|Year : 2015 | Volume
| Issue : 6 | Page : 507-512
Comparison of prevalence of periodontal disease in women with polycystic ovary syndrome and healthy controls
Mohammad Ehsan Rahiminejad1, Amirhossein Moaddab2, Hassan Zaryoun3, Soghra Rabiee1, Arta Moaddab4, Amin Khodadoustan Khodadoustan3
1 Department of Obstetrics and Gynecology, Faculty of Dentistry, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran
2 Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas, USA
3 Department of Periodontology, Faculty of Dentistry, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran
4 Department of Dentistry, Standard Dental Health Care, Potomac, Maryland, USA
|Date of Web Publication||27-Nov-2015|
F1040-01, 6621 Fannin St., Pavilion For Women, Baylor College of Medicine, Houston, Texas 77030
Source of Support: None, Conflict of Interest: None
Background: Polycystic ovary syndrome (PCOS) is the most common endocrine disorder among women of reproductive age, affecting 4-18% of them. Previous studies also showed that periodontal diseases are associated with different components of the metabolic syndrome. The aim of this study is to determine the association between PCOS and periodontal diseases.
Materials and Methods: A total of 196 women (98 with PCOS and 98 healthy controls) were enrolled. PCOS diagnosis was confirmed by history, clinical signs, physical examination, laboratory parameters, and ultrasound studies. Both cases and controls were examined by the same periodontist. Periodontal parameters including bleeding on probing (BOP), probing depth, clinical attachment loss (CAL), plaque index, and tooth loss were investigated in all participants. Pregnant women, smokers, individuals with a history of malignancy or osteoporosis, and those taking prophylactic antibiotics for dental procedures or receiving periodontal treatment during the 6-month period before examination were excluded. Data were analyzed using t-test, Chi-square test, and linear regression. Statistical significance was set at P < 0.05.
Results: CAL and sites with BOP were significantly higher in women with PCOS (P < 0.05). However, no significant difference was observed in the tooth loss rate between PCOS and non-PCOS participants (P = 0.384).
Conclusion: The prevalence of periodontal disease seems to be higher in women with PCOS. This may be related to the role of chronic systemic inflammation in the pathophysiology of both PCOS and periodontal diseases.
Keywords: Dental plaque index, menstrual disturbance, periodontal diseases, polycystic ovary syndrome
|How to cite this article:|
Rahiminejad ME, Moaddab A, Zaryoun H, Rabiee S, Moaddab A, Khodadoustan AK. Comparison of prevalence of periodontal disease in women with polycystic ovary syndrome and healthy controls. Dent Res J 2015;12:507-12
|How to cite this URL:|
Rahiminejad ME, Moaddab A, Zaryoun H, Rabiee S, Moaddab A, Khodadoustan AK. Comparison of prevalence of periodontal disease in women with polycystic ovary syndrome and healthy controls. Dent Res J [serial online] 2015 [cited 2019 Mar 22];12:507-12. Available from: http://www.drjjournal.net/text.asp?2015/12/6/507/170547
| Introduction|| |
Polycystic ovary syndrome (PCOS) is the most common endocrine disorder among women of reproductive age, affecting 4-18% of them. , In addition to reproductive derangements, patients with PCOS may develop other metabolic and psycological comorbidities.  Classically, PCOS is characterized by the presence of menstrual abnormalities (oligomenorrhea or amenorrhea), chronic anovulation or oligoovulation, clinical/biochemical evidence of hyperandrogenism (hirsutism, acne, or androgenic alopecia), and ultrasound findings.  Patients with this gender-specific form of metabolic syndrome are at higher risk for developing insulin resistance (IR), obesity, dyslipidemia, cardiovascular disease (CVD), and hypertension. , Moreover, recent studies have shown the higher prevalence of impaired glucose tolerance (IGT), type II diabetes mellitus (DM), and lipid profile disturbances in women with PCOS. ,,
Periodontal diseases are chronic inflammatory processes that may lead to tooth loss by affecting tooth-supporting tissues, including the gingiva, alveolar bone, and periodontal ligaments. In addition to the role of bacterial infections, earlier studies have demonstrated the association of periodontal diseases and systemic conditions such as dyslipidemia, obesity, IR, DM, and CVD. ,,,,
Previous studies showed higher levels of oxidative stress and systemic inflammatory markers such as interleukin-6 and C-reactive protein in both periodontal diseases and PCOS. ,, This association may be explained by the role of oxidative stress as the potential link between periodontitis and PCOS based on some recent studies. , This might suggest a possible common pathophysiologic mechanism in concur manifestations of these conditions. In this present study, we aimed to compare the prevalence of periodontal disease in women with PCOS and healthy controls.
