Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 635023, 12 pages
http://dx.doi.org/10.1155/2015/635023
Review Article

The Ovariectomized Rat as a Model for Studying Alveolar Bone Loss in Postmenopausal Women

1Faculty of Applied Health Sciences, Brock University, St. Catharines, ON, Canada L2S 3A1
2Centre for Bone and Muscle Health, Brock University, St. Catharines, ON, Canada L2S 3A1

Received 7 October 2014; Accepted 2 March 2015

Academic Editor: Andrea Vecchione

Copyright © 2015 Bryan D. Johnston and Wendy E. Ward. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. K. Väänänen and P. L. Härkönen, “Estrogen and bone metabolism,” Maturitas, vol. 23, pp. S65–S69, 1996. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Pacifici, “Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis,” Journal of Bone and Mineral Research, vol. 11, no. 8, pp. 1043–1051, 1996. View at Google Scholar · View at Scopus
  3. O. Johnell and J. A. Kanis, “An estimate of the worldwide prevalence and disability associated with osteoporotic fractures,” Osteoporosis International, vol. 17, no. 12, pp. 1726–1733, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Odén, E. V. McCloskey, H. Johansson, and J. A. Kanis, “Assessing the impact of osteoporosis on the burden of hip fractures,” Calcified Tissue International, vol. 92, no. 1, pp. 42–49, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. N. C. Wright, A. C. Looker, K. G. Saag et al., “The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine,” Journal of Bone and Mineral Research, vol. 29, no. 11, pp. 2520–2526, 2014. View at Publisher · View at Google Scholar
  6. B. L. Riggs, S. Khosla, and L. J. Melton III, “A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men,” Journal of Bone and Mineral Research, vol. 13, no. 5, pp. 763–773, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. J. A. Cauley, N. S. Wampler, J. M. Barnhart et al., “Incidence of fractures compared to cardiovascular disease and breast cancer: the Women's Health Initiative Observational Study,” Osteoporosis International, vol. 19, no. 12, pp. 1717–1723, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. O. Johnell and J. Kanis, “Epidemiology of osteoporotic fractures,” Osteoporosis International, vol. 16, no. 2, pp. S3–S7, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. O. Johnell, J. A. Kanis, A. Odén et al., “Mortality after osteoporotic fractures,” Osteoporosis International, vol. 15, no. 1, pp. 38–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Darcey, K. Horner, T. Walsh, H. Southern, E. J. Marjanovic, and H. Devlin, “Tooth loss and osteoporosis: to assess the association between osteoporosis status and tooth number,” British Dental Journal, vol. 214, no. 4, pp. 1–10, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Iwasaki, K. Nakamura, A. Yoshihara, and H. Miyazaki, “Change in bone mineral density and tooth loss in Japanese community-dwelling postmenopausal women: a 5-year cohort study,” Journal of Bone and Mineral Metabolism, vol. 30, no. 4, pp. 447–453, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. E. A. Krall, R. I. Garcia, and B. Dawson-Hughes, “Increased risk of tooth loss is related to bone loss at the whole body, hip, and spine,” Calcified Tissue International, vol. 59, no. 6, pp. 433–437, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. J. B. Payne, R. A. Reinhardt, P. V. Nummikoski, and K. D. Patil, “Longitudinal alveolar bone loss in postmenopausal osteoporotic/osteopenic women,” Osteoporosis International, vol. 10, no. 1, pp. 34–40, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Sheiham, J. G. Steele, W. Marcenes et al., “The relationship among dental status, nutrient intake, and nutritional status in older people,” Journal of Dental Research, vol. 80, no. 2, pp. 408–413, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. R. B. Ervin and B. A. Dye, “The effect of functional dentition on healthy eating index scores and nutrient intakes in a nationally representative sample of older adults,” Journal of Public Health Dentistry, vol. 69, no. 4, pp. 207–216, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. N. R. Sahyoun, C.-L. Lin, and E. Krall, “Nutritional status of the older adult is associated with dentition status,” Journal of the American Dietetic Association, vol. 103, no. 1, pp. 61–66, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. D. S. Brennan, K. A. Singh, P. Liu, and A. J. Spencer, “Fruit and vegetable consumption among older adults by tooth loss and socio-economic status,” Australian Dental Journal, vol. 55, no. 2, pp. 143–149, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Cauley, J. Robbins, Z. Chen et al., “Effects of estrogen plus progestin on risk of fracture and bone mineral density: the Women's Health Initiative randomized trial,” Journal of the American Medical Association, vol. 290, no. 13, pp. 1729–1738, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. R. D. Jackson, J. Wactawski-Wende, A. Z. LaCroix et al., “Effects of conjugated equine estrogen on risk of fractures and BMD in postmenopausal women with hysterectomy: results from the women's health initiative randomized trial,” Journal of Bone and Mineral Research, vol. 21, no. 6, pp. 817–828, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Grodstein, G. A. Colditz, and M. J. Stampfer, “Post-menopausal hormone use and tooth loss: a prospective study,” Journal of the American Dental Association, vol. 127, no. 3, pp. 370–377, 1996. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Paganini-Hill, “The benefits of estrogen replacement therapy on oral health: the leisure world cohort,” Archives of Internal Medicine, vol. 155, no. 21, pp. 2325–2329, 1995. View at Publisher · View at Google Scholar · View at Scopus
