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Bone markers and bone mineral density associates with periodontitis in females with poly-cystic ovarian syndrome

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Abstract

Introduction

Studies suggest an association between poly-cystic ovarian syndrome (PCOS) and chronic periodontitis (CP), both being inflammatory conditions. However, insufficient evidence assesses the impact of this inflammation on bone metabolism and bone turnover markers (BTMs). The present study aimed to determine the association between BTMs, bone mineral density (BMD), and clinical periodontal parameters in PCOS women with CP.

Materials and methods

Three groups, each with 40 newly diagnosed (1) PCOS+CP, (2) PCOS alone, (3) CP alone, and fourth group (n = 20) systemically and periodontally healthy females aged 18–30 years were included in the study. Full mouth clinical periodontal parameters, C-terminal telopeptides of type I collagen (CTX), bone alkaline phosphatase (ALP), BMD and 25-hydroxyvitamin D (VD) were recorded for all.

Results

Low BMD (0.89 ± 0.11 g/cm2), increased CTX levels (2.76 ± 4.64 ng/ml), decreased bone ALP levels (11.09 ± 6.86 ng/ml), higher VD levels (289.02 ± 168.28 nmol/l) and poor clinical periodontal status were observed in PCOS + CP females. BMD-spine showed weak positive correlation with CTX, bone ALP, VD (r = 0.02, r = 0.07, r = 0.15, respectively) in PCOS + CP group. ANCOVA depicted covariates had no confounding effect. Multiple regression model explained 21.0% for BMD-spine and 12.7% for BMD-femur of total variability signifying association with all measured parameters among all groups.

Conclusion

Enhanced inflammatory thrust by periodontitis increases CTX levels and decreases bone ALP and BMD levels in women with PCOS. Screening PCOS women for periodontal disease and vice versa may have a direct bearing on overall bone health.

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References

  1. Rodriguez PV, Solon-Biet SM, Senior AM, Edwards MC, Desai R, Tedla N, Cox MJ, Ledger WL, Gilchrist RB, Simpson SJ, David J, Handelsman G, Walters KA (2020) Defining the impact of dietary macronutrient balance on PCOS traits. Nat Commun 11:1–15. https://doi.org/10.1038/s41467-020-19003-5

    Article  CAS  Google Scholar 

  2. Takaishi Y, Okamoto Y, Ikeo T, Morii H, Takeda M, Hide K, Arai T, Nonaka K (2005) Correlations between periodontitis and loss of mandibular bone in relation to systemic bone changes in postmenopausal Japanese women. Osteoporosis Int 16:1875–1882. https://doi.org/10.1007/s00198-005-1955-8

    Article  Google Scholar 

  3. Schulze-Späte U, Turner R, Wang Y, Chao R, Schulze PC, Phipps K, Orwoll E, Dam TT (2015) Relationship of bone metabolism biomarkers and periodontal disease: the osteoporotic fractures in men (MrOS) study. J Clin Endocrinol Metab 100:2425–2433. https://doi.org/10.1210/jc.2014-4180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kellesarian S, Malignaggi V, Kellesarian T, Al-Kheraif AA, Alwageet MM, Malmstrom H, Romanos GE, Javed F (2017) Association between periodontal disease and polycystic ovary syndrome: a systematic review. Int J Impot Res 29:89–95. https://doi.org/10.1038/ijir.2017.7

    Article  CAS  PubMed  Google Scholar 

  5. Márquez-Arrico CF, Silvestre-Rangil J, Gutiérrez-Castillo L, Martinez-Herrera M, Silvestre FJ, Rocha M (2020) Association between periodontal diseases and polycystic ovary syndrome: a systematic review. J Clin Med 9:1586. https://doi.org/10.3390/jcm9051586

    Article  PubMed Central  Google Scholar 

  6. Gil-Montoya JA, Garrido-Martinez M, Barrios-Rodriguez R, Ramos-Garcia P, Lenouvel D, Montes-Castillo C, Martinez-Ramirez MJ (2020) Association between low bone mineral density and periodontitis in generally healthy perimenopausal women. J Periodontol 1:1–9. https://doi.org/10.1002/JPER.20-0029