| Materials and Methods|| |
In a cross-sectional study (December 2012 to August 2013), a total of 196 women, aged 18-45 years old, visiting the clinics of Fatemieh Women's Hospital, Hamadan, Iran, were enrolled after providing adequate explanation and obtaining informed consent. The study protocol was approved by the Institutional Review Board of Hamadan University of Medical Sciences, Hamadan, Iran. A unique questionnaire containing past medical history, habitual history, and anthropometric parameters was completed for all subjects consisting 98 women with PCOS and 98 systematically healthy subjects. PCOS diagnosis was made based on history, clinical signs, physical examination, laboratory parameters, and ultrasound findings, known as the Rotterdam criteria.  Fasting blood glucose (FBS), high density lipoprotein (HDL), low density lipoprotein (LDL) cholesterol, triglyceride (TG), testosterone, and serum nitric oxide (NO) levels were assessed in both groups. In order to exclude, other conditions including thyroid diseases, hyperprolactinemia, Cushing's syndrome, androgenic tumors, 21-hydroxylase deficiency, thyroid stimulating hormone, and prolactin were measured when it was appropriate.
Pregnant women, smokers, individuals with history of alcoholic drinks consumption, malignancy, osteoporosis, those took prophylactic antibiotics for dental procedures, and patients who received periodontal treatment during the 6-month period before examination were excluded.
Due to the effects of obesity and IGT on periodontal diseases, PCOS patients who had a body mass index (BMI) >25 or IGT were also excluded. ,
Both groups of participants underwent examinations by a single investigator using periodontal probe and mirror to determine the periodontal parameters at the Periodontics Clinic of Hamadan University of Medical Sciences. The periodontal parameters included bleeding on probing (BOP), clinical attachment loss (CAL), probing depth (PD), and plaque index (PI).
In order to minimize the effects of hormonal changes during the menstrual cycle on the status of periodontal tissue, the examinations of all the subjects were carried out in the early follicular phase of the menstrual cycle. ,,,
The BOP, PD, and CAL were calculated at six sites on each tooth except for the third molars. The BOP was assessed based on NIDCR protocol and after drying gums with dental compressed air. This index was reported in percentage.  According to the classification proposed by the American Academy of Periodontology, PD was calculated in percentages and based on involvement of the gums around the tooth surfaces. The involvement of more than 30% and <30% of all surfaces were described as generalized periodontitis and localized periodontitis, respectively. , CAL was determined by measuring the distance from the bottom of the periodontal pocket to the cemento-enamel junction using a periodontal probe. This index was used for describing the severity of periodontitis (slight: 1-2 mm of CAL; moderate: 3-4 mm of CAL; and severe >5 mm of CAL). ,
To calculate the PI, all participants rinsed for 30 s with a disclosing solution.
The O'Leary index consisted of recording the presence or absence of disclosed plaque on the mesial, distal, buccal, and lingual surfaces of all teeth. The percentage of disclosed plaque was then calculated for each participant. When 10% or less of the surfaces contain plaques, a reasonable periodontal health exists. 
Statistical analysis was done using SPSS software version 20.0 (SPSS Inc., Chicago, IL, USA). For all variables, the Kolmogorov-Smirnov test was used to assess normality. For normally distributed variables, independent sample t-tests were applied, and data were presented in mean ± standard deviation. The Mann-Whitney U-test was applied for nonnormally distributed variables. Pearson's Chi-square test was used to compare qualitative data. If the data in a group were <5, Fisher's exact test was used. The relationship between PCOS and CAL was investigated using univariate analysis of variance and by controlling for confounding variables such as BMI and PI. Statistical significance was defined at P < 0.05.
| Results|| |
The mean age in the systematically healthy control group and patient with PCOS group were 29.1 ± 6.6 years (ranging 19-45 years) and 28.6 ± 6.4 years (ranging 19-45 years), respectively. Clinical characteristics and periodontal parameters of both groups are summarized in [Table 1]. BMI, FBS, TG, LDL, HDL, testosterone, and serum NO levels were not significantly different between two groups. Although two groups were matched, the number of women suffering from hirsutism in the case group was significantly higher (P < 0.001).
|Table 1: Clinical characteristics and periodontal parameters of the PCOS and control groups|
Click here to view
The mean number of missing teeth in the PCOS group was 2.2 ± 1.9 (range: 0-7). In the non-PCOS group, the mean number of missing teeth was 2.0 ± 1.7 (range: 0-8) which was not statistically different from the PCOS group (P = 0.384).
