Inflammation

, Volume 35, Issue 2, pp 671–683

Neutrophilic Inflammatory Response and Oxidative Stress in Premenopausal Women Chronically Exposed to Indoor Air Pollution from Biomass Burning

  • Anirban Banerjee
  • Nandan Kumar Mondal
  • Debangshu Das
  • Manas Ranjan Ray
Article

Abstact

The possibility of inflammation and neutrophil activation in response to indoor air pollution (IAP) from biomass fuel use has been investigated. For this, 142 premenopausal, never-smoking women (median age, 34 years) who cook exclusively with biomass (wood, dung, crop wastes) and 126 age-matched control women who cook with cleaner fuel liquefied petroleum gas (LPG) were enrolled. The neutrophil count in blood and sputum was significantly higher (p < 0.05) in biomass users than the control group. Flow cytometric analysis revealed marked increase in the surface expression of CD35 (complement receptor-1), CD16 (FCγ receptor III), and β2 Mac-1 integrin (CD11b/CD18) on circulating neutrophils of biomass users. Besides, enzyme-linked immunosorbent assay showed that they had 72%, 67%, and 54% higher plasma levels of the proinflammatory cytokines tumor necrosis factor-alpha, interleukin-6, and interleukin-12, respectively, and doubled neutrophil chemoattractant interleukin-8. Immunocytochemical study revealed significantly higher percentage of airway neutrophils expressing inducible nitric oxide synthase, while the serum level of nitric oxide was doubled in women who cooked with biomass. Spectrophotometric analysis documented higher myeloperoxidase activity in circulating neutrophils of biomass users, suggesting neutrophil activation. Flow cytometry showed excess generation of reactive oxygen species (ROS) by leukocytes of biomass-using women, whereas their erythrocytes contained a depleted level of antioxidant enzyme superoxide dismutase (SOD). Indoor air of biomass-using households had two to four times more particulate matter with diameters of <10 μm (PM10) and <2.5 μm (PM2.5) as measured by real-time laser photometer. After controlling potential confounders, rise in proinflammatory mediators among biomass users were positively associated with PM10 and PM2.5 in indoor air, suggesting a close relationship between IAP and neutrophil activation. Besides, the levels of neutrophil activation and inflammation markers were positively associated with generation of ROS and negatively with SOD, indicating a role of oxidative stress in mediating neutrophilic inflammatory response following chronic inhalation of biomass smoke.

