Abstract
In recent years, a growing number of studies have found that air pollution plays critical roles in the onset and development of autoimmune diseases, but few studies have shown an association between air pollutants and dermatomyositis (DM). We sought to investigate the relationship between short-term exposure to air pollution and outpatient visits for DM and to quantify the burden of DM due to exposure to air pollutants in Hefei, China. Daily records of hospital outpatient visits for DM, air pollutants and meteorological factors data in Hefei from January 1, 2018 to December 31, 2021 were obtained. We used a distributed lag non-linear model (DLNM) in conjunction with a generalized linear model (GLM) to explore the association between air pollution and outpatient visits for DM, and conducted stratified analyses by gender, age and season. Moreover, we used attributable fraction (AF) and attributable number (AN) to reflect the burden of disease. A total of 4028 DM clinic visits were recorded during this period. High concentration nitrogen dioxide (NO2) exposure was associated with increased risk of DM outpatient visits (relative risk (RR) 1.063, 95% confidence interval (CI) 1.015–1.114, lag 0–5). Intriguingly, exposure to high concentration ozone (O3) was associated with reduced risk of outpatient visits for DM (RR 0.974, 95% CI 0. 0.954–0.993, lag 0–6). The results of stratified analyses showed that the cold season (vs. warm season) were more susceptible to outpatient visits for DM associated with NO2 and O3 exposure. In addition, we observed that an increased risk of DM outpatient visits was attributable to high concentration NO2 exposure, while high concentration O3 exposure was associated with a decreased risk of DM outpatient visits. This study provided a scientific basis for the etiology research and health protection of DM.
Similar content being viewed by others
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Arias-Pérez, R. D., Taborda, N. A., Gómez, D. M., Narvaez, J. F., Porras, J., & Hernandez, J. C. (2020). Inflammatory effects of particulate matter air pollution. Environmental Science and Pollution Research, 27, 42390–404. https://doi.org/10.1007/s11356-020-10574-w
Bax, C. E., Maddukuri, S., Ravishankar, A., Pappas-Taffer, L., & Werth, V. P. (2021). Environmental triggers of dermatomyositis: A narrative review. Annals of Translational Medicine, 9(5), 434. https://doi.org/10.21037/atm-20-3719
Bellinato, F., Adami, G., Vaienti, S., Benini, C., Gatti, D., Idolazzi, L., Fassio, A., Rossini, M., Girolomoni, G., & Gisondi, P. (2022). Association between short-term exposure to environmental air pollution and psoriasis flare. JAMA Dermatol, 158, 375–81. https://doi.org/10.1001/jamadermatol.2021.6019
Bernatsky, S., Smargiassi, A., Barnabe, C., Svenson, L. W., Brand, A., Martin, R. V., Hudson, M., Clarke, A. E., Fortin, P. R., van Donkelaar, A., & Edworthy, S. (2016). Fine particulate air pollution and systemic autoimmune rheumatic disease in two Canadian provinces. Environmental Research, 146, 85–91. https://doi.org/10.1016/j.envres.2015.12.021
Bernatsky, S., Smargiassi, A., Johnson, M., Kaplan, G. G., Barnabe, C., Svenson, L., Brand, A., Bertazzon, S., Hudson, M., Clarke, A. E., & Fortin, P. R. (2015). Fine particulate air pollution, nitrogen dioxide, and systemic autoimmune rheumatic disease in Calgary, Alberta. Environmental Research, 140, 474–478. https://doi.org/10.1016/j.envres.2015.05.007
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. https://doi.org/10.1093/ije/dyt092
Ceribelli, A., De Santis, M., Isailovic, N., Gershwin, M. E., & Selmi, C. (2017). The immune response and the pathogenesis of idiopathic inflammatory myositis: A critical review. Clinical Reviews in Allergy and Immunology, 52, 58–70. https://doi.org/10.1007/s12016-016-8527-x
Chang, K. H., Hsu, C. C., Muo, C. H., Hsu, C. Y., Liu, H. C., Kao, C. H., Chen, C. Y., Chang, M. Y., & Hsu, Y. C. (2016). Air pollution exposure increases the risk of rheumatoid arthritis: A longitudinal and nationwide study. Environment International, 94, 495–499. https://doi.org/10.1016/j.envint.2016.06.008
Chatkin, J., Correa, L., & Santos, U. (2022). External environmental pollution as a risk factor for asthma. Clinical Reviews in Allergy and Immunology, 62, 72–89. https://doi.org/10.1007/s12016-020-08830-5
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. https://doi.org/10.1016/j.envres.2022.114017
Delgado-Roche, L., Riera-Romo, M., Mesta, F., Hernández-Matos, Y., Barrios, J. M., Martínez-Sánchez, G., & Al-Dalaien, S. M. (2017). Medical ozone promotes Nrf2 phosphorylation reducing oxidative stress and pro-inflammatory cytokines in multiple sclerosis patients. European Journal of Pharmacology, 811, 148–154. https://doi.org/10.1016/j.ejphar.2017.06.017
DeWane, M. E., Waldman, R., & Lu, J. (2020). Dermatomyositis: Clinical features and pathogenesis. Journal of the American Academy of Dermatology, 82, 267–281. https://doi.org/10.1016/j.jaad.2019.06.1309
Elgabsi, M., Novack, L., Yarza, S., Elgabsi, M., Shtein, A., & Ifergane, G. (2021). An impact of air pollution on moderate to severe relapses among multiple sclerosis patients. Multiple Sclerosis and Related Disorders, 53, 103043. https://doi.org/10.1016/j.msard.2021.103043
Fiorito, G., Vlaanderen, J., Polidoro, S., Gulliver, J., Galassi, C., Ranzi, A., Krogh, V., Grioni, S., Agnoli, C., Sacerdote, C., & Panico, S. (2018). Oxidative stress and inflammation mediate the effect of air pollution on cardio- and cerebrovascular disease: A prospective study in nonsmokers. Environmental and Molecular Mutagenesis, 59, 234–246. https://doi.org/10.1002/em.22153
Gao, J., Yu, F., Xu, Z., Duan, J., Cheng, Q., Bai, L., Zhang, Y., Wei, Q., Yi, W., Pan, R., & Su, H. (2019). The association between cold spells and admissions of ischemic stroke in Hefei, China: Modified by gender and age. Science of the Total Environment, 669, 140–147. https://doi.org/10.1016/j.scitotenv.2019.02.452
Gasparrini, A. (2011). Distributed lag linear and non-linear models in R: The package dlnm. Journal of Statistical Software, 43, 1–20.
Gasparrini, A., Armstrong, B., & Kenward, M. G. (2010). Distributed lag non-linear models. Statistics in Medicine, 29, 2224–2234. https://doi.org/10.1002/sim.3940
Glencross, D. A., Ho, T. R., Camina, N., Hawrylowicz, C. M., & Pfeffer, P. E. (2020). Air pollution and its effects on the immune system. Free Radical Biology & Medicine, 151, 56–68. https://doi.org/10.1016/j.freeradbiomed.2020.01.179
Huang, K., Ding, K., Yang, X. J., Hu, C. Y., Jiang, W., Hua, X. G., Liu, J., Cao, J. Y., Zhang, T., Kan, X. H., & Zhang, X. J. (2020). Association between short-term exposure to ambient air pollutants and the risk of tuberculosis outpatient visits: A time-series study in Hefei, China. Environmental Research, 184, 109343. https://doi.org/10.1016/j.envres.2020.109343
Huang, L. J., Zha, J. J., Cao, N. W., Zhou, H. Y., Chu, X. J., Wang, H., Li, X. B., & Li, B. Z. (2022). Temperature might increase the hospital admission risk for rheumatoid arthritis patients in Anqing, China: A time-series study. International Journal of Biometeorology, 66, 201–211. https://doi.org/10.1007/s00484-021-02207-9
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, 342–49. https://doi.org/10.1016/j.scitotenv.2019.03.018
Kamperman, R. G., van der Kooi, A. J., de Visser, M., Aronica, E., & Raaphorst, J. (2022). Pathophysiological mechanisms and treatment of dermatomyositis and immune mediated necrotizing myopathies: A focused review. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms23084301
Kuhn, A., Landmann, A., & Bonsmann, G. (2016). The skin in autoimmune diseases-Unmet needs. Autoimmunity Reviews, 15, 948–954. https://doi.org/10.1016/j.autrev.2016.07.013
Kus, K. J. B., LaChance, A. H., & Vleugels, R. A. (2021). Recognition and management of cutaneous connective tissue diseases. Medical Clinics of North America, 105, 757–782. https://doi.org/10.1016/j.mcna.2021.04.011
Lundberg, I. E., Tjärnlund, A., Bottai, M., Werth, V. P., Pilkington, C., de Visser, M., Alfredsson, L., Amato, A. A., Barohn, R. J., Liang, M. H., & Singh, J. A. (2017). 2017 European League Against Rheumatism/American College of rheumatology classification criteria for adult and juvenile idiopathic inflammatory myopathies and their major subgroups. Arthritis Rheumatology, 69, 2271–2282.
Marie, I. (2012). Morbidity and mortality in adult polymyositis and dermatomyositis. Current Rheumatology Reports, 14, 275–285. https://doi.org/10.1007/s11926-012-0249-3
McCann, L. J., Livermore, P., Wilkinson, M. G. L., & Wedderburn, L. R. (2022). Juvenile dermatomyositis. Where are we now? Clinical and Experimental Rheumatology, 40, 394–403. https://doi.org/10.55563/clinexprheumatol/56ilob
Meyer, A., Meyer, N., Schaeffer, M., Gottenberg, J. E., Geny, B., & Sibilia, J. (2015). Incidence and prevalence of inflammatory myopathies: A systematic review. Rheumatology (Oxford), 54, 50–63. https://doi.org/10.1093/rheumatology/keu289
Ngo, S. T., Steyn, F. J., & McCombe, P. A. (2014). Gender differences in autoimmune disease. Frontiers in Neuroendocrinology, 35, 347–369. https://doi.org/10.1016/j.yfrne.2014.04.004
Norval, M., Lucas, R. M., Cullen, A. P., De Gruijl, F. R., Longstreth, J., Takizawa, Y., & Van Der Leun, J. C. (2011). The human health effects of ozone depletion and interactions with climate change. Photochemical & Photobiological Sciences, 10, 199–225. https://doi.org/10.1039/c0pp90044c
Orru, H., Ebi, K. L., & Forsberg, B. (2017). The interplay of climate change and air pollution on health. Current Environmental Health Reports, 4, 504–513. https://doi.org/10.1007/s40572-017-0168-6
Pope, C. A., III., Bhatnagar, A., McCracken, J. P., Abplanalp, W., Conklin, D. J., & O’Toole, T. (2016). Exposure to fine particulate air pollution is associated with endothelial injury and systemic inflammation. Circulation Research, 119, 1204–14. https://doi.org/10.1161/circresaha.116.309279
Robinson, A. B., & Reed, A. M. (2011). Clinical features, pathogenesis and treatment of juvenile and adult dermatomyositis. Nature Reviews Rheumatology, 7, 664–675. https://doi.org/10.1038/nrrheum.2011.139
Schlecht, N., Sunderkötter, C., Niehaus, S., & Nashan, D. (2020). Update on dermatomyositis in adults. Journal der Deutschen Dermatologischen Gesellschaft, 18, 995–1013. https://doi.org/10.1111/ddg.14267
Schober, P., Boer, C., & Schwarte, L. A. (2018). Correlation Coefficients: Appropriate Use and Interpretation. Anesthesia and Analgesia, 126, 1763–1768. https://doi.org/10.1213/ane.0000000000002864
Selmi, C., Lu, Q., & Humble, M. C. (2012). Heritability versus the role of the environment in autoimmunity. Journal of Autoimmunity, 39, 249–252. https://doi.org/10.1016/j.jaut.2012.07.011
Vaillant, J. D., Fraga, A., Díaz, M. T., Mallok, A., Viebahn-Hänsler, R., Fahmy, Z., Barberá, A., Delgado, L., Menéndez, S., & Fernández, O. S. L. (2013). Ozone oxidative postconditioning ameliorates joint damage and decreases pro-inflammatory cytokine levels and oxidative stress in PG/PS-induced arthritis in rats. European Journal of Pharmacology, 714, 318–324. https://doi.org/10.1016/j.ejphar.2013.07.034
