Skip to main content
SpringerLink
Log in

The effect of PM2.5-related hazards on biomarkers of bronchial epithelial cells (A549) inflammation in Karaj and Fardis cities

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Fine particles (especially PM2.5 particles) in ambient air can cause irreversible effects on human health. In the present study, seasonal variations in toxicity PM2.5 (cell viability and release of pro-inflammatory cytokines) were exposed human lung cells (A549) to concentrations of PM2.5 samples in summer (sPM2.5) and winter (wPM2.5) seasons. Cells were separately exposed to three concentrations of PM2.5 (25, 50, and 100 μg/mL) and three times (12 h, 1 and 2 days). We evaluated cell viability by MTT assay [3- (4, 5-dimethylthiazol-2-yl) -2, 5-diphenyltetrazolium bromide] and liberation of pro-inflammatory cytokines (interleukin-6 and interleukin-8) by the ELISA method. The toxicological results of this study showed that increasing the concentration of PM2.5 particulates and contact time with it reduces cell viability and increases inflammatory responses. Seasonal cytotoxicity of PM2.5 particles in high-traffic areas at summer season compared to winter season was lower. The lowest percent of viability at 2 days of exposure and 100 μg/mL exposure in the winter sample was observed. Also, PM2.5 particles were influential in the amount of interleukins 8 and 6. The average release level of IL-6 and IL-8 in the cold season (winter) and the enormous exposure time and concentrations (2 days–100 μg/mL) was much higher than in the hot season (summer). These values were twice as high for winter PM2.5 samples as for summer samples. The compounds in PM2.5 at different seasons can cause some biological effects. The samples’ chemical characteristics in two seasons displayed that the PMs were diverse in chemical properties. In general, heavy metals and polycyclic aromatic hydrocarbons were more in the winter samples. However, the samples of wPM2.5 had a lower mass quota of metals such as aluminum, iron, copper, zinc, and magnesium. Concentrations of chromium, cadmium, arsenic, mercury, nickel, and lead were more significant in the sample of wPM2.5.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Amarloei A, Fazlzadeh M, Jafari AJ, Zarei A, Mazloomi S (2020) Particulate matters and bioaerosols during Middle East dust storms events in Ilam, Iran. Microchem J 152:104280

    CAS  Google Scholar 

  • Arfaeinia H, Moradi M, Sharafi K, Mahdi Esfahan N, Dobaradaran S (2015) Evaluation of public health impacts related to urban air pollution in Shiraz and Bushehr, Iran. Int J Pharm Technol 7:9811–9824

  • Atafar Z, Pourpak Z, Yunesian M, Nicknam MH, Hassanvand MS, Soleimanifar N, Saghafi S, Alizadeh Z, Rezaei S, Ghanbarian M, Ghozikali MG, Osornio-Vargas AR, Naddafi K (2019) Proinflammatory effects of dust storm and thermal inversion particulate matter (PM10) on human peripheral blood mononuclear cells (PBMCs) in vitro: a comparative approach and analysis. J Environ Health Sci Eng 17:433–444

    CAS  Google Scholar 

  • Bi C, Chen Y, Zhao Z, Li Q, Zhou Q, Ye Z, Ge X (2020) Characteristics, sources and health risks of toxic species (PCDD/Fs, PAHs and heavy metals) in PM2. 5 during fall and winter in an industrial area. Chemosphere 238:124620

    CAS  Google Scholar 

  • Chen Y, Luo XS, Zhao Z, Chen Q, Wu D, Sun X, Wu L, Jin L (2018) Summer-winter differences of PM2.5 toxicity to human alveolar epithelial cells (A549) and the roles of transition metals. Ecotoxicol Environ Saf 165:505–509

    CAS  Google Scholar 

  • Chen Q, Luo X-S, Chen Y, Zhao Z, Hong Y, Pang Y, Huang W, Wang Y, Jin L (2019) Seasonally varied cytotoxicity of organic components in PM2. 5 from urban and industrial areas of a Chinese megacity. Chemosphere 230:424–431

    CAS  Google Scholar 

  • Dabass A, Talbott EO, Rager JR, Marsh GM, Venkat A, Holguin F, Sharma RK (2018) Systemic inflammatory markers associated with cardiovascular disease and acute and chronic exposure to fine particulate matter air pollution (PM2. 5) among US NHANES adults with metabolic syndrome. Environ Res 161:485–491

    CAS  Google Scholar 

  • Dai Q-L, Bi X-H, Wu J-H, Zhang Y-F, Wang J, Xu H, Yao L, Jiao L, Feng Y-C (2014) Characterization and source identification of heavy metals in ambient PM10 and PM2. 5 in an integrated iron and steel industry zone compared with a background site. Aerosol Air Qual Res 15:875–887

    Google Scholar 

  • Dehghani MH, Jarahzadeh S, Hadei M, Mansouri N, Rashidi Y, Yousefi M (2018) The data on the dispersion modeling of traffic-related PM10 and CO emissions using CALINE3; A case study in Tehran, Iran. Data in brief 19:2284–2290

    Google Scholar 

  • Dehghani S, Fararouei M, Rafiee A, Hoepner L, Oskoei V, Hoseini M (2022) Prenatal exposure to polycyclic aromatic hydrocarbons and effects on neonatal anthropometric indices and thyroid-stimulating hormone in a Middle Eastern population. Chemosphere 286:131605

    CAS  Google Scholar 

  • Eapen MS, Myers S, Walters EH, Sohal SS (2017) Airway inflammation in chronic obstructive pulmonary disease (COPD): a true paradox. Expert Rev Respir Med 11:827–839

    CAS  Google Scholar 

  • Fu H, Liu X, Li W, Zu Y, Zhou F, Shou Q, Ding Z (2020) PM2.5 Exposure induces inflammatory response in macrophages via the TLR4/COX-2/NF-kappaB pathway. Inflammation 43:1948–1958

    CAS  Google Scholar 

  • Gualtieri M, Ovrevik J, Holme JA, Perrone MG, Bolzacchini E, Schwarze PE, Camatini M (2010a) Differences in cytotoxicity versus pro-inflammatory potency of different PM fractions in human epithelial lung cells. Toxicol in Vitro 24:29–39

    CAS  Google Scholar 

  • Gualtieri M, Øvrevik J, Holme JA, Perrone MG, Bolzacchini E, Schwarze PE, Camatini M (2010b) Differences in cytotoxicity versus pro-inflammatory potency of different PM fractions in human epithelial lung cells. Toxicol in Vitro 24:29–39

    CAS  Google Scholar 

  • Guo H, Gu X, Ma G, Shi S, Wang W, Zuo X, Zhang X (2019) Spatial and temporal variations of air quality and six air pollutants in China during 2015–2017. Sci Rep 9:1–11

    Google Scholar 

  • Hadei M, Hopke PK, Nazari SSH, Yarahmadi M, Shahsavani A, Alipour MR (2017) Estimation of mortality and hospital admissions attributed to criteria air pollutants in Tehran metropolis, Iran (2013-2016). Aerosol Air Qual Res 17:2474–2481

    CAS  Google Scholar 

  • Haghnazari L, Mirzaei N, Arfaeinia H, Karimyan K, Sharafi H, Fattahi N (2018) Speciation of As (ΙΙΙ)/As (V) and total inorganic arsenic in biological fluids using new mode of liquid-phase microextraction and electrothermal atomic absorption spectrometry. Biol Trace Elem Res 183:173–181

    CAS  Google Scholar 

  • Hajizadeh Y, Mokhtari M, Faraji M, Abdolahnejad A, Mohammadi A (2019) Biomonitoring of airborne metals using tree leaves: protocol for biomonitor selection and spatial trend. MethodsX 6:1694–1700

