Prevalence of periodontal disease in patients with polycystic ovary syndrome in a tertiary centre at Kerala: A cross-sectional study

Harithrra Venkataraman; Maya Rajan Peter; Sarala Sreedhar; Reshma Suresh; Rajesh Vyloppillil; MR Sreelakshmi

doi:10.4103/jdmimsu.jdmimsu_75_22

ORIGINAL ARTICLE

Year : 2022 | Volume : 17 | Issue : 4 | Page : 898-903

Prevalence of periodontal disease in patients with polycystic ovary syndrome in a tertiary centre at Kerala: A cross-sectional study

Harithrra Venkataraman¹, Maya Rajan Peter¹, Sarala Sreedhar², Reshma Suresh¹, Rajesh Vyloppillil¹, MR Sreelakshmi¹
¹ Department of Periodontics, Amrita School of Dentistry, Amrita Institute of Medical Sciences, Kochi, Kerala, India
² Department of Obstetrics and Gynaecology, Amrita Institute of Medical Sciences, Kochi, Kerala, India

Date of Submission	23-Feb-2022
Date of Acceptance	24-Aug-2022
Date of Web Publication	10-Feb-2023

Correspondence Address:
Dr. Maya Rajan Peter
Department of Periodontics, Amrita School of Dentistry, Amrita Institute of Medical Sciences, Kochi - 682 041, Kerala
India

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/jdmimsu.jdmimsu_75_22

Abstract

Background: Polycystic ovary syndrome (PCOS) is commonly associated with periodontal disease. Aims: The aim of the study is to assess the prevalence of periodontal diseases in female patients with PCOS in a tertiary centre at Kerala. Subjects and Methods: The study was held between December 2019 and December 2021 where a total of 320 female subjects in the age group of 20–35 years were included and among them 160 were PCOS diagnosed and 160 were healthy controls. Anthropometric and periodontal parameters were recorded and assessed among the groups. Statistical Analysis Used: Bivariate analysis between periodontal diseases and other covariant were done using Chi-square test. Those variables which were showing significant level up to 10% were taken to logistic regression model for estimating the adjusted risk for the periodontal diseases in PCOS patients. Results: In the PCOS group, 70 subjects (43.7%) were affected by gingivitis, 68 subjects (42.5%) were affected by mild periodontitis and 22 patients (13.7%) were diagnosed with moderate periodontitis. Gingivitis was observed in 153 subjects (95.6%) in the control group and mild periodontitis was only observed in 7 subjects (4.3%) (P < 0.001). Conclusions: We can conclude that a dental check-up should be made mandatory in the management protocol of PCOS and the gynaecologist should also play a pivotal role along with the periodontist in the prevention, diagnosis and treatment of periodontal disease in PCOS patients.

Keywords: Gingivitis, periodontal disease, polycystic ovary syndrome

How to cite this article:
Venkataraman H, Peter MR, Sreedhar S, Suresh R, Vyloppillil R, Sreelakshmi M R. Prevalence of periodontal disease in patients with polycystic ovary syndrome in a tertiary centre at Kerala: A cross-sectional study. J Datta Meghe Inst Med Sci Univ 2022;17:898-903

How to cite this URL:
Venkataraman H, Peter MR, Sreedhar S, Suresh R, Vyloppillil R, Sreelakshmi M R. Prevalence of periodontal disease in patients with polycystic ovary syndrome in a tertiary centre at Kerala: A cross-sectional study. J Datta Meghe Inst Med Sci Univ [serial online] 2022 [cited 2023 Nov 29];17:898-903. Available from: https://journals.lww.com/dmms/pages/default.aspx/text.asp?2022/17/4/898/369517

Introduction

Polycystic ovary syndrome (PCOS) is a prevalent disorder of the endocrine system characterized by a disharmony in the hormonal levels which affects the systemic as well as oral health of women of reproductive age.^[1] It was previously known as “Stein-Leventhal syndrome” or “Polycystic Ovarian disease.” PCOS is complex with reproductive, metabolic and psychological features.^[2] Women with PCOS have higher rates of insulin resistance (IR), abdominal obesity, dyslipidemia, and cardiac risk factors. As a result, PCOS is a variant of the metabolic syndrome that is particular to women.^[3],[4],[5]

It affects five to eighteen percent females of reproductive age. This tends to begin immediately after puberty, thus inducing a build-up of follicles within the ovaries leading to a development of cyst.^[4],[6] By definition, “PCOS is a heterogeneous disorder that is a combination of signs and symptoms of androgen excess (hirsutism and/or hyperandrogenaemia) and ovarian dysfunction (Oligo-ovulation and/or polycystic ovarian morphology), provided that other specific diagnoses, such as hyperprolactinaemia and nonclassic congenital adrenal hyperplasia, have been excluded.”^[7]

A persistent inflammatory state can be an outcome of chronic infectious disease, one of them being periodontal diseases.^[6] In simple terms, periodontitis is the inflammation of the gums and supporting structures of teeth and can be defined as a “chronic inflammatory disease of the tooth supporting structures, triggered against pathogenic bacterial microflora. The excessive inflammatory response that ensues, leads to alveolar bone loss and tooth loss.”^[8]

According to the literature, periodontal disease and PCOS have been linked with greater levels of oxidative stress and systemic inflammatory indicators like pro-inflammatory cytokines and C-reactive protein.^[9] Apart from the impact of bacterial infections, previous research has linked periodontal disease to systemic disorders like dyslipidemia, obesity, IR, Diabetes Mellitus (DM), and Cardiovascular Diseases.^{[8],[10],[11]} This could suggest a possible specific pathophysiological mechanism in order to cope with these conditions.^[9]

There are no published reports done in Indian population till date to study the prevalence of periodontal disease in patients with PCOS. The current study was done to bridge this gap there by assessing prevalence of periodontal disease in patients with PCOS in a tertiary centre in Kerala, India.

Subjects and Methods

Study population

Patients reporting to the Department of Obstetrics and Gynaecology, Amrita Institute of Medical Sciences (AIMS), Kochi, Kerala, India who are diagnosed with PCOS and the patients reporting to the Department of Periodontology, Amrita School of Dentistry (ASD), Kochi, Kerala, India, were included in this cross-sectional study. Prior to commencing the study, ethical approval was obtained (IRB-AIMS-2019-288). The study period range was 3 years that extended from December 2019 to December 2021 where a total of 320 female subjects were included after obtaining their due consent. PCOS was diagnosed based on Rotterdam criteria.^[12]

The study included 160 participants (aged 20–35 years, mean age: 26.45 years) who had recently been diagnosed with PCOS and had not yet initiated medical therapy for the syndrome. The participants were recruited from the Outpatient Department of Obstetrics and Gynaecology, AIMS, Kochi, Kerala. 160 systemically healthy controls matched for age (aged 20–35 years, mean age: 26.45 years) were recruited from the regular Outpatient Department of Periodontics, ASD, Kochi. The diagnosis of PCOS was done based on Rotterdam criteria in the presence of ≥2 of the following: (1) clinical and/or biochemical hyperandrogenism; (2) chronic oligo-or anovulation; and (3) polycystic ovaries on ultrasound (presence of ≥12 follicles in each ovary measuring 2–9 mm in diameter and/or increased ovarian volume >10 mL). Enrollment criteria was presence of more than 20 natural teeth, nonobese female patients (<30 kg/m²) [Figure 1].^[12] Study included participants who were alcoholic and smokers and also participants with systemic conditions like hypertension, cardiovascular disease, epilipesy and inorder to assess whether PCOS patients always were having the presence of confounding factors. Patients with history of congenital adrenal hyperplasia, thyroid dysfunction, DMs, females using confounding medications, including oral contraceptive agents, steroid hormones, cancer that has been active in the recent 5 years, undergoing periodontal treatment in the last 6-month and individuals who have been treated for PCOS for more than 6 months were excluded from the study.

Figure 1: Consort methodology flow chart. PCOS: Polycystic ovary syndrome, BOP: Bleeding on probing, CAL: Clinical attachment level

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Anthropometric parameters

The waist circumference (WC) was measured in centimetres at the midpoint between the lower margin of the lowest palpable rib and the top of the iliac crest. The hip circumference was measured around the broadest part of the buttocks to determine the Waist-to-Hip Ratio (WHR). Body mass index (BMI) was calculated by dividing weight in kilograms by height in metres squared.

Periodontal parameters

The clinical gingival index (GI) (Loe H and Silness J, 1963), Oral Hygiene Index–Simplified (OHI-S) (John C Greene and Jack R Vermillion, 1964), Probing depth (PD) and Clinical attachment level (CAL) were recorded for both the groups. William's periodontal probe was used to record PD, CAL and GI while explorer was used to record OHI-S.

Statistical analysis

Statistical analysis was done using Statistical Package for Social Sciences IBM (SPSS) Version 20 (IBM SPSS for Windows, SPSS Inc., Chicago, IL, USA). The frequency distribution for categorical variables and mean and standard deviation for continuous variables were used to characterize the attributes of the subject's variables. Bivariate analysis between periodontal diseases and other co-variants was done using Chi-square test. Those variables which were significant up to 10% was taken to logistic regression model for estimating the adjusted risk for the periodontal diseases in PCOS patients. The odds ratio and 95% confidence intervals (CIs) for the association between PD and PCOS were calculated using logistic regression analysis. The presence or absence of periodontitis was used as the outcome variable, whereas PCOS disease status was used as a categorical predictor variable. As estimated by software, all statistical analyses were two-tailed with a significance level of 0.05 CIs.

Results

[Table 1] describes the characteristics of study population according to demographics and risk factors. Among the 320 participants aged 20–35 years, 68.8% were found to be married (n = 220) and 51.9% were found to be Unemployed (n = 166). When covariates were assessed 94.7% participants presented with no risk factors but 0.9% (n = 3) had a history of hypertension, 0.9% (n = 3) had cardiovascular disease, 1.9% (n = 6) had a habit of alcohol consumption.

Table 1: Distribution of study population based on demographics and risk factors

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[Table 2] depicts a detailed association of the various risk factors associated with PCOS. Based on the marital status, in the PCOS group 119 (54.1%) were married and 41 (41%) were not married, and in the non-PCOS group 101 (45.9%) were married and 59 (59%) were not married. Thus it is inferred that married women tend to have higher significance of PCOS in comparison to the unmarried category (P < 0.04). Based on the occupational status, within the PCOS group 81 (48.8%) were employed and 79 (51.3%) were unemployed; and in the non-PCOS group 85 (51.2%) were employed and 75 (48.7%) were unemployed. Occupational status between the PCOS and non-PCOS group was not statistically (P > 0.737). Based on these results it can be inferred that women who were employed had higher chances of being affected by PCOS than the unemployed category. This highlights the role of stress in working women contributing to PCOS.

Table 2: Association of the various risk factors with polycystic ovary syndrome

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Based on the presence of covariate, 3 participants in PCOS group were found to be hypertensive, 6 subjects had the habit of alcohol consumption and 3 had cardiovascular issues.

Based on WHR, in the PCOS group 65 (80.2%) had high health risk, 34 (54%) tend to have moderate health risk and 61 (34.7%) possess low health risk factor.

In the PCOS group, 70 subjects (43.7%) were affected by gingivitis, 68 subjects (42.5%) were affected by mild periodontitis and 22 patients (13.7%) were diagnosed with moderate periodontitis. Gingivitis was observed in 153 subjects (95.6%) in the control group and mild periodontitis was only observed in 7 subjects (4.3%).

The results of the logistic regression analysis [Table 3] indicated that the risks of developing periodontitis in the PCOS group were 28 times greater than in the control group, a statistically significant difference (P < 0.001).

Table 3: Association of the periodontal disease with polycystic ovary syndrome

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Discussion

PCOS is a multifaceted endocrine condition characterised by a wide variety of clinical signs and symptoms.^[4] It is difficult to establish a specific causative element for this condition. Gingival inflammation may be influenced by PCOS or vice versa. If it remains unaddressed, periodontitis will progress.^[13]

The inclusion of age and BMI-matched controls in this study allows for a more accurate comparison of the test groups. The participants in the study belonged to the same ethnicity. Because BMI alone has measurement flaws, combining WHR and WC with BMI improves adiposity prediction.

Those with PCOS had a greater rate of periodontal disease than women without PCOS (healthy controls) in this study, despite the fact that the subgroups were comparable in terms of potential confounding factors like age and BMI. Women with PCOS also showed increased periodontal indices in accordance to the study conducted by Dursun et al.^[14] Hormonal changes that occur during puberty, pregnancy, and menstrual cycles have been shown to have an impact on women's gingival health.^[4],[15]

Ovulation and follicle growth are frequently absent in PCOS women due to altered levels of luteinising hormone (LH) and follicular stimulating hormone. Excessive LH secretion results in an increased androgen production. Excessive androgen production cause hirsutism, acne, and weight gain, along with several other factors. Elevated esrtrogen levels are one of the known causes for gingival inflammation.

Menstrual irregularities and infertility are caused by hyperandrogenism, which is frequently seen in PCOS patients. In women with PCOS, a rise in steroid levels affects the response of gingiva to microbial invasion. Indeed the slightest microbial deposit renders the gingiva hypersensitive, thereby resulting in increased periodontal damage and risk of periodontal disease activity in such patients. Gingival tissues react to variations in hormone levels by microbial alterations and inturn increase the secretion of cytokines that tend to produce a pro-inflammatory effect. These modifications have a negative impact on the alveolar bone and adjoining structures, culminating in tooth loss.^[4] Hormonal changes in the PCOS may affect salivary levels of potential periodontal pathogens and/or their systemic antibody responses in the presence of gingival inflammation. This may be due to the accumulation of active progesterone and estrogen levels in periodontal tissues, which provides an ideal medium for the bacterial growth. According to literature, oxidative stress, which itself is prominent in PCOS patients, may indeed be a unifying linkage connecting periodontitis with metabolic syndrome, diabetes, and thyroid disorders.^[16],[17]

In accordance with previous researches the effect of hyperandrogenism on vascular flora has contributed to increased bleeding on probing (BOP) in the PCOS group.^[18] The elevated CAL in the PCOS group also contributed to a hyper responsive inflammatory phase which is triggered in response to a hormonal imbalance. These inflammatory processes are crucial in the progression of periodontal disease, as well as in the subsequent deepening of the gingival sulcus and bone loss. In contrast to current study, where moderate periodontitis was higher in the PCOS group (100%, n = 22) in comparison to healthy control group (0%, n = 0) without PCOS, Porwal et al. found no statistically significant difference in the prevalence of periodontitis in females with and without PCOS.^[19]

Gingivitis and hormonal changes throughout adolescence, pregnancy, and menstrual cycles have all been widely researched. Elevated steroid hormone synthesis is linked to increased gingival inflammation. Estrogen's effects on the gingival epithelium, collagen formation, osteoblasts, and bone structures are significant in the pathogenesis of periodontal disease. The capillary system, inflammation, and angiogenesis are affected by oestrogen and progesterone. These changes cause excessive vascular endothelial cell growth and epithelial keratinisation in the gingiva. Patients with PCOS who have hyperandrogenism encounter not only menstrual irregularities and infertility, but also have a higher risk of periodontal disease.^[9],[17]

The elevated gingival indices in PCOS patients were congruent with the known effect of hyperandrogenism on vascular flora.^{[9],[14],[20]} Furthermore, the elevated clinical attachment loss in the PCOS group could be due to a higher vulnerability to inflammatory process activation. Periodontal disease and gingival supporting tissue involvement, as well as gingival sulcus deepening and bone loss, are all influenced by these inflammatory processes.

