SpringerLink
Log in

Air particulate pollution exposure associated with impaired cognition via microbiota gut-brain axis: an evidence from rural elderly female in northwest China

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

Abstract

This study aimed to reveal harm of exposure to indoor air pollution to cognitive function through “gut-brain-axis” among rural elderly residents. There were 120 participants recruited in rural villages of northwest China from December 2021 to February 2022. The cognitive level was assessed by eight-item ascertain dementia (AD) questionnaire, and indoor air pollution exposure was measured by air quality sensor. Inflammatory cytokines and oxidative stress-related index were detected in blood serum. Fecal samples were collected for gut microbiota analysis. The 120 participants were divided into impaired cognition (AD8) (81/67.5%) and cognition normal (NG) (39/32.5%). And there had more female in AD8 (FAD) (55/67.9%) than NG (FNG) (18/46.2%) (P = 0.003). Exposure of air pollution in FAD was higher than FNG (PM1, PM2.5, PM10, P < 0.001; NO2, P < 0.001; CO, P = 0.014; O3, P = 0.002). The risk of cognitive impairment increases 6.8%, 3.6%, 2.6%, 11%, and 2.4% in female for every 1 μg/m3 increased in exposure of PM1, PM2.5, PM10, NO2, and O3, separately. And GSH-Px and T-SOD in FAD were significantly lower than the FNG group (P = 0.011, P = 0.019). Gut microbiota in FAD is disordered with lower richness and diversity. Relative abundance of core bacteria Faecalibacterium (top 1 genus) in FAD was reduced (13.65% vs 19.81%, P = 0.0235), while Escherichia_Shigella and Akkermansia was increased. Correlation analysis showed Faecalibacterium was negatively correlated with age, and exposure of O3, PM1, PM2.5, and PM10; Akkermansia and Monoglobus were positively correlated with exposure of PM1, PM2.5 and PM10; Escherichia_Shigella was significantly positively correlated with NO2. Indoor air pollution exposure impaired cognitive function in elderly people, especially female, which may cause systemic inflammation, dysbiosis of the gut microbiota, and ultimately leading to early cognitive impairment through the gut-brain axis.

Graphical Abstract

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Data availability

The datasets presented in this study can be found in online repositories. The accession number(s) can be found in the article. And the detail data and materials are available on request.

References

  • Ali MU, Yu Y, Yousaf B, Munir MAM, Ullah S, Zheng CM, Kuang XX, Wong MH (2021) Health impacts of indoor air pollution from household solid fuel on children and women. J Hazard Mater 416:126127

    Article  CAS  Google Scholar 

  • Alkasir R, Li J, Li X, ** M, Zhu B (2017) Human gut microbiota: the links with dementia development. Protein Cell 8:90–102

    Article  CAS  Google Scholar 

  • Bailey MJ, Naik NN, Wild LE, Patterson WB, Alderete TL (2020) Exposure to air pollutants and the gut microbiota: a potential link between exposure, obesity, and type 2 diabetes. Gut Microbes 11:1188–1202

    Article  CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) Dada2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581

    Article  CAS  Google Scholar 

  • Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D et al (2017) Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging 49:60–68

    Article  CAS  Google Scholar 

  • Cheng Y, Selma-Royo M, Cao X, Calatayud M, Qi Q, Zhou J, Zeng LX, Garcia-Mantrana I, Collado MC, Han B (2022) Influence of geographical location on maternal-infant microbiota: study in two populations from Asia and Europe. Front Cell Infect Microbiol 11:663513

    Article  Google Scholar 

  • Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV, Guzzetta KE, Jaggar M, Long-Smith CM, Lyte JM, Martin JA, Molinero-Perez A, Moloney G, Morelli E, Morillas E et al (2019) The microbiota-gut-brain axis. Physiol Rev 99:1877–2013

    Article  CAS  Google Scholar 

  • Ehsanifar M, Montazeri Z, Zavareh MS, Rafati M, Wang J (2023) Cognitive impairment, depressive-like behaviors and hippocampal microglia activation following exposure to air pollution nanoparticles. Environ Sci Pollut Res Int 30(9):23527–23537

    Article  CAS  Google Scholar 

  • Galvin JE, Roe CM, Coats MA, Morris JC (2007) Patient’s rating of cognitive ability: using the AD8, a brief informant interview, as a self-rating tool to detect dementia. Arch Neurol 64:725–730

    Article  Google Scholar 

  • Galvin JE, Roe CM, Powlishta KK, Coats MA, Muich SJ, Grant E, Miller JP, Storandt M, Morris JC (2005) The AD8: a brief informant interview to detect dementia. Neurology 65:559–564

    Article  CAS  Google Scholar 

  • Galvin JE, Roe CM, **ong C, Morris JC (2006) Validity and reliability of the AD8 informant interview in dementia. Neurology 67:1942–1948

    Article  Google Scholar 

  • 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:e105–e125

    Article  Google Scholar 

  • Gordon SB, Bruce NG, Grigg J, Hibberd PL, Kurmi OP, Lam KB, Mortimer K, Asante KP, Balakrishnan K, Balmes J, Bar-Zeev N, Bates MN, Breysse PN, Buist S, Chen Z, Havens D, Jack D, **dal S, Kan H et al (2014) Respiratory risks from household air pollution in low- and middle-income countries. Lancet Respir Med 2:823–860

