Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1984 Jul;45(1):172–179. doi: 10.1128/iai.45.1.172-179.1984

Effects of an immunomodulating agent on peripheral blood lymphocytes and subgingival microflora in ligature-induced periodontitis.

F Manti, K Kornman, I Goldschneider
PMCID: PMC263296  PMID: 6234232

Abstract

The peripheral blood lymphocyte populations and the subgingival levels of black-pigmented Bacteroides species were monitored during the conversion of chronic gingivitis to progressing periodontitis in cynomolgus monkeys. In addition, the effects of an immunomodulating agent, the pentapeptide of thymopoietin (TP5), were determined. After the induction of active periodontitis, proportions of helper T-cells (OKT-4 positive) decreased from 31.5 to 26.4%, and proportions of B-cells (surface immunoglobulin positive) increased from 44.5 to 51.8%. Proportions of suppressor T-cells (OKT-8 positive) remained unchanged, but the numbers of OKT-8-positive cells increased. During this same time period the total cultivable subgingival flora increased from 1.5 X 10(6) to 3.5 X 10(6) per sample, with Bacteroides gingivalis increasing from 5.3 to 16.6% of the total cultivable subgingival flora. After 10 weeks of active periodontitis, animals were treated with either TP5 or placebo. Treatment with TP5 produced an increase in helper T-cells but had no effect on B-cells. The OKT-4/OKT-8 cell ratio, which decreased from 1.3 to 0.8 with disease induction, was increased to 1.1 after TP5 treatment but remained at 0.9 in placebo-treated animals. TP5 had no effect on the total cultivable subgingival flora but significantly decreased the subgingival proportions of B. gingivalis and other black-pigmented Bacteroides species. In this model system, active periodontitis was associated with an increase in B. gingivalis, a decreased helper/suppressor T-cell ratio, and increased levels of B-cells. Treatment with TP5 increased the helper/suppressor T-cell ratio and decreased B. gingivalis levels, suggesting that lymphocyte subsets have the potential to influence subgingival levels of potential periodontal pathogens.

