Skip to main content
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 2003 Sep;111(12):1471–1477. doi: 10.1289/ehp.6300

Metal composition of ambient PM2.5 influences severity of allergic airways disease in mice.

Stephen H Gavett 1, Najwa Haykal-Coates 1, Lisa B Copeland 1, Joachim Heinrich 1, M Ian Gilmour 1
PMCID: PMC1241649  PMID: 12948886

Abstract

Children living in Hettstedt in eastern Germany have been reported to have a higher prevalence of sensitization to common aeroallergens than another cohort living in the neighboring city of Zerbst; these differences correlated with the presence of industrial air pollution. Samples of fine particulate matter (< 2.5 micro m aerodynamic diameter; PM(2.5)) collected in Hettstedt in 1999 had several-fold higher levels of zinc, magnesium, lead, copper, and cadmium than samples from Zerbst. To determine if the results from epidemiologic studies could be repeated in an animal model, we administered PM(2.5) from Hettstedt and Zerbst to ovalbumin-allergic mice. In Balb/c mice, PM(2.5) from Hettstedt, but not PM(2.5) from Zerbst or control filter extract, caused a significant increase in immediate responses to ovalbumin challenge when aspirated 2 hr before challenge, but not when aspirated immediately before sensitization 2 weeks earlier. Antigen-specific IgE was increased by Hettstedt PM(2.5) whether administered before sensitization or challenge. Airway responsiveness to methacholine aerosol and lung inflammatory cell numbers were significantly increased only in allergic mice exposed to Hettstedt PM(2.5) before challenge. Both Hettstedt and Zerbst PM(2.5) significantly increased lung injury parameters and proinflammatory cytokines. These results are consistent with epidemiologic findings and show that metal composition of ambient PM(2.5) influences the severity of allergic respiratory disease.

Full Text

The Full Text of this article is available as a PDF (171.4 KB).

