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. 1996 Jul;64(7):2500–2505. doi: 10.1128/iai.64.7.2500-2505.1996

Influence of smoking and race on immunoglobulin G subclass concentrations in early-onset periodontitis patients.

S M Quinn 1, J B Zhang 1, J C Gunsolley 1, J G Schenkein 1, H A Schenkein 1, J G Tew 1
PMCID: PMC174103  PMID: 8698472

Abstract

Recent data indicate that smoking is an important risk factor for the development of periodontitis. Smoking is also known to reduce serum immunoglobulin G (IgG) levels. Interestingly, patients with the localized form of early-onset periodontitis (LJP) have elevated levels of serum IgG2, and those who smoke are not clinically different from nonsmoking LJ subjects. In contrast, patients with the generalized form of early-onset periodontitis (G-EOP) who smoke have more extensive destruction than their nonsmoking counterparts. Given the effects of smoking on EOP and the association of IgG2 with less severe disease, we hypothesized that smoking might reduce serum IgG2 and that this might be most apparent in G-EOP. We therefore examined the effects of smoking on serum IgG subclass concentrations in race-matched groups: LJP, G-EOP, and age-matched periodontally healthy controls (NPs). Smoking status was established from serum cotinine levels, and serum IgG subclass concentrations were determined by using radial immunodiffusion. The data indicated that the effects of smoking were remarkably selective with respect to both IgG subclass and race. Smoking did not appear to have any effect on the concentration of IgG1 or IgG3 in either black or white subjects. In contrast, smoking was associated with depressed serum IgG2 concentrations in both white NP and G-EOP subgroups. Serum IgG2 levels in black subjects did not appear to be depressed by smoking, with the single striking exception of the black G-EOP subgroup which also had depressed serum IgG4 levels. The results here confirm that smoking has effects on serum immunoglobulin levels, but the effects were both race and serum IgG subclass specific. Furthermore, the periodontal diagnosis of EOP subjects appeared to be important, as indicated by the fact that IgG2 and IgG4 levels were reduced in smoking black G-EOP subjects whereas the IgG2 and IgG4 levels in black LJP and NP subjects were not reduced by smoking.

