Derleme
BibTex RIS Kaynak Göster

A Review on the Relationship Between Osteoporosis and Periodontal Diseases

Yıl 2024, , 142 - 164, 22.04.2024
https://doi.org/10.22312/sdusbed.1398573

Öz

Periodontitis and osteoporosis are conditions associated with widespread inflammation that pose significant public health problems for the ageing population. Periodontal diseases consist of a series of disorders in the dento-gingival tissues that are predominantly dysbiotic and inflammatory in nature. Osteoporosis is an age- related bone disease characterised by deterioration of bone density and structure with an increased risk of fracture. This review aims to provide an update on the relationship between osteoporosis and periodontitis by evaluating the literature published in the last 25 years, followed by a discussion of their mechanistic links, common risk factors and therapeutic implications. In clinical trials examining the relationship between systemic and alveolar bone loss (ABL), all 10 studies published between 1996 and 2020 revealed an inverse correlation between systemic bone mineral density (BMD) and ABL. Although radiographic assessment of alveolar bone loss is an important criterion, CAL reflects the lifetime experience of periodontitis and is a critical measure for the diagnosis and staging of periodontitis. Of the 23 studies published between 1995 and 2020, 17 showed a significant association between CAL and osteoporosis. In both diseases, age-related oxidative stress and ageing are the underlying mechanisms that drive a pro-inflammatory tissue microenvironment, thus leading to impairment of the bone remodelling process. These mechanistic links are implicated in common risk factors such as vitamin D deficiency and smoking. Understanding these factors and their interaction requires interdisciplinary management and well-controlled longitudinal studies to examine potential therapeutics for both diseases.

Kaynakça

  • [1] Demmer RT, Papapanou PN. Epidemiologic patterns of chronic and aggressive periodontitis. Periodontol 2000 2010;53:28–44. [PubMed: 20403103]
  • [2] American Academy of Periodontology Task Force Report on the Update to the 1999 Classification of Periodontal Diseases and Conditions. J Periodontol 1999;2015(86):835–838.
  • [3] Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol 1996;67:1041–1049.
  • [4] Reginster JY, Burlet N. Osteoporosis: a still increasing prevalence. Bone 2006;38:S4–9. [PubMed: 16455317]
  • [5] Kawai M, Modder UI, Khosla S, Rosen CJ. Emerging therapeutic opportunities for skeletal restoration. Nat Rev Drug Discov 2011;10:141–156. [PubMed: 21283108]
  • [6] Groen JJ, Duyvensz F, Halsted JA. Diffuse alveolar atrophy of the jaw (non-inflammatory form of paradental disease) and pre-senile osteoporosis. Gerontol Clin 1960;2:68–86.
  • [7] Armitage GC. Development of a classification system for periodontal diseases and conditions. Northwest Dent 2000;79:31–35. [PubMed: 11413609]
  • [8] Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol 2018;89(Suppl 1):S159–s172. [PubMed: 29926952]
  • [9] Caton JG, Armitage G, Berglundh T, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Periodontol 2018;89(Suppl 1):s1–s8. [PubMed: 29926946]
  • [10] Albandar JM, Susin C, Hughes FJ. Manifestations of systemic diseases and conditions that affect the periodontal attachment apparatus: Case definitions and diagnostic considerations. J Periodontol 2018;89(Suppl 1):s183–s203. [PubMed: 29926941]
  • [11] Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol 2018;45:S162–S170. [PubMed: 29926490]
  • [12] Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet (London, England) 2002;359:1929–1936.
  • [13] Yu B, Wang CY. Osteoporosis and periodontal diseases - An update on their association and mechanistic links. Periodontol 2000. 2022 Jun;89(1):99-113. doi: 10.1111/prd.12422. Epub 2022 Mar 4. PMID: 35244945; PMCID: PMC9067601.
  • [14] Okabe S, Morimoto Y, Ansai T, et al. Assessment of the relationship between the mandibular cortex on panoramic radiographs and the risk of bone fracture and vascular disease in 80-year-olds. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:433–442. [PubMed: 18299222]
  • [15] Brennan RM, Genco RJ, Hovey KM, Trevisan M, Wactawski-Wende J. Clinical attachment loss, systemic bone density, and subgingival calculus in postmenopausal women. J Periodontol 2007;78:2104–2111. [PubMed: 17970676]
  • [16] Ishii K, Taguchi A, Nakamoto T, et al. Diagnostic efficacy of alveolar bone loss of the mandible for identifying postmenopausal women with femoral osteoporosis. Dentomaxillofac Radiol 2007;36:28–33. [PubMed: 17329585]
  • [17] Taguchi A, Ohtsuka M, Tsuda M, et al. Risk of vertebral osteoporosis in post-menopausal women with alterations of the mandible. Dentomaxillofac Radiol 2007;36:143–148. [PubMed: 17463098]
  • [18] Takaishi Y, Okamoto Y, Ikeo T, et al. Correlations between periodontitis and loss of mandibular bone in relation to systemic bone changes in postmenopausal Japanese women. Osteoporos Int 2005;16:1875–1882. [PubMed: 16027956]
  • [19] Hildebolt CF, Pilgram TK, Yokoyama-Crothers N, et al. The pattern of alveolar crest height change in healthy postmenopausal women after 3 years of hormone/estrogen replacement. Therapy 2002;73:1279–1284.
  • [20] 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 Endodontol 2001;92:346–352. [21] 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. [PubMed: 11022780]
  • [22] Taguchi A, Suei Y, Ohtsuka M, Otani K, Tanimoto K, Hollender LG. Relationship between bone mineral density and tooth loss in elderly Japanese women. Dentomaxillofac Radiol 1999;28:219–223. [PubMed: 10455385]
  • [23] Payne JB, Reinhardt RA, Nummikoski PV, Patil KD. Longitudinal alveolar bone loss in postmenopausal osteoporotic/osteopenic women. Osteoporos Int 1999;10:34–40. [PubMed: 10501777]
  • [24] Hausmann E, Allen K, Carpio L, Christersson LA, Clerehugh V. Computerized methodology for detection of alveolar crestal bone loss from serial intraoral radiographs. J Periodontol 1992;63:657–662. [PubMed: 1507045]
  • [25] von Wowern N Bone mass of mandibles. In vitro and in vivo analyses. Dan Med Bull 1986;33:23–44. [PubMed: 3948537]
  • [26] Horner K, Devlin H, Harvey L. Detecting patients with low skeletal bone mass. J Dent 2002;30:171–175. [PubMed: 12450724]
  • [27] Devlin H, Allen PD, Graham J, et al. Automated osteoporosis risk assessment by dentists: a new pathway to diagnosis. Bone 2007;40:835–842. [PubMed: 17188590]
  • [28] Jonasson G, Sundh V, Hakeberg M, Hassani-Nejad A, Lissner L, Ahlqwist M. Mandibular bone changes in 24 years and skeletal fracture prediction. Clin Oral Invest 2013;17:565–572.
  • [29] Hassani-Nejad A, Ahlqwist M, Hakeberg M, Jonasson G. Mandibular trabecular bone as fracture indicator in 80-year-old men and women. Eur J Oral Sci 2013;121:525–531. [PubMed: 24102691]
  • [30] Lindh C, Horner K, Jonasson G, et al. The use of visual assessment of dental radiographs for identifying women at risk of having osteoporosis: the OSTEODENT project. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:285–293. [PubMed: 18299223]
  • [31] Jonasson G, Jonasson L, Kiliaridis S. Skeletal bone mineral density in relation to thickness, bone mass, and structure of the mandibular alveolar process in dentate men and women. Eur J Oral Sci 2007;115:117–123. [PubMed: 17451501]
  • [32] Lindh C, Obrant K, Petersson A. Maxillary bone mineral density and its relationship to the bone mineral density of the lumbar spine and hip. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;98:102–109. [PubMed: 15243479]
  • [33] Elders PJ, Habets LL, Netelenbos JC, van der Linden LW, van der Stelt PF. The relation between periodontitis and systemic bone mass in women between 46 and 55 years of age. J Clin Periodontol 1992;19:492–496. [PubMed: 1430285]
  • [34] Jacobs R, Ghyselen J, Koninckx P, van Steenberghe D. Long-term bone mass evaluation of mandible and lumbar spine in a group of women receiving hormone replacement therapy. Eur J Oral Sci 1996;104:10–16. [PubMed: 8653490]
  • [35] Buyukkaplan US, Tonguc MO, Guldag MU, Yildiz M, Gumus BA. Comparison of mandibular bone mineral densities in dentate and edentulous patients. J Prosthodont. 2013 Jan;22(1):23-7. doi: 10.1111/j.1532- 849X.2012.00908.x. Epub 2012 Sep 4. PMID: 22946895
  • [36] Mashalkar VN, Suragimath G, Zope SA, Varma SA. A cross-sectional study to assess and correlate osteoporosis and periodontitis among postmenopausal women: a dual energy X-ray absorptiometry study. J Mid- Life Health 2018;9:2–7.
  • [37] Passos-Soares JS, Vianna MIP, Gomes-Filho IS, et al. Association between osteoporosis treatment and severe periodontitis in post-menopausal women. Menopause (New York, NY) 2017;24:789–795.
  • [38] Penoni DC, Torres SR, Farias ML, Fernandes TM, Luiz RR, Leão AT. Association of osteoporosis and bone medication with the periodontal condition in elderly women. Osteoporos Int 2016;27:1887–1896. [PubMed: 26626187]
  • [39] Juluri R, Prashanth E, Gopalakrishnan D, et al. Association of post-menopausal osteoporosis and periodontal disease: a double-blind case-control study. J Int Oral Health 2015;7:119–123. [40] Singh A, Sharma RK, Siwach RC, Tewari S, Narula SC. Association of bone mineral density with periodontal status in postmeno-pausal women. J Invest Clin Dent 2014;5:275–282.
  • [41] Tak I-H, Shin M-H, Kweon S-S, et al. The association between periodontal disease, tooth loss and bone mineral density in a Korean population. J Clin Periodontol 2014;41:1139–1144. [PubMed: 25207848]
  • [42] Gondim V, Aun J, Fukuda CT, et al. Severe loss of clinical attachment level: an independent association with low hip bone mineral density in postmenopausal females. J Periodontol 2013;84:352–359. [PubMed: 22548585]
  • [43] Passos JS, Vianna MI, Gomes-Filho IS, et al. Osteoporosis/osteopenia as an independent factor associated with periodontitis in postmenopausal women: a case-control study. Osteoporos Int 2013;24:1275–1283. [PubMed: 23001114]
  • [44] Iwasaki M, Taylor GW, Nakamura K, Yoshihara A, Miyazaki H. Association between low bone mineral density and clinical attachment loss in Japanese postmenopausal females. J Periodontol 2013;84:1708–1716. [PubMed: 23451986]
  • [45] Marjanovic EJ, Southern HN, Coates P, et al. Do patients with osteoporosis have an increased prevalence of periodontal disease? A cross-sectional study. Osteoporos Int 2013;24:1973–1979. [PubMed: 23340948]
  • [46] Moeintaghavi A, Pourjavad M, Dadgar S, Tabbakh NS. Evaluation of the association between periodontal parameters, osteoporosis and osteopenia in post menopausal women. J Dent (Tehran, Iran) 2013;10:443–448.
  • [47] Grocholewicz K, Bohatyrewicz A. Oral health and bone mineral density in postmenopausal women. Arch Oral Biol 2012;57:245–251. [PubMed: 22153129]
  • [48] Al Habashneh R, Alchalabi H, Khader YS, Hazza’a AM, Odat Z, Johnson GK. Association between periodontal disease and osteoporosis in postmenopausal women in Jordan. J Periodontol 2010;81:1613– 1621. [PubMed: 20681809]
  • [49] Gomes-Filho IS, Passos JDS, Cruz SS, et al. The association between postmenopausal osteoporosis and periodontal disease. J Periodontol 2007;78:1731–1740. [PubMed: 17760543]
  • [50] Taguchi A, Fujiwara S, Masunari N, Suzuki G. Self-reported number of remaining teeth is associated with bone mineral density of the femoral neck, but not of the spine, in Japanese men and women. Osteoporos Int 2004;15:842–846. [PubMed: 14991229]
  • [51] 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. [PubMed: 12873107]
  • [52] Pilgram TK, Hildebolt CF, Dotson M, et al. Relationships between clinical attachment level and spine and hip bone mineral density: data from healthy postmenopausal women. J Periodontol 2002;73:298–301. [PubMed: 11922259]
  • [53] Lundström A, Jendle J, Stenström B, Toss G, Ravald N. Periodontal conditions in 70-year-old women with osteoporosis. Swed Dent J 2001;25:89–96. [PubMed: 11813450]
  • [54] 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. [PubMed: 10505800]
  • [55] Mohammad AR, Bauer RL, Yeh CK. Spinal bone density and tooth loss in a cohort of postmenopausal women. Int J Prosthodont 1997;10:381–385. [PubMed: 9484049]
  • [56] Hildebolt CF, Pilgram TK, Dotson M, et al. Attachment loss with postmenopausal age and smoking. J Periodont Res 1997;32:619–625.
  • [57] Mohammad AR, Brunsvold M, Bauer R. The strength of association between systemic postmenopausal osteoporosis and periodontal disease. Int J Prosthodont 1996;9:479–483. [PubMed: 9108750]
  • [58] Penoni DC, Fidalgo TK, Torres SR, et al. Bone density and clinical periodontal attachment in postmenopausal women: a systematic review and meta-analysis. J Dent Res 2017;96:261–269. [PubMed: 28048966]
  • [59] Martínez-Maestre M, González-Cejudo C, Machuca G, Torrejón R, Castelo-Branco C. Periodontitis and osteoporosis: a systematic review. Climacteric 2010;13:523–529. [PubMed: 20690866] [60] Oztürk Tonguç M, Büyükkaplan US, Fentoglu O, Gümüs BA, Çerçi SS, Kirzioglu FY. Comparison of bone mineral density in the jaws of patients with and without chronic periodontitis. Dentomaxillofac Radiol. 2012 Sep;41(6):509-14. doi: 10.1259/dmfr/21900076. Epub 2012 Jan 12. PMID: 22241867; PMCID: PMC3520387).
  • [61] Nicopoulou-Karayianni K, Tzoutzoukos P, Mitsea A, et al. Tooth loss and osteoporosis: the OSTEODENT study. J Clin Periodontol 2009;36:190–197. [PubMed: 19236531]
  • [62] Krall EA, Garcia RI, Dawson-Hughes B. Increased risk of tooth loss is related to bone loss at the whole body, hip, and spine. Calcif Tissue Int 1996;59:433–437. [PubMed: 8939767]
  • [63] Drozdzowska B, Pluskiewicz W, Michno M. Tooth count in elderly women in relation to their skeletal status. Maturitas 2006;55:126–131. [PubMed: 16822625]
  • [64] Krall EA, Dawson-Hughes B, Papas A, Garcia RI. Tooth loss and skeletal bone density in healthy postmenopausal women. Osteoporos Int 1994;4:104–109. [PubMed: 8003839]
  • [65] May H, Reader R, Murphy S, Khaw KT. Self-reported tooth loss and bone mineral density in older men and women. Age Ageing 1995;24:217–221. [PubMed: 7645442]
  • [66] Hajishengallis G Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 2014;35:3–11. [PubMed: 24269668]
  • [67] Yu B, Wang C-Y. Osteoporosis: the result of an ‘aged’ bone micro-environment. Trends Mol Med 2016;22:641–644. [PubMed: 27354328]
  • [68] Graves D Cytokines that promote periodontal tissue destruction. J Periodontol 2008;79:1585–1591. [PubMed: 18673014]
  • [69] Sczepanik FSC, Grossi ML, Casati M, et al. Periodontitis is an inflammatory disease of oxidative stress: We should treat it that way. Periodontol 2000 2020;84:45–68. [PubMed: 32844417]
  • [70] Mahanonda R, Pichyangkul S. Toll-like receptors and their role in periodontal health and disease. Periodontol 2000 2007;43(1):41–55. [PubMed: 17214834]
  • [71] Kawai T, Matsuyama T, Hosokawa Y, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 2006;169:987–998. [PubMed: 16936272]
  • [72] Pacios S, Xiao W, Mattos M, et al. Osteoblast lineage cells play an essential role in periodontal bone loss through activation of nuclear factor-kappa B. Sci Rep 2015;5:16694. [PubMed: 26666569]
  • [73] Chang J, Wang Z, Tang E, et al. Inhibition of osteoblastic bone formation by nuclear factor-kappaB. Nat Med 2009;15:682–689. [PubMed: 19448637]
  • [74] Jimi E, Aoki K, Saito H, et al. Selective inhibition of NF-[kappa] B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat Med 2004;10:617–624. [PubMed: 15156202]
  • [75] Redlich K, Görtz B, Hayer S, et al. Repair of local bone erosions and reversal of systemic bone loss upon therapy with anti-tumor necrosis factor in combination with osteoprotegerin or parathy-roid hormone in tumor necrosis factor-mediated arthritis. Am J Pathol 2004;164:543–555. [PubMed: 14742260]
  • [76] Haugeberg G, Conaghan PG, Quinn M, Emery P. Bone loss in patients with active early rheumatoid arthritis: infliximab and methotrexate compared with methotrexate treatment alone. Explorative analysis from a 12-month randomised, double-blind, placebo-controlled study. Ann Rheum Dis 2009;68:1898–1901. [PubMed: 19386610]
  • [77] Ghosh S, Karin M. Missing Pieces in the NF-κB Puzzle. Cell 2002;109(2):S81–S96. [PubMed: 11983155]
  • [78] Wang CY, Guttridge DC, Mayo MW, Baldwin AS Jr. NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to prefer-entially suppress chemotherapy-induced apoptosis. Mol Cell Biol 1999;19:5923–5929. [PubMed: 10454539]
  • [79] Wang CY, Mayo MW, Baldwin AS Jr. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996;274:784–787. [PubMed: 8864119]
  • [80] Lee HJ, Kang IK, Chung CP, Choi SM. The subgingival microflora and gingival crevicular fluid cytokines in refractory periodontitis. J Clin Periodontol 1995;22:885–890. [PubMed: 8550866]
  • [81] Delima AJ, Karatzas S, Amar S, Graves DT. Inflammation and tissue loss caused by periodontal pathogens is reduced by interleukin-1 antagonists. J Infect Dis 2002;186:511–516. [PubMed: 12195378] [82] Chiang CY, Kyritsis G, Graves DT, Amar S. Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide. Infect Immun 1999;67:4231–4236. [PubMed: 10417196]
  • [83] Dayan S, Stashenko P, Niederman R, Kupper TS. Oral epithelial overexpression of IL-1alpha causes periodontal disease. J Dent Res 2004;83:786–790. [PubMed: 15381720]
  • [84] Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 2000;106:1481– 1488. [PubMed: 11120755]
  • [85] Pacifici R, Rifas L, McCracken R, Avioli LV. The role of interleukin-1 in postmenopausal bone loss. Exp Gerontol 1990;25:309–316. [PubMed: 2226666]
  • [86] Barbour KE, Lui LY, Ensrud KE, et al. Inflammatory markers and risk of hip fracture in older white women: the study of osteoporotic fractures. J Bone Mineral Res 2014;29:2057–2064. [87] Pacifici R Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J Bone Mineral Res 1996;11:1043–1051.
  • [88] Hajishengallis G, Reis ES, Mastellos DC, Ricklin D, Lambris JD. Novel mechanisms and functions of complement. Nat Immunol 2017;18:1288–1298. [PubMed: 29144501]
  • [89] Zhang X, Kimura Y, Fang C, et al. Regulation of Toll-like receptor–mediated inflammatory response by complement in vivo. Blood 2007;110:228–236. [PubMed: 17363730]
  • [90] Hajishengallis G, Kajikawa T, Hajishengallis E, et al. Complement-dependent mechanisms and interventions in periodontal disease. Front Immunol 2019;10. doi:10.3389/fimmu.2019.00406 [PubMed: 30723470]
  • [91] Courts FJ, Boackle RJ, Fudenberg HH, Silverman M. Detection of functional complement components in gingival crevicular fluid from humans with periodontal disease. J Dent Res 1977;56:327–331. [PubMed: 323317]
  • [92] Patters M, Niekrash C, Lang NP. Assessment of complement cleavage in gingival fluid during experimental gingivitis in man. J Clin Periodontol 1989;16:33–37. [PubMed: 2644312]
  • [93] Niekrash CE, Patters MR. Simultaneous assessment of complement components C3, C4, and B and their cleavage products in human gingival fluid: II. Longitudinal changes during periodontal therapy. J Periodontal Res 1985;20:268–275. [PubMed: 3160842]
  • [94] Maekawa T, Abe T, Hajishengallis E, et al. Genetic and intervention studies implicating complement C3 as a major target for the treatment of periodontitis. J Immunol 2014;192:6020. [PubMed: 24808362]
  • [95] MacKay DL, Kean TJ, Bernardi KG, et al. Reduced bone loss in a murine model of postmenopausal osteoporosis lacking complement component 3. J Orthopaedic Res 2018;3(36):118–128.
  • [96] Matsuo K, Owens JM, Tonko M, Elliott C, Chambers TJ, Wagner EF. Fosl1 is a transcriptional target of c-Fos during osteoclast differentiation. Nat Genet 2000;24:184–187. [PubMed: 10655067]
  • [97] Redlich K, Smolen JS. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nat Rev Drug Discov 2012;11:234–250. [PubMed: 22378270]
  • [98] Takayanagi H, Kim S, Koga T, et al. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 2002;3:889–901. [PubMed: 12479813]
  • [99] Teitelbaum SL. Osteoclasts: what do they do and how do they do it? Am J Pathol 2007;170:427–435. [PubMed: 17255310]
  • [100] Lee SK, Lorenzo JA. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology 1999;140:3552–3561. [PubMed: 10433211]
  • [101] Horwood NJ, Elliott J, Martin TJ, Gillespie MT. Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 1998;139:4743–4746. [PubMed: 9794488]
  • [102] Han JH, Choi SJ, Kurihara N, Koide M, Oba Y, Roodman GD. Macrophage inflammatory protein-1alpha is an osteoclastogenic factor in myeloma that is independent of receptor activator of nuclear factor kappaB ligand. Blood 2001;97:3349–3353. [PubMed: 11369623] [103] Gilbert L, He X, Farmer P, et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2αA) is inhibited by tumor necrosis factor-α. J Biol Chem 2002;277:2695–2701. [PubMed: 11723115]
  • [104] Kaneki H, Guo R, Chen D, et al. Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J Biol Chem 2006;281:4326–4333. [PubMed: 16373342]
  • [105] Chang J, Liu F, Lee M, et al. NF-kappaB inhibits osteogenic differentiation of mesenchymal stem cells by promoting beta-catenin degradation. Proc Natl Acad Sci USA 2013;110:9469–9474. [PubMed: 23690607]
  • [106] Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007;13:156–163. [PubMed: 17237793]
  • [107] Li X, Zhang Y, Kang H, et al. Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem 2005;280:19883–19887. [PubMed: 15778503]
  • [108] Mundy GR. Osteoporosis and inflammation. Nutr Rev 2007;65:S147–S151. [PubMed: 18240539]
  • [109] Ginaldi L, Di Benedetto M, De Martinis M. Osteoporosis, inflammation and ageing. Immun Ageing 2005;2:14. [PubMed: 16271143]
  • [110] Lin CL, Moniz C, Chambers TJ, Chow JW. Colitis causes bone loss in rats through suppression of bone formation. Gastroenterology 1996;111:1263–1271. [PubMed: 8898640]
  • [111] Khosla S, Melton LJ 3rd, Riggs BL. The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Mineral Res 2011;26:441–451.
  • [112] López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013;153:1194– 1217. [PubMed: 23746838]
  • [113] Manolagas SC, Parfitt AM. What old means to bone. Trends Endocrinol Metab 2010;21:369–374. [PubMed: 20223679]
  • [114] Tilstra JS, Robinson AR, Wang J, et al. NF-κB inhibition delays DNA damage–induced senescence and aging in mice. J Clin Investig 2012;122:2601–2612. [PubMed: 22706308]
  • [115] Yu B, Huo L, Liu Y, et al. PGC-1α controls skeletal stem cell fate and bone-fat balance in osteoporosis and skeletal aging by inducing TAZ. Cell Stem Cell 2018;23:193–209.e195. [PubMed: 30017591]
  • [116] Persson GR. Periodontal complications with age. Periodontol 2000 2018;78(1):185–194. [PubMed: 30198125]
  • [117] Papapanou PN, Lindhe J. Preservation of probing attachment and alveolar bone levels in 2 random population samples. J Clin Periodontol 1992;19:583–588. [PubMed: 1447383]
  • [118] Hajishengallis G Aging and its impact on innate immunity and inflammation: implications for periodontitis. J Oral Biosci 2014;56:30–37. [PubMed: 24707191]
  • [119] Wu Y, Dong G, Xiao W, et al. Effect of aging on periodontal inflammation, microbial colonization, and disease susceptibility. J Dent Res 2016;95:460–466. [PubMed: 26762510]
  • [120] Bodineau A, Folliguet M, Séguier S. Tissular senescence and modifications of oral ecosystem in the elderly: risk factors for mucosal pathologies. Curr Aging Sci 2009;2:109–120. [PubMed: 20021405]
  • [121] Fransson C, Mooney J, Kinane DF, Berglundh T. Differences in the inflammatory response in young and old human subjects during the course of experimental gingivitis. J Clin Periodontol 1999;26:453–460. [PubMed: 10412850]
  • [122] Ebersole JL, Steffen MJ, Gonzalez-Martinez J, Novak MJ. Effects of age and oral disease on systemic inflammatory and immune parameters in nonhuman primates. Clin Vaccine Immunol CVI 2008;15:1067–1075. [PubMed: 18448617]
  • [123] Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocrinol Rev 2010;31:266–300.
  • [124] Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003;112:481–490. [PubMed: 12600312] [125] Almeida M, Han L, Martin-Millan M, et al. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 2007;282:27285–27297. [PubMed: 17623659]
  • [126] Goettsch C, Babelova A, Trummer O, et al. NADPH oxidase 4 limits bone mass by promoting osteoclastogenesis. J Clin Invest 2013;123:4731–4738. [PubMed: 24216508]
  • [127] Lean JM, Davies JT, Fuller K, et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J Clin Invest 2003;112:915–923. [PubMed: 12975476]
  • [128] Bartell SM, Kim H-N, Ambrogini E, et al. FoxO proteins restrain osteoclastogenesis and bone resorption by attenuating H2O2 accumulation. Nat Commun 2014;5:3773. [PubMed: 24781012]
  • [129] Ambrogini E, Almeida M, Martin-Millan M, et al. FoxO-mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab 2010;11:136–146. [PubMed: 20142101]
  • [130] Cervellati C, Bonaccorsi G, Cremonini E, et al. Oxidative stress and bone resorption interplay as a possible trigger for postmenopausal osteoporosis. Biomed Res Int 2014;2014:569563. [PubMed: 24524081]
