Endocrinology of sex steroid hormones and cell dynamics in the periodontium

Periodontology 2000

Volumn 61, Issue 1, 2013, Pages 69-88

  Mariotti, Angelo ^a   Mawhinney, Michael ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; SEX HORMONE;

ANTIBODY SPECIFICITY; ARTICLE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CYTOLOGY; HUMAN; PERIODONTAL DISEASE; PERIODONTIUM; PHYSIOLOGY;

CELL PHYSIOLOGICAL PROCESSES; GONADAL STEROID HORMONES; HUMANS; ORGAN SPECIFICITY; PERIODONTAL DISEASES; PERIODONTIUM; RECEPTORS, CELL SURFACE;

EID: 84871225097     PISSN: 09066713     EISSN: 16000757     Source Type: Journal    
DOI: 10.1111/j.1600-0757.2011.00424.x     Document Type: Article

References (219)

1. American Autoimmune and Related Diseases Association. Autoimmune disease in women, 2011. American Autoimmune and Related Diseases Association. http://www.aarda.org/women_and_autoimmunity.php. (accessed March 1, 2011).
2. Amino N, Miyai K, Kuro R, Tanizawa O, Azukizawa M, Takai S, Tanaki F, Nishi K, Kawashima M, Kumahara Y. Transient postpartum hypothyroidism: fourteen cases with autoimmune thyroiditis. Ann Intern Med 1977: 87: 155-159.
3. Amino N, Miyai K, Yamamoto T, Kuro R, Tanaka F. Transient recurrence of hyperthyroidism after delivery in Graves' disease. J Clin Endocrinol Metab 1977: 44: 130-136.
4. Arafat AH. Periodontal status during pregnancy. J Periodontol 1974: 45: 641-643.
5. Armitage G. Bi-directional relationship between pregnancy and periodontal disease. Periodontol 2000 2013: 61: 160-176.
6. Arnal JF, Fontaine C, Billon-Gales A, Favre J, Laurell H, Lenfant F, Gourdy P. Estrogen receptors and endothelium. Arterioscler Thromb Vasc Biol 2010: 30: 1506-1512.
7. Aufdemorte TB, Sheridan PJ. Nuclear uptake of sex steroids in gingiva of the baboon. J Periodontol 1981: 52: 430-434.
8. Baum BJ. Characteristics of participants in the oral physiology component of the Baltimore longitudinal study of aging. Community Dent Oral Epidemiol 1981: 9: 128-134.
9. Beagrie GS. Observations on cell biology of gingival tissues of mice. Br Dent J 1966: 121: 417-420.
10. Becerik S, Ozcaka O, Nalbantsoy A, Atilla G, Celec P, Behuliak M, Emingil G. Effects of menstrual cycle on periodontal health and gingival crevicular fluid markers. J Periodontol 2010: 81: 673-681.
11. Bengtsson B. Estrogen induced inhibition of 3H-noradrenaline release in the uterus and portal vein of the rat. Acta Physiol Scand 1978: 104: 287-298.
12. Blackmore PF, Beebe SJ, Danforth DR, Alexander N. Progesterone and 17 alpha- hydroxyprogesterone. Novel stimulators of calcium influx in human sperm. J Biol Chem 1990: 265: 1376-1380.
13. Buduneli N, Becerik S, Buduneli E, Baylas H, Kinnby B. Gingival status, crevicular fluid tissue-type plasminogen activator, plasminogen activator inhibitor-2 levels in pregnancy versus post-partum. Aust Dent J 2010: 55: 292-297.
14. Coletta RD, Reynolds MA, Martelli-Junior H, Graner E, Almeida OP, Sauk JJ. Testosterone stimulates proliferation and inhibits interleukin-6 production of normal and hereditary gingival fibromatosis fibroblasts. Oral Microbiol Immunol 2002: 17: 186-192.
15. Colucci WS, Gimbrone MA Jr, McLaughlin MK, Halpern W, Alexander RW. Increased vascular catecholamine sensitivity and alpha-adrenergic receptor affinity in female and estrogen-treated male rats. Circ Res 1982: 50: 805-811.
16. Curilovic Z, Mazor Z, Berchtold H. Gingivitis in Zurich schoolchildren. A reexamination after 20years. SSO Schweiz Monatsschr Zahnheilkd 1977: 87: 801-808.
17. Cutress TW. Periodontal health and periodontal disease in young people: global epidemiology. Int Dent J 1986: 36: 146-152.
18. Daltaban O, Saygun I, Bolu E. Periodontal status in men with hypergonadotropic hypogonadism: effects of testosterone deficiency. J Periodontol 2006: 77: 1179-1183.
19. Daniell HW. Postmenopausal tooth loss. Contributions to edentulism by osteoporosis and cigarette smoking. Arch Intern Med 1983: 143: 1678-1682.
20. Dickson RB, Lippman ME. Control of human breast cancer by estrogen, growth factors and oncogenes. Lippman ME, Dickson R, editors. Breast cancer, cellular and molecular biology. Boston: Kluwer Academic Publishers, 1988: 119-166.
21. Dunn JF, Nisula BC, Rodbard D. Transport of steroid hormones: binding of 21 endogenous steroids to both testosterone-binding globulin and corticosteroid-binding globulin in human plasma. J Clin Endocrinol Metab 1981: 53: 58-68.
