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Increased Risk of Polycystic Ovary Syndrome in Taiwanese Women with Chronic Periodontitis: a Nationwide Population-Based Retrospective Cohort Study

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Increased Risk of Polycystic Ovary Syndrome in Taiwanese Women with Chronic Periodontitis: a Nationwide Population-Based Retrospective Cohort Study JOURNAL OF WOMEN’S HEALTH Volume 28, Number 10, 2019 ª Mary Ann Liebert, Inc. DOI: 10.1089/jwh.2018.7648 Increased Risk of Polycystic Ovary Syndrome in Taiwanese Women with Chronic Periodontitis: A Nationwide Population-Based Retrospective Cohort Study Ching Tong, MSD,1,2 Yu-Hsun Wang, MS,3 Hui-Chieh Yu, PhD,1 and Yu-Chao Chang, PhD1,4 Abstract Background: Polycystic ovary syndrome (PCOS) is one of the most common endocrine disorders among women of reproductive age. Both hormonal and inflammatory influences are assumed to affect periodontal tissues. Previous studies have shown that PCOS patients could have higher prevalence of gingival inflammation. However, the relationship between PCOS and chronic periodontitis (CP) is not clear. Materials and Methods: In this study, we evaluated the risk of PCOS from CP exposure in a nationwide population-based retrospective cohort study in Taiwan. We studied the claims data of Taiwanese population from 2001 to 2012. The 24,410 female patients with CP were identified from the National Health Insurance Database. The 24,410 controls were selected with randomly frequency matched by age, sex, and index year from the general population. The risk of PCOS was analyzed by Cox proportional hazards regression models, including sex, age, and comorbidities. Results: In this study, 24,410 female patients with CP (mean age: 35.14 – 8.81 years) and 24,410 controls (mean age: 35.14 – 8.8 years) were observed for 8.89 and 8.85 years, respectively. A total of 441 cases of PCOS were identified in CP cohort and 304 cases in non-CP cohort. Multivariate Cox regression analysis indicated that the incidence rate of PCOS was significantly higher in CP cohort than those in non-CP cohort (adjusted hazard ratio: 1.44, 95% confidence interval: 1.24–1.67). Conclusions: Taken together, this nationwide retrospective cohort study demonstrated that the risk of PCOS was significantly higher in female patients with CP than those without CP in Taiwan. Keywords: polycystic ovary syndrome, chronic periodontitis, women, nationwide population, cohort study, Taiwan Introduction Polycystic ovary syndrome (PCOS) is a complex endo- crine disorder among women and affects about 5%–14% of eriodontal disease, an infectious disease, is triggered women in reproductive age.8 PCOS is characterized by by bacterial products exaggerated gingival inflammation, menstrual irregularity, obesity, infertility, excessive amounts Downloaded by TAICHUNG VETERANS GENERAL HOSP from www.liebertpub.com at 12/06/19. For personal use only. P recognized as gingivitis in the initial phase. Gingivitis could of androgenic hormones, and polycystic ovaries.9 Recently, further destroy the periodontium, leading to alveolar bone de- PCOS was reported to link with an increased risk for car- struction and even tooth loss, which is diagnosed as period- diovascular diseases,10 diabetes,11 and psychiatric disor- ontitis.1 Female sex steroid hormones also play important ders.12 Therefore, PCOS could be recognized not only as a accelerator factors in the pathogenesis of periodontal diseases.2 reproductive problem but also a crucial systemic condition in Inflammatory markers were found to be highly expressed in affected women. periodontal tissues, blood, and salivary or gingival crevice From the literature review, studies had clearly demon- fluid.3,4 Low-grade inflammation of chronic periodontitis (CP) strated that PCOS was associated with gingival inflamma- is emerging as a conceivable etiologic mechanism correlated by tion. Higher levels of oxidative stress and systemic many systemic diseases such as cardiovascular diseases,5 dia- inflammatory markers were found in both gingivitis and betes,6 and chronic pulmonary disease.7 PCOS.13–18 However, gingival inflammation is just one of the 1School of Dentistry, Chung Shan Medical University, Taichung, Taiwan. 2Division of Endodontics and Periodontology, Department of Stomatology, Taichung Veterans General Hospital, Taichung, Taiwan. Departments of 3Medical Research and 4Dentistry, Chung Shan Medical University Hospital, Taichung, Taiwan. 