Skip to main content
Top
Published in: Clinical Oral Investigations 3/2021

Open Access 01-03-2021 | Insulins | Original Article

Subgingival microflora in adolescent females with polycystic ovary syndrome and its association with oral hygiene, gingivitis, and selected metabolic and hormonal parameters

Published in: Clinical Oral Investigations | Issue 3/2021

Login to get access

Abstract

Objectives

Research studies suggest that polycystic ovary syndrome (PCOS) may influence the composition of the oral microflora in women. This study aimed to investigate factors affecting the number of selected periopathogens in a young cohort of females with PCOS and to assess the association between oral hygiene, subgingival microbiome, gingival health, and metabolic and hormonal parameters.

Materials and methods

Thirty-two subjects with PCOS and twenty-three healthy controls aged 15–19 years were examined periodontally by a calibrated dentist. A real-time PCR method was used for the identification of 9 subgingival microorganisms. Subjects with PCOS underwent blood tests for determination of FSH, LH, total testosterone, DHEA-S, estradiol, SHBG, fasting glucose, fasting insulin, and lipid profile.

Results

Gingival index (GI), the proportion of bleeding sites (BOP%), probing depth (PD), and plaque index (PLI) did not differ significantly between cases and healthy age-mates. The control group had significantly higher levels of Peptostreptococcus micros and substantially greater percentage of subjects infected by Treponema denticola. Capnocytophaga gingivalis count was positively correlated with the level of estradiol, while the concentration of HDL-C was negatively correlated with the number of Aggregatibacter actinomycetemcomitans and orange complex bacteria.

Conclusions

PCOS in young patients was not associated with higher pathogenicity of subgingival biofilms.