  22. E. A. Krall, B. Dawson-Hughes, M. T. Hannan, P. W. F. Wilson, and D. P. Kiel, “Postmenopausal estrogen replacement and tooth retention,” The American Journal of Medicine, vol. 102, no. 6, pp. 536–542, 1997. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Taguchi, M. Sanada, Y. Suei et al., “Effect of estrogen use on tooth retention, oral bone height, and oral bone porosity in Japanese postmenopausal women,” Menopause, vol. 11, no. 5, pp. 556–562, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Civitelli, T. K. Pilgram, M. Dotson et al., “Alveolar and postcranial bone density in postmenopausal women receiving hormone/estrogen replacement therapy: a randomized, double-blind, placebo-controlled trial,” Archives of Internal Medicine, vol. 162, no. 12, pp. 1409–1415, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. A. C. Ross, J. E. Manson, S. A. Abrams et al., “The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know,” The Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 1, pp. 53–58, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Boeing, A. Bechthold, A. Bub et al., “Critical review: vegetables and fruit in the prevention of chronic diseases,” European Journal of Nutrition, vol. 51, no. 6, pp. 637–663, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. Y.-M. Chen, S. C. Ho, and J. L. F. Woo, “Greater fruit and vegetable intake is associated with increased bone mass among postmenopausal Chinese women,” British Journal of Nutrition, vol. 96, no. 4, pp. 745–751, 2006. View at Google Scholar · View at Scopus
  28. D. D. Thompson, H. A. Simmons, C. M. Pirie, and H. Z. Ke, “FDA guidelines and animal models for osteoporosis,” Bone, vol. 17, no. 4, supplement, pp. 125S–133S, 1995. View at Google Scholar · View at Scopus
  29. C. H. Turner, R. K. Roeder, A. Wieczorek, T. Foroud, G. Liu, and M. Peacock, “Variability in skeletal mass, structure, and biomechanical properties among inbred strains of rats,” Journal of Bone and Mineral Research, vol. 16, no. 8, pp. 1532–1539, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Sengupta, M. Arshad, S. Sharma, M. Dubey, and M. M. Singh, “Attainment of peak bone mass and bone turnover rate in relation to estrous cycle, pregnancy and lactation in colony-bred Sprague-Dawley rats: suitability for studies on pathophysiology of bone and therapeutic measures for its management,” Journal of Steroid Biochemistry and Molecular Biology, vol. 94, no. 5, pp. 421–429, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. P. P. Lelovas, T. T. Xanthos, S. E. Thorma, G. P. Lyritis, and I. A. Dontas, “The laboratory rat as an animal model for osteoporosis research,” Comparative Medicine, vol. 58, no. 5, pp. 424–430, 2008. View at Google Scholar · View at Scopus
  32. M. M. Leitner, A. E. Tami, P. M. Montavon, and K. Ito, “Longitudinal as well as age-matched assessments of bone changes in the mature ovariectomized rat model,” Laboratory Animals, vol. 43, no. 3, pp. 266–271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. W. S. Jee and W. Yao, “Overview: animal models of osteopenia and osteoporosis,” Journal of Musculoskeletal & Neuronal Interactions, vol. 1, no. 3, pp. 193–207, 2001. View at Google Scholar
  34. D. N. Kalu, “The ovariectomized rat model of postmenopausal bone loss,” Bone and Mineral, vol. 15, no. 3, pp. 175–191, 1991. View at Publisher · View at Google Scholar · View at Scopus
  35. T. J. Wronski, M. Cintron, and L. M. Dann, “Temporal relationship between bone loss and increased bone turnover in ovariectomized rats,” Calcified Tissue International, vol. 43, no. 3, pp. 179–183, 1988. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Li, Y. Shen, and T. J. Wronski, “Time course of femoral neck osteopenia in ovariectomized rats,” Bone, vol. 20, no. 1, pp. 55–61, 1997. View at Google Scholar
  37. T. J. Wronski, L. M. Dann, and S. L. Horner, “Time course of vertebral osteopenia in ovariectomized rats,” Bone, vol. 10, no. 4, pp. 295–301, 1989. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Tanaka, S. Ejiri, E. Toyooka, S. Kohno, and H. Ozawa, “Effects of ovariectomy on trabecular structures of rat alveolar bone,” Journal of Periodontal Research, vol. 37, no. 2, pp. 161–165, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Irie, Y. Sakakura, E. Tsuruga, Y. Hosokawa, and T. Yajima, “Three-dimensional changes of the mandible and alveolar bone in the ovariectomized rat examined by micro-focus computed tomography,” Journal of the Japanese Society of Periodontology, vol. 46, no. 4, pp. 288–293, 2004. View at Publisher · View at Google Scholar