1436 INCREASED RISK OF PCOS WITH CP 1437 symptoms/signs of periodontitis. The definition of period- Exposure of CP ontitis should be resulting in alveolar bone loss. The associ- After approval by the Chung Shan Medical University ation between PCOS and CP still remains to be elucidated. In Hospital institutional review board (CS2-15071), we identified previous cross-section studies, women with newly diagnosed the ambulatory patients for dental visit with newly diagnosed PCOS had higher prevalence of periodontitis with increased 19,20 CP (ICD-9-CM code: 523.4) from 2001 to 2012 as a newly clinical attachment loss. However, the association be- onset CP cohort. The first-time CP diagnosis served as the tween CP and PCOS needs further investigation such as co- index date. In Taiwan, NHI has established the strict guideline hort design and relatively large sample size. that only board-registered dentists can execute the periodontal In this study, we hypothesized that CP may have a higher treatment according to the strict NHI therapeutic guidelines. risk for developing subsequent PCOS in affected women. To ensure the accuracy of CP diagnosis, only patients with at Therefore, a nationwide population-based retrospective co- least three outpatient service claims were recruited. hort study was conducted to investigate the possible link Subjects without periodontitis were randomly selected from between CP and PCOS from Taiwanese National Health In- the data set and identified as healthy controls. The comparison surance Research Database (NHIRD). group included the participations who were never diagnosed with CP from 2000 to 2013. To reduce the confounding bias, Materials and Methods we used propensity score matching to select controls. Pro- Data source pensity score of participants, which predicted the probability of CP exposure for participants, was estimated by logistic re- In 2014, up to 99.9% Taiwanese population was enrolled gression modeling. The predictors involved birth year, sex, and in this compulsory National Health Insurance (NHI) pro- 21 comorbidities at baseline. The 1:1 matched comparisons were gram. The Longitudinal Health Insurance Database 2010 selected with the same propensity score as exposure subjects. (LHID 2010) was used for this cohort study. LHID 2010 Patients diagnosed with any type of periodontal diseases before collected the registration information and dental and medical 2001 were excluded. The flow chart of case selection and ex- data, which contain 1 million beneficiaries randomly sampled clusion is shown in Figure 1. from the 2010 registry of beneficiaries in NHIRD. This da- tabase provides scrambled patient identification number, date PCOS event of birth, sex, diagnostic codes in the format of the Interna- tional Classification of Disease, Revision 9, Clinical Mod- The patients with newly diagnosed PCOS (ICD-9-CM code: ification (ICD-9-CM) code, and the date of visit to medical 256.4X) from January 2001 to December 2012 were selected. institutes as described previously.22,23 In addition to clinical diagnosis, the changes of blood hormones FIG. 1. The flowchart of case selection and exclusion of cases from NHIRD. Downloaded by TAICHUNG VETERANS GENERAL HOSP from www.liebertpub.com at 12/06/19. For personal use only. NHIRD, National Health Insurance Research Database. 1438 TONG ET AL. of LH, FSH, or testosterone (NHI codes: 09078B2, 09126B, no age and urbanization variations ( p > 0.05). The percentage 09126C, 09078B1, 09125B, 09125C, 09064B2, 09121B, and of comorbidities also showed no significant difference be- 09121C) and the findings on gynecologic ultrasonography tween female patients with CP and the healthy controls (NHI code: 19003C) were reviewed to ensure the accuracy of ( p > 0.05). PCOS diagnosis. We also excluded patients with a history of The newly diagnosed PCOS female patients were 441 in CP endocrine disorders, which could have a clinical presentation group and 304 female individuals in non-CP group. The inci- similar to PCOS. ICD9-CM codes for these possible con- dence density (ID) rates of PCOS in non-CP group was only founding factors were listed as follows: Cushing syndrome 1.4 per 1,000 person-years (Table 2), but the ID rates were (255.0), nonclassic congenital adrenal hyperplasia (255.2), about 1.429-fold higher in CP group than in non-CP group. hyperprolactinemia, (253.1), thyroid dysfunction (242, 244), Figure 2 shows the cumulative curve of PCOS incidence and androgen-secreting tumors (227.0, 194.0). All partici- and reveals that the curve of CP patients was significantly pants were followed up from index date to the date of the higher than the curve of control subjects (log rank test, primary outcome, withdrawal from the NHI program, or the p < 0.001). After adjustment of age, urbanization, and co- end of 2013, whichever came first. morbidities, PCOS female patients showed a 1.44-fold in- creased risk of PCOS compared with non-CP female patients Comorbidities (95% confidence interval; CI 1.24–1.67). The age group 30– 39 years old (0.26, 95% CI 0.11–0.58) and 40–50-year olds Potential comorbidities such as chronic pulmonary disease (0.03, 95% CI 0.01–0.07) had lower risk compared with <20- (ICD-9: 490, 491, 492, 494, and 496), diabetes (ICD-9: 250), year-old group, respectively. However, there was no signif- hypertension (ICD-9: 401–405), hyperlipidemia (ICD-9: icant risk for PCOS with comorbidities in the adjusted model. 272), insomnia (ICD-9: 780.52), and major depressive dis- The mean follow-up duration and time to PCOS between order (ICD-9: 296.2, 296.3) were included in this study. To CP and non-CP group is shown in Table 3. The mean follow- improve the validity of confounders, these comorbidities up duration of PCOS was 8.89 and 8.85 years for CP and non- were identified as ‡2 outpatient visits or at least 1 admission CP group, respectively. The mean time to PCOS was 4.35 and within 1 year before index date.
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