    Article  CAS  Google Scholar 

  7. Schmidt J, Dahlgren E, Brannstrom M, Landin WK (2012) Body composition, bone mineral density and fractures in late postmenopausal women with poly-cystic ovary syndrome—a long-term follow-up study. Clin Endocrinol 77:207–214. https://doi.org/10.1111/j.1365-2265.2012.04378.x

    Article  CAS  Google Scholar 

  8. Zborowski JV, Cauley JA, Talbott EO, Guzick DS, Winters SJ (2000) Bone mineral density, androgens, and the poly-cystic ovary: the complex and controversial issue of androgenic influence in female bone. J Clin Endocrinol Metab 85:3496–3506. https://doi.org/10.1210/jcem.85.10.6902

    Article  CAS  PubMed  Google Scholar 

  9. Lingaiah S, Morin PL, Piltonen T, Puurunen J, Sundstrom PI, Stener VE, Bloigu R, Risteli J, Tapanainen JS (2017) Bone markers in poly-cystic ovary syndrome: a multicenter study. Clin Endocrinol 87:673–679. https://doi.org/10.1111/cen.13456

    Article  CAS  Google Scholar 

  10. Penoni DC, Fidalgo TKS, Torres SR, Varela VM, Masterson D, Leao ATT, Maia LC (2017) Bone density and clinical periodontal attachment in postmenopausal women: a systematic review and meta-analysis. J Dent Res 96:261–269. https://doi.org/10.1177/0022034516682017

    Article  CAS  PubMed  Google Scholar 

  11. Kim JW, Kong KA, Kim HY, Lee HS, Kim SJ, Lee SH, Sim KW, Kim MR, Lee JH (2014) The association between bone mineral density and periodontitis in Korean adults (KNHANES 2008–2010). Oral Dis 20:609–615. https://doi.org/10.1111/odi.12179

    Article  CAS  PubMed  Google Scholar 

  12. Oztürk TM, Büyükkaplan US, Fentoglu O, Gümüs BA, Çerçi SS, Kirzioglu FY (2012) Comparison of bone mineral density in the jaws of patients with and without chronic periodontitis. Dento Maxillo Facial Radiol 41:509–514. https://doi.org/10.1259/dmfr/21900076

    Article  Google Scholar 

  13. Betsy J, Ahmed JM, Mohasin AK, Mohammed A, Nabeeh AAQ (2019) Diagnostic accuracy of salivary biomarkers of bone turnover in identifying patients with periodontitis in a Saudi Arabian population. J Dent Sci 14:269–276. https://doi.org/10.1016/j.jds.2019.03.002

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ismail TST, Muda BC, Rosdi RAM, Zainuddin A, Isa S, Mustapaha Z (2017) Determining the required vitamin D Level for bone health based on bone turnover markers. Korean J Clin Lab Sci 49:337–344. https://doi.org/10.15324/kjcls.2017.49.4.337

    Article  Google Scholar 

  15. Caton GJ, Armitage G, Berglundh T, Chapple ILC, Jepsen SS, Kornman KL, Mealey B, Papapanou PN, Sanz M, Tonetti SM (2018) A new classification scheme for periodontal and peri-implant diseases and conditions—introduction and key changes from the 1999 classification. J Clin Periodontol 45:S1–S8. https://doi.org/10.1111/jcpe.12935

    Article  PubMed  Google Scholar 

  16. Witchel SF, Oberfield SE, Pena AS (2019) Polycystic ovary syndrome: pathophysiology, presentation, and treatment with emphasis on adolescent girls. J Endocr Soc 3:1545–1573. https://doi.org/10.1210/js.2019-00078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ozcaka O, Buduneli N, Ceyhan BO, Akcali A, Hannah V, Nile C, Lappin DF (2013) Is interleukin-17 involved in the interaction between polycystic ovary syndrome and gingival inflammation? J Periodontol 84:1827–1837. https://doi.org/10.1902/jop.2013.120483

    Article  CAS  PubMed  Google Scholar 

  18. Wang F, Dai W, Yang XH, Guo YH, Sun YP (2016) Analyses of optimal body mass index for infertile patients with either poly-cystic or non-polycystic ovary syndrome during assisted reproductive treatment in China. Sci Rep 6:1–9. https://doi.org/10.1038/srep34538

