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. 1995 Nov;102(2):406–416. doi: 10.1111/j.1365-2249.1995.tb03798.x

A possible role for lysozyme in determining acute exacerbation in chronic bronchitis.

D C Taylor 1, A W Cripps 1, R L Clancy 1
PMCID: PMC1553411  PMID: 7586699

Abstract

The aggregation of non-serotypable Haemophilus influenzae (NTHI) by whole saliva from patients with chronic obstructive lung disease (COLD) was investigated. Significant differences were observed between salivary aggregating activity of a control and COLD population (P < 0.001). Saliva from patients less prone to acute exacerbations had a greater capacity to aggregate bacteria compared with saliva from patients with a predilection to infection. The mechanism of saliva-mediated aggregation of NTHI was investigated and shown to be related to lysozyme content. Lysozyme activity in saliva was measured by the turbidimetric technique and results showed that patients with chronic bronchitis had increased levels of salivary lysozyme, with a subpopulation within the non-infection-prone group having greater amounts. A significant difference was observed in salivary lysozyme between controls and non-infection-prone (P < 0.005) and infection-prone (P < 0.05) patients, respectively: the non-infection-prone patients having significantly (P < 0.005) more than the infection-prone patients. There was significant correlation (r = 0.742, P < 0.001) between salivary aggregation of NTHI and lysozyme activity. Chromatographically purified human lysozyme had a similar aggregation profile to that of saliva. There was no difference in serum and saliva lactoferrin concentrations between groups, but there was a significant increase (P < 0.05) in serum lysozyme concentration in the non-infection-prone group. This study suggests that the level of salivary lysozyme derived from macrophages may play an important role in determining resistance or susceptibility to acute bronchitis.

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Selected References

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  1. Bainton D. F. Sequential degranulation of the two types of polymorphonuclear leukocyte granules during phagocytosis of microorganisms. J Cell Biol. 1973 Aug;58(2):249–264. doi: 10.1083/jcb.58.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennett R. M., Kokocinski T. Lactoferrin turnover in man. Clin Sci (Lond) 1979 Nov;57(5):453–460. doi: 10.1042/cs0570453. [DOI] [PubMed] [Google Scholar]
  3. Burns M. W. The pattern of bacterial infection in bronchial diseases in Australia: a serological and bacteriological survey. Med J Aust. 1972 Sep 23;2(13):697–701. doi: 10.5694/j.1326-5377.1972.tb103502.x. [DOI] [PubMed] [Google Scholar]
  4. Butt H. L., Clancy R. L., Cripps A. W., Murree-Allen K., Saunders N. A., Sutherland D. C., Hensley M. J. Bacterial colonisation of the respiratory tract in chronic bronchitis. Aust N Z J Med. 1990 Feb;20(1):35–38. doi: 10.1111/j.1445-5994.1990.tb00367.x. [DOI] [PubMed] [Google Scholar]
  5. Clancy R. L., Cripps A. W., Gebski V. Protection against recurrent acute bronchitis after oral immunization with killed Haemophilus influenzae. Med J Aust. 1990 Apr 16;152(8):413–416. doi: 10.5694/j.1326-5377.1990.tb125268.x. [DOI] [PubMed] [Google Scholar]
  6. Cole M. F., Hsu S. D., Baum B. J., Bowen W. H., Sierra L. I., Aquirre M., Gillespie G. Specific and nonspecific immune factors in dental plaque fluid and saliva from young and old populations. Infect Immun. 1981 Mar;31(3):998–1002. doi: 10.1128/iai.31.3.998-1002.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ericson T., Rundegren J. Characterization of a salivary agglutinin reacting with a serotype c strain of Streptococcus mutans. Eur J Biochem. 1983 Jun 15;133(2):255–261. doi: 10.1111/j.1432-1033.1983.tb07456.x. [DOI] [PubMed] [Google Scholar]
