periodontologyПародонтологияParodontologiya1683-37591726-7269Russian Periodontal Association (RPA)10.33925/1683-3759-2024-896periodontology-896Research ArticleОБЗОРREVIEWВзаимосвязь метаболического синдрома и сахарного диабета 2 типа с патологией пародонта (систематический обзор)Association between metabolic syndrome, type 2 diabetes mellitus, and periodontal pathology: a systematic reviewhttps://orcid.org/0000-0002-5593-085XСенинаВ. О.SeninaV. O.

Сенина Валерия Олеговна, аспирант кафедры терапевтической стоматологии

Уфа

Valeriia O. Senina, DMD, PhD-student, Department of Operative Dentistry, Assistant Professor

Ufa

lera.senina2012@yandex.ruhttps://orcid.org/0000-0002-1781-0291УсмановаИ. Н.UsmanovaI. N.

Усманова Ирина Николаевна, доктор медицинских наук, профессор кафедры терапевтической стоматологии

Уфа

Irina N. Usmanova, DMD, PhD, DSc, Professor, Department of Operative Dentistry

Ufa

irinausma@mail.ruhttps://orcid.org/0000-0001-9876-9202ЛакманИ. А.LakmanI. А.

Лакман Ирина Александровна, кандидат технических наук, доцент кафедры биомедицинской инженерии, заведующая научной лабораторией исследования социально-экономических проблем регионов

Уфа

Irina A. Lakman, PhD, Associate Professor, Department of Biomedical Engineering, Head of the Scientific Laboratory for the Study of Social and Economic Problems

Ufa

lackmania@mail.ruhttps://orcid.org/0000-0002-1145-6500ГерасимоваЛ. П.GerasimovaL. P.

Герасимова Лариса Павловна, доктор медицинских наук, профессор, заведующая кафедрой терапевтической стоматологии

Уфа

Larisa P. Gerasimova, DMD, PhD, DSc, Professor, Head of the Department of Operative Dentistry

Ufa

gerasimovalarisa@rambler.ruhttps://orcid.org/0000-0002-5473-2034ТуйгуновМ. М.TuigunovМ. М.

Туйгунов Марсель Маратович, доктор медицинских наук, профессор, завeдующий кафедрой микробиологии и вирусологии

Уфа

Marcel M. Tuigunov, PhD, DSc, Professor, Head of the Department of Microbiology and Virology

Ufa

tuygunov@mail.ruhttps://orcid.org/0000-0003-0892-0058ИшмухаметоваА. Н.IshmukhametovaA. N.

Ишмухаметова Амина Насимовна, кандидат медицинских наук. доцент кафедры внутренних болезней и клинической психологии

Уфа

Amina N. Ishmukhametova, MD, PhD, Associate Professor, Department of Internal Medicine and Clinical Psychology

Ufa

amina.ishmukhametova@mail.ruhttps://orcid.org/0000-0002-1590-6433АвзалетдиноваД. Ш.AvzaletdinovaD. Sh.

Авзалетдинова Диана Шамилевна, доктор медицинских наук, доцент кафедры эндокринологии

Уфа

Diana S. Avzaletdinova, MD, PhD, DSc, Associate Professor, Department of the Endocrinology

Ufa

hyppocrat@mail.ruhttps://orcid.org/0000-0002-6020-1686КузнецоваЛ. И.KuznetsovaL. I.

Кузнецова Лилия Ильинична, кандидат медицинских наук, доцент кафедры терапевтической стоматологии

Уфа

Lilia I. Kuznetsova, DMD, PhD, Associate Professor, Department of the Operative Dentistry

Ufa

89177859529@mail.ruБашкирский государственный медицинский университетРоссияBashkir State Medical UniversityRussian FederationУфимский университет науки и технологийРоссияUfa University of Science and TechnologyRussian Federation202426062024292135149Copyright © Сенина В.О., Усманова И.Н., Лакман И.А., Герасимова Л.П., Туйгунов М.М., Ишмухаметова А.Н., Авзалетдинова Д.Ш., Кузнецова Л.И., 20242024Сенина В.О., Усманова И.Н., Лакман И.А., Герасимова Л.П., Туйгунов М.М., Ишмухаметова А.Н., Авзалетдинова Д.Ш., Кузнецова Л.И.Senina V.O., Usmanova I.N., Lakman I.А., Gerasimova L.P., Tuigunov М.М., Ishmukhametova A.N., Avzaletdinova D.S., Kuznetsova L.I.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.parodont.ru/jour/article/view/896Актуальность

Актуальность. Метаболический синдром (МС) и сахарный диабет 2 типа (СД2) является актуальной проблемой современной медицины в связи с его высокой распространенностью в общей популяции и существенной ролью в развитии и прогрессировании воспалительных заболеваний пародонта.

Цель

Цель. Изучение взаимосвязи заболеваний пародонта на фоне проявлений метаболического синдрома и сахарного диабета 2 типа (СД2).

Материалы и методы

Материалы и методы. Использован поиск современных источников литературы в PubMed, Medline, elibrary.ru, в период с 2016 по 2022 год. Для поиска публикаций (доступных на момент проведения поиска) основными критериями являлись распространенность метаболического синдрома – метаболический синдром (МС), сахарный диабет 2 типа (СД2) и инсулинорезистентность, наличие гингивита, пародонтита, гликемический контроль, дислипидемия, метаболизма липопротеинов.

Результаты

Результаты. Из 71 проанализированного источника в 39,1% работ рассматривается распространенность данных метаболических заболеваний. В подавляющем количестве исследований (50%) изучается взаимосвязь патологии пародонта и метаболических заболеваний, связанных с инсулинорезистентностью и СД2, уровня гликемии, дислипидемии и метаболизма жировой ткани. В 49,3% рассмотренных публикациях приводятся данные о состоянии поддесневой микробиоты, десневой борозды, слюны.

Заключение

Заключение. Анализ современных источников литературы показал достаточно широкое взаимодействие метаболических заболеваний и патологии пародонта, их общие патогенетические процессы, данные о гликемическом контроле, состоянии микробиоты ротовой жидкости и пародонтальных карманов.

Relevance

Relevance. The metabolic syndrome (MS) and type 2 diabetes mellitus (T2DM) are significant concerns in modern medicine due to their high prevalence in the general population and their crucial role in the development and progression of inflammatory periodontal diseases.

Purpose

Purpose. To investigate the association between periodontal diseases and the manifestations of metabolic syndrome and type 2 diabetes mellitus (T2DM).

Materials and methods

Materials and methods. The metabolic syndrome (MS) and type 2 diabetes mellitus (T2DM) are significant concerns in modern medicine due to their high prevalence in the general population and their crucial role in the development and progression of inflammatory periodontal diseases.

Results

Results. Out of 71 analysed sources, 39.1% of the studies discussed the prevalence of these metabolic diseases. In the majority of the studies (50%), the relationship between periodontal pathology and metabolic diseases related to insulin resistance and T2DM, glycaemia levels, dyslipidaemia, and fat tissue metabolism was examined. In 49.3% of the reviewed publications, data on the state of the subgingival microbiota, gingival sulcus, and saliva were presented.

Conclusion

Conclusion. The analysis of contemporary literature sources revealed a broad interaction between metabolic diseases and periodontal pathology, highlighting their shared pathogenetic processes and providing data on glycaemic control, the condition of the oral fluid microbiota, and periodontal pockets.

метаболический синдроминсулинорезистентностьсахарный диабет 2 типаиндекс массы телагликированный гемоглобинвоспалениепародонтитгингивитmetabolic syndromeinsulin resistancetype 2 diabetes mellitusbody mass indexglycated haemoglobininflammationperiodontitisgingivitisРазработка плана и дизайна исследования производилась всеми авторами, внесшими равнозначный вклад в написание рукописи. Окончательная версия рукописи была одобрена всеми авторами. Авторы не получали гонорар за исследование.The development of the research plan and design was carried out by all the authors who made an equal contribution to the writing of the manuscript. The final version of the manuscript was approved by all the authors. The authors did not receive a research fee.ReferencesCampos JR, Martins CC, Faria SFS, Carvalho AP, Pereira AG, Costa FO, et al. Association between components of metabolic syndrome and periodontitis: a systematic review and meta-analysis. Clin Oral Investig. 2022;26(9):5557-5574. doi: 10.1007/s00784-022-04583-xCampos JR, Martins CC, Faria SFS, Carvalho AP, Pereira AG, Costa FO, et al. Association between components of metabolic syndrome and periodontitis: a systematic review and meta-analysis. Clin Oral Investig. 2022;26(9):5557-5574. doi: 10.1007/s00784-022-04583-xCho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, et al. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271-281. doi: 10.1016/j.diabres.2018.02.023Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, et al. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271-281. doi: 10.1016/j.diabres.2018.02.023Graves DT, Ding Z, Yang Y. The impact of diabetes on periodontal diseases. Periodontol 2000. 2020;82(1):214-224. doi: 10.1111/prd.12318Graves DT, Ding Z, Yang Y. The impact of diabetes on periodontal diseases. Periodontol 2000. 2020;82(1):214-224. doi: 10.1111/prd.12318Iqbal J, Al Qarni A, Hawwari A, Alghanem AF, Ahmed G. Metabolic Syndrome, Dyslipidemia and Regulation of Lipoprotein Metabolism. Curr Diabetes Rev. 2018;14(5):427-433. doi: 10.2174/1573399813666170705161039Iqbal J, Al Qarni A, Hawwari A, Alghanem AF, Ahmed G. Metabolic Syndrome, Dyslipidemia and Regulation of Lipoprotein Metabolism. Curr Diabetes Rev. 2018;14(5):427-433. doi: 10.2174/1573399813666170705161039Ranjit R, Bista S, Manandhar P, Subedi S. Periodontitis and Diabetes: How Well the Patients have Knowledge about the Established Interrelationship? Kathmandu Univ Med J (KUMJ). 2022;20(77):87-92. Available from https://pubmed.ncbi.nlm.nih.gov/36273298/Ranjit R, Bista S, Manandhar P, Subedi S. Periodontitis and Diabetes: How Well the Patients have Knowledge about the Established Interrelationship? Kathmandu Univ Med J (KUMJ). 2022;20(77):87-92. Available from https://pubmed.ncbi.nlm.nih.gov/36273298/Rask Larsen J, Dima L, Correll CU, Manu P. The pharmacological management of metabolic syndrome. Expert Rev Clin Pharmacol. 2018;11(4):397-410. doi: 10.1080/17512433.2018.1429910Rask Larsen J, Dima L, Correll CU, Manu P. The pharmacological management of metabolic syndrome. Expert Rev Clin Pharmacol. 2018;11(4):397-410. doi: 10.1080/17512433.2018.1429910Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, Colagiuri S, et.all. IDF Diabetes Atlas Committee. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9 th edition. Diabetes Res Clin Pract. 2019;157:107843. doi: 10.1016/j.diabres.2019.107843Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, Colagiuri S, et.all. IDF Diabetes Atlas Committee. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9 th edition. Diabetes Res Clin Pract. 2019;157:107843. doi: 10.1016/j.diabres.2019.107843Sakurai SI, Yamada SI, Karasawa I, Sakurai A, Kurita H. A longitudinal study on the relationship between dental health and metabolic syndrome in Japan. J. Periodontol. 2019;90(7):728-746. doi: 10.1002/JPER.18-0523Sakurai SI, Yamada SI, Karasawa I, Sakurai A, Kurita H. A longitudinal study on the relationship between dental health and metabolic syndrome in Japan. J. Periodontol. 2019;90(7):728-746. doi: 10.1002/JPER.18-0523Кытикова ОЮ, Антонюк МВ, Кантур ТА, Новгородцева ТП, Денисенко ЮК. Распространенность и биомаркеры метаболического синдрома. Ожирение и метаболизм. 2021;18(3):302-312. doi: 10.14341/omet12704Kytikova OY, Antonyuk MV, Kantur TA, Novgorodtseva TP, Denisenko YK. Prevalence and biomarkers in metabolic syndrome. Obesity and metabolism. 2021;18(3):302-312 (In Russ.). doi: 10.14341/omet12704Bikbov MM, Kazakbaeva GM, Gilmanshin TR, Zainullin RM, Iakupova EM, Fakhretdinova AA, et al. Prevalence of metabolic syndrome in a Russian population: The Ural Eye and Medical Study and the Ural Very Old Study. Metabol Open. 2022;14:100183. doi: 10.1016/j.metop.2022.100183Bikbov MM, Kazakbaeva GM, Gilmanshin TR, Zainullin RM, Iakupova EM, Fakhretdinova AA, et al. Prevalence of metabolic syndrome in a Russian population: The Ural Eye and Medical Study and the Ural Very Old Study. Metabol Open. 2022;14:100183. doi: 10.1016/j.metop.2022.100183Беленков ЮН, Привалова ЕВ, Каплунова ВЮ, Зекцер ВЮ, Виноградова НН, Ильгисонис ИС, и др. Метаболический синдром: история развития, основные критерии диагностики. Рациональная Фармакотерапия в Кардиологиия. 2018;14(5):757-764. doi: 10.20996/1819-6446-2018-14-5-757-764Belenkov YN, Privalova EV, Kaplunova VY, Zektser VY, Vinogradova NN, Ilgisonis IS, et al. Metabolic Syndrome: Development of the Issue, Main Diagnostic Criteria. Rational Pharmacotherapy in Cardiology. 2018;14(5):757-764 (In Russ). doi: 10.20996/1819-6446-2018-14-5-757-764Успенский ЮП, Соусова ЯВ, Гулунов ЗХ, Фоминых ЮВ, Захаров ДВ. Актуальные проблемы метаболического синдрома и ассоциированных с ним клинических состояний. Дневник казанской медицинской школы. 2018;(3):182-187. Режим доступа. https://www.elibrary.ru/item.asp?id=36855759Uspenskiy YuP, Sousova YaV, Gulunov ZK, Fominykh YA, Zakharov DV, et al. Actual problems of metabolic syndrome and associated clinical conditions. Dnevnik kazanskoj medicinskoj shkoly. 2018;(3):182-187 (In Russ). Available from https://www.elibrary.ru/item.asp?id=36855759Иванова ЕГ, Потемина ТЕ. Метаболический синдром у пришлых жителей Крайнего Севера (на примере Ханты-Мансийского автономного округа – Югры). Ожирение и метаболизм. 2022;19(4):396-403. doi: 10.14341/omet12777Ivanova EG, Potemina TE. Metabolic syndrome in patients with arterial hypertension living in the Far North (on the example of the Khanty-Mansi Autonomous Okrug – Yugra). Obesity and metabolism. 2022;19(4):396-403 (In Russ.). doi: 10.14341/omet12777Saklayen MG. The Global Epidemic of the Metabolic Syndrome. Curr Hypertens Rep. 2018;20(2):12. doi: 10.1007/s11906-018-0812-zSaklayen MG. The Global Epidemic of the Metabolic Syndrome. Curr Hypertens Rep. 2018;20(2):12. doi: 10.1007/s11906-018-0812-zFahed G, Aoun L, Bou Zerdan M, Allam S, Bou Zerdan M, Bouferraa Y, Assi HI. Metabolic Syndrome: Updates on Pathophysiology and Management in 2021. Int J Mol Sci. 2022;12;23(2):786. doi: 10.3390/ijms23020786Fahed G, Aoun L, Bou Zerdan M, Allam S, Bou Zerdan M, Bouferraa Y, Assi HI. Metabolic Syndrome: Updates on Pathophysiology and Management in 2021. Int J Mol Sci. 2022;12;23(2):786. doi: 10.3390/ijms23020786Фоминых ЮА, Горбачева ИА, Успенский ЮП, Гулунов ЗХ, Соусова ЯВ. Психологический статус и качество жизни пациентов с метаболическим синдромом. Медицинский алфавит. 2019;3(20):46-50. doi 10.33667/2078-5631-2019-2-20(395)-46-50Fominykh YuA, Gorbachyova IA, Uspenskiy YuP, Gulunov ZKh, Sousova YaV. Psychological status and quality of life of patients with metabolic syndrome. Medical alphabet. 2019;3(20):46-50 (In Russ.). doi 10.33667/2078-5631-2019-2-20(395)-46-50Успенский ЮП, Горбачева ИА, Фоминых ЮА, Барышникова НВ, Шевяков МА. Роль инфекции Helicobacter pylori и дрожжеподобных грибов Candida spp. в патогенезе метаболического синдрома. University Therapeutic Journal. 2021;3(3):35-46. Режим доступа: https://ojs3.gpmu.org/index.php/Un-ther-journal/article/view/3834Uspenskiy YP, Gorbacheva IA, Fominykh YuA, Baryshnikova NV, Shevyakov MA. The role of Helicobacter pylori infection and Сandida spp. in the pathogenesis of metabolic syndrome. University Therapeutic Journal. 2021;3(3):35-46 (In Russ.). Available from: https://ojs3.gpmu.org/index.php/Un-ther-journal/article/view/3834Фоминых ЮА, Шапорова НЛ, Горбачева ИА, Иванов СВ, Успенский ЮП. Инфекционные агенты, микробиота и метаболический синдром. Дневник казанской медицинской школы. 2018;(1):104-107. Режим доступа: https://www.elibrary.ru/item.asp?id=32850041Fominykh YuA, Shaporova NL, Gorbacheva IA, Ivanov SV, Uspenskiy YP. Infectious agents, microbiota and metabolic syndrome. Dnevnik kazanskoj medicinskoj shkoly. 2018;(1):104-107 (In Russ.).Available from: https://www.elibrary.ru/item.asp?id=32850041Abdalla-Aslan R, Findler M, Levin L, Zini A, Shay B, Twig G, et al. Where periodontitis meets metabolic syndrome-The role of common health-related risk factors. J Oral Rehabil. 2019;46(7):647-656. doi: 10.1111/joor.12798Abdalla-Aslan R, Findler M, Levin L, Zini A, Shay B, Twig G, et al. Where periodontitis meets metabolic syndrome-The role of common health-related risk factors. J Oral Rehabil. 2019;46(7):647-656. doi: 10.1111/joor.12798Ansarimoghaddam A, Adineh HA, Zareban I, Iranpour S, Hossein Zadeh A, Kh F. Prevalence of metabolic syndrome in Middle-East countries: Meta-analysis of cross-sectional studies. Diabetes Metab Syndr. 2018;12(2):195-201. doi: 10.1016/j.dsx.2017.11.004Ansarimoghaddam A, Adineh HA, Zareban I, Iranpour S, Hossein Zadeh A, Kh F. Prevalence of metabolic syndrome in Middle-East countries: Meta-analysis of cross-sectional studies. Diabetes Metab Syndr. 2018;12(2):195-201. doi: 10.1016/j.dsx.2017.11.004Ranasinghe P, Mathangasinghe Y, Jayawardena R, Hills AP, Misra A. Prevalence and trends of metabolic syndrome among adults in the asia-pacific region: a systematic review. BMC Public Health. 2017;17(1):101. doi: 10.1186/s12889-017-4041-1Ranasinghe P, Mathangasinghe Y, Jayawardena R, Hills AP, Misra A. Prevalence and trends of metabolic syndrome among adults in the asia-pacific region: a systematic review. BMC Public Health. 2017;17(1):101. doi: 10.1186/s12889-017-4041-1Mongraw-Chaffin M, Foster MC, Anderson CAM [et.all]. Metabolically Healthy Obesity, Transition to Metabolic Syndrome, and Cardiovascular Risk. J. Am Coll Cardiol. 2018;71(17):1857-1865 doi: 10.1016/j.jacc.2018.02.055Mongraw-Chaffin M, Foster MC, Anderson CAM [et.all]. Metabolically Healthy Obesity, Transition to Metabolic Syndrome, and Cardiovascular Risk. J. Am Coll Cardiol. 2018;71(17):1857-1865 doi: 10.1016/j.jacc.2018.02.055Wu CZ, Yuan YH, Liu HH, Li SS, Zhang BW, Chen W, et al. Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health. 2020;20(1):204. doi: 10.1186/s12903-020-01180-wWu CZ, Yuan YH, Liu HH, Li SS, Zhang BW, Chen W, et al. Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health. 2020;20(1):204. doi: 10.1186/s12903-020-01180-wGobin R, Tian D, Liu Q, Wang J. Periodontal Diseases and the Risk of Metabolic Syndrome: An Updated Systematic Review and Meta-Analysis. Front Endocrinol (Lausanne). 2020;11:336. doi: 10.3389/fendo.2020.00336Gobin R, Tian D, Liu Q, Wang J. Periodontal Diseases and the Risk of Metabolic Syndrome: An Updated Systematic Review and Meta-Analysis. Front Endocrinol (Lausanne). 2020;11:336. doi: 10.3389/fendo.2020.00336Campos JR, Costa FO, Cota LOM. Association between periodontitis and metabolic syndrome: A case-control study. J Periodontol. 2020;91(6):784-791. doi: 10.1002/JPER.19-0298Campos JR, Costa FO, Cota LOM. Association between periodontitis and metabolic syndrome: A case-control study. J Periodontol. 2020;91(6):784-791. doi: 10.1002/JPER.19-0298Janem WF, Scannapieco FA, Sabharwal A, Tsompana M, Berman HA, Haase EM, et al. Salivary inflammatory markers and microbiome in normoglycemic lean and obese children compared to obese children with type 2 diabetes. PLoS One. 2017;12(3):e0172647. doi: 10.1371/journal.pone.0172647Janem WF, Scannapieco FA, Sabharwal A, Tsompana M, Berman HA, Haase EM, et al. Salivary inflammatory markers and microbiome in normoglycemic lean and obese children compared to obese children with type 2 diabetes. PLoS One. 2017;12(3):e0172647. doi: 10.1371/journal.pone.0172647Kaye EK, Chen N, Cabral HJ, Vokonas P, Garcia RI. Metabolic Syndrome and Periodontal Disease Progression in Men. J. Dent Res. 2016;95(7):822-8. doi: 0.1177/0022034516641053Kaye EK, Chen N, Cabral HJ, Vokonas P, Garcia RI. Metabolic Syndrome and Periodontal Disease Progression in Men. J. Dent Res. 2016;95(7):822-8. doi: 0.1177/0022034516641053Devi OM, Sood S, Gupta J, Jain A. Prevalence and Severity of Periodontal Disease and its Association with Type-II Diabetes Mellitus and Smoking by Using Periodontal Screening and Recording: A Retrospective Study. Indian J Community Med. 2024;49(1):56-63. doi: 10.4103/ijcm.ijcm_642_22Devi OM, Sood S, Gupta J, Jain A. Prevalence and Severity of Periodontal Disease and its Association with Type-II Diabetes Mellitus and Smoking by Using Periodontal Screening and Recording: A Retrospective Study. Indian J Community Med. 2024;49(1):56-63. doi: 10.4103/ijcm.ijcm_642_22Trentin MS, De Carli JP, Ferreira MD, Gambin DJ, da Silva SO, Lisboa H. Prevalence and severity of periodontal disease in type 2 diabetes mellitus patients: a cross-sectional study. Biosci J. 2018;34(4):1114-1123. doi: 10.14393/BJ-v34n1a2018-41485Trentin MS, De Carli JP, Ferreira MD, Gambin DJ, da Silva SO, Lisboa H. Prevalence and severity of periodontal disease in type 2 diabetes mellitus patients: a cross-sectional study. Biosci J. 2018;34(4):1114-1123. doi: 10.14393/BJ-v34n1a2018-41485Musskopf ML, Daudt LD, Weidlich P, Gerchman F, Gross JL, Oppermann RV. Metabolic syndrome as a risk indicator for periodontal disease and tooth loss. Clin Oral Investig. 2017;21(2):675-683. doi: 10.1007/s00784-016-1935-8Musskopf ML, Daudt LD, Weidlich P, Gerchman F, Gross JL, Oppermann RV. Metabolic syndrome as a risk indicator for periodontal disease and tooth loss. Clin Oral Investig. 2017;21(2):675-683. doi: 10.1007/s00784-016-1935-8Pirih FQ, Monajemzadeh S, Singh N, Sinacola RS, Shin JM, Chen T, et. al. Association between metabolic syndrome and periodontitis: The role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 2000. 2021;87(1):50-75. doi: 10.1111/prd.12379Pirih FQ, Monajemzadeh S, Singh N, Sinacola RS, Shin JM, Chen T, et. al. Association between metabolic syndrome and periodontitis: The role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 2000. 2021;87(1):50-75. doi: 10.1111/prd.12379Wu LT, Shen YF, Hu L, Zhang MY, Lai XY. Prevalence and associated factors of metabolic syndrome in adults: a population-based epidemiological survey in Jiangxi province, China. BMC Public Health. 2020;20(1):133. doi: 10.1186/s12889-020-8207-xWu LT, Shen YF, Hu L, Zhang MY, Lai XY. Prevalence and associated factors of metabolic syndrome in adults: a population-based epidemiological survey in Jiangxi province, China. BMC Public Health. 2020;20(1):133. doi: 10.1186/s12889-020-8207-xNascimento GG, Leite FRM, Peres KG, Demarco FF, Corrêa MB, Peres MA. Metabolic syndrome and periodontitis: A structural equation modeling approach. J. Periodontol. 2019;90(6):655-662. doi: 10.1002/JPER.18-0483Nascimento GG, Leite FRM, Peres KG, Demarco FF, Corrêa MB, Peres MA. Metabolic syndrome and periodontitis: A structural equation modeling approach. J. Periodontol. 2019;90(6):655-662. doi: 10.1002/JPER.18-0483Bandiwadekar AS, Shanbhag N, Madhuniranjanswamy MS, Khanagar SB, Naik S, Siddeeqh S. Association of Periodontitis With Metabolic Syndrome: A Case-Control Study. J Int Soc Prev Community Dent. 2020;10(4):458-465. doi: 10.4103/jispcd.JISPCD_91_20Bandiwadekar AS, Shanbhag N, Madhuniranjanswamy MS, Khanagar SB, Naik S, Siddeeqh S. Association of Periodontitis With Metabolic Syndrome: A Case-Control Study. J Int Soc Prev Community Dent. 2020;10(4):458-465. doi: 10.4103/jispcd.JISPCD_91_20Jaramillo A, Contreras A, Lafaurie GI, Duque A, Ardila CM, Duarte S, et al. Association of metabolic syndrome and chronic periodontitis in Colombians. Clin Oral Investig. 2017;21(5):1537-1544. doi: 10.1007/s00784-016-1942-9Jaramillo A, Contreras A, Lafaurie GI, Duque A, Ardila CM, Duarte S, et al. Association of metabolic syndrome and chronic periodontitis in Colombians. Clin Oral Investig. 2017;21(5):1537-1544. doi: 10.1007/s00784-016-1942-9Org E, Blum Y, Kasela S, Mehrabian M, Kuusisto J, Kangas AJ, Soininen P,et al. Relationships between gut microbiota, plasma metabolites, and metabolic syndrome traits in the METSIM cohort. Genome Biol. 2017;18(1):70. doi: 10.1186/s13059-017-1194-2Org E, Blum Y, Kasela S, Mehrabian M, Kuusisto J, Kangas AJ, Soininen P,et al. Relationships between gut microbiota, plasma metabolites, and metabolic syndrome traits in the METSIM cohort. Genome Biol. 2017;18(1):70. doi: 10.1186/s13059-017-1194-2Rodríguez-Monforte M, Sánchez E, Barrio F, Costa B, Flores-Mateo G. Metabolic syndrome and dietary patterns: a systematic review and meta-analysis of observational studies. Eur J. Nutr. 2017;56(3):925-947. doi: 10.1007/s00394-016-1305-yRodríguez-Monforte M, Sánchez E, Barrio F, Costa B, Flores-Mateo G. Metabolic syndrome and dietary patterns: a systematic review and meta-analysis of observational studies. Eur J. Nutr. 2017;56(3):925-947. doi: 10.1007/s00394-016-1305-ySingh M, Bains VK, Jhingran R, Srivastava R, Madan R, Maurya SC, et al. Prevalence of Periodontal Disease in Type 2 Diabetes Mellitus Patients: A Cross-sectional Study. Contemp Clin Dent. 2019;10(2):349-357. doi: 10.4103/ccd.ccd_652_18Singh M, Bains VK, Jhingran R, Srivastava R, Madan R, Maurya SC, et al. Prevalence of Periodontal Disease in Type 2 Diabetes Mellitus Patients: A Cross-sectional Study. Contemp Clin Dent. 2019;10(2):349-357. doi: 10.4103/ccd.ccd_652_18Souza ML, Massignan C, Glazer Peres K, Aurélio Peres M. Association between metabolic syndrome and tooth loss: A systematic review and meta-analysis. J. Am Dent Assoc. 2019;150(12):1027-1039.e7. doi: 10.1016/j.adaj.2019.07.023Souza ML, Massignan C, Glazer Peres K, Aurélio Peres M. Association between metabolic syndrome and tooth loss: A systematic review and meta-analysis. J. Am Dent Assoc. 2019;150(12):1027-1039.e7. doi: 10.1016/j.adaj.2019.07.023Navarro BG, Salas EJ, López JL, Sánchez AR, Corbella X, Sala XP. Relationship between metabolic syndrome and oral/dental pathology. Atherosclerosis. 2018;275:e113. doi: 10.1016/j.atherosclerosis.2018.06.316Navarro BG, Salas EJ, López JL, Sánchez AR, Corbella X, Sala XP. Relationship between metabolic syndrome and oral/dental pathology. Atherosclerosis. 2018;275:e113. doi: 10.1016/j.atherosclerosis.2018.06.316Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71Daudt LD, Musskopf ML, Mendez M, Remonti LLR, Leitão CB, Gross JL, et al. Association between metabolic syndrome and periodontitis: a systematic review and meta-analysis. Braz Oral Res. 2018;32:e35. doi: 10.1590/1807-3107bor-2018.vol32.0035Daudt LD, Musskopf ML, Mendez M, Remonti LLR, Leitão CB, Gross JL, et al. Association between metabolic syndrome and periodontitis: a systematic review and meta-analysis. Braz Oral Res. 2018;32:e35. doi: 10.1590/1807-3107bor-2018.vol32.0035Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, et al. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40-50. doi: 10.1016/j.diabres.2017.03.024Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, et al. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40-50. doi: 10.1016/j.diabres.2017.03.024Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K , Duncan BB, Stein C, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 2022;183:109119. doi: 10.1016/j.diabres.2021.109119Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K , Duncan BB, Stein C, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 2022;183:109119. doi: 10.1016/j.diabres.2021.109119Echouffo-Tcheugui JB, Selvin E. Prediabetes and What It Means: The Epidemiological Evidence. Annu Rev Public Health. 2021;42:59-77. doi: 10.1146/annurev-publhealth-090419-102644Echouffo-Tcheugui JB, Selvin E. Prediabetes and What It Means: The Epidemiological Evidence. Annu Rev Public Health. 2021;42:59-77. doi: 10.1146/annurev-publhealth-090419-102644Rooney MR, Fang M, Ogurtsova K, Ozkan B, Echouffo-Tcheugui JB, Boyko EJ, et al. Global Prevalence of Prediabetes. Diabetes Care. 2023;46(7):1388-1394. doi: 10.2337/dc22-2376.Rooney MR, Fang M, Ogurtsova K, Ozkan B, Echouffo-Tcheugui JB, Boyko EJ, et al. Global Prevalence of Prediabetes. Diabetes Care. 2023;46(7):1388-1394. doi: 10.2337/dc22-2376.Ramón-Arbués E, Martínez-Abadía B, Gracia-Tabuenca T, Yuste-Gran C, Pellicer-García B, Juárez-Vela R, et al. Prevalencia de sobrepeso/obesidad y su asociación con diabetes, hipertensión, dislipemia y síndrome metabólico: estudio transversal de una muestra de trabajadores en Aragón, España [Prevalence of overweight/obesity and its association with diabetes, hypertension, dyslipidemia and metabolic syndrome: a cross-sectional study of a sample of workers in Aragón, Spain]. Nutr Hosp. 2019;36(1):51-59 (In Spanish). doi: 10.20960/nh.1980Ramón-Arbués E, Martínez-Abadía B, Gracia-Tabuenca T, Yuste-Gran C, Pellicer-García B, Juárez-Vela R, et al. Prevalencia de sobrepeso/obesidad y su asociación con diabetes, hipertensión, dislipemia y síndrome metabólico: estudio transversal de una muestra de trabajadores en Aragón, España [Prevalence of overweight/obesity and its association with diabetes, hypertension, dyslipidemia and metabolic syndrome: a cross-sectional study of a sample of workers in Aragón, Spain]. Nutr Hosp. 2019;36(1):51-59 (In Spanish). doi: 10.20960/nh.1980Suwanprasit W, Lertpimonchai A, Thienpramuk L, Vathesatogkit P, Sritara P, Tamsailom S. Metabolic syndrome and severe periodontitis were associated in Thai adults: A cross-sectional study. J. Periodontol. 