{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T22:34:46Z","timestamp":1794004486085,"version":"4.8.0"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T00:00:00Z","timestamp":1774224000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T00:00:00Z","timestamp":1774224000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100009042","name":"Universidad de Sevilla","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100009042","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Clin Oral Invest"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Objectives<\/jats:title>\n                    <jats:p>To investigate whether menopause is associated with adverse clinical periodontal outcomes by systematically comparing postmenopausal and premenopausal women.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Materials and methods<\/jats:title>\n                    <jats:p>A systematic review of observational studies was conducted following PRISMA guidelines. Electronic databases were searched up to March 2025 March 2025 for observational studies reporting clinical periodontal parameters in postmenopausal women not undergoing hormone replacement therapy. Risks of bias and certainty of evidence were assessed using ROBINS-I and GRADE frameworks.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Nine studies met inclusion criteria. Postmenopausal women showed greater clinical attachment loss, increased probing depths, and more pronounced signs of inflammation. However, the certainty of evidence was rated as moderate to low, mainly due to methodological variability.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>While the observed trends suggest that menopause is a clinically relevant factor in periodontal health, the current evidence base is weak. High-quality prospective studies are urgently needed to confirm these findings before informing clinical practice or developing new guidelines.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Clinical relevance<\/jats:title>\n                    <jats:p>Findings contribute to the current understanding of systemic influences on periodontal disease, with relevance to aging, women\u2019s health, and menopause as a physiological stage of life.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1007\/s00784-026-06813-y","type":"journal-article","created":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T07:46:18Z","timestamp":1774251978000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Impact of menopause on clinical periodontal outcomes: a systematic review"],"prefix":"10.1007","volume":"30","author":[{"given":"Fabiola Civiletto-S.","family":"Mart\u00edn","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria J.","family":"Rus","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela","family":"de la Cruz G\u00e1ndara Alvarez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aurea","family":"Simon-Soro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cristiane","family":"Cantiga-Silva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,3,23]]},"reference":[{"key":"6813_CR1","doi-asserted-by":"publisher","first-page":"17038","DOI":"10.1038\/nrdp.2017.38","volume":"3","author":"DF Kinane","year":"2017","unstructured":"Kinane DF, Stathopoulou PG, Papapanou PN (2017) Periodontal diseases. Nat Rev Dis Primers 3:17038. https:\/\/doi.org\/10.1038\/nrdp.2017.38","journal-title":"Nat Rev Dis Primers"},{"key":"6813_CR2","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/s40496-022-00313-2","volume":"9","author":"F Sayar","year":"2022","unstructured":"Sayar F, Buduneli N (2022) Impact of menopause on periodontal tissues. Curr Oral Health Rep 