Women with PCOS had significantly higher PI as compared with non-PCOS group (41.1 ± 14.2% vs. 32.8 ± 11.3%, P = 0.0001) in the PCOS and non-PCOS groups, respectively, which indicated a significantly higher rate of PI in women with PCOS.
The BOP in the case and control groups was 3.0 ± 2.6% and 1.4 ± 1.8%, respectively, which showed higher rate of BOP in women suffering from PCOS (P = 0.0001).
CAL in the PCOS group was 2.2 ± 0.4 mm. The mean CAL for the control group was 2.0 ± 0.3 mm. Mann-Whitney U-test indicated a significant difference between CAL between study groups (P = 0.001). Although univariate analysis of variance with regard to confounding factors such as PI and BMI showed that CAL as the main indicator of periodontitis in the two groups was not statistically significant (adjusted R2 = 0.408 P = 0.201), this finding reflected the impact of confounding variables.
In the PCOS group, 92 subjects (93.9%) were affected by slight periodontitis and 6 patients (6.1%) were diagnosed with moderate periodontitis. Slight periodontitis was observed in 97 subjects (99%) in the control group while only one subject (1%) was reported to have moderate periodontitis. Fisher's exact test failed to reveal any significant difference between these groups in terms of periodontitis severity. The detailed results of periodontal examination are presented in [Table 2].
| Discussion|| |
Very few studies are focused on the periodontal parameters in women suffering from PCOS. , Our results revealed higher prevalence of periodontal disease parameters in PCOS women comparing to systematically healthy controls who were matched in terms of possible confounding variables such as age and BMI. These findings are compatible with Dursun et al.  study that showed higher periodontal disease indexes including significant among women with PCOS.
The association of gingivitis with hormonal changes during puberty, pregnancy, and menstrual cycles has been studied well.  Increased production of steroid hormones is associated with increased gingival inflammation. The effects of estrogen on the gingival epithelium, collagen synthesis, osteoblasts, and bony tissues are important factors in the development of periodontal disease. Estrogen and progesterone affect the capillary system, inflammation, and angiogenesis processes. These alterations lead to excessive proliferation of vascular endothelial cells and epithelial keratinization in gums.
The hyperandrogenism status in patients with PCOS not only results in menstrual abnormalities and infertility but also may pose an increased risk of periodontal diseases to these patients. Regarding the conversion of testosterone to estrogen in women with PCOS, the paradox of co-excising of high levels of estrogen and testosterone is appreciable.
The increased vulnerability of PCOS patients to periodontal diseases can be explained regarding the influence of altered circulating hormones in on periodontal tissues. These derangements impact gingival tissues through initiating changes in oral flora and pro-inflammatory cytokines. In turn, these changes adversely affect bones, adhesive joints and eventually lead to tooth loss.  Furthermore, enhanced oxidative stress in affected periodontal tissues may participate in the pathology of PCOS by mechanisms such as increasing glucose intolerance and dyslipidemia. 
Our analysis failed to show any significant difference in tooth loss rate and disease severity between study groups. Of note, periodontal disease and their subsequent complications such as tooth loss and bone loss are chronic in nature.  Our results may be due to relatively low age of PCOS patients (28.8 ± 6.5 years) in our study. Longstanding periodontitis and severe forms of disease accentuate the progression of adverse outcomes. Comparison of tooth loss index in an older study population including women with and without PCOS may reveal greater contribution to the assessment of this index. In a recent study, Porwal et al.  showed that the frequency of mild periodontitis in PCOS and healthy women was not statistically significant which is consistent with our study. However, the frequency of moderate periodontitis was higher in PCOS group compare to control subjects. In our study, neither case nor control groups were periodontally healthy which opposed to the Porwal et al. study.
