Skip to main content
SpringerLink
Log in

Air pollution associated with cognitive decline by the mediating effects of sleep cycle disruption and changes in brain structure in adults

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

Abstract

The effects of air pollution on sleep and dementia remain unclear. The objective of this study was to investigate the effects of air pollution on cognitive function as mediated by the sleep cycle. A cross-sectional study design was conducted to recruit 4866 subjects on which PSG had been performed. Fifty of them were further given a cognitive function evaluation by the MMSE and CASI as well as brain images by CT and MRI. Associations of 1-year air pollution parameters with sleep parameters, cognitive function, and brain structure were examined. We observed that O3 was associated with a decrease in arousal, an increase in the N1 stage, and a decrease in the N2 stage of sleep. NO2 was associated with an increase in the N1 stage, a decrease in the N2 stage, and an increase in REM. PM2.5 was associated with a decrease in the N1 stage, increases in the N2 and N3 stages, and a decrease in REM. The N1 and N2 stages were associated with cognitive decline, but REM was associated with an increase in cognitive function. The N1 stage was a mediator of the effects of PM2.5 on the concentration domain of the MMSE. O3 was associated with an increase in the pars orbitalis volume of the left brain. NO2 was associated with increases in the rostral middle frontal volume, supramarginal gyrus volume, and transverse temporal volume of the left brain, and the pars opercularis volume of the right brain. PM2.5 was associated with increases in the pars triangularis volume of the left brain and the fusiform thickness of the right brain. In conclusion, we observed that air pollution was associated with cognitive decline by mediating effects on the sleep cycle with changes in the brain structure in controlling executive, learning, and language functions in adults.

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

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

3% ODI :

3% Oxygen desaturation index

AHI :

Apnea-hypopnea index

SaO 2 :

Arterial oxygen saturation

BMI :

Body mass index

CO :

Carbon monoxide

CASI :

Cognitive Abilities Screening Instrument

CT :

Computed tomography

CPAP :

Continuous positive airway pressure

GABA :

Gamma-aminobutyric acid

GMC :

Gray matter changes

IQR :

Interquartile range

LUR :

Land-use regression

MRI :

Magnetic resonance imaging

MMSE :

Mini-Mental State Examination

NO 2 :

Nitrogen dioxide

NOx :

Nitrogen oxides

NREM :

Non-rapid eye movement

ODI :

Oxygen desaturation index

PM 10 :

Particulate matter less than 10 μm in aerodynamic diameter

PM 2.5 :

Particulate matter less than 2.5 μm in aerodynamic diameter

PSG :

Polysomnography

REM :

Rapid eye movement

RDI :

Respiratory disturbance index

TST :

Total sleep time

WASO :

Wake after sleep onset

WMC :

White matter changes

WHO :

World Health Organization

References

  • Ardila A, Bernal B, Rosselli M (2016) How Localized are Language Brain Areas? A Review of Brodmann Areas Involvement in Oral Language. Arch Clin Neuropsychol 31, 112-22

  • Aretz B, Janssen F, Vonk JM, Heneka MT, Boezen HM, Doblhammer G (2021) Long-term exposure to fine particulate matter, lung function and cognitive performance: A prospective Dutch cohort study on the underlying routes. Environ Res 201, 111533

  • Shalom DB, Poeppel D (2008) Functional anatomic models of language: assembling the pieces. Neuroscientist 14, 119-27

  • Billings ME, Gold D, Szpiro A, Aaron CP, Jorgensen N, Gassett A, Leary PJ, Kaufman JD, Redline SR (2019) The Association of Ambient Air Pollution with Sleep Apnea: The Multi-Ethnic Study of Atherosclerosis. Ann Am Thorac Soc 16, 363-370

    Article  Google Scholar 

  • Blackwell T, Yaffe K, Ancoli-Israel S, Schneider JL, Cauley JA, Hillier TA, Fink HA, Stone KL (2006) Poor sleep is associated with impaired cognitive function in older women: the study of osteoporotic fractures. J Gerontol A Biol Sci Med Sci 61, 405-10

