D, Wu S, Service SK, Yoon D, Suei Y, Nakamoto T, Tanimoto K (2005) Clinical and panoramic predictors of femur bone mineral density. Osteoporos Int 16:339–346
von Wowern N, Kollerup G (1992) Symptomatic osteoporosis: a risk factor for residual ridge reduction of the jaws. J Prosthet Dent 67:656–660
Hirai T, Ishijima T, Hashikawa Y, Yajima T (1993) Osteoporosis and reduction of residual ridge in edentulous patients. J Prosthet Dent 69:49–56
Jonasson G, Kiliaridis S (2005) Changes in the bucco-lingual thickness of the mandibular alveolar process and skeletal bone mineral density in dentate women: a 5-yr prospective study. Eur J Oral Sci 113:114–120
Yamada M, Ito M, Hayashi K, Sato H, Nakamura T (1997) Mandibular condyle bone mineral density measurement by quantitative computed tomography: a gender-related difference in correlation to spinal bone mineral density. Bone (NY) 21:441–445
Irie K, Sakakura Y, Tsuruga E, Hosokawa Y, Yajima T (2004) Three-dimensional changes of the mandible and alveolar bone in the ovariectomized rats examined by micro-focus computed tomography. J Jpn Soc Periodontal 46:288–293
Miller SC, Hunziker J, Mecham M, Wronski TJ (1997) Intermittent parathyroid hormone administration stimulates bone formation in the mandibles of aged ovariectomized rats. J Dent Res 76:1471–1476
Nakajima M, Ejiri S, Tanaka M, Toyooka E, Kohno S, Ozawa H (2000) Effect of intermittent administration of human parathyroid hormone (1–34) on the mandibular condyle of ovariectomized rats. J Bone Miner Metab 18:9–17
Yang J, Pham SM, Crabbe DL (2003) Effects of oestrogen deficiency on rat mandibular and tibial microarchitecture. Dentomaxillofac Radiol 32:247–251
Yang J, Farnell D, Devlin H, Horner K, Graham J (2005) The effect of ovariectomy on mandibular cortical thickness in the rat. J Dent 33:123–129
Armada L, Nogueira CR, Neves UL, dos Santos Souza P, Detogne JP, Armada-Dias L, Moreira RM, Nascimento-Saba CC (2006) Mandible analysis in sex steroid-deficient rats. Oral Dis 12:181–186
Anbinder AL, Prado FD, Prado MD, Balducci I, Rocha RF (2007) The influence of ovariectomy, simvastatin and sodium alendronate on alveolar bone in rats. Braz Oral Res 21:247–252
Tanaka M, Ejiri S, Toyooka E, Kohno S, Ozawa H (2002) Effects of ovariectomy on trabecular structures of rat alveolar bone. J Periodont Res 37:161–165
Tanaka M, Toyooka E, Kohno S, Ozawa H, Ejiri S (2003) Longterm changes in trabecular structure of aged rat alveolar bone after ovariectomy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 95:495–502
Moriya Y, Ito K, Murai S (1998) Effects of experimental osteoporosis on alveolar bone loss in rats. J Oral Sci 40:171–175
Ishihara A, Sasaki T, Debari K, Furuya R, Kawawa T, Ramamurthy NS, Golub LM (1999) Effects of ovariectomy on bone morphology in maxillae of mature rats. J Electron Microsc (Tokyo) 48:465–469
Hara T, Sato T, Oka M, Mori S, Shirai H (2001) Effects of ovariectomy and/or dietary calcium deficiency on bone dynamics in the rat hard palate, mandible and proximal tibia. Arch Oral Biol 46:443–451
Kuroda S, Mukohyama H, Kondo H, Aoki K, Ohya K, Ohyama T, Kasugai S (2003) Bone mineral density of the mandible in ovariectomized rats: analyses using dual energy X-ray absorptiometry and peripheral quantitative computed tomography. Oral Dis 9:24–28
Elovic RP, Hipp JA, Hayes WC (1995) Ovariectomy decreases the bone area fraction of the rat mandible. Calcif Tissue Int 56:305–310
Mavropoulos A, Rizzoli R, Ammann P (2007) Different responsiveness of alveolar and tibial bone to bone loss stimuli. J Bone Miner Res 22:403–410
Han ZH, Palnitkar S, Rao DS, Nelson D, Parfitt AM (1997) Effects of ethnicity and age or menopause on the remodeling and turnover of iliac bone: implications for mechanisms of bone loss. J Bone Miner Res 12:498–508
Ejiri S, Toyooka E, Tanaka M, Anwar RB, Kohno S (2006) Histological and histomorphometrical changes in rat alveolar bone following antagonistic tooth extraction and/or ovariectomy. Arch Oral Biol 51:941–950
Weinreb M, Rodan GA, Thompson DD (1989) Osteopenia in the immobilized rat hind limb is associated with increased bone resorption and decreased bone formation. Bone (NY) 10:187–194
Jee WS, Ma Y (1999) Animal models of immobilization osteopenia. Morphologie 83:25–34
Frost HM, Jee WS (1992) On the rat model of human osteopenias and osteoporoses. Bone Miner 18:227–236
