Association between Frequency of Toothbrushing and Metabolic Syndrome among Adolescents: A 5-Year Follow-Up Study

Jagan Kumar Baskaradoss 1, Mary Tavares 2, Fahd Al-Mulla 3, Ebaa Al-Ozairi 3 4, Mohamed Abu-Farha 3, Saadoun Bin-Hasan 3 5, Aishah Alsumait 6, Sriraman Devarajan 3, Hend Alqaderi 3 6 7

Affiliations

01 March 2022

-

doi: 10.3390/ijerph19010508

Abstract

This study longitudinally examines the relationship between the frequency of toothbrushing and the development of selected components of metabolic syndrome (MetS), along with the potential role of salivary biomarkers in this relationship. In 2014, 6317 12-year-old children underwent health examinations (T1), of which, 348 children participated in the second stage of data collection in 2019 (T2). The association between the change in the metabolic status during the 5-year follow-up examination (between T1 and T2) and frequency of toothbrushing was assessed using multinomial logistic regression analyses. At T2, healthy adolescents had significantly higher odds of toothbrushing twice or more daily compared with adolescents with components of MetS (OR = 1.99, 95% CI 1.15-3.45). Adolescents who were healthy at T1 but developed components of MetS at T2, had significantly higher frequencies of dining-out compared with adolescents with components of MetS at both T1 and T2 (OR = 0.09, 95% CI 0.02 to 0.49). Adolescents who were 'healthy' at both T1 and T2 had significantly (p < 0.05) lower levels of C-reactive protein (T2), insulin (T1 and T2), interleukin-6 (T1) and adiponectin (T1) compared with adolescents who had components of MetS. Toothbrushing and frequency of dining-out were associated with the presence of MetS components.

Keywords: C-reactive protein; biomarkers; children; diet; inflammatory; oral hygiene.

Conflict of interest statement

The authors declare no conflict of interest.

Similar articles

Relationship of toothbrushing to metabolic syndrome in middle-aged adults.

Tanaka A, Takeuchi K, Furuta M, Takeshita T, Suma S, Shinagawa T, Shimazaki Y, Yamashita Y.J Clin Periodontol. 2018 May;45(5):538-547. doi: 10.1111/jcpe.12876. Epub 2018 Apr 17.PMID: 29421856

Association between Dietary Inflammatory Index, C-Reactive Protein and Metabolic Syndrome: A Cross-Sectional Study.

Ren Z, Zhao A, Wang Y, Meng L, Szeto IM, Li T, Gong H, Tian Z, Zhang Y, Wang P.Nutrients. 2018 Jun 27;10(7):831. doi: 10.3390/nu10070831.PMID: 29954070 Free PMC article.

Oral health behavior and metabolic syndrome and its components in adults.

Kobayashi Y, Niu K, Guan L, Momma H, Guo H, Cui Y, Nagatomi R.J Dent Res. 2012 May;91(5):479-84. doi: 10.1177/0022034512440707. Epub 2012 Feb 29.PMID: 22378694

The role of multicomponent therapy in the metabolic syndrome, inflammation and cardiovascular risk in obese adolescents.

Masquio DC, de Piano A, Campos RM, Sanches PL, Carnier J, Corgosinho FC, Netto BD, Carvalho-Ferreira JP, Oyama LM, Nascimento CM, de Mello MT, Tufik S, Dâmaso AR.Br J Nutr. 2015 Jun 28;113(12):1920-30. doi: 10.1017/S0007114515001129. Epub 2015 Apr 24.PMID: 25907896

Zähneputzen schützt wohl vor Fettleber.

Müssig K.MMW Fortschr Med. 2021 Oct;163(18):33. doi: 10.1007/s15006-021-0427-1.PMID: 34652656 Review. German. No abstract available.

Cited by

Systemic Disorders Closely Associated with Malocclusion in Late Adolescence: A Review and Perspective.

Abe M, Mitani A, Yao A, Hoshi K, Yanagimoto S.Int J Environ Res Public Health. 2022 Mar 14;19(6):3401. doi: 10.3390/ijerph19063401.PMID: 35329087 Free PMC article. Review.

KMEL References

ubmed.ncbi.nlm.nih.gov

References

  1.  
    1. Grundy S.M., Brewer H.B., Jr., Cleeman J.I., Smith S.C., Jr., Lenfant C. Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004;109:433–438. doi: 10.1161/01.CIR.0000111245.75752.C6. - DOI - PubMed
  2.  
    1. Zimmet P., Alberti K.G., Kaufman F., Tajima N., Silink M., Arslanian S., Wong G., Bennett P., Shaw J., Caprio S., et al. The metabolic syndrome in children and adolescents-an IDF consensus report. Pediatr. Diabetes. 2007;8:299–306. doi: 10.1111/j.1399-5448.2007.00271.x. - DOI - PubMed
  3.  
    1. Skinner A.C., Ravanbakht S.N., Skelton J.A., Perrin E.M., Armstrong S.C. Prevalence of Obesity and Severe Obesity in US Children, 1999–2016. Pediatrics. 2018;141 doi: 10.1542/peds.2017-3459. - DOI - PubMed
  4.  
    1. Ogden C.L., Flegal K.M., Carroll M.D., Johnson C.L. Prevalence and trends in overweight among US children and adolescents, 1999–2000. JAMA. 2002;288:1728–1732. doi: 10.1001/jama.288.14.1728. - DOI - PubMed
  5.  
    1. Palatini P., Julius S. Elevated heart rate: A major risk factor for cardiovascular disease. Clin. Exp. Hypertens. 2004;26:637–644. doi: 10.1081/CEH-200031959. - DOI - PubMed
  6.  
    1. Flynn J. The changing face of pediatric hypertension in the era of the childhood obesity epidemic. Pediatr. Nephrol. 2013;28:1059–1066. doi: 10.1007/s00467-012-2344-0. - DOI - PubMed
  7.  
    1. Jepsen S., Suvan J., Deschner J. The association of periodontal diseases with metabolic syndrome and obesity. Periodontol. 2000. 2020;83:125–153. doi: 10.1111/prd.12326. - DOI - PubMed
  8.  
    1. Petersen P.E. Global policy for improvement of oral health in the 21st century–implications to oral health research of World Health Assembly 2007, World Health Organization. Community Dent. Oral Epidemiol. 2009;37:1–8. doi: 10.1111/j.1600-0528.2008.00448.x. - DOI - PubMed
  9.  
    1. Janket S.J., Javaheri H., Ackerson L.K., Ayilavarapu S., Meurman J.H. Oral Infections, Metabolic Inflammation, Genetics, and Cardiometabolic Diseases. J. Dent. Res. 2015;94:119S–127S. doi: 10.1177/0022034515580795. - DOI - PubMed
  10.  
    1. Genco R.J., Grossi S.G., Ho A., Nishimura F., Murayama Y. A Proposed Model Linking Inflammation to Obesity, Diabetes, and Periodontal Infections. J. Periodontol. 2005;76((Suppl. 11)):2075–2084. doi: 10.1902/jop.2005.76.11-S.2075. - DOI - PubMed
  11.  
    1. Furuta M., Liu A., Shinagawa T., Takeuchi K., Takeshita T., Shimazaki Y., Yamashita Y. Tooth loss and metabolic syndrome in middle-aged Japanese adults. J. Clin. Periodontol. 2016;43:482–491. doi: 10.1111/jcpe.12523. - DOI - PubMed
  12.  
    1. Gomes-Filho I.S., das Mercês M.C., de Santana Passos-Soares J., Seixas da Cruz S., Teixeira Ladeia A.M., Trindade S.C., de Moraes Marcílio Cerqueira E., Freitas Coelho J.M., Marques Monteiro F.M., Barreto M.L. Severity of periodontitis and metabolic syndrome: Is there an association? J. Periodontol. 2016;87:357–366. doi: 10.1902/jop.2015.150367. - DOI - PubMed
  13.  
    1. Kwon Y.E., Ha J.E., Paik D.I., Jin B.H., Bae K.H. The relationship between periodontitis and metabolic syndrome among a Korean nationally representative sample of adults. J. Clin. Periodontol. 2011;38:781–786. doi: 10.1111/j.1600-051X.2011.01756.x. - DOI - PubMed
  14.  
    1. Srikanthan K., Feyh A., Visweshwar H., Shapiro J.I., Sodhi K. Systematic Review of Metabolic Syndrome Biomarkers: A Panel for Early Detection, Management, and Risk Stratification in the West Virginian Population. Int. J. Med. Sci. 2016;13:25–38. doi: 10.7150/ijms.13800. - DOI - PMC - PubMed
  15.  
    1. Nomura Y., Shimada Y., Hanada N., Numabe Y., Kamoi K., Sato T., Gomi K., Arai T., Inagaki K., Fukuda M., et al. Salivary biomarkers for predicting the progression of chronic periodontitis. Arch. Oral Biol. 2012;57:413–420. doi: 10.1016/j.archoralbio.2011.09.011. - DOI - PubMed
  16.  
    1. Tanaka A., Takeuchi K., Furuta M., Takeshita T., Suma S., Shinagawa T., Shimazaki Y., Yamashita Y. Relationship of toothbrushing to metabolic syndrome in middle-aged adults. J. Clin. Periodontol. 2018;45:538–547. doi: 10.1111/jcpe.12876. - DOI - PubMed
  17.  
    1. Kobayashi Y., Niu K., Guan L., Momma H., Guo H., Cui Y., Nagatomi R. Oral health behavior and metabolic syndrome and its components in adults. J. Dent. Res. 2012;91:479–484. doi: 10.1177/0022034512440707. - DOI - PubMed
  18.  
    1. Furuta M., Takeuchi K., Takeshita T., Tanaka A., Suma S., Shinagawa T., Shimazaki Y., Yamashita Y. Longitudinal associations of toothbrushing with obesity and hyperglycemia. J. Epidemiol. 2020 doi: 10.2188/jea.JE20190165. - DOI - PMC - PubMed
  19.  
    1. von Elm E., Altman D.G., Egger M., Pocock S.J., Gotzsche P.C., Vandenbroucke J.P., Initiative S. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for reporting observational studies. Int. J. Surg. 2014;12:1495–1499. doi: 10.1016/j.ijsu.2014.07.013. - DOI - PubMed
  20.  
    1. Schwab J.A. Multinomial Logistic Regression: Basic Relationships and Complete Problems. The University of Texas in Austin; Austin, TX, USA: 2002.
  21.  
    1. Goodson J.M., Kantarci A., Hartman M.L., Denis G.V., Stephens D., Hasturk H., Yaskell T., Vargas J., Wang X., Cugini M., et al. Metabolic disease risk in children by salivary biomarker analysis. PLoS ONE. 2014;9:e98799. doi: 10.1371/journal.pone.0098799. - DOI - PMC - PubMed
  22.  
    1. Hartman M.L., Goodson J.M., Barake R., Alsmadi O., Al-Mutawa S., Ariga J., Soparkar P., Behbehani J., Behbehani K. Salivary Biomarkers in Pediatric Metabolic Disease Research. Pediatr. Endocrinol. Rev. 2016;13:602–611. - PubMed
  23.  
    1. Goodson J.M., Tavares M., Wang X., Niederman R., Cugini M., Hasturk H., Barake R., Alsmadi O., Al-Mutawa S., Ariga J., et al. Obesity and dental decay: Inference on the role of dietary sugar. PLoS ONE. 2013;8:e74461. doi: 10.1371/journal.pone.0074461. - DOI - PMC - PubMed
  24.  
    1. Alqaderi H., Tavares M., Hartman M., Goodson J.M. Effect of Sleep and Salivary Glucose on Gingivitis in Children. J. Dent. Res. 2016;95:1387–1393. doi: 10.1177/0022034516661509. - DOI - PubMed
  25.  
    1. Alqaderi H., Tavares M., Al-Mulla F., Al-Ozairi E., Goodson J.M. Late bedtime and dental caries incidence in Kuwaiti children: A longitudinal multilevel analysis. Community Dent. Oral Epidemiol. 2020;48:181–187. doi: 10.1111/cdoe.12523. - DOI - PubMed
  26.  