  • Boothby H, Blizard R, Livingston G, Mann AH (1994) The Gospel Oak Study stage III: the incidence of dementia. Psychol Med 24:89–95

    Article  CAS  Google Scholar 

  • Bose S, Ross KR, Rosa MJ, Chiu YM, Just A, Kloog I, Wilson A, Thompson J, Svensson K, Rojo MMT, Schnaas L, Osorio-Valencia E, Oken E, Wright RO, Wright RJ (2019) Prenatal particulate air pollution exposure and sleep disruption in preschoolers: Windows of susceptibility. Environ Int 124, 329-335

  • Brooks PL, Peever JH (2011) Impaired GABA and glycine transmission triggers cardinal features of rapid eye movement sleep behavior disorder in mice. J Neurosci 31, 7111-21

  • Chen G, Xiang H, Mao Z, Huo W, Guo Y, Wang C, Li S (2019) Is long-term exposure to air pollution associated with poor sleep quality in rural China? Environ Int 133, 105205

  • Chen MC, Wang CF, Lai BC, Hsieh SW, Chen SC, Hung CH, Kuo CH (2021) Air Pollution Is Associated with Poor Cognitive Function in Taiwanese Adults. Int J Environ Res Public Health 18

  • Chen T-H, Hsu Y-C, Zeng Y-T, Candice Lung S-C, Su H-J, Chao HJ, Wu C-D (2020) A hybrid kriging/land-use regression model with Asian culture-specific sources to assess NO2 spatial-temporal variations. Environ Pollut 259:113875

    Article  CAS  Google Scholar 

  • Cho J et al. (2020) Long-Term Ambient Air Pollution Exposures and Brain Imaging Markers in Korean Adults: The Environmental Pollution-Induced Neurological EFfects (EPINEF) Study. Environ Health Perspect 128, 117006

  • Crous-Bou M, Gascon M, Gispert JD, Cirach M, Sánchez-Benavides G, Falcon C, Arenaza-Urquijo EM, Gotsens X, Fauria K, Sunyer J, Nieuwenhuijsen MJ, Luis Molinuevo J (2020) Impact of urban environmental exposures on cognitive performance and brain structure of healthy individuals at risk for Alzheimer's dementia. Environ Int 138, 105546

  • Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11, 114-26

  • Gatto NM, Henderson VW, Hodis HN, St John JA, Lurmann F, Chen JC, Mack WJ (2014) Components of air pollution and cognitive function in middle-aged and older adults in Los Angeles. Neurotoxicology 40:1–7

    Article  CAS  Google Scholar 

  • Hardy J (1996) New insights into the genetics of Alzheimer’s disease. Ann Med 28:255–258

    Article  CAS  Google Scholar 

  • Li CY, Li CH, Martini S, Hou WH (2019) Association between air pollution and risk of vascular dementia: a multipollutant analysis in Taiwan. Environ Int 133:105233

    Article  CAS  Google Scholar 

  • Liu S, Pan J, Tang K, Lei Q, He L, Meng Y, Cai X, Li Z (2020) Sleep spindles, K-complexes, limb movements and sleep stage proportions may be biomarkers for amnestic mild cognitive impairment and Alzheimer's disease. Sleep Breath 24, 637-651

  • Lo K, Chiang LL, Hsu SM, Tsai CY, Wu D, Chou CJ, Chuang HC, Liu WT (2021) Association of short-term exposure to air pollution with depression in patients with sleep-related breathing disorders. Sci Total Environ 786:147291

    Article  CAS  Google Scholar 

  • Lubczyńska MJ, Muetzel RL, El Marroun H, Hoek G, Kooter IM, Thomson EM, Hillegers M, Vernooij MW, White T, Tiemeier H, Guxens M (2021) Air pollution exposure during pregnancy and childhood and brain morphology in preadolescents. Environ Res 198, 110446

  • Monti JM (2011) Serotonin control of sleep-wake behavior. Sleep Med Rev 15, 269-81