KEY WORDS

biomass fuel neutrophil inflammation oxidative stress premenopausal women India 

ABBREVIATIONS

ACD

acid citrate dextrose

BMF

biomass fuel

BSA

bovine serum albumin

DCF-DA

dichlorofluorescein diacetate

EDTA

ethylenediaminetetraacetic acid

ELISA

enzyme-linked immunosorbent assay

FACS

fluorescence-activated cell sorter

FITC

fluorescein isothiocyanate

HRP

horseradish peroxidase

IAP

indoor air pollution

ICC

immunocytochemistry

IL

interleukin

iNOS

inducible nitric oxide synthase

LPG

liquefied petroleum gas

MFI

mean fluorescence intensity

MPO

myeloperoxidase

NO

nitric oxide

PAP

Papanicolaou

PBS

phosphate-buffered saline

PE

phycoerythrin

PM

particulate matter

ROS

reactive oxygen species

SOD

superoxide dismutase

TNF

tumor necrosis factor

References

  1. 1.
    Zhang, J., and K.R. Smith. 1996. Hydrocarbon emissions and health risks from cook stoves in developing countries. Journal of Exposure Analysis and Environmental Epidemiology 6: 147–161.PubMedGoogle Scholar
  2. 2.
    Smith, K.R. 2000. National burden of disease in India from indoor air pollution. Proceedings of the National Academy of Sciences of the United States of America 97: 3286–3293.Google Scholar
  3. 3.
    Pandey, M.R., J.S.M. Boleij, K.R. Smith, and E.M. Wafula. 1989. Indoor air pollution in developing countries and acute respiratory infections in children. Lancet 1: 424–429.Google Scholar
  4. 4.
    Ghio, A.J., and R.B. Devlin. 2001. Inflammatory lung injury after bronchial instillation of air pollution particles. American Journal of Respiratory and Critical Care Medicine 164: 704–708.PubMedGoogle Scholar
  5. 5.
    Mukae, H., R. Vincent, K. Quinlan, D. English, J. Hards, J.C. Hogg, and S.F. van Eeden. 2001. The effect of repeated exposure to particulate air pollution (PM10) on the bone marrow. American Journal of Respiratory and Critical Care Medicine 163: 201–209.PubMedGoogle Scholar
  6. 6.
    Nordenhall, C., J. Pourazar, A. Blomberg, J.O. Levin, T. Sandstrom, and E. Adelroth. 2000. Airway inflammation following exposure to diesel exhaust: A study of time kinetics using induced sputum. The European Respiratory Journal 15: 1046–1051.PubMedCrossRefGoogle Scholar
  7. 7.
    Rudell, B., A. Blomberg, R. Helleday, M.C. Ledin, B. Lundbäck, N. Stjernberg, P. Hörstedt, and T. Sandström. 1999. Bronchoalveolar inflammation after exposure to diesel exhaust: Comparison between unfiltered and particle trap filtered exhaust. Occupational and Environmental Medicine 56: 527–534.PubMedCrossRefGoogle Scholar
  8. 8.
    Salvi, S., A. Blomberg, B. Rudell, F. Kelly, T. Sandström, S.T. Holgate, and A. Frew. 1999. Acute inflammatory responses in the airways and peripheral blood after short term exposure to diesel exhaust in healthy human volunteers. American Journal of Respiratory and Critical Care Medicine 159: 702–709.PubMedGoogle Scholar
  9. 9.
    Seaton, A., W. Macnee, K. Donaldson, and D. Godden. 1995. Particulate air pollution and acute health effects. Lancet 345: 176–178.PubMedCrossRefGoogle Scholar
  10. 10.
    Ishii, T., K. Itoh, E. Ruiz, D.S. Leake, H. Unoki, M. Yamamoto, and G.E. Mann. 2004. Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: Activation by oxidatively modified LDL and 4-hydroxynonenal. Circulation Research 94: 609–616.PubMedCrossRefGoogle Scholar
  11. 11.
    Suwa, T., J.C. Hogg, K.B. Quinlan, A. Ohgami, R. Vincent, and S.F. van Eeden. 2002. Particulate air pollution induces progression of atherosclerosis. Journal of the American College of Cardiology 39: 935–942.PubMedCrossRefGoogle Scholar
  12. 12.
    van Eeden, S.F., W.C. Tan, T. Suwa, H. Mukae, T. Terashima, T. Fujii, D. Qui, R. Vincent, and J.C. Hogg. 2001. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM10). American Journal of Respiratory and Critical Care Medicine 164: 826–830.PubMedGoogle Scholar
  13. 13.
    Naeher, L.P., M. Brauer, M. Lipsett, J.T. Zelikoff, C.D. Simpson, J.Q. Koenig, and K.R. Smith. 2007. Wood smoke health effects: A review. Inhalation Toxicology 19: 67–106.PubMedCrossRefGoogle Scholar
  14. 14.
    Fujii, T., S. Hayashi, J.C. Hogg, R. Vincent, and S.F. van Eeden. 2001. Particulate matter induces cytokine expression in human bronchial epithelial cells. American Journal of Respiratory Cell and Molecular Biology 25: 265–271.PubMedGoogle Scholar
  15. 15.
    Balamayooran, G., S. Batra, M.B. Fessler, K.I. Happel, and S. Jeyaseelan. 2010. Mechanisms of neutrophil accumulation in the lungs against bacteria. American Journal of Respiratory Cell and Molecular Biology 43: 5–16.PubMedCrossRefGoogle Scholar
  16. 16.
    Liu, Y., S.K. Shaw, and S. Ma. 2004. Regulation of leukocyte transmigration: Cell surface interactions and signaling events. Journal of Immunology 172: 7–13.Google Scholar
  17. 17.
    Chung, K.F. 1986. Role played by inflammation in the hyperreactivity of the airways in asthma. Thorax 41: 657–662.PubMedCrossRefGoogle Scholar
  18. 18.
    Gibson, P.G., J.L. Simpson, and N. Saltos. 2001. Heterogeneity of airway inflammation in persistent asthma: Evidence of neutrophilic inflammation and increased sputum interleukin-8. Chest 119: 1329–1336.PubMedCrossRefGoogle Scholar
  19. 19.
    Jatakanon, A., C. Uasuf, W. Maziak, S. Lim, K.F. Chung, and P.J. Barnes. 1999. Neutrophilic inflammation in severe persistent asthma. American Journal of Respiratory and Critical Care Medicine 160: 1532–1539.PubMedGoogle Scholar
  20. 20.
    Tonnel, A.B., P. Gosset, and I. Tillie-Leblond. 2001. Characteristics of the inflammatory response in bronchial lavage fluids from patients with status asthmaticus. International Archives of Allergy and Immunology 124: 267–271.PubMedCrossRefGoogle Scholar
  21. 21.
    Voynow, J.A., B.M. Fischer, D.E. Malarkey, L.H. Burch, T. Wong, M. Longphre, S.B. Ho, and W.M. Foster. 2004. Neutrophil elastase induces mucus cell metaplasia in mouse lung. American Journal of Physiology. Lung Cellular and Molecular Physiology 287: L1293–L1302.PubMedCrossRefGoogle Scholar
  22. 22.
    Huang, C.D., H.H. Chen, C.H. Wang, C.L. Chou, S.M. Lin, H.C. Lin, and H.P. Kuo. 2004. Human neutrophil-derived elastase induces airway smooth muscle cell proliferation. Life Sciences 74: 2479–2492.PubMedCrossRefGoogle Scholar
  23. 23.
    Oltmanns, U., M.B. Sukkar, S. Xie, M. John, and K.F. Chung. 2005. Induction of human airway smooth muscle apoptosis by neutrophils and neutrophil elastase. American Journal of Respiratory Cell and Molecular Biology 32: 334–341.PubMedCrossRefGoogle Scholar
  24. 24.
    Ikitimur, B., and B. Karadag. 2010. Role of myeloperoxidase in cardiology. Future Cardiology 6: 693–702.PubMedCrossRefGoogle Scholar
  25. 25.
    Yamagata, T., H. Sugiura, T. Yokoyama, S. Yanagisawa, T. Ichikawa, K. Ueshima, K. Akamatsu, T. Hirano, M. Nakanishi, Y. Yamagata, K. Matsunaga, Y. Minakata, and M. Ichinose. 2007. Overexpression of CD-11b and CXCR1 on circulating neutrophils: Its possible role in COPD. Chest 132: 890–899.PubMedCrossRefGoogle Scholar
  26. 26.
    Inoue, K., H. Takano, and Y. Zasshi. 2011. Biology of diesel exhaust effects on allergic pulmonary inflammation. Yakugaku Zasshi 131: 367–371.PubMedCrossRefGoogle Scholar
  27. 27.
    Budinger, G.R., J.L. McKell, D. Urich, N. Foiles, I. Weiss, S.E. Chiarella, A. Gonzalez, S. Soberanes, A.J. Ghio, R. Nigdelioglu, E.A. Mutlu, K.A. Radigan, D. Green, H.C. Kwaan, and G.M. Mutlu. 2011. Particulate matter-induced lung inflammation increases systemic levels of PAI-1 and activates coagulation through distinct mechanisms. PloS One 6: e18525.PubMedCrossRefGoogle Scholar
  28. 28.
    Carpentier, J.L., D.P. Lew, J.P. Paccaud, R. Gil, B. Iacopetta, M. Kazatchkine, O. Stendahl, and T. Pozzan. 1991. Internalization pathway of C3b receptors in human neutrophils and its transmodulation by chemoattractant receptors stimulation. Cell Regulation 2: 41–55.PubMedGoogle Scholar
  29. 29.
    Smith, J., A. Gray, D. Pyne, M. Baker, R. Telford, and M. Weidemann. 1996. Moderate exercise triggers both priming and activation of neutrophil subpopulations. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 270: R838–R845.Google Scholar
  30. 30.
    Davey, P.C., M. Zuzel, A.S. Kamiguti, J.A. Hunt, and K.A. Aziz. 2000. Activation-dependent proteolytic degradation of polymorphonuclear CD11b. British Journal of Haematology 111: 934–942.PubMedCrossRefGoogle Scholar
  31. 31.
    Fleit, H.B., C.D. Kobasiuk, C. Daly, R. Furie, P.C. Levy, and R.O. Webster. 1992. A soluble form of Fc gamma RIII is present in human serum and other body fluids and is elevated at sites of inflammation. Blood 79: 2721–2728.PubMedGoogle Scholar
  32. 32.
    Sadallah, S., E. Lach, H.U. Lutz, S. Schwarz, P.A. Guerne, and J.A. Schifferli. 1997. CR1, CD35 in synovial fluid from patients with inflammatory joint diseases. Arthritis and Rheumatism 40: 520–526.PubMedCrossRefGoogle Scholar
  33. 33.
    Babcock, G.F., J.W. Alexander, and G.D. Warden. 1990. Flow cytometric analysis of neutrophil subsets in thermally injured patients developing infection. Clinical Immunology and Immunopathology 54: 117–125.PubMedCrossRefGoogle Scholar
  34. 34.
    Crockett-Torabi, E., and J.C. Fantone. 1990. Soluble and insoluble immune complexes activate human neutrophil NADPH oxidase by distinct Fc gamma receptor-specific mechanisms. Journal of Immunology 145: 3026–3032.Google Scholar
  35. 35.
    Weiss, S. 1989. Tissue destruction by neutrophils. The New England Journal of Medicine 320: 365–379.PubMedCrossRefGoogle Scholar
  36. 36.
    Mondal, N.K., A. Dutta, A. Banerjee, S. Chakraborty, T. Lahiri, and M.R. Ray. 2009. Effect of indoor air pollution from biomass fuel use on argyrophilic nuclear organizer regions in buccal epithelial cells. Journal of Environmental Pathology, Toxicology and Oncology 28: 253–259.PubMedGoogle Scholar
  37. 37.
    Mondal, N.K., D. Das, B. Mukherjee, and M.R. Ray. 2011. Upregulation of AgNOR expression in epithelial cells and neutrophils in the airways and leukocytes in peripheral blood of women chronically exposed to biomass smoke. Analytical and Quantitative Cytology and Histology 33: 50–59.PubMedGoogle Scholar
  38. 38.
    Mondal, N.K., B. Mukherjee, D. Das, and M.R. Ray. 2010. Micronucleus formation, DNA damage and repair in premenopausal women chronically exposed to high level of indoor air pollution from biomass fuel use in rural India. Mutation Research 697: 47–54.PubMedGoogle Scholar
  39. 39.
    Mondal, N.K., P. Bhattacharya, and M.R. Ray. 2011b. Assessment of DNA damage by comet assay and fast halo assay in buccal epithelial cells of Indian women chronically exposed to biomass smoke. International Journal of Hygiene and Environmental Health. doi:10.1016/j.ijheh.2011.04.003.
  40. 40.
    Mondal, N.K., A. Roy, B. Mukherjee, D. Das, and M.R. Ray. 2010. Indoor air pollution from biomass burning activates Akt in airway cells and peripheral blood lymphocytes: A study among premenopausal women in rural India. Toxicologic Pathology 38: 1085–1098.PubMedCrossRefGoogle Scholar
  41. 41.
    Dutta, A., B. Mukherjee, D. Das, A. Banerjee, and M.R. Ray. 2011. Hypertension with elevated levels of oxidized low-density lipoprotein and anticardiolipin antibody in the circulation of premenopausal Indian women chronically exposed to biomass smoke during cooking. Indoor Air 21: 165–176.PubMedCrossRefGoogle Scholar
  42. 42.
    Erkilic, S., C. Ozsarac, and S. Kullu. 2003. Sputum cytology for the diagnosis of lung cancer: Comparison of smear and modified cell block methods. Acta Cytologica 47: 1023–1027.PubMedCrossRefGoogle Scholar