Full text

PDF
172

Selected References

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

  1. Aiuti F., Businco L., Fiorilli M., Galli E., Quinti I., Rossi P., Seminara R., Goldstein G. Thymopoietin pentapeptide treatment of primary immunodeficiencies. Lancet. 1983 Mar 12;1(8324):551–554. doi: 10.1016/s0140-6736(83)92810-6. [DOI] [PubMed] [Google Scholar]
  2. Basch R. S., Goldstein G. Antigenic and functional evidence for the in vitro inductive activity of thymopoietin (thymin) on thymocyte precursors. Ann N Y Acad Sci. 1975 Feb 28;249:290–299. doi: 10.1111/j.1749-6632.1975.tb29076.x. [DOI] [PubMed] [Google Scholar]
  3. Burckhardt J. J., Guggenheim B., Hefti A. Are Actinomyces viscosus antigens B cell mitogens? J Immunol. 1977 Apr;118(4):1460–1465. [PubMed] [Google Scholar]
  4. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  5. Carney W. P., Rubin R. H., Hoffman R. A., Hansen W. P., Healey K., Hirsch M. S. Analysis of T lymphocyte subsets in cytomegalovirus mononucleosis. J Immunol. 1981 Jun;126(6):2114–2116. [PubMed] [Google Scholar]
  6. Engel D., Clagett J., Page R., Williams B. Mitogenic activity of Actinomyces viscosus. I. Effects on murine B and T lymphocytes, and partial characterization. J Immunol. 1977 Apr;118(4):1466–1471. [PubMed] [Google Scholar]
  7. Fiorilli M., Sirianni M. C., Pandolfi F., Quinti I., Tosti U., Aiuti F., Goldstein G. Improvement of natural killer activity and of T cells after thymopoietin pentapeptide therapy in a patient with severe combined immunodeficiency. Clin Exp Immunol. 1981 Aug;45(2):344–351. [PMC free article] [PubMed] [Google Scholar]
  8. Goldstein G., Scheid M. P., Boyse E. A., Schlesinger D. H., Van Wauwe J. A synthetic pentapeptide with biological activity characteristic of the thymic hormone thymopoietin. Science. 1979 Jun 22;204(4399):1309–1310. doi: 10.1126/science.451537. [DOI] [PubMed] [Google Scholar]
  9. Kagan W. A., O'Neill G. J., Incefy G. S., Goldstein G., Good R. A. Induction of human granulocyte differentiation in vitro by ubiquitin and thymopoietin. Blood. 1977 Aug;50(2):275–288. [PubMed] [Google Scholar]
  10. Komuro K., Boyse E. A. In-vitro demonstration of thymic hormone in the mouse by conversion of precursor cells into lymphocytes. Lancet. 1973 Apr 7;1(7806):740–743. doi: 10.1016/s0140-6736(73)92127-2. [DOI] [PubMed] [Google Scholar]
  11. Kornman K. S., Holt S. C., Robertson P. B. The microbiology of ligature-induced periodontitis in the cynomolgus monkey. J Periodontal Res. 1981 Jul;16(4):363–371. doi: 10.1111/j.1600-0765.1981.tb00987.x. [DOI] [PubMed] [Google Scholar]
  12. LOE H., SILNESS J. PERIODONTAL DISEASE IN PREGNANCY. I. PREVALENCE AND SEVERITY. Acta Odontol Scand. 1963 Dec;21:533–551. doi: 10.3109/00016356309011240. [DOI] [PubMed] [Google Scholar]
  13. Lang N. P., Smith F. N. Lymphocyte response to T-cell mitogen during experimental gingivitis in humans. Infect Immun. 1976 Jan;13(1):108–113. doi: 10.1128/iai.13.1.108-113.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lehner T., Wilton J. M., Challacombe S. J., Ivanyi L. Sequential cell-mediated immune responses in experimental gingivitis in man. Clin Exp Immunol. 1974 Mar;16(3):481–492. [PMC free article] [PubMed] [Google Scholar]
  15. Letvin N. L., Eaton K. A., Aldrich W. R., Sehgal P. K., Blake B. J., Schlossman S. F., King N. W., Hunt R. D. Acquired immunodeficiency syndrome in a colony of macaque monkeys. Proc Natl Acad Sci U S A. 1983 May;80(9):2718–2722. doi: 10.1073/pnas.80.9.2718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lindhe J., Ericsson I. Effect of ligature placement and dental plaque on periodontal tissue breakdown in the dog. J Periodontol. 1978 Jul;49(7):343–350. doi: 10.1902/jop.1978.49.7.343. [DOI] [PubMed] [Google Scholar]
  17. Loesche W. J., Hockett R. N., Syed S. A. The predominant cultivable flora of tooth surface plaque removed from institutionalized subjects. Arch Oral Biol. 1972 Sep;17(9):1311–1325. doi: 10.1016/0003-9969(72)90164-1. [DOI] [PubMed] [Google Scholar]
  18. Lurie A. G., Greenberg R. J., Kornman K. S. Subtraction radiology demonstrates crestal bone loss in experimentally induced marginal periodontitis. Oral Surg Oral Med Oral Pathol. 1983 May;55(5):537–541. doi: 10.1016/0030-4220(83)90243-8. [DOI] [PubMed] [Google Scholar]
  19. Mackler B. F., Frostad K. B., Robertson P. B., Levy B. M. Immunoglobulin bearing lymphocytes and plasma cells in human periodontal disease. J Periodontal Res. 1977 Jan;12(1):37–45. doi: 10.1111/j.1600-0765.1977.tb00107.x. [DOI] [PubMed] [Google Scholar]