  • Nakamura-Palacios EM, Souza RS, Zago-Gomes MP, de Melo AM, Braga FS, Kubo TT, Gasparetto EL (2014) Gray matter volume in left rostral middle frontal and left cerebellar cortices predicts frontal executive performance in alcoholic subjects. Alcohol Clin Exp Res 38, 1126-33

  • WHO (2016) Ambient (outdoor) air quality and health. Fact sheet, updated September 2016

  • Oudin A, Forsberg B, Adolfsson AN, Lind N, Modig L, Nordin M, Nordin S, Adolfsson R, Nilsson LG (2016) Traffic-related air pollution and dementia incidence in Northern Sweden: a longitudinal study. Environ Health Perspect 124:306–312

    Article  CAS  Google Scholar 

  • Pase MP, Himali JJ, Grima NA, Beiser AS, Satizabal CL, Aparicio HJ, Thomas RJ, Gottlieb DJ, Auerbach SH, Seshadri S (2017) Sleep architecture and the risk of incident dementia in the community. Neurology 89, 1244-1250

  • Paz C, Huitron-Resendiz S (1996) The effects of ozone exposure on the sleep-wake cycle and serotonin contents in the pons of the rat. Neurosci Lett 204, 49-52

  • Rubinstein DY, Camarillo-Rodriguez L, Serruya MD, Herweg NA, Waldman ZJ, Wanda PA, Sharan AD, Weiss SA, Sperling MR (2021) Contribution of left supramarginal and angular gyri to episodic memory encoding: An intracranial EEG study. Neuroimage 225, 117514

  • Ruehland WR, Rochford PD, O’Donoghue FJ, Pierce RJ, Singh P, Thornton AT (2009) The new AASM criteria for scoring hypopneas: impact on the apnea hypopnea index. Sleep 32:150–157

    Article  Google Scholar 

  • SchikowskiT, Altug H (2020) The role of air pollution in cognitive impairment and decline. Neurochem Int. 104708

  • Shatzmiller RA, Gonzalez A, Ko D, Zeidler M (2010) Sleep stage scoring [https://emedicine.medscape.com/article/1188142-overview]

  • Shen YL, Liu WT, Lee KY, Chuang HC, Chen HW, Chuang KJ (2018) Association of PM2.5 with sleep-disordered breathing from a population-based study in Northern Taiwan urban areas. Environ Pollut 233:109–113

    Article  CAS  Google Scholar 

  • Shih CH, Chen JK, Kuo LW, Cho KH, Hsiao TC, Lin ZW, Lin YS, Kang JH, Lo YC, Chuang KJ, Cheng TJ, Chuang HC (2018) Chronic pulmonary exposure to traffic-related fine particulate matter causes brain impairment in adult rats. Part Fibre Toxicol 15:44

    Article  CAS  Google Scholar 

  • Teng EL, Hasegawa K, Homma A, Imai Y, Larson E, Graves A, Sugimoto K, Yamaguchi T, Sasaki H, Chiu D et al (1994) The Cognitive Abilities Screening Instrument (CASI): a practical test for cross-cultural epidemiological studies of dementia. Int Psychogeriatr 6:45–58 (discussion 62)

    Article  CAS  Google Scholar 

  • Thiel VE, Audus KL (2001) Nitric oxide and blood-brain barrier integrity. Antioxid Redox Signal 3, 273-8

  • Tsai DH, Riediker M, Wuerzner G, Maillard M, Marques-Vidal P, Paccaud F, Vollenweider P, Burnier M, Bochud M (2012) Short-term increase in particulate matter blunts nocturnal blood pressure dipping and daytime urinary sodium excretion. Hypertension 60:1061–1069

    Article  CAS  Google Scholar 

  • Tung NT, Ho KF, Niu X, Sun J, Shen Z, Wu F, Cao J, Dung HB, Thuy TPC, Hsiao TC, Liu WT, Chuang HC (2021a) Loss of E-cadherin due to road dust PM(2.5) activates the EGFR in human pharyngeal epithelial cells. Environ Sci Pollut Res Int 28, 53872-53887

