Cognitive impairment associated with individual and joint exposure to PM_2.5 constituents in a Chinese national cohort

Highlights

● A national cohort to assess nexus between cognition function and PM_2.5 constituents.

● Cognitive impairment was related to individual and joint exposure to PM_2.5 constituents.

● BC displayed the highest negative effect on PM_2.5-related cognitive impairment.

● Female, younger, and well-educated individuals were more vulnerable.

Abstract

Nationwide longitudinal evidence linking cognitive decline with exposure to fine particulate matter (PM_2.5) constituents remains scarce in China. By constructing a dynamic cohort based on the China Health and Retirement Longitudinal Study, we aimed to assess individual and joint associations of PM_2.5 constituents with cognitive function among middle-aged and older adults in China. Linear mixed-effects models incorporated with quantile-based g-computation were applied to investigate individual and joint associations of long-term exposures to PM_2.5 constituents with cognitive function. Among 13,507 respondents, we evaluated 38,950 follow-up records of cognitive function tests. Declines in global cognitive score associated with an interquartile range (IQR) increase in exposure were −1.477 (95% CI: −1.722, −1.232) for nitrate, followed by −1.331 (−1.529, −1.133) for ammonium, −1.033 (−1.184, −0.883) for sulfate, −0.988 (−1.144, −0.832) for organic matter and −0.822 (−0.946, −0.699) for black carbon. An IQR-equivalent increase in joint exposure to these PM_2.5 constituents was associated with a decline of −1.353 (−1.659, −1.048) in global cognitive score. Female, younger, and well-educated individuals were at greater vulnerability to cognitive impairment related to individual and joint exposure to PM_2.5 constituents. This study suggested that later-life exposures to PM_2.5 constituents were associated with cognitive decline in middle-aged and older adults in China.

Graphical abstract

Keywords

Air pollution / PM_2.5 constituents / Cognitive function / Joint exposure / Middle-aged and older adults

References

[1] Ayton S, Faux NG, Bush AI, Alzheimer’s Disease Neuroimaging Initiative. (2015). Ferritin levels in the cerebrospinal fluid predict Alzheimer’s disease outcomes and are regulated by APOE. Nature Communications, 6(1): 6760

[2] Azur MJ, Stuart EA, Frangakis C, Leaf PJ (2011). Multiple imputation by chained equations: What is it and how does it work? International Journal of Methods in Psychiatric Research, 20(1): 40–49

[3] Bello-Medina PC, Rodriguez-Martinez E, Prado-Alcala RA, Rivas-Arancibia S. (2022). Ozone pollution, oxidative stress, synaptic plasticity, and neurodegeneration. Neurología, 37(4): 277–286

[4] DaoXDiS ZhangXGao PWangLYanLTangG HeLKrafftT ZhangF (2022). Composition and sources of particulate matter in the Beijing-Tianjin-Hebei region and its surrounding areas during the heating season. Chemosphere, 291(Pt 1): 132779

[5] Gaidin SG, Zinchenko VP, Kosenkov AM. (2020). Mechanisms of ammonium-induced neurotoxicity. Neuroprotective effect of alpha-2 adrenergic agonists. Archives of Biochemistry and Biophysics, 693: 108593

[6] Gong J, Wang G, Wang Y, Chen X, Chen Y, Meng Q, Yang P, Yao Y, Zhao Y. (2022). Nowcasting and forecasting the care needs of the older population in China: analysis of data from the China Health and Retirement Longitudinal Study (CHARLS). Lancet Public Health, 7(12): e1005–e1013

[7] Goyal MS, Vlassenko AG, Blazey TM, Su Y, Couture LE, Durbin TJ, Bateman RJ, Benzinger TL, Morris JC, Raichle ME. (2017). Loss of brain aerobic glycolysis in normal human aging. Cell Metabolism, 26(2): 353–360.e3

[8] Harrell J F E (2001). Regression Modeling Strategies: with Applications to Linear Models, Logistic Regression, and Survival Analysis. New York: Springer

[9] Hautekiet P, Saenen ND, Demarest S, Keune H, Pelgrims I, Van Der Heyden J, De Clercq EM, Nawrot TS. (2022). Air pollution in association with mental and self-rated health and the mediating effect of physical activity. Environmental Health, 21(1): 29

