Skip to main content

Advertisement

Log in

Biological monitoring of particulate matter accumulated in the lungs of urban asthmatic children in the Tel-Aviv area

  • Original Article
  • Published:
International Archives of Occupational and Environmental Health Aims and scope Submit manuscript

Abstract

Purpose

Lung inflammation from exposure to airborne particulate matter (PM) may be responsible for morbidity in asthma, but several studies using environmental monitoring data showed inconsistent results. Thus, the aim of this study was to evaluate the capability of induced sputum (IS) technology in order to biologically monitor PM in the lungs of urban asthmatic children.

Methods

We collected clinical, demographic, biological and environmental monitoring data on 136 children referred for asthma evaluations. The study participants were divided into two groups according to IS eosinophil counts of <3 % (non-eosinophilic inflammation, n = 52) and ≥3 % (eosinophilic inflammation, n = 84).

Results

The eosinophilic group displays significantly higher levels of fractional exhaled nitric oxide than the non-eosinophilic one (58.8 ± 47.5 vs 28.9 ± 34.2 ppm, p = 0.007). Particles (0–2.5 and 0–5 µm) comprised a strong risk factor for eosinophilic inflammation in IS (≥3 %). Children with >80 % of particles (0–2.5 µm) out of the total PM accumulated in the airways displayed the highest OR 10.7 (CI 2.052–56.4 p = 0.005) for an existing eosinophilic inflammation. Heme oxygenase-1 (HO-1) enzyme levels in IS positively correlated with % eosinophils and with particles in IS ranging between 2 and 3 μm. The level of HO-1 enzyme activity and FEV1/FVC in children with <3 % eosinophils, but not ≥3 %, was positively and significantly correlated, showing a protective effect of HO-1.

Conclusion

Accumulation of PM involves oxidative stress pathways and is a risk factor for developing eosinophilic inflammation in asthmatic children. IS can biologically monitor this process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • American Academy of Pediatrics: Policy Statement (2004) Ambient air pollution: health hazards to children. Pediatrics 114:1699

  • American Thoracic Society; European Respiratory Society (2005) ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide. Am J Respir Crit Care Med 171:912–930

    Article  Google Scholar 

  • Atzori L, Chua F, Dunsmore SE, Dunsmore SE, Willis D, Barbarisi M et al (2004) Attenuation of bleomycin induced pulmonary fibrosis in mice using the heme oxygenase inhibitor Zn-deuteroporphyrin IX-2,4-bisethylene glycol. Thorax 59:217–223

    Article  CAS  Google Scholar 

  • Brunekreef B, Holgate ST (2002) Air pollution and health. The Lancet 360:1233–1242

    Article  CAS  Google Scholar 

  • Carvalhoa TC, Peters JI, Williams RO III (2011) Influence of particle size on regional lung deposition—what evidence is there? Int J Pharm 406:1–10

    Article  Google Scholar 

  • Chen BY, Chan CC, Lee CT, Cheng TJ, Huang WC, Jhou JC, Han YY, Chen CC, Guo YL (2012) The association of ambient air pollution with airway inflammation in schoolchildren. Am J Epidemiol 175(8):764–774

    Article  Google Scholar 

  • Chimenti G, Morici A, Paterno A, Paternò A, Bonanno L, Siena A, Licciardi et al (2007) Endurance training damages small airway epithelium in mice Am J Respir Crit Care Med 175(5):442–449

  • Chung KF (2014) Defining phenotypes in asthma: a step towards personalized medicine. Drugs 74:442–449

    Article  Google Scholar 

  • Fireman E, Lerman Y, Ganor E, Greif J, Fireman-Shoresh S, Lioy PJ et al (2004) Induced sputum assessment in New York City firefighters exposed to World Trade Center dust. Environ Health Perspect 112:1564–1569

    Article  CAS  Google Scholar 

  • Fireman E, Lerman Y, Stark M, Schwartz Y, Ganor E, Grinberg N et al (2008) Detection of occult lung impairment in welders by induced sputum particles and breath oxidation. Am J Ind Med 51:503–511

    Article  Google Scholar 

  • Fireman E, Lerman Y, Stark M, Pardo A, Elliott J, VanDyke M et al (2010) Combined environmental and biological monitoring in workers exposed to beryllium. Proc Am Thorac Soc 7:155

    Google Scholar 

  • Fleming L, Tsartsali L, Wilson N, Regamey N, Bush A (2012) Sputum inflammatory phenotypes are not stable in children with asthma. Thorax 67:675–681

    Article  Google Scholar 

  • Forno E, Celedón JC (2012) Predicting asthma exacerbations in children. Curr Opin Pulm Med 18:63–69

    Article  Google Scholar 

  • Fredenburgh MA, Perrella A, Mitsialis SA (2007) The role of heme-oxygenase-1 in pulmonary disease. Am J Respir Cell Mol Biol 36:158–165

    Article  CAS  Google Scholar 

  • Gauvreau GM, O’Byrne PM, Boulet LP, Wang Y, Cockcroft D, Bigler J et al (2014) Effects of an anti-TSLP antibody on allergen-induced asthmatic responses. N Engl J Med 370:2102–2110

