Advertisement

Current Oral Health Reports

, Volume 4, Issue 4, pp 301–308 | Cite as

Periodontitis: from Infection to Inflammation

  • Gustavo G. Nascimento
  • Fabio R. M. Leite
  • Flemming Scheutz
  • Rodrigo LópezEmail author
Epidemiology (M Laine, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Epidemiology

Abstract

Purpose of the Review

The purpose of this study is to discuss the current understanding of periodontitis causation.

Recent Findings

The understanding of periodontitis as a monocausal infection has hindered the investigation of other potential causes that influence periodontitis morbidity and does not reflect the complexity of periodontitis etiology. Still today, the periodontal literature frequently defines periodontitis as an infection, whereas other potential causes of periodontitis, like smoking, which seems to be causally related to periodontitis, are typically called modifying or susceptibility factors. Instead of addressing the complexity of periodontitis, the field has narrowed its focus trying to find the most important bacteria or gene. Distal causes of periodontitis and interaction between constellations of causes at multiple levels have been commonly neglected.

Summary

Understanding periodontitis as a group of signs and symptoms characterized by inflammatory destruction of the periodontium would provide a better frame for future etiological research.

Keywords

Longitudinal studies Periodontal diseases Periodontitis Periodontitis risk Periodontitis risk factors Periodontitis causes 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Susser M, Susser E. Choosing a future for epidemiology: I. Eras and paradigms. Am J Public Health. 1996;86:668–73.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Talbot ES. Pyorrhea alveolaris. Dental Cosmos. 1886;28(689):692.Google Scholar
  3. 3.
    Harris GB. The treatment of pyorrhea by bacterial vaccines, and the results of animal experimentation. Dental Cosmos. 1913;55(4):388–92.Google Scholar
  4. 4.
    Harlan AW. Treatment of pyorrhea alveolaris. Dental Cosmos. 1883;25:517–21.Google Scholar
  5. 5.
    Hujoel PP, Zina LG, Cunha-Cruz J, Lopez R. Historical perspectives on theories of periodontal disease etiology. Periodontol 2000. 2012;58:153–60.CrossRefPubMedGoogle Scholar
  6. 6.
    Löe H, Theilade E, Jensen SB. Experimental gingivitis in man. J Periodontol. 1965;36:177–87.  https://doi.org/10.1902/jop.1965.36.3.177.CrossRefPubMedGoogle Scholar
  7. 7.
    Kinane DF, Attstrom R. European Workshop in Periodontology group B. Advances in the pathogenesis of periodontitis. Group B consensus report of the fifth European Workshop in Periodontology. J Clin Periodontol. 2005;32(Suppl 6):130–1.  https://doi.org/10.1111/j.1600-051X.2005.00823.x.CrossRefPubMedGoogle Scholar
  8. 8.
    Kinane D, Lindhe J, Trombelli L. Chronic periodontitis. In: Lindhe J, Lang N, editors. Clinical periodontology and implant dentistry. West Sussex: Wiley; 2015. p. 381–9.Google Scholar
  9. 9.
    Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000. 1994;5:78–111.CrossRefPubMedGoogle Scholar
  10. 10.
    • Scheutz F, Poulsen S. Determining causation in epidemiology. Community Dent Oral Epidemiol. 1999;27(3):161–70. A review on how to infer causality in oral health studies based on epidemiological concepts. CrossRefPubMedGoogle Scholar
  11. 11.
