Skip to main content

Advertisement

SpringerLink
Log in

Associations between particulate matter air pollutants and hospitalization risk for systemic lupus erythematosus: a time-series study from Xi’an, China

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Air pollution exposure is an important environmental risk factor involved in the development of systemic lupus erythematosus (SLE). This study was conducted to investigate the relationships between particulate matter (PM) air pollutants exposure and the risk of SLE admission in Xi’an, China. The records of SLE admission, air pollutants and meteorological data were retrieved from the First Affiliated Hospital of Xi’an Jiaotong University, the Xi’an Environmental Monitoring Station and China Meteorological Data Network, respectively. A distributed lagged nonlinear model combined with Poisson generalized linear regression was used to evaluate the effect of air pollution on SLE admission. Exposure–response curves showed positive associations of PM ≤ 2.5 (PM2.5) and 10 microns (PM10) in aerodynamic diameter exposures with the risk of SLE admission. Subgroup analyses showed that PM2.5 exposure was associated with the increased risk of SLE admission in women, age over 65 years old, and during the cold season, and PM10 exposure showed an increased risk of SLE in women and during the cold season, but additional tests did not observe the significant associations of PM2.5 and PM10 exposure with SLE admission between subgroups. In addition, null associations of carbon monoxide (CO), nitrogen dioxide (NO2), ozone (O3), and sulfur dioxide (SO2) with the risk of SLE admission were found. Our study indicates that PM2.5 and PM10 exposures have significant effects on the risk of SLE admission, and early measures should be taken for high PM2.5 and PM10 exposure to protect vulnerable populations, rational use of limited health care resources.

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

The data and material that support the findings of this study are available upon reasonable request.

References

  • Adami, G., Pontalti, M., Cattani, G., Rossini, M., Viapiana, O., Orsolini, G., Benini, C., Bertoldo, E., Fracassi, E., Gatti, D., & Fassio, A. (2022). Association between long-term exposure to air pollution and immune-mediated diseases: A population-based cohort study. RMD Open, 8, e002055.

    Article  Google Scholar 

  • Ao, T., Kikuta, J., & Ishii, M. (2021). The effects of vitamin D on immune system and inflammatory diseases. Biomolecules, 11, 1624.

    Article  CAS  Google Scholar 

  • Azrielant, S., & Shoenfeld, Y. (2016). Eppur Si Muove: Vitamin D is essential in preventing and modulating SLE. Lupus, 25, 563–572.

    Article  CAS  Google Scholar 

  • Barbhaiya, M., & Costenbader, K. H. (2016). Environmental exposures and the development of systemic lupus erythematosus. Current Opinion in Rheumatology, 28, 497–505.

    Article  CAS  Google Scholar 

  • Bhaskaran, K., Gasparrini, A., Hajat, S., Smeeth, L., & Armstrong, B. (2013). Time series regression studies in environmental epidemiology. International Journal of Epidemiology, 42, 1187–1195.

    Article  Google Scholar 

  • Brugha, R., & Grigg, J. (2014). Urban air pollution and respiratory infections. Paediatric Respiratory Reviews, 15, 194–199.

    Article  Google Scholar 

  • Cakmak, S., Blanco-Vidal, C., Lukina, A. O., & Dales, R. (2021). The association between air pollution and hospitalization for patients with systemic lupus erythematosus in Chile: A daily time series analysis. Environmental Research, 192, 110469.

    Article  CAS  Google Scholar 

  • Chen, Y., He, Y. S., Feng, Y. T., Wu, Z. D., Wang, J., Yin, K. J., Huang, J. X., & Pan, H. F. (2022). The effect of air pollution exposure on risk of outpatient visits for Sjogren’s syndrome: A time-series study. Environmental Research, 214, 114017.

    Article  CAS  Google Scholar 

  • Fernandes, E. C., Silva, C. A., Braga, A. L., Sallum, A. M., Campos, L. M., & Farhat, S. C. (2015). Exposure to air pollutants and disease activity in juvenile-onset systemic lupus erythematosus patients. Arthritis Care & Research, 67, 1609–1614.

    Article  CAS  Google Scholar 

  • Gasparrini, A., Armstrong, B., & Kenward, M. G. (2010). Distributed lag non-linear models. Statistics in Medicine, 29, 2224–2234.

    Article  CAS  Google Scholar 

  • Gawda, A., Majka, G., Nowak, B., & Marcinkiewicz, J. (2017). Air pollution, oxidative stress, and exacerbation of autoimmune diseases. Central European Journal of Immunology, 42, 305–312.