  8. FRANCIS R. S., MAY J. R., SPICER C. C. Chemotherapy of bronchitis. Influence of penicillin and tetracycline administered daily, or intermittently for exacerbations. A report to the Research Committee of the British Tuberculosis Association by its Bronchitis Subcommittee. Br Med J. 1961 Oct 14;2(5258):979–985. doi: 10.1136/bmj.2.5258.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fainstein V., Musher D. M. Bacterial adherence to pharyngeal cells in smokers, nonsmokers, and chronic bronchitics. Infect Immun. 1979 Oct;26(1):178–182. doi: 10.1128/iai.26.1.178-182.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Falchuk K. R., Perrotto J. L., Isselbacher K. J. Serum lysozyme in Crohn's disease. A useful index of disease activity. Gastroenterology. 1975 Oct;69(4):893–896. [PubMed] [Google Scholar]
  11. Fan S., Fehr H. G., Adams D. Activation of macrophages for ADCC in vitro: effects of IL-4, TNF, interferons-alpha/beta, interferon-gamma, and GM-CSF. Cell Immunol. 1991 Jun;135(1):78–87. doi: 10.1016/0008-8749(91)90255-a. [DOI] [PubMed] [Google Scholar]
  12. Fisher M., Akhtar A. J., Calder M. A., Moffat M. A., Stewart S. M., Zealley H., Crofton J. W. Pilot study of factors associated with exacerbations in chronic bronchitis. Br Med J. 1969 Oct 25;4(5677):187–192. doi: 10.1136/bmj.4.5677.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gaweł J., Rudnik J., Pryjma J., Zebrak J., Hałuszka J., Rudnik I., Majewska-Zalewska H. Proteins in bronchial secretion of children with chronic pulmonary diseases. I. Relation to clinical diagnosis. Scand J Respir Dis. 1979 Apr;60(2):63–68. [PubMed] [Google Scholar]
  14. Germaine G. R., Tellefson L. M. Potential role of lysozyme in bactericidal activity of in vitro-acquired salivary pellicle against Streptococcus faecium 9790. Infect Immun. 1986 Dec;54(3):846–854. doi: 10.1128/iai.54.3.846-854.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gibbons R. J., de Stoppelaar J. D., Harden L. Lysozyme insensitivity of bacteria indigenous to the oral cavity of man. J Dent Res. 1966 May-Jun;45(3):877–881. doi: 10.1177/00220345660450036201. [DOI] [PubMed] [Google Scholar]
  16. Golub E. E., Thaler M., Davis C., Malamud D. Bacterial aggregating activity in human saliva: simultaneous determination of free and bound cells. Infect Immun. 1979 Dec;26(3):1028–1034. doi: 10.1128/iai.26.3.1028-1034.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gordon L. I., Douglas S. D., Kay N. E., Yamada O., Osserman E. F., Jacob H. S. Modulation of neutrophil function by lysozyme. Potential negative feedback system of inflammation. J Clin Invest. 1979 Jul;64(1):226–232. doi: 10.1172/JCI109443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haneberg B., Glette J., Talstad I., Sørnes S., Solberg C. O. In vitro release of lysozyme from monocytes and granulocytes. J Leukoc Biol. 1984 Jun;35(6):573–582. doi: 10.1002/jlb.35.6.573. [DOI] [PubMed] [Google Scholar]
  19. Harbitz O., Jenssen A. O., Smidsrød O. Lysozyme and lactoferrin in sputum from patients with chronic obstructive lung disease. Eur J Respir Dis. 1984 Oct;65(7):512–520. [PubMed] [Google Scholar]
  20. Hinman L. M., Stevens C. A., Matthay R. A., Gee J. B. Elastase and lysozyme activities in human alveolar macrophages. Effects of cigarette smoking. Am Rev Respir Dis. 1980 Feb;121(2):263–271. doi: 10.1164/arrd.1980.121.2.263. [DOI] [PubMed] [Google Scholar]
  21. Hogg S. D., Embery G. The isolation and partial characterization of a sulphated glycoprotein from human whole saliva which aggregates strains of Streptococcus sanguis but not Streptococcus mutans. Arch Oral Biol. 1979;24(10-11):791–797. doi: 10.1016/0003-9969(79)90040-2. [DOI] [PubMed] [Google Scholar]
  22. Husband A. J., Dunkley M. L., Scicchitano R., Sheldrake R. F. Induction and delivery of mucosal immune responses. J Dent Res. 1984 Mar;63(3):465–469. doi: 10.1177/00220345840630032001. [DOI] [PubMed] [Google Scholar]
  23. Iacono V. J., MacKay B. J., DiRienzo S., Pollock J. J. Selective antibacterial properties of lysozyme for oral microorganisms. Infect Immun. 1980 Aug;29(2):623–632. doi: 10.1128/iai.29.2.623-632.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jenssen A. O., Smidsrød O. Preparation of enzymically active lysozyme from sputum and its distribution between the sol and gel phases. Eur J Respir Dis. 1982 Nov;63(6):584–590. [PubMed] [Google Scholar]