Clinical relevance

Further studies are needed to explain the relationship between hormonal and metabolic abnormalities, subgingival microflora, and periodontal health in patients with PCOS.
Literature
1.
go back to reference Mascarenhas P, Gapski R, Al-Shammari K, Wang HL (2003) Influence of sex hormones on the periodontium. J Clin Periodontol 30:671–681CrossRef Mascarenhas P, Gapski R, Al-Shammari K, Wang HL (2003) Influence of sex hormones on the periodontium. J Clin Periodontol 30:671–681CrossRef
2.
go back to reference Caton JG, Armitage G, Berglundh T, Chapple ILC, Jepsen S, Kornman KS, Mealey BL, Papapanou PN, Sanz M, Tonetti MS (2018) A new classification scheme for periodontal and peri-implant diseases and conditions - introduction and key changes from the 1999 classification. J Periodontol 89(Suppl 1):S1–S8PubMed Caton JG, Armitage G, Berglundh T, Chapple ILC, Jepsen S, Kornman KS, Mealey BL, Papapanou PN, Sanz M, Tonetti MS (2018) A new classification scheme for periodontal and peri-implant diseases and conditions - introduction and key changes from the 1999 classification. J Periodontol 89(Suppl 1):S1–S8PubMed
3.
go back to reference Kellesarian SV, Malignaggi VR, Kellesarian TV, 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 29:89–95CrossRef Kellesarian SV, Malignaggi VR, Kellesarian TV, 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 29:89–95CrossRef
4.
go back to reference Özçaka Ö, Ceyhan BO, Akcali A, Bicakci N, Lappin DF, Buduneli N (2012) Is there an interaction between policystic ovary syndrome and gingival inflammation? J Periodontol 83:1529–1537CrossRef Özçaka Ö, Ceyhan BO, Akcali A, Bicakci N, Lappin DF, Buduneli N (2012) Is there an interaction between policystic ovary syndrome and gingival inflammation? J Periodontol 83:1529–1537CrossRef
5.
go back to reference Akcali A, Bostanci N, Özçaka Ö, Öztürk-Ceyhan B, Gümüş P, Buduneli N, Belibasakis GN (2014) Association between polycystic ovary syndrome, oral microbiota and systemic antibody responses. PLoS One 9:e108074CrossRef Akcali A, Bostanci N, Özçaka Ö, Öztürk-Ceyhan B, Gümüş P, Buduneli N, Belibasakis GN (2014) Association between polycystic ovary syndrome, oral microbiota and systemic antibody responses. PLoS One 9:e108074CrossRef
6.
go back to reference Rahiminejad ME, Moaddab A, Zaryoun H, Rabiee S, Moaddab A, Khodadoustan A (2015) Comparison of prevalence of periodontal disease in woman with polycystic ovary syndrome and healthy controls. Dent Res J (Ishfahan) 21:619–625 Rahiminejad ME, Moaddab A, Zaryoun H, Rabiee S, Moaddab A, Khodadoustan A (2015) Comparison of prevalence of periodontal disease in woman with polycystic ovary syndrome and healthy controls. Dent Res J (Ishfahan) 21:619–625
7.
go back to reference Dursun E, Akalin FA, Guncu GN, Cinar N, Aksoy DY, Tozum TF, Kılınc K, Yıldız BO (2011) Periodontal disease in polycystic ovary syndrome. Fertil Steril 95:320–323CrossRef Dursun E, Akalin FA, Guncu GN, Cinar N, Aksoy DY, Tozum TF, Kılınc K, Yıldız BO (2011) Periodontal disease in polycystic ovary syndrome. Fertil Steril 95:320–323CrossRef
8.
go back to reference 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 85:1380–1389CrossRef 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 85:1380–1389CrossRef
9.
go back to reference Varadan M, Gopalkrishna P, Bhat PV, Kamath SU, Krithishree S, Thriveni GK, Kumar S (2019) Influence of polycystic ovary syndrome on the periodontal health of Indian women visiting a secondary health care centre. Clin Oral Investig 23:3249–3255CrossRef Varadan M, Gopalkrishna P, Bhat PV, Kamath SU, Krithishree S, Thriveni GK, Kumar S (2019) Influence of polycystic ovary syndrome on the periodontal health of Indian women visiting a secondary health care centre. Clin Oral Investig 23:3249–3255CrossRef
10.
go back to reference Sirmans SM, Pate KA (2014) Epidemiology. Diagnosis. And management of polycystic ovary syndrome. Clin Epidemiol 6:1–13 Sirmans SM, Pate KA (2014) Epidemiology. Diagnosis. And management of polycystic ovary syndrome. Clin Epidemiol 6:1–13
11.
go back to reference The Rotterdam ESHRE/ASRM-Sponsored PCOS consensus workshop group (2004) Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod 19:41–47CrossRef The Rotterdam ESHRE/ASRM-Sponsored PCOS consensus workshop group (2004) Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod 19:41–47CrossRef
13.
go back to reference Yıldız BO, Bolour S, Woods K, Moore A, Azziz R (2010) Visually scoring hirsutism. Hum Reprod Update 16:51–64CrossRef Yıldız BO, Bolour S, Woods K, Moore A, Azziz R (2010) Visually scoring hirsutism. Hum Reprod Update 16:51–64CrossRef
14.
go back to reference Melina A, Dinh NN, Tafuri B, Schipani G, Nisticò S, Cosentino C, Amato F, Thiboutot D, Cherubini A (2018) Artificial intelligence for the objective evaluation of acne investigator global assessment. J Drugs Dermatol 17:1006–1009PubMed Melina A, Dinh NN, Tafuri B, Schipani G, Nisticò S, Cosentino C, Amato F, Thiboutot D, Cherubini A (2018) Artificial intelligence for the objective evaluation of acne investigator global assessment. J Drugs Dermatol 17:1006–1009PubMed
17.
go back to reference Hiremath SS (2011) Dental public health. Indices. In: Hiremath SS (ed) Textbook of preventive and community dentistry, 2nd edn. Elsevier, New Delhi, pp 198–221 Hiremath SS (2011) Dental public health. Indices. In: Hiremath SS (ed) Textbook of preventive and community dentistry, 2nd edn. Elsevier, New Delhi, pp 198–221
18.
go back to reference Kotsilkov K, Popova C, Boyanova L, Setchanova L, Mitov I (2015) Comparison of culture method and real-time PCR for detection of putative periodontopathogenic bacteria in deep periodontal pockets. Biotechnol Biotechnol Equip 29:1–7CrossRef Kotsilkov K, Popova C, Boyanova L, Setchanova L, Mitov I (2015) Comparison of culture method and real-time PCR for detection of putative periodontopathogenic bacteria in deep periodontal pockets. Biotechnol Biotechnol Equip 29:1–7CrossRef
19.
go back to reference Loe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38(Suppl):610–606CrossRef Loe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38(Suppl):610–606CrossRef
20.
go back to reference Bui HN, Sluss PM, Hayes FJ, Blincko S, Knol DL, Blankenstein MA, Heijboer AC (2015) Testosterone, free testosterone, and free androgen index in women: reference intervals, biological variation, and diagnostic value in polycystic ovary syndrome. Clin Chim Acta 23:227–232CrossRef Bui HN, Sluss PM, Hayes FJ, Blincko S, Knol DL, Blankenstein MA, Heijboer AC (2015) Testosterone, free testosterone, and free androgen index in women: reference intervals, biological variation, and diagnostic value in polycystic ovary syndrome. Clin Chim Acta 23:227–232CrossRef
22.
go back to reference Banaszewska B, Spaczyński RZ, Pelesz M, Pawelczyk L (2003) Incidence of elevated LH/FSH ratio in polycystic ovary syndrome women with normo- and hyperinsulinemia. Rocz Akad Med Bialymst 48:131–134PubMed Banaszewska B, Spaczyński RZ, Pelesz M, Pawelczyk L (2003) Incidence of elevated LH/FSH ratio in polycystic ovary syndrome women with normo- and hyperinsulinemia. Rocz Akad Med Bialymst 48:131–134PubMed
23.
go back to reference Chapple ILC, Mealey BL, Van Dyke TE, Bartold PM, Dommisch H, Eickholz P, Geisinger ML, Genco RJ, Glogauer M, Goldstein M (2018) Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: consensus report of workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions. J Clin Periodontol 45:68–77. https://doi.org/10.1111/jcpe.12940CrossRef Chapple ILC, Mealey BL, Van Dyke TE, Bartold PM, Dommisch H, Eickholz P, Geisinger ML, Genco RJ, Glogauer M, Goldstein M (2018) Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: consensus report of workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions. J Clin Periodontol 45:68–77. https://​doi.​org/​10.​1111/​jcpe.​12940CrossRef
24.
go back to reference Güncü GN, Tözüm TF, Cağlayan F (2005) Effects of endogenous sex hormones on the periodontium-review of literature. Aust Dent J 503:138–145CrossRef Güncü GN, Tözüm TF, Cağlayan F (2005) Effects of endogenous sex hormones on the periodontium-review of literature. Aust Dent J 503:138–145CrossRef
26.
go back to reference Kornman KS, Loesche WJ (1982) Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun 35:256–263CrossRef Kornman KS, Loesche WJ (1982) Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun 35:256–263CrossRef
28.