[10] Helbich M, Yao Y, Liu Y, Zhang J, Liu P, Wang R. (2019). Using deep learning to examine street view green and blue spaces and their associations with geriatric depression in Beijing, China. Environment International, 126: 107–117

[11] Hu Y, Peng W, Ren R, Wang Y, Wang G. (2022). Sarcopenia and mild cognitive impairment among elderly adults: the first longitudinal evidence from CHARLS. Journal of Cachexia, Sarcopenia and Muscle, 13(6): 2944–2952

[12] HuangSSong QHuWYuanBLiuJ JiangBLi WWuCJiangFChenW, . (2022). Chemical composition and sources of amines in PM_2.5 in an urban site of PRD, China. Environmental Research, 212(Pt B): 113261

[13] Huang W, Zhou Y, Chen X, Zeng X, Knibbs L D, Zhang Y, Jalaludin B, Dharmage SC, Morawska L, Guo Y. . (2023). Individual and joint associations of long-term exposure to air pollutants and cardiopulmonary mortality: a 22-year cohort study in Northern China. Lancet Regional Health. Western Pacific, 36: 100776

[14] Jia L, Du Y, Chu L, Zhang Z, Li F, Lyu D, Li Y, Li Y, Zhu M, Jiao H. . (2020). Prevalence, risk factors, and management of dementia and mild cognitive impairment in adults aged 60 years or older in China: a cross-sectional study. Lancet Public Health, 5(12): e661–e671

[15] Kaumbekova S, Torkmahalleh MA, Shah D. (2021). Impact of ultrafine particles and secondary inorganic ions on early onset and progression of amyloid aggregation: insights from molecular simulations. Environmental Pollution, 284: 117147

[16] Keil AP, Buckley JP, O’Brien KM, Ferguson KK, Zhao S, White AJ. (2020). A quantile-based g-computation approach to addressing the effects of exposure mixtures. Environmental Health Perspectives, 128(4): 047004

[17] Kulick ER, Wellenius GA, Boehme AK, Joyce NR, Schupf N, Kaufman JD, Mayeux R, Sacco RL, Manly JJ, Elkind MSV. (2020). Long-term exposure to air pollution and trajectories of cognitive decline among older adults. Neurology, 94(17): e1782–e1792

[18] Liu J, Liu R, Zhang Y, Lao X, Mandeville KL, Ma X, Di Q. (2023). Leisure-time physical activity mitigated the cognitive effect of PM_2.5 and PM_2.5 components exposure: evidence from a nationwide longitudinal study. Environment International, 179: 108143

[19] Liu S, Geng G, Xiao Q, Zheng Y, Liu X, Cheng J, Zhang Q. (2022). Tracking daily concentrations of PM_2.5 chemical composition in China since 2000. Environmental Science & Technology, 56(22): 16517–16527

[20] Livingston G, Huntley J, Sommerlad A, Ames D, Ballard C, Banerjee S, Brayne C, Burns A, Cohen-Mansfield J, Cooper C. . (2020). Dementia prevention, intervention, and care: 2020 report of the Lancet Commission. Lancet, 396(10248): 413–446

[21] Lo YC, Lu YC, Chang YH, Kao S, Huang HB. (2019). Air Pollution exposure and cognitive function in Taiwan older adults: a repeated measurement study. International Journal of Environmental Research and Public Health, 16(16): 2976

[22] Luo L, Bai X, Liu S, Wu B, Liu W, Lv Y, Guo Z, Lin S, Zhao S, Hao Y. . (2022). Fine particulate matter (PM_2.5/PM_1.0) in Beijing, China: variations and chemical compositions as well as sources. Journal of Environmental Sciences, 121: 187–198

[23] Mo S, Wang Y, Peng M, Wang Q, Zheng H, Zhan Y, Ma Z, Yang Z, Liu L, Hu K. . (2023). Sex disparity in cognitive aging related to later-life exposure to ambient air pollution. Science of the Total Environment, 886: 163980

[24] GBD 2019 Dementia Forecasting Collaborators. (2022). Estimation of the global prevalence of dementia in 2019 and forecasted prevalence in 2050: an analysis for the Global Burden of Disease Study 2019. Lancet. Public Health, 7(2): e105–e125