  • Tung NT, Lee YL, Lin SY, Wu CD, Dung HB, Thuy TPC, Kuan YC, Tsai CY, Lo CC, Lo K, Ho KF, Liu WT, Chuang HC (2021b) Associations of ambient air pollution with overnight changes in body composition and sleep-related parameters. Sci Total Environ 791:148265

  • Vertes RP, Eastman KE (2000) The case against memory consolidation in REM sleep. Behav Brain Sci 23:867–876

    Article  CAS  Google Scholar 

  • Weinreich G, Wessendorf TE, Pundt N, Weinmayr G, Hennig F, Moebus S, Möhlenkamp S, Erbel R, Jöckel KH, Teschler H, Hoffmann B (2015) Association of short-term ozone and temperature with sleep disordered breathing. Eur Respir J 46, 1361-9

  • Wortmann M (2012) Dementia: a global health priority—highlights from an ADI and World Health Organization report. Alzheimers Res Ther 4:40

    Article  Google Scholar 

  • Wu C-D, Zeng Y-T, Lung S-CC (2018) A hybrid kriging/land-use regression model to assess PM2.5 spatial-temporal variability. Sci Total Environ 645:1456–1464

    Article  CAS  Google Scholar 

  • Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O’Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373–377

    Article  CAS  Google Scholar 

  • Yan W, Ji X, Shi J, Li G, Sang N (2015) Acute nitrogen dioxide inhalation induces mitochondrial dysfunction in rat brain. Environ Res 138, 416-24

  • Yao Y, Lv X, Qiu C, Li J, Wu X, Zhang H, Yue D, Liu K, Eshak ES, Lorenz T, Anstey KJ, Livingston G, Xue T, Zhang J, Wang H, Zeng Y (2022) The effect of China's Clean Air Act on cognitive function in older adults: a population-based, quasi-experimental study. Lancet Healthy Longev 3, e98-e108

  • Yildiz Gulhan P, Gulec Balbay E, Elverisli MF, Ercelik M, Arbak P (2020) Do the levels of particulate matters less than 10 mum and seasons affect sleep? Aging Male 23:36–41

    Article  CAS  Google Scholar 

  • Yokota S, Moriya N, Iwata M, Umezawa M, Oshio S, Takeda K (2013) Exposure to diesel exhaust during fetal period affects behavior and neurotransmitters in male offspring mice. J Toxicol Sci 38, 13-23

  • Yuan D, Luo D, Kwok VPY, Zhou Y, Tian H, Yu Q, An J, Gao JH, Qiu S, Tan LH (2021): Myeloarchitectonic Asymmetries of Language Regions in the Human Brain. Cereb Cortex 31, 4169-4179

  • Zanobetti A, Redline S, Schwartz J, Rosen D, Patel S, O'Connor GT, Lebowitz M, Coull BA, Gold DR (2010) Associations of PM10 with sleep and sleep-disordered breathing in adults from seven U.S. urban areas. Am J Respir Crit Care Med 182, 819-25

  • Zhao X, Yang T, Cheng F, Yang S, Zhu W, Li S, Fan Y (2021) Abnormalcortical thickness in relapsing-remitting multiple sclerosis, correlations with cognition impairment, and effect of modified Bushenyisui decoction on cognitive function of multiple sclerosis. J Tradit Chin Med 41, 316-325

  • Zou ML, Jiang CB, Chen YH, Wu CD, Candice Lung SC, Chien LC, Kallawicha K, Yang YT, Lo YC, Chao HJ (2021) Effects of air pollution, land-use type, and maternal mental health on child development in the first two years of life in the Greater Taipei area. Environ Res 197, 111168

Download references

Acknowledgements

The authors heartedly thank all of the staff in the Sleep Center of Shuang Ho Hospital for technical assistance during this project.