    Article  CAS  Google Scholar 

  19. Kalyan S, Patel MS, Kingwell E, Cote HCF, Liu D, Prior JC (2017) Competing factors link to bone health in poly-cystic ovary syndrome: chronic low-grade inflammation takes a toll. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-03685-x

    Article  CAS  Google Scholar 

  20. Vasikaran S, Cooper C, Eastell R, Griesmacher A, Morris HA, Trenti T, Kanis JA (2011) International osteoporosis foundation and international federation of clinical chemistry and laboratory medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med 49:1271–1274. https://doi.org/10.1515/CCLM.2011.602

    Article  CAS  PubMed  Google Scholar 

  21. Garnero P, Ferreras M, Karsdal MA, Nicamhlaoibh R, Risteli J, Borel O, Qvist P, Delmas PD, Foged NT, Delaisse JM (2003) The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation. J Bone Miner Res 18:859–867. https://doi.org/10.1359/jbmr.2003.18.5.859

    Article  CAS  PubMed  Google Scholar 

  22. Greenblatt MB, Tsai JN, Wein MN (2017) Bone turnover markers in the diagnosis and monitoring of metabolic bone disease. Clin Chem 63:464–474. https://doi.org/10.1373/clinchem.2016.259085

    Article  CAS  PubMed  Google Scholar 

  23. Krul-Poel YHM, Snackey C, Louwers Y, Lips P, Lambalk CB, Laven JSE, Simsek S (2013) The role of vitamin D in metabolic disturbances in poly-cystic ovary syndrome: a systematic review. Eur J Endocrinol 169:853–865. https://doi.org/10.1530/EJE-13-0617

    Article  CAS  PubMed  Google Scholar 

  24. Gallagher JC, Sai AJ (2010) Vitamin D insufficiency, deficiency, and bone health. J Clin Endocrinol Metab 95:2630–2633. https://doi.org/10.1210/jc.2010-0918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tan KML, Saw S, Sethi SK (2013) Vitamin D and its relationship with markers of bone metabolism in healthy Asian women. J Clin Lab Anal 27:301–304. https://doi.org/10.1002/jcla.21602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Thiering E, Bruske I, Kratzsch J, Hofbauer LC, Berdel D, Von BA, Lehmann I, Hoffmann B, Bauer CP, Koletzko S, Heinrich J (2015) Associations between serum 25-hydroxyvitamin D and bone turnover markers in a population-based sample of German children. Sci Rep 5:1–8. https://doi.org/10.1038/srep18138

    Article  CAS  Google Scholar 

  27. Kuchuk NO, Van-Schoor NM, Pluijm SM, Chines A, Lips P (2009) Vitamin D status, parathyroid function, bone turnover, and BMD in postmenopausal women with osteoporosis: global perspective. J Bone Miner Res 24:693–701. https://doi.org/10.1359/jbmr.081209

    Article  CAS  PubMed  Google Scholar 

  28. Deepti TS, Narula SC, Singhal SR, Sharma RK (2017) Effect of non-surgical periodontal therapy along with myo-inositol on high-sensitivity C-reactive protein and insulin resistance in women with polycystic ovary syndrome and chronic periodontitis: a randomized controlled trial. J Periodontol 88:999–1011. https://doi.org/10.1902/jop.2017.170121

    Article  CAS  PubMed  Google Scholar 

  29. Porwal S, Tewari S, Sharma RK, Singhal SR, Narula SC (2014) Periodontal status and high-sensitivity C-reactive protein levels in polycystic ovary syndrome with and without medical treatment. J Periodontol 85:1380–1389. https://doi.org/10.1902/jop.2014.130756

    Article  PubMed  Google Scholar 

  30. Akcali A, Bostanci N, Ozcaka O, Gumu P, Ozturk-Ceyhan B (2017) Gingival Inflammation and salivary or serum granulocyte-secreted enzymes in patients with polycystic ovary syndrome. J Periodontol 88:1145–1152. https://doi.org/10.1902/jop.2017.170043

    Article  CAS  PubMed  Google Scholar 

  31. Ozcaka O, Ceyhan BO, Akcali A, Bicaki N, Lappin DF, Buduneli N (2012) Is there an interaction between polycystic ovary syndrome and gingival inflammation? J Periodontol 83:1529–1537. https://doi.org/10.1902/jop.2012.110588