    Article  CAS  Google Scholar 

  • Gehr P, Schürch S, Berthiaume Y, Im Hof V, Geiser M (1990) Particle retention in airways by surfactant. J Aerosol Med 3:27–43

    Article  Google Scholar 

  • Green RH, Brightling CE, McKenna S, Hargadon B, Parker D, Bradding P et al (2002) Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet 360:1715–1721

    Article  Google Scholar 

  • He M, Ichinose T, Yoshida S, Nishikawa M, Mori I, Yanagisawa R et al (2010) Urban particulate matter in Beijing, China, enhances allergen-induced murine lung eosinophilia. Inhal Toxicol 22:709–718

    Article  CAS  Google Scholar 

  • Heinrich J, Slama R (2007) Fine particles, a major threat to children. Int J Hyg Environ Health 210:617–622

    Article  CAS  Google Scholar 

  • Horváth I, Donnelly LE, Kiss A, Paredi P, Kharitonov SA, Barnes PJ (1998) Raised levels of exhaled carbon monoxide are associated with an increased expression of heme oxygenase-1 in airway macrophages in asthma: a new marker of oxidative stress. Thorax 53:668–672

    Article  Google Scholar 

  • Kokturk N, Sabag M, Stark M, Grief J, Fireman E (2009) High extracellular induced sputum heme oxygenase-1 in sarcoidosis and chronic beryllium disease. Eur J Clin Invest 39:584–590

    Article  CAS  Google Scholar 

  • Kreyling W, Scheuch G (2000) Clearance of particles deposited in the lungs. In: Heyder J, Gehr P (eds) Particle lung interactions. Marcel Dekker, New York, pp 323–376

  • Kreyling WG, Blanchard JD, Godleski JJ, Haeussermann S, Heyder J, Hutzler P et al (1999) Anatomic localization of 24- and 96-h particle retention in canine airways. Appl Physiol 87:269–284

    CAS  Google Scholar 

  • Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, Choi AM (1996) Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol 14:556–568

    Article  CAS  Google Scholar 

  • Lerman Y, Segal B, Rochvarger M, Weinberg D, Kivity O, Fireman E (2003) Induced-sputum particle size distribution and pulmonary function in foundry workers. Arch Environ Health 58:565–571

    Article  Google Scholar 

  • Lu F, Zander DS, Visner GA (2002) Increased expression of heme oxygenase-1 in human lung transplantation. J Heart Lung Transplant 21:1120–1126

    Article  Google Scholar 

  • Maestrelli P, Páska C, Saetta M, Turato G, Nowicki Y, Monti S et al (2003) Decreased heme oxygenase-1 and increased inducible nitric oxide synthase in the lung of severe COPD patients. Eur Respir J 21:971–976

    Article  CAS  Google Scholar 

  • Mazzoli-Rocha F, Fernandes S, Einicker-Lamas M, Zin WA (2010) Roles of oxidative stress in signaling and inflammation induced by particulate matter. Cell Biol Toxicol 26:481–498

    Article  CAS  Google Scholar 

  • Meister KR, Zheng Y (2006) Biological monitoring. In: LaDou J (ed) Occupational and environmental medicine, 2nd edn. Appleton and lange, pp 324–333

  • Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, ATS/ERS Task Force (2005) Standardisation of spirometry. Eur Respir J 26:319–338

    Article  CAS  Google Scholar 

  • Möller W, Kreyling WG, Schmid O, Semmler-Behnke M, Schulz H (2009) Deposition, retention and clearance, and translocation of inhaled fine and nano-particles in the respiratory tract (Chapter 5). In: Gehr P, Mühlfeld C, Rothen-Rutishauser B, Blank F (eds) Particle–lung interactions. 2nd edn. Informa Healthcare USA, New York, New York, pp 79–107

  • Møller P, Jacobsen NR, Folkmann JK, Danielsen PH, Mikkelsen L, Hemmingsen JG et al (2010) Role of oxidative damage in toxicity of particulates. Free Radic Res 44:1–46

    Article  Google Scholar 

  • Ning Li M, Venkatesan I, Miguel A, Kaplan R, Gujuluva C, Alam J et al (2000) Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. J Immunol 165:3393–3401

    Article  Google Scholar 

  • O’Byrne PM (2011) Therapeutic strategies to reduce asthma exacerbations. J Allergy Clin Immunol 128:257–263

    Article  Google Scholar 

  • Pavord ID (2013) Eosinophilic phenotypes of airway disease. Ann Am Thorac Soc 10(Suppl):S143–S149

    Article  Google Scholar 

  • Petsky HL, Cates CJ, Lasserson TJ, Li AM, Turner C, Kynaston JA et al (2012) A systematic review and meta-analysis: tailoring asthma treatment on eosinophilic markers (exhaled nitric oxide or sputum eosinophils). Thorax 67:199–208

    Article  CAS  Google Scholar 

  • Pin I, Gibson PG, Kolendowicz R, Girgis-Gabardo A, Denburg JA, Hargreave FE et al (1992) Use of induced sputum cell counts to investigate airway inflammation in asthma. Thorax 47:25–29