Funding

This study was funded by the Ministry of Science and Technology of Taiwan (MOST 109–2314-B-038–093-MY3).

Author information

Author notes

  1. Chen-Chen Lo and Wen-Te Liu are equal first authors.

Authors and Affiliations

  1. School of Respiratory Therapy, College of Medicine, Taipei Medical University, 250 Wuxing Street, Taipei, 11031, Taiwan

    Chen-Chen Lo, Wen-Te Liu, Lo Kang & Hsiao-Chi Chuang

  2. Sleep Center, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Chen-Chen Lo, Wen-Te Liu & Lo Kang

  3. Division of Pulmonary Medicine, Department of Internal Medicine, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Wen-Te Liu & Hsiao-Chi Chuang

  4. Department of Radiology, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Yueh-Hsun Lu

  5. Department of Radiology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Yueh-Hsun Lu

  6. Department of Neurology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Dean Wu

  7. Department of Neurology, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Dean Wu

  8. Department of Geomatics, National Cheng Kung University, Tainan, Taiwan

    Chih-Da Wu

  9. National Institute of Environmental Health Sciences, National Health Research Institutes, Miaoli, Taiwan

    Chih-Da Wu

  10. Department of Biomedical Engineering, National Yang Ming Chiao Tung University, Taipei, Taiwan

    Ting-Chieh Chen, Yu-Ting Fang & You-Yin Chen

  11. The Ph.D. Program for Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University, Taipei, Taiwan

    Yu-Chun Lo & You-Yin Chen

  12. Industrial Ph.D. Program of Biomedical Science and Engineering, National Yang Ming Chiao Tung University, Taipei, Taiwan

    You-Yin Chen

  13. Department of Civil and Environmental Engineering, Imperial College London, London, UK

    Cheng-Yu Tsai

  14. Department of Microbiology and Immunology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Yueh-Lun Lee

  15. School of Public Health, College of Public Health, Taipei Medical University, Taipei, Taiwan

    Kai-Jen Chuang

  16. Department of Public Health, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Kai-Jen Chuang

  17. JC School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong, China

    Kin-Fai Ho

  18. Department of Occupational Safety and Health, College of Public Health, China Medical University, Taichung, Taiwan

    Ta-Yuan Chang

  19. Cell Physiology and Molecular Image Research Center, Wan Fang Hospital, Taipei Medical University, Taipei, Taiwan

    Hsiao-Chi Chuang

Authors
  1. Chen-Chen Lo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wen-Te Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yueh-Hsun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dean Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chih-Da Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ting-Chieh Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yu-Ting Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yu-Chun Lo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. You-Yin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lo Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Cheng-Yu Tsai
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yueh-Lun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Kai-Jen Chuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Kin-Fai Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Ta-Yuan Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Hsiao-Chi Chuang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HCC and CCL contributed to the completion of interpretation of the data and the manuscript. HCC and WTL contributed substantially to the concept, design, interpretation of the data, and completion of the study and manuscript. YHL, TCC, YTF, YCL, and YYC contributed to brain image collection and analyses. DW contributed to dementia data collection. LK and CYT contributed to sleep data collection. CDW, KJC, and TYC contributed to air pollution data collection. YLL and KFH contributed to critical revision of the manuscript for important intellectual content. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Hsiao-Chi Chuang.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Ethics Committee of the Taipei Medical University-Joint Institutional Review Board (TMU-JIRB no. N201910048; Taipei, Taiwan).

All patients received written information and provided informed consent.

Consent for publication

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.

Capsule of main finding

The significance and novelty of this study were that air pollution was associated with cognitive decline by mediating effects on the sleep cycle with changes in brain structure in adults, thereby could increase the risks of dementia.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 698 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lo, CC., Liu, WT., Lu, YH. et al. Air pollution associated with cognitive decline by the mediating effects of sleep cycle disruption and changes in brain structure in adults. Environ Sci Pollut Res 29, 52355–52366 (2022). https://doi.org/10.1007/s11356-022-19482-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-19482-7

Keywords

Search

Navigation