Periodontal disease, tooth loss and incident rheumatoid arthritis: Results from the First National Health and Nutrition Examination Survey and its epidemiological follow-up study

Journal of Clinical Periodontology

Volumn 38, Issue 11, 2011, Pages 998-1006

  Demmer, Ryan T ^a   Molitor, Jerry A ^b   Jacobs Jr , David R ^c,d   Michalowicz, Bryan S ^e  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF OSLO   (Norway)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

bias; cohort studies; infections; periodontal; rheumatoid arthritis

Indexed keywords

ADULT; AGE; AGED; ARTICLE; CHRONIC PERIODONTITIS; CROSS-SECTIONAL STUDY; FEMALE; GINGIVITIS; HUMAN; INCIDENCE; MALE; MIDDLE AGED; PERIODONTAL DISEASE; PERIODONTICS; PREVALENCE; RHEUMATOID ARTHRITIS; RISK; SEX DIFFERENCE; SMOKING; UNITED STATES;

ADULT; AGE FACTORS; AGED; ARTHRITIS, RHEUMATOID; CHRONIC PERIODONTITIS; CROSS-SECTIONAL STUDIES; FEMALE; GINGIVITIS; HUMANS; INCIDENCE; MALE; MIDDLE AGED; ODDS RATIO; PERIODONTAL INDEX; PREVALENCE; SEX FACTORS; SMOKING; TOOTH LOSS; UNITED STATES;

EID: 80054067470     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/j.1600-051X.2011.01776.x     Document Type: Article

References (50)

1. Al-Katma, M. K., Bissada, N. F., Bordeaux, J. M., Sue, J., &, Askari, A. D., (2007) Control of periodontal infection reduces the severity of active rheumatoid arthritis. Journal of Clinical Rheumatology 13, 134-137. (Pubitemid 46884200)
2. Arkema, E. V., Karlson, E. W., &, Costenbader, K. H., (2010) A prospective study of periodontal disease and risk of rheumatoid arthritis. Journal of Rheumatology 37, 1800-1804.
3. Arnett, F. C., Edworthy, S. M., Bloch, D. A., Mcshane, D. J., Fries, J. F., Cooper, N. S., Healey, L. A., Kaplan, S. R., Liang, M. H., Luthra, H. S., Medsger, T. A., Mitchell, D. M., Neustadt, D. H., Pinals, R. S., Schaller, J. G., Sharp, J. T., Wilder, R. L., &, Hunder, G. G., (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis and Rheumatism 31, 315-324. (Pubitemid 18091653)
4. Bartold, P. M., Marino, V., Cantley, M., &, Haynes, D. R., (2010) Effect of Porphyromonas gingivalis-induced inflammation on the development of rheumatoid arthritis. Journal of Clinical Periodontology 37, 405-411.
5. Cantley, M. D., Haynes, D. R., Marino, V., &, Bartold, P. M., (2011) Pre-existing periodontitis exacerbates experimental arthritis in a mouse model. Journal of Clinical Periodontology 38, 532-541.
6. Criswell, L. A., Merlino, L. A., Cerhan, J. R., Mikuls, T. R., Mudano, A. S., Burma, M., Folsom, A. R., &, Saag, K. G., (2002) Cigarette smoking and the risk of rheumatoid arthritis among postmenopausal women: results from the Iowa Women's Health Study. American Journal of Medicine 112, 465-471. (Pubitemid 34450707)
7. Culshaw, S., Mcinnes, I. B., &, Liew, F. Y., (2011) What can the periodontal community learn from the pathophysiology of rheumatoid arthritis? Journal of Clinical Periodontology 38 (Suppl. 11), 106-113.
8. De Pablo, P., Chapple, I. L., Buckley, C. D., &, Dietrich, T., (2009) Periodontitis in systemic rheumatic diseases. Nature Reviews Rheumatology 5, 218-224.
9. De Pablo, P., Dietrich, T., &, Mcalindon, T. E., (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. Journal of Rheumatology 35, 70-76.
10. Demmer, R. T., Jacobs, D. R., Jr., &, Desvarieux, M., (2008a) Periodontal disease and incident type 2 diabetes: results from the First National Health and Nutrition Examination Survey and its epidemiologic follow-up study. Diabetes Care 31, 1373-1379.
11. Demmer, R. T., Kocher, T., Schwahn, C., Volzke, H., Jacobs, D. R., Jr., &, Desvarieux, M., (2008b) Refining exposure definitions for studies of periodontal disease and systemic disease associations. Community Dentistry and Oral Epidemiology 36, 493-502.
12. Demmer, R. T., Papapanou, P. N., Jacobs, D. R., Jr., &, Desvarieux, M., (2008c) Bleeding on probing differentially relates to bacterial profiles: the Oral Infections and Vascular Disease Epidemiology Study. Journal of Clinical Periodontology 35, 479-486.
13. Destefano, F., Anda, R. F., Kahn, H. S., Williamson, D. F., &, Russell, C. M., (1993) Dental disease and risk of coronary heart disease and mortality. BMJ 306, 688-691. (Pubitemid 23070231)
14. Desvarieux, M., Demmer, R. T., Rundek, T., Boden-Albala, B., Jacobs, D. R., Jr., Papapanou, P. N., &, Sacco, R. L., (2003) Relationship between periodontal disease, tooth loss, and carotid artery plaque: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Stroke 34, 2120-2125. (Pubitemid 37099823)
15. Desvarieux, M., Schwahn, C., Volzke, H., Demmer, R. T., Ludemann, J., Kessler, C., Jacobs, D. R., Jr., John, U., &, Kocher, T., (2004) Gender differences in the relationship between periodontal disease, tooth loss, and atherosclerosis. Stroke 35, 2029-2035. (Pubitemid 39129554)
16. Gabriel, S. E., (2008) Cardiovascular morbidity and mortality in rheumatoid arthritis. American Journal of Medicine 121, S9-S14.
17. Haffajee, A. D., &, Socransky, S. S., (1994) Microbial etiological agents of destructive periodontal diseases. Periodontology 5, 78-111.
18. Hung, H. C., Willett, W., Merchant, A., Rosner, B. A., Ascherio, A., &, Joshipura, K. J., (2003) Oral health and peripheral arterial disease. Circulation 107, 1152-1157. (Pubitemid 36297207)
19. Jansson, L., Lavstedt, S., &, Zimmerman, M., (2002) Prediction of marginal bone loss and tooth loss-a prospective study over 20 years. Journal of Clinical Periodontology 29, 672-678. (Pubitemid 41697806)
20. Joshipura, K. J., Hung, H.-C., Rimm, E. B., Willett, W. C., &, Ascherio, A., (2003) Periodontal disease, tooth loss, and incidence of ischemic stroke. Stroke 34, 47-52. (Pubitemid 36070799)
21. Karlson, E. W., Lee, I. M., Cook, N. R., Manson, J. E., Buring, J. E., &, Hennekens, C. H., (1999) A retrospective cohort study of cigarette smoking and risk of rheumatoid arthritis in female health professionals. Arthritis and Rheumatism 42, 910-917. (Pubitemid 29215001)
22. Kelly, J. E., &, Harvey, C. R., (1979) Basic data on dental examination findings of persons 1-74 years, United States, 1971-1974. Hyattsville, MD: U.S. Dept. of Health, Education, and Welfare, Public Health Service, Office of Health Research, Statistics.
23. Kinane, D. F., Riggio, M. P., Walker, K. F., Mackenzie, D., &, Shearer, B., (2005) Bacteraemia following periodontal procedures. Journal of Clinical Periodontology 32, 708-713. (Pubitemid 40923043)
24. Klareskog, L., Catrina, A. I., &, Paget, S., (2009) Rheumatoid arthritis. Lancet 373, 659-672.
25. Klareskog, L., Stolt, P., Lundberg, K., Kallberg, H., Bengtsson, C., Grunewald, J., Ronnelid, J., Harris, H. E., Ulfgren, A. K., Rantapaa-Dahlqvist, S., Eklund, A., Padyukov, L., &, Alfredsson, L., (2006) A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis and Rheumatism 54, 38-46. (Pubitemid 43122184)
26. Lundberg, K., Wegner, N., Yucel-Lindberg, T., &, Venables, P. J., (2010) Periodontitis in RA-the citrullinated enolase connection. Nature Reviews. Rheumatology 6, 727-730.