    Lalla E, Papapanou P. Modifying factors. In: Lindhe J, Lang NP, editors. Clinical periodontology and implant dentistry. 6th ed. West Sussex: John Wiley & Sons, Ltd; 2015. p. 270–89.Google Scholar
  12. 12.
    Knight ET, Liu J, Seymour GJ, Faggion CM, Cullinan MP. Risk factors that may modify the innate and adaptive immune responses in periodontal diseases. Periodontol 2000. 2016;71(1):22–51.  https://doi.org/10.1111/prd.12110.CrossRefPubMedGoogle Scholar
  13. 13.
    Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontol 2000. 2004;34:9–21.CrossRefPubMedGoogle Scholar
  14. 14.
    Research, Science and Therapy Committee of the American Academy of Periodontology. Periodontal diseases of children and adolescents. Pediatr Dent. 2008;30(Suppl 7):240–7.Google Scholar
  15. 15.
    Lindhe J, Ranney R, Lamster I, Charles A, Chung CP, Flemmig T, et al. 1999 International Workshop for a Classification of Periodontal Diseases and Conditions. Papers. Oak Brook, Illinois, October 30–November 2, 1999. Consensus report: Chronic periodontitis. Ann Periodontol. 1999;4:38.CrossRefGoogle Scholar
  16. 16.
    Lang N, Bartold PM, Cullinan M, Jeffcoat M, Mombelli A, Murakami S, et al. 1999 International Workshop for a Classification of Periodontal Diseases and Conditions. Papers. Oak Brook, Illinois, October 30–November 2, 1999. Consensus report: Aggressive periodontitis. Ann Periodontol. 1999;4:53.CrossRefGoogle Scholar
  17. 17.
    Yalda B, Offenbacher S, Collins JG. Diabetes as a modifier of periodontal disease expression. Periodontol 2000. 1994;6:37–49.CrossRefPubMedGoogle Scholar
  18. 18.
    Rothman KJ, Greenland S, Poole C, Lash TL. Causation and causal inference. In: Rothman KJ, Greenland S, Lash TL, editors. Modern Epidemiology. Philadelphia: Lippincott Williams & Wilkins; 2008. p. 5–31.Google Scholar
  19. 19.
    •• Rothman KJ, Greenland S. Causation and causal inference in epidemiology. Am J Public Health. 2005;95(Suppl 1):S144–50.  https://doi.org/10.2105/AJPH.2004.059204. Rothman and Greenland discuss causation and causal inference in epidemiology, reviewing, and introducing key concepts for future studies. CrossRefPubMedGoogle Scholar
  20. 20.
    •• López R, Hujoel P, Belibasakis GN. On putative periodontal pathogens: an epidemiological perspective. Virulence. 2015;6(3):249–57.  https://doi.org/10.1080/21505594.2015.1014266. The authors discuss the role of bacteria in periodontitis onset and progression. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Rothman KJ. Causes. Am J Epidemiol. 1976;104(6):587–92.CrossRefPubMedGoogle Scholar
  22. 22.
    Chalmers AF. What is this thing called science? King’s Lynn: Biddles Ltd; 1999.Google Scholar
  23. 23.
    Hujoel PP, Cunha-Cruz J, Kressin NR. Spurious associations in oral epidemiological research: the case of dental flossing and obesity. J Clin Periodontol. 2006;33(8):520–3.  https://doi.org/10.1111/j.1600-051X.2006.00954.x.CrossRefPubMedGoogle Scholar
  24. 24.
    MacMahon B, Trichopoulos D. Principles of epidemiology. Boston: Little, Brown; 1996.Google Scholar
  25. 25.
    Hill AB. The environment and disease: association or causation? Proc R Soc Med. 1965;58:295–300.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Murad MH, Asi N, Alsawas M, Alahdab F. New evidence pyramid. Evid Based Med. 2016;21(4):125–7.  https://doi.org/10.1136/ebmed-2016-110401.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Wang J, Lv J, Wang W, Jiang X. Alcohol consumption and risk of periodontitis: a meta-analysis. J Clin Periodontol. 2016;43(7):572–83.  https://doi.org/10.1111/jcpe.12556.CrossRefPubMedGoogle Scholar