Consistent with previous studies, the higher BOP rates in patients with PCOS were compatible with the known impact of hyperandrogenism on vascular flora.  Also, the increased CAL in the patients with PCOS group might be attributed to an increased susceptibility to activation of inflammatory processes. These inflammatory processes play a great role in the development of periodontal disease and involvement of gingival supporting tissues, and subsequent gingival sulcus depth and bone loss.
The PI index was higher in PCOS group which may be considered as the main limitation of our study. The similar periodontitis severity in study groups may be due to the leading role of PI in the pathogenesis of periodontal disease. Future studies should focus on investigations in individuals matched for PI.
In this study, by matching individuals and excluding some factors such as age, obesity (BMI >25), smoking, and antibiotic therapy within the 6 months period prior to the study, we aimed to minimize the effects of confounding factors. In order to eliminate other factors such as socioeconomic status and genetics, subjects were selected from the same family or residential area. It is worth noting that many PCOS patients with abnormal glucose tolerance and metabolic syndrome are obese. In these patients, adipose tissue converts testosterone to estrogen by aromatase enzyme, triggering a vicious cycle of intense hormonal effects on periodontal tissues. These effects may cause greater likelihood for development of more severe forms of periodontitis in these patients. Therefore, further investigations in obese patients and patients with different degrees of PCOS severity are recommended.
Our study showed higher prevalence of periodontal disease parameters in nonobese women with PCOS comparing to systematically healthy controls. The findings need further confirmation in future studies systematically studying women with PCOS to elucidate any underlying relationships.
This study was supported by a grant from Vice Chancellor of Research of Hamadan University of Medical Sciences.
Financial support and sponsorship
This study was supported by a grant from Vice Chancellor of Research of Hamadan University of Medical Sciences.
Conflicts of interest
The authors of this manuscript declare that they have no conflicts of interest, real or perceived, financial or non-financial in this article.
| References|| |
Diamanti-Kandarakis E, Kouli CR, Bergiele AT, Filandra FA, Tsianateli TC, Spina GG, et al.
A survey of the polycystic ovary syndrome in the Greek island of Lesbos: Hormonal and metabolic profile. J Clin Endocrinol Metab 1999;84:4006-11.
March WA, Moore VM, Willson KJ, Phillips DI, Norman RJ, Davies MJ. The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Hum Reprod 2010;25:544-51.
Rahiminejad ME, Moaddab A, Rabiee R, Esna-Ashari F, Borzoui Sh, Hosseini SM. The relationship between clinicobiochemichal markers and depression in patient with polycystic ovary syndrome. Iran J Reprod Med 2014; 12:811-6.
Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 2004;81:19-25.
Sam S, Dunaif A. Polycystic ovary syndrome: Syndrome XX? Trends Endocrinol Metab 2003;14:365-70.
Evangelista O, McLaughlin MA. Review of cardiovascular risk factors in women. Gend Med 2009;6 Suppl 1:17-36.
Moran LJ, Misso ML, Wild RA, Norman RJ. Impaired glucose tolerance, type 2 diabetes and metabolic syndrome in polycystic ovary syndrome: A systematic review and meta-analysis. Hum Reprod Update 2010;16:347-63.
Wild RA. Dyslipidemia in PCOS. Steroids 2012;77:295-9.
Korhonen S, Hippeläinen M, Vanhala M, Heinonen S, Niskanen L. The androgenic sex hormone profile is an essential feature of metabolic syndrome in premenopausal women: A controlled community-based study. Fertil Steril 2003;79:1327-34.
Katz J, Flugelman MY, Goldberg A, Heft M. Association between periodontal pockets and elevated cholesterol and low density lipoprotein cholesterol levels. J Periodontol 2002;73:494-500.
Reeves AF, Rees JM, Schiff M, Hujoel P. Total body weight and waist circumference associated with chronic periodontitis among adolescents in the United States. Arch Pediatr Adolesc Med 2006;160:894-9.
Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol 2005;76 11 Suppl:2075-84.
Kim J, Amar S. Periodontal disease and systemic conditions: A bidirectional relationship. Odontology 2006;94:10-21.
Marchetti E, Monaco A, Procaccini L, Mummolo S, Gatto R, Tetè S, et al.
Periodontal disease: The influence of metabolic syndrome. Nutr Metab (Lond) 2012;9:88.
