Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1991 Dec;59(12):4363–4370. doi: 10.1128/iai.59.12.4363-4370.1991

Humoral immunity of older adults with periodontal disease to Porphyromonas gingivalis.

A M De Nardin 1, H T Sojar 1, S G Grossi 1, L A Christersson 1, R J Genco 1
PMCID: PMC259050  PMID: 1682261

Abstract

The effect of age on the humoral response to Porphyromonas gingivalis was assessed in groups of adults (25 to 54 years and 55 to 74 years) with periodontal disease and compared with that in age-matched healthy controls. To determine whether there was an antibody response against P. gingivalis, we measured serum antibodies against whole cells of P. gingivalis 381, A7A1-28, and W50. In addition, antibody levels against purified P. gingivalis outer membrane proteins (i.e., the 43-kDa fimbrial protein and a 75-kDa protein) were also evaluated. Elderly subjects showed the same response to P. gingivalis as younger subjects. Immunoglobulin G (IgG) antibodies to both purified proteins were also elevated in both diseased groups as compared with the normal groups. Total serum IgG, IgA, and IgM levels were also determined by an enzyme-linked immunosorbent assay for all four groups. Total serum IgG levels were elevated in older adults with periodontitis and total IgA levels were elevated in both groups of older adults compared with the younger groups of similar disease status. Total serum IgM levels were comparable for the four groups. Antinuclear antibody titers were assessed in the two groups of older adults and were also found to be higher for the group with periodontitis. These studies show that older adults as well as younger adults have markedly elevated specific antibodies of the IgG and IgA classes to antigens of P. gingivalis, a putative pathogen in both groups. Furthermore, older adults with periodontitis have significantly elevated levels of total serum IgG which may possibly be related to higher levels of autoantibodies.