Selected References

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

  1. Chew F. T., Goh D. Y., Ooi B. C., Saharom R., Hui J. K., Lee B. W. Association of ambient air-pollution levels with acute asthma exacerbation among children in Singapore. Allergy. 1999 Apr;54(4):320–329. doi: 10.1034/j.1398-9995.1999.00012.x. [DOI] [PubMed] [Google Scholar]
  2. Chung F. Anti-inflammatory cytokines in asthma and allergy: interleukin-10, interleukin-12, interferon-gamma. Mediators Inflamm. 2001 Apr;10(2):51–59. doi: 10.1080/09629350120054518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Diaz-Sanchez D., Garcia M. P., Wang M., Jyrala M., Saxon A. Nasal challenge with diesel exhaust particles can induce sensitization to a neoallergen in the human mucosa. J Allergy Clin Immunol. 1999 Dec;104(6):1183–1188. doi: 10.1016/s0091-6749(99)70011-4. [DOI] [PubMed] [Google Scholar]
  4. Dye J. A., Adler K. B., Richards J. H., Dreher K. L. Role of soluble metals in oil fly ash-induced airway epithelial injury and cytokine gene expression. Am J Physiol. 1999 Sep;277(3 Pt 1):L498–L510. doi: 10.1152/ajplung.1999.277.3.L498. [DOI] [PubMed] [Google Scholar]
  5. Dye J. A., Lehmann J. R., McGee J. K., Winsett D. W., Ledbetter A. D., Everitt J. I., Ghio A. J., Costa D. L. Acute pulmonary toxicity of particulate matter filter extracts in rats: coherence with epidemiologic studies in Utah Valley residents. Environ Health Perspect. 2001 Jun;109 (Suppl 3):395–403. doi: 10.1289/ehp.01109s3395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Foster W. M., Walters D. M., Longphre M., Macri K., Miller L. M. Methodology for the measurement of mucociliary function in the mouse by scintigraphy. J Appl Physiol (1985) 2001 Mar;90(3):1111–1117. doi: 10.1152/jappl.2001.90.3.1111. [DOI] [PubMed] [Google Scholar]
  7. Gavett S. H., Madison S. L., Dreher K. L., Winsett D. W., McGee J. K., Costa D. L. Metal and sulfate composition of residual oil fly ash determines airway hyperreactivity and lung injury in rats. Environ Res. 1997 Feb;72(2):162–172. doi: 10.1006/enrs.1997.3732. [DOI] [PubMed] [Google Scholar]
  8. Gavett S. H., Madison S. L., Stevens M. A., Costa D. L. Residual oil fly ash amplifies allergic cytokines, airway responsiveness, and inflammation in mice. Am J Respir Crit Care Med. 1999 Dec;160(6):1897–1904. doi: 10.1164/ajrccm.160.6.9901053. [DOI] [PubMed] [Google Scholar]
  9. Ghio A. J., Devlin R. B. Inflammatory lung injury after bronchial instillation of air pollution particles. Am J Respir Crit Care Med. 2001 Aug 15;164(4):704–708. doi: 10.1164/ajrccm.164.4.2011089. [DOI] [PubMed] [Google Scholar]
  10. Ghio Andrew J., Silbajoris Robert, Carson Johnny L., Samet James M. Biologic effects of oil fly ash. Environ Health Perspect. 2002 Feb;110 (Suppl 1):89–94. doi: 10.1289/ehp.02110s1189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamelmann E., Schwarze J., Takeda K., Oshiba A., Larsen G. L., Irvin C. G., Gelfand E. W. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am J Respir Crit Care Med. 1997 Sep;156(3 Pt 1):766–775. doi: 10.1164/ajrccm.156.3.9606031. [DOI] [PubMed] [Google Scholar]
  12. Heinrich J., Hoelscher B., Frye C., Meyer I., Wjst M., Wichmann H. E. Trends in prevalence of atopic diseases and allergic sensitization in children in Eastern Germany. Eur Respir J. 2002 Jun;19(6):1040–1046. doi: 10.1183/09031936.02.00261802. [DOI] [PubMed] [Google Scholar]
  13. Heinrich J., Hoelscher B., Wichmann H. E. Decline of ambient air pollution and respiratory symptoms in children. Am J Respir Crit Care Med. 2000 Jun;161(6):1930–1936. doi: 10.1164/ajrccm.161.6.9906105. [DOI] [PubMed] [Google Scholar]
  14. Heinrich J., Hoelscher B., Wjst M., Ritz B., Cyrys J., Wichmann H. Respiratory diseases and allergies in two polluted areas in East Germany. Environ Health Perspect. 1999 Jan;107(1):53–62. doi: 10.1289/ehp.9910753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Heinrich Joachim, Hoelscher Bernd, Frye Christian, Meyer Ines, Pitz Mike, Cyrys Josef, Wjst Matthias, Neas Lucas, Wichmann H-Erich. Improved air quality in reunified Germany and decreases in respiratory symptoms. Epidemiology. 2002 Jul;13(4):394–401. doi: 10.1097/00001648-200207000-00006. [DOI] [PubMed] [Google Scholar]
  16. Henderson R. F., Benson J. M., Hahn F. F., Hobbs C. H., Jones R. K., Mauderly J. L., McClellan R. O., Pickrell J. A. New approaches for the evaluation of pulmonary toxicity: bronchoalveolar lavage fluid analysis. Fundam Appl Toxicol. 1985 Jun;5(3):451–458. doi: 10.1016/0272-0590(85)90092-2. [DOI] [PubMed] [Google Scholar]
  17. Hylkema Machteld N., Timens Wim, Luinge Marjan, Van Der Werf Nienke, Hoekstra Maarten O. The effect of bacillus Calmette-Guérin immunization depends on the genetic predisposition to Th2-type responsiveness. Am J Respir Cell Mol Biol. 2002 Aug;27(2):244–249. doi: 10.1165/ajrcmb.27.2.4735. [DOI] [PubMed] [Google Scholar]
  18. Kobayashi T. Exposure to diesel exhaust aggravates nasal allergic reaction in guinea pigs. Am J Respir Crit Care Med. 2000 Aug;162(2 Pt 1):352–356. doi: 10.1164/ajrccm.162.2.9809035. [DOI] [PubMed] [Google Scholar]
  19. Lambert A. L., Dong W., Selgrade M. K., Gilmour M. I. Enhanced allergic sensitization by residual oil fly ash particles is mediated by soluble metal constituents. Toxicol Appl Pharmacol. 2000 May 15;165(1):84–93. doi: 10.1006/taap.2000.8932. [DOI] [PubMed] [Google Scholar]
  20. Lambert A. L., Dong W., Winsett D. W., Selgrade M. K., Gilmour M. I. Residual oil fly ash exposure enhances allergic sensitization to house dust mite. Toxicol Appl Pharmacol. 1999 Aug 1;158(3):269–277. doi: 10.1006/taap.1999.8709. [DOI] [PubMed] [Google Scholar]
  21. Lambert A. L., Selgrade M. K., Winsett D. W., Gilmour M. I. TNF-alpha enhanced allergic sensitization to house dust mite in brown Norway rats. Exp Lung Res. 2001 Oct-Nov;27(7):617–635. doi: 10.1080/019021401753181863. [DOI] [PubMed] [Google Scholar]
  22. Medoff Benjamin D., Sauty Alain, Tager Andrew M., Maclean James A., Smith R. Neal, Mathew Anuja, Dufour Jennifer H., Luster Andrew D. IFN-gamma-inducible protein 10 (CXCL10) contributes to airway hyperreactivity and airway inflammation in a mouse model of asthma. J Immunol. 2002 May 15;168(10):5278–5286. doi: 10.4049/jimmunol.168.10.5278. [DOI] [PubMed] [Google Scholar]
  23. Ostro B., Lipsett M., Mann J., Braxton-Owens H., White M. Air pollution and exacerbation of asthma in African-American children in Los Angeles. Epidemiology. 2001 Mar;12(2):200–208. doi: 10.1097/00001648-200103000-00012. [DOI] [PubMed] [Google Scholar]
  24. Patton Lucinda, Lopez Manuel. Effects of air pollutants on the allergic response. Allergy Asthma Proc. 2002 Jan-Feb;23(1):9–14. [PubMed] [Google Scholar]
  25. Peden D. B. Air pollution in asthma: effect of pollutants on airway inflammation. Ann Allergy Asthma Immunol. 2001 Dec;87(6 Suppl 3):12–17. doi: 10.1016/s1081-1206(10)62334-4. [DOI] [PubMed] [Google Scholar]
  26. Pope C. A., 3rd Respiratory disease associated with community air pollution and a steel mill, Utah Valley. Am J Public Health. 1989 May;79(5):623–628. doi: 10.2105/ajph.79.5.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Salvi S. Pollution and allergic airways disease. Curr Opin Allergy Clin Immunol. 2001 Feb;1(1):35–41. doi: 10.1097/01.all.0000010982.31993.84. [DOI] [PubMed] [Google Scholar]
  28. Steerenberg P. A., Dormans J. A., van Doorn C. C., Middendorp S., Vos J. G., van Loveren H. A pollen model in the rat for testing adjuvant activity of air pollution components. Inhal Toxicol. 1999 Dec;11(12):1109–1122. doi: 10.1080/089583799196619. [DOI] [PubMed] [Google Scholar]
  29. Yoshida Makoto, Leigh Richard, Matsumoto Koichiro, Wattie Jennifer, Ellis Russ, O'Byrne Paul M., Inman Mark D. Effect of interferon-gamma on allergic airway responses in interferon-gamma-deficient mice. Am J Respir Crit Care Med. 2002 Aug 15;166(4):451–456. doi: 10.1164/rccm.200202-095OC. [DOI] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Sciences

RESOURCES