  25. Johanson W. G., Jr, Higuchi J. H., Chaudhuri T. R., Woods D. E. Bacterial adherence to epithelial cells in bacillary colonization of the respiratory tract. Am Rev Respir Dis. 1980 Jan;121(1):55–63. doi: 10.1164/arrd.1980.121.1.55. [DOI] [PubMed] [Google Scholar]
  26. Kashket S., Donaldson C. G. Saliva-induced aggregation of oral streptococci. J Bacteriol. 1972 Dec;112(3):1127–1133. doi: 10.1128/jb.112.3.1127-1133.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kokoshis P. L., Di Luzio N. R. Serum lysozyme: an index of macrophage function. J Reticuloendothel Soc. 1979 Jan;25(1):85–99. [PubMed] [Google Scholar]
  28. Komiyama K., Habbick B. F., Tumber S. K. Whole, submandibular, and parotid saliva-mediated aggregation of Pseudomonas aeruginosa in cystic fibrosis. Infect Immun. 1989 Apr;57(4):1299–1304. doi: 10.1128/iai.57.4.1299-1304.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Laible N. J., Germaine G. R. Adsorption of lysozyme from human whole saliva by Streptococcus sanguis 903 and other oral microorganisms. Infect Immun. 1982 Apr;36(1):148–159. doi: 10.1128/iai.36.1.148-159.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lawrence G., Walker P. D. Pathogenesis of enteritis necroticans in Papula New Guinea. Lancet. 1976 Jan 17;1(7951):125–126. doi: 10.1016/s0140-6736(76)93160-3. [DOI] [PubMed] [Google Scholar]
  31. Lehmann D., Coakley K. J., Coakley C. A., Spooner V., Montgomery J. M., Michael A., Riley I. D., Smith T., Clancy R. L., Cripps A. W. Reduction in the incidence of acute bronchitis by an oral Haemophilus influenzae vaccine in patients with chronic bronchitis in the highlands of Papua New Guinea. Am Rev Respir Dis. 1991 Aug;144(2):324–330. doi: 10.1164/ajrccm/144.2.324. [DOI] [PubMed] [Google Scholar]
  32. Levine M. J., Herzberg M. C., Levine M. S., Ellison S. A., Stinson M. W., Li H. C., van Dyke T. Specificity of salivary-bacterial interactions: role of terminal sialic acid residues in the interaction of salivary glycoproteins with Streptococcus sanguis and Streptococcus mutans. Infect Immun. 1978 Jan;19(1):107–115. doi: 10.1128/iai.19.1.107-115.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Liljemark W. F., Bloomquist C. G., Ofstehage J. C. Aggregation and adherence of Streptococcus sanguis: role of human salivary immunoglobulin A. Infect Immun. 1979 Dec;26(3):1104–1110. doi: 10.1128/iai.26.3.1104-1110.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. MAY J. R. The bacteriology of chronic bronchitis. Lancet. 1953 Sep 12;265(6785):534–537. doi: 10.1016/s0140-6736(53)90274-8. [DOI] [PubMed] [Google Scholar]
  35. Malamud D., Appelbaum B., Kline R., Golub E. E. Bacterial aggregating activity in human saliva: comparisons of bacterial species and strains. Infect Immun. 1981 Mar;31(3):1003–1006. doi: 10.1128/iai.31.3.1003-1006.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mason D. Y., Taylor C. R. The distribution of muramidase (lysozyme) in human tissues. J Clin Pathol. 1975 Feb;28(2):124–132. doi: 10.1136/jcp.28.2.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Masson P. L., Heremans J. F., Schonne E. Lactoferrin, an iron-binding protein in neutrophilic leukocytes. J Exp Med. 1969 Sep 1;130(3):643–658. doi: 10.1084/jem.130.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. McBride B. C., Gisslow M. T. Role of sialic acid in saliva-induced aggregation of Streptococcus sanguis. Infect Immun. 1977 Oct;18(1):35–40. doi: 10.1128/iai.18.1.35-40.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Murphy T. F., Dudas K. C., Mylotte J. M., Apicella M. A. A subtyping system for nontypable Haemophilus influenzae based on outer-membrane proteins. J Infect Dis. 1983 May;147(5):838–846. doi: 10.1093/infdis/147.5.838. [DOI] [PubMed] [Google Scholar]
  40. Pascual R. S., Gee J. B., Finch S. C. Usefulness of serum lysozyme measurement in diagnosis and evaluation of sarcoidosis. N Engl J Med. 1973 Nov 15;289(20):1074–1076. doi: 10.1056/NEJM197311152892007. [DOI] [PubMed] [Google Scholar]
  41. Perillie P. E., Khan K., Finch S. C. Serum lysozyme in pulmonary tuberculosis. Am J Med Sci. 1973 Apr;265(4):297–302. doi: 10.1097/00000441-197304000-00005. [DOI] [PubMed] [Google Scholar]
  42. Pines A., Raafat H., Greenfield J. S., Linsell W. D., Solari M. E. Antibiotic regimens in moderately ill patients with purulent exacerbations of chronic bronchitis. Br J Dis Chest. 1972 Apr;66(2):107–115. [PubMed] [Google Scholar]
  43. Rosan B., Appelbaum B., Golub E., Malamud D., Mandel I. D. Enhanced saliva-mediated bacterial aggregation and decreased bacterial adhesion in caries-resistant versus caries-susceptible individuals. Infect Immun. 1982 Dec;38(3):1056–1059. doi: 10.1128/iai.38.3.1056-1059.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Rundegren J., Ericson T. An evaluation of the specificity of salivary agglutinins. J Oral Pathol. 1981 Aug;10(4):261–268. doi: 10.1111/j.1600-0714.1981.tb01272.x. [DOI] [PubMed] [Google Scholar]
  45. Rundegren J., Ericson T. An evaluation of the specificity of salivary agglutinins. J Oral Pathol. 1981 Aug;10(4):261–268. doi: 10.1111/j.1600-0714.1981.tb01272.x. [DOI] [PubMed] [Google Scholar]
  46. Tandon M. K., Gebski V. A controlled trial of a killed Haemophilus influenzae vaccine for prevention of acute exacerbations of chronic bronchitis. Aust N Z J Med. 1991 Aug;21(4):427–432. doi: 10.1111/j.1445-5994.1991.tb01346.x. [DOI] [PubMed] [Google Scholar]
  47. Taylor D. C., Clancy R. L., Cripps A. W., Butt H., Bartlett L., Murree-Allen K. An alteration in the host-parasite relationship in subjects with chronic bronchitis prone to recurrent episodes of acute bronchitis. Immunol Cell Biol. 1994 Apr;72(2):143–151. doi: 10.1038/icb.1994.22. [DOI] [PubMed] [Google Scholar]
  48. Taylor D. C., Cripps A. W., Clancy R. L. Measurement of lysozyme by an enzyme-linked immunosorbent assay. J Immunol Methods. 1992 Jan 21;146(1):55–61. doi: 10.1016/0022-1759(92)90048-x. [DOI] [PubMed] [Google Scholar]
  49. Tellefson L. M., Germaine G. R. Adherence of Streptococcus sanguis to hydroxyapatite coated with lysozyme and lysozyme-supplemented saliva. Infect Immun. 1986 Mar;51(3):750–759. doi: 10.1128/iai.51.3.750-759.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Thacore H., Willett H. P. The formation of spheroplasts of Mycobacterium tuberculosis in tissue culture cells. Am Rev Respir Dis. 1966 May;93(5):786–796. doi: 10.1164/arrd.1966.93.5.786. [DOI] [PubMed] [Google Scholar]
  51. Thompson A. B., Bohling T., Payvandi F., Rennard S. I. Lower respiratory tract lactoferrin and lysozyme arise primarily in the airways and are elevated in association with chronic bronchitis. J Lab Clin Med. 1990 Feb;115(2):148–158. [PubMed] [Google Scholar]
  52. Venge P. A critical look at blood samples in CB and COAD. Agents Actions Suppl. 1990;30:109–119. doi: 10.1007/978-3-0348-7488-5_8. [DOI] [PubMed] [Google Scholar]
  53. Wallace F. J., Clancy R. L., Cripps A. W. An animal model demonstration of enhanced clearance of nontypable Haemophilus influenzae from the respiratory tract after antigen stimulation of gut-associated lymphoid tissue. Am Rev Respir Dis. 1989 Aug;140(2):311–316. doi: 10.1164/ajrccm/140.2.311. [DOI] [PubMed] [Google Scholar]
  54. Williams R. C., Gibbons R. J. Inhibition of streptococcal attachment to receptors on human buccal epithelial cells by antigenically similar salivary glycoproteins. Infect Immun. 1975 Apr;11(4):711–718. doi: 10.1128/iai.11.4.711-718.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Woods D. E., Bass J. A., Johanson W. G., Jr, Straus D. C. Role of adherence in the pathogenesis of Pseudomonas aeruginosa lung infection in cystic fibrosis patients. Infect Immun. 1980 Dec;30(3):694–699. doi: 10.1128/iai.30.3.694-699.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Yeung S., Pang G., Cripps A. W., Clancy R. L. Development of an immunoglobulin A-specific anti-Haemophilus influenzae antibody assay for detection of antibody in human mucosal secretions. J Clin Microbiol. 1987 Apr;25(4):667–671. doi: 10.1128/jcm.25.4.667-671.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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