  20. Mangan D. F., Lopatin D. E. In vitro stimulation of immunoglobulin production from human peripheral blood lymphocytes by a soluble preparation of Actinomyces viscosus. Infect Immun. 1981 Jan;31(1):236–244. doi: 10.1128/iai.31.1.236-244.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mangan D. F., Lopatin D. E. Polyclonal activation of human peripheral blood B lymphocytes by Fusobacterium nucleatum. Infect Immun. 1983 Jun;40(3):1104–1111. doi: 10.1128/iai.40.3.1104-1111.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nash L., Good R. A., Hatzfeld A., Goldstein G., Incefy G. S. In vitro differentiation of two surface markers for immature T cells by the synthetic pentapeptide, thymopoietin. J Immunol. 1981 Jan;126(1):150–153. [PubMed] [Google Scholar]
  23. Onderdonk A. B., Markham R. B., Zaleznik D. F., Cisneros R. L., Kasper D. L. Evidence for T cell-dependent immunity to Bacteroides fragilis in an intraabdominal abscess model. J Clin Invest. 1982 Jan;69(1):9–16. doi: 10.1172/JCI110445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Page R. C., Schroeder H. E. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest. 1976 Mar;34(3):235–249. [PubMed] [Google Scholar]
  25. Patters M. R., Sedransk N., Genco R. J. Lymphoproliferative response during resolution and recurrence of naturally occurring gingivitis. J Periodontol. 1977 Jul;48(7):373–380. doi: 10.1902/jop.1977.48.7.373. [DOI] [PubMed] [Google Scholar]
  26. Patters M. R., Sedransk N., Genco R. J. The lymphoproliferative response during human experimental gingivitis. J Periodontal Res. 1979 Jul;14(4):269–278. doi: 10.1111/j.1600-0765.1979.tb00791.x. [DOI] [PubMed] [Google Scholar]
  27. Reinherz E. L., Kung P. C., Goldstein G., Schlossman S. F. A monoclonal antibody reactive with the human cytotoxic/suppressor T cell subset previously defined by a heteroantiserum termed TH2. J Immunol. 1980 Mar;124(3):1301–1307. [PubMed] [Google Scholar]
  28. SILNESS J., LOE H. PERIODONTAL DISEASE IN PREGNANCY. II. CORRELATION BETWEEN ORAL HYGIENE AND PERIODONTAL CONDTION. Acta Odontol Scand. 1964 Feb;22:121–135. doi: 10.3109/00016356408993968. [DOI] [PubMed] [Google Scholar]
  29. Seymour G. J., Greaves M. F. Identification of cells expressing T and p28,33 (Ia-like) antigens in sections of human chronic inflammatory periodontal disease. J Periodontal Res. 1980 Jul;15(4):453–461. doi: 10.1111/j.1600-0765.1980.tb00303.x. [DOI] [PubMed] [Google Scholar]
  30. Seymour G. J., Greenspan J. S. The phenotypic characterization of lymphocyte subpopulations in established human periodontal disease. J Periodontal Res. 1979 Jan;14(1):39–46. doi: 10.1111/j.1600-0765.1979.tb00216.x. [DOI] [PubMed] [Google Scholar]
  31. Shapiro M. E., Onderdonk A. B., Kasper D. L., Finberg R. W. Cellular immunity to Bacteroides fragilis capsular polysaccharide. J Exp Med. 1982 Apr 1;155(4):1188–1197. doi: 10.1084/jem.155.4.1188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Siegrist B., Kornman K. S. The effect of supragingival plaque control on the composition of the subgingival microbial flora in ligature-induced periodontitis in the monkey. J Dent Res. 1982 Jul;61(7):936–941. doi: 10.1177/00220345820610071001. [DOI] [PubMed] [Google Scholar]
  33. Silverman A. Y., Darnell B. J., Montiel M. M., Smith C. G., Asch R. H. Response of rhesus monkey lymphocytes to short-term administration of THC. Life Sci. 1982 Jan 4;30(1):107–115. doi: 10.1016/0024-3205(82)90642-7. [DOI] [PubMed] [Google Scholar]
  34. Slots J., Hausmann E. Longitudinal study of experimentally induced periodontal disease in Macaca arctoides: relationship between microflora and alveolar bone loss. Infect Immun. 1979 Feb;23(2):260–269. doi: 10.1128/iai.23.2.260-269.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith S., Bick P. H., Miller G. A., Ranney R. R., Rice P. L., Lalor J. H., Tew J. G. Polyclonal B-cell activation: severe periodontal disease in young adults. Clin Immunol Immunopathol. 1980 Jul;16(3):354–366. doi: 10.1016/0090-1229(80)90141-5. [DOI] [PubMed] [Google Scholar]
  36. Syed S. A., Svanberg M., Svanberg G. The predominant cultivable dental plaque flora of beagle dogs with gingivitis. J Periodontal Res. 1980 Mar;15(2):123–136. doi: 10.1111/j.1600-0765.1980.tb00266.x. [DOI] [PubMed] [Google Scholar]
  37. Wallace J. I., Coral F. S., Rimm I. R., Lane H., Levine H., Reinherz E. L., Schlossman S. F., Sonnabend J. T-cell ratios in homosexuals. Lancet. 1982 Apr 17;1(8277):908–908. doi: 10.1016/s0140-6736(82)92177-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES