Infect Chemother.  2010 Dec;42(6):391-396. 10.3947/ic.2010.42.6.391.

Effect of Smoking on Influenza Illness and Vaccine-induced Immune Response in Mice

Affiliations
  • 1Department of Internal Medicine, Inha University College of Medicine, Incheon, Korea.
  • 2Department of Internal Medicine, Konkuk University College of Medicine, Chungju, Korea.
  • 3Department of Internal Medicine, Korea University College of Medicine, Seoul, Korea. heejinmd@medimail.co.kr
  • 4Department of Occupational and Environmental Medicine, Inha University College of Medicine, Incheon, Korea.
  • 5Department of Pathology, Inha University College of Medicine, Incheon, Korea.

Abstract

BACKGROUND
Since cigarette smoking is an important risk factor for respiratory infections and alters the immune response, the severity of influenza illness and the immunogenicity of influenza vaccination may differ between cigarette smokers and non-smokers. This study investigated the effect of cigarette smoke exposure on the severity of influenza illness and vaccine-induced antibody production in mice.
MATERIALS AND METHODS
Cigarette smoke exposed (CE) and non-cigarette smoke exposed (NCE) mice were infected with mouse-adapted influenza A/PR8/8/34 (H1N1). Influenza virus was quantified in bronchoalveolar lavage fluid by real-time polymerase chain reaction and the lung pathology was examined to investigate the influence of smoke exposure on the severity of illness. To assess immunogenicity, hemagglutination inhibition antibodies were measured in pre- and post-influenza vaccination blood samples from CE and NCE mice.
RESULTS
Influenza viral proliferation was higher and inflammatory changes such as macrophage infiltration in the alveolar space and necrotizing bronchitis were more pronounced in CE mice, compared with controls. Vaccine-induced immunogenicity was achieved in both CE and NCE mice.
CONCLUSIONS
Cigarette smoke exposure enhanced influenza viral replication and the inflammatory changes associated with influenza illness, but had no significant effect on vaccine-induced immunogenicity.

Keyword

Immunogenicity; Inflammation; Influenza; Vaccine; Smoking

MeSH Terms

Animals
Antibodies
Antibody Formation
Bronchitis
Bronchoalveolar Lavage Fluid
Hemagglutination
Inflammation
Influenza, Human
Lung
Macrophages
Mice
Orthomyxoviridae
Real-Time Polymerase Chain Reaction
Respiratory Tract Infections
Risk Factors
Smoke
Smoking
Tobacco Products
Vaccination
Antibodies
Smoke

Figure

  • Figure 1 Treatment allocation.

  • Figure 2 Mean body weight before and after influenza virus challenge in cigarette smoke exposed and non-cigarette smoke exposed mice.

  • Figure 3 A representative lung histology following influenza virus infection after cigarette smoke exposure. (A) Necrotizing bronchitis has occurred after cigarette smoke exposure (H&E, ×200). (B) Neutrophils and lymphocytes are seen in the peribronchial area and alveolar spaces (H&E, ×200).

  • Figure 4 Seroconversion factors following influenza vaccination in cigarette smoke exposed and non-cigarette smoke exposed mice.