  • [131] Chapple IL, Matthews J. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007;43:160–232. [PubMed: 17214840]
  • [132] Löe H Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329–334. [PubMed: 8422804]
  • [133] Aquino-Martinez R, Rowsey JL, Fraser DG, et al. LPS-induced premature osteocyte senescence: Implications in inflammatory alveolar bone loss and periodontal disease pathogenesis. Bone 2020;132:115220. [PubMed: 31904537]
  • [134] Baker DJ, Wijshake T, Tchkonia T, et al. Clearance of p16Ink4a-positive senescent cells delays ageing- associated disorders. Nature 2011;479:232–236. [PubMed: 22048312]
  • [135] Farr JN, Xu M, Weivoda MM, et al. Targeting cellular senescence prevents age-related bone loss in mice. Nat Med 2017;23:1072–1079. [PubMed: 28825716]
  • [136] Palmer AK, Tchkonia T, LeBrasseur NK, Chini EN, Xu M, Kirkland JL. Cellular senescence in type 2 diabetes: a therapeutic opportunity. Diabetes 2015;64:2289–2298. [PubMed: 26106186]
  • [137] Zhou Bo O, Yue R, Murphy Malea M, Peyer JG, Morrison SJ. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 2014;15:154–168. [PubMed: 24953181]
  • [138] Bianco P, Cao X, Frenette PS, et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med 2013;19:35–42. [PubMed: 23296015]
  • [139] Bianco P, Robey PG. Skeletal stem cells. Development 2015;142:1023–1027. [PubMed: 25758217]
  • [140] Oh J, Lee YD, Wagers AJ. Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat Med 2014;20:870. [PubMed: 25100532]
  • [141] Li H, Liu P, Xu S, et al. FOXP1 controls mesenchymal stem cell commitment and senescence during skeletal aging. J Clin Invest 2017;127:1241–1253. [PubMed: 28240601]
  • [142] Liu W, Zhang L, Xuan K, et al. Alpl prevents bone ageing sensitivity by specifically regulating senescence and differentiation in mesenchymal stem cells. Bone Res 2018;6:27. [PubMed: 30210899]
  • [143] Farr JN, Fraser DG, Wang H, et al. Identification of senescent cells in the bone microenvironment. J Bone Miner Res 2016;31:1920–1929. [PubMed: 27341653]
  • [144] Kim HN, Chang J, Iyer S, et al. Elimination of senescent osteoclast progenitors has no effect on the age- associated loss of bone mass in mice. Aging Cell 2019;18:e12923. [PubMed: 30773784]
  • [145] Pignolo RJ, Samsonraj RM, Law SF, Wang H, Chandra A. Targeting cell senescence for the treatment of age-related bone loss. Curr Osteoporos Rep 2019;17:70–85. [PubMed: 30806947]
  • [146] Zhang P, Wang Q, Nie L, et al. Hyperglycemia-induced inflammaging accelerates gingival senescence via NLRC4 phosphorylation. J Biol Chem 2019;294:18807–18819. [PubMed: 31676687] [147] Bischoff-Ferrari HA, Willett WC, Wong JB, Giovannucci E, Dietrich T, Dawson-Hughes B. Fracture prevention with vitamin D supple-mentation: a meta-analysis of randomized controlled trials. J Am Med Assoc 2005;293:2257–2264.
  • [148] Shimazaki Y, Shirota T, Uchida K, et al. Intake of dairy products and periodontal disease: the Hisayama Study. J Periodontol 2008;79:131–137. [PubMed: 18166102]
  • [149] Al-Zahrani MS. Increased intake of dairy products is related to lower periodontitis prevalence. J Periodontol 2006;77:289–294. [PubMed: 16460256]
  • [150] Yoshida T, Stern PH. How vitamin D works on bone. Endocrinol Metab Clin North Am 2012;41:557–569. [PubMed: 22877429]
  • [151] Bischoff-Ferrari HA, Dietrich T, Orav EJ, Dawson-Hughes B. Positive association between 25-hydroxy vitamin D levels and bone mineral density: a population-based study of younger and older adults. Am J Med 2004;116:634–639. [PubMed: 15093761]
  • [152] Laird E, Ward M, McSorley E, Strain JJ, Wallace J. Vitamin D and bone health: potential mechanisms. Nutrients 2010;2:693–724. [PubMed: 22254049]
  • [153] Kliewer SA, Umesono K, Mangelsdorf DJ, Evans RM. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 1992;355:446–449. [PubMed: 1310351]
  • [154] Takahashi N, Udagawa N, Suda T. Vitamin D endocrine system and osteoclasts. Bonekey Rep 2014;3:495. [PubMed: 24605212]
  • [155] Zarei A, Morovat A, Javaid K, Brown CP. Vitamin D receptor expression in human bone tissue and dose- dependent activation in resorbing osteoclasts. Bone Res 2016;4:16030. [PubMed: 27785371]
  • [156] Baldock PA, Thomas GP, Hodge JM, et al. Vitamin D action and regulation of bone remodeling: suppression of osteoclastogenesis by the mature osteoblast. J Bone Miner Res 2006;21:1618–1626. [PubMed: 16995817]
  • [157] Jilka RL, Weinstein RS, Bellido T, Roberson P, Parfitt AM, Manolagas SC. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 1999;104:439–446. [PubMed: 10449436]
  • [158] Müller K, Haahr PM, Diamant M, Rieneck K, Kharazmi A, Bendtzen K. 1,25-Dihydroxyvitamin D3 inhibits cytokine production by human blood monocytes at the post-transcriptional level. Cytokine 1992;4:506–512. [PubMed: 1337987]
  • [159] Inanir A, Ozoran K, Tutkak H, Mermerci B. The effects of calcitriol therapy on serum interleukin-1, interleukin-6 and tumour necrosis factor-alpha concentrations in post-menopausal patients with osteoporosis. J Int Med Res 2004;32:570–582. [PubMed: 15587751]
  • [160] Grossi SG, Genco RJ, Machtei EE, et al. Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol 1995;66:23–29. [PubMed: 7891246]
  • [161] Kanis JA, Johnell O, Oden A, et al. Smoking and fracture risk: a meta-analysis. Osteoporos Int 2005;16:155–162. [PubMed: 15175845]
  • [162] Giannopoulou C, Kamma JJ, Mombelli A. Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J Clin Periodontol 2003;30:145–153. [PubMed: 12622857]
  • [163] Tymkiw KD, Thunell DH, Johnson GK, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol 2011;38:219–228. [PubMed: 21198766]
  • [164] Buduneli N, Buduneli E, Kütükçüler N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. J Periodontol 2009;80:1274–1280. [PubMed: 19656027]
  • [165] César-Neto JB, Duarte PM, de Oliveira MC, Tambeli CH, Sallum EA, Nociti FH Jr. Smoking modulates interleukin-6:interleukin-10 and RANKL:osteoprotegerin ratios in the periodontal tissues. J Periodontal Res 2007;42:184–191. [PubMed: 17305878]
  • [166] Lappin DF, Sherrabeh S, Jenkins WM, Macpherson LM. Effect of smoking on serum RANKL and OPG in sex, age and clinically matched supportive-therapy periodontitis patients. J Clin Periodontol 2007;34:271–277. [PubMed: 17378883] [167] Tang TH, Fitzsimmons TR, Bartold PM. Effect of smoking on concentrations of receptor activator of nuclear factor kappa B ligand and osteoprotegerin in human gingival crevicular fluid. J Clin Periodontol 2009;36:713–718. [PubMed: 19570104]
  • [168] Aziz AS, Kalekar MG, Suryakar AN, et al. Assessment of some bio-chemical oxidative stress markers in male smokers with chronic periodontitis. Indian J Clin Biochem IJCB 2013;28:374–380. [PubMed: 24426240]
  • [169] Fredriksson MI, Figueredo CM, Gustafsson A, Bergström KG, Asman BE. Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. J Periodontol 1999;70:1355–1360. [PubMed: 10588499]
  • [170] Chang CH, Han ML, Teng NC, et al. Cigarette smoking aggravates the activity of periodontal disease by disrupting redox homeostasisan observational study. Sci Rep 2018;8:11055. [PubMed: 30038248]
  • [171] Agnihotri R, Pandurang P, Kamath SU, et al. Association of cigarette smoking with superoxide dismutase enzyme levels in subjects with chronic periodontitis. J Periodontol 2009;80:657–662. [PubMed: 19335086]
  • [172] Al-Bashaireh AM, Haddad LG, Weaver M, Chengguo X, Kelly DL, Yoon S. The effect of tobacco smoking on bone mass: an overview of pathophysiologic mechanisms. J Osteoporos 2018;2018:1206235. [PubMed: 30631414]
  • [173] Reddy MS, Morgan SL. Decreased bone mineral density and periodontal management. Periodontol 2000 2013;61:195–218. [PubMed: 23240950]
  • [174] Penoni DC, Vettore MV, Torres SR, Farias MLF, Leão ATT. An investigation of the bidirectional link between osteoporosis and periodontitis. Arch Osteoporos 2019;14:94. [PubMed: 31444638]
  • [175] Passos-Soares JDS, Vianna MIP, Gomes-Filho IS, et al. Association between osteoporosis treatment and severe periodontitis in post-menopausal women. Menopause 2017;24:789–795. [PubMed: 28225430]
  • [176] Krall EA, Dawson-Hughes B, Hannan MT, Wilson PW, Kiel DP. Postmenopausal Estrogen Replacement and Tooth Retention. The Am J Med 1997;102(6):536–542. [PubMed: 9217668]
  • [177] Garcia MN, Hildebolt CF, Miley DD, et al. One-year effects of vitamin D and calcium supplementation on chronic periodontitis. J Periodontol 2011;82:25–32. [PubMed: 20809866]
  • [178] Dixon D, Hildebolt CF, Miley DD, et al. Calcium and vitamin D use among adults in periodontal disease maintenance programmes. Br Dent J 2009;206:627–631. [PubMed: 19557061]
  • [179] Millen AE, Andrews CA, LaMonte MJ, et al. Vitamin D status and 5-year changes in periodontal disease measures among post-menopausal women: the Buffalo OsteoPerio Study. J Periodontol 2014;85:1321–1332. [PubMed: 24794688]
  • [180] Pavlesen S, Mai X, Wactawski-Wende J, et al. Vitamin D status and tooth loss in postmenopausal females: the buffalo osteoporosis and periodontal disease (OsteoPerio) study. J Periodontol 2016;87:852–863. [PubMed: 27086615]
  • [181] Thorin MH, Wihlborg A, Åkesson K, Gerdhem P. Smoking, smoking cessation, and fracture risk in elderly women followed for 10 years. Osteoporos Int 2016;27:249–255. [PubMed: 26302684]
  • [182] Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 2000;71:743–751.
  • [183] Rocha M, Nava LE, Vázquez de la Torre C, Sánchez-Márin F, Garay-Sevilla ME, Malacara JM. Clinical and radiological improvement of periodontal disease in patients with type 2 diabetes mellitus treated with alendronate: a randomized, placebo-controlled trial. J Periodontol 2001;72:204–209. [PubMed: 11288794]
  • [184] Akram Z, Abduljabbar T, Kellesarian SV, Abu Hassan MI, Javed F, Vohra F. Efficacy of bisphosphonate as an adjunct to nonsurgical periodontal therapy in the management of periodontal disease: a systematic review. Br J Clin Pharmacol 2017;83:444–454. [PubMed: 27718252]
  • [185] Aghaloo TL, Kang B, Sung EC, et al. Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat. J Bone Miner Res 2011;26:1871–1882. [PubMed: 21351151]
  • [186] Diniz-Freitas M, Fernández-Feijoo J, Diz Dios P, Pousa X, Limeres J. Denosumab-related osteonecrosis of the jaw following non-surgical periodontal therapy: A case report. J Clin Periodontol 2018;45:570–577. [PubMed: 29479739] [187] Barros SP, Silva MA, Somerman MJ, Nociti FH Jr. Parathyroid hormone protects against periodontitis- associated bone loss. J Dent Res 2003;82:791–795. [PubMed: 14514758]
  • [188] Kim JH, Kim AR, Choi YH, et al. Intermittent PTH administration improves alveolar bone formation in type 1 diabetic rats with periodontitis. J Transl Med 2018;16:70. [PubMed: 29544500]
  • [189] Yamashita J The therapeutic potential of parathyroid hormone in dental and oral medicine. Oral Sci Int 2020;17:3–14.
  • [190] Taut AD, Jin Q, Chung J-H, et al. Sclerostin antibody stimulates bone regeneration after experimental periodontitis. J Bone Miner Res 2013;28:2347–2356. [PubMed: 23712325]
  • [191] Yao Y, Kauffmann F, Maekawa S, et al. Sclerostin antibody stimulates periodontal regeneration in large alveolar bone defects. Sci Rep 2020;10:16217. [PubMed: 33004873]
  • [192] Chen H, Xu X, Liu M, et al. Sclerostin antibody treatment causes greater alveolar crest height and bone mass in an ovariectomized rat model of localized periodontitis. Bone 2015;76:141–148. [PubMed: 25868799]
  • [193] Yu SH, Hao J, Fretwurst T, et al. Sclerostin-Neutralizing Antibody Enhances Bone Regeneration Around Oral Implants. Tissue Eng Part A 2018;24:1672–1679. [PubMed: 29921173]

Osteoporoz ve Periodontal Hastalıklar Arasındaki İlişki Üzerine Derleme

Yıl 2024, , 142 - 164, 22.04.2024
https://doi.org/10.22312/sdusbed.1398573

Öz

Periodontitis ve osteoporoz, yaşlanan nüfus için önemli halk sağlığı sorunları oluşturan yaygın inflamasyonla ilişkili durumlardır. Periodontal hastalıklar, ağırlıklı olarak dento-gingival dokulardaki disbiyozis ve inflamatuvar nitelikli bir dizi bozukluktan oluşur. Osteoporoz, artan kırık riski ile birlikte kemik mineral yoğunluğu (KMY)’ nun ve yapısının bozulması ile karakterize, yaşa bağlı bir kemik hastalığıdır. Bu derlemede, osteoporoz ve periodontitis arasındaki ilişki hakkında bir güncelleme sağlamak için son 25 yıldaki literatür değerlendirilip, bunların mekanistik bağlantılarının, ortak risk faktörlerinin ve terapötik etkilerinin tartışılması amaçlanmaktadır. Sistemik ve alveolar kemik kaybı (AKK) arasındaki ilişkiyi inceleyen klinik çalışmalarda, 1996-2020 yılları arasındaki 10 araştırma, KMY ile AKK arasında ters bir korelasyon olduğunu ortaya koymuştur. Alveolar kemik kaybının radyografik olarak değerlendirilmesi önemli bir kriter olsa da, klinik ataçman kaybı (KAK); hastanın yaşamı boyunca periodontitis prognozunu yansıtan, teşhisi ve evrelendirilmesi için kritik bir ölçümdür. 1995-2020 yılları arasındaki 23 çalışmadan 17'si KAS ile osteoporoz arasında anlamlı bir ilişki olduğunu ortaya koymuştur. Her iki hastalıkta yaşa bağlı oksidatif stres ve yaşlanma, proinflamatuvar doku mikroçevresini yönlendiren ve kemik yeniden şekillenme sürecinin bozulmasına neden olan altta yatan mekanizmalardır. D vitamini eksikliği ve sigara kullanımı gibi ortak risk faktörleri bu mekanistik ilişkide önemli rol oynamaktadır. Bu faktörlerin ve aralarındaki etkileşimin anlaşılması, disiplinler arası yönetimi ve her iki hastalığa yönelik potansiyel terapötikleri incelemek için iyi kontrollü uzun dönem çalışmalar yapılmasını gerektirmektedir.

Etik Beyan

Etik onay gerekli değildir.

Destekleyen Kurum

Destekleyen kurum yoktur.

Kaynakça

  • [1] Demmer RT, Papapanou PN. Epidemiologic patterns of chronic and aggressive periodontitis. Periodontol 2000 2010;53:28–44. [PubMed: 20403103]
  • [2] American Academy of Periodontology Task Force Report on the Update to the 1999 Classification of Periodontal Diseases and Conditions. J Periodontol 1999;2015(86):835–838.
  • [3] Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol 1996;67:1041–1049.
  • [4] Reginster JY, Burlet N. Osteoporosis: a still increasing prevalence. Bone 2006;38:S4–9. [PubMed: 16455317]
  • [5] Kawai M, Modder UI, Khosla S, Rosen CJ. Emerging therapeutic opportunities for skeletal restoration. Nat Rev Drug Discov 2011;10:141–156. [PubMed: 21283108]
  • [6] Groen JJ, Duyvensz F, Halsted JA. Diffuse alveolar atrophy of the jaw (non-inflammatory form of paradental disease) and pre-senile osteoporosis. Gerontol Clin 1960;2:68–86.
  • [7] Armitage GC. Development of a classification system for periodontal diseases and conditions. Northwest Dent 2000;79:31–35. [PubMed: 11413609]
  • [8] Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol 2018;89(Suppl 1):S159–s172. [PubMed: 29926952]
  • [9] Caton JG, Armitage G, Berglundh T, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Periodontol 2018;89(Suppl 1):s1–s8. [PubMed: 29926946]
  • [10] Albandar JM, Susin C, Hughes FJ. Manifestations of systemic diseases and conditions that affect the periodontal attachment apparatus: Case definitions and diagnostic considerations. J Periodontol 2018;89(Suppl 1):s183–s203. [PubMed: 29926941]
  • [11] Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol 2018;45:S162–S170. [PubMed: 29926490]
  • [12] Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet (London, England) 2002;359:1929–1936.
  • [13] Yu B, Wang CY. Osteoporosis and periodontal diseases - An update on their association and mechanistic links. Periodontol 2000. 2022 Jun;89(1):99-113. doi: 10.1111/prd.12422. Epub 2022 Mar 4. PMID: 35244945; PMCID: PMC9067601.
  • [14] Okabe S, Morimoto Y, Ansai T, et al. Assessment of the relationship between the mandibular cortex on panoramic radiographs and the risk of bone fracture and vascular disease in 80-year-olds. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:433–442. [PubMed: 18299222]
  • [15] Brennan RM, Genco RJ, Hovey KM, Trevisan M, Wactawski-Wende J. Clinical attachment loss, systemic bone density, and subgingival calculus in postmenopausal women. J Periodontol 2007;78:2104–2111. [PubMed: 17970676]
  • [16] Ishii K, Taguchi A, Nakamoto T, et al. Diagnostic efficacy of alveolar bone loss of the mandible for identifying postmenopausal women with femoral osteoporosis. Dentomaxillofac Radiol 2007;36:28–33. [PubMed: 17329585]
  • [17] Taguchi A, Ohtsuka M, Tsuda M, et al. Risk of vertebral osteoporosis in post-menopausal women with alterations of the mandible. Dentomaxillofac Radiol 2007;36:143–148. [PubMed: 17463098]
  • [18] Takaishi Y, Okamoto Y, Ikeo T, et al. Correlations between periodontitis and loss of mandibular bone in relation to systemic bone changes in postmenopausal Japanese women. Osteoporos Int 2005;16:1875–1882. [PubMed: 16027956]
  • [19] Hildebolt CF, Pilgram TK, Yokoyama-Crothers N, et al. The pattern of alveolar crest height change in healthy postmenopausal women after 3 years of hormone/estrogen replacement. Therapy 2002;73:1279–1284.
  • [20] 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 Endodontol 2001;92:346–352. [21] 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. [PubMed: 11022780]
  • [22] Taguchi A, Suei Y, Ohtsuka M, Otani K, Tanimoto K, Hollender LG. Relationship between bone mineral density and tooth loss in elderly Japanese women. Dentomaxillofac Radiol 1999;28:219–223. [PubMed: 10455385]
  • [23] Payne JB, Reinhardt RA, Nummikoski PV, Patil KD. Longitudinal alveolar bone loss in postmenopausal osteoporotic/osteopenic women. Osteoporos Int 1999;10:34–40. [PubMed: 10501777]
  • [24] Hausmann E, Allen K, Carpio L, Christersson LA, Clerehugh V. Computerized methodology for detection of alveolar crestal bone loss from serial intraoral radiographs. J Periodontol 1992;63:657–662. [PubMed: 1507045]
  • [25] von Wowern N Bone mass of mandibles. In vitro and in vivo analyses. Dan Med Bull 1986;33:23–44. [PubMed: 3948537]
  • [26] Horner K, Devlin H, Harvey L. Detecting patients with low skeletal bone mass. J Dent 2002;30:171–175. [PubMed: 12450724]
  • [27] Devlin H, Allen PD, Graham J, et al. Automated osteoporosis risk assessment by dentists: a new pathway to diagnosis. Bone 2007;40:835–842. [PubMed: 17188590]
  • [28] Jonasson G, Sundh V, Hakeberg M, Hassani-Nejad A, Lissner L, Ahlqwist M. Mandibular bone changes in 24 years and skeletal fracture prediction. Clin Oral Invest 2013;17:565–572.
  • [29] Hassani-Nejad A, Ahlqwist M, Hakeberg M, Jonasson G. Mandibular trabecular bone as fracture indicator in 80-year-old men and women. Eur J Oral Sci 2013;121:525–531. [PubMed: 24102691]
  • [30] Lindh C, Horner K, Jonasson G, et al. The use of visual assessment of dental radiographs for identifying women at risk of having osteoporosis: the OSTEODENT project. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:285–293. [PubMed: 18299223]
  • [31] Jonasson G, Jonasson L, Kiliaridis S. Skeletal bone mineral density in relation to thickness, bone mass, and structure of the mandibular alveolar process in dentate men and women. Eur J Oral Sci 2007;115:117–123. [PubMed: 17451501]
  • [32] Lindh C, Obrant K, Petersson A. Maxillary bone mineral density and its relationship to the bone mineral density of the lumbar spine and hip. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;98:102–109. [PubMed: 15243479]
  • [33] Elders PJ, Habets LL, Netelenbos JC, van der Linden LW, van der Stelt PF. The relation between periodontitis and systemic bone mass in women between 46 and 55 years of age. J Clin Periodontol 1992;19:492–496. [PubMed: 1430285]
  • [34] Jacobs R, Ghyselen J, Koninckx P, van Steenberghe D. Long-term bone mass evaluation of mandible and lumbar spine in a group of women receiving hormone replacement therapy. Eur J Oral Sci 1996;104:10–16. [PubMed: 8653490]
  • [35] Buyukkaplan US, Tonguc MO, Guldag MU, Yildiz M, Gumus BA. Comparison of mandibular bone mineral densities in dentate and edentulous patients. J Prosthodont. 2013 Jan;22(1):23-7. doi: 10.1111/j.1532- 849X.2012.00908.x. Epub 2012 Sep 4. PMID: 22946895
  • [36] Mashalkar VN, Suragimath G, Zope SA, Varma SA. A cross-sectional study to assess and correlate osteoporosis and periodontitis among postmenopausal women: a dual energy X-ray absorptiometry study. J Mid- Life Health 2018;9:2–7.
  • [37] Passos-Soares JS, Vianna MIP, Gomes-Filho IS, et al. Association between osteoporosis treatment and severe periodontitis in post-menopausal women. Menopause (New York, NY) 2017;24:789–795.
  • [38] Penoni DC, Torres SR, Farias ML, Fernandes TM, Luiz RR, Leão AT. Association of osteoporosis and bone medication with the periodontal condition in elderly women. Osteoporos Int 2016;27:1887–1896. [PubMed: 26626187]
  • [39] Juluri R, Prashanth E, Gopalakrishnan D, et al. Association of post-menopausal osteoporosis and periodontal disease: a double-blind case-control study. J Int Oral Health 2015;7:119–123. [40] Singh A, Sharma RK, Siwach RC, Tewari S, Narula SC. Association of bone mineral density with periodontal status in postmeno-pausal women. J Invest Clin Dent 2014;5:275–282.
  • [41] Tak I-H, Shin M-H, Kweon S-S, et al. The association between periodontal disease, tooth loss and bone mineral density in a Korean population. J Clin Periodontol 2014;41:1139–1144. [PubMed: 25207848]
  • [42] Gondim V, Aun J, Fukuda CT, et al. Severe loss of clinical attachment level: an independent association with low hip bone mineral density in postmenopausal females. J Periodontol 2013;84:352–359. [PubMed: 22548585]
  • [43] Passos JS, Vianna MI, Gomes-Filho IS, et al. Osteoporosis/osteopenia as an independent factor associated with periodontitis in postmenopausal women: a case-control study. Osteoporos Int 2013;24:1275–1283. [PubMed: 23001114]
  • [44] Iwasaki M, Taylor GW, Nakamura K, Yoshihara A, Miyazaki H. Association between low bone mineral density and clinical attachment loss in Japanese postmenopausal females. J Periodontol 2013;84:1708–1716. [PubMed: 23451986]
  • [45] Marjanovic EJ, Southern HN, Coates P, et al. Do patients with osteoporosis have an increased prevalence of periodontal disease? A cross-sectional study. Osteoporos Int 2013;24:1973–1979. [PubMed: 23340948]
  • [46] Moeintaghavi A, Pourjavad M, Dadgar S, Tabbakh NS. Evaluation of the association between periodontal parameters, osteoporosis and osteopenia in post menopausal women. J Dent (Tehran, Iran) 2013;10:443–448.
  • [47] Grocholewicz K, Bohatyrewicz A. Oral health and bone mineral density in postmenopausal women. Arch Oral Biol 2012;57:245–251. [PubMed: 22153129]
  • [48] Al Habashneh R, Alchalabi H, Khader YS, Hazza’a AM, Odat Z, Johnson GK. Association between periodontal disease and osteoporosis in postmenopausal women in Jordan. J Periodontol 2010;81:1613– 1621. [PubMed: 20681809]
  • [49] Gomes-Filho IS, Passos JDS, Cruz SS, et al. The association between postmenopausal osteoporosis and periodontal disease. J Periodontol 2007;78:1731–1740. [PubMed: 17760543]
  • [50] Taguchi A, Fujiwara S, Masunari N, Suzuki G. Self-reported number of remaining teeth is associated with bone mineral density of the femoral neck, but not of the spine, in Japanese men and women. Osteoporos Int 2004;15:842–846. [PubMed: 14991229]
  • [51] 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. [PubMed: 12873107]
  • [52] Pilgram TK, Hildebolt CF, Dotson M, et al. Relationships between clinical attachment level and spine and hip bone mineral density: data from healthy postmenopausal women. J Periodontol 2002;73:298–301. [PubMed: 11922259]
  • [53] Lundström A, Jendle J, Stenström B, Toss G, Ravald N. Periodontal conditions in 70-year-old women with osteoporosis. Swed Dent J 2001;25:89–96. [PubMed: 11813450]
  • [54] 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. [PubMed: 10505800]
  • [55] Mohammad AR, Bauer RL, Yeh CK. Spinal bone density and tooth loss in a cohort of postmenopausal women. Int J Prosthodont 1997;10:381–385. [PubMed: 9484049]
  • [56] Hildebolt CF, Pilgram TK, Dotson M, et al. Attachment loss with postmenopausal age and smoking. J Periodont Res 1997;32:619–625.
  • [57] Mohammad AR, Brunsvold M, Bauer R. The strength of association between systemic postmenopausal osteoporosis and periodontal disease. Int J Prosthodont 1996;9:479–483. [PubMed: 9108750]
  • [58] Penoni DC, Fidalgo TK, Torres SR, et al. Bone density and clinical periodontal attachment in postmenopausal women: a systematic review and meta-analysis. J Dent Res 2017;96:261–269. [PubMed: 28048966]
  • [59] Martínez-Maestre M, González-Cejudo C, Machuca G, Torrejón R, Castelo-Branco C. Periodontitis and osteoporosis: a systematic review. Climacteric 2010;13:523–529. [PubMed: 20690866] [60] Oztürk Tonguç M, Büyükkaplan US, Fentoglu O, Gümüs BA, Çerçi SS, Kirzioglu FY. Comparison of bone mineral density in the jaws of patients with and without chronic periodontitis. Dentomaxillofac Radiol. 2012 Sep;41(6):509-14. doi: 10.1259/dmfr/21900076. Epub 2012 Jan 12. PMID: 22241867; PMCID: PMC3520387).
  • [61] Nicopoulou-Karayianni K, Tzoutzoukos P, Mitsea A, et al. Tooth loss and osteoporosis: the OSTEODENT study. J Clin Periodontol 2009;36:190–197. [PubMed: 19236531]
  • [62] Krall EA, Garcia RI, Dawson-Hughes B. Increased risk of tooth loss is related to bone loss at the whole body, hip, and spine. Calcif Tissue Int 1996;59:433–437. [PubMed: 8939767]