    Article  CAS  Google Scholar 

  • Gergianaki, I., Bortoluzzi, A., & Bertsias, G. (2018). Update on the epidemiology, risk factors, and disease outcomes of systemic lupus erythematosus. Best Practice & Research Clinical Rheumatology, 32, 188–205.

    Article  Google Scholar 

  • Ghio, A. J., Carraway, M. S., & Madden, M. C. (2012). Composition of air pollution particles and oxidative stress in cells, tissues, and living systems. Journal of Toxicology and Environmental Health: Part B, Critical Reviews, 15, 1–21.

    Article  CAS  Google Scholar 

  • Glencross, D. A., Ho, T. R., Camiña, N., Hawrylowicz, C. M., & Pfeffer, P. E. (2020). Air pollution and its effects on the immune system. Free Radical Biology & Medicine, 151, 56–68.

    Article  CAS  Google Scholar 

  • Goshua, A., Akdis, C. A., & Nadeau, K. C. (2022). World Health Organization global air quality guideline recommendations: Executive summary. Allergy, 77, 1955–1960.

    Article  Google Scholar 

  • He, Y. S., Wang, G. H., Wu, Q., Wu, Z. D., Chen, Y., Tao, J. H., Fang, X. Y., Xu, Z., & Pan, H. F. (2021). The relationship between ambient air pollution and hospitalizations for gout in a humid subtropical Region of China. Journal of Inflammation Research, 14, 5827–5835.

    Article  CAS  Google Scholar 

  • Hua-Li, Z., Shi-Chao, X., De-Shen, T., Dong, L., & Hua-Feng, L. (2011). Seasonal distribution of active systemic lupus erythematosus and its correlation with meteorological factors. Clinics, 66, 1009–1013.

    Article  Google Scholar 

  • Jankowska-Kieltyka, M., Roman, A., & Nalepa, I. (2021). The air we breathe: Air pollution as a prevalent proinflammatory stimulus contributing to neurodegeneration. Frontiers in Cellular Neuroscience, 15, 647643.

    Article  CAS  Google Scholar 

  • Jeng, H. A. (2010). Chemical composition of ambient particulate matter and redox activity. Environmental Monitoring and Assessment, 169, 597–606.

    Article  CAS  Google Scholar 

  • Jung, C. R., Chung, W. T., Chen, W. T., Lee, R. Y., & Hwang, B. F. (2019). Long-term exposure to traffic-related air pollution and systemic lupus erythematosus in Taiwan: A cohort study. Science of the Total Environment, 668, 342–349.

    Article  CAS  Google Scholar 

  • Kan, H. D. (2012). A review of standard value of fine particulate matter (PM(2.5)) ruled by National Ambient Air Quality Standards (GB3095-2012) in China. Zhonghua Yu Fang Yi Xue Za Zhi, 46, 396–398.

    Google Scholar 

  • Kuo, N. C., Lin, C. H., & Lin, M. C. (2022). Prenatal and early life exposure to air pollution and the incidence of Kawasaki disease. Science and Reports, 12, 3415.

    Article  CAS  Google Scholar 

  • Mokoena, K. K., Ethan, C. J., Yu, Y., Shale, K., & Liu, F. (2019). Ambient air pollution and respiratory mortality in Xi’an, China: A time-series analysis. Respiratory Research, 20, 139.

    Article  Google Scholar 

  • Murdaca, G., Tonacci, A., Negrini, S., Greco, M., Borro, M., Puppo, F., & Gangemi, S. (2019). Emerging role of vitamin D in autoimmune diseases: An update on evidence and therapeutic implications. Autoimmunity Reviews, 18, 102350.

    Article  CAS  Google Scholar 

  • Parks, C. G., Cooper, G. S., Nylander-French, L. A., Sanderson, W. T., Dement, J. M., Cohen, P. L., Dooley, M. A., Treadwell, E. L., St Clair, E. W., Gilkeson, G. S., Hoppin, J. A., & Savitz, D. A. (2002). Occupational exposure to crystalline silica and risk of systemic lupus erythematosus: A population-based, case-control study in the southeastern United States. Arthritis and Rheumatism, 46, 1840–1850.

    Article  Google Scholar 

  • Parks, C. G., Cooper, G. S., Nylander-French, L. A., Storm, J. F., & Archer, J. D. (2003). Assessing exposure to crystalline silica from farm work: A population-based study in the Southeastern United States. Annals of Epidemiology, 13, 385–392.

    Article  Google Scholar 

  • Piao, M. J., Ahn, M. J., Kang, K. A., Ryu, Y. S., Hyun, Y. J., Shilnikova, K., Zhen, A. X., Jeong, J. W., Choi, Y. H., Kang, H. K., Koh, Y. S., & Hyun, J. W. (2018). Particulate matter 2.5 damages skin cells by inducing oxidative stress, subcellular organelle dysfunction, and apoptosis. Archives of Toxicology, 92, 2077–2091.

    Article  CAS  Google Scholar 

  • Prunicki, M., Cauwenberghs, N., Lee, J., Zhou, X., Movassagh, H., Noth, E., Lurmann, F., Hammond, S. K., Balmes, J. R., Desai, M., Wu, J. C., & Nadeau, K. C. (2021). Air pollution exposure is linked with methylation of immunoregulatory genes, altered immune cell profiles, and increased blood pressure in children. Science and Reports, 11, 4067.

    Article  CAS  Google Scholar 

  • Robertson, S., & Miller, M. R. (2018). Ambient air pollution and thrombosis. Particle and Fibre Toxicology, 15, 1.

    Article  Google Scholar 

  • Wu, Q., Xu, Z., Dan, Y. L., Cheng, J., Zhao, C. N., Mao, Y. M., Xiang, K., Hu, Y. Q., He, Y. S., & Pan, H. F. (2021a). Association between traffic-related air pollution and hospital readmissions for rheumatoid arthritis in Hefei, China: A time-series study. Environmental Pollution, 268, 115628.

    Article  CAS  Google Scholar 

  • Wu, Q., Xu, Z., Dan, Y. L., Wang, P., Mao, Y. M., Zhao, C. N., Zou, Y. F., Ye, D. Q., Hu, W., & Pan, H. F. (2021b). Low ambient temperature increases hospital re-admissions for systemic lupus erythematosus in humid subtropical region: A time series study. Environmental Science and Pollution Research International, 28, 530–537.

    Article  Google Scholar 

  • Xiang, K., Wang, P., Xu, Z., Hu, Y. Q., He, Y. S., Chen, Y., Feng, Y. T., Yin, K. J., Huang, J. X., Wang, J., Wu, Z. D., Yang, X. K., Wang, D. G., Ye, D. Q., & Pan, H. F. (2021). Causal effects of gut microbiome on systemic lupus erythematosus: A two-sample Mendelian randomization study. Frontiers in Immunology, 12, 667097.

    Article  CAS  Google Scholar 

  • Yang, J., Lu, Y. W., Pan, H. F., Tao, J. H., Zou, Y. F., Bao, W., & Ye, D. Q. (2012). Seasonal distribution of systemic lupus erythematosus activity and its correlation with climate factors. Rheumatology International, 32, 2393–2399.

    Article  Google Scholar 

  • Yariwake, V. Y., Torres, J. I., Dos Santos, A. R. P., Freitas, S. C. F., De Angelis, K., Farhat, S. C. L., Câmara, N. O. S., & Veras, M. M. (2021). Chronic exposure to PM2.5 aggravates SLE manifestations in lupus-prone mice. Particle and Fibre Toxicology, 18, 15.

    Article  CAS  Google Scholar 

  • Zhang, L., Qing, P., Yang, H., Wu, Y., Liu, Y., & Luo, Y. (2021). Gut microbiome and metabolites in systemic lupus erythematosus: Link, mechanisms and intervention. Frontiers in Immunology, 12, 686501.

    Article  CAS  Google Scholar 

  • Zhao, C. N., Mei, Y. J., Wu, G. C., Mao, Y. M., Wu, Q., Dan, Y. L., & Pan, H. F. (2019a). Effect of air pollution on hospital admissions for systemic lupus erythematosus in Bengbu, China: A time series study. Lupus, 28, 1541–1548.

    Article  CAS  Google Scholar 

  • Zhao, C. N., Xu, Z., Wu, G. C., Mao, Y. M., Liu, L. N., Wu-Qian, Y. L. D., Tao, S. S., Zhang, Q., Sam, N. B., Fan, Y. G., Zou, Y. F., Ye, D. Q., & Pan, H. F. (2019b). Emerging role of air pollution in autoimmune diseases. Autoimmunity Reviews, 18, 607–614.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the National Natural Science Foundation of China, Anhui Provincial Natural Science Foundation, Research Fund of Anhui Institute of Translational Medicine, Natural Science Foundation of Anhui Medical University and Postgraduate Innovation Research and Practice Program of Anhui Medical University for funding support.