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Selected References

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  1. Andersen P., Pedersen O. F., Bach B., Bonde G. J. Serum antibodies and immunoglobulins in smokers and nonsmokers. Clin Exp Immunol. 1982 Feb;47(2):467–473. [PMC free article] [PubMed] [Google Scholar]
  2. Bergström J., Eliasson S., Preber H. Cigarette smoking and periodontal bone loss. J Periodontol. 1991 Apr;62(4):242–246. doi: 10.1902/jop.1991.62.4.242. [DOI] [PubMed] [Google Scholar]
  3. Bolin A., Eklund G., Frithiof L., Lavstedt S. The effect of changed smoking habits on marginal alveolar bone loss. A longitudinal study. Swed Dent J. 1993;17(5):211–216. [PubMed] [Google Scholar]
  4. Ebersole J. L., Taubman M. A., Smith D. J., Genco R. J., Frey D. E. Human immune responses to oral micro-organisms. I. Association of localized juvenile periodontitis (LJP) with serum antibody responses to Actinobacillus actinomycetemcomitans. Clin Exp Immunol. 1982 Jan;47(1):43–52. [PMC free article] [PubMed] [Google Scholar]
  5. Ebersole J. L., Taubman M. A., Smith D. J., Socransky S. S. Humoral immune responses and diagnosis of human periodontal disease. J Periodontal Res. 1982 Sep;17(5):478–480. doi: 10.1111/j.1600-0765.1982.tb02032.x. [DOI] [PubMed] [Google Scholar]
  6. Ferson M., Edwards A., Lind A., Milton G. W., Hersey P. Low natural killer-cell activity and immunoglobulin levels associated with smoking in human subjects. Int J Cancer. 1979 May 15;23(5):603–609. doi: 10.1002/ijc.2910230504. [DOI] [PubMed] [Google Scholar]
  7. Genco R. J., Zambon J. J., Murray P. A. Serum and gingival fluid antibodies as adjuncts in the diagnosis of Actinobacillus actinomycetemcomitans-associated periodontal disease. J Periodontol. 1985 Nov;56(11 Suppl):41–50. doi: 10.1902/jop.1985.56.11s.41. [DOI] [PubMed] [Google Scholar]
  8. Gerrard J. W., Heiner D. C., Ko C. G., Mink J., Meyers A., Dosman J. A. Immunoglobulin levels in smokers and non-smokers. Ann Allergy. 1980 May;44(5):261–262. [PubMed] [Google Scholar]
  9. Granoff D. M., Shackelford P. G., Pandey J. P., Boies E. G. Antibody responses to Haemophilus influenzae type b polysaccharide vaccine in relation to Km(1) and G2m(23) immunoglobulin allotypes. J Infect Dis. 1986 Aug;154(2):257–264. doi: 10.1093/infdis/154.2.257. [DOI] [PubMed] [Google Scholar]
  10. Grossi S. G., Genco R. J., Machtei E. E., Ho A. W., Koch G., Dunford R., Zambon J. J., Hausmann E. Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol. 1995 Jan;66(1):23–29. doi: 10.1902/jop.1995.66.1.23. [DOI] [PubMed] [Google Scholar]
  11. Grossi S. G., Zambon J. J., Ho A. W., Koch G., Dunford R. G., Machtei E. E., Norderyd O. M., Genco R. J. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol. 1994 Mar;65(3):260–267. doi: 10.1902/jop.1994.65.3.260. [DOI] [PubMed] [Google Scholar]
  12. Gulsvik A., Fagerhoi M. K. Smoking and immunoglobulin levels. Lancet. 1979 Feb 24;1(8113):449–449. doi: 10.1016/s0140-6736(79)90934-6. [DOI] [PubMed] [Google Scholar]
  13. Gunsolley J. C., Burmeister J. A., Tew J. G., Best A. M., Ranney R. R. Relationship of serum antibody to attachment level patterns in young adults with juvenile periodontitis or generalized severe periodontitis. J Periodontol. 1987 May;58(5):314–320. doi: 10.1902/jop.1987.58.5.314. [DOI] [PubMed] [Google Scholar]
  14. Gunsolley J. C., Tew J. G., Gooss C. M., Burmeister J. A., Schenkein H. A. Effects of race and periodontal status on antibody reactive with Actinobacillus actinomycetemcomitans strain Y4. J Periodontal Res. 1988 Sep;23(5):303–307. doi: 10.1111/j.1600-0765.1988.tb01421.x. [DOI] [PubMed] [Google Scholar]
  15. Haber J., Kent R. L. Cigarette smoking in a periodontal practice. J Periodontol. 1992 Feb;63(2):100–106. doi: 10.1902/jop.1992.63.2.100. [DOI] [PubMed] [Google Scholar]
  16. Haber J., Wattles J., Crowley M., Mandell R., Joshipura K., Kent R. L. Evidence for cigarette smoking as a major risk factor for periodontitis. J Periodontol. 1993 Jan;64(1):16–23. doi: 10.1902/jop.1993.64.1.16. [DOI] [PubMed] [Google Scholar]
  17. Horning G. M., Hatch C. L., Cohen M. E. Risk indicators for periodontitis in a military treatment population. J Periodontol. 1992 Apr;63(4):297–302. doi: 10.1902/jop.1992.63.4.297. [DOI] [PubMed] [Google Scholar]
  18. Ismail A. I., Burt B. A., Eklund S. A. Epidemiologic patterns of smoking and periodontal disease in the United States. J Am Dent Assoc. 1983 May;106(5):617–621. doi: 10.14219/jada.archive.1983.0137. [DOI] [PubMed] [Google Scholar]
  19. Kaniuk A. S., Lortan J. E., Monteil M. A. Specific IgG subclass antibody levels and phagocytosis of serotype 14 pneumococcus following immunization. Scand J Immunol Suppl. 1992;11:96–98. doi: 10.1111/j.1365-3083.1992.tb01628.x. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Leitch A. G., Lumb E. M., Kay A. B. Mediators of hypersensitivity in the sputum of young, symptomatic cigarette smokers. Clin Allergy. 1981 May;11(3):257–262. doi: 10.1111/j.1365-2222.1981.tb01592.x. [DOI] [PubMed] [Google Scholar]
  22. Lortan J. E., Kaniuk A. S., Monteil M. A. Relationship of in vitro phagocytosis of serotype 14 Streptococcus pneumoniae to specific class and IgG subclass antibody levels in healthy adults. Clin Exp Immunol. 1993 Jan;91(1):54–57. doi: 10.1111/j.1365-2249.1993.tb03353.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lu H., Wang M., Gunsolley J. C., Schenkein H. A., Tew J. G. Serum immunoglobulin G subclass concentrations in periodontally healthy and diseased individuals. Infect Immun. 1994 May;62(5):1677–1682. doi: 10.1128/iai.62.5.1677-1682.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. MacFarlane G. D., Herzberg M. C., Wolff L. F., Hardie N. A. Refractory periodontitis associated with abnormal polymorphonuclear leukocyte phagocytosis and cigarette smoking. J Periodontol. 1992 Nov;63(11):908–913. doi: 10.1902/jop.1992.63.11.908. [DOI] [PubMed] [Google Scholar]
  25. Marazita M. L., Burmeister J. A., Gunsolley J. C., Koertge T. E., Lake K., Schenkein H. A. Evidence for autosomal dominant inheritance and race-specific heterogeneity in early-onset periodontitis. J Periodontol. 1994 Jun;65(6):623–630. doi: 10.1902/jop.1994.65.6.623. [DOI] [PubMed] [Google Scholar]
  26. McSharry C., Banham S. W., Boyd G. Effect of cigarette smoking on the antibody response to inhaled antigens and the prevalence of extrinsic allergic alveolitis among pigeon breeders. Clin Allergy. 1985 Sep;15(5):487–494. doi: 10.1111/j.1365-2222.1985.tb02299.x. [DOI] [PubMed] [Google Scholar]
  27. Merrill W. W., Naegel G. P., Olchowski J. J., Reynolds H. Y. Immunoglobulin G subclass proteins in serum and lavage fluid of normal subjects. Quantitation and comparison with immunoglobulins A and E. Am Rev Respir Dis. 1985 Apr;131(4):584–587. doi: 10.1164/arrd.1985.131.4.584. [DOI] [PubMed] [Google Scholar]
  28. O'Keeffe S., Gzel A., Drury R., Cullina M., Greally J., Finnegan P. Immunoglobulin G subclasses and spirometry in patients with chronic obstructive pulmonary disease. Eur Respir J. 1991 Sep;4(8):932–936. [PubMed] [Google Scholar]
  29. Papadea C., Check I. J. Human immunoglobulin G and immunoglobulin G subclasses: biochemical, genetic, and clinical aspects. Crit Rev Clin Lab Sci. 1989;27(1):27–58. doi: 10.3109/10408368909106589. [DOI] [PubMed] [Google Scholar]
  30. Ranney R. R., Yanni N. R., Burmeister J. A., Tew J. G. Relationship between attachment loss and precipitating serum antibody to Actinobacillus actinomycetemcomitans in adolescents and young adults having severe periodontal destruction. J Periodontol. 1982 Jan;53(1):1–7. doi: 10.1902/jop.1982.53.1.1. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Schenck K., Michaelsen T. E. IgG subclass distribution of serum antibodies against lipopolysaccharide from Bacteroides gingivalis in periodontal health and disease. Acta Pathol Microbiol Immunol Scand C. 1987 Apr;95(2):41–46. doi: 10.1111/j.1699-0463.1987.tb00007.x. [DOI] [PubMed] [Google Scholar]
  33. Schenkein H. A., Gunsolley J. C., Koertge T. E., Schenkein J. G., Tew J. G. Smoking and its effects on early-onset periodontitis. J Am Dent Assoc. 1995 Aug;126(8):1107–1113. doi: 10.14219/jada.archive.1995.0327. [DOI] [PubMed] [Google Scholar]
  34. Scott M. G., Briles D. E., Shackelford P. G., Smith D. S., Nahm M. H. Human antibodies to phosphocholine. IgG anti-PC antibodies express restricted numbers of V and C regions. J Immunol. 1987 May 15;138(10):3325–3331. [PubMed] [Google Scholar]
  35. Scott M. G., Shackelford P. G., Briles D. E., Nahm M. H. Human IgG subclasses and their relation to carbohydrate antigen immunocompetence. Diagn Clin Immunol. 1988;5(5):241–248. [PubMed] [Google Scholar]
  36. Spiegelberg H. L. Biological activities of immunoglobulins of different classes and subclasses. Adv Immunol. 1974;19(0):259–294. doi: 10.1016/s0065-2776(08)60254-0. [DOI] [PubMed] [Google Scholar]
  37. Whitney C., Ant J., Moncla B., Johnson B., Page R. C., Engel D. Serum immunoglobulin G antibody to Porphyromonas gingivalis in rapidly progressive periodontitis: titer, avidity, and subclass distribution. Infect Immun. 1992 Jun;60(6):2194–2200. doi: 10.1128/iai.60.6.2194-2200.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wilson M. E., Hamilton R. G. Immunoglobulin G subclass response of juvenile periodontitis subjects to principal outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect Immun. 1995 Mar;63(3):1062–1069. doi: 10.1128/iai.63.3.1062-1069.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wilson M. E., Hamilton R. G. Immunoglobulin G subclass response of localized juvenile periodontitis patients to Actinobacillus actinomycetemcomitans Y4 lipopolysaccharide. Infect Immun. 1992 May;60(5):1806–1812. doi: 10.1128/iai.60.5.1806-1812.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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