    1. World Health Organization (WHO) Obesity and Overweight. 2020. [(accessed on 28 May 2021)]. Available online: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight.
  27.  
    1. de Onis M., Onyango A.W., Borghi E., Siyam A., Nishida C., Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull. World Health Organ. 2007;85:660–667. doi: 10.2471/BLT.07.043497. - DOI - PMC - PubMed
  28.  
    1. Allafi A., Al-Haifi A.R., Al-Fayez M.A., Al-Athari B.I., Al-Ajmi F.A., Al-Hazzaa H.M., Musaiger A.O., Ahmed F. Physical activity, sedentary behaviours and dietary habits among Kuwaiti adolescents: Gender differences. Public Health Nutr. 2014;17:2045–2052. doi: 10.1017/S1368980013002218. - DOI - PubMed
  29.  
    1. Ainsworth B.E., Haskell W.L., Herrmann S.D., Meckes N., Bassett D.R., Jr., Tudor-Locke C., Greer J.L., Vezina J., Whitt-Glover M.C., Leon A.S. 2011 Compendium of Physical Activities: A second update of codes and MET values. Med. Sci. Sports Exerc. 2011;43:1575–1581. doi: 10.1249/MSS.0b013e31821ece12. - DOI - PubMed
  30.  
    1. Steinberger J., Daniels S.R., Eckel R.H., Hayman L., Lustig R.H., McCrindle B., Mietus-Snyder M.L. Progress and challenges in metabolic syndrome in children and adolescents: A scientific statement from the American Heart Association Atherosclerosis, Hypertension, and Obesity in the Young Committee of the Council on Cardiovascular Disease in the Young; Council on Cardiovascular Nursing; and Council on Nutrition, Physical Activity, and Metabolism. Circulation. 2009;119:628–647. - PubMed
  31.  
    1. Shi P., Goodson J.M., Hartman M.L., Hasturk H., Yaskell T., Vargas J., Cugini M., Barake R., Alsmadi O., Al-Mutawa S., et al. Continuous Metabolic Syndrome Scores for Children Using Salivary Biomarkers. PLoS ONE. 2015;10:e0138979. doi: 10.1371/journal.pone.0138979. - DOI - PMC - PubMed
  32.  
    1. Campbell K.L., Kushner H., Falkner B. Obesity and high blood pressure: A clinical phenotype for the insulin resistance syndrome in African Americans. J. Clin. Hypertens. 2004;6:364–370. doi: 10.1111/j.1524-6175.2004.03536.x. quiz 371-362. - DOI - PMC - PubMed
  33.  
    1. Scannapieco F.A., Cantos A. Oral inflammation and infection, and chronic medical diseases: Implications for the elderly. Periodontol. 2000. 2016;72:153–175. doi: 10.1111/prd.12129. - DOI - PubMed
  34.  
    1. American Dental Association Oral Health Topics: General Recommendations for the Prevention of Caries and Gingivitis. 2020. [(accessed on 19 October 2020)]. Available online: https://www.ada.org/en/member-center/oral-health-topics/home-care.
  35.  
    1. Zimmermann H., Zimmermann N., Hagenfeld D., Veile A., Kim T.S., Becher H. Is frequency of tooth brushing a risk factor for periodontitis? A systematic review and meta-analysis. Community Dent. Oral. Epidemiol. 2015;43:116–127. doi: 10.1111/cdoe.12126. - DOI - PubMed
  36.  
    1. Tada A., Matsukubo T. Relationship between oral health behaviors and general health behaviors in a Japanese adult population. J. Public Health Dent. 2003;63:250–254. doi: 10.1111/j.1752-7325.2003.tb03508.x. - DOI - PubMed
  37.  
    1. Kuwabara M., Motoki Y., Ichiura K., Fujii M., Inomata C., Sato H., Morisawa T., Morita Y., Kuwabara K., Nakamura Y. Association between toothbrushing and risk factors for cardiovascular disease: A large-scale, cross-sectional Japanese study. BMJ Open. 2016;6:009870. doi: 10.1136/bmjopen-2015-009870. - DOI - PMC - PubMed
  38.  
    1. Kobayashi D., Mizuno A., Mitsui R., Shimbo T. Frequency of daily tooth brushing and subsequent cardiovascular events. Coron. Artery Dis. 2020;31:545–549. doi: 10.1097/MCA.0000000000000882. - DOI - PubMed
  39.  
    1. Lee Y.-H., Pratley R.E. The evolving role of inflammation in obesity and the metabolic syndrome. Curr. Diabetes Rep. 2005;5:70–75. doi: 10.1007/s11892-005-0071-7. - DOI - PubMed
  40.  
    1. Baskaradoss J.K., Geevarghese A., Al-Mthen A., Al-Ghamdi H., Al-Haudayris R., Al-Obaidy S., Al-Saadi W. Influence of Lifestyle on Dental Health Behavior. J. Lifestyle Med. 2019;9:119–124. doi: 10.15280/jlm.2019.9.2.119. - DOI - PMC - PubMed
  41.  
    1. Koivusilta L., Honkala S., Honkala E., Rimpelä A. Toothbrushing as part of the adolescent lifestyle predicts education level. J. Dent. Res. 2003;82:361–366. doi: 10.1177/154405910308200507. - DOI - PubMed
  42.  
    1. Aarø L.E., Laberg J.C., Wold B. Health behaviours among adolescents: Towards a hypothesis of two dimensions. Health Educ. Res. 1995;10:83–93. doi: 10.1093/her/10.1.83. - DOI
  43.  
    1. Festa A., D’Agostino R., Jr., Howard G., Mykkanen L., Tracy R.P., Haffner S.M. Chronic subclinical inflammation as part of the insulin resistance syndrome: The Insulin Resistance Atherosclerosis Study (IRAS) Circulation. 2000;102:42–47. doi: 10.1161/01.CIR.102.1.42. - DOI - PubMed
  44.  
    1. Wang X., Bao W., Liu J., OuYang Y.-Y., Wang D., Rong S., Xiao X., Shan Z.-L., Zhang Y., Yao P. Inflammatory markers and risk of type 2 diabetes: A systematic review and meta-analysis. Diabetes Care. 2013;36:166–175. doi: 10.2337/dc12-0702. - DOI - PMC - PubMed
  45.  
    1. Burbelo P.D., Bayat A., Lebovitz E.E., Iadarola M.J. New technologies for studying the complexity of oral diseases. Oral Dis. 2012;18:121–126. doi: 10.1111/j.1601-0825.2011.01863.x. - DOI - PMC - PubMed
  46.  
    1. Briancon-Marjollet A., Weiszenstein M., Henri M., Thomas A., Godin-Ribuot D., Polak J. The impact of sleep disorders on glucose metabolism: Endocrine and molecular mechanisms. Diabetol. Metab. Syndr. 2015;7:25. doi: 10.1186/s13098-015-0018-3. - DOI - PMC - PubMed
  47.  
    1. Naska A., Orfanos P., Trichopoulou A., May A., Overvad K., Jakobsen M.U., Tjønneland A., Halkjær J., Fagherazzi G., Clavel-Chapelon F. Eating out, weight and weight gain. A cross-sectional and prospective analysis in the context of the EPIC-PANACEA study. Int. J. Obes. 2011;35:416–426. doi: 10.1038/ijo.2010.142. - DOI - PubMed
  48.  
    1. Ho M., Garnett S.P., Baur L., Burrows T., Stewart L., Neve M., Collins C. Effectiveness of lifestyle interventions in child obesity: Systematic review with meta-analysis. Pediatrics. 2012;130:e1647–e1671. doi: 10.1542/peds.2012-1176. - DOI - PubMed
  49.  
    1. Fujita M., Ueno K., Hata A. Lower frequency of daily teeth brushing is related to high prevalence of cardiovascular risk factors. Exp. Biol. Med. 2009;234:387–394. doi: 10.3181/0809-RM-265. - DOI - PubMed

Page Navigation