9:107\u2013112. https:\/\/doi.org\/10.1007\/s40496-022-00313-2","journal-title":"Curr Oral Health Rep"},{"issue":"5","key":"6813_CR3","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1016\/j.jdent.2012.01.013","volume":"40","author":"C Bab\u00fcr","year":"2012","unstructured":"Bab\u00fcr C, Ozcan G, Cebi DU, Pervane B, Ozdemir B, Y\u00fccel A, Biri AA, Bab\u00fcr C (2012) Gingival crevicular fluid levels of osteoprotegerin (OPG) in premenopausal and postmenopausal women with or without chronic periodontitis. J Dent 40(5):364\u2013371. https:\/\/doi.org\/10.1016\/j.jdent.2012.01.013","journal-title":"J Dent"},{"issue":"5","key":"6813_CR4","doi-asserted-by":"publisher","first-page":"ZC10","DOI":"10.7860\/JCDR\/2018\/32504.11488","volume":"12","author":"P Agrawal","year":"2018","unstructured":"Agrawal P, Sanikop S, Patil S, Agrawal P, Agrawal A, Malleshappa A (2018) Estimation of salivary tumour necrosis factor-\u03b1 levels in post-menopausal women with chronic periodontitis. J Clin Diagn Res 12(5):ZC10\u2013ZC14. https:\/\/doi.org\/10.7860\/JCDR\/2018\/32504.11488","journal-title":"J Clin Diagn Res"},{"issue":"3","key":"6813_CR5","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1002\/JPER.23-0124","volume":"95","author":"N Yakar","year":"2024","unstructured":"Yakar N, Bostanci N, \u00d6zdemir G, Atmaca H, T\u00fcredi A, \u015eahin \u00c7, K\u00f6se T, Emingil G (2024) Salivary inflammatory burden in pre- and postmenopausal women: associations with body mass index, patient-reported health, serum cytokines, and periodontal parameters. J Periodontol 95(3):209\u2013218. https:\/\/doi.org\/10.1002\/JPER.23-0124","journal-title":"J Periodontol"},{"issue":"9","key":"6813_CR6","doi-asserted-by":"publisher","first-page":"3972","DOI":"10.13040\/IJPSR.0975-8232.5(9).3972-76","volume":"5","author":"KE Thomas","year":"2014","unstructured":"Thomas KE (2014) Prevalence of chronic periodontitis among postmenopausal women: hormone replacement therapy a remedy? Int J Pharm Sci Res 5(9):3972\u20133976. https:\/\/doi.org\/10.13040\/IJPSR.0975-8232.5(9).3972-76","journal-title":"Int J Pharm Sci Res"},{"issue":"1","key":"6813_CR7","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1002\/JPER.24-0267","volume":"96","author":"N Yakar","year":"2025","unstructured":"Yakar N, Yilmaz B, Emingil G, Chen T, Ozdemir G, Kantarci A (2025) Subgingival microbial profiles in pre- and postmenopausal women: associations with serum estradiol levels. J Periodontol 96(1):97\u2013108. https:\/\/doi.org\/10.1002\/JPER.24-0267","journal-title":"J Periodontol"},{"issue":"22","key":"6813_CR8","first-page":"3262","volume":"123","author":"X Zhang","year":"2010","unstructured":"Zhang X, Dai J, Long Y, Wu H, Li XJ, Ding Y (2010) Correlation of estrogen receptor alpha gene polymorphisms and bone mineral density in Chinese women with chronic periodontitis. Chin Med J 123(22):3262\u20133267","journal-title":"Chin Med J"},{"issue":"5","key":"6813_CR9","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1590\/1678-775720150232","volume":"23","author":"C Alves","year":"2015","unstructured":"Alves C, Rossa C Jr, Diniz S et al (2015) Effect of menopause on periodontitis progression in female rats: A histomorphometric and immunohistochemical study. J Appl Oral Sci 23(5):561\u2013569. https:\/\/doi.org\/10.1590\/1678-775720150232","journal-title":"J Appl Oral Sci"},{"key":"6813_CR10","doi-asserted-by":"publisher","first-page":"n71","DOI":"10.1136\/bmj.n71","volume":"372","author":"MJ Page","year":"2021","unstructured":"Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https:\/\/doi.org\/10.1136\/bmj.n71","journal-title":"BMJ"},{"key":"6813_CR11","unstructured":"Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, eds (2024) Cochrane Handbook for Systematic Reviews of Interventions. Version 6.5 (updated August 2024). Cochrane. Available from: https:\/\/training.cochrane.org\/handbook"},{"issue":"1","key":"6813_CR12","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1007\/s00423-024-03399-5","volume":"409","author":"G Montori","year":"2024","unstructured":"Montori G, Botteri E, Ortenzi M, Gerardi C, Allocati E, Giordano A et al (2024) Systematic review and meta-analysis of the use of high-energy devices for thyroid surgery. Langenbecks Arch Surg 409(1):217. https:\/\/doi.org\/10.1007\/s00423-024-03399-5","journal-title":"Langenbecks Arch Surg"},{"key":"6813_CR13","unstructured":"GRADE Working Group (2024) GRADE Handbook. Cochrane. https:\/\/training.cochrane.org\/resource\/grade-handbook. Accessed 19 May 2025"},{"issue":"9","key":"6813_CR14","doi-asserted-by":"publisher","first-page":"1380","DOI":"10.1902\/jop.2009.090082","volume":"80","author":"AN Haas","year":"2009","unstructured":"Haas AN, R\u00f6sing CK, Oppermann RV, Albandar JM, Susin C (2009) Association among menopause, hormone replacement therapy, and periodontal attachment loss in southern Brazilian women. J Periodontol 80(9):1380\u20131387. https:\/\/doi.org\/10.1902\/jop.2009.090082","journal-title":"J Periodontol"},{"key":"6813_CR15","doi-asserted-by":"publisher","first-page":"S997","DOI":"10.4103\/jpbs.jpbs_145_21","volume":"13","author":"R Agrawal","year":"2021","unstructured":"Agrawal R, Ahmed H, Soorgani N, Naik L, Reddy S, Medabalmi M (2021) Assessment of periodontal status in pre- and postmenopausal women with chronic periodontitis: a cross-sectional study. J Pharm Bioallied Sci 13:S997\u2013S999. https:\/\/doi.org\/10.4103\/jpbs.jpbs_145_21","journal-title":"J Pharm Bioallied Sci"},{"issue":"2","key":"6813_CR16","doi-asserted-by":"publisher","first-page":"e1045","DOI":"10.1111\/j.1741-2358.2011.00608.x","volume":"29","author":"GA Scardina","year":"2012","unstructured":"Scardina GA, Messina P (2012) Oral microcirculation in post-menopause: a possible correlation with periodontitis. Gerodontology 29(2):e1045\u2013e1051. https:\/\/doi.org\/10.1111\/j.1741-2358.2011.00608.x","journal-title":"Gerodontology"},{"issue":"3","key":"6813_CR17","doi-asserted-by":"publisher","first-page":"e0265631","DOI":"10.1371\/journal.pone.0265631","volume":"17","author":"Y Lee","year":"2022","unstructured":"Lee Y (2022) Association between osteoporosis and periodontal disease among menopausal women: the 2013\u20132015 Korea National Health and Nutrition Examination Survey. PLoS One 17(3):e0265631. https:\/\/doi.org\/10.1371\/journal.pone.0265631","journal-title":"PLoS One"},{"issue":"11","key":"6813_CR18","doi-asserted-by":"publisher","first-page":"2173","DOI":"10.1902\/jop.2008.070127","volume":"79","author":"S Fujita","year":"2008","unstructured":"Fujita S, Kikuchi T, Sobue T, Suzuki M, Koide M, Noguchi T (2008) Lipopolysaccharide-mediated enhancement of bone metabolism in estrogen-deficient mice. J Periodontol 79(11):2173\u20132181. https:\/\/doi.org\/10.1902\/jop.2008.070127","journal-title":"J Periodontol"},{"issue":"3","key":"6813_CR19","doi-asserted-by":"publisher","first-page":"e00410-24","DOI":"10.1128\/iai.00410-24","volume":"93","author":"F Huang","year":"2025","unstructured":"Huang F, Su Z, Zhou F, Wu Y, Li J, Ren B (2025) Estrogen prevented gingival barrier injury from Porphyromonas gingivalis lipopolysaccharide. Infect Immun 93(3):e00410-24. https:\/\/doi.org\/10.1128\/iai.00410-24","journal-title":"Infect Immun"},{"issue":"2","key":"6813_CR20","doi-asserted-by":"publisher","first-page":"157","DOI":"10.4103\/jmh.jmh_61_21","volume":"13","author":"B Soundarya","year":"2022","unstructured":"Soundarya