  43. 43.
    Hughes, H.E., and T.C. Dodds. 1968. Handbook of diagnostic cytology. Edinburgh: E&S Livingstone.Google Scholar
  44. 44.
    Grubb, C. 1988. Diagnostic cytopathology—A textbook and colour atlas. Edinburgh: Churchill Livingstone.Google Scholar
  45. 45.
    Drábiková, K., R. Nosál, V. Jancinová, M. Cíz, and A. Lojek. 2002. Reactive oxygen metabolite production is inhibited by histamine and H1-antagonist dithiaden in human PMN leukocytes. Free Radical Research 36: 975–980.PubMedCrossRefGoogle Scholar
  46. 46.
    Kurutas, E.B., O. Arican, and S. Sasmaz. 2005. Superoxide dismutase and myeloperoxidase activities in polymorphonuclear leukocytes in acne vulgaris. Acta Dermatovenerologica Alpina, Panonica, et Adriatica 14: 39–42.PubMedGoogle Scholar
  47. 47.
    Rothe, G., and G. Valet. 1990. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2, 7-dichlorofluorescein. Journal of Leukocyte Biology 47: 440–448.PubMedGoogle Scholar
  48. 48.
    Paoletti, F., D. Aldinucci, A. Mocali, and A. Caparrini. 1986. A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Analytical Biochemistry 154: 536–541.PubMedCrossRefGoogle Scholar
  49. 49.
    Lehocky, A.H., and L.P. Williams. 1996. Comparison of respirable samplers to direct-reading real-time aerosol monitors for measuring coal dust. American Industrial Hygiene Association Journal 57: 1013–1018.CrossRefGoogle Scholar
  50. 50.
    Siddiqui, A.R., K. Lee, D. Bennett, X. Yang, K.H. Brown, Z.A. Bhutta, and E.B. Gold. 2009. Indoor carbon monoxide and PM2.5 concentrations by cooking fuels in Pakistan. Indoor Air 19: 75–82.PubMedCrossRefGoogle Scholar
  51. 51.
    Chung, A., D.P. Chang, M.J. Kleeman, K.D. Perry, T.A. Cahill, D. Dutcher, E.M. McDougall, and K. Stroud. 2001. Comparison of real-time instruments used to monitor airborne particulate matter. Journal of the Air & Waste Management Association 51: 109–120.Google Scholar
  52. 52.
    Muller Kobold, A.C., J.G. Zijlstra, H.R. Koene, M. de Haas, C.G. Kallenberg, and J.W. Tervaert. 1998. Levels of soluble Fc gammaRIII correlate with disease severity in sepsis. Clinical and Experimental Immunology 114: 220–227.PubMedCrossRefGoogle Scholar
  53. 53.
    Barregard, L., G. Sällsten, L. Andersson, A.C. Almstrand, P. Gustafson, M. Andersson, and A.C. Olin. 2008. Experimental exposure to wood smoke: Effects on airway inflammation and oxidative stress. Occupational and Environmental Medicine 65: 319–324.PubMedCrossRefGoogle Scholar
  54. 54.
    Frampton, M.W., J.C. Stewart, G. Oberdorster, P.E. Morrow, D. Chalupa, A.P. Pietropaoli, L.M. Frasier, D.M. Speers, C. Cox, L.S. Huang, and M.J. Utell. 2006. Inhalation of ultrafine particles alters blood leukocyte expressions of adhesion molecules in humans. Environmental Health Perspectives 114: 51–58.PubMedCrossRefGoogle Scholar
  55. 55.
    Il'yasova, D., A. Ivanova, J.D. Morrow, M. Cesari, and M. Pahor. 2008. Correlation between two markers of inflammation, serum C-reactive protein and interleukin 6, and indices of oxidative stress in patients with high risk of cardiovascular disease. Biomarkers 13: 41–51.PubMedCrossRefGoogle Scholar
  56. 56.
    Parkos, C.A., C. Delp, M.A. Arnaout, and J.L. Madara. 1991. Neutrophil migration across a cultured intestinal epithelium: Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. The Journal of Clinical Investigation 88: 1605–1612.PubMedCrossRefGoogle Scholar
  57. 57.
    Koethe, S.M., J.R. Kuhnmuench, and C.G. Becker. 2000. Neutrophil priming by cigarette smoke condensate and a tobacco antiidiotypic antibody. The American Journal of Pathology 157: 1735–1743.PubMedCrossRefGoogle Scholar
  58. 58.
    Edwards, S.W., and F. Watson. 1995. The cell biology of phagocytes. Immunology Today 16: 508–510.PubMedCrossRefGoogle Scholar