27. Machlin, S. R., Kleinman, J. C., &, Madans, J. H., (1989) Validity of mortality analysis based on retrospective smoking information. Statistics in Medicine 8, 997-1009. (Pubitemid 19214480)
28. Mattila, P. T., Niskanen, M. C., Vehkalahti, M. M., Nordblad, A., &, Knuuttila, M. L., (2010) Prevalence and simultaneous occurrence of periodontitis and dental caries. Journal of Clinical Periodontology 37, 962-967.
29. Mcgraw, W. T., Potempa, J., Farley, D., &, Travis, J., (1999) Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infection and Immunity 67, 3248-3256. (Pubitemid 29291488)
30. Mclaughlin, J. K., Dietz, M. S., Mehl, E. S., &, Blot, W. J., (1987) Reliability of surrogate information on cigarette smoking by type of informant. American Journal of Epidemiology 126, 144-146. (Pubitemid 17117701)
31. Miller, H. W., & NATIONAL CENTER FOR HEALTH STATISTICS (U.S.) (1973) Plan and operation of the Health and Nutrition Examination Survey, United States-1971-1973; a description of a national health and nutrition examination survey of a probability sample of the U.S. population 1-74 years of age. Rockville, MD: U.S. National Center for Health Statistics; [for sale by the Supt. of Docs].
32. Molitor, J. A., Alonso, A., Wener, M. H., Michalowicz, B. S., Beck, J. D., Gersuk, V. H., Buckner, J. H., &, Folsom, A. R., (2009) Moderate to severe adult periodontitis increases risk of rheumatoid arthritis in non-smokers and is associated with elevated ACPA titers: The ARIC Study. Arthritis & Rheumatism 60, S433.
33. Ortiz, P., Bissada, N. F., Palomo, L., Han, Y. W., Al-Zahrani, M. S., Panneerselvam, A., &, Askari, A., (2009) Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. Journal of Periodontology 80, 535-540.
34. Padyukov, L., Silva, C., Stolt, P., Alfredsson, L., &, Klareskog, L., (2004) A gene-environment interaction between smoking and shared epitope genes in HLA-DR provides a high risk of seropositive rheumatoid arthritis. Arthritis and Rheumatism 50, 3085-3092. (Pubitemid 39371983)
35. Papapanou, P. N., Baelum, V., Luan, W. M., Madianos, P. N., Chen, X., Fejerskov, O., &, Dahlen, G., (1997) Subgingival microbiota in adult Chinese: prevalence and relation to periodontal disease progression. Journal of Periodontology 68, 651-666. (Pubitemid 127519634)
36. Paster, B. J., Olsen, I., Aas, J. A., &, Dewhirst, F. E., (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontology 2000 42, 80-87. (Pubitemid 44286048)
37. Pischon, N., Pischon, T., Kroger, J., Gulmez, E., Kleber, B. M., Bernimoulin, J. P., Landau, H., Brinkmann, P. G., Schlattmann, P., Zernicke, J., Buttgereit, F., &, Detert, J., (2008) Association among rheumatoid arthritis, oral hygiene, and periodontitis. Journal of Periodontology 79, 979-986.
38. Rafferty, B., Jonsson, D., Kalachikov, S., Demmer, R. T., Nowygrod, R., Elkind, M. S., Bush, H., Jr., &, Kozarov, E., (2011) Impact of monocytic cells on recovery of uncultivable bacteria from atherosclerotic lesions. Journal of Internal Medicine 270, 273-280.
39. Rajasuo, A., Nyfors, S., Kanervo, A., Jousimies-Somer, H., Lindqvist, C., &, Suuronen, R., (2004a) Bacteremia after plate removal and tooth extraction. International Journal of Oral and Maxillofacial Surgery 33, 356-360. (Pubitemid 38786416)
40. Rajasuo, A., Perkki, K., Nyfors, S., Jousimies-Somer, H., &, Meurman, J. H., (2004b) Bacteremia following surgical dental extraction with an emphasis on anaerobic strains. Journal of Dental Research 83, 170-174. (Pubitemid 41713804)
41. Rosenstein, E. D., Greenwald, R. A., Kushner, L. J., &, Weissmann, G., (2004) Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 28, 311-318. (Pubitemid 41504274)
42. Russell, A. L., (1956) A system of classification and scoring for prevalence surveys of periodontal disease. Journal of Dental Research 35, 350-359.
43. SAS. PROC SURVEYLOGISTIC [Online]. Available at: [accessed December, 2010].
44. Timmerman, M. F., Van Der Weijden, G. A., Arief, E. M., Armand, S., Abbas, F., Winkel, E. G., Van Winkelhoff, A. J., &, Van Der Velden, U., (2001) Untreated periodontal disease in Indonesian adolescents. Subgingival microbiota in relation to experienced progression of periodontitis. Journal of Clinical Periodontology 28, 617-627. (Pubitemid 33755169)
45. Tobon, G. J., Youinou, P., &, Saraux, A., (2010) The environment, geo-epidemiology, and autoimmune disease: rheumatoid arthritis. Journal of Autoimmunity 35, 10-14.
46. Van Der Velden, U., Abbas, F., Armand, S., Loos, B. G., Timmerman, M. F., Van Der Weijden, G. A., Van Winkelhoff, A. J., &, Winkel, E. G., (2006) Java project on periodontal diseases. The natural development of periodontitis: risk factors, risk predictors and risk determinants. Journal of Clinical Periodontology 33, 540-548. (Pubitemid 44098398)
47. Van Winkelhoff, A. J., Loos, B. G., Van Der Reijden, W. A., &, Van Der Velden, U., (2002) Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. Journal of Clinical Periodontology 29, 1023-1028. (Pubitemid 41697772)
48. Volzke, H., Schwahn, C., Dorr, M., Schwarz, S., Robinson, D., Doren, M., Rettig, R., Felix, S. B., John, U., &, Kocher, T., (2006) Gender differences in the relation between number of teeth and systolic blood pressure. Journal of Hypertension 24, 1257-1263. (Pubitemid 43948323)
49. Wegner, N., Wait, R., Sroka, A., Eick, S., Nguyen, K. A., Lundberg, K., Kinloch, A., Culshaw, S., Potempa, J., &, Venables, P. J., (2010) Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis and Rheumatism 62, 2662-2672.
50. Wu, T., Trevisan, M., Genco, R. J., Dorn, J. P., Falkner, K. L., &, Sempos, C. T., (2000) Periodontal disease and risk of cerebrovascular disease: the first national health and nutrition examination survey and its follow-up study. Archives of Internal Medicine 160, 2749-2755.