    Google Scholar 

  • Hajizadeh Y, Jafari N, Mohammadi A, Momtaz SM, Fanaei F, Abdolahnejad A (2020) Concentrations and mortality due to short-and long-term exposure to PM 2.5 in a megacity of Iran (2014–2019). Environ Sci Pollut Res 27:38004–38014

    CAS  Google Scholar 

  • Hassanvand MS, Naddafi K, Faridi S, Nabizadeh R, Sowlat MH, Momeniha F, Gholampour A, Arhami M, Kashani H, Zare A (2015) Characterization of PAHs and metals in indoor/outdoor PM10/PM2. 5/PM1 in a retirement home and a school dormitory. Sci Total Environ 527:100–110

    Google Scholar 

  • Heydari G, Taghizdeh F, Fazlzadeh M, Jafari AJ, Asadgol Z, Mehrizi EA, Moradi M, Arfaeinia H (2019) Levels and health risk assessments of particulate matters (PM 2.5 and PM 10) in indoor/outdoor air of waterpipe cafés in Tehran, Iran. Environ Sci Pollut Res 26:7205–7215

    CAS  Google Scholar 

  • Hoseini M, Yunesian M, Nabizadeh R, Yaghmaeian K, Ahmadkhaniha R, Rastkari N, Parmy S, Faridi S, Rafiee A, Naddafi K (2016) Characterization and risk assessment of polycyclic aromatic hydrocarbons (PAHs) in urban atmospheric Particulate of Tehran, Iran. Environ Sci Pollut Res Int 23:1820–1832

    CAS  Google Scholar 

  • Huebert BJ, Ming-Xing W, WEI-XIU L (1988) Atmospheric nitrate, sulfate, ammonium and calcium concentrations in China. Tellus B 40:260–269

    Google Scholar 

  • Huremović J, Žero S, Bubalo E, Dacić M, Čeliković A, Musić I, Bašić M, Huseinbašić N, Džepina K, Cepić M, Muratović N, Pašalić A, Salihagić S, Krvavac Z, Zelić-Hadžiomerović J, Gojak-Salimović S (2020) Analysis of PM10, Pb, Cd, and Ni atmospheric concentrations during domestic heating season in Sarajevo, Bosnia and Herzegovina, from 2010 to 2019. Air Qual Atmos Health 13:965–976

    Google Scholar 

  • Jiang N, Liu X, Wang S, Yu X, Yin S, Duan S, Wang S, Zhang R, Li S (2019) Pollution characterization, source identification, and health risks of atmospheric-particle-bound heavy metals in PM10 and PM2.5 at multiple sites in an emerging megacity in the central region of China. Aerosol Air Qual Res 19:247–271

    CAS  Google Scholar 

  • Jordanova D, Jordanova N, Lanos P, Petrov P, Tsacheva T (2012) Magnetism of outdoor and indoor settled dust and its utilization as a tool for revealing the effect of elevated particulate air pollution on cardiovascular mortality. Geochemistry, Geophysics, Geosystems 13:Q08Z49. https://doi.org/10.1029/2012GC004160

  • Karbasdehi VN, Dobaradaran S, Nabipour I, Arfaeinia H, Mirahmadi R, Keshtkar M (2016) Data on metal contents (As, Ag, Sr, Sn, Sb, and Mo) in sediments and shells of Trachycardium lacunosum in the northern part of the Persian Gulf. Data in brief 8:966–971

    Google Scholar 

  • Kermani M, Arfaeinia H, Masroor K, Abdolahnejad A, Fanaei F, Shahsavani A, Tahmasbizadeh M, Vahidi MH (2020) Health impacts and burden of disease attributed to long-term exposure to atmospheric PM10/PM2. 5 in Karaj, Iran: effect of meteorological factors. Int J Environ Anal Chem:1–17. https://doi.org/10.1080/03067319.2020.1807534

  • Kermani M, Jafari AJ, Gholami M, Arfaeinia H, Shahsavani A, Fanaei F (2021a) Characterization, possible sources and health risk assessment of PM2. 5-bound Heavy metals in the most industrial city of Iran. J Environ Health Sci Eng 19:151–163

  • Kermani M, Jonidi Jafari A, Gholami M, Taghizadeh F, Masroor K, Abdolahnejad A, Shahsavani A, Fanaei F (2021b) Characterisation of PM2. 5–bound PAHs in outdoor air of Karaj megacity: the effect of meteorological factors. Int J Environ Anal Chem:1–19. https://doi.org/10.1080/03067319.2021.1906425

  • Kocbach A, Herseth JI, Låg M, Refsnes M, Schwarze PE (2008) Particles from wood smoke and traffic induce differential pro-inflammatory response patterns in co-cultures. Toxicol Appl Pharmacol 232:317–326

    CAS  Google Scholar 

  • Kurosaki Y, Mikami M (2003) Recent frequent dust events and their relation to surface wind in East Asia. Geophys Res Lett 30 (14):1736–1739

  • Lim J-M, Lee J-H, Moon J-H, Chung Y-S, Kim K-H (2010) Source apportionment of PM10 at a small industrial area using positive matrix factorization. Atmos Res 95:88–100

    CAS  Google Scholar 

  • Liu Q, Baumgartner J, Zhang Y, Schauer JJ (2016a) Source apportionment of Beijing air pollution during a severe winter haze event and associated pro-inflammatory responses in lung epithelial cells. Atmos Environ 126:28–35

    CAS  Google Scholar 

  • Liu X, Li C, Tu H, Wu Y, Ying C, Huang Q, Wu S, Xie Q, Yuan Z, Lu Y (2016b) Analysis of the effect of meteorological factors on PM2. 5-associated PAHs during autumn-winter in urban Nanchang. Aerosol Air Qual Res 16:3222–3229

    CAS  Google Scholar 

  • Liu J, Chen Y, Chao S, Cao H, Zhang A, Yang Y (2018) Emission control priority of PM2. 5-bound heavy metals in different seasons: a comprehensive analysis from health risk perspective. Sci Total Environ 644:20–30

    CAS  Google Scholar 

  • Longhin E, Holme JA, Gualtieri M, Camatini M, Ovrevik J (2018) Milan winter fine particulate matter (wPM2.5) induces IL-6 and IL-8 synthesis in human bronchial BEAS-2B cells, but specifically impairs IL-8 release. Toxicol in Vitro 52:365–373

    CAS  Google Scholar 

  • Luo X, Zhao Z, Xie J, Luo J, Chen Y, Li H, Jin L (2019) Pulmonary bioaccessibility of trace metals in PM2. 5 from different megacities simulated by lung fluid extraction and DGT method. Chemosphere 218:915–921

    CAS  Google Scholar 

  • Lyu Y, Su S, Wang B, Zhu X, Wang X, Zeng EY, Xing B, Tao S (2018) Seasonal and spatial variations in the chemical components and the cellular effects of particulate matter collected in Northern China. Sci Total Environ 627:1627–1637

    CAS  Google Scholar 

  • MohseniBandpi A, Eslami A, Shahsavani A, Khodagholi F, Alinejad A (2017) Physicochemical characterization of ambient PM2.5 in Tehran air and its potential cytotoxicity in human lung epithelial cells (A549). Sci Total Environ 593-594:182–190

    CAS  Google Scholar 

  • Nabizadeh R, Yousefi M, Azimi F (2018) Study of particle number size distributions at Azadi terminal in Tehran, comparing high-traffic and no traffic area. MethodsX 5:1549–1555

    Google Scholar 

  • Ndong Ba A, Cazier F, Verdin A, Garcon G, Cabral M, Courcot L, Diouf A, Courcot D, Gualtieri M, Fall M (2019) Physico-chemical characterization and in vitro inflammatory and oxidative potency of atmospheric particles collected in Dakar city’s (Senegal). Environ Pollut 245:568–581

    CAS  Google Scholar 

  • Niu X, Ho SSH, Ho KF, Huang Y, Sun J, Wang Q, Zhou Y, Zhao Z, Cao J (2017) Atmospheric levels and cytotoxicity of polycyclic aromatic hydrocarbons and oxygenated-PAHs in PM2. 5 in the Beijing-Tianjin-Hebei region. Environ Pollut 231:1075–1084

    CAS  Google Scholar 

  • Pehnec G, Jakovljevic I (2018) Carcinogenic potency of airborne polycyclic aromatic hydrocarbons in relation to the particle fraction size. Int J Environ Res Public Health 15(11):2485

  • Qishlaqi A, Beiramali F (2019) Potential sources and health risk assessment of polycyclic aromatic hydrocarbons in street dusts of Karaj urban area, northern Iran. J Environ Health Sci Eng 17:1029–1044

  • Rai P, Chakraborty A, Mandariya AK, Gupta T (2016) Composition and source apportionment of PM1 at urban site Kanpur in India using PMF coupled with CBPF. Atmos Res 178:506–520

    Google Scholar 

  • Ramgolam K, Chevaillier S, Marano F, Baeza-Squiban A, Martinon L (2008) Proinflammatory effect of fine and ultrafine particulate matter using size-resolved urban aerosols from Paris. Chemosphere 72:1340–1346

    CAS  Google Scholar 

  • Roig N, Sierra J, Rovira J, Schuhmacher M, Domingo JL, Nadal M (2013) In vitro tests to assess toxic effects of airborne PM10 samples Correlation with metals and chlorinated dioxins and furans. Sci Total Environ 443:791–797

    CAS  Google Scholar 

  • Sajjadi SA, Atarodi Z, Lotfi AH, Zarei A (2018) Levels of particulate matters in air of the Gonabad city, Iran. MethodsX 5:1534–1539

    Google Scholar 

  • Schilirò T, Bonetta S, Alessandria L, Gianotti V, Carraro E, Gilli G (2015) PM10 in a background urban site: chemical characteristics and biological effects. Environ Toxicol Pharmacol 39:833–844

    Google Scholar 

  • Schwartz C, Bølling AK, Carlsten C (2020) Controlled human exposures to wood smoke: a synthesis of the evidence. Particle and fibre toxicology 17:1–17

    Google Scholar 

  • Soleimani M, Amini N, Sadeghian B, Wang D, Fang L (2018) Heavy metals and their source identification in particulate matter (PM2. 5) in Isfahan City, Iran. J Environ Sci 72:166–175

    CAS  Google Scholar 

  • Sowlat MH, Naddafi K, Yunesian M, Jackson PL, Shahsavani A (2012) Source apportionment of total suspended particulates in an arid area in southwestern Iran using positive matrix factorization. Bull Environ Contam Toxicol 88:735–740

    CAS  Google Scholar 

  • Torkashvand J, Jafari AJ, Hopke PK, Shahsavani A, Hadei M, Kermani M (2021) Airborne particulate matter in Tehran’s ambient air. J Environ Health Sci Eng 19:1179–1191

    CAS  Google Scholar 

  • Vahidi MH, Fanaei F, Kermani M (2020) Long-term health impact assessment of PM2. 5 and PM10: Karaj, Iran. International Journal of Environmental Health Engineering 9:8

    CAS  Google Scholar 

  • Wang F, Guo Z, Lin T, Rose NL (2016) Seasonal variation of carbonaceous pollutants in PM2.5 at an urban ‘supersite’ in Shanghai, China. Chemosphere 146:238–244

    CAS  Google Scholar 

  • Wang F, Wang J, Han M, Jia C, Zhou Y (2019a) Heavy metal characteristics and health risk assessment of PM2. 5 in students’ dormitories in a university in Nanjing, China. Build Environ 160:106206

    Google Scholar 

  • Wang J, Zhang WJ, Xiong W, Lu WH, Zheng HY, Zhou X, Yuan J (2019b) PM2.5 stimulated the release of cytokines from BEAS-2B cells through activation of IKK/NF-kappaB pathway. Hum Exp Toxicol 38:311–320

    CAS  Google Scholar 

  • Yang H-H, Lee W-J, Chen S-J, Lai S-O (1998) PAH emission from various industrial stacks. J Hazard Mater 60:159–174

    CAS  Google Scholar 

  • Yang H-H, Lai S-O, Hsieh L-T, Hsueh H-J, Chi T-W (2002) Profiles of PAH emission from steel and iron industries. Chemosphere 48:1061–1074

    CAS  Google Scholar 

  • Yin X, Sun Z, Miao S, Yan Q, Wang Z, Shi G, Li Z, Xu W (2019) Analysis of abrupt changes in the PM2.5 concentration in Beijing during the conversion period from the summer to winter half-year in 2006–2015. Atmos Environ 200:319–328

    CAS  Google Scholar 

  • Yunesian M, Rostami R, Zarei A, Fazlzadeh M, Janjani H (2019) Exposure to high levels of PM2. 5 and PM10 in the metropolis of Tehran and the associated health risks during 2016–2017. Microchem J 150:104174

    CAS  Google Scholar 

  • Zhang HH, Li Z, Liu Y, Xinag P, Cui XY, Ye H, Hu BL, Lou LP (2018) Physical and chemical characteristics of PM2.5 and its toxicity to human bronchial cells BEAS-2B in the winter and summer. J Zhejiang Univ Sci B 19:317–326

    CAS  Google Scholar 

Download references

Funding

The authors received support of this work from the Iran University of Medical Sciences, Tehran, Iran (Grant Number:98-3-37-16392) (Ethics Code: IR.IUMS.REC.1398.949).

Author information

Authors and Affiliations

  1. Research Center for Environmental Health Technology, Iran University of Medical Sciences, Tehran, Iran

    Tahereh Rahmatinia, Majid Kermani, Mahdi Farzadkia, Ahmad Jonidi Jafari & Farzad Fanaei

  2. Department of Environmental Health Engineering, School of Public Health, Iran University of Medical Sciences, Tehran, Iran

    Tahereh Rahmatinia, Majid Kermani, Mahdi Farzadkia, Ahmad Jonidi Jafari & Farzad Fanaei

  3. Immunology Research Center, Institute of Immunology and Infectious Diseases, Iran University of Medical Sciences, Tehran, Iran

    Ali-Akbar Delbandi & Nesa Rashidi

  4. Department of Immunology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

    Ali-Akbar Delbandi & Nesa Rashidi

Authors
  1. Tahereh Rahmatinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Majid Kermani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahdi Farzadkia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ahmad Jonidi Jafari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ali-Akbar Delbandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nesa Rashidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Farzad Fanaei
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Tahereh Rahmatinia: investigation, writing - original draft writing – review & editing. Farzad Fanaei: Sampling, writing. Majid Kermani: Supervision, writing – review & editing. Nesa Rashidi: sampling, writing. Ahmad Jonidi Jafari: writing – editing. Mahdi Farzadkia and Ali-Akbar Delbandi: writing – review & editing.

Corresponding authors

Correspondence to Majid Kermani or Farzad Fanaei.

Ethics declarations

Ethics approval

The authors of this article have covered all the ethical points, including non-plagiarism, duplicate publishing, data distortion, and data creation in this article. This project has been registered in Iran University of Medical Sciences with the code of ethics of IR.IUMS.REC.1398.949.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Lotfi Aleya

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahmatinia, ., Kermani, M., Farzadkia, M. et al. The effect of PM2.5-related hazards on biomarkers of bronchial epithelial cells (A549) inflammation in Karaj and Fardis cities. Environ Sci Pollut Res 29, 2172–2182 (2022). https://doi.org/10.1007/s11356-021-15723-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-15723-3

Keywords

Search

Navigation