Reference

1. Nicholson KG, Wood JM, Zambon M. Influenza. Lancet. 2003. 362:1733–1745.
Article
2. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA. 2003. 289:179–186.
Article
3. Arcavi L, Benowitz NL. Cigarette smoking and infection. Arch Intern Med. 2004. 164:2206–2216.
Article
4. Richardson MA. Upper airway complications of cigarette smoking. J Allergy Clin Immunol. 1988. 81:1032–1035.
Article
5. Finklea JF, Sandifer SH, Smith DD. Cigarette smoking and epidemic influenza. Am J Epidemiol. 1969. 90:390–399.
6. Finklea JF, Hasselblad V, Riggan WB, Nelson WC, Hammer DI, Newill VA. Cigarette smoking and hemagglutination inhibition response to influenza after natural disease and immunization. Am Rev Respir Dis. 1971. 104:368–376.
Article
7. Cruijff M, Thijs C, Govaert T, Aretz K, Dinant GJ, Knottnerus A. The effect of smoking on influenza, influenza vaccination efficacy and on the antibody response to influenza vaccination. Vaccine. 1999. 17:426–432.
Article
8. Langley RJ, Kalra R, Mishra NC, Hahn FF, Razani-Boroujerdi S, Singh SP, Benson JM, Peña-Philippides JC, Barr EB, Sopori ML. A biphasic response to silica: I. Immunostimulation is restricted to the early stage of silicosis in Lewis rats. Am J Respir Cell Mol Biol. 2004. 30:823–829.
9. Zhang WD, Evans DH. Detection and identification of human influenza viruses by the polymerase chain reaction. J Virol Methods. 1991. 33:165–189.
Article
10. Admon D, Engelhard D, Strauss N, Goldman N, Zakay-Rones Z. Antibody response to influenza immunization in patients after heart transplantation. Vaccine. 1997. 15:1518–1522.
Article
11. Kark JD, Lebiush M, Rannon L. Cigarette smoking as a risk factor for epidemic a(h1n1) influenza in young men. N Engl J Med. 1982. 307:1042–1046.
Article
12. Kark JD, Lebiush M. Smoking and epidemic influenza-like illness in female military recruits: a brief survey. Am J Public Health. 1981. 71:530–532.
Article
13. Dye JA, Adler KB. Effects of cigarette smoke on epithelial cells of the respiratory tract. Thorax. 1994. 49:825–834.
Article
14. Leuchtenberger C, Leuchtenberger R, Ruch F, Tanaka K, Tanaka T. Cytological and cytochemical alterations in the respiratory tract of mice after exposure to cigarette smoke, influenza virus, and both. Cancer Res. 1963. 23:555–565.
15. Gebel S, Gerstmayer B, Bosio A, Haussmann HJ, Van Miert E, Müller T. Gene expression profiling in respiratory tissues from rats exposed to mainstream cigarette smoke. Carcinogenesis. 2004. 25:169–178.
Article
16. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002. 2:372–377.
Article
17. Razani-Boroujerdi S, Singh SP, Knall C, Hahn FF, Peña-Philippides JC, Kalra R, Langley RJ, Sopori ML. Chronic nicotine inhibits inflammation and promotes influenza infection. Cell Immunol. 2004. 230:1–9.
Article
18. Gualano RC, Hansen MJ, Vlahos R, Jones JE, Park-Jones RA, Deliyannis G, Turner SJ, Duca KA, Anderson GP. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir Res. 2008. 9:53.
Article
19. Robbins CS, Bauer CM, Vujicic N, Gaschler GJ, Lichty BD, Brown EG, Stämpfli MR. Cigarette smoke impacts immune inflammatory responses to influenza in mice. Am J Respir Crit Care Med. 2006. 174:1342–1351.
Article
20. Andersen P, Pedersen OF, Bach B, Bonde GJ. Serum antibodies and immunoglobulins in smokers and nonsmokers. Clin Exp Immunol. 1982. 47:467–473.
21. Hughes DA, Haslam PL, Townsend PJ, Turner-Warwick M. Numerical and functional alterations in circulatory lymphocytes in cigarette smokers. Clin Exp Immunol. 1985. 61:459–466.
22. Fisher GL, McNeill KL, Finch GL, Wilson FD, Golde DW. Functional evaluation of lung macrophages from cigarette smokers and nonsmokers. J Reticuloendothel Soc. 1982. 32:311–321.
23. Tollerud DJ, Clark JW, Brown LM, Neuland CY, Mann DL, Pankiw-Trost LK, Blattner WA, Hoover RN. Association of cigarette smoking with decreased numbers of circulating natural killer cells. Am Rev Respir Dis. 1989. 139:194–198.
Article
24. McCrea KA, Ensor JE, Nall K, Bleecker ER, Hasday JD. Altered cytokine regulation in the lungs of cigarette smokers. Am J Respir Crit Care Med. 1994. 150:696–703.
Article
25. Note for Guidance on Harmonisation of Requirements for Influenza Vaccines. CPMP/BWP/214/96. Committee for Proprietary Medicinal Products (CPMP). Accessed 25 July 2010. Available at: http://www.emea.europa.eu/pdfs/human/bwp/021496en.pdf.
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