Effects of estrogen deficiency on microstructural changes in rat alveolar bone proper and periodontal ligament

Liu,Zhongshuang; Liu,Lisha; Kang,Chen; Xie,Qi; Zhang,Bin; Li,Ying

doi:10.3892/mmr.2015.3891

Effects of estrogen deficiency on microstructural changes in rat alveolar bone proper and periodontal ligament

Authors:
- Zhongshuang Liu
- Lisha Liu
- Chen Kang
- Qi Xie
- Bin Zhang
- Ying Li
View Affiliations

Affiliations: Sino‑Russian Institute of Hard Tissue Development and Regeneration, The Second Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China, School of Stomatology, Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China
Published online on: June 4, 2015 https://doi.org/10.3892/mmr.2015.3891
Pages: 3508-3514

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The present study aimed to analyze the effects of estrogen deficiency on buccal alveolar bone proper and the periodontal ligament in ovariectomized (OVX) rats, compared with rats that had been subjected to sham treatment. Morphological and histological changes in the periodontium were analyzed using micro‑computed tomography and paraffin sectioning. Sections were stained using hematoxylin and eosin, and tartrate‑resistant acid phosphatase. Expression of receptor activator of nuclear factor‑κB ligand (RANKL), dentin matrix protein 1 C‑terminal (DMP1‑C) and osteopontin (OPN) were analyzed using immunohistochemistry. Histomorphometric analysis of buccal alveolar bone proper samples revealed porotic changes and disorganized bone structure in OVX rats. Furthermore, bone mineral density and pore spacing were significantly lower in OVX rats compared with sham rats. Porosity was significantly higher in OVX rats compared with sham rats (P<0.01). A greater number of osteoclasts were observed along the margins of the buccal alveolar bone proper samples from OVX rats compared with those from the sham rats. Expression of OPN and RANKL was significantly higher, and that of DMP1‑C was significantly lower, in OVX rats compared with sham rats. Ovariectomy‑induced osteoporosis is capable of changing the structure of buccal alveolar bone proper and the periodontal ligament, which is likely to increase the risk of periodontal disease.

View Figures

View References

1	Irfan UM, Dawson DV and Bissada NF: Epidemiology of periodontal disease: A review and clinical perspectives. J Int Acad Periodontol. 3:14–21. 2001.
2	Michaud DS, Joshipura K, Giovannucci E and Fuchs CS: A prospective study of periodontal disease and pancreatic cancer in US male health professionals. J Natl Cancer Inst. 99:171–175. 2007. View Article : Google Scholar : PubMed/NCBI
3	Kanis JA, Melton LJ III, Christiansen C, Johnston CC and Khaltaev N: The diagnosis of osteoporosis. J Bone Miner Res. 9:1137–1141. 1994. View Article : Google Scholar : PubMed/NCBI
4	Genant HK, Cooper C, Poor G, Reid I, Ehrlich G, Kanis J, Nordin BE, Barrett-Connor E, Black D, Bonjour JP, et al: Interim report and recommendations of the World Health Organization task-force for osteoporosis. Osteoporos Int. 10:259–264. 1999. View Article : Google Scholar
5	Binte Anwar R, Tanaka M, Kohno S, Ikegame M, Watanabe N, Nowazesh Ali M and Ejiri S: Relationship between porotic changes in alveolar bone and spinal osteoporosis. J Dent Res. 86:52–57. 2007. View Article : Google Scholar
6	Bollen AM, Taguchi A, Hujoel PP and Hollender LG: Case-control study on self-reported osteoporotic fractures and mandibular cortical bone. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 90:518–524. 2000. View Article : Google Scholar : PubMed/NCBI
7	Kalu DN: The ovariectomized rat model of postmenopausal bone loss. Bone Miner. 15:175–191. 1991. View Article : Google Scholar : PubMed/NCBI
8	Wronski TJ, Dann LM, Qi H and Yen CF: Skeletal effects of withdrawal of estrogen and diphosphonate treatment in ovariectomized rats. Calcif Tissue Int. 53:210–216. 1993. View Article : Google Scholar : PubMed/NCBI
9	Wronski TJ, Yen CF, Burton KW, Mehta RC, Newman PS, Soltis EE and DeLuca PP: Skeletal effects of calcitonin in ovariectomized rats. Endocrinology. 129:2246–2250. 1991. View Article : Google Scholar : PubMed/NCBI
10	Kribbs PJ: Comparison of mandibular bone in normal and osteoporotic women. J Prosthet Dent. 63:218–222. 1990. View Article : Google Scholar : PubMed/NCBI
11	Groen JJ, Menczel J and Shapiro S: Chronic destructive periodontal disease in patients with presenile osteoporosis. J Periodontol. 39:19–23. 1968. View Article : Google Scholar : PubMed/NCBI
12	Jagelaviciene E and Kubilius R: The relationship between general osteoporosis of the organism and periodontal diseases. Medicina (Kaunas). 42:613–618. 2006.
13	Moriya Y, Ito K and Murai S: Effects of experimental osteoporosis on alveolar bone loss in rats. J Oral Sci. 40:171–175. 1998. View Article : Google Scholar
14	Kribbs PJ, Smith DE and Chesnut CH III: Oral findings in osteoporosis. Part II: Relationship between residual ridge and alveolar bone resorption and generalized skeletal osteopenia. J Prosthet Dent. 50:719–724. 1983. View Article : Google Scholar : PubMed/NCBI
15	Klemetti E and Vainio P: Effect of bone mineral density in skeleton and mandible on extraction of teeth and clinical alveolar height. J Prosthet Dent. 70:21–25. 1993. View Article : Google Scholar : PubMed/NCBI
16	Bays RA and Weinstein RS: Systemic bone disease in patients with mandibular atrophy. J Oral Maxillofac Surg. 40:270–272. 1982. View Article : Google Scholar : PubMed/NCBI
17	Dvorak G, Reich KM, Tangl S, Goldhahn J, Haas R and Gruber R: Cortical porosity of the mandible in an osteoporotic sheep model. Clin Oral Implants Res. 22:500–505. 2011. View Article : Google Scholar
18	Fen JQ, Zhang J, Dallas SL, Lu Y, Chen S, Tan X, Owen M, Harris SE and MacDougall M: Dentin matrix protein 1, a target molecule for Cbfa1 in bone, is a unique bone marker gene. J Bone Miner Res. 17:1822–1831. 2002. View Article : Google Scholar : PubMed/NCBI
19	Ejiri S, Toyooka E, Tanaka M, Anwar RB and Kohno S: Histological and histomorphometrical changes in rat alveolar bone following antagonistic tooth extraction and/or ovariectomy. Arch Oral Biol. 51:941–950. 2006. View Article : Google Scholar : PubMed/NCBI
20	Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, et al: Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 12:657–664. 2006. View Article : Google Scholar : PubMed/NCBI
21	Sodek J, Ganss B and McKee MD: Osteopontin. Crit Rev Oral Biol Med. 11:279–303. 2000. View Article : Google Scholar : PubMed/NCBI
22	Jaiprakash A, Prasadam I, Feng JQ, Liu Y, Crawford R and Xiao Y: Phenotypic characterization of osteoarthritic osteocytes from the sclerotic zones: A possible pathological role in subchondral bone sclerosis. Int J Biol Sci. 8:406–417. 2012. View Article : Google Scholar : PubMed/NCBI
23	Zhang B, Sun Y, Chen L, Guan C, Guo L and Qin C: Expression and distribution of SIBLING proteins in the predentin/dentin and mandible of hyp mice. Oral Dis. 16:453–464. 2010. View Article : Google Scholar : PubMed/NCBI
24	Tanaka M, Ejiri S, Toyooka E, Kohno S and Ozawa H: Effects of ovariectomy on trabecular structures of rat alveolar bone. J Periodontal Res. 37:161–165. 2002. View Article : Google Scholar : PubMed/NCBI
25	Bando K, Nitta H, Matsubara M and Ishikawa I: Bone mineral density in periodontally healthy and edentulous postmenopausal women. Ann Periodontol. 3:322–326. 1998. View Article : Google Scholar : PubMed/NCBI
26	Weyant RJ, Pearlstein ME, Churak AP, Forrest K, Famili P and Cauley JA: The association between osteopenia and periodontal attachment loss in older women. J Periodontol. 70:982–991. 1999. View Article : Google Scholar : PubMed/NCBI
27	Kribbs PJ, Chesnut CH III, Ott SM and Kilcoyne RF: Relationships between mandibular and skeletal bone in an osteoporotic population. J Prosthet Dent. 62:703–707. 1989. View Article : Google Scholar : PubMed/NCBI
28	Payne JB, Zachs NR, Reinhardt RA, Nummikoski PV and Patil K: The association between estrogen status and alveolar bone density changes in postmenopausal women with a history of periodontitis. J Periodontol. 68:24–31. 1997. View Article : Google Scholar : PubMed/NCBI
29	Wactawski-Wende J, Grossi SG, Trevisan M, Genco RJ, Tezal M, Dunford RG, Ho AW, Hausmann E and Hreshchyshyn MM: The role of osteopenia in oral bone loss and periodontal disease. J Periodontol. 67(Suppl 10): 1076–1084. 1996. View Article : Google Scholar : PubMed/NCBI
30	Majeska RJ, Ryaby JT and Einhorn TA: Direct modulation of osteoblastic activity with estrogen. J Bone Joint Surg Am. 76:713–721. 1994.PubMed/NCBI
31	Manolagas SC and Jilka RL: Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med. 332:305–311. 1995. View Article : Google Scholar : PubMed/NCBI
32	Pacifici R: Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J Bone Miner Res. 11:1043–1051. 1996. View Article : Google Scholar : PubMed/NCBI
33	Hughes DE, Dai A, Tiffee JC, Li HH, Mundy GR and Boyce BF: Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat Med. 2:1132–1136. 1996. View Article : Google Scholar : PubMed/NCBI
34	Udagawa N, Takahashi N, Yasuda H, Mizuno A, Itoh K, Ueno Y, Shinki T, Gillespie MT, Martin TJ, Higashio K and Suda T: Osteoprotegerin produced by osteoblasts is an important regulator in osteoclast development and function. Endocrinology. 141:3478–3484. 2000.PubMed/NCBI
35	Kawamoto S, Ejiri S, Nagaoka E and Ozawa H: Effects of oestrogen deficiency on osteoclastogenesis in the rat periodontium. Arch Oral Biol. 47:67–73. 2002. View Article : Google Scholar
36	Rajachar RM, Truong AQ and Giachelli CM: The influence of surface mineral and osteopontin on the formation and function of murine bone marrow-derived osteoclasts. J Mater Sci Mater Med. 19:3279–3285. 2008. View Article : Google Scholar : PubMed/NCBI
37	Ono N, Nakashima K, Rittling SR, Schipani E, Hayata T, Soma K, Denhardt DT, Kronenberg HM, Ezura Y and Noda M: Osteopontin negatively regulates parathyroid hormone receptor signaling in osteoblasts. J Biol Chem. 283:19400–19409. 2008. View Article : Google Scholar : PubMed/NCBI
38	Namkung-Matthai H, Appleyard R, Jansen J, Hao Lin J, Maastricht S, Swain M, Mason RS, Murrell GA, Diwan AD and Diamond T: Osteoporosis influences the early period of fracture healing in a rat osteoporotic model. Bone. 28:80–86. 2001. View Article : Google Scholar : PubMed/NCBI
39	Maciejewska I, Qin D, Huang B, Sun Y, Mues G, Svoboda K, Bonewald L, Butler WT, Feng JQ and Qin C: Distinct compartmentalization of dentin matrix protein 1 fragments in mineralized tissues and cells. Cells Tissues Organs. 189:186–191. 2009. View Article : Google Scholar :