[25] Niranjan R, Thakur A K. (2017). The toxicological mechanisms of environmental soot (black carbon) and carbon black: focus on oxidative stress and inflammatory pathways. Frontiers in Immunology, 8: 763

[26] Pan R, Zhang Y, Xu Z, Yi W, Zhao F, Song J, Sun Q, Du P, Fang J, Cheng J. . (2022). Exposure to fine particulate matter constituents and cognitive function performance, potential mediation by sleep quality: a multicenter study among Chinese adults aged 40–89 years. Environment International, 170: 107566

[27] Popescu LL, Popescu RS, Catalina T. (2022). Indoor particle’s pollution in bucharest, Romania. Toxics, 10(12): 757

[28] Qi J, Zhao N, Liu M, Guo Y, Fu J, Zhang Y, Wang W, Su Z, Zeng Y, Yao Y. . (2024). Long-term exposure to fine particulate matter constituents and cognitive impairment among older adults: an 18-year Chinese nationwide cohort study. Journal of Hazardous Materials, 468: 133785

[29] Ren R, Qi J, Lin S, Liu X, Yin P, Wang Z, Tang R, Wang J, Huang Q, Li J. . (2022). The China alzheimer report 2022. General Psychiatry, 35(1): e100751

[30] Richmond-Rakerd LS, D’Souza S, Milne B J, Caspi A, Moffitt T E. (2022). Longitudinal associations of mental disorders with dementia: 30-year analysis of 1.7 million New Zealand citizens. JAMA Psychiatry, 79(4): 333–340

[31] Rotenstein L S, Ramos M A, Torre M, Segal J B, Peluso M J, Guille C, Sen S, Mata D A. (2016). Prevalence of depression, depressive symptoms, and suicidal ideation among medical students: a systematic review and meta-analysis. Journal of the American Medical Association, 316(21): 2214–2236

[32] Salinas-Rodríguez A, Fernandez-Nino J A, Manrique-Espinoza B, Moreno-Banda G L, Sosa-Ortiz A L, Qian Z M, Lin H. (2018). Exposure to ambient PM_2.5 concentrations and cognitive function among older Mexican adults. Environment International, 117: 1–9

[33] Shi L, Zhu Q, Wang Y, Hao H, Zhang H, Schwartz J, Amini H, Van Donkelaar A, Martin RV, Steenland K. . (2023). Incident dementia and long-term exposure to constituents of fine particle air pollution: a national cohort study in the United States. Proceedings of the National Academy of Sciences of the United States of America, 120(1): e2211282119

[34] Sumien N, Cunningham JT, Davis DL, Engelland R, Fadeyibi O, Farmer G E, Mabry S, Mensah-Kane P, Trinh O T P, Vann P H. . (2021). Neurodegenerative disease: roles for sex, hormones, and oxidative stress. Endocrinology, 162(11): bqab185

[35] Tan L, Nakanishi E, Lee M. (2022). Association between exposure to air pollution and late-life neurodegenerative disorders: an umbrella review. Environment International, 158: 106956

[36] Tian Y, Shi Z. (2022). Effects of physical activity on daily physical function in Chinese middle-aged and older adults: a longitudinal study from CHARLS. Journal of Clinical Medicine, 11(21): 6514

[37] Wang J, Wang J, Nie W, Chi X, Ge D, Zhu C, Wang L, Li Y, Huang X, Qi X. . (2023). Response of organic aerosol characteristics to emission reduction in Yangtze River Delta region. Frontiers of Environmental Science & Engineering, 17(9): 114

[38] Wang Q, Fan D, Zhao L, Wu W. (2019). A Study on the design method of indoor fine particulate matter (PM_2.5) pollution control in China. International Journal of Environmental Research and Public Health, 16(23): 4588

[39] Wang X Q, Chen P J. (2014). Population ageing challenges health care in China. Lancet, 383(9920): 870

[40] Winblad B, Amouyel P, Andrieu S, Ballard C, Brayne C, Brodaty H, Cedazo-Minguez A, Dubois B, Edvardsson D, Feldman H. . (2016). Defeating Alzheimer’s disease and other dementias: a priority for European science and society. Lancet Neurology, 15(5): 455–532

[41] WuSWangB YangDWei HLiHPanLHuangJ WangXQin YZhengC, . (2016). Ambient particulate air pollution and circulating antioxidant enzymes: a repeated-measure study in healthy adults in Beijing, China. Environmental Pollution, 208(Pt A): 16-24

[42] Wurth R, Kioumourtzoglou MA, Tucker KL, Griffith J, Manjourides J, Suh H. (2018). Fine particle sources and cognitive function in an older Puerto Rican cohort in Greater Boston. Environmental Epidemiology, 2(3): e022

[43] Xiao Q, Geng G, Xue T, Liu S, Cai C, He K, Zhang Q. (2022). Tracking PM_2.5 and O₃ pollution and the related health burden in China 2013–2020. Environmental Science & Technology, 56(11): 6922–6932

[44] Xie Y, Wu D, Zhu S. (2021). Can new energy vehicles subsidy curb the urban air pollution? Empirical evidence from pilot cities in China. Science of the Total Environment, 754: 142232

[45] Xu J, Wang J, Wimo A, Fratiglioni L, Qiu C. (2017). The economic burden of dementia in China, 1990–2030: implications for health policy. Bulletin of the World Health Organization, 95(1): 18–26

[46] Xue J, Li J, Liang J, Chen S. (2018). The prevalence of mild cognitive impairment in China: a systematic review. Aging and Disease, 9(4): 706–715

[47] Xue T, Han Y, Fan Y, Zheng Y, Geng G, Zhang Q, Zhu T. (2021). Association between a rapid reduction in air particle pollution and improved lung function in adults. Annals of the American Thoracic Society, 18(2): 247–256

[48] Yang H, Huang X, Hu J, Thompson J R, Flower R J. (2022). Achievements, challenges and global implications of China’s carbon neutral pledge. Frontiers of Environmental Science & Engineering, 16(8): 111

[49] Yang Y, Ruan Z, Wang X, Yang Y, Mason T G, Lin H, Tian L. (2019). Short-term and long-term exposures to fine particulate matter constituents and health: a systematic review and meta-analysis. Environmental Pollution, 247: 874–882

[50] Yao Y, Wang K, Xiang H. (2022). Association between cognitive function and ambient particulate matters in middle-aged and elderly Chinese adults: evidence from the China Health and Retirement Longitudinal Study (CHARLS). Science of the Total Environment, 828: 154297

[51] Younan D, Wang X, Casanova R, Barnard R, Gaussoin S A, Saldana S, Petkus A J, Beavers D P, Resnick S M, Manson J E. . (2020). PM_2.5 associated with gray matter atrophy reflecting increased Alzheimers risk in older women. Neurology, 96(8): e1190–e1201

[52] Yuan Y, Wang K, Sun H Z, Zhan Y, Yang Z, Hu K, Zhang Y. (2023). Excess mortality associated with high ozone exposure: a national cohort study in China. Environmental Science and Ecotechnology, 15: 100241

[53] Zeng Y, Feng Q, Hesketh T, Christensen K, Vaupel J W. (2017). Survival, disabilities in activities of daily living, and physical and cognitive functioning among the oldest-old in China: a cohort study. Lancet, 389(10079): 1619–1629

[54] Zhao N, Al-Aly Z, Zheng B, Van Donkelaar A, Martin RV, Pineau CA, Bernatsky S. (2022). Fine particulate matter components and interstitial lung disease in rheumatoid arthritis. European Respiratory Journal, 60(1): 2102149

Acknowledgements

This study was funded by Provincial University Students’ Innovative Entrepreneurial Training Program in Hubei (No. S202310488170), Social Sciences General Project of Hubei Provincial Department of Education (No. 23Y152), Wuhan Knowledge Innovation Project (No. 2023020201020410), and “The 14th Five Year Plan” Hubei Provincial Advantaged Characteristic Disciplines (Groups) Project of Wuhan University of Science and Technology (No. 2023C0102). We would like to express our gratitude to the National Development Research Institute of Peking University and China Social Science Research Center of Peking University for providing the data.

Conflict of Interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1869-3 and is accessible for authorized users.

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