Full text

PDF
4364

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beck J. D. Epidemiologic changes in older adult periodontal disease. Gerodontology. 1988 Autumn;7(3):103–107. doi: 10.1111/j.1741-2358.1988.tb00313.x. [DOI] [PubMed] [Google Scholar]
  2. Buckley C. E., 3rd, Buckley E. G., Dorsey F. C. Longitudinal changes in serum immunoglobulin levels in older humans. Fed Proc. 1974 Sep;33(9):2036–2039. [PubMed] [Google Scholar]
  3. Chen P. B., Neiders M. E., Millar S. J., Reynolds H. S., Zambon J. J. Effect of immunization on experimental Bacteroides gingivalis infection in a murine model. Infect Immun. 1987 Oct;55(10):2534–2537. doi: 10.1128/iai.55.10.2534-2537.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Delespesse G., Gausset P., Sarfati M., Dubi-Rucquoy M., Debisschop M. J., van Haelst L. Circulating immune complexes in old people and in diabetics: correlation with autoantibodies. Clin Exp Immunol. 1980 Apr;40(1):96–102. [PMC free article] [PubMed] [Google Scholar]
  5. Delfraissy J. F., Galanaud P., Dormont J., Wallon C. Age-related impairment of the in vitro antibody response in the human. Clin Exp Immunol. 1980 Jan;39(1):208–214. [PMC free article] [PubMed] [Google Scholar]
  6. Deslauriers M., ní Eidhin D., Lamonde L., Mouton C. SDS-PAGE analysis of protein and lipopolysaccharide of extracellular vesicules and Sarkosyl-insoluble membranes from Bacteroides gingivalis. Oral Microbiol Immunol. 1990 Feb;5(1):1–7. doi: 10.1111/j.1399-302x.1990.tb00217.x. [DOI] [PubMed] [Google Scholar]
  7. Dzink J. L., Socransky S. S., Haffajee A. D. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol. 1988 May;15(5):316–323. doi: 10.1111/j.1600-051x.1988.tb01590.x. [DOI] [PubMed] [Google Scholar]
  8. Ebersole J. L., Frey D. E., Taubman M. A., Smith D. J. An ELISA for measuring serum antibodies to Actinobacillus actinomycetemcomitans. J Periodontal Res. 1980 Nov;15(6):621–632. doi: 10.1111/j.1600-0765.1980.tb00321.x. [DOI] [PubMed] [Google Scholar]
  9. Ebersole J. L., Taubman M. A., Smith D. J., Frey D. E. Human immune responses to oral microorganisms: patterns of systemic antibody levels to Bacteroides species. Infect Immun. 1986 Feb;51(2):507–513. doi: 10.1128/iai.51.2.507-513.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fujiwara M., Kishimoto S. IgE antibody formation and aging. I. Age-related changes in IgE antibody formation and avidity for the DNP-determinant in mice. J Immunol. 1979 Jul;123(1):263–268. [PubMed] [Google Scholar]
  11. Genco R. J., Zambon J. J., Christersson L. A. The origin of periodontal infections. Adv Dent Res. 1988 Nov;2(2):245–259. doi: 10.1177/08959374880020020901. [DOI] [PubMed] [Google Scholar]
  12. Gerbase-DeLima M., Wilkinson J., Smith G. S., Walford R. L. Age-related decline in thymic-independent immune function in a long-lived mouse strain. J Gerontol. 1974 May;29(3):261–268. doi: 10.1093/geronj/29.3.261. [DOI] [PubMed] [Google Scholar]
  13. Goidl E. A., Innes J. B., Weksler M. E. Immunological studies of aging. II. Loss of IgG and high avidity plaque-forming cells and increased suppressor cell activity in aging mice. J Exp Med. 1976 Oct 1;144(4):1037–1048. doi: 10.1084/jem.144.4.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grundbacher F. J., Shreffler D. C. Changes in human serum immunoglobulin levels with age and sex. Z Immunitatsforsch Allerg Klin Immunol. 1970;141(1):20–26. [PubMed] [Google Scholar]
  15. Hirsch H. Z., Tarkowski A., Miller E. J., Gay S., Koopman W. J., Mestecky J. Autoimmunity to collagen in adult periodontal disease. J Oral Pathol. 1988 Nov;17(9-10):456–459. doi: 10.1111/j.1600-0714.1988.tb01315.x. [DOI] [PubMed] [Google Scholar]
  16. Holt S. C., Ebersole J., Felton J., Brunsvold M., Kornman K. S. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science. 1988 Jan 1;239(4835):55–57. doi: 10.1126/science.3336774. [DOI] [PubMed] [Google Scholar]
  17. Ismail A. I., Eklund S. A., Burt B. A., Calderone J. J. Prevalence of deep periodontal pockets in New Mexico adults aged 27 to 74 years. J Public Health Dent. 1986 Fall;46(4):199–206. doi: 10.1111/j.1752-7325.1986.tb03142.x. [DOI] [PubMed] [Google Scholar]
  18. Kalff M. W. A population study on serum immunoglobulin levels. Clin Chim Acta. 1970 May;28(2):277–289. doi: 10.1016/0009-8981(70)90092-6. [DOI] [PubMed] [Google Scholar]
  19. Kishimoto S., Tomino S., Mitsuya H., Fujiwara H., Tsuda H. Age-related decline in the in vitro and in vivo syntheses of anti-tetanus toxoid antibody in humans. J Immunol. 1980 Nov;125(5):2347–2352. [PubMed] [Google Scholar]
  20. Listgarten M. A. Structure of the microbial flora associated with periodontal health and disease in man. A light and electron microscopic study. J Periodontol. 1976 Jan;47(1):1–18. doi: 10.1902/jop.1976.47.1.1. [DOI] [PubMed] [Google Scholar]
  21. Mackay I. R. Ageing and immunological function in man. Gerontologia. 1972;18(5-6):285–304. doi: 10.1159/000211941. [DOI] [PubMed] [Google Scholar]
  22. Makinodan T., Kay M. M. Age influence on the immune system. Adv Immunol. 1980;29:287–330. doi: 10.1016/s0065-2776(08)60047-4. [DOI] [PubMed] [Google Scholar]