Wang, J., Yu, L., Deng, J., Gao, X., Chen, Y., Shao, M., Zhang, T., Ni, M., & Pan, F. (2022). Short-term effect of meteorological factors on the risk of rheumatoid arthritis hospital admissions: A distributed lag non-linear analysis in Hefei, China. Environmental Research, 207, 112168. https://doi.org/10.1016/j.envres.2021.112168
WHO. (2021). WHO global air quality guidelines: Particulate matter (PM2.5 and PM10), ozone, nitrogen dioxide, sulfur dioxide and carbon monoxide: executive summary. Retrieved December 25, 2021, from https://apps.who.int/iris/handle/10665/345334
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. (2021). Association between traffic-related air pollution and hospital readmissions for rheumatoid arthritis in Hefei, China: A time-series study. Environmental Pollution, 268, 115628. https://doi.org/10.1016/j.envpol.2020.115628
Zhang, Q., Sun, S., Sui, X., Ding, L., Yang, M., Li, C., Zhang, C., Zhang, X., Hao, J., Xu, Y., & Lin, S. (2021). Associations between weekly air pollution exposure and congenital heart disease. Science of The Total Environment, 757, 143821. https://doi.org/10.1016/j.scitotenv.2020.143821
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. https://doi.org/10.1177/0961203319882503
Zhao, C. N., Xu, Z., Wu, G. C., Mao, Y. M., Liu, L. N., Dan, Y. L., Tao, S. S., Zhang, Q., Sam, N. B., Fan, Y. G., & Zou, Y. F. (2019b). Emerging role of air pollution in autoimmune diseases. Autoimmunity Reviews, 18, 607–14. https://doi.org/10.1016/j.autrev.2018.12.010
Zhao, N., Smargiassi, A., Jean, S., Gamache, P., Laouan-Sidi, E. A., Chen, H., Goldberg, M. S., & Bernatsky, S. (2022). Long-term exposure to fine particulate matter and ozone and the onset of systemic autoimmune rheumatic diseases: An open cohort study in Quebec, Canada. Arthritis Research & Therapy, 24, 151. https://doi.org/10.1186/s13075-022-02843-5
Acknowledgements
We appreciate the efforts of all the researchers whose articles were included in this study.
Funding
This study was funded by grants from the National Natural Science Foundation of China (82273710, 81872687), Anhui Provincial Natural Science Foundation (2108085Y26, 2108085QH361), Research Fund of Anhui Institute of Translational Medicine (2021zhyx-B04) and Postgraduate Innovation Research and Practice Program of Anhui Medical University (YJS20230007).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. H-F P and J-H T conceived the present idea and were responsible for the design of the study. Z-D W performed the statistical analysis and manuscript writing. C C and Y-S H participated in acquisition of data and data analysis. Y C and Y-T F participated in modification of English. Literature search by J-X H, K-J Y and J W. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
This study was approved by the Ethical Committee of Anhui Medical University (Hefei, Anhui, China).
Consent for publication
Not applicable (This study did not contain any individual person’s data in any form).
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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.
About this article
Cite this article
Wu, ZD., Chen, C., He, YS. et al. Association between air pollution exposure and outpatient visits for dermatomyositis in a humid subtropical region of China: a time-series study. Environ Geochem Health 45, 6095–6107 (2023). https://doi.org/10.1007/s10653-023-01616-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-023-01616-6