  28. 28.
    Chávarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009;7(2):107–27.PubMedGoogle Scholar
  29. 29.
    Zimmermann H, Zimmermann N, Hagenfeld D, Veile A, Kim TS, Becher H. Is frequency of tooth brushing a risk factor for periodontitis? A systematic review and meta-analysis. Community Dent Oral Epidemiol. 2015;43(2):116–27.  https://doi.org/10.1111/cdoe.12126.CrossRefPubMedGoogle Scholar
  30. 30.
    Nascimento GG, Leite FR, Do LG, Peres KG, Correa MB, Demarco FF, et al. Is weight gain associated with the incidence of periodontitis? A systematic review and meta-analysis. J Clin Periodontol. 2015;42(6):495–505.  https://doi.org/10.1111/jcpe.12417.CrossRefPubMedGoogle Scholar
  31. 31.
    Hujoel P, Zina L, Cunha-Cruz J, Lopez R. Specific infections as the etiology of destructive periodontal disease: a systematic review. Eur J Oral Sci. 2013;121(1):2–6.  https://doi.org/10.1111/eos.12011.CrossRefPubMedGoogle Scholar
  32. 32.
    Schuch HS, Peres KG, Singh A, Peres MA, Do LG. Socioeconomic position during life and periodontitis in adulthood: a systematic review. Community Dent Oral Epidemiol. 2017;45(3):201–8.  https://doi.org/10.1111/cdoe.12278.CrossRefPubMedGoogle Scholar
  33. 33.
    Pitiphat W, Merchant AT, Rimm EB, Joshipura KJ. Alcohol consumption increases periodontitis risk. J Dent Res. 2003;82(7):509–13.  https://doi.org/10.1177/154405910308200704.CrossRefPubMedGoogle Scholar
  34. 34.
    Okamoto Y, Tsuboi S, Suzuki S, Nakagaki H, Ogura Y, Maeda K, et al. Effects of smoking and drinking habits on the incidence of periodontal disease and tooth loss among Japanese males: a 4-yr longitudinal study. J Periodontal Res. 2006;41(6):560–6.  https://doi.org/10.1111/j.1600-0765.2006.00907.x.CrossRefPubMedGoogle Scholar
  35. 35.
    Hach M, Holm-Pedersen P, Adegboye AR, Avlund K. The effect of alcohol consumption on periodontitis in older Danes. Int J Dent Hyg. 2015;13(4):261–7.  https://doi.org/10.1111/idh.12121.CrossRefPubMedGoogle Scholar
  36. 36.
    Nishida N, Yamamoto Y, Tanaka M, Kataoka K, Kuboniwa M, Nakayama K, et al. Association between involuntary smoking and salivary markers related to periodontitis: a 2-year longitudinal study. J Periodontol. 2008;79(12):2233–40.  https://doi.org/10.1902/jop.2008.080149.CrossRefPubMedGoogle Scholar
  37. 37.
    Firatli E. The relationship between clinical periodontal status and insulin-dependent diabetes mellitus. Results after 5 years. J Periodontol. 1997;68(2):136–40.  https://doi.org/10.1902/jop.1997.68.2.136.CrossRefPubMedGoogle Scholar
  38. 38.
    Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, et al. Non-insulin dependent diabetes mellitus and alveolar bone loss progression over 2 years. J Periodontol. 1998;69(1):76–83.  https://doi.org/10.1902/jop.1998.69.1.76.CrossRefPubMedGoogle Scholar
  39. 39.
    Sbordone L, Ramaglia L, Barone A, Ciaglia RN, Iacono VJ. Periodontal status and subgingival microbiota of insulin-dependent juvenile diabetics: a 3-year longitudinal study. J Periodontol. 1998;69(2):120–8.  https://doi.org/10.1902/jop.1998.69.2.120.CrossRefPubMedGoogle Scholar
  40. 40.
    Novaes AB Jr, Silva MAP, Batista EL Jr, Dos Anjos BA, Novaes AB, Pereira ALA. Manifestations of insulin-dependent diabetes mellitus in the periodontium of young Brazilian patients. A 10-year follow-up study. J Periodontol. 1997;68(4):328–34.CrossRefPubMedGoogle Scholar
  41. 41.
    Teng HC, Lee CH, Hung HC, Tsai CC, Chang YY, Yang YH, et al. Lifestyle and psychosocial factors associated with chronic periodontitis in Taiwanese adults. J Periodontol. 2003;74(8):1169–75.  https://doi.org/10.1902/jop.2003.74.8.1169.CrossRefPubMedGoogle Scholar
  42. 42.
    Gelskey SC, Young TK, Singer DL. Factors associated with adult periodontitis in a dental teaching clinic population. Community Dent Oral Epidemiol. 1998;26(4):226–32.CrossRefPubMedGoogle Scholar
  43. 43.
    Saxlin T, Ylostalo P, Suominen-Taipale L, Aromaa A, Knuuttila M. Overweight and obesity weakly predict the development of periodontal infection. J Clin Periodontol. 2010;37(12):1059–67.  https://doi.org/10.1111/j.1600-051X.2010.01633.x.CrossRefPubMedGoogle Scholar
  44. 44.
    Morita I, Okamoto Y, Yoshii S, Nakagaki H, Mizuno K, Sheiham A, et al. Five-year incidence of periodontal disease is related to body mass index. J Dent Res. 2011;90(2):199–202.  https://doi.org/10.1177/0022034510382548.CrossRefPubMedGoogle Scholar
  45. 45.
    Jimenez M, Hu FB, Marino M, Li Y, Joshipura KJ. Prospective associations between measures of adiposity and periodontal disease. Obesity. 2012;20(8):1718–25.  https://doi.org/10.1038/oby.2011.291.CrossRefPubMedGoogle Scholar
  46. 46.
    Ekuni D, Mizutani S, Kojima A, Tomofuji T, Irie K, Azuma T, et al. Relationship between increases in BMI and changes in periodontal status: a prospective cohort study. J Clin Periodontol. 2014;41(8):772–8.  https://doi.org/10.1111/jcpe.12273.CrossRefPubMedGoogle Scholar
  47. 47.
    Gorman A, Kaye EK, Apovian C, Fung TT, Nunn M, Garcia RI. Overweight and obesity predict time to periodontal disease progression in men. J Clin Periodontol. 2012;39(2):107–14.  https://doi.org/10.1111/j.1600-051X.2011.01824.x.CrossRefPubMedGoogle Scholar
  48. 48.
    Van der Velden U, Abbas F, Armand S, Loos BG, Timmerman MF, Van der Weijden GA, et al. Java project on periodontal diseases. The natural development of periodontitis: risk factors, risk predictors and risk determinants. J Clin Periodontol. 2006;33(8):540–8.  https://doi.org/10.1111/j.1600-051X.2006.00953.x.CrossRefPubMedGoogle Scholar
  49. 49.
    Fine DH, Markowitz K, Furgang D, Fairlie K, Ferrandiz J, Nasri C, et al. Aggregatibacter actinomycetemcomitans and its relationship to initiation of localized aggressive periodontitis: longitudinal cohort study of initially healthy adolescents. J Clin Microbiol. 2007;45(12):3859–69.  https://doi.org/10.1128/JCM.00653-07.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Haubek D, Ennibi OK, Poulsen K, Vaeth M, Poulsen S, Kilian M. Risk of aggressive periodontitis in adolescent carriers of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans in Morocco: a prospective longitudinal cohort study. Lancet. 2008;371(9608):237–42.  https://doi.org/10.1016/S0140-6736(08)60135-X.CrossRefPubMedGoogle Scholar
  51. 51.
    Baljoon M, Natto S, Bergström J. Long-term effect of smoking on vertical periodontal bone loss. J Clin Periodontol. 2005;32(7):789–97.  https://doi.org/10.1111/j.1600-051X.2005.00765.x.CrossRefPubMedGoogle Scholar
  52. 52.
    Craig RG, Yip JK, Mijares DQ, LeGeros RZ, Socransky SS, Haffajee AD. Progression of destructive periodontal diseases in three urban minority populations: role of clinical and demographic factors. J Clin Periodontol. 2003;30(12):1075–83.  https://doi.org/10.1046/j.0303-6979.2003.00421.x.CrossRefPubMedGoogle Scholar
  53. 53.
    Gilbert GH, Shelton BJ, Fisher MA. Forty-eight-month periodontal attachment loss incidence in a population-based cohort study: role of baseline status, incident tooth loss, and specific behavioral factors. J Periodontol. 2005;76(7):1161–70.  https://doi.org/10.1902/jop.2005.76.7.1161.CrossRefPubMedGoogle Scholar
  54. 54.
    Gätke D, Holtfreter B, Biffar R, Kocher T. Five-year change of periodontal diseases in the Study of Health in Pomerania (SHIP). J Clin Periodontol. 2012;39(4):357–67.  https://doi.org/10.1111/j.1600-051X.2011.01849.x.CrossRefPubMedGoogle Scholar
  55. 55.
    Haas AN, Wagner MC, Oppermann RV, Rosing CK, Albandar JM, Susin C. Risk factors for the progression of periodontal attachment loss: a 5-year population-based study in South Brazil. J Clin Periodontol. 2014;41(3):215–23.  https://doi.org/10.1111/jcpe.12213.CrossRefPubMedGoogle Scholar
  56. 56.
    Kibayashi M, Tanaka M, Nishida N, Kuboniwa M, Kataoka K, Nagata H, et al. Longitudinal study of the association between smoking as a periodontitis risk and salivary biomarkers related to periodontitis. J Periodontol. 2007;78(5):859–67.  https://doi.org/10.1902/jop.2007.060292.CrossRefPubMedGoogle Scholar
  57. 57.
    Mdala I, Olsen I, Haffajee AD, Socransky SS, Thoresen M, de Blasio BF. 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. 2014;41(9):837–45.  https://doi.org/10.1111/jcpe.12278.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Norderyd O, Hugoson A, Grusovin G. Risk of severe periodontal disease in a Swedish adult population. A longitudinal study. J Clin Periodontol. 1999;26(9):608–15.CrossRefPubMedGoogle Scholar
  59. 59.
    Ogawa H, Yoshihara A, Hirotomi T, Ando Y, Miyazaki H. Risk factors for periodontal disease progression among elderly people. J Clin Periodontol. 2002;29(7):592–7.CrossRefPubMedGoogle Scholar
  60. 60.
    Thomson WM, Shearer DM, Broadbent JM, Foster Page LA, Poulton R. The natural history of periodontal attachment loss during the third and fourth decades of life. J Clin Periodontol. 2013;40(7):672–80.  https://doi.org/10.1111/jcpe.12108.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Poulton R, Caspi A, Milne BJ, Thomson WM, Taylor A, Sears MR, et al. Association between children’s experience of socioeconomic disadvantage and adult health: a life-course study. Lancet. 2002;360(9346):1640–5.  https://doi.org/10.1016/S0140-6736(02)11602-3.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Paulander J, Wennstrom JL, Axelsson P, Lindhe J. Some risk factors for periodontal bone loss in 50-year-old individuals. A 10-year cohort study. J Clin Periodontol. 2004;31(7):489–96.  https://doi.org/10.1111/j.1600-051X.2004.00514.x.CrossRefPubMedGoogle Scholar
  63. 63.
    Machtei EE, Hausmann E, Dunford R, Grossi S, Ho A, Davis G, et al. Longitudinal study of predictive factors for periodontal disease and tooth loss. J Clin Periodontol. 1999;26(6):374–80.CrossRefPubMedGoogle Scholar
  64. 64.
    Lu HX, Wong MC, Lo EC, McGrath C. Trends in oral health from childhood to early adulthood: a life course approach. Community Dent Oral Epidemiol. 2011;39(4):352–60.  https://doi.org/10.1111/j.1600-0528.2011.00611.x.CrossRefPubMedGoogle Scholar
  65. 65.
    Ismail AI, Morrison EC, Burt BA, Caffesse RG, Kavanagh MT. Natural history of periodontal disease in adults: findings from the Tecumseh Periodontal Disease Study, 1959–87. J Dent Res. 1990;69(2):430–5.  https://doi.org/10.1177/00220345900690020201.CrossRefPubMedGoogle Scholar
  66. 66.
    Haas AN, Gaio EJ, Oppermann RV, Rosing CK, Albandar JM, Susin C. Pattern and rate of progression of periodontal attachment loss in an urban population of South Brazil: a 5-years population-based prospective study. J Clin Periodontol. 2012;39(1):1–9.  https://doi.org/10.1111/j.1600-051X.2011.01818.x.CrossRefPubMedGoogle Scholar
  67. 67.
    Buchwald S, Kocher T, Biffar R, Harb A, Holtfreter B, Meisel P. Tooth loss and periodontitis by socio-economic status and inflammation in a longitudinal population-based study. J Clin Periodontol. 2013;40(3):203–11.  https://doi.org/10.1111/jcpe.12056.CrossRefPubMedGoogle Scholar
  68. 68.
    Balshem H, Helfand M, Schunemann HJ, Oxman AD, Kunz R, Brozek J, et al. GRADE guidelines: 3. Rating the quality of evidence. J Clin Epidemiol. 2011;64(4):401–6.  https://doi.org/10.1016/j.jclinepi.2010.07.015.CrossRefPubMedGoogle Scholar
  69. 69.
    Susser M. Should the epidemiologist be a social scientist or a molecular biologist? Int J Epidemiol. 1999;28(5):S1019–22.CrossRefPubMedGoogle Scholar
  70. 70.
    Rose G. Sick individuals and sick populations. Int J Epidemiol. 1985;14(1):32–8.CrossRefPubMedGoogle Scholar
  71. 71.
    Pearce N. Traditional epidemiology, modern epidemiology, and public health. Am J Public Health. 1996;86(5):678–83.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Baelum V, Lopez R. Periodontal epidemiology: towards social science or molecular biology? Community Dent Oral Epidemiol. 2004;32:239–49.CrossRefPubMedGoogle Scholar
  73. 73.
    Krieger N. Epidemiology and the web of causation: has anyone seen the spider? Soc Sci Med. 1994;39(7):887–903.CrossRefPubMedGoogle Scholar
  74. 74.
    • Baker SR, Gibson BG. Social oral epidemi(olog)(2)y where next: one small step or one giant leap? Community Dent Oral Epidemiol. 2014;42(6):481–94.  https://doi.org/10.1111/cdoe.12118. The authors present a discussion on the caveats and the future of oral epidemiology. CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Nascimento GG, Peres MA, Mittinty MN, Peres KG, Do LG, Horta BL, et al. Diet-induced overweight and obesity and periodontitis risk: an application of the parametric g-formula in the 1982 Pelotas Birth Cohort. Am J Epidemiol. 2017;185(6):442–451.  https://doi.org/10.1093/aje/kww187.
  76. 76.
    Robins JM, Greenland S. Identifiability and exchangeability for direct and indirect effects. Epidemiology. 1992;3(2):143–55.CrossRefPubMedGoogle Scholar
  77. 77.
    Robins JM, Hernan MA, Brumback B. Marginal structural models and causal inference in epidemiology. Epidemiology. 2000;11(5):550–60.CrossRefPubMedGoogle Scholar
  78. 78.
    •• Baelum V, Lopez R. Defining and classifying periodontitis: need for a paradigm shift? Eur J Oral Sci. 2003;111(1):2–6. The authors discuss new perspectives regarding the classification of periodontitis. CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Gustavo G. Nascimento
    • 1
  • Fabio R. M. Leite
    • 1
  • Flemming Scheutz
    • 1
  • Rodrigo López
    • 1
    Email author
  1. 1.Section of Periodontology, Department of Dentistry and Oral HealthAarhus UniversityAarhus CDenmark

Personalised recommendations