go back to reference Fteita D, Könönen E, Gürsoy M, Söderling E, Gürsoy UK (2015) Does estradiol have an impact on the dipeptidyl peptidase IV enzyme activity of the Prevotella intermedia group bacteria? Anaerobe 36:14–18CrossRef Fteita D, Könönen E, Gürsoy M, Söderling E, Gürsoy UK (2015) Does estradiol have an impact on the dipeptidyl peptidase IV enzyme activity of the Prevotella intermedia group bacteria? Anaerobe 36:14–18CrossRef
30.
go back to reference Nakagawa S, Fujii H, Machida Y, Okuda K (1994) A longitudinal study from prepuberty to puberty of gingivitis. Correlation between the occurrence of Prevotella intermedia and sex hormones. J Clin Periodontol 21:658–665CrossRef Nakagawa S, Fujii H, Machida Y, Okuda K (1994) A longitudinal study from prepuberty to puberty of gingivitis. Correlation between the occurrence of Prevotella intermedia and sex hormones. J Clin Periodontol 21:658–665CrossRef
31.
go back to reference Al-Hebshi NN, Shuga-Aldin HM, Al-Sharabi AK, Ghandour I (2014) Subgingival periodontal pathogens associated with chronic periodontitis in Yemenis. BMC Oral Health 18:14–13 Al-Hebshi NN, Shuga-Aldin HM, Al-Sharabi AK, Ghandour I (2014) Subgingival periodontal pathogens associated with chronic periodontitis in Yemenis. BMC Oral Health 18:14–13
32.
go back to reference Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144CrossRef Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144CrossRef
34.
go back to reference Pawlaczyk-Kamieńska T, Batura-Gabryel H, Borysewicz-Lewicka M, Cofta S (2019) Periodontal status and subgingival biofilms in cystic fibrosis adults. Pol J Microbiol 68:377–382CrossRef Pawlaczyk-Kamieńska T, Batura-Gabryel H, Borysewicz-Lewicka M, Cofta S (2019) Periodontal status and subgingival biofilms in cystic fibrosis adults. Pol J Microbiol 68:377–382CrossRef
36.
go back to reference Gołyńska M, Polkowska I, Bartoszcze-Tomaszewska M, Sobczyńska-Rak A, Matuszewski Ł (2017) Molecular-level evaluation of selected periodontal pathogens from subgingival regions in canines and humans with periodontal disease. J Vet Sci 18:51–58CrossRef Gołyńska M, Polkowska I, Bartoszcze-Tomaszewska M, Sobczyńska-Rak A, Matuszewski Ł (2017) Molecular-level evaluation of selected periodontal pathogens from subgingival regions in canines and humans with periodontal disease. J Vet Sci 18:51–58CrossRef
37.
go back to reference Tanner AC, Kent RJ, Kanasi E, Lu SC, Paster BJ, Sonis ST, Murray LA, Van Dyke TE (2007) Clinical characteristics and microbiota of progressing slight chronic periodontitis in adults. J Clin Periodontol 34:917–930CrossRef Tanner AC, Kent RJ, Kanasi E, Lu SC, Paster BJ, Sonis ST, Murray LA, Van Dyke TE (2007) Clinical characteristics and microbiota of progressing slight chronic periodontitis in adults. J Clin Periodontol 34:917–930CrossRef
38.
go back to reference Mitova N, Rashkova M, Popova C (2019) Studying subgingival microorganisms in children with gingivitis in puberty. J of IMAB 25:2822–2827 Mitova N, Rashkova M, Popova C (2019) Studying subgingival microorganisms in children with gingivitis in puberty. J of IMAB 25:2822–2827
39.
go back to reference Ehrmann E, Jolivet-Gougeon A, Bonnaure-Mallet M, Fosse T (2016) Multidrug-resistant oral Capnocytophaga gingivalis responsible for an acute exacerbation of chronic obstructive pulmonary disease: case report and literature review. Anaerobe 42:50–54 Ehrmann E, Jolivet-Gougeon A, Bonnaure-Mallet M, Fosse T (2016) Multidrug-resistant oral Capnocytophaga gingivalis responsible for an acute exacerbation of chronic obstructive pulmonary disease: case report and literature review. Anaerobe 42:50–54
40.
go back to reference Abraham S, Premnath A, Arunima PR, Reejamol MK (2019) Critical appraisal of bidirectional relationship between periodontitis and hyperlipidemia. J Int Soc Prev Community Dent 9:112–118CrossRef Abraham S, Premnath A, Arunima PR, Reejamol MK (2019) Critical appraisal of bidirectional relationship between periodontitis and hyperlipidemia. J Int Soc Prev Community Dent 9:112–118CrossRef
41.
go back to reference Lee KS, Lee SG, Kim EK (2015) Metabolic syndrome parameters in adolescents may be determinants for the future periodontal diseases. J Clin Periodontol 42:105–112CrossRef Lee KS, Lee SG, Kim EK (2015) Metabolic syndrome parameters in adolescents may be determinants for the future periodontal diseases. J Clin Periodontol 42:105–112CrossRef
42.