2021;92(10):1420-1429. doi: 10.1002/JPER.20-0651Suwanprasit W, Lertpimonchai A, Thienpramuk L, Vathesatogkit P, Sritara P, Tamsailom S. Metabolic syndrome and severe periodontitis were associated in Thai adults: A cross-sectional study. J. Periodontol. 2021;92(10):1420-1429. doi: 10.1002/JPER.20-0651Pham T. The association between periodontal disease severity and metabolic syndrome in Vietnamese patients. Int J. Dent Hyg. 2018;16(4):484-491. doi: 10.1111/idh.12350Pham T. The association between periodontal disease severity and metabolic syndrome in Vietnamese patients. Int J. Dent Hyg. 2018;16(4):484-491. doi: 10.1111/idh.12350Kim OS, Shin MH, Kweon SS, Lee YH, Kim OJ, Kim YJ, et al. The severity of periodontitis and metabolic syndrome in Korean population: The Dong-gu study. J. Periodontal Res. 2018;53(3):362-368. doi: 10.1111/jre.12521Kim OS, Shin MH, Kweon SS, Lee YH, Kim OJ, Kim YJ, et al. The severity of periodontitis and metabolic syndrome in Korean population: The Dong-gu study. J. Periodontal Res. 2018;53(3):362-368. doi: 10.1111/jre.12521Kotin J, Walther C, Wenzel U, Zyriax BC, Borof K, Schnabel RB, et al. Association between periodontitis and metabolic syndrome in the Hamburg City Health Study. J. Periodontol. 2022;93(8):1150-1160. doi: 10.1002/JPER.21-0464Kotin J, Walther C, Wenzel U, Zyriax BC, Borof K, Schnabel RB, et al. Association between periodontitis and metabolic syndrome in the Hamburg City Health Study. J. Periodontol. 2022;93(8):1150-1160. doi: 10.1002/JPER.21-0464Hlushchenko TA, Batig VM, Borysenko AV, Tokar OM, Batih IV, Vynogradova OM, et al. Prevalence and Intensity of Periodontal Disease in Individuals with Metabolic Syndrome. J. Med Life. 2020;13(3):289-292. doi: 10.25122/jml-2020-0073Hlushchenko TA, Batig VM, Borysenko AV, Tokar OM, Batih IV, Vynogradova OM, et al. Prevalence and Intensity of Periodontal Disease in Individuals with Metabolic Syndrome. J. Med Life. 2020;13(3):289-292. doi: 10.25122/jml-2020-0073Ермолаева ЛА, Шишкин АН, Шевелева НА, Пенькова ЕА, Шевелева МА, Соколович НА, и др. Особенности патологии пародонта у больных разных возрастных групп c метаболическим синдромом. Успехи геронтологии. 2016;29(2):318-323. Режим доступа: https://www.elibrary.ru/item.asp?id=26745031Ermolaeva LA, Shishkin AN, Sheveleva NA, Penkova EA, Sheveleva MA, Sokolovich NA, Khabarova OV, Mihailova ES. Features of the periodontal pathology at patients with metabolic syndrome. Advances in gerontology. 2016;29(2):318-323 (In Russ.). Available from: https://www.elibrary.ru/item.asp?id=26745031Слажнева ЕС, Атрушкевич ВГ, Орехова ЛЮ, Лобода ЕС. Распространенность заболеваний пародонта у пациентов с различным индексом массы тела. Пародонтология. 2022;27(3):202-208. doi: 10.33925/1683-3759-2022-27-3-202-208Slazhneva ES, Atrushkevitch VG, Orekhova LYu, Loboda ES. Prevalence of periodontal diseases in patients with different body mass index. Parodontologiya. 2022;27(3):202-208 (In Russ.). doi: 10.33925/1683-3759-2022-27-3-202-208Tegelberg P, Tervonen T, Knuuttila M, Jokelainen J, Keinänen-Kiukaanniemi S, Auvinen J, et al. Long-term metabolic syndrome is associated with periodontal pockets and alveolar bone loss. J Clin Periodontol. 2019;46(8):799-808. doi: 10.1111/jcpe.13154Tegelberg P, Tervonen T, Knuuttila M, Jokelainen J, Keinänen-Kiukaanniemi S, Auvinen J, et al. Long-term metabolic syndrome is associated with periodontal pockets and alveolar bone loss. J Clin Periodontol. 2019;46(8):799-808. doi: 10.1111/jcpe.13154Dhir S, Wangnoo S, Kumar V. Impact of Glycemic Levels in Type 2 Diabetes on Periodontitis. Indian J. Endocrinol Metab. 2018;22(5):672-677. doi: 10.4103/ijem.IJEM_566_17Dhir S, Wangnoo S, Kumar V. Impact of Glycemic Levels in Type 2 Diabetes on Periodontitis. Indian J. Endocrinol Metab. 2018;22(5):672-677. doi: 10.4103/ijem.IJEM_566_17Kebede TG, Pink C, Rathmann W, Kowall B, Völzke H, Petersmann A, et al. Does periodontitis affect diabetes incidence and haemoglobin A1c change? An 11-year follow-up study. Diabetes Metab. 2018;44(3):243-249. doi: 10.1016/j.diabet.2017.11.003Kebede TG, Pink C, Rathmann W, Kowall B, Völzke H, Petersmann A, et al. Does periodontitis affect diabetes incidence and haemoglobin A1c change? An 11-year follow-up study. Diabetes Metab. 2018;44(3):243-249. doi: 10.1016/j.diabet.2017.11.003Farina R, Severi M, Carrieri A, Miotto E, Sabbioni S, Trombelli L, et al Whole metagenomic shotgun sequencing of the subgingival microbiome of diabetics and non-diabetics with different periodontal conditions. Arch Oral Biol. 2019;104:13-23. doi: 10.1016/j.archoralbio.2019.05.025Farina R, Severi M, Carrieri A, Miotto E, Sabbioni S, Trombelli L, et al Whole metagenomic shotgun sequencing of the subgingival microbiome of diabetics and non-diabetics with different periodontal conditions. Arch Oral Biol. 2019;104:13-23. doi: 10.1016/j.archoralbio.2019.05.025Goodson JM, Hartman ML, Shi P, Hasturk H, Yaskell T, Vargas J, Song X, et al. The salivary microbiome is altered in the presence of a high salivary glucose concentration. PLoS One. 2017;12(3):e0170437. doi: 10.1371/journal.pone.0170437Goodson JM, Hartman ML, Shi P, Hasturk H, Yaskell T, Vargas J, Song X, et al. The salivary microbiome is altered in the presence of a high salivary glucose concentration. PLoS One. 2017;12(3):e0170437. doi: 10.1371/journal.pone.0170437Longo PL, Dabdoub S, Kumar P, Artese HPC, Dib SA, Romito GA, et al. Glycaemic status affects the subgingival microbiome of diabetic patients. J. Clin Periodontol. 2018;45(8):932-940. doi: 10.1111/jcpe.12908.Longo PL, Dabdoub S, Kumar P, Artese HPC, Dib SA, Romito GA, et al. Glycaemic status affects the subgingival microbiome of diabetic patients. J. Clin Periodontol. 2018;45(8):932-940. doi: 10.1111/jcpe.12908.Matsha TE, Prince Y, Davids S, Chikte U, Erasmus RT, Kengne AP, et al. Oral Microbiome Signatures in Diabetes Mellitus and Periodontal Disease. J. Dent Res. 2020;99(6):658-665. doi: 10.1177/0022034520913818.Matsha TE, Prince Y, Davids S, Chikte U, Erasmus RT, Kengne AP, et al. Oral Microbiome Signatures in Diabetes Mellitus and Periodontal Disease. J. Dent Res. 2020;99(6):658-665. doi: 10.1177/0022034520913818.Rodríguez-Hernández AP, Márquez-Corona ML, Pontigo-Loyola AP, Medina-Solís CE, Ximenez-Fyvie LA. Subgingival Microbiota of Mexicans with Type 2 Diabetes with Different Periodontal and Metabolic Conditions. Int J. Environ Res Public Health. 2019;16(17):3184. doi: 10.3390/ijerph16173184Rodríguez-Hernández AP, Márquez-Corona ML, Pontigo-Loyola AP, Medina-Solís CE, Ximenez-Fyvie LA. Subgingival Microbiota of Mexicans with Type 2 Diabetes with Different Periodontal and Metabolic Conditions. Int J. Environ Res Public Health. 2019;16(17):3184. doi: 10.3390/ijerph16173184Sabharwal A, Ganley K, Miecznikowski JC, Haase EM, Barnes V, Scannapieco FA. The salivary microbiome of diabetic and non-diabetic adults with periodontal disease. J Periodontol. 2019;90(1):26–34. doi: 10.1002/jper.18-0167Sabharwal A, Ganley K, Miecznikowski JC, Haase EM, Barnes V, Scannapieco FA. The salivary microbiome of diabetic and non-diabetic adults with periodontal disease. J Periodontol. 2019;90(1):26–34. doi: 10.1002/jper.18-0167Shi B, Lux R, Klokkevold P, Chang M, Barnard E, Haake S, et al. The subgingival microbiome associated with periodontitis in type 2 diabetes mellitus. ISME J. 2020;14(2):519-530. doi: 10.1038/s41396-019-0544-3Shi B, Lux R, Klokkevold P, Chang M, Barnard E, Haake S, et al. The subgingival microbiome associated with periodontitis in type 2 diabetes mellitus. ISME J. 2020;14(2):519-530. doi: 10.1038/s41396-019-0544-3Ganesan SM, Joshi V, Fellows M, Dabdoub SM, Nagaraja HN, O'Donnell B, et al. A tale of two risks: smoking, diabetes and the subgingival microbiome. ISME J. 2017;11(9):2075-2089. doi: 10.1038/ismej.2017.73Ganesan SM, Joshi V, Fellows M, Dabdoub SM, Nagaraja HN, O'Donnell B, et al. A tale of two risks: smoking, diabetes and the subgingival microbiome. ISME J. 2017;11(9):2075-2089. doi: 10.1038/ismej.2017.73Moore JX, Chaudhary N, Akinyemiju T. Metabolic Syndrome Prevalence by Race/Ethnicity and Sex in the United States, National Health and Nutrition Examination Survey, 1988-2012. Prev Chronic Dis. 2017;14:160287. doi: 10.5888/pcd14.160287Moore JX, Chaudhary N, Akinyemiju T. Metabolic Syndrome Prevalence by Race/Ethnicity and Sex in the United States, National Health and Nutrition Examination Survey, 1988-2012. Prev Chronic Dis. 2017;14:160287. doi: 10.5888/pcd14.160287Tam J, Hoffmann T, Fischer S, Bornstein S, Gräßler J, Noack B. Obesity alters composition and diversity of the oral microbiota in patients with type 2 diabetes mellitus independently of glycemic control. PLoS One. 2018;13(10):e0204724. doi: 10.1371/journal.pone.0204724Tam J, Hoffmann T, Fischer S, Bornstein S, Gräßler J, Noack B. Obesity alters composition and diversity of the oral microbiota in patients with type 2 diabetes mellitus independently of glycemic control. PLoS One. 2018;13(10):e0204724. doi: 10.1371/journal.pone.0204724Babaev EA, Balmasova IP, Mkrtumyan AM, Kostryukova SN, Vakhitova ES, Il'ina EN, et al. Metagenomic Analysis of Gingival Sulcus Microbiota and Pathogenesis of Periodontitis Associated with Type 2 Diabetes Mellitus. Bull Exp Biol Med. 2017;163(6):718-721. doi: 10.1007/s10517-017-3888-6Babaev EA, Balmasova IP, Mkrtumyan AM, Kostryukova SN, Vakhitova ES, Il'ina EN, et al. Metagenomic Analysis of Gingival Sulcus Microbiota and Pathogenesis of Periodontitis Associated with Type 2 Diabetes Mellitus. Bull Exp Biol Med. 2017;163(6):718-721. doi: 10.1007/s10517-017-3888-6Kapila YL. Oral health's inextricable connection to systemic health: Special populations bring to bear multimodal relationships and factors connecting periodontal disease to systemic diseases and conditions. Periodontol. 2000. 2021;87(1):11-16. doi: 10.1111/prd.12398Kapila YL. Oral health's inextricable connection to systemic health: Special populations bring to bear multimodal relationships and factors connecting periodontal disease to systemic diseases and conditions. Periodontol. 2000. 2021;87(1):11-16. doi: 10.1111/prd.12398Ogawa T, Honda-Ogawa M, Ikebe K, Notomi Y, Iwamoto Y, Shirobayashi I, et al. Characterizations of oral microbiota in elderly nursing home residents with diabetes. J Oral Sci. 2017;59(4):549-555. doi: 10.2334/josnusd.16-0722Ogawa T, Honda-Ogawa M, Ikebe K, Notomi Y, Iwamoto Y, Shirobayashi I, et al. Characterizations of oral microbiota in elderly nursing home residents with diabetes. J Oral Sci. 2017;59(4):549-555. doi: 10.2334/josnusd.16-0722Li J, Lu H, Wu H, Huang S, Chen L, Gui Q, Zhou W, et al. Periodontitis in elderly patients with type 2 diabetes mellitus: impact on gut microbiota and systemic inflammation. Aging (Albany NY). 2020;12(24):25956-25980. doi: 10.18632/aging.202174Li J, Lu H, Wu H, Huang S, Chen L, Gui Q, Zhou W, et al. Periodontitis in elderly patients with type 2 diabetes mellitus: impact on gut microbiota and systemic inflammation. Aging (Albany NY). 2020;12(24):25956-25980. doi: 10.18632/aging.202174

The authors declare that there are no conflicts of interest present.