In contrast to the study by Porwal et al. neither the case nor the control group in current study were periodontally healthy. Consistent with previous studies, higher OHI-S, GI and CAL rates were observed in patients with PCOS in comparison to the control group.^[14]

In most of the studies, confounding variables or risk factors like hypertension, cardiovascular disease and alcohol consumption were excluded. However, these confounding variables were included in the present study so as to assess the influence of systemic conditions in PCOS patients. The results of this study stated that only 0.9% of the PCOS patients had systemic conditions like hypertension and cardiovascular disease and 1.9% of the PCOS subjects were addicted to alcohol, which further explains that not all the PCOS patients with periodontal disease has presence of risk factors.

Metabolic disruption in PCOS refers to hormonal imbalances and altered metabolic pathways that result in IR, hyperinsulinemia, and hyperandrogenism.^[21],[22] Chronic low-grade inflammation is linked to hormonal disturbance, and both these factors have higher probability to raise the risk of periodontal disease.^[19],[23] In women with PCOS, several studies have found a link between inflammatory markers (tumour necrosis factor alpha, interleukin (IL)-17A, C-reactive protein, and IL-6) and periodontal parameters (BOP, plaque index, and PD).^[4] While the etiopathogenesis remains unknown, IR has been suggested as a possible association, which leads to low-grade chronic inflammation in both PCOS and periodontal disease. A bidirectional association can be established between PCOS and periodontal disease based on studies that analysed levels of serum and salivary biomarkers [Figure 2].^[19]

Figure 2: Factors linking polycystic ovary syndrome and periodontal disease.^[22] CRP: C-reactive protein, IL-6: Interleukin-6, TNF-α: Tumor necrosis factor-alpha, T2DM: Type 2 diabetes

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Young and Ward et al.(2021), suggested that PCOS, had a link to IR, hyperandrogenism and Type 2 DM, which also can produce low grade chronic inflammation due to increased inflammatory cytokine production.^[22] Probably this may lead to a direct impact on the underlying periodontium. Elevated estrogen and progesterone levels in PCOS women have an effect on oral health, and numerous studies imply a hormonal relationship between PCOS and periodontal disease.^[10] Individuals newly diagnosed with PCOS, according to Porwal et al., had poor periodontal parameters than women who had been regularly under medication (with metformin and/or changes in lifestyle) for at least 6 months.^[19]

PCOS patients exhibited lower periodontal parameters than non-PCOS patients. We can introspect that PCOS, through many pathophysiological linkages, such as low-grade systemic inflammation, oxidative stress, IR, Advanced glycation end products, and systemic hormone imbalances, may exacerbate the preexisting periodontal disease caused by plaque. Periodontal disease produces chronic subclinical inflammation that leads to IR, triggering the onset of type 2 diabetes, which is a common hallmark of PCOS. As a result, we can speculate that PCOS and periodontal disease are linked reciprocally.

The limitations of the study include short duration which resulted in a smaller sample size. Hence in future a longitudinal study with large population needs to be assessed to signify the link between periodontal disease and PCOS.

This prevalence study based on patient reported outcome revealed that ignorant attitude towards periodontal treatment, lack of knowledge on maintenance of oral health and its importance seemed to be a trivial matter in comparison with their systemic condition PCOS.

The first line of treatment for PCOS includes healthy diet, regular exercise and medication. A healthy and balanced diet has already been established to play a major effect in periodontal health. Emphasis on healthy diet and lifestyle modification is essential in the management of PCOS patients. To reduce chronic inflammation associated with periodontal disease, it is mandatory to encourage proper oral hygiene and regular dental visits, as elevation in inflammatory markers may raise the risk of chronic diseases to which PCOS patients already are predisposed.

Hence the prevalence of periodontal disease in PCOS patients should be brought to the knowledge of the gynaecologists thus enlightening them to play a pivotal role in treating both these conditions.

Conclusions

Although PCOS influences the pathogenesis of periodontal disease, patients were not aware of the significance of maintaining a healthy periodontium. This prevalence study concludes that PCOS associated periodontal disease can be differentiated as a separate entity from the usual plaque induced periodontal disease. Hence we can emphasize that a dental check-up should be made mandatory in the management protocol of PCOS and the gynaecologist should also play a pivotal role along with the periodontist in the prevention, diagnosis and treatment of periodontal disease in PCOS patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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