J Periodontal Implant Sci.  2014 Dec;44(6):274-279. 10.5051/jpis.2014.44.6.274.

Association between immunoglobulin G1 against Tannerella forsythia and reduction in the loss of attachment tissue

• Ardila CM
• Olarte-Sossa M
• Guzman IC

• KMID: 1820399
• DOI: http://doi.org/10.5051/jpis.2014.44.6.274

Abstract

PURPOSE
To evaluate whether the levels of immunoglobulin G (IgG) antibody to Tanerella forsythia are associated with periodontal status.
METHODS
Patients with a diagnosis of chronic periodontitis were considered candidates for the study; thus 80 chronic periodontitis patients and 28 healthy persons (control group) were invited to participate in this investigation. The presence of T. forsythia was detected by polymerase chain reaction (PCR) analysis using primers designed to target the respective 16S rRNA gene sequences. Peripheral blood was collected from each subject to identify the IgG1 and IgG2 serum antibodies against T. forsythia. All microbiological and immunological laboratory processes were completed blindly, without awareness of the clinical status of the study patients or of the periodontal sites tested.
RESULTS
The bivariate analysis showed that lower mean levels of clinical attachment level (CAL) and probing depth were found in the presence of the IgG1 antibody titers against whole-cell T. forsythia; however, only the difference in CAL was statistically significant. In the presence of the IgG2 antibody titers against whole-cell T. forsythia, the periodontal parameters evaluated were higher but they did not show statistical differences, except for plaque. The unadjusted linear regression model showed that the IgG1 antibody against whole-cell T. forsythia in periodontitis patients was associated with a lower mean CAL (beta=-0.654; 95% confidence interval [CI], -1.27 to -0.28; P<0.05). This statistically significant association remained after adjusting for possible confounders (beta=-0.655; 95% CI, -1.28 to -0.29; P<0.05). On the other hand, smoking was a statistically significant risk factor in the model (beta=0.704; 95% CI, 0.24 to 1.38; P<0.05).
CONCLUSIONS
Significantly lower mean levels of CAL were shown in the presence of the IgG1 antibody titers against whole-cell T. forsythia in periodontitis patients. Thus, the results of this study suggest that IgG1 antibody to T. forsythia may have been a protective factor from periodontitis in this sample.

Keyword

Chronic periodontitis; Immunoglobulin G; Periodontal disease; Periodontitis

MeSH Terms

Antibodies
Chronic Periodontitis
Diagnosis
Forsythia*
Genes, rRNA
Hand
Humans
Immunoglobulin G
Immunoglobulins*
Linear Models
Periodontal Diseases
Periodontitis
Polymerase Chain Reaction
Risk Factors
Smoke
Smoking
Antibodies
Immunoglobulin G
Immunoglobulins
Smoke

Reference

1. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998; 25:134–144.

2. Amano A, Chen C, Honma K, Li C, Settem RP, Sharma A. Genetic characteristics and pathogenic mechanisms of periodontal pathogens. Adv Dent Res. 2014; 26:15–22.

3. Onishi H, Arakawa S, Nakajima T, Izumi Y. Levels of specific immunoglobulin G to the forsythia detaching factor of Tannerella forsythia in gingival crevicular fluid are related to the periodontal status. J Periodontal Res. 2010; 45:672–680.

4. Onishi H, Ro M, Hayashi J, Tatsumi J, Satomi N, Yatabe K, et al. Modification of forsythia detaching factor by gingival crevicular fluid in periodontitis. Arch Oral Biol. 2013; 58:1007–1013.

5. Yoo JY, Kim HC, Zhu W, Kim SM, Sabet M, Handfield M, et al. Identification of Tannerella forsythia antigens specifically expressed in patients with periodontal disease. FEMS Microbiol Lett. 2007; 275:344–352.

6. Hall LM, Dunford RG, Genco RJ, Sharma A. Levels of serum immunoglobulin G specific to bacterial surface protein A of Tannerella forsythia are related to periodontal status. J Periodontol. 2012; 83:228–234.