  40. M. S. Ames, S. Hong, H. R. Lee, H. W. Fields, W. M. Johnston, and D.-G. Kim, “Estrogen deficiency increases variability of tissue mineral density of alveolar bone surrounding teeth,” Archives of Oral Biology, vol. 55, no. 8, pp. 599–605, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Moriya, K. Ito, and S. Murai, “Effects of experimental osteoporosis on alveolar bone loss in rats,” Journal of oral Science, vol. 40, no. 4, pp. 171–175, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. R. P. Elovic, J. A. Hipp, and W. C. Hayes, “Maxillary molar extraction decreases stiffness of the mandible in ovariectomized rats,” Journal of Dental Research, vol. 73, no. 11, pp. 1735–1741, 1994. View at Google Scholar · View at Scopus
  43. I. M. F. Patullo, L. Takayama, R. F. Patullo, V. Jorgetti, and R. M. R. Pereira, “Influence of ovariectomy and masticatory hypofunction on mandibular bone remodeling,” Oral Diseases, vol. 15, no. 8, pp. 580–586, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Hara, T. Sato, M. Oka, S. Mori, and H. Shirai, “Effects of ovariectomy and/or dietary calcium deficiency on bone dynamics in the rat hard palate, mandible and proximal tibia,” Archives of Oral Biology, vol. 46, no. 5, pp. 443–451, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Yang, S. M. Pham, and D. L. Crabbe, “Effects of oestrogen deficiency on rat mandibular and tibial microarchitecture,” Dentomaxillofacial Radiology, vol. 32, no. 4, pp. 247–251, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Mavropoulos, R. Rizzoli, and P. Ammann, “Different responsiveness of alveolar and tibial bone to bone loss stimuli,” Journal of Bone and Mineral Research, vol. 22, no. 3, pp. 403–410, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. R. P. Elovic, J. A. Hipp, and W. C. Hayes, “Ovariectomy decreases the bone area fraction of the rat mandible,” Calcified Tissue International, vol. 56, no. 4, pp. 305–310, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Tanaka, E. Toyooka, S. Kohno, H. Ozawa, and S. Ejiri, “Long-term changes in trabecular structure of aged rat alveolar bone after ovariectomy,” Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, vol. 95, no. 4, pp. 495–502, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Jiang, H. Matsumoto, and A. Fujii, “Mandible bone loss in osteoporosis rats,” Journal of Bone and Mineral Metabolism, vol. 21, no. 6, pp. 388–395, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. G.-Z. Jiang, H. Matsumoto, M. Hori et al., “Correlation among geometric, densitometric, and mechanical properties in mandible and femur of osteoporotic rats,” Journal of Bone and Mineral Metabolism, vol. 26, no. 2, pp. 130–137, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Kuroda, H. Mukohyama, H. Kondo et al., “Bone mineral density of the mandible in ovariectomized rats: analyses using dual energy X-ray absorptiometry and peripheral quantitative computed tomography,” Oral Diseases, vol. 9, no. 1, pp. 24–28, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Yang, D. Farnell, H. Devlin, K. Horner, and J. Graham, “The effect of ovariectomy on mandibular cortical thickness in the rat,” Journal of Dentistry, vol. 33, no. 2, pp. 123–129, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. P. G. Reeves, F. H. Nielsen, and G. C. Fahey Jr., “AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet,” The Journal of Nutrition, vol. 123, no. 11, pp. 1939–1951, 1993. View at Google Scholar · View at Scopus
  54. S. Kawamoto, S. Ejiri, E. Nagaoka, and H. Ozawa, “Effects of oestrogen deficiency on osteoclastogenesis in the rat periodontium,” Archives of Oral Biology, vol. 47, no. 1, pp. 67–73, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Hidaka, Y. Okamoto, Y. Yamada et al., “Alterations in the periodontium after ovariectomy in rats: the effects of a Japanese herbal medicine, Chujo-to,” Phytotherapy Research, vol. 14, no. 7, pp. 527–533, 2000. View at Google Scholar
  56. P. M. Duarte, P. Gonçalves, M. Z. Casati, S. de Toledo, E. A. Sallum, and F. H. Nociti Jr., “Estrogen and alendronate therapies may prevent the influence of estrogen deficiency on the tooth-supporting alveolar bone: a histometric study in rats,” Journal of Periodontal Research, vol. 41, no. 6, pp. 541–546, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. G. Jiang, H. Matsumoto, J. Yamane, N. Kuboyama, Y. Akimoto, and A. Fujii, “Prevention of trabecular bone loss in the mandible of ovariectomized rats,” Journal of oral science, vol. 46, no. 2, pp. 75–85, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Hunziker, T. J. Wronski, and S. C. Miller, “Mandibular bone formation rates in aged ovariectomized rats treated with anti-resorptive agents alone and in combination with intermittent parathyroid hormone,” Journal of Dental Research, vol. 79, no. 6, pp. 1431–1438, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. S. C. Miller, J. Hunziker, M. Mecham, and T. J. Wronski, “Intermittent parathyroid hormone administration stimulates bone formation in the mandibles of aged ovariectomized rats,” Journal of Dental Research, vol. 76, no. 8, pp. 1471–1476, 1997. View at Publisher · View at Google Scholar · View at Scopus