  59. 59.
    Noguera, A., X. Busquets, J. Sauleda, J.M. Villaverde, W. MacNee, and A.G. Agustí. 1998. Expression of adhesion molecules and G proteins in circulating neutrophils in chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine 158: 1664–1668.PubMedGoogle Scholar
  60. 60.
    Goldmann, B.U., V. Rudolph, T.K. Rudolph, A.K. Holle, M. Hillebrandt, T. Meinertz, and S. Baldus. 2009. Neutrophil activation precedes myocardial injury in patients with acute myocardial infarction. Free Radical Biology & Medicine 47: 79–83.CrossRefGoogle Scholar
  61. 61.
    Lange, M., A. Hamahata, D.L. Traber, Y. Nakano, L.D. Traber, and P. Enkhbaatar. 2011. Specific inhibition of nitric oxide synthases at different time points in a murine model of pulmonary sepsis. Biochemical and Biophysical Research Communications 404: 877–881.PubMedCrossRefGoogle Scholar
  62. 62.
    Shang, L.H., Z.Q. Luo, X.D. Deng, M.J. Wang, F.R. Huang, D.D. Feng, and S.J. Yue. 2010. Expression of N-methyl-D-aspartate receptor and its effect on nitric oxide production of rat alveolar macrophages. Nitric Oxide 23: 327–331.PubMedCrossRefGoogle Scholar
  63. 63.
    Ding, R., J. Han, Y. Tian, R. Guo, and X. Ma. 2011. Sphingosine-1-phosphate attenuates lung injury induced by intestinal ischemia/reperfusion in mice: Role of inducible nitric-oxide synthase. Inflammation. doi:10.1007/s10753-011-9301-0.
  64. 64.
    Rus, A., L. Castro, M.L. Del Moral, and A. Peinado. 2010. Inducible NOS inhibitor 1400 W reduces hypoxia/re-oxygenation injury in rat lung. Redox Report 15: 169–178.PubMedCrossRefGoogle Scholar
  65. 65.
    Jiménez, L.A., E.M. Drost, P.S. Gilmour, I. Rahman, F. Antonicelli, H. Ritchie, W. MacNee, and K. Donaldson. 2002. PM10-exposed macrophages stimulate a pro inflammatory response in lung epithelial cells via TNF-α. American Journal of Physiology. Lung Cellular and Molecular Physiology 282: L237–L248.PubMedGoogle Scholar
  66. 66.
    Keatings, V.M., P.D. Collins, and D.M. Scott. 1996. Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. American Journal of Respiratory and Critical Care Medicine 153: 530–534.PubMedGoogle Scholar
  67. 67.
    Khalequzzaman, M., M. Kamijima, K. Sakai, B.A. Hoque, and T. Nakajima. 2010. Indoor air pollution and the health of children in biomass- and fossil-fuel users of Bangladesh: Situation in two different seasons. Environmental Health and Preventive Medicine 15: 236–243.PubMedCrossRefGoogle Scholar
  68. 68.
    Kimata, H. 2004. Effect of exposure to volatile organic compounds on plasma levels of neuropeptides, nerve growth factor and histamine in patients with self-reported multiple chemical sensitivity. International Journal of Hygiene and Environmental Health 207: 159–163.PubMedCrossRefGoogle Scholar
  69. 69.
    D'Amato, G., L. Cecchi, M. D'Amato, and G. Liccardi. 2010. Urban air pollution and climate change as environmental risk factors of respiratory allergy: An update. Journal of Investigational Allergology & Clinical Immunology 20: 95–102.Google Scholar
  70. 70.
    Gilmour, M.I., M.S. Jaakkola, S.J. London, A.E. Nel, and C.A. Rogers. 2006. How exposure to environmental tobacco smoke, outdoor air pollutants, and increased pollen burdens influences the incidence of asthma. Environmental Health Perspectives 114: 627–633.PubMedCrossRefGoogle Scholar
  71. 71.
    Scapellato, M.L., and M. Lotti. 2007. Short-term effects of particulate matter: An inflammatory mechanism? Critical Reviews in Toxicology 37: 461–487.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Anirban Banerjee
    • 1
  • Nandan Kumar Mondal
    • 1
  • Debangshu Das
    • 1
  • Manas Ranjan Ray
    • 1
  1. 1.Department of Experimental HematologyChittaranjan National Cancer InstituteKolkataIndia

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