  23. Manoussakis M. N., Tzioufas A. G., Silis M. P., Pange P. J., Goudevenos J., Moutsopoulos H. M. High prevalence of anti-cardiolipin and other autoantibodies in a healthy elderly population. Clin Exp Immunol. 1987 Sep;69(3):557–565. [PMC free article] [PubMed] [Google Scholar]
  24. McKearn J. P., Miller G. W., Quintáns J. The immune response in NZB mice of different ages to thymus-dependent and thymus-independent phosphorylcholine antigens. Immunology. 1978 Jun;34(6):1063–1069. [PMC free article] [PubMed] [Google Scholar]
  25. Mouton C., Hammond P. G., Slots J., Genco R. J. Serum antibodies to oral Bacteroides asaccharolyticus (Bacteroides gingivalis): relationship to age and periondontal disease. Infect Immun. 1981 Jan;31(1):182–192. doi: 10.1128/iai.31.1.182-192.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Naor D., Bonavida B., Walford R. L. Autoimmunity and aging: the age-related response of mice of a long-lived strain to trinitrophenylated syngeneic mouse red blood cells. J Immunol. 1976 Dec;117(6):2204–2208. [PubMed] [Google Scholar]
  27. Ogawa T., Kusumoto Y., Hamada S., McGhee J. R., Kiyono H. Bacteroides gingivalis-specific serum IgG and IgA subclass antibodies in periodontal diseases. Clin Exp Immunol. 1990 Nov;82(2):318–325. doi: 10.1111/j.1365-2249.1990.tb05446.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Plewa M. C. Altered host response and special infections in the elderly. Emerg Med Clin North Am. 1990 May;8(2):193–206. [PubMed] [Google Scholar]
  29. Radl J., Sepers J. M., Skvaril F., Morell A., Hijmans W. Immunoglobulin patterns in humans over 95 years of age. Clin Exp Immunol. 1975 Oct;22(1):84–90. [PMC free article] [PubMed] [Google Scholar]
  30. Rodysill K. J., Hansen L., O'Leary J. J. Cutaneous-delayed hypersensitivity in nursing home and geriatric clinic patients. Implications for the tuberculin test. J Am Geriatr Soc. 1989 May;37(5):435–443. doi: 10.1111/j.1532-5415.1989.tb02640.x. [DOI] [PubMed] [Google Scholar]
  31. Saltzman R. L., Peterson P. K. Immunodeficiency of the elderly. Rev Infect Dis. 1987 Nov-Dec;9(6):1127–1139. doi: 10.1093/clinids/9.6.1127. [DOI] [PubMed] [Google Scholar]
  32. Slots J., Genco R. J. Black-pigmented Bacteroides species, Capnocytophaga species, and Actinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival, and tissue destruction. J Dent Res. 1984 Mar;63(3):412–421. doi: 10.1177/00220345840630031101. [DOI] [PubMed] [Google Scholar]
  33. Slots J. Microflora in the healthy gingival sulcus in man. Scand J Dent Res. 1977 May;85(4):247–254. doi: 10.1111/j.1600-0722.1977.tb00560.x. [DOI] [PubMed] [Google Scholar]
  34. Slots J. The predominant cultivable organisms in juvenile periodontitis. Scand J Dent Res. 1976 Jan;84(1):1–10. doi: 10.1111/j.1600-0722.1976.tb00454.x. [DOI] [PubMed] [Google Scholar]
  35. Sojar H. T., Lee J. Y., Bedi G. S., Cho M. I., Genco R. J. Purification, characterization and immunolocalization of fimbrial protein from Porphyromonas (bacteroides) gingivalis. Biochem Biophys Res Commun. 1991 Mar 15;175(2):713–719. doi: 10.1016/0006-291x(91)91624-l. [DOI] [PubMed] [Google Scholar]
  36. Spiegel C. A., Hayduk S. E., Minah G. E., Krywolap G. N. Black-pigmented Bacteroides from clinically characterized periodontal sites. J Periodontal Res. 1979 Sep;14(5):376–382. doi: 10.1111/j.1600-0765.1979.tb00234.x. [DOI] [PubMed] [Google Scholar]
  37. Szewczuk M. R., Campbell R. J. Loss of immune competence with age may be due to auto-anti-idiotypic antibody regulation. Nature. 1980 Jul 10;286(5769):164–166. doi: 10.1038/286164a0. [DOI] [PubMed] [Google Scholar]
  38. Tanner A. C., Socransky S. S., Goodson J. M. Microbiota of periodontal pockets losing crestal alveolar bone. J Periodontal Res. 1984 May;19(3):279–291. doi: 10.1111/j.1600-0765.1984.tb00819.x. [DOI] [PubMed] [Google Scholar]
  39. Tolo K., Jorkjend L. Serum antibodies and loss of periodontal bone in patients with rheumatoid arthritis. J Clin Periodontol. 1990 May;17(5):288–291. doi: 10.1111/j.1600-051x.1990.tb01091.x. [DOI] [PubMed] [Google Scholar]
  40. Tolo K., Schenck K. Activity of serum immunoglobulins G, A, and M to six anaerobic, oral bacteria in diagnosis of periodontitis. J Periodontal Res. 1985 Mar;20(2):113–121. doi: 10.1111/j.1600-0765.1985.tb00418.x. [DOI] [PubMed] [Google Scholar]
  41. Yoshimura F., Sugano T., Kawanami M., Kato H., Suzuki T. Detection of specific antibodies against fimbriae and membrane proteins from the oral anaerobe Bacteroides gingivalis in patients with periodontal diseases. Microbiol Immunol. 1987;31(9):935–941. doi: 10.1111/j.1348-0421.1987.tb03154.x. [DOI] [PubMed] [Google Scholar]
  42. Yoshimura F., Watanabe K., Takasawa T., Kawanami M., Kato H. Purification and properties of a 75-kilodalton major protein, an immunodominant surface antigen, from the oral anaerobe Bacteroides gingivalis. Infect Immun. 1989 Nov;57(11):3646–3652. doi: 10.1128/iai.57.11.3646-3652.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zambon J. J., Christersson L. A., Slots J. Actinobacillus actinomycetemcomitans in human periodontal disease. Prevalence in patient groups and distribution of biotypes and serotypes within families. J Periodontol. 1983 Dec;54(12):707–711. doi: 10.1902/jop.1983.54.12.707. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES