To examine associations between periodontal disease severity and clinical and microbiological measures of caries in adults.
Materials and methods
A cross-sectional study of 94 healthy adults ((mean ± SD) 55.4 ± 13.0 years) was conducted. Data were collected by means of questionnaire and a clinical examination that included the Decayed, Missing, Filled teeth Surfaces (DMFS) index, probing depth (PD), clinical attachment level (CAL), and gingival bleeding and plaque scores. Supra- and subgingival plaque samples were collected to assess the presence of Streptococcus mutans and six periodontal pathogens. Participants were subsequently categorized using Center for Disease Control and Prevention/American Academy of Periodontology (CDC-AAP) definitions and tertiles of percentage of sites with CAL ≥ 3mm.
Significant positive associations were found between the periodontal disease severity (CDC-AAP) and the DMFS (aOR = 1.03; 95% CI 1.01–1.05) and DS indices (aOR = 1.18; 95% CI 1.05–1.32) as well as between the tertiles of percentage of sites with CAL ≥ 3 mm and DMFS (aOR = 1.03; 95% CI 1.00–1.05) and DS indices (aOR = 1.12; 95% CI 1.00–1.25). A significant positive association was also found between oral levels of F. nucleatum and S. mutans (aOR = 6.03; 95% CI 1.55–23.45).
A small but positive association was found between clinical measures of caries and periodontal disease severity. Further research is warranted to examine the association between these two common oral diseases.
Periodontal diseases and caries are the two most common oral diseases. There was a positive association between clinical and microbiological markers of both diseases. Therefore, strategies in oral health education should involve both caries and periodontitis prevention.
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Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366(9499):1809–1820. https://doi.org/10.1016/S0140-6736(05)67728-8
Petersen PE, Bourgeois D, Ogawa H, Estupinan-Day S, Ndiaye C (2005) The global burden of oral diseases and risks to oral health. Bull World Health Organ 83(9):661–669
Sanz M, Beighton D, Curtis MA, Cury JA, Dige I, Dommisch H, Ellwood R, Giacaman RA, Herrera D, Herzberg MC, Kononen E, Marsh PD, Meyle J, Mira A, Molina A, Mombelli A, Quirynen M, Reynolds EC, Shapira L, Zaura E (2017) Role of microbial biofilms in the maintenance of oral health and in the development of dental caries and periodontal diseases. Consensus report of group 1 of the Joint EFP/ORCA workshop on the boundaries between caries and periodontal disease. J Clin Periodontol 44(Suppl 18):S5–S11. https://doi.org/10.1111/jcpe.12682
Selwitz RH, Ismail AI, Pitts NB (2007) Dental caries. Lancet 369(9555):51–59. https://doi.org/10.1016/S0140-6736(07)60031-2
Darveau RP (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8(7):481–490. https://doi.org/10.1038/nrmicro2337
Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25(2):134–144
Holt SC, Ebersole JL (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 38:72–122. https://doi.org/10.1111/j.1600-0757.2005.00113.x
Curtis MA, Zenobia C, Darveau RP (2011) The relationship of the oral microbiotia to periodontal health and disease. Cell Host Microbe 10(4):302–306. https://doi.org/10.1016/j.chom.2011.09.008
Kinane DF, Jenkins WM, Adonogianaki E, Murray GD (1991) Cross-sectional assessment of caries and periodontitis risk within the same subject. Community Dent Oral Epidemiol 19(2):78–81
Frentzen M, Schuler N, Nolden R (1990) Correlation between caries prevalence (DMFS) and periodontal condition (CPITN) in more than 2000 patients. Int Dent J 40(5):313–318
Skier J, Mandel ID (1980) Comparative periodontal status of caries resistant versus susceptible adults. J Periodontol 51(10):614–616. https://doi.org/10.1902/jop.1918.104.22.1684
Iwano Y, Sugano N, Matsumoto K, Nishihara R, Iizuka T, Yoshinuma N, Ito K (2010) Salivary microbial levels in relation to periodontal status and caries development. J Periodontal Res 45(2):165–169. https://doi.org/10.1111/j.1600-0765.2009.01213.x
Sioson PB, Furgang D, Steinberg LM, Fine DH (2000) Proximal caries in juvenile periodontitis patients. J Periodontol 71(5):710–716. https://doi.org/10.1902/jop.2000.71.5.710
Sewon LA, Parvinen TH, Sinisalo TV, Larmas MA, Alanen PJ (1988) Dental status of adults with and without periodontitis. J Periodontol 59(9):595–598
Albandar JM, Buischi YA, Axelsson P (1995) Caries lesions and dental restorations as predisposing factors in the progression of periodontal diseases in adolescents. A 3-year longitudinal study. J Periodontol 66(4):249–254. https://doi.org/10.1902/jop.1922.214.171.124
Ekstrand KR, Bruun G, Bruun M (1998) Plaque and gingival status as indicators for caries progression on approximal surfaces. Caries Res 32(1):41–45
Saotome Y, Tada A, Hanada N, Yoshihara A, Uematsu H, Miyazaki H, Senpuku H (2006) Relationship of cariogenic bacteria levels with periodontal status and root surface caries in elderly Japanese. Gerodontology 23(4):219–225. https://doi.org/10.1111/j.1741-2358.2006.00127.x
Vehkalahti M, Paunio I (1994) Association between root caries occurrence and periodontal state. Caries Res 28(4):301–306
Mattila PT, Niskanen MC, Vehkalahti MM, Nordblad A, Knuuttila ML (2010) Prevalence and simultaneous occurrence of periodontitis and dental caries. J Clin Periodontol 37(11):962–967. https://doi.org/10.1111/j.1600-051X.2010.01620.x
Rosan B, Lamont RJ (2000) Dental plaque formation. Microb Infect Instit Pasteur 2(13):1599–1607
Tervonen T, Knuuttila M, Nieminen P (1991) Risk factors associated with abundant dental caries and periodontal pocketing. Community Dent Oral Epidemiol 19(2):82–87
Hobdell MH, Oliveira ER, Bautista R, Myburgh NG, Lalloo R, Narendran S, Johnson NW (2003) Oral diseases and socio-economic status (SES). Br Dent J 194(2):91–96; discussion 88. https://doi.org/10.1038/sj.bdj.4809882
Broadbent JM, Thomson WM (2005) For debate: problems with the DMF index pertinent to dental caries data analysis. Community Dent Oral Epidemiol 33(6):400–409. https://doi.org/10.1111/j.1600-0528.2005.00259.x
O'Leary TJ, Drake RB, Naylor JE (1972) The plaque control record. J Periodontol 43(1):38
Kingman A, Susin C, Albandar JM (2008) Effect of partial recording protocols on severity estimates of periodontal disease. J Clin Periodontol 35(8):659–667. https://doi.org/10.1111/j.1600-051X.2008.01243.x
Susin C, Kingman A, Albandar JM (2005) Effect of partial recording protocols on estimates of prevalence of periodontal disease. J Periodontol 76(2):262–267. https://doi.org/10.1902/jop.2005.76.2.262
Page RC, Eke PI (2007) Case definitions for use in population-based surveillance of periodontitis. J Periodontol 78(7 Suppl):1387–1399. https://doi.org/10.1902/jop.2007.060264
Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ (2012) Update of the case definitions for population-based surveillance of periodontitis. J Periodontol 83(12):1449–1454. https://doi.org/10.1902/jop.2012.110664
Fouad AF, Barry J, Caimano M, Clawson M, Zhu Q, Carver R, Hazlett K, Radolf JD (2002) PCR-based identification of bacteria associated with endodontic infections. J Clin Microbiol 40(9):3223–3231
Tran SD, Rudney JD (1999) Improved multiplex PCR using conserved and species-specific 16S rRNA gene primers for simultaneous detection of Actinobacillus actinomycetemcomitans, Bacteroides forsythus, and Porphyromonas gingivalis. J Clin Microbiol 37(11):3504–3508
Garcia L, Tercero JC, Legido B, Ramos JA, Alemany J, Sanz M (1998) Rapid detection of Actinobacillus actinomycetemcomitans, Prevotella intermedia and Porphyromona gingivalis by multiplex PCR. J Periodontal Res 33(1):59–64
Ashimoto A, Chen C, Bakker I, Slots J (1996) Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 11(4):266–273
Guillot E, Mouton C (1996) A PCR-DNA probe assay specific for Bacteroides forsythus. Mol Cell Probes 10(6):413–421. https://doi.org/10.1006/mcpr.1996.0057
Psoter WJ, Ge Y, Russell SL, Chen Z, Katz RV, Jean-Charles G, Li Y (2011) PCR detection of Streptococcus mutans and Aggregatibacter actinomycetemcomitans in dental plaque samples from Haitian adolescents. Clin Oral Investig 15(4):461–469. https://doi.org/10.1007/s00784-010-0413-y
Castillo A, Mesa F, Liebana J, Garcia-Martinez O, Ruiz S, Garcia-Valdecasas J, O'Valle F (2007) Periodontal and oral microbiological status of an adult population undergoing haemodialysis: a cross-sectional study. Oral Dis 13(2):198–205. https://doi.org/10.1111/j.1601-0825.2006.01267.x
Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ, Cdc Periodontal Disease Surveillance workgroup: James Beck GDRP (2012) Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res 91(10):914–920. https://doi.org/10.1177/0022034512457373
Axelsson P, Lindhe J, Nystrom B (1991) On the prevention of caries and periodontal disease. Results of a 15-year longitudinal study in adults. J Clin Periodontol 18(3):182–189
Sakki TK, Knuuttila ML, Vimpari SS, Hartikainen MS (1995) Association of lifestyle with periodontal health. Community Dent Oral Epidemiol 23(3):155–158
Sakki TK, Knuuttila ML, Vimpari SS, Kivela SL (1994) Lifestyle, dental caries and number of teeth. Community Dent Oral Epidemiol 22(5 Pt 1):298–302
Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG (2010) The human oral microbiome. J Bacteriol 192(19):5002–5017. https://doi.org/10.1128/JB.00542-10
Ding AM, Palmer RJ Jr, Cisar JO, Kolenbrander PE (2010) Shear-enhanced oral microbial adhesion. Appl Environ Microbiol 76(4):1294–1297. https://doi.org/10.1128/AEM.02083-09
Valm AM, Mark Welch JL, Rieken CW, Hasegawa Y, Sogin ML, Oldenbourg R, Dewhirst FE, Borisy GG (2011) Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proc Natl Acad Sci U S A 108(10):4152–4157. https://doi.org/10.1073/pnas.1101134108
Kozlovsky A, Wolff A, Saminsky M, Mazor Y, Venezia E, Bar-Ness Greenstein R (2015) Effect of Aggregatibacter actinomycetemcomitans from aggressive periodontitis patients on Streptococcus mutans. Oral Dis 21(8):955–961. https://doi.org/10.1111/odi.12362
Fine DH, Furgang D, Goldman D (2007) Saliva from subjects harboring Actinobacillus actinomycetemcomitans kills Streptococcus mutans in vitro. J Periodontol 78(3):518–526. https://doi.org/10.1902/jop.2007.060229
Kaplan JB, Schreiner HC, Furgang D, Fine DH (2002) Population structure and genetic diversity of Actinobacillus actinomycetemcomitans strains isolated from localized juvenile periodontitis patients. J Clin Microbiol 40(4):1181–1187
DiRienzo JM, Slots J, Sixou M, Sol MA, Harmon R, McKay TL (1994) Specific genetic variants of Actinobacillus actinomycetemcomitans correlate with disease and health in a regional population of families with localized juvenile periodontitis. Infect Immun 62(8):3058–3065
Paju S, Carlson P, Jousimies-Somer H, Asikainen S (2000) Heterogeneity of Actinobacillus actinomycetemcomitans strains in various human infections and relationships between serotype, genotype, and antimicrobial susceptibility. J Clin Microbiol 38(1):79–84
Zambon JJ, Slots J, Genco RJ (1983) Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect Immun 41(1):19–27
Johannsen A, Susin C, Gustafsson A (2014) Smoking and inflammation: evidence for a synergistic role in chronic disease. Periodontol 64(1):111–126. https://doi.org/10.1111/j.1600-0757.2012.00456.x
Nascimento GG, Leite FRM, Vestergaard P, Scheutz F, Lopez R (2018) Does diabetes increase the risk of periodontitis? A systematic review and meta-regression analysis of longitudinal prospective studies. Acta Diabetol. https://doi.org/10.1007/s00592-018-1120-4
Corsi DJ, Boyle MH, Lear SA, Chow CK, Teo KK, Subramanian SV (2014) Trends in smoking in Canada from 1950 to 2011: progression of the tobacco epidemic according to socioeconomic status and geography. Cancer Causes Control 25(1):45–57. https://doi.org/10.1007/s10552-013-0307-9
Christersson LA, Zambon JJ, Genco RJ (1991) Dental bacterial plaques. Nature and role in periodontal disease. J Clin Periodontol 18(6):441–446
Mdala I, Olsen I, Haffajee AD, Socransky SS, Thoresen M, de Blasio BF (2014) Comparing clinical attachment level and pocket depth for predicting periodontal disease progression in healthy sites of patients with chronic periodontitis using multi-state Markov models. J Clin Periodontol 41(9):837–845. https://doi.org/10.1111/jcpe.12278
Michalowicz BS, Hodges JS, Pihlstrom BL (2013) Is change in probing depth a reliable predictor of change in clinical attachment loss? J Am Dent Assoc 144(2):171–178
Hill EG, Slate EH, Wiegand RE, Grossi SG, Salinas CF (2006) Study design for calibration of clinical examiners measuring periodontal parameters. J Periodontol 77(7):1129–1141. https://doi.org/10.1902/jop.2006.050395
Osborn JB, Stoltenberg JL, Huso BA, Aeppli DM, Pihlstrom BL (1992) Comparison of measurement variability in subjects with moderate periodontitis using a conventional and constant force periodontal probe. J Periodontol 63(4):283–289. https://doi.org/10.1902/jop.19126.96.36.1993
Brennan RM, Genco RJ, Wilding GE, Hovey KM, Trevisan M, Wactawski-Wende J (2007) Bacterial species in subgingival plaque and oral bone loss in postmenopausal women. J Periodontol 78(6):1051–1061. https://doi.org/10.1902/jop.2007.060436
Saygun I, Nizam N, Keskiner I, Bal V, Kubar A, Acikel C, Serdar M, Slots J (2011) Salivary infectious agents and periodontal disease status. J Periodontal Res 46(2):235–239. https://doi.org/10.1111/j.1600-0765.2010.01335.x
Darout IA, Skaug N, Albandar JM (2003) Subgingival microbiota levels and their associations with periodontal status at the sampled sites in an adult Sudanese population using miswak or toothbrush regularly. Acta Odontol Scand 61(2):115–122
Papapanou PN, Teanpaisan R, Obiechina NS, Pithpornchaiyakul W, Pongpaisal S, Pisuithanakan S, Baelum V, Fejerskov O, Dahlen G (2002) Periodontal microbiota and clinical periodontal status in a rural sample in southern Thailand. Eur J Oral Sci 110(5):345–352
Zambon JJ (1985) Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol 12(1):1–20
The authors wish to express their gratitude to Ms. Chantal Morand for her assistance in recruiting the participants, Dr. Jean Barbeau for his logistical support and expertise, and Ms. Annie Leduc and Mr. Jabrane Azelmat for their training and assistance with the microbiological assessments in the laboratory. They would also like to thank Drs. Véronique Benhamou and Paul Allison for their support in recruiting participants at the McGill University dental clinics.
This study was supported by the Ernest-Charron research fund of the Faculty of Dental Medicine at the Université de Montréal.
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The authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
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Durand, R., Roufegarinejad, A., Chandad, F. et al. Dental caries are positively associated with periodontal disease severity. Clin Oral Invest 23, 3811–3819 (2019). https://doi.org/10.1007/s00784-019-02810-6
- Periodontal disease