J Periodontal Implant Sci.  2015 Oct;45(5):178-183. 10.5051/jpis.2015.45.5.178.

Humoral immune responses to periodontal pathogens in the elderly

• Shet U
• Oh HK
• Chung HJ
• Kim YJ
• Kim OS
• Lim HJ
• Shin MH
• Lee SW

• KMID: 2212006
• DOI: http://doi.org/10.5051/jpis.2015.45.5.178

Abstract

PURPOSE
Elderly people are thought to be more susceptible to periodontal disease due to reduced immune function associated with aging. However, little information is available on the nature of immune responses against putative periodontal pathogens in geriatric patients. The purpose of this study was to evaluate the serum IgG antibody responses to six periodontal pathogens in geriatric subjects.
METHODS
The study population consisted of 85 geriatric patients and was divided into three groups: 29 mild (MCP), 27 moderate (MoCP) and 29 severe (SCP) chronic periodontitis patients. Serum levels of IgG antibody to Porphyromonas gingivalis, Tannerella forsythia, Treponema denticola, Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum and Prevotella intermedia were measured by enzyme-linked immunosorbent assay (ELISA) and compared among the groups.
RESULTS
All three groups showed levels of serum IgG in response to P. gingivalis, A. actinomycetemcomitans, and P. intermedia that were three to four times higher than levels of IgG to T. forsythia, T. denticola, and F. nucleatum. There were no significant differences among all three groups in IgG response to P. gingivalis (P=0.065), T. forsythia (P=0.057), T. denticola (P=0.1), and P. intermedia (P=0.167), although the IgG levels tended to be higher in patients with SCP than in those with MCP or MoCP (with the exception of those for P. intermedia). In contrast, there were significant differences among the groups in IgG levels in response to F. nucleatum (P=0.001) and A. actinomycetemcomitans (P=0.003). IgG levels to A. actinomycetemcomitans were higher in patients with MCP than in those with MoCP or SCP.
CONCLUSIONS
When IgG levels were compared among three periodontal disease groups, only IgG levels to F. nucleatum significantly increased with the severity of disease. On the contrary, IgG levels to A. actinomycetemcomitans decreased significantly in patients with SCP compared to those with MCP. There were no significant differences in the IgG levels for P. gingivalis, T. forsythia, T. denticola, and P. intermedia among geriatric patients with chronic periodontitis.

Keyword

Chronic periodontitis; Disease progression; Enzyme-Linked Immunosorbent Assay; Geriatrics; Immunoglobulin G

MeSH Terms

Aged*
Aggregatibacter actinomycetemcomitans
Aging
Antibody Formation
Chronic Periodontitis
Disease Progression
Enzyme-Linked Immunosorbent Assay
Forsythia
Fusobacterium nucleatum
Geriatrics
Humans
Immunity, Humoral*
Immunoglobulin G
Periodontal Diseases
Porphyromonas gingivalis
Prevotella intermedia
Treponema denticola
Immunoglobulin G

Reference

1. Lee R. The outlook for population growth. Science. 2011; 333:569–573.

2. Davé S, Van Dyke T. The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis. 2008; 14:95–101.

3. Katz J, Wallet S, Cha S. Periodontal disease and the oral-systemic connection: "is it all the RAGE?". Quintessence Int. 2010; 41:229–237.

4. Papapanou PN. Systemic effects of periodontitis: lessons learned from research on atherosclerotic vascular disease and adverse pregnancy outcomes. Int Dent J. Forthcoming 2015.

5. Cullinan MP, Seymour GJ. Periodontal disease and systemic illness: will the evidence ever be enough? Periodontol 2000. 2013; 62:271–286.

6. Agarwal S, Busse PJ. Innate and adaptive immunosenescence. Ann Allergy Asthma Immunol. 2010; 104:183–190.

7. Boraschi D, Del Giudice G, Dutel C, Ivanoff B, Rappuoli R, Grubeck-Loebenstein B. Ageing and immunity: addressing immune senescence to ensure healthy ageing. Vaccine. 2010; 28:3627–3631.

8. Ebersole JL, Cappelli D, Holt SC. Periodontal diseases: to protect or not to protect is the question. Acta Odontol Scand. 2001; 59:161–166.

9. Ebersole JL, Taubman MA. The protective nature of host responses in periodontal diseases. Periodontol 2000. 1994; 5:112–141.

10. Darby IB, Mooney J, Kinane DF. Changes in subgingival microflora and humoral immune response following periodontal therapy. J Clin Periodontol. 2001; 28:796–805.

11. Ishikawa I, Nakashima K, Koseki T, Nagasawa T, Watanabe H, Arakawa S, et al. Induction of the immune response to periodontopathic bacteria and its role in the pathogenesis of periodontitis. Periodontol 2000. 1997; 14:79–111.

12. Teng YT. The role of acquired immunity and periodontal disease progression. Crit Rev Oral Biol Med. 2003; 14:237–252.

13. Teng YT. Protective and destructive immunity in the periodontium: Part 1--innate and humoral immunity and the periodontium. J Dent Res. 2006; 85:198–208.

14. Craig RG, Boylan R, Yip J, Mijares D, Imam M, Socransky SS, et al. Serum IgG antibody response to periodontal pathogens in minority populations: relationship to periodontal disease status and progression. J Periodontal Res. 2002; 37:132–146.

15. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999; 4:1–6.

16. Shet UK, Oh HK, Kim HJ, Chung HJ, Kim YJ, Kim OS, et al. Quantitative analysis of periodontal pathogens present in the saliva of geriatric subjects. J Periodontal Implant Sci. 2013; 43:183–190.

17. McArthur WP, Bloom C, Taylor M, Smith J, Wheeler T, Magnusson NI. Antibody responses to suspected periodontal pathogens in elderly subjects with periodontal disease. J Clin Periodontol. 1995; 22:842–849.

18. De Nardin AM, Sojar HT, Grossi SG, Christersson LA, Genco RJ. Humoral immunity of older adults with periodontal disease to Porphyromonas gingivalis. Infect Immun. 1991; 59:4363–4370.

19. Califano JV, Gunsolley JC, Schenkein HA, Tew JG. A comparison of IgG antibody reactive with Bacteroides forsythus and Porphyromonas gingivalis in adult and early-onset periodontitis. J Periodontol. 1997; 68:734–738.

20. Baker PJ, Carter S, Dixon M, Evans RT, Roopenian DC. Serum antibody response to oral infection precedes but does not prevent Porphyromonas gingivalis-induced alveolar bone loss in mice. Oral Microbiol Immunol. 1999; 14:194–196.

21. Albandar JM, DeNardin AM, Adesanya MR, Diehl SR, Winn DM. Associations between serum antibody levels to periodontal pathogens and early-onset periodontitis. J Periodontol. 2001; 72:1463–1469.

22. Nabers CL, Stalker WH, Esparza D, Naylor B, Canales S. Tooth loss in 1535 treated periodontal patients. J Periodontol. 1988; 59:297–300.

23. Papapanou PN, Wennström JL, Gröndahl K. Periodontal status in relation to age and tooth type. A cross-sectional radiographic study. J Clin Periodontol. 1988; 15:469–478.

24. Dye BA, Herrera-Abreu M, Lerche-Sehm J, Vlachojannis C, Pikdoken L, Pretzl B, et al. Serum antibodies to periodontal bacteria as diagnostic markers of periodontitis. J Periodontol. 2009; 80:634–647.

25. Iwasaki M, Minagawa K, Sato M, Kaneko N, Imai S, Yoshihara A, et al. Serum antibody to Porphyromonas gingivalis in metabolic syndrome among an older Japanese population. Gerodontology. Forthcoming 2014.

26. Beck JD, Eke P, Heiss G, Madianos P, Couper D, Lin D, et al. Periodontal disease and coronary heart disease: a reappraisal of the exposure. Circulation. 2005; 112:19–24.

27. Iwasaki M, Taylor GW, Manz MC, Kaneko N, Imai S, Yoshihara A, et al. Serum antibody to Porphyromonas gingivalis in chronic kidney disease. J Dent Res. 2012; 91:828–833.

28. Michaud DS, Izard J, Wilhelm-Benartzi CS, You DH, Grote VA, Tjønneland A, et al. Plasma antibodies to oral bacteria and risk of pancreatic cancer in a large European prospective cohort study. Gut. 2013; 62:1764–1770.