7. Kinane DF, Mooney J, Ebersole JL. Humoral immune response to Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in periodontal disease. Periodontol 2000. 1999; 20:289–340.

8. Haffajee AD, Socransky SS, Dzink JL, Taubman MA, Ebersole JL. Clinical, microbiological and immunological features of subjects with refractory periodontal diseases. J Clin Periodontol. 1988; 15:390–398.

9. Persson GR, Schlegel-Bregenzer B, Chung WO, Houston L, Oswald T, Roberts MC. Serum antibody titers to Bacteroides forsythus in elderly subjects with gingivitis or periodontitis. J Clin Periodontol. 2000; 27:839–845.

10. Yoneda M, Hirofuji T, Motooka N, Nozoe K, Shigenaga K, Anan H, et al. Humoral immune responses to S-layer-like proteins of Bacteroides forsythus. Clin Diagn Lab Immunol. 2003; 10:383–387.

11. Vlachojannis C, Dye BA, Herrera-Abreu M, Pikdoken L, Lerche-Sehm J, Pretzl B, et al. Determinants of serum IgG responses to periodontal bacteria in a nationally representative sample of US adults. J Clin Periodontol. 2010; 37:685–696.

12. 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.

13. Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ. Update of the case definitions for population-based surveillance of periodontitis. J Periodontol. 2012; 83:1449–1454.

14. Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol. 1996; 11:266–273.

15. Bishop RF, Cipriani E, Lund JS, Barnes GL, Hosking CS. Estimation of rotavirus immunoglobulin G antibodies in human serum samples by enzyme-linked immunosorbent assay: expression of results as units derived from a standard curve. J Clin Microbiol. 1984; 19:447–452.

16. Walker C, Sedlacek MJ. An in vitro biofilm model of subgingival plaque. Oral Microbiol Immunol. 2007; 22:152–161.

17. Murayama Y, Nagai A, Okamura K, Kurihara H, Nomura Y, Kokeguchi S, et al. Serum immunoglobulin G antibody to periodontal bacteria. Adv Dent Res. 1988; 2:339–345.

18. Aliprantis AO, Yang RB, Mark MR, Suggett S, Devaux B, Radolf JD, et al. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science. 1999; 285:736–739.

19. Raetz CR, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem. 2002; 71:635–700.

20. Lee HR, Jun HK, Choi BK. Tannerella forsythia BspA increases the risk factors for atherosclerosis in ApoE(-/-) mice. Oral Dis. 2014; 20:803–808.

21. Gemmell E, Yamazaki K, Seymour GJ. The role of T cells in periodontal disease: homeostasis and autoimmunity. Periodontol 2000. 2007; 43:14–40.

22. 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.

23. 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.

24. Guglielmetti MR, Rosa EF, Lourencao DS, Inoue G, Gomes EF, De Micheli G, et al. Detection and quantification of periodontal pathogens in smokers and never-smokers with chronic periodontitis by real-time polymerase chain reaction. J Periodontol. 2014; 85:1450–1457.

25. Quinn SM, Zhang JB, Gunsolley JC, Schenkein HA, Tew JG. The influence of smoking and race on adult periodontitis and serum IgG2 levels. J Periodontol. 1998; 69:171–177.

26. Chung HY, Lu HC, Chen WL, Lu CT, Yang YH, Tsai CC. Immunoglobulin G profiles in different forms of periodontitis. J Periodontal Res. 2003; 38:471–476.

27. Chen HA, Johnson BD, Sims TJ, Darveau RP, Moncla BJ, Whitney CW, et al. Humoral immune responses to Porphyromonas gingivalis before and following therapy in rapidly progressive periodontitis patients. J Periodontol. 1991; 62:781–791.

28. Whitney C, Ant J, Moncla B, Johnson B, Page RC, Engel D. Serum immunoglobulin G antibody to Porphyromonas gingivalis in rapidly progressive periodontitis: titer, avidity, and subclass distribution. Infect Immun. 1992; 60:2194–2200.