go back to reference Jaramillo A, Lafaurie GI, Millan LV, Ardila CM, Duque A, Novoa C, Lopez D, Contreras A (2013) Association between periodontal disease and plasma levels of cholesterol and triglycerides. Colomb Med (Cali) 44:80–86CrossRef Jaramillo A, Lafaurie GI, Millan LV, Ardila CM, Duque A, Novoa C, Lopez D, Contreras A (2013) Association between periodontal disease and plasma levels of cholesterol and triglycerides. Colomb Med (Cali) 44:80–86CrossRef
45.
go back to reference Chen S, Lin G, You X, Lei L, Li Y, Lin M, Luo K, Yan F (2014) Hyperlipidemia causes changes in inflammatory responses to periodontal pathogen challenge: implications in acute and chronic infections. Arch Oral Biol 49:1075–1084CrossRef Chen S, Lin G, You X, Lei L, Li Y, Lin M, Luo K, Yan F (2014) Hyperlipidemia causes changes in inflammatory responses to periodontal pathogen challenge: implications in acute and chronic infections. Arch Oral Biol 49:1075–1084CrossRef
46.
go back to reference Shrestha D, Choi YH, Zhang J, Hazlett LJ, Merchant AT (2015) Relationship between serologic markers of periodontal bacteria and metabolic syndrome and its components. J Periodontol 86:418–430CrossRef Shrestha D, Choi YH, Zhang J, Hazlett LJ, Merchant AT (2015) Relationship between serologic markers of periodontal bacteria and metabolic syndrome and its components. J Periodontol 86:418–430CrossRef
47.
go back to reference Demmer RT, Jacobs DR, Singh JR, Zuk A, Rosenbaum M, Papapanou PN, Desvarieux M (2015) Periodontal bacteria and prediabetes prevalence in ORIGINS: the oral infections, glucose intolerance, and insulin resistance study. J Dent Res 94(Suppl 9):201–211CrossRef Demmer RT, Jacobs DR, Singh JR, Zuk A, Rosenbaum M, Papapanou PN, Desvarieux M (2015) Periodontal bacteria and prediabetes prevalence in ORIGINS: the oral infections, glucose intolerance, and insulin resistance study. J Dent Res 94(Suppl 9):201–211CrossRef
48.
go back to reference Nogueira Moreira A, Luna Davila G, Bianchini H, Alonso C, Piovano S (2000) Effect of supragingival plaque control on subgingival microflora and gingivo-periodontal tissues. Acta Odontol Latinoam 13:73–86PubMed Nogueira Moreira A, Luna Davila G, Bianchini H, Alonso C, Piovano S (2000) Effect of supragingival plaque control on subgingival microflora and gingivo-periodontal tissues. Acta Odontol Latinoam 13:73–86PubMed
49.
go back to reference De David SC, Mário TG, De Freitas GC, Kantorski KZ, Wikesjö UME, Moreira CHC (2018) Correlation between plaque control and gingival health using short and extended oral hygiene intervals. Clin Oral Investig 22:2593–2597CrossRef De David SC, Mário TG, De Freitas GC, Kantorski KZ, Wikesjö UME, Moreira CHC (2018) Correlation between plaque control and gingival health using short and extended oral hygiene intervals. Clin Oral Investig 22:2593–2597CrossRef
50.
go back to reference Drosdzol-Cop A, Sidło-Stawowy A, Sajda D, Skrzypulec-Plinta V (2014) Diagnosing polycystic ovary syndrome of adolescent girls. Ginekol Pol 85:145–148CrossRef Drosdzol-Cop A, Sidło-Stawowy A, Sajda D, Skrzypulec-Plinta V (2014) Diagnosing polycystic ovary syndrome of adolescent girls. Ginekol Pol 85:145–148CrossRef
51.
go back to reference Committee on Adolescent Health Care (2019) Screening and management of the hyperandrogenic adolescent: ACOG Committee Opinion, Number 789. Obstet Gynecol 134:106–114CrossRef Committee on Adolescent Health Care (2019) Screening and management of the hyperandrogenic adolescent: ACOG Committee Opinion, Number 789. Obstet Gynecol 134:106–114CrossRef
52.
go back to reference Kato I, Vasquez A, Moyerbrailean G, Land S, Djuric Z, Sun J, Lin H, Ram JL (2017) Nutritional correlates of human oral microbiome. J Am Coll Nutr 36:88–98CrossRef Kato I, Vasquez A, Moyerbrailean G, Land S, Djuric Z, Sun J, Lin H, Ram JL (2017) Nutritional correlates of human oral microbiome. J Am Coll Nutr 36:88–98CrossRef
Metadata
Title
Subgingival microflora in adolescent females with polycystic ovary syndrome and its association with oral hygiene, gingivitis, and selected metabolic and hormonal parameters
Publication date
01-03-2021
Published in
Clinical Oral Investigations / Issue 3/2021
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-020-03456-5

Other articles of this Issue 3/2021

Clinical Oral Investigations 3/2021 Go to the issue