Liu Z, Liu Y, Song Y, Zhang X, Wang S, Wang Z. Systemic oxidative stress biomarkers in chronic periodontitis: A meta-analysis. Dis Markers 2014;2014:931083.
Duleba AJ, Dokras A. Is PCOS an inflammatory process? Fertil Steril 2012;97:7-12.
Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M. Metabolic syndrome and periodontitis: Is oxidative stress a common link? J Dent Res 2009;88:503-18.
Murri M, Luque-Ramírez M, Insenser M, Ojeda-Ojeda M, Escobar-Morreale HF. Circulating markers of oxidative stress and polycystic ovary syndrome (PCOS): A systematic review and meta-analysis. Hum Reprod Update 2013;19:268-88.
Chaffee BW, Weston SJ. Association between chronic periodontal disease and obesity: A systematic review and meta-analysis. J Periodontol 2010;81:1708-24.
Sharland G, Rollings S, Simpson J, Anderson D. Hypoplastic left-heart syndrome. Lancet 2001;357:722.
Koreeda N, Iwano Y, Kishida M, Otsuka A, Kawamoto A, Sugano N, et al.
Periodic exacerbation of gingival inflammation during the menstrual cycle. J Oral Sci 2005;47:159-64.
Machtei EE, Mahler D, Sanduri H, Peled M. The effect of menstrual cycle on periodontal health. J Periodontol 2004;75:408-12.
Shourie V, Dwarakanath CD, Prashanth GV, Alampalli RV, Padmanabhan S, Bali S. The effect of menstrual cycle on periodontal health - A clinical and microbiological study. Oral Health Prev Dent 2012;10:185-92.
Dursun E, Akalin FA, Güncü GN, Çinar N, Aksoy DY, Tözüm TF, et al.
Periodontal disease in polycystic ovary syndrome. Fertil Steril 2011;95:320-3.
Ramachandra SS, Mehta DS, Sandesh N, Baliga V, Amarnath J. Periodontal probing systems: A review of available equipment. Compend Contin Educ Dent 2011;32:71-7.
Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: Diagnosis and treatment. Clin Microbiol Rev 2001;14:727-52.
Kinane DF. Periodontitis modified by systemic factors. Ann Periodontol 1999;4:54-64.
Tonetti MS, Mombelli A. Early-onset periodontitis. Ann Periodontol 1999;4:39-53.
Butler BL, Morejon O, Low SB. An accurate, time-efficient method to assess plaque accumulation. J Am Dent Assoc 1996;127:1763-6.
Porwal S, Tewari S, Sharma RK, Singhal SR, Narula SC. Periodontal status and high-sensitivity C-reactive protein levels in polycystic ovary syndrome with and without medical treatment. J Periodontol 2014;85:1380-9.
Markou E, Eleana B, Lazaros T, Antonios K. The influence of sex steroid hormones on gingiva of women. Open Dent J 2009;3:114-9.
Brooks JK. The effects of hormonal oral contraceptives on the female human periodontium and experimental animal models, a review of the literature. J Baltimore Coll Dent Surg 1980;33:12-6.
[Table 1], [Table 2]
|This article has been cited by|
||Evaluation of Oxidative Status in Patients With Chronic Periodontitis and Polycystic Ovary Syndrome: A Cross-Sectional Study
| ||Ebru Saglam,Cenk Fatih Canakci,Saime Ozbek Sebin,Nesrin Saruhan,Metin Ingec,Hümeyra Canakci,Ufuk Sezer |
| ||Journal of Periodontology. 2017; : 1 |
|[Pubmed] | [DOI]|
||Association between periodontal disease and polycystic ovary syndrome: a systematic review
| ||S V Kellesarian,V R Malignaggi,T V Kellesarian,A A Al-Kheraif,M M Alwageet,H Malmstrom,G E Romanos,F Javed |
| ||International Journal of Impotence Research. 2017; |
|[Pubmed] | [DOI]|
||The Salivary Microbiome in Polycystic Ovary Syndrome (PCOS) and Its Association with Disease-Related Parameters: A Pilot Study
| ||Lisa Lindheim,Mina Bashir,Julia Münzker,Christian Trummer,Verena Zachhuber,Thomas R. Pieber,Gregor Gorkiewicz,Barbara Obermayer-Pietsch |
| ||Frontiers in Microbiology. 2016; 7 |
|[Pubmed] | [DOI]|