    Article  CAS  Google Scholar 

  • Popov T, Gottschalk R, Kolendowicz R, Dolovich J, Powers P, Hargreave FE (1994) The evaluation of a cell dispersion method of sputum examination. Clin Exp Allergy 24:778–783

    Article  CAS  Google Scholar 

  • Sackett DL, Strauss SE, Richardson WS, Rosenberg W, Haynes RB (2000) Evidence-based medicine: how to practice and teach EBM. Churchill-Livingstone, London

    Google Scholar 

  • Schneider A, Schwarzbach J, Faderl B, Welker L, Karsch-Völk M, Jörres RA (2013) FENO measurement and sputum analysis for diagnosing asthma in clinical practice. Respir Med 107:209–216

    Article  Google Scholar 

  • Schürch S, Gehr P (1990) Im Hof V, Geiser M, Green F. Surfactant displaces particles toward the epithelium in airways and alveoli. Respir Physiol 80:17–32

    Article  Google Scholar 

  • Slebos DJ, Ryter SW, Choi AM (2003) Heme oxygenase-1 and carbon monoxide in pulmonary medicine. Respir Res 4:7–10

    Article  Google Scholar 

  • Stark M, Lerman Y, Kapel A, Pardo A, Schwarz Y, Newman L et al (2014) Biological exposure metrics of beryllium-exposed dental technicians. Arch Environ Occup Health 69:89–99

    Article  Google Scholar 

  • Steinvil A, Fireman E, Kordova-Biezuner L, Cohen M, Shapira I, Berliner S et al (2009) Environmental air pollution has decremental effects on pulmonary function test parameters up to one week after exposure. Am J Med Sci 338:4273–4279

    Article  Google Scholar 

  • Suttner DM, Dennery PA (1999) Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 13:1800–1809

    CAS  Google Scholar 

  • Tsoumakidou M, Tzanakis N, Chrysofakis G, Siafakas NM (2005) Nitrosative stress, heme oxygenase-1 expression and airway inflammation during severe exacerbations of COPD. Chest 127:1911–1918

    Article  CAS  Google Scholar 

  • Turner MO, Johnston PR, Pizzichini E, Pizzichini MM, Hussack PA, Hargreave FE (1998) Anti-inflammatory effects of salmeterol compared with beclomethasone in eosinophilic mild exacerbations of asthma: a randomized, placebo controlled trial. Can Respir J 5:261

    CAS  Google Scholar 

  • Vawda S, Mansour R, Takeda A, Funnell P, Kerry S, Mudway I et al (2013) Associations between inflammatory and immune response genes and adverse respiratory outcomes following exposure to outdoor air pollution: a HuGE systematic review. Am J Epidemiol 179:432–442

    Article  Google Scholar 

  • Walford HH, Doherty TA (2014) Diagnosis and management of eosinophilic asthma: a US perspective J Asthma. Allergy 7:53–65

    Google Scholar 

  • Wang F, He XY, Baines KJ, Gunawardhana LP, Simpson JL, Li F, Gibson PG (2011) Different inflammatory phenotypes in adults and children with acute asthma. Eur Respir J 38:567–574

    Article  CAS  Google Scholar 

  • Wardlaw AJ, Brightling C, Green R, Woltmann G, Pavord I (2000) Eosinophils in asthma and other allergic diseases. Br Med Bull 56:985–1003

    Article  CAS  Google Scholar 

  • Watt AP, Courtney J (2005) Moore, Ennis M, Elborn JS. Neutrophil cell death, activation and bacterial infection in cystic fibrosis. Thorax 60:659–664

    Article  CAS  Google Scholar 

  • Wright RJ, Kelly BJ (2013) Programming of respiratory health in childhood: influence of outdoor air pollution. Curr Opin Pediatr 25:232–239

    Article  CAS  Google Scholar 

  • Yeatts K, Svendsen E, Creason J, Alexis N, Herbst M, Scott J et al (2007) Coarse particulate matter (PM2.5-10) affects heart rate variability, blood lipids, and circulating eosinophils in adults with asthma. Environ Health Perspect 115:709–714

    Article  CAS  Google Scholar 

  • Yet SF, Melo LG, Layne MD, Perrella MA (2002) Heme oxygenase 1 in regulation of inflammation and oxidative damage. Methods Enzymol 353:163–176

    Article  CAS  Google Scholar 

  • Zhou H, Lu F, Latham C, Zander DS, Visner GA (2004) Heme oxygenase-1 expression in human lungs with cystic fibrosis and cytoprotective effects against Pseudomonas aeruginosa in vitro. Am J Respir Crit Care Med 170:633–640

    Article  Google Scholar 

Download references

Acknowledgments

Esther Eshkol is thanked for editorial assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elizabeth Fireman.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fireman, E., Bliznuk, D., Schwarz, Y. et al. Biological monitoring of particulate matter accumulated in the lungs of urban asthmatic children in the Tel-Aviv area. Int Arch Occup Environ Health 88, 443–453 (2015). https://doi.org/10.1007/s00420-014-0972-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00420-014-0972-3

Keywords

Navigation