B, Massillamani F, Kailasam S, Jayashree G, Narmadha N, Sornaa N (2022) Salivary menopausal markers and oral health status \u2013 a hidden hook up. J Midlife Health 13(2):157\u2013162. https:\/\/doi.org\/10.4103\/jmh.jmh_61_21","journal-title":"J Midlife Health"},{"key":"6813_CR21","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.3390\/nu13041194","volume":"13","author":"V Machado","year":"2021","unstructured":"Machado V, Botelho J, Viana J, Pereira P, Lopes LB, Proen\u00e7a L et al (2021) Association between Dietary Inflammatory Index and periodontitis: a cross-sectional and mediation analysis. Nutrients 13:1194. https:\/\/doi.org\/10.3390\/nu13041194","journal-title":"Nutrients"},{"key":"6813_CR22","doi-asserted-by":"publisher","first-page":"3755","DOI":"10.1038\/s41598-023-30203-z","volume":"13","author":"R Tamashiro","year":"2023","unstructured":"Tamashiro R, Strange L, Schnackenberg K, Santos J, Gadalla H, Zhao L et al (2023) Smoking-induced subgingival dysbiosis precedes clinical signs of periodontal disease. Sci Rep 13:3755. https:\/\/doi.org\/10.1038\/s41598-023-30203-z","journal-title":"Sci Rep"},{"key":"6813_CR23","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1111\/jcpe.13094","volume":"46","author":"JP Woelber","year":"2019","unstructured":"Woelber JP, G\u00e4rtner M, Breuninger L, Anderson A, K\u00f6nig D, Hellwig E et al (2019) The influence of an anti-inflammatory diet on gingivitis: a randomized controlled trial. J Clin Periodontol 46:481\u2013490. https:\/\/doi.org\/10.1111\/jcpe.13094","journal-title":"J Clin Periodontol"},{"key":"6813_CR24","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1111\/prd.12270","volume":"83","author":"RJ Genco","year":"2020","unstructured":"Genco RJ, Borgnakke WS (2020) Diabetes as a potential risk for periodontitis: association studies. Periodontol 2000 83:40\u201345. https:\/\/doi.org\/10.1111\/prd.12270","journal-title":"Periodontol 2000"},{"key":"6813_CR25","doi-asserted-by":"publisher","first-page":"1088","DOI":"10.1177\/00220345231179897","volume":"102","author":"FV Bitencourt","year":"2023","unstructured":"Bitencourt FV, Nascimento GG, Costa SA, Andersen A, Sandb\u00e6k A, Leite FRM (2023) Co-occurrence of periodontitis and diabetes-related complications. J Dent Res 102:1088\u20131097. https:\/\/doi.org\/10.1177\/00220345231179897","journal-title":"J Dent Res"},{"issue":"5","key":"6813_CR26","doi-asserted-by":"publisher","first-page":"648","DOI":"10.1002\/JPER.20-0445","volume":"92","author":"MJ LaMonte","year":"2021","unstructured":"LaMonte MJ, Andrews CA, Hovey KM, Buck MJ, Li L, McSkimming DI et al (2021) Subgingival microbiome is associated with alveolar bone loss measured 5 years later in postmenopausal women. J Periodontol 92(5):648\u2013661. https:\/\/doi.org\/10.1002\/JPER.20-0445","journal-title":"J Periodontol"},{"issue":"8","key":"6813_CR27","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1034\/j.1600-051x.2003.00055.x","volume":"30","author":"P Mascarenhas","year":"2003","unstructured":"Mascarenhas P, Gapski R, Al-Shammari K, Wang H-L (2003) Influence of sex hormones on the periodontium: sex hormones and periodontium. J Clin Periodontol 30(8):671\u2013681. https:\/\/doi.org\/10.1034\/j.1600-051x.2003.00055.x","journal-title":"J Clin Periodontol"},{"issue":"1","key":"6813_CR28","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1111\/j.1600-0757.2011.00398.x","volume":"61","author":"PS Kumar","year":"2013","unstructured":"Kumar PS (2013) Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000 61(1):103\u2013124. https:\/\/doi.org\/10.1111\/j.1600-0757.2011.00398.x","journal-title":"Periodontol 2000"},{"key":"6813_CR29","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1007\/s40496-018-0168-0","volume":"5","author":"F Batool","year":"2018","unstructured":"Batool F, Akcali Z, Petit C, Huck O, Akcal\u0131 A (2018) Are sex steroid hormones influencing periodontal conditions? A systematic review. Curr Oral Health Rep 5:33\u201338. https:\/\/doi.org\/10.1007\/s40496-018-0168-0","journal-title":"Curr Oral Health Rep"},{"key":"6813_CR30","doi-asserted-by":"publisher","DOI":"10.1111\/odi.13059","author":"C Pannuti","year":"2020","unstructured":"Pannuti C, Figueredo T, Steffens J, Warnavin S, Chaves J (2020) Sex hormone replacement therapy in periodontology \u2013 a systematic review. Oral Dis. https:\/\/doi.org\/10.1111\/odi.13059","journal-title":"Oral Dis"},{"key":"6813_CR31","doi-asserted-by":"publisher","first-page":"572","DOI":"10.3390\/healthcare9050572","volume":"9","author":"E Ferrara","year":"2021","unstructured":"Ferrara E, Di Naro E, Loverro M, Converti I, Rapone B, Loverro M (2021) The effect of menopause hypoestrogenism on osteogenic differentiation of periodontal ligament cells (PDLC) and stem cells (PDLCs): a systematic review. Healthcare 9:572. https:\/\/doi.org\/10.3390\/healthcare9050572","journal-title":"Healthcare"},{"issue":"4","key":"6813_CR32","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1097\/gme.0b013e31824d8f40","volume":"19","author":"SD Harlow","year":"2012","unstructured":"Harlow SD, Gass M, Hall JE, Lobo R, Maki P, Rebar RW et al (2012) Executive summary of the Stages of Reproductive Aging Workshop + 10: addressing the unfinished agenda of staging reproductive aging. Menopause 19(4):387\u2013395. https:\/\/doi.org\/10.1097\/gme.0b013e31824d8f40","journal-title":"Menopause"},{"issue":"1","key":"6813_CR33","doi-asserted-by":"publisher","first-page":"S173","DOI":"10.1002\/JPER.17-0721","volume":"89","author":"PN Papapanou","year":"2018","unstructured":"Papapanou PN, Sanz M, Jepsen S, Tonetti MS, Berglundh T, Bouchard P et al (2018) Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 89(1):S173\u2013S182. https:\/\/doi.org\/10.1002\/JPER.17-0721","journal-title":"J Periodontol"},{"issue":"1","key":"6813_CR34","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1111\/prd.12117","volume":"70","author":"KM Jaedicke","year":"2016","unstructured":"Jaedicke KM, Preshaw PM, Taylor JJ (2016) Salivary cytokines as biomarkers of periodontal diseases. Periodontol 2000 70(1):164\u2013183. https:\/\/doi.org\/10.1111\/prd.12117","journal-title":"Periodontol 2000"}],"container-title":["Clinical Oral Investigations"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00784-026-06813-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00784-026-06813-y","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00784-026-06813-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T20:41:14Z","timestamp":1781642474000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00784-026-06813-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,3,23]]},"references-count":34,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2026,4]]}},"alternative-id":["6813"],"URL":"https:\/\/doi.org\/10.1007\/s00784-026-06813-y","relation":{},"ISSN":["1436-3771"],"issn-type":[{"value":"1436-3771","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,3,23]]},"assertion":[{"value":"10 July 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 March 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 March 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This systematic review was prospectively registered in PROSPERO (ID: CRD420251055123) and no patients were involved.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics statement"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}}],"article-number":"143"}}