    Article  CAS  PubMed  Google Scholar 

  32. Saglam E, Canakci CF, Sebin SO, Saruhan N, Ingec M, Canakci H, Sezer U (2017) Evaluation of oxidative status in patients with chronic periodontitis and polycystic ovary syndrome: a cross-sectional study. J Periodontol 2:1–16. https://doi.org/10.1902/jop.2017.170129

    Article  CAS  Google Scholar 

  33. Varadan M, Gopalkrishna P, Bhat PV, Kamath SU, Krithishree S, Thriveni KG, Kumar S (2019) Influence of poly-cystic ovary syndrome on the periodontal health of Indian women visiting a secondary health care centre. Clin Oral Investig 23:3249–3255. https://doi.org/10.1007/s00784-018-2741-2

    Article  PubMed  Google Scholar 

  34. Alghadir AH, Gabr SA, Al-Eisa E (2015) Physical activity and lifestyle effects on bone mineral density among young adults: sociodemographic and biochemical analysis. J Phys Ther Sci 27:2261–2270. https://doi.org/10.1589/jpts.27.2261

    Article  PubMed  PubMed Central  Google Scholar 

  35. Yuskel O, Dokmetas HS, Tocpu S, Erselcan T, Sencan M (2001) Relationship between bone mineral density and insulin resistance in poly-cystic ovary syndrome. J Bone Miner Metab 19:257–262. https://doi.org/10.1007/s007740170029

    Article  Google Scholar 

  36. Katulski K, Slawek S, Czyzyk A, Podfigurna-Stopa A, Paczkowska K, Ignaszak N, Podkowa N, Meczekalski B (2014) Bone mineral density in women with polycystic ovary syndrome. J Endocrinol Invest 37:1219–1224. https://doi.org/10.1007/s40618-014-0175-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. To WWK, Wong MWN (2012) A comparison of bone mineral density in normal weight and obese adolescents with polycystic ovary syndrome. J Pediatr Adolesc Gynecol 25:248–253. https://doi.org/10.1016/j.jpag.2011.12.073

    Article  PubMed  Google Scholar 

  38. Ganie MA, Chakraborty S, Sehgal A, Sreejith M, Kandasamy D, Jana M, Rashid A (2018) Bone mineral density is unaltered in women with polycystic ovary syndrome. Horm Metab Res 50:754–760. https://doi.org/10.1055/a-0733-7768

    Article  CAS  PubMed  Google Scholar 

  39. Mongkornkarn S, Suthasinekul R, Sritara C, Lertpimonchai A, Tamsailom S, Udomsak A (2019) Significant association between skeletal bone mineral density and moderate to severe periodontitis in fair oral hygiene individuals. J Invest Clin Dentist 10:e12441. https://doi.org/10.1111/jicd.12441

    Article  Google Scholar 

  40. Tezal M, Wactawski-Wende J, Grossi SG, Ho AW, Dunford R, Genco RJ (2000) The relationship between bone mineral density and periodontitis in postmenopausal women. J Periodontol 71:1492–1498. https://doi.org/10.1902/jop.2000.71.9.1492

    Article  CAS  PubMed  Google Scholar 

  41. Yoshihara A, Seida Y, Hanada N, Miyazaki H (2004) A longitudinal study of the relationship between periodontal disease and bone mineral density in community-dwelling older adults. J Clin Periodontol 31:680–684. https://doi.org/10.1111/j.1600-051X.2004.00548.x

    Article  PubMed  Google Scholar 

  42. Hattatoglu SE, Ozcakar L, Gokce KY, Karaaagaolu E, Demiralp B, Nazliel-Erverdi H (2008) No alteration in bone mineral density in patients with periodontitis. J Dent Res 87:79–83. https://doi.org/10.1177/154405910808700114

    Article  Google Scholar 

  43. Mezzavilla M, Zupin L, Navarra CO, Di-Lenarda R, Gasparini P, Crovella S, Robino A, Bevilacqua L (2020) Deleterious variants in genes associated with bone mineral density are linked to susceptibility to periodontitis development. Meta Gene 24:100670. https://doi.org/10.1016/j.mgene.2020.100670

