Allergy Asthma Immunol Res.  2019 Sep;11(5):632-643. 10.4168/aair.2019.11.5.632.

Short-term Haze Exposure Predisposes Healthy Volunteers to Nasal Inflammation

Affiliations
  • 1Beijing Institute of Otolaryngology, Department of Otolaryngology Head and Neck Surgery, Beijing TongRen Hospital, Capital Medical University, Beijing, China. dr.luozhang@139.com, wangcs830@126.com
  • 2Beijing Key Laboratory of Nasal Diseases, Beijing Institute of Otolaryngology, Beijing, China.

Abstract

PURPOSE
This study aimed to investigate the impact of short-term haze exposure on nasal inflammation in healthy volunteers.
METHODS
Thirty-three healthy university students were assessed for nasal symptoms, nasal patency, upper and lower respiratory tract nitric oxide (NO) as well as inflammatory mediators and neuropeptides in nasal secretions before and after a 5-day haze episode. Peripheral blood mononuclear cells (PBMCs) were stimulated with particulate matter with an aerodynamic diameter of less than 2.5 μm (PM(2.5)), and cytokines in the supernatants were examined.
RESULTS
Mild nasal symptoms were reported by some participants during the haze episode. Objective measures of nasal patency demonstrated that nasal airway resistance was significantly increased from baseline levels, while nasal cavity volume and minimum cross-sectional area were significantly decreased. Similarly, the levels of nasal and exhaled NO, eotaxin, interleukin (IL)-5, chemokine (C-C motif) ligand 17, IL-8, substance P, nerve growth factor and vasoactive intestinal peptides in nasal secretions were significantly increased from baseline values following the haze episode. In contrast, the levels of interferon-γ, IL-10, transforming growth factor-β and neuropeptide Y were significantly decreased. Incubation with 0.1-10 μg/mL PM(2.5) significantly increased release of IL-1β, IL-4, IL-5, IL-8 and IL-10 from PBMCs.
CONCLUSIONS
Short-term haze exposure may lead to nasal inflammation and hypersensitivity in healthy subjects predominantly by Th2 cytokine-mediated immune responses.

Keyword

Air pollution; particulate matter; nasal inflammation; cytokines; neuropeptides

MeSH Terms

Air Pollution
Airway Resistance
Cytokines
Healthy Volunteers*
Humans
Hypersensitivity
Inflammation*
Interleukin-10
Interleukin-4
Interleukin-5
Interleukin-8
Interleukins
Nasal Cavity
Nerve Growth Factor
Neuropeptide Y
Neuropeptides
Nitric Oxide
Particulate Matter
Peptides
Respiratory System
Substance P
Cytokines
Interleukin-10
Interleukin-4
Interleukin-5
Interleukin-8
Interleukins
Nerve Growth Factor
Neuropeptide Y
Neuropeptides
Nitric Oxide
Particulate Matter
Peptides
Substance P

Figure

  • Fig. 1 Time course of 24-hour mean air pollutant concentration in Beijing between March 17th and 29th of 2014. The left Y axis stands for ambient PM2.5, PM10, SO2, NO2 and O3 (µg/m3); the right Y axis stands for ambient CO (mg/m3). Visits 1 and 2 took place on March 22nd and March 29th, respectively. Before the baseline visit the 24-hour mean PM2.5 concentration was lower than 100 µg/m3 for 5 consecutive days, whereas before the second visit, Beijing had experienced a haze episode for 5 consecutive days with 24-hour mean PM2.5 concentration higher than 100 µg/m3.

  • Fig. 2 Changes in nasal patency in each subject before and during the haze episode. (A) NAR, (B) total NCV and (C) MCA (n=33 for each experiment). NAR, nasal airway resistance; NCV, nasal cavity volume; MCA, minimum cross-sectional area.

  • Fig. 3 Change in (A) nNO and (B) eNO concentrations in each subject before and during the haze episode (n=33 for each experiment). nNO, nasal nitric oxide; eNO, exhaled nitric oxide.

  • Fig. 4 Changes in inflammatory cytokines concentration (pg/mL) in nasal secretions of the participants before and during the haze episode. (A) eotaxin, (B) IL-5, (C) CCL17, (D) IL-8, (E) IFN-γ, (F) IL-10, (G) TGF-β1, (H) TGF-β2 and (I) IL-17 (n=33 for each experiment). IL, interleukin; CCL17, chemokine (C-C motif) ligand 17; IFN, interferon; TGF, transforming growth factor; NS, not significant.

  • Fig. 5 Changes in neuropeptide concentration (pg/mL) in nasal secretions of the participants before and during the haze episode. (A) SP, (B) NGF, (C) VIP and (D) NPY (n=33 for each experiment). SP, substance P; NGF, nerve growth factor; VIP, vasoactive intestinal peptide; NPY, neuropeptide Y.