Funding

This study was funded by grants from the National Natural Science Foundation of China (81872687, 82103932), Anhui Provincial Natural Science Foundation (2108085Y26, 2108085QH361), Research Fund of Anhui Institute of Translational Medicine (2021zhyx-B04) and Natural Science Foundation of Anhui Medical University (2020xkj0), Postgraduate Innovation Research and Practice Program of Anhui Medical University (YJS20210286).

Author information

Author notes

  1. Ying Pan, Yang Fang and Yue Chen have contributed equally to this work and should be considered co-first authors.

Authors and Affiliations

  1. Department of Rheumatology and Immunology, The First Affiliated Hospital of Xi’an Jiaotong University, Yanta West Road No. 277, Xi’an, 710061, Shaanxi, China

    Ying Pan

  2. Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, 230032, Anhui, China

    Yang Fang, Yue Chen, Cong Chen, Ruo-Di Zhang, Xi Fang, Yan Zhao, Ling-Qiong Jiang, Jing Ni & Hai-Feng Pan

  3. Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, 81 Meishan Road, Hefei, 230032, Anhui, China

    Yang Fang, Yue Chen, Cong Chen, Ruo-Di Zhang, Xi Fang, Yan Zhao, Ling-Qiong Jiang, Jing Ni & Hai-Feng Pan

  4. Teaching Center for Preventive Medicine, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, 230032, Anhui, China

    Peng Wang

Authors
  1. Ying Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yang Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yue Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruo-Di Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xi Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ling-Qiong Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jing Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Peng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hai-Feng Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HP, PW and JN conceived of the presented idea. YF, YC and RZ developed the theory and performed the computations. XF, YZ and LJ verified the analytical methods. YP, and YF drafted the manuscript. All authors discussed the results and contributed to the final manuscript.

Corresponding authors

Correspondence to Peng Wang or Hai-Feng Pan.

Ethics declarations

Conflict of interest

The authors declare that they have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript.

Ethical approval

This study was approved by the Medical Ethics Committee of Anhui Medical University and the First Affiliated Hospital of Xi’an Jiaotong University.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

10653_2022_1409_MOESM1_ESM.jpg

Figure S1 Spearman's correlation coefficients between the different meteorological factors and air pollutants (JPG 199 KB)

10653_2022_1409_MOESM2_ESM.jpg

Figure S2 Concentration-response relationship curves between PM2.5 and PM10 exposure levels and daily hospitalization in patients admitted with SLE (JPG 61 KB)

Figure S3 Time series of PM2.5, PM10 and PM2.5/PM10 during cold season in Xi'an from 2014 to 2020 (JPG 113 KB)

Figure S4 Time series of PM2.5, PM10 and PM2.5/PM10 during warm season in Xi'an from 2014 to 2020 (JPG 251 KB)

10653_2022_1409_MOESM5_ESM.jpg

Figure S5 Concentration-response relationship curves between CO, NO2, O3, SO2 exposure levels and daily hospitalization in patients admitted with SLE (JPG 309 KB)

10653_2022_1409_MOESM6_ESM.jpg

Figure S6 The single-day association between an increase of IQR of PM2.5 and SLE admissions was increased when varying the degrees of freedom of SO2, humidity, NO2, average temperature, wind speed (3-5dfs) and time of df (6-8dfs/year) (JPG 251 KB)

10653_2022_1409_MOESM7_ESM.jpg

Figure S7 Single-day association between an increase of IQR of PM10 and SLE admissions when varying CO, humidity, NO2, O3, average temperature, wind speed of freedom (3-5dfs) and time of df (6-8dfs/year) (JPG 309 KB)

10653_2022_1409_MOESM8_ESM.docx

Table S1 The association between an increase of every IQR μg/m3 of PM2.5 and SLE outpatients in different subgroups and season (RR and 95% CI) (DOCX 23 KB)

10653_2022_1409_MOESM9_ESM.docx

Table S2 The association between an increase of every IQR μg/m3 of PM10 and SLE outpatients in different subgroups and season (RR and 95% CI) (DOCX 23 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, Y., Fang, Y., Chen, Y. et al. Associations between particulate matter air pollutants and hospitalization risk for systemic lupus erythematosus: a time-series study from Xi’an, China. Environ Geochem Health 45, 3317–3330 (2023). https://doi.org/10.1007/s10653-022-01409-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-022-01409-3

Keywords

Search

Navigation