22. Dyer RF, Sodek J, Heersche JN. The effect of 17 beta-estradiol on collagen and noncollagenous protein synthesis in the uterus and some periodontal tissues. Endocrinology 1980: 107: 1014-1021.
23. El-Ashiry GM, El-Kafrawy AH, Nasr MF, Younis N. Comparative study of the influence of pregnancy and oral contraceptives on the gingivae. Oral Surg Oral Med Oral Pathol 1970: 30: 472-475.
24. El Attar TM, Roth GD, Hugoson A. Comparative metabolism of 4- 14 C-progesterone in normal and chronically inflamed human gingival tissue. J Periodontal Res 1973: 8: 79-85.
25. El Attar TM. The in vitro conversion of male sex steroid, (1, 2-3-H)-androstenedione in normal and inflamed human gingiva. Arch Oral Biol 1974: 19: 1185-1190.
26. El Attar TM. Metabolism of progesterone-7-alpha-3 H in vitro in human gingiva with periodontitis. J Periodontol 1971: 42: 721-725.
27. El Attar TM, Hugoson A. Comparative metabolism of female sex steroids in normal and chronically inflamed gingiva of the dog. J Periodontal Res 1974: 9: 284-289.
28. El Attar TM, Hugoson A. The in vitro conversion of female sex steroid, oestrone, in normal and inflamed human gingiva. Arch Oral Biol 1974: 19: 425-429.
29. Ferguson MM, McKay Hart D, Lindsay R, Stephen KW. Progeston therapy for menstrually related aphthae. Int J Oral Surg 1978: 7: 463-470.
30. Figuero E, Carrillo-de-Albornoz A, Herrera D, Bascones-Martinez A. Gingival changes during pregnancy: I. Influence of hormonal variations on clinical and immunological parameters. J Clin Periodontol 2010: 37: 220-229.
31. Foligno L, Forni F, D'Addona A. Hormonal influence on the physiology and pathology of the dental gingival unit: the preliminary results of a pilot study. Minerva Stomatol 2010: 59: 13-21.
32. Forabosco A, Criscuolo M, Coukos G, Uccelli E, Weinstein R, Spinato S, Botticelli A, Volpe A. Efficacy of hormone replacement therapy in postmenopausal women with oral discomfort. Oral Surg Oral Med Oral Pathol 1992: 73: 570-574.
33. Formicola AJ, Weatherford T 3rd, Grupe H Jr. The uptake of H3-estradiol by the oral tissues of rats. J Periodontal Res 1970: 5: 269-275.
34. Friederici HH. The early response of uterine capillaries to estrogen stimulation. An electron microscopic study. Lab Invest 1967: 17: 322-333.
35. Friedlander AH. The physiology, medical management and oral implications of menopause. J Am Dent Assoc 2002: 133: 73-81.
36. Fukuda H. [Experimental studies on the effect of sex hormones on the proliferation of cells derived from the gingival tissue in culture]. Shikwa Gakuho 1971: 71: 1214-1232.
37. Funder JW. Steroids, receptors, and response elements: the limits of signal specificity. Recent Prog Horm Res 1991: 47: 191-207.
38. Genco RJ. Host responses in periodontal diseases: current concepts. J Periodontol 1992: 63: 338-355.
39. Gornstein RA, Lapp CA, Bustos-Valdes SM, Zamorano P. Androgens modulate interleukin-6 production by gingival fibroblasts in vitro. J Periodontol 1999: 70: 604-609.
40. Gorski J, Toft D, Shyamala G, Smith D, Notides A. Hormone receptors: studies on the interaction of estrogen with the uterus. Recent Prog Horm Res 1968: 24: 45-80.
41. Greiss FC Jr, Anderson SG. Effect of ovarian hormones on the uterine vascular bed. Am J Obstet Gynecol 1970: 107: 829-836.
42. Groen JJ, Menczel J, Shapiro S. Chronic destructive periodontal disease in patients with presenile osteoporosis. J Periodontol 1968: 39: 19-23.
43. Guay AT, Bansal S, Heatley GJ. Effect of raising endogenous testosterone levels in impotent men with secondary hypogonadism: double blind placebo-controlled trial with clomiphene citrate. J Clin Endocrinol Metab 1995: 80: 3546-3552.
44. Gursoy M, Pajukanta R, Sorsa T, Kononen E. Clinical changes in periodontium during pregnancy and post-partum. J Clin Periodontol 2008: 35: 576-583.
45. Gutierrez G, Dagnino R, Mintz G. Polymyositis/dermatomyositis and pregnancy. Arthritis Rheum 1984: 27: 291-294.
46. Hamlet MA, Rorie DK, Tyce GM. Effects of estradiol on release and disposition of norepinephrine from nerve endings. Am J Physiol 1980: 239: H450-H456.
47. Hansen CJ, Welshons WV, Gorski J. Toward a more unified model of steroid hormone receptor structure and function. Sheridan PJ, Blum K, Trachtenberg MC, editors. Steroid receptors and disease: cancer, autoimmune, bone, and circulatory disorders. New York: Marcel Dekker, 1988: 3-22.
48. Haytac MC, Ozcelik O, Mariotti A. Periodontal disease in men. Periodontol 2000 2013: 61: 252-265.
49. Hechtor O, Krohn L, Harris J. Effects of estrogens and other steroids on capillary permeability. Endocrinology 1942: 30: 598-608.
50. Hefti A, Engelberger T, Buttner M. Gingivitis in Basel schoolchildren. SSO Schweiz Monatsschr Zahnheilkd 1981: 91: 1087-1092.
51. Hench PA. The potential reversibility of rheumatoid arthritis. Mayo Clin Proc 1949: 24: 167-178.
52. Hess RA. Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol 2003: 1: 52; doi:10.1186/1477-7827-1-52.
53. Hildebolt CF. Osteoporosis and oral bone loss. Dentomaxillofac Radiol 1997: 26: 3-15.
54. Hoffman BB, Lavin TN, Lefkowitz RJ, Ruffolo RR Jr. Alpha adrenergic receptor subtypes in rabbit uterus: mediation of myometrial contraction and regulation by estrogens. J Pharmacol Exp Ther 1981: 219: 290-295.
55. Hohlweg-Majert B, Schmelzeisen R, Pfeiffer BM, Schneider E. Significance of osteoporosis in craniomaxillofacial surgery: a review of the literature. Osteoporos Int 2006: 17: 167-179.
56. Holm-Pedersen P, Loe H. Flow of gingival exudate as related to menstruation and pregnancy. J Periodontal Res 1967: 2: 13-20.
57. Huang WT, Lu HK, Chou HH, Kuo MY. Immunohistochemical analysis of Th1/Th2 cytokine profiles and androgen receptor expression in the pathogenesis of nifedipine - induced gingival overgrowth. J Periodontal Res 2003: 38: 422-427.
58. Hugoson A. Gingivitis in pregnant women. A longitudinal clinical study. Odontol Revy 1971: 22: 65-84.
59. Hugoson A, Lindhe J. Gingival tissue regeneration in female dogs treated with sex hormones. Clinical observations. Odontol Revy 1971: 22: 237-249.
60. Jensen EV, Suzuki T, Kawashima T, Stumpf WE, Jungblut PW, DeSombre ER. A two- step mechanism for the interaction of estradiol with rat uterus. Proc Natl Acad Sci U S A 1968: 59: 632-638.
61. Johnston CC Jr, Hui SL, Witt RM, Appledorn R, Baker RS, Longcope C. Early menopausal changes in bone mass and sex steroids. J Clin Endocrinol Metab 1985: 61: 905-911.
62. Jonasson G, Bankvall G, Kiliaridis S. Estimation of skeletal bone mineral density by means of the trabecular pattern of the alveolar bone, its interdental thickness, and the bone mass of the mandible. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001: 92: 346-352.
63. Jonsson D, Nilsson J, Odenlund M, Bratthall G, Broman J, Ekblad E, Lydrup ML, Nilsson BO. Demonstration of mitochondrial oestrogen receptor beta and oestrogen- induced attenuation of cytochrome c oxidase subunit I expression in human periodontal ligament cells. Arch Oral Biol 2007: 52: 669-676.
64. Jonsson D, Wahlin A, Idvall I, Johnsson I, Bratthall G, Nilsson BO. Differential effects of estrogen on DNA synthesis in human periodontal ligament and breast cancer cells. J Periodontal Res 2005: 40: 401-406.
65. Kalman SM. The effect of estrogens on uterine blood flow in the rat. J Pharmacol Exp Ther 1958: 124: 179-181.
66. Kaufman AY. An oral contraceptive as an etiologic factor in producing hyperplastic gingivitis and a neoplasm of the pregnancy tumor type. Oral Surg Oral Med Oral Pathol 1969: 28: 666-670.
67. Kawahara K, Shimazu A. Expression and intracellular localization of progesterone receptors in cultured human gingival fibroblasts. J Periodontal Res 2003: 38: 242-246.
68. Ke FC, Ramirez VD. Binding of progesterone to nerve cell membranes of rat brain using progesterone conjugated to 125I-bovine serum albumin as a ligand. J Neurochem 1990: 54: 467-472.
69. Klein A. Die Veränderung der Mundhöhle während der Menstruation. Zahnärztl Rdsch 1934: 43: 1531-1539.
70. Klinger G, Borner A, Carol W. Effects of an intranasally administered low dose progestogen on the gingival epithelium. Endokrinologie 1981: 78: 301-304.
71. Knight GM, Wade AB. The effects of hormonal contraceptives on the human periodontium. J Periodontal Res 1974: 9: 18-22.
72. Knisely WH, Grunt JA, Berry RJ. In vivo observation on the seminal vesicles of adult neonatally castrated rats before and after intravenous testosterone. Am J Physiol 1957: 189: 437-440.
73. Kochakian CD, Arimasa N. The metabolism in vitro of anabolic-androgenic steroids in mammalian tissues. Kochakian CD editor. Anabolic-androgenic steroids. New York: Springer-Verlag, 1976: 287-360.
74. Koenig H, Fan CC, Goldstone AD, Lu CY, Trout JJ. Polyamines mediate androgenic stimulation of calcium fluxes and membrane transport in rat heart myocytes. Circ Res 1989: 64: 415-426.
75. Kofoed JA. Concentration and synthesis of acidic glycosaminoglycans in gingiva of normal and orchidectomized rats injected with testosterone. J Periodontal Res 1971: 6: 278-281.
76. Kovesi G, Banoczy J. Follow-up studies in oral lichen planus. Int J Oral Surg 1973: 2: 13-19.
77. Kribbs PJ. Comparison of mandibular bone in normal and osteoporotic women. J Prosthet Dent 1990: 63: 218-222.
78. Kumar PS. Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000 2013: 61: 103-124.
79. Lan NC, Chen JS, Belelli D, Pritchett DB, Seeburg PH, Gee KW. A steroid recognition site is functionally coupled to an expressed GABA(A)-benzodiazepine receptor. Eur J Pharmacol 1990: 188: 403-406.
80. Lapp CA, Thomas ME, Lewis JB. Modulation by progesterone of interleukin-6 production by gingival fibroblasts. J Periodontol 1995: 66: 279-284.
81. Lewko WM, Anderson A. Estrogen receptors and growth response in cultured human periodontal ligament cells. Life Sci 1986: 39: 1201-1206.
82. Liang L, Yu JF, Wang Y, Wang G, Ding Y. Effect of estrogen receptor beta on the osteoblastic differentiation function of human periodontal ligament cells. Arch Oral Biol 2008: 53: 553-557.
83. Lindhe J, Attsfrom R. Gingival exudation during the menstrual cycle. J Periodontal Res 1967: 2: 194-198.
84. Lindhe J, Attstrom R, Bjorn AL. Influence of sex hormones on gingival exudation in dogs with chronic gingivitis. J Periodontal Res 1968: 3: 279-283.
85. Lindhe J, Attstrom R, Bjorn AL. Influence of sex hormones on gingival exudation in gingivitis-free female dogs. J Periodontal Res 1968: 3: 273-278.
86. Lindhe J, Bjorn AL. Influence of hormonal contraceptives on the gingiva of women. J Periodontal Res 1967: 2: 1-6.
87. Lindhe J, Branemark PI. Changes in microcirculation after local application of sex hormones. J Periodontal Res 1967: 2: 185-193.
88. Lindhe J, Branemark PI. Changes in vascular permeability after local application of sex hormones. J Periodontal Res 1967: 2: 259-265.
89. Lindhe J, Branemark PI, Lundskog J. Changes in vascular proliferation after local application of sex hormones. J Periodontal Res 1967: 2: 266-272.
90. Litwack D, Kennedy JE, Zander HA. Response of oral epithelia to ovariectomy and estrogen replacement. J Periodontal Res 1970: 5: 263-268.
91. Löe H. Periodontal changes in pregnancy. J Periodontol 1965: 36: 209-217.
92. Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963: 21: 533-551.
93. Lorz HM, Frumin AM. Spontaneous remission in chronic idiopathic thrombocytopenic purpura during pregnancy. Obstet Gynecol 1961: 17: 362-363.
94. Losordo DW, Isner JM. Estrogen and angiogenesis: a review. Arterioscler Thromb Vasc Biol 2001: 21: 6-12.
95. Lunenfeld B. Androgen therapy in the aging male. World J Urol 2003: 21: 292-305.
96. Lynn BD. "The pill" as an etiologic agent in hypertrophic gingivitis. Oral Surg Oral Med Oral Pathol 1967: 24: 333-334.
97. MacDonald PC, Dombroski RA, Casey ML. Recurrent secretion of progesterone in large amounts: an endocrine/metabolic disorder unique to young women? Endocr Rev 1991: 12: 372-401.
98. Machtei EE, Mahler D, Sanduri H, Peled M. The effect of menstrual cycle on periodontal health. J Periodontol 2004: 75: 408-412.
99. Machuca G, Khoshfeiz O, Lacalle JR, Machuca C, Bullon P. The influence of general health and socio-cultural variables on the periodontal condition of pregnant women. J Periodontol 1999: 70: 779-785.
100. Magness RR, Rosenfeld CR. Steroid control of blood vessel function. Alexander NJ, d'Arcangues C, editors. Steroid hormones and uterine bleeding. Washington, DC: AAAS Press, 1992: 107-120.
101. Maier AW, Orban B. Gingivitis in pregnancy. Oral Surg Oral Med Oral Pathol 1949: 2: 334-373.
102. Manson JD. Bone morphology and bone loss in periodontal disease. J Clin Periodontol 1976: 3: 14-22.
103. Mariotti A. Dental plaque-induced gingival diseases. Ann Periodontol 1999: 4: 7-19.
104. Mariotti A. Desquamative gingivitis: revisited. Todays FDA 1991: 3: 1C-2C.
105. Mariotti A. The extracellular matrix of the periodontium: dynamic and interactive tissues. Periodontol 2000 1993: 3: 39-63.
106. Mariotti A. A primer on inflammation. Compend Contin Educ Dent 2004: 25: 7-15.
107. Mariotti A. Sex steroid hormones and cell dynamics in the periodontium. Crit Rev Oral Biol Med 1994: 5: 27-53.
108. Mariotti AJ. Estrogen and extracellular matrix influence human gingival fibroblast proliferation and protein production. J Periodontol 2005: 76: 1391-1397.
109. Marshall-Day CD. The epidemiology of periodontal disease. J Periodontol 1951: 22: 13-22.
110. Martin MB, Saceda M, Lindsey RK. Estrogen and progesterone receptors. Lippman M, Dickson R, editors. Regulatory mechanisms in breast cancer. Boston: Kluwer Academic Publishers, 1991: 273-288.
111. Massler M, Schour I, Chopra B. Occurrence of gingivitis in suburban Chicago school children. J Periodontol 1950: 21: 146-164.
112. Mawhinney MG, Neubauer BL. Actions of estrogen in the male. Invest Urol 1979: 16: 409-420.
113. McCartan BE, Sullivan A. The association of menstrual cycle, pregnancy, and menopause with recurrent oral aphthous stomatitis: a review and critique. Obstet Gynecol 1992: 80: 455-458.
114. McCarty KS Jr, McCarty KS Sr. Steroid modulation of the expression of growth factors and oncogenes in breast cancer. Cancer Treat Res 1991: 53: 197-220.
115. Miyagi M, Aoyama H, Morishita M, Iwamoto Y. Effects of sex hormones on chemotaxis of human peripheral polymorphonuclear leukocytes and monocytes. J Periodontol 1992: 63: 28-32.
116. Miyazaki H, Yamashita Y, Shirahama R, Goto-Kimura K, Shimada N, Sogame A, Takehara T. Periodontal condition of pregnant women assessed by CPITN. J Clin Periodontol 1991: 18: 751-754.
117. Mohamed AH. The localization of H3-progesterone in the oral mucosa of rabbits. J Periodontol 1974: 45: 844-852.
118. Mohammad AR, Hooper DA, Vermilyea SG, Mariotti A, Preshaw PM. An investigation of the relationship between systemic bone density and clinical periodontal status in post-menopausal Asian-American women. Int Dent J 2003: 53: 121-125.
119. Mombelli A, Gusberti FA, van Oosten MA, Lang NP. Gingival health and gingivitis development during puberty. A 4-year longitudinal study. J Clin Periodontol 1989: 16: 451-456.
120. Mooradian AD, Morley JE, Korenman SG. Biological actions of androgens. Endocr Rev 1987: 8: 1-28.
121. Morishita M, Yamamura T, Shimazu A, Bachchu AH, Iwamoto Y. Estradiol enhances the production of mineralized nodules by human periodontal ligament cells. J Clin Periodontol 1999: 26: 748-751.
122. Moshchil AI, Volozhin AI, Smetnik VP, Kangel'dieva AA, Iureneva SV. [Status of tissue mineralization and the periodontium in women with impaired ovarian function]. Akush Ginekol (Mosk) 1991: 37: 71-74.
123. Muhlemann HR. [Eine gingivitis intermenstrualis]. SSO Schweiz Monatsschr Zahnheilkd 1948: 58: 865-885.
124. Muhlemann HR, Mazor ZS. Gingivitis in Zurich school children. Helv Odontol Acta 1958: 2: 3-12.
125. Mund A, Simson J, Rothfield N. Effect of pregnancy on course of systemic lupus erythematosus. JAMA 1963: 183: 917-920.
126. Musajo F, Nardelli GB, Passi P, Petrillo M. [Estradiol hormone receptors in human gingiva: preliminary results]. G Stomatol Ortognatodonzia 1985: 3: 75-79.
127. Nakagawa S, Fujii H, Machida Y, Okuda K. A longitudinal study from prepuberty to puberty of gingivitis. Correlation between the occurrence of Prevotella intermedia and sex hormones. J Clin Periodontol 1994: 21: 658-665.
128. Narayanan AS, Page RC. Connective tissues of the periodontium: a summary of current work. Coll Relat Res 1983: 3: 33-64.
129. Nicolau J, Paiva YA. Sialic acid concentration in the attached gingival tissue of rats related to age and sex. J Periodontal Res 1979: 14: 503-504.
130. Nilsson S, Gustafsson JA. Estrogen receptors: therapies targeted to receptor subtypes. Clin Pharmacol Ther 2011: 89: 44-55.
131. Nisengard RJ, Rogers RS 3rd. The treatment of desquamative gingival lesions. J Periodontol 1987: 58: 167-172.
132. Nutlay AG, Bhaskar SN, Weinmann JP, Budy AM. The effect of estrogen on the gingiva and alveolar bone of molars in rats and mice. J Dent Res 1954: 33: 115-127.
133. O'Malley BW, Tsai SY, Bagchi M, Weigel NL, Schrader WT, Tsai MJ. Molecular mechanism of action of a steroid hormone receptor. Recent Prog Horm Res 1991: 47: 1-24.
134. Offenbacher S, Lin D, Strauss R, McKaig R, Irving J, Barros SP, Moss K, Barrow DA, Hefti A, Beck JD. Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters, and pregnancy outcomes: a pilot study. J Periodontol 2006: 77: 2011-2024.
135. Ojanotko-Harri A. Metabolism of progesterone by healthy and inflamed human gingiva in vitro. J Steroid Biochem 1985: 23: 1031-1035.
136. Ojanotko-Harri A, Forssell H, Laine M, Hurttia H, Blauer M, Tuohimaa P. Immunohistochemical detection of androgen receptors in human oral mucosa. Arch Oral Biol 1992: 37: 511-514.
137. Ojanotko A, Nienstedt W, Harri MP. Metabolism of testosterone by human healthy and inflamed gingiva in vitro. Arch Oral Biol 1980: 25: 481-484.
138. Ordonez-Moran P, Munoz A. Nuclear receptors: genomic and non-genomic effects converge. Cell Cycle 2009: 8: 1675-1680.
139. Ozcelik O, Haytac MC, Seydaoglu G. The effects of anabolic androgenic steroid abuse on gingival tissues. J Periodontol 2006: 77: 1104-1109.
140. Pan F, Zhang R, Wang G, Ding Y. Oestrogen receptors are involved in the osteogenic differentiation of periodontal ligament stem cells. Biosci Rep 2011: 31: 117-124.
141. Pankhurst CL, Waite IM, Hicks KA, Allen Y, Harkness RD. The influence of oral contraceptive therapy on the periodontium - duration of drug therapy. J Periodontol 1981: 52: 617-620.
142. Parfitt GJ. A five year longitudinal study of the gingival condition of a group of children in England. J Periodontol 1957: 28: 26-32.
143. Parkar M, Tabona P, Newman H, Olsen I. IL-6 expression by oral fibroblasts is regulated by androgen. Cytokine 1998: 10: 613-619.
144. Phillips HB, Ashley FP. The relationship between periodontal disease and a metacarpal bone index. Br Dent J 1973: 134: 237-239.
145. Pilgram TK, Hildebolt CF, Dotson M, Cohen SC, Hauser JF, Kardaris E, Civitelli R. Relationships between clinical attachment level and spine and hip bone mineral density: data from healthy postmenopausal women. J Periodontol 2002: 73: 298-301.
146. Pizzo G, Guiglia R, Licata ME, Pizzo I, Davies JM, Giuliana G. Effect of hormone replacement therapy on periodontal status of postmenopausal women. Sci Monit 2011: 17: PH23-PH27.
147. Porter R, Beers MH, Berkow R. The Merck manual of diagnosis and therapy, 18th edn. Rahway, NJ: Merck Research Laboratories, 2006, 290.
148. Preshaw P. Oral contraceptives and the periodontium. Periodontol 2000 2013: 61: 125-159.
149. Prill HJ, Goetz F. Blood flow in the myometrium and endometrium of the uterus. Am J Obstet Gynecol 1961: 82: 102-108.
150. Raber-Durlacher JE, Leene W, Palmer-Bouva CC, Raber J, Abraham-Inpijn L. Experimental gingivitis during pregnancy and post-partum: immunohistochemical aspects. J Periodontol 1993: 64: 211-218.
151. Reinhardt RA, Payne JB, Maze CA, Patil KD, Gallagher SJ, Mattson JS. Influence of estrogen and osteopenia/osteoporosis on clinical periodontitis in postmenopausal women. J Periodontol 1999: 70: 823-828.
152. Richman MJ, Abarbanel AR. Effect of estradiol and diethylstilbesterol upon the atropic human buccal mucosa with a preliminary report on the use of estrogens in the management of senile gingivitis. J Clin Endocrinol 1943: 3: 224-226.
153. Richman MJ, Abarbanel AR. Effects of estradiol, testoterone, diethylstilbesteriol and several of their derivatives upon the human oral mucous membrane. J Am Dent Assoc 1943: 30: 913-923.
154. Ronderos M, Jacobs DR, Himes JH, Pihlstrom BL. Associations of periodontal disease with femoral bone mineral density and estrogen replacement therapy: cross-sectional evaluation of US adults from NHANES III. J Clin Periodontol 2000: 27: 778-786.
155. Rubens R, Dhont M, Vermeulen A. Further studies on Leydig cell function in old age. J Clin Endocrinol Metab 1974: 39: 40-45.
156. Sartorius GA, Nieschlag E. Paternal age and reproduction. Hum Reprod Update 2010: 16: 65-79.
157. Savouret JF, Misrahi M, Loosfelt H, Atger M, Bailly A, Perrot-Applanat M, Vu Hai MT, Guiochon-Mantel A, Jolivet A, Lorenzo F, Logeat F, Pichon MF, Bouchard P, Milgrom E. Molecular and cellular biology of mammalian progesterone receptors. Recent Prog Horm Res 1989: 45: 65-116.
158. Segal AL, Katcher AH, Brightman VJ, Miller MF. Recurrent herpes labialis, recurrent aphthous ulcers, and the menstrual cycle. J Dent Res 1974: 53: 797-803.
159. Sheridan PJ, Blum K, Martin PM. Steroid receptor dynamics: a function of cellular equilibrium. Sheridan PJ, Blum K, Trachtenberg MC, editors. Steroid receptors and disease : cancer, autoimmune, bone, and circulatory disorders. New York: Marcel Dekker, 1988: 46-69.
160. Shiau HJ, Reynolds MA. Sex differences in destructive periodontal disease: exploring the biologic basis. J Periodontol 2010: 81: 1505-1517.
161. Ship IS, Morris AL, Durocher RT, Burket LW. Recurrent aphthous ulcerations in professional school student populations. IV. Twelve month study of natural disease patterns. Oral Surg Oral Med Oral Pathol 1961: 14: 30-39.
162. Shklar G, Chauncey HH, Shapiro S. The effect of testosterone on the periodontium of normal and hypophysectomized rats. J Periodontol 1967: 38: 203-210.
163. Shklar G, McCarthy PL. Oral lesions of mucous membrane pemphigoid. A study of 85 cases. Arch Otolaryngol 1971: 93: 354-364.
164. Shrout MK, Hildebolt CF, Potter BJ, Brunsden TK, Pilgram TK, Dotson M, Yokoyama-Crothers N, Hauser J, Cohen S, Kardaris E, Civitelli R, Hanes P. Comparison of morphological measurements extracted from digitized dental radiographs with lumbar and femoral bone mineral density measurements in postmenopausal women. J Periodontol 2000: 71: 335-340.
165. Shu L, Guan SM, Fu SM, Guo T, Cao M, Ding Y. Estrogen modulates cytokine expression in human periodontal ligament cells. J Dent Res 2008: 87: 142-147.
166. Siiteri PK, MacDonald PC. Role of extraglandular estrogen in human endocrinology. Greep RO, Astwood EB, editors. Handbook of physiology Section 7: endocrinolgy volume II: female reproductive system. Washington, DC: American Physiology Society, 1973: 615-630.
167. Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand 1964: 22: 121-135.
168. Silverman S Jr, Gorsky M, Lozada-Nur F, Liu A. Oral mucous membrane pemphigoid. A study of sixty-five patients. Oral Surg Oral Med Oral Pathol 1986: 61: 233-237.
169. Silverman S Jr, Griffith M. Studies on oral lichen planus. II. Follow-up on 200 patients, clinical characteristics, and associated malignancy. Oral Surg Oral Med Oral Pathol 1974: 37: 705-710.
170. Sooriyamoorthy M, Gower DB, Eley BM. Androgen metabolism in gingival hyperplasia induced by nifedipine and cyclosporin. J Periodontal Res 1990: 25: 25-30.
171. Sooriyamoorthy M, Harvey W, Gower DB. Metabolism of testosterone by human gingival fibroblasts in culture. Biochem Soc Trans 1984: 12: 1113-1114.
172. Sooriyamoorthy M, Harvey W, Gower DB. The use of human gingival fibroblasts in culture for studying the effects of phenytoin on testosterone metabolism. Arch Oral Biol 1988: 33: 353-359.
173. Soory M. Targets for steroid hormone mediated actions of periodontal pathogens, cytokines and therapeutic agents: some implications on tissue turnover in the periodontium. Curr Drug Targets 2000: 1: 309-325.
174. Southard KA, Southard TE, Schlechte JA, Meis PA. The relationship between the density of the alveolar processes and that of post-cranial bone. J Dent Res 2000: 79: 964-969.
175. Southren AL, Rappaport SC, Gordon GG, Vittek J. Specific 5 alpha- dihydrotestosterone receptors in human gingiva. J Clin Endocrinol Metab 1978: 47: 1378-1382.
176. Spaziani E. Accessory reproductive organs in mammals: control of cell and tissue transport by sex hormones. Pharmacol Rev 1975: 27: 207-286.
177. Sperber GH. Oral contraceptive hypertrophic gingivitis. J Dent Assoc S Afr 1969: 24: 37-40.
178. Staffolani N, Guerra M, Pugliese M, Cardinale G, Gulino A. [Hormonal receptors in gingival inflammation]. Minerva Stomatol 1989: 38: 823-826.
179. Stearns EL, MacDonnell JA, Kaufman BJ, Padua R, Lucman TS, Winter JS, Faiman C. Declining testicular function with age. Hormonal and clinical correlates. Am J Med 1974: 57: 761-766.
180. Steinberg KK, Freni-Titulaer LW, DePuey EG, Miller DT, Sgoutas DS, Coralli CH, Phillips DL, Rogers TN, Clark RV. Sex steroids and bone density in premenopausal and perimenopausal women. J Clin Endocrinol Metab 1989: 69: 533-539.
181. Stepan JJ, Lachman M, Zverina J, Pacovsky V, Baylink DJ. Castrated men exhibit bone loss: effect of calcitonin treatment on biochemical indices of bone remodeling. J Clin Endocrinol Metab 1989: 69: 523-527.
182. Stice SL, Ford SP, Rosazza JP, Van Orden DE. Interaction of 4-hydroxylated estradiol and potential-sensitive Ca2+ channels in altering uterine blood flow during the estrous cycle and early pregnancy in gilts. Biol Reprod 1987: 36: 369-375.
183. Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007: 28: 521-574.
184. Strauss K. Vitamin B1 therapy in cyclic habitual aphthous stomatitis in women. Br Dent J 1947: 83: 77-80.
185. Sutcliffe P. A longitudinal study of gingivitis and puberty. J Periodontal Res 1972: 7: 52-58.
186. Tang X, Meng H, Han J, Zhang L, Hou J, Zhang F. Up-regulation of estrogen receptor- beta expression during osteogenic differentiation of human periodontal ligament cells. J Periodontal Res 2008: 43: 311-321.
187. Tezal M, Wactawski-Wende J, Grossi SG, Ho AW, Dunford R, Genco RJ. The relationship between bone mineral density and periodontitis in postmenopausal women. J Periodontol 2000: 71: 1492-1498.
188. Tilakaratne A, Soory M, Ranasinghe AW, Corea SM, Ekanayake SL, de Silva M. Periodontal disease status during pregnancy and 3months post-partum, in a rural population of Sri-Lankan women. J Clin Periodontol 2000: 27: 787-792.
189. Tomes J, Tomes C. Dental Surgery, 4th edn. London: J & A Churchill, 1894.
190. Trott JR. An histological investigation into the keratinisation found in human gingiva. Br Dent J 1957: 103: 421-427.
191. Trussell J. Contraceptive efficacy. Hatcher RA, Trussell J, Nelson AL, Cates W, Stewart F, Kowal D, editors. Contraceptive Technology 19th revised edition. New York: Ardent Media, 2007: 747-756.
192. Unsal B, Saygun I, Daltaban O, Bal B, Bolu E. The relationship between periodontal status and alkaline phosphatase levels in gingival crevicular fluid in men with hypergonadotropic hypogonadism. Yonsei Med J 2008: 49: 71-78.
193. Valimaa H, Savolainen S, Soukka T, Silvoniemi P, Makela S, Kujari H, Gustafsson JA, Laine M. Estrogen receptor-beta is the predominant estrogen receptor subtype in human oral epithelium and salivary glands. J Endocrinol 2004: 180: 55-62.
194. Van Minden F. Use of female sex hormone in the treatment of chronic desquamative gingivitis. J Am Dent Assoc 1946: 33: 1294-1297.
195. Vittek J, Altman K, Gordon GG, Southren AL. The metabolism of 7alpha-3H- testosterone by rat mandibular bone. Endocrinology 1974: 94: 325-329.
196. Vittek J, Gordon GG, Rappaport SC, Munnangi PR, Southren AL. Specific progesterone receptors in rabbit gingiva. J Periodontal Res 1982: 17: 657-661.
197. Vittek J, Hernandez MR, Wenk EJ, Rappaport SC, Southren AL. Binding of 3H- methyltrienolone (3H-R1881) to androgen receptors in human gingiva. J Periodontal Res 1985: 20: 41-46.
198. Vittek J, Hernandez MR, Wenk EJ, Rappaport SC, Southren AL. Specific estrogen receptors in human gingiva. J Clin Endocrinol Metab 1982: 54: 608-612.
199. Vittek J, Munnangi PR, Gordon GG, Rappaport SC, Southern AL. Progesterone "receptors" in human gingiva. IRCS Med Sci 1982: 10: 381.
200. Vittek J, Rappaport SC, Gordon GG, Munnangi PR, Southren AL. Concentration of circulating hormones and metabolism of androgens by human gingiva. J Periodontol 1979: 50: 254-264.
201. von Wowern N. Bone mineral content of mandibles: normal reference values--rate of age-related bone loss. Calcif Tissue Int 1988: 43: 193-198.
202. von Wowern N, Klausen B, Kollerup G. Osteoporosis: a risk factor in periodontal disease. J Periodontol 1994: 65: 1134-1138.
203. von Wowern N, Klausen B, Olgaard K. Steroid-induced mandibular bone loss in relation to marginal periodontal changes. J Clin Periodontol 1992: 19: 182-186.
204. Ward VJ, Manson JD. Alveolar bone loss in periodontal disease and the metacarpal index. J Periodontol 1973: 44: 763-769.
205. Weaker FJ, Sheridan PJ, Aufdemorte TB, Gages GA, Triplett RG. Nuclear uptake of progesterone in oral and laryngeal tissues. Exp Clin Endocrinol 1988: 7: 177-180.
206. Weinstein RL, Kelch RP, Jenner MR, Kaplan SL, Grumbach MM. Secretion of unconjugated androgens and estrogens by the normal and abnormal human testis before and after human chorionic gonadotropin. J Clin Invest 1974: 53: 1-6.
207. Weyant RJ, Pearlstein ME, Churak AP, Forrest K, Famili P, Cauley JA. The association between osteopenia and periodontal attachment loss in older women. J Periodontol 1999: 70: 982-991.
208. Willershausen B, Lemmen C, Hamm G, Sonnabend E. [Human fibroblast cultures under the effect of the hormones estradiol and progesterone]. Dtsch Zahnarztl Z 1986: 41: 976-978.
209. Wilson EM, Simental JA, French FS, Sar M. Molecular analysis of the androgen receptor. Ann N Y Acad Sci 1991: 637: 56-63.
210. Wilson JD. Metabolism of testicular androgens. Greep RO, Astwood EB, editors. Hanbook of physiology Section 7: endocrinology Volume V: male reproductive system. Washington, DC: American Physiology Society, 1975: 491-508.
211. Wu CH, Motohashi T, Abdel-Rahman HA, Flickinger GL, Mikhail G. Free and protein- bound plasma estradiol-17 beta during the menstrual cycle. J Clin Endocrinol Metab 1976: 43: 436-445.
212. Yen SS. The biology of menopause. J Reprod Med 1977: 18: 287-296.
213. Yokoyama M, Hinode D, Masuda K, Yoshioka M, Grenier D. Effect of female sex hormones on Campylobacter rectus and human gingival fibroblasts. Oral Microbiol Immunol 2005: 20: 239-243.
214. Younes M, Honma N. Estrogen receptor beta. Arch Pathol Lab Med 2011: 135: 63-66.
215. Zhou Y, Fu Y, Li JP, Qi LY. The role of estrogen in osteogenetic cytokine expression in human periodontal ligament cells. Int J Periodontics Restorative Dent 2009: 29: 507-513.
216. Ziskin DE. Effects of male sex hormone on gingivae and oral mucous membranes. J Dent Res 1941: 20: 419-423.
217. Ziskin DE, Blackberg SN, Slanetz CA. Effects of subcutaneous injections of estrogenic and gonadotropic hormones on gums and oral mucous membranes of normal and castrated rhesus monkeys. J Dent Res 1935: 15: 407-428.
218. Ziskin DE, Nesse GJ. Pregnancy gingivitis; history, classification, etiology. Am J Orthod Oral Surg 1946: 32: 390-432.
219. Ziskin DE, Zegarelli EV. Chronic desquamative gingivitis: a report of twelve cases. Am J Orthod Oral Surg 1945: 31: C1-C33.