Wronski TJ, Yen CF (1991) The ovariectomized rat as an animal model for postmenopausal bone loss. Cells Materials 1(suppl): 69–74
Miller LC, Weaver DS, McAlister JA, Koritni DR (1986) Effects of ovariectomy on vertebral trabecular bone in the cynomolgus monkey (Macaca fascicularis). Calcif Tissue Int 38:62–65
Thorndike EA, Turner AS (1998) In search of an animal model for postmenopausal diseases. Front Biosci 3:c17–c26
Martin RB, Butcher RL, Sherwood LL, Buckendahl P, Boyd RD, Farris D, Sharkey N, Dannucci G (1987) Effects of ovariectomy in beagle dogs. Bone (NY) 8:23–31
Anwar RB, Tanaka M, Kohno S, Ikegame M, Watanabe N, Nowazesh Ali M, Ejiri S (2007) Relationship between porotic changes in alveolar bone and spinal osteoporosis. J Dent Res 86:52–57
Taguchi A, Sanada M, Krall E, Nakamoto T, Ohtsuka M, Suei Y, Tanimoto K, Kodama I, Tsuda M, Ohama K (2003) Relationship between dental panoramic radiographic findings and biochemical markers of bone turnover. J Bone Miner Res 18:1689–1694
Bollen AM, Taguchi A, Hujoel PP, Hollender LG (2000) Casecontrol study on self-reported osteoporotic fractures and mandibular cortical bone. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 90:518–524
Taguchi A, Suei Y, Ohtsuka M, Otani K, Tanimoto K, Ohtaki M (1996) Usefulness of panoramic radiography in the diagnosis of postmenopausal osteoporosis in women. Width and morphology of inferior cortex of the mandible. Dentomaxillofac Radiol 25:263–267
Klemetti E, Kolmakov S, Kroger H (1994) Pantomography in assessment of the osteoporosis risk group. Scand J Dent Res 102: 68–72
Bassi F, Procchio M, Fava C, Schierano G, Preti G (1999) Bone density in human dentate and edentulous mandibles using computed tomography. Clin Oral Implants Res 10:356–361
Klemetti E, Vainio P, Lassila V, Alhava E (1993) Cortical bone mineral density in the mandible and osteoporosis status in postmenopausal women. Scand J Dent Res 101:219–223
Horner K, Devlin H (1998) The relationships between two indices of mandibular bone quality and bone mineral density measured by dual energy X-ray absorptiometry. Dentomaxillofac Radiol 27:17–21
von Wowern N, Storm TL, Olgaard K (1988) Bone mineral content by photon absorptiometry of the mandible compared with that of the forearm and the lumbar spine. Calcif Tissue Int 42:157–161
Payne JB, Reinhardt RA, Nummikoski PV, Patil KD (1999) Longitudinal alveolar bone loss in postmenopausal osteoporotic/osteopenic women. Osteoporos Int 10:34–40
Kribbs PJ, Smith DE, Chesnut CH III (1983) Oral findings in osteoporosis. Part I: Measurement of mandibular bone density. J Prosthet Dent 50:576–579
Karayianni K, Horner K, Mitsea A, Berkas L, Mastoris M, Jacobs R, Lindh C, van der Stelt PF, Harrison E, Adams JE, Pavitt S, Devlin H (2007) Accuracy in osteoporosis diagnosis of a combination of mandibular cortical width measurement on dental panoramic radiographs and a clinical risk index (OSIRIS): the OSTEODENT project. Bone (NY) 40:223–229
Taguchi A, Ohtsuka M, Tsuda M, Nakamoto T, Kodama I, Inagaki K, Noguchi T, Kudo Y, Suei Y, Tanimoto K (2007) Risk of vertebral osteoporosis in post-menopausal women with alterations of the mandible. Dentomaxillofac Radiol 36:143–148
Taguchi A, Tsuda M, Ohtsuka M, Kodama I, Sanada M, Nakamoto T, Inagaki K, Noguchi T, Kudo Y, Suei Y, Tanimoto K, Bollen AM (2006) Use of dental panoramic radiographs in identifying younger postmenopausal women with osteoporosis. Osteoporos Int 17:387–394
Lee K, Taguchi A, Ishii K, Suei Y, Fujita M, Nakamoto T, Ohtsuka M, Sanada M, Tsuda M, Ohama K, Tanimoto K, White SC (2005) Visual assessment of the mandibular cortex on panoramic radiographs to identify postmenopausal women with low bone mineral densities. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 100:226–231
Horner K, Devlin H, Harvey L (2002) Detecting patients with low skeletal bone mass. J Dent 30:171–175
Author information
Authors and Affiliations
Corresponding author
Additional information
S. Ejiri is a recipient of JSBMR Academic Award 2004
About this article
Cite this article
Ejiri, S., Tanaka, M., Watanabe, N. et al. Estrogen deficiency and its effect on the jaw bones. J Bone Miner Metab 26, 409–415 (2008). https://doi.org/10.1007/s00774-008-0870-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00774-008-0870-4