  • Fig. 6 Concentrations (pg/mL) of inflammatory cytokines in supernatants of peripheral blood mononuclear cells exposed to phosphate-buffered saline (0 mg/mL), 0.1 mg/mL PM2.5 or 10 mg/mL PM2.5. (A) IL-4, (B) IL-5, (C) IL-1β, (D) IL-8 and (E) IL-10 (n=8 for each experiment). Data on cytokines (IL-13, IL-17A, IL-33, eotaxin, transforming growth factor-βs and IFN-γ), which were not significantly affected by different doses of PM2.5, were not provided here. IL, interleukin; IFN, interferon; NS, not significant. *P < 0.05, **P < 0.01, ***P< 0.001.


Reference

1. Xu P, Chen Y, Ye X. Haze, air pollution, and health in China. Lancet. 2013; 382:2067.
Article
2. Jin Q, Fang X, Wen B, Shan A. Spatio-temporal variations of PM2.5 emission in China from 2005 to 2014. Chemosphere. 2017; 183:429–436.
Article
3. Li M, Zhang L. Haze in China: current and future challenges. Environ Pollut. 2014; 189:85–86.
Article
4. Guan WJ, Zheng XY, Chung KF, Zhong NS. Impact of air pollution on the burden of chronic respiratory diseases in China: time for urgent action. Lancet. 2016; 388:1939–1951.
Article
5. Keleş N, Ilicali C. The impact of outdoor pollution on upper respiratory diseases. Rhinology. 1998; 36:24–27.
6. Zhang Y, Zhang L. Prevalence of allergic rhinitis in china. Allergy Asthma Immunol Res. 2014; 6:105–113.
Article
7. Chen F, Lin Z, Chen R, Norback D, Liu C, Kan H, et al. The effects of PM2.5 on asthmatic and allergic diseases or symptoms in preschool children of six Chinese cities, based on China, children, homes and health (CCHH) project. Environ Pollut. 2018; 232:329–337.
Article
8. Stevens WW, Lee RJ, Schleimer RP, Cohen NA. Chronic rhinosinusitis pathogenesis. J Allergy Clin Immunol. 2015; 136:1442–1453.
Article
9. Ramanathan M Jr, London NR Jr, Tharakan A, Surya N, Sussan TE, Rao X, et al. Airborne particulate matter induces nonallergic eosinophilic sinonasal inflammation in mice. Am J Respir Cell Mol Biol. 2017; 57:59–65.
Article
10. Chen Y, Wong GW, Li J. Environmental exposure and genetic predisposition as risk factors for asthma in China. Allergy Asthma Immunol Res. 2016; 8:92–100.
Article
11. Guarnieri M, Balmes JR. Outdoor air pollution and asthma. Lancet. 2014; 383:1581–1592.
Article
12. Ni L, Chuang CC, Zuo L. Fine particulate matter in acute exacerbation of COPD. Front Physiol. 2015; 6:294.
Article
13. Krämer U, Koch T, Ranft U, Ring J, Behrendt H. Traffic-related air pollution is associated with atopy in children living in urban areas. Epidemiology. 2000; 11:64–70.
Article
14. Watelet JB, Gevaert P, Holtappels G, Van Cauwenberge P, Bachert C. Collection of nasal secretions for immunological analysis. Eur Arch Otorhinolaryngol. 2004; 261:242–246.
Article
15. World Health Organization, Regional Office for Europe. Air quality guidelines global update 2005: particulate matter, ozone, nitrogen dioxide and sulfur dioxide. Copenhagen: WHO Regional Office for Europe;2006.
16. Inoue Y, Sato S, Manabe T, Makita E, Chiyotanda M, Takahashi K, et al. Measurement of exhaled nitric oxide in children: a comparison between NObreath® and NIOX VERO® analyzers. Allergy Asthma Immunol Res. 2018; 10:478–489.
Article
17. American Thoracic Society. European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med. 2005; 171:912–930.
18. Scarpa MC, Kulkarni N, Maestrelli P. The role of non-invasive biomarkers in detecting acute respiratory effects of traffic-related air pollution. Clin Exp Allergy. 2014; 44:1100–1118.
Article
19. Nightingale JA, Rogers DF, Barnes PJ. Effect of inhaled ozone on exhaled nitric oxide, pulmonary function, and induced sputum in normal and asthmatic subjects. Thorax. 1999; 54:1061–1069.
Article
20. Olin AC, Stenfors N, Torén K, Blomberg A, Helleday R, Ledin MC, et al. Nitric oxide (NO) in exhaled air after experimental ozone exposure in humans. Respir Med. 2001; 95:491–495.
Article
21. Biewenga J, Stoop AE, Baker HE, Swart SJ, Nauta JJ, van Kamp GJ, et al. Nasal secretions from patients with polyps and healthy individuals, collected with a new aspiration system: evaluation of total protein and immunoglobulin concentrations. Ann Clin Biochem. 1991; 28:260–266.
Article
22. Steerenberg PA, Nierkens S, Fischer PH, van Loveren H, Opperhuizen A, Vos JG, et al. Traffic-related air pollution affects peak expiratory flow, exhaled nitric oxide, and inflammatory nasal markers. Arch Environ Health. 2001; 56:167–174.
Article
23. Barraza-Villarreal A, Sunyer J, Hernandez-Cadena L, Escamilla-Nuñez MC, Sienra-Monge JJ, Ramírez-Aguilar M, et al. Air pollution, airway inflammation, and lung function in a cohort study of Mexico City schoolchildren. Environ Health Perspect. 2008; 116:832–838.
Article
24. Romieu I, Barraza-Villarreal A, Escamilla-Nuñez C, Almstrand AC, Diaz-Sanchez D, Sly PD, et al. Exhaled breath malondialdehyde as a marker of effect of exposure to air pollution in children with asthma. J Allergy Clin Immunol. 2008; 121:903–909.e6.
Article
25. Wu W, Peden DB, McConnell R, Fruin S, Diaz-Sanchez D. Glutathione-S-transferase M1 regulation of diesel exhaust particle-induced pro-inflammatory mediator expression in normal human bronchial epithelial cells. Part Fibre Toxicol. 2012; 9:31.
Article
26. Bernstein DI. Diesel exhaust exposure, wheezing and sneezing. Allergy Asthma Immunol Res. 2012; 4:178–183.
Article
27. Smarr CB, Bryce PJ, Miller SD. Antigen-specific tolerance in immunotherapy of Th2-associated allergic diseases. Crit Rev Immunol. 2013; 33:389–414.
Article
28. Wawrzyniak M, O'Mahony L, Akdis M. Role of regulatory cells in oral tolerance. Allergy Asthma Immunol Res. 2017; 9:107–115.
Article
29. Baraniuk JN, Lundgren JD, Okayama M, Goff J, Mullol J, Merida M, et al. Substance P and neurokinin A in human nasal mucosa. Am J Respir Cell Mol Biol. 1991; 4:228–236.
Article
30. Hanf G, Schierhorn K, Brunnée T, Noga O, Verges D, Kunkel G. Substance P induced histamine release from nasal mucosa of subjects with and without allergic rhinitis. Inflamm Res. 2000; 49:520–523.
Article
31. Kaliner MA. The physiology and pathophysiology of the parasympathetic nervous system in nasal disease: an overview. J Allergy Clin Immunol. 1992; 90:1044–1045.
Article
32. Kim DH, Park IH, Cho JS, Lee YM, Choi H, Lee HM. Alterations of vasoactive intestinal polypeptide receptors in allergic rhinitis. Am J Rhinol Allergy. 2011; 25:e44–7.
Article
33. Baraniuk JN, Castellino S, Lundgren JD, Goff J, Mullol J, Merida M, et al. Neuropeptide Y (NPY) in human nasal mucosa. Am J Respir Cell Mol Biol. 1990; 3:165–173.
Article
34. Raap U, Braunstahl GJ. The role of neurotrophins in the pathophysiology of allergic rhinitis. Curr Opin Allergy Clin Immunol. 2010; 10:8–13.
Article
35. Knipping S, Holzhausen HJ, Riederer A, Schrom T. Allergic and idiopathic rhinitis: an ultrastructural study. Eur Arch Otorhinolaryngol. 2009; 266:1249–1256.
Article
36. Sanico AM, Stanisz AM, Gleeson TD, Bora S, Proud D, Bienenstock J, et al. Nerve growth factor expression and release in allergic inflammatory disease of the upper airways. Am J Respir Crit Care Med. 2000; 161:1631–1635.
Article
37. Wang H, Song L, Ju W, Wang X, Dong L, Zhang Y, et al. The acute airway inflammation induced by PM2.5 exposure and the treatment of essential oils in Balb/c mice. Sci Rep. 2017; 7:44256.
Article
38. De Falco G, Colarusso C, Terlizzi M, Popolo A, Pecoraro M, Commodo M, et al. Chronic obstructive pulmonary disease-derived circulating cells release IL-18 and IL-33 under ultrafine particulate matter exposure in a caspase-1/8-independent manner. Front Immunol. 2017; 8:1415.
Article
39. Srivastava A, Sharma A, Yadav S, Flora SJ, Dwivedi UN, Parmar D. Gene expression profiling of candidate genes in peripheral blood mononuclear cells for predicting toxicity of diesel exhaust particles. Free Radic Biol Med. 2014; 67:188–194.
Article
40. Chen B, Lu S, Li S, Wang B. Impact of fine particulate fluctuation and other variables on Beijing's air quality index. Environ Sci Pollut Res Int. 2015; 22:5139–5151.
Article
41. Burte E, Leynaert B, Bono R, Brunekreef B, Bousquet J, Carsin AE, et al. Association between air pollution and rhinitis incidence in two European cohorts. Environ Int. 2018; 115:257–266.
Article
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