  • [63] Drozdzowska B, Pluskiewicz W, Michno M. Tooth count in elderly women in relation to their skeletal status. Maturitas 2006;55:126–131. [PubMed: 16822625]
  • [64] Krall EA, Dawson-Hughes B, Papas A, Garcia RI. Tooth loss and skeletal bone density in healthy postmenopausal women. Osteoporos Int 1994;4:104–109. [PubMed: 8003839]
  • [65] May H, Reader R, Murphy S, Khaw KT. Self-reported tooth loss and bone mineral density in older men and women. Age Ageing 1995;24:217–221. [PubMed: 7645442]
  • [66] Hajishengallis G Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 2014;35:3–11. [PubMed: 24269668]
  • [67] Yu B, Wang C-Y. Osteoporosis: the result of an ‘aged’ bone micro-environment. Trends Mol Med 2016;22:641–644. [PubMed: 27354328]
  • [68] Graves D Cytokines that promote periodontal tissue destruction. J Periodontol 2008;79:1585–1591. [PubMed: 18673014]
  • [69] Sczepanik FSC, Grossi ML, Casati M, et al. Periodontitis is an inflammatory disease of oxidative stress: We should treat it that way. Periodontol 2000 2020;84:45–68. [PubMed: 32844417]
  • [70] Mahanonda R, Pichyangkul S. Toll-like receptors and their role in periodontal health and disease. Periodontol 2000 2007;43(1):41–55. [PubMed: 17214834]
  • [71] Kawai T, Matsuyama T, Hosokawa Y, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 2006;169:987–998. [PubMed: 16936272]
  • [72] Pacios S, Xiao W, Mattos M, et al. Osteoblast lineage cells play an essential role in periodontal bone loss through activation of nuclear factor-kappa B. Sci Rep 2015;5:16694. [PubMed: 26666569]
  • [73] Chang J, Wang Z, Tang E, et al. Inhibition of osteoblastic bone formation by nuclear factor-kappaB. Nat Med 2009;15:682–689. [PubMed: 19448637]
  • [74] Jimi E, Aoki K, Saito H, et al. Selective inhibition of NF-[kappa] B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat Med 2004;10:617–624. [PubMed: 15156202]
  • [75] Redlich K, Görtz B, Hayer S, et al. Repair of local bone erosions and reversal of systemic bone loss upon therapy with anti-tumor necrosis factor in combination with osteoprotegerin or parathy-roid hormone in tumor necrosis factor-mediated arthritis. Am J Pathol 2004;164:543–555. [PubMed: 14742260]
  • [76] Haugeberg G, Conaghan PG, Quinn M, Emery P. Bone loss in patients with active early rheumatoid arthritis: infliximab and methotrexate compared with methotrexate treatment alone. Explorative analysis from a 12-month randomised, double-blind, placebo-controlled study. Ann Rheum Dis 2009;68:1898–1901. [PubMed: 19386610]
  • [77] Ghosh S, Karin M. Missing Pieces in the NF-κB Puzzle. Cell 2002;109(2):S81–S96. [PubMed: 11983155]
  • [78] Wang CY, Guttridge DC, Mayo MW, Baldwin AS Jr. NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to prefer-entially suppress chemotherapy-induced apoptosis. Mol Cell Biol 1999;19:5923–5929. [PubMed: 10454539]
  • [79] Wang CY, Mayo MW, Baldwin AS Jr. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996;274:784–787. [PubMed: 8864119]
  • [80] Lee HJ, Kang IK, Chung CP, Choi SM. The subgingival microflora and gingival crevicular fluid cytokines in refractory periodontitis. J Clin Periodontol 1995;22:885–890. [PubMed: 8550866]
  • [81] Delima AJ, Karatzas S, Amar S, Graves DT. Inflammation and tissue loss caused by periodontal pathogens is reduced by interleukin-1 antagonists. J Infect Dis 2002;186:511–516. [PubMed: 12195378] [82] Chiang CY, Kyritsis G, Graves DT, Amar S. Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide. Infect Immun 1999;67:4231–4236. [PubMed: 10417196]
  • [83] Dayan S, Stashenko P, Niederman R, Kupper TS. Oral epithelial overexpression of IL-1alpha causes periodontal disease. J Dent Res 2004;83:786–790. [PubMed: 15381720]
  • [84] Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 2000;106:1481– 1488. [PubMed: 11120755]
  • [85] Pacifici R, Rifas L, McCracken R, Avioli LV. The role of interleukin-1 in postmenopausal bone loss. Exp Gerontol 1990;25:309–316. [PubMed: 2226666]
  • [86] Barbour KE, Lui LY, Ensrud KE, et al. Inflammatory markers and risk of hip fracture in older white women: the study of osteoporotic fractures. J Bone Mineral Res 2014;29:2057–2064. [87] Pacifici R Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J Bone Mineral Res 1996;11:1043–1051.
  • [88] Hajishengallis G, Reis ES, Mastellos DC, Ricklin D, Lambris JD. Novel mechanisms and functions of complement. Nat Immunol 2017;18:1288–1298. [PubMed: 29144501]
  • [89] Zhang X, Kimura Y, Fang C, et al. Regulation of Toll-like receptor–mediated inflammatory response by complement in vivo. Blood 2007;110:228–236. [PubMed: 17363730]
  • [90] Hajishengallis G, Kajikawa T, Hajishengallis E, et al. Complement-dependent mechanisms and interventions in periodontal disease. Front Immunol 2019;10. doi:10.3389/fimmu.2019.00406 [PubMed: 30723470]
  • [91] Courts FJ, Boackle RJ, Fudenberg HH, Silverman M. Detection of functional complement components in gingival crevicular fluid from humans with periodontal disease. J Dent Res 1977;56:327–331. [PubMed: 323317]
  • [92] Patters M, Niekrash C, Lang NP. Assessment of complement cleavage in gingival fluid during experimental gingivitis in man. J Clin Periodontol 1989;16:33–37. [PubMed: 2644312]
  • [93] Niekrash CE, Patters MR. Simultaneous assessment of complement components C3, C4, and B and their cleavage products in human gingival fluid: II. Longitudinal changes during periodontal therapy. J Periodontal Res 1985;20:268–275. [PubMed: 3160842]
  • [94] Maekawa T, Abe T, Hajishengallis E, et al. Genetic and intervention studies implicating complement C3 as a major target for the treatment of periodontitis. J Immunol 2014;192:6020. [PubMed: 24808362]
  • [95] MacKay DL, Kean TJ, Bernardi KG, et al. Reduced bone loss in a murine model of postmenopausal osteoporosis lacking complement component 3. J Orthopaedic Res 2018;3(36):118–128.
  • [96] Matsuo K, Owens JM, Tonko M, Elliott C, Chambers TJ, Wagner EF. Fosl1 is a transcriptional target of c-Fos during osteoclast differentiation. Nat Genet 2000;24:184–187. [PubMed: 10655067]
  • [97] Redlich K, Smolen JS. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nat Rev Drug Discov 2012;11:234–250. [PubMed: 22378270]
  • [98] Takayanagi H, Kim S, Koga T, et al. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 2002;3:889–901. [PubMed: 12479813]
  • [99] Teitelbaum SL. Osteoclasts: what do they do and how do they do it? Am J Pathol 2007;170:427–435. [PubMed: 17255310]
  • [100] Lee SK, Lorenzo JA. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology 1999;140:3552–3561. [PubMed: 10433211]
  • [101] Horwood NJ, Elliott J, Martin TJ, Gillespie MT. Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 1998;139:4743–4746. [PubMed: 9794488]
  • [102] Han JH, Choi SJ, Kurihara N, Koide M, Oba Y, Roodman GD. Macrophage inflammatory protein-1alpha is an osteoclastogenic factor in myeloma that is independent of receptor activator of nuclear factor kappaB ligand. Blood 2001;97:3349–3353. [PubMed: 11369623] [103] Gilbert L, He X, Farmer P, et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2αA) is inhibited by tumor necrosis factor-α. J Biol Chem 2002;277:2695–2701. [PubMed: 11723115]
  • [104] Kaneki H, Guo R, Chen D, et al. Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J Biol Chem 2006;281:4326–4333. [PubMed: 16373342]
  • [105] Chang J, Liu F, Lee M, et al. NF-kappaB inhibits osteogenic differentiation of mesenchymal stem cells by promoting beta-catenin degradation. Proc Natl Acad Sci USA 2013;110:9469–9474. [PubMed: 23690607]
  • [106] Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007;13:156–163. [PubMed: 17237793]
  • [107] Li X, Zhang Y, Kang H, et al. Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem 2005;280:19883–19887. [PubMed: 15778503]
  • [108] Mundy GR. Osteoporosis and inflammation. Nutr Rev 2007;65:S147–S151. [PubMed: 18240539]
  • [109] Ginaldi L, Di Benedetto M, De Martinis M. Osteoporosis, inflammation and ageing. Immun Ageing 2005;2:14. [PubMed: 16271143]
  • [110] Lin CL, Moniz C, Chambers TJ, Chow JW. Colitis causes bone loss in rats through suppression of bone formation. Gastroenterology 1996;111:1263–1271. [PubMed: 8898640]
  • [111] Khosla S, Melton LJ 3rd, Riggs BL. The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Mineral Res 2011;26:441–451.
  • [112] López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013;153:1194– 1217. [PubMed: 23746838]
  • [113] Manolagas SC, Parfitt AM. What old means to bone. Trends Endocrinol Metab 2010;21:369–374. [PubMed: 20223679]
  • [114] Tilstra JS, Robinson AR, Wang J, et al. NF-κB inhibition delays DNA damage–induced senescence and aging in mice. J Clin Investig 2012;122:2601–2612. [PubMed: 22706308]
  • [115] Yu B, Huo L, Liu Y, et al. PGC-1α controls skeletal stem cell fate and bone-fat balance in osteoporosis and skeletal aging by inducing TAZ. Cell Stem Cell 2018;23:193–209.e195. [PubMed: 30017591]
  • [116] Persson GR. Periodontal complications with age. Periodontol 2000 2018;78(1):185–194. [PubMed: 30198125]
  • [117] Papapanou PN, Lindhe J. Preservation of probing attachment and alveolar bone levels in 2 random population samples. J Clin Periodontol 1992;19:583–588. [PubMed: 1447383]
  • [118] Hajishengallis G Aging and its impact on innate immunity and inflammation: implications for periodontitis. J Oral Biosci 2014;56:30–37. [PubMed: 24707191]
  • [119] Wu Y, Dong G, Xiao W, et al. Effect of aging on periodontal inflammation, microbial colonization, and disease susceptibility. J Dent Res 2016;95:460–466. [PubMed: 26762510]
  • [120] Bodineau A, Folliguet M, Séguier S. Tissular senescence and modifications of oral ecosystem in the elderly: risk factors for mucosal pathologies. Curr Aging Sci 2009;2:109–120. [PubMed: 20021405]
  • [121] Fransson C, Mooney J, Kinane DF, Berglundh T. Differences in the inflammatory response in young and old human subjects during the course of experimental gingivitis. J Clin Periodontol 1999;26:453–460. [PubMed: 10412850]
  • [122] Ebersole JL, Steffen MJ, Gonzalez-Martinez J, Novak MJ. Effects of age and oral disease on systemic inflammatory and immune parameters in nonhuman primates. Clin Vaccine Immunol CVI 2008;15:1067–1075. [PubMed: 18448617]
  • [123] Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocrinol Rev 2010;31:266–300.
  • [124] Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003;112:481–490. [PubMed: 12600312] [125] Almeida M, Han L, Martin-Millan M, et al. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 2007;282:27285–27297. [PubMed: 17623659]
  • [126] Goettsch C, Babelova A, Trummer O, et al. NADPH oxidase 4 limits bone mass by promoting osteoclastogenesis. J Clin Invest 2013;123:4731–4738. [PubMed: 24216508]
  • [127] Lean JM, Davies JT, Fuller K, et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J Clin Invest 2003;112:915–923. [PubMed: 12975476]
  • [128] Bartell SM, Kim H-N, Ambrogini E, et al. FoxO proteins restrain osteoclastogenesis and bone resorption by attenuating H2O2 accumulation. Nat Commun 2014;5:3773. [PubMed: 24781012]
  • [129] Ambrogini E, Almeida M, Martin-Millan M, et al. FoxO-mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab 2010;11:136–146. [PubMed: 20142101]
  • [130] Cervellati C, Bonaccorsi G, Cremonini E, et al. Oxidative stress and bone resorption interplay as a possible trigger for postmenopausal osteoporosis. Biomed Res Int 2014;2014:569563. [PubMed: 24524081]
  • [131] Chapple IL, Matthews J. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007;43:160–232. [PubMed: 17214840]
  • [132] Löe H Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329–334. [PubMed: 8422804]
  • [133] Aquino-Martinez R, Rowsey JL, Fraser DG, et al. LPS-induced premature osteocyte senescence: Implications in inflammatory alveolar bone loss and periodontal disease pathogenesis. Bone 2020;132:115220. [PubMed: 31904537]
  • [134] Baker DJ, Wijshake T, Tchkonia T, et al. Clearance of p16Ink4a-positive senescent cells delays ageing- associated disorders. Nature 2011;479:232–236. [PubMed: 22048312]
  • [135] Farr JN, Xu M, Weivoda MM, et al. Targeting cellular senescence prevents age-related bone loss in mice. Nat Med 2017;23:1072–1079. [PubMed: 28825716]
  • [136] Palmer AK, Tchkonia T, LeBrasseur NK, Chini EN, Xu M, Kirkland JL. Cellular senescence in type 2 diabetes: a therapeutic opportunity. Diabetes 2015;64:2289–2298. [PubMed: 26106186]
  • [137] Zhou Bo O, Yue R, Murphy Malea M, Peyer JG, Morrison SJ. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 2014;15:154–168. [PubMed: 24953181]
  • [138] Bianco P, Cao X, Frenette PS, et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med 2013;19:35–42. [PubMed: 23296015]
  • [139] Bianco P, Robey PG. Skeletal stem cells. Development 2015;142:1023–1027. [PubMed: 25758217]
  • [140] Oh J, Lee YD, Wagers AJ. Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat Med 2014;20:870. [PubMed: 25100532]
  • [141] Li H, Liu P, Xu S, et al. FOXP1 controls mesenchymal stem cell commitment and senescence during skeletal aging. J Clin Invest 2017;127:1241–1253. [PubMed: 28240601]
  • [142] Liu W, Zhang L, Xuan K, et al. Alpl prevents bone ageing sensitivity by specifically regulating senescence and differentiation in mesenchymal stem cells. Bone Res 2018;6:27. [PubMed: 30210899]
  • [143] Farr JN, Fraser DG, Wang H, et al. Identification of senescent cells in the bone microenvironment. J Bone Miner Res 2016;31:1920–1929. [PubMed: 27341653]
  • [144] Kim HN, Chang J, Iyer S, et al. Elimination of senescent osteoclast progenitors has no effect on the age- associated loss of bone mass in mice. Aging Cell 2019;18:e12923. [PubMed: 30773784]
  • [145] Pignolo RJ, Samsonraj RM, Law SF, Wang H, Chandra A. Targeting cell senescence for the treatment of age-related bone loss. Curr Osteoporos Rep 2019;17:70–85. [PubMed: 30806947]
  • [146] Zhang P, Wang Q, Nie L, et al. Hyperglycemia-induced inflammaging accelerates gingival senescence via NLRC4 phosphorylation. J Biol Chem 2019;294:18807–18819. [PubMed: 31676687] [147] Bischoff-Ferrari HA, Willett WC, Wong JB, Giovannucci E, Dietrich T, Dawson-Hughes B. Fracture prevention with vitamin D supple-mentation: a meta-analysis of randomized controlled trials. J Am Med Assoc 2005;293:2257–2264.
  • [148] Shimazaki Y, Shirota T, Uchida K, et al. Intake of dairy products and periodontal disease: the Hisayama Study. J Periodontol 2008;79:131–137. [PubMed: 18166102]
  • [149] Al-Zahrani MS. Increased intake of dairy products is related to lower periodontitis prevalence. J Periodontol 2006;77:289–294. [PubMed: 16460256]
  • [150] Yoshida T, Stern PH. How vitamin D works on bone. Endocrinol Metab Clin North Am 2012;41:557–569. [PubMed: 22877429]
  • [151] Bischoff-Ferrari HA, Dietrich T, Orav EJ, Dawson-Hughes B. Positive association between 25-hydroxy vitamin D levels and bone mineral density: a population-based study of younger and older adults. Am J Med 2004;116:634–639. [PubMed: 15093761]
  • [152] Laird E, Ward M, McSorley E, Strain JJ, Wallace J. Vitamin D and bone health: potential mechanisms. Nutrients 2010;2:693–724. [PubMed: 22254049]
  • [153] Kliewer SA, Umesono K, Mangelsdorf DJ, Evans RM. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 1992;355:446–449. [PubMed: 1310351]
  • [154] Takahashi N, Udagawa N, Suda T. Vitamin D endocrine system and osteoclasts. Bonekey Rep 2014;3:495. [PubMed: 24605212]
  • [155] Zarei A, Morovat A, Javaid K, Brown CP. Vitamin D receptor expression in human bone tissue and dose- dependent activation in resorbing osteoclasts. Bone Res 2016;4:16030. [PubMed: 27785371]
  • [156] Baldock PA, Thomas GP, Hodge JM, et al. Vitamin D action and regulation of bone remodeling: suppression of osteoclastogenesis by the mature osteoblast. J Bone Miner Res 2006;21:1618–1626. [PubMed: 16995817]
  • [157] Jilka RL, Weinstein RS, Bellido T, Roberson P, Parfitt AM, Manolagas SC. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 1999;104:439–446. [PubMed: 10449436]
  • [158] Müller K, Haahr PM, Diamant M, Rieneck K, Kharazmi A, Bendtzen K. 1,25-Dihydroxyvitamin D3 inhibits cytokine production by human blood monocytes at the post-transcriptional level. Cytokine 1992;4:506–512. [PubMed: 1337987]
  • [159] Inanir A, Ozoran K, Tutkak H, Mermerci B. The effects of calcitriol therapy on serum interleukin-1, interleukin-6 and tumour necrosis factor-alpha concentrations in post-menopausal patients with osteoporosis. J Int Med Res 2004;32:570–582. [PubMed: 15587751]
  • [160] Grossi SG, Genco RJ, Machtei EE, et al. Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol 1995;66:23–29. [PubMed: 7891246]
  • [161] Kanis JA, Johnell O, Oden A, et al. Smoking and fracture risk: a meta-analysis. Osteoporos Int 2005;16:155–162. [PubMed: 15175845]
  • [162] Giannopoulou C, Kamma JJ, Mombelli A. Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J Clin Periodontol 2003;30:145–153. [PubMed: 12622857]
  • [163] Tymkiw KD, Thunell DH, Johnson GK, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol 2011;38:219–228. [PubMed: 21198766]
  • [164] Buduneli N, Buduneli E, Kütükçüler N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. J Periodontol 2009;80:1274–1280. [PubMed: 19656027]
  • [165] César-Neto JB, Duarte PM, de Oliveira MC, Tambeli CH, Sallum EA, Nociti FH Jr. Smoking modulates interleukin-6:interleukin-10 and RANKL:osteoprotegerin ratios in the periodontal tissues. J Periodontal Res 2007;42:184–191. [PubMed: 17305878]
  • [166] Lappin DF, Sherrabeh S, Jenkins WM, Macpherson LM. Effect of smoking on serum RANKL and OPG in sex, age and clinically matched supportive-therapy periodontitis patients. J Clin Periodontol 2007;34:271–277. [PubMed: 17378883] [167] Tang TH, Fitzsimmons TR, Bartold PM. Effect of smoking on concentrations of receptor activator of nuclear factor kappa B ligand and osteoprotegerin in human gingival crevicular fluid. J Clin Periodontol 2009;36:713–718. [PubMed: 19570104]
  • [168] Aziz AS, Kalekar MG, Suryakar AN, et al. Assessment of some bio-chemical oxidative stress markers in male smokers with chronic periodontitis. Indian J Clin Biochem IJCB 2013;28:374–380. [PubMed: 24426240]
  • [169] Fredriksson MI, Figueredo CM, Gustafsson A, Bergström KG, Asman BE. Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. J Periodontol 1999;70:1355–1360. [PubMed: 10588499]
  • [170] Chang CH, Han ML, Teng NC, et al. Cigarette smoking aggravates the activity of periodontal disease by disrupting redox homeostasisan observational study. Sci Rep 2018;8:11055. [PubMed: 30038248]
  • [171] Agnihotri R, Pandurang P, Kamath SU, et al. Association of cigarette smoking with superoxide dismutase enzyme levels in subjects with chronic periodontitis. J Periodontol 2009;80:657–662. [PubMed: 19335086]
  • [172] Al-Bashaireh AM, Haddad LG, Weaver M, Chengguo X, Kelly DL, Yoon S. The effect of tobacco smoking on bone mass: an overview of pathophysiologic mechanisms. J Osteoporos 2018;2018:1206235. [PubMed: 30631414]
  • [173] Reddy MS, Morgan SL. Decreased bone mineral density and periodontal management. Periodontol 2000 2013;61:195–218. [PubMed: 23240950]
  • [174] Penoni DC, Vettore MV, Torres SR, Farias MLF, Leão ATT. An investigation of the bidirectional link between osteoporosis and periodontitis. Arch Osteoporos 2019;14:94. [PubMed: 31444638]
  • [175] Passos-Soares JDS, Vianna MIP, Gomes-Filho IS, et al. Association between osteoporosis treatment and severe periodontitis in post-menopausal women. Menopause 2017;24:789–795. [PubMed: 28225430]
  • [176] Krall EA, Dawson-Hughes B, Hannan MT, Wilson PW, Kiel DP. Postmenopausal Estrogen Replacement and Tooth Retention. The Am J Med 1997;102(6):536–542. [PubMed: 9217668]
  • [177] Garcia MN, Hildebolt CF, Miley DD, et al. One-year effects of vitamin D and calcium supplementation on chronic periodontitis. J Periodontol 2011;82:25–32. [PubMed: 20809866]
  • [178] Dixon D, Hildebolt CF, Miley DD, et al. Calcium and vitamin D use among adults in periodontal disease maintenance programmes. Br Dent J 2009;206:627–631. [PubMed: 19557061]
  • [179] Millen AE, Andrews CA, LaMonte MJ, et al. Vitamin D status and 5-year changes in periodontal disease measures among post-menopausal women: the Buffalo OsteoPerio Study. J Periodontol 2014;85:1321–1332. [PubMed: 24794688]
  • [180] Pavlesen S, Mai X, Wactawski-Wende J, et al. Vitamin D status and tooth loss in postmenopausal females: the buffalo osteoporosis and periodontal disease (OsteoPerio) study. J Periodontol 2016;87:852–863. [PubMed: 27086615]
  • [181] Thorin MH, Wihlborg A, Åkesson K, Gerdhem P. Smoking, smoking cessation, and fracture risk in elderly women followed for 10 years. Osteoporos Int 2016;27:249–255. [PubMed: 26302684]
  • [182] Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 2000;71:743–751.
  • [183] Rocha M, Nava LE, Vázquez de la Torre C, Sánchez-Márin F, Garay-Sevilla ME, Malacara JM. Clinical and radiological improvement of periodontal disease in patients with type 2 diabetes mellitus treated with alendronate: a randomized, placebo-controlled trial. J Periodontol 2001;72:204–209. [PubMed: 11288794]
  • [184] Akram Z, Abduljabbar T, Kellesarian SV, Abu Hassan MI, Javed F, Vohra F. Efficacy of bisphosphonate as an adjunct to nonsurgical periodontal therapy in the management of periodontal disease: a systematic review. Br J Clin Pharmacol 2017;83:444–454. [PubMed: 27718252]
  • [185] Aghaloo TL, Kang B, Sung EC, et al. Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat. J Bone Miner Res 2011;26:1871–1882. [PubMed: 21351151]
  • [186] Diniz-Freitas M, Fernández-Feijoo J, Diz Dios P, Pousa X, Limeres J. Denosumab-related osteonecrosis of the jaw following non-surgical periodontal therapy: A case report. J Clin Periodontol 2018;45:570–577. [PubMed: 29479739] [187] Barros SP, Silva MA, Somerman MJ, Nociti FH Jr. Parathyroid hormone protects against periodontitis- associated bone loss. J Dent Res 2003;82:791–795. [PubMed: 14514758]
  • [188] Kim JH, Kim AR, Choi YH, et al. Intermittent PTH administration improves alveolar bone formation in type 1 diabetic rats with periodontitis. J Transl Med 2018;16:70. [PubMed: 29544500]
  • [189] Yamashita J The therapeutic potential of parathyroid hormone in dental and oral medicine. Oral Sci Int 2020;17:3–14.
  • [190] Taut AD, Jin Q, Chung J-H, et al. Sclerostin antibody stimulates bone regeneration after experimental periodontitis. J Bone Miner Res 2013;28:2347–2356. [PubMed: 23712325]
  • [191] Yao Y, Kauffmann F, Maekawa S, et al. Sclerostin antibody stimulates periodontal regeneration in large alveolar bone defects. Sci Rep 2020;10:16217. [PubMed: 33004873]
  • [192] Chen H, Xu X, Liu M, et al. Sclerostin antibody treatment causes greater alveolar crest height and bone mass in an ovariectomized rat model of localized periodontitis. Bone 2015;76:141–148. [PubMed: 25868799]
  • [193] Yu SH, Hao J, Fretwurst T, et al. Sclerostin-Neutralizing Antibody Enhances Bone Regeneration Around Oral Implants. Tissue Eng Part A 2018;24:1672–1679. [PubMed: 29921173]
Toplam 183 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Konular Periodontoloji
Bölüm Derlemeler
Yazarlar

Rabia Karaaslan 0009-0008-6823-1477

Nilsun Bağış 0000-0003-4301-8502

Özlem Fentoğlu 0000-0003-2138-2004

Yayımlanma Tarihi 22 Nisan 2024
Gönderilme Tarihi 2 Aralık 2023
Kabul Tarihi 17 Ocak 2024
Yayımlandığı Sayı Yıl 2024

Kaynak Göster

Vancouver Karaaslan R, Bağış N, Fentoğlu Ö. Osteoporoz ve Periodontal Hastalıklar Arasındaki İlişki Üzerine Derleme. Süleyman Demirel Üniversitesi Sağlık Bilimleri Dergisi. 2024;15(1):142-64.

Cc-by-nc-nd-icon-svg

Creative Commons Attribution 4.0 International License 

Atıf gereklidir, ticari olmayan amaçlarla kullanılabilir ve değişiklik yapılarak türev eser üretilemez.