    Article  Google Scholar 

  44. Zhang X, Dai J, Long Y, Wu H, Li XJ, Ding Y (2010) Correlation of oestrogen receptor alpha gene polymorphisms and bone mineral density in Chinese women with chronic periodontitis. Chin Med J 123:3262–3267. https://doi.org/10.3760/cma.j.issn.0366-6999.2010.22.017

    Article  CAS  PubMed  Google Scholar 

  45. Glintborg D, Hermann AP, Andersen M (2013) Bone mineral density and vitamin D in PCOS and hirsutism. Expert Rev Endocrinol Metab 8:449–459. https://doi.org/10.1586/17446651.2013.827384

    Article  CAS  PubMed  Google Scholar 

  46. Risal S, Pei Y, Lu H, Manti M, Fornes R et al (2019) Prenatal androgen exposure and transgenerational susceptibility to poly-cystic ovary syndrome. Nat Med 25:1894–1904. https://doi.org/10.1038/s41591-019-0666-1

    Article  CAS  PubMed  Google Scholar 

  47. Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, Taylor R (2012) Periodontitis and diabetes: a two-way relationship. Diabetologia 55:21–31. https://doi.org/10.1007/s00125-011-2342-y

    Article  CAS  PubMed  Google Scholar 

  48. De Moura-Grec PG, Marsicano JA, de Carvalho CAP, de Sales-Peres SHC (2014) Obesity and periodontics: systematic review and meta-analysis. Cienc Saude Coletiva 19:1763–1772. https://doi.org/10.1590/1413-81232014196.13482013

    Article  Google Scholar 

  49. Kassanos D, Trakakis E, Baltas CS, Papakonstantinou O, Simeonidis G, Salamalekis G, Grammatikakis I, Basios G, Labos G, Skarantavos G, Balanika A (2010) Augmentation of cortical bone mineral density in women with polycystic ovary syndrome: a peripheral quantitative computed tomography (PQCT) study. Hum Reprod 25:2107–2114. https://doi.org/10.1093/humrep/deq149

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the women who participated in this project. We also express our sincere thanks to Rajiv Gandhi Endocrinology Centre, JNMC, Aligarh for their laboratory assistance. We thank our colleagues in Dr. ZADC and the Department of Statistics, AMU, for their comments and guidance on this work.

Funding

Support provided by Science and Engineering Research Board, Govt of India. (ECR2016/001632).

Author information

Authors and Affiliations

  1. Department of Periodontics and Community Dentistry, Dr. Ziauddin Ahmed Dental College (DRZADC), Aligarh Muslim University (AMU), Aligarh, 202002, Uttar Pradesh, India

    Afaf Zia & A. Bey

  2. Department of Obstetrics and Gynaecology, Jawaharlal Nehru Medical College and Hospital (JNMCH), AMU, Aligarh, Uttar Pradesh, India

    S. Hakim & S. Parveen

  3. Interdisciplinary Biotechnology Unit, AMU, Aligarh, Uttar Pradesh, India

    A. U. Khan & S. Khalid

  4. Department of Biochemistry, AMU, Aligarh, Uttar Pradesh, India

    H. Ateeq

  5. Department of Statistics and Operations, AMU, Aligarh, Uttar Pradesh, India

    FNK. Yusufi

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  1. Afaf Zia
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Contributions

AZ contributed to conception, design, data analysis, interpretation, drafted and critically revised the manuscript. SH and SP contributed to data acquisition and critically revised the manuscript. AUK and SK contributed to data analysis and critically revised the manuscript. AB contributed to the conception, design and critically revised the manuscript. HA contributed to data acquisition, analysis, interpretation and drafted the manuscript. FNKY contributed to data analysis, interpretation and critically revised the manuscript. All authors gave their final approval and agree to be accountable for all aspects of the work.

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Correspondence to Afaf Zia.

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The authors declare no potential conflicts of interest for the authorship and publication of this article.

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The trial is registered with the Indian Clinical Trials Registry (CTRI/2019/09/021214).

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Zia, A., Hakim, S., Khan, A.U. et al. Bone markers and bone mineral density associates with periodontitis in females with poly-cystic ovarian syndrome. J Bone Miner Metab 40, 487–497 (2022). https://doi.org/10.1007/s00774-021-01302-6

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