    Article  Google Scholar 

  • Jiang C, Li G, Huang P, Liu Z, Zhao B (2017) The gut microbiota and Alzheimer’s disease. J Alzheimers Dis 58:1–15

    Article  Google Scholar 

  • Jung CR, Lin YT, Hwang B (2015) Ozone, particulate matter, and newly diagnosed Alzheimer’s disease: a population-based cohort study in Taiwan. J Alzheimers Dis 44:573–584

    Article  CAS  Google Scholar 

  • Kreyling WG, Blanchard JD, Godleski JJ, Haeussermann S, Heyder J, Hutzler P, Schulz H, Sweeney TD, Takenaka S, Ziesenis A (1999) Anatomic localization of 24-and 96-h particle retention in canine airways. J Appl Physiol 87:269–284

    Article  CAS  Google Scholar 

  • Leiva GMA, Santibañez DA, Ibarra ES, Matus CP, Seguel R (2013) A five-year study of particulate matter (PM2.5) and cerebrovascular diseases. Environ Pollut 181:1–6

    Article  Google Scholar 

  • Li B, He Y, Ma J, Huang P, Du J, Cao L, Wang Y, **ao Q, Tang H, Chen S (2019) Mild cognitive impairment has similar alterations as Alzheimer’s disease in gut microbiota. Alzheimers Dement 15:1357–1366

    Article  Google Scholar 

  • Li T, Fang J, Tang S, Du H, Zhao L, Wang Y, Deng F, Liu Y, Du Y, Cui L, Shi W, Wang Y, Wang J, Zhang Y, Dong X, Gao Y, Shen Y, Dong L, Zhou H et al (2022) PM2.5 exposure associated with microbiota gut-brain axis: multi-omics mechanistic implications from the BAPE study. Innovation (Camb) 3:100213

    CAS  Google Scholar 

  • Liu LJ, Shi L, Li P, Ma XX, Hou XY, Jiang SJ, Lv J, Xu HM, Cheng Y, Han B (2022) Seasonal dynamics survey and association analysis of microbiota communities, antibiotic resistance genes distribution and biotoxicities characterization in landfill-leachate. Ecotox Environ Safe 245:114103

    Article  CAS  Google Scholar 

  • Liu P, Wu L, Peng G, Han Y, Tang R, Ge J, Zhang L, Jia L, Yue S, Zhou K, Li L, Luo B, Wang B (2019) Altered microbiomes distinguish Alzheimer’s disease from amnestic mild cognitive impairment and health in a Chinese cohort. Brain Behav Immun 80:633–643

    Article  Google Scholar 

  • Michaelson DM (2014) APOEε4: The most prevalent yet understudied risk factor for Alzheimer’s disease. Alzheimers Dement 10:861–868

    Article  Google Scholar 

  • Möller W, Häussinger K, Winkler-Heil R, Stahlhofen W, Meyer T, Hofmann W, Heyder J (2004) Mucociliary and long-term particle clearance in the airways of healthy nonsmoker subjects. J Appl Physiol 97:2200–2206

    Article  Google Scholar 

  • Mutlu EA, Comba IY, Cho T, Engen PA, Yazici C, Soberanes S, Hamanaka RB, Nigdelioglu R, Meliton AY, Ghio AJ, Budinger GRS, Mutlu GM (2018) Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ Pollut 240:817–830

    Article  CAS  Google Scholar 

  • Oliveros E, Ramirez M, Vazquez E, Barranco A, Gruart A, Delgado-Garcia JM, Buck R, Rueda R, Martin MJ (2016) Oral supplementation of 2′-fucosyllactose during lactation improves memory and learning in rats. J Nutr Biochem 31:20–27

    Article  CAS  Google Scholar 

  • Razavi M, Tolea MI, Margrett J, Martin P, Oakland A, Tscholl DW, Ghods S, Mina M, Galvin JE (2014) Comparison of 2 informant questionnaire screening tools for dementia and mild cognitive impairment: AD8 and IQCODE. Alzheimer Dis Assoc Disord 28:156–161

    Article  Google Scholar 

  • Sang S, Chu C, Zhang T, Chen H, Yang X (2022) The global burden of disease attributable to ambient fine particulate matter in 204 countries and territories, 1990-2019: A systematic analysis of the global burden of disease study 2019. Ecotoxicol Environ Saf 238:113588

    Article  CAS  Google Scholar 

  • Sheng C, Lin L, Lin H, Wang X, Han Y, Liu SL (2021) Altered gut microbiota in adults with subjective cognitive decline: the silcode study. J Alzheimers Dis 82:513–526

    Article  CAS  Google Scholar 

  • Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M et al (2011) Toward defining the preclinical stages of Alzheimer’s disease: recommendations from the national institute on aging-Alzheimer’s association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7:280–292

    Article  Google Scholar 

  • Ueda A, Shinkai S, Shiroma H, Taniguchi Y, Tsuchida S, Kariya T, Kawahara T, Kobayashi Y, Kohda N, Ushida K, Kitamura A, Yamada T (2021) Identification of Faecalibacterium prausnitzii strains for gut microbiome-based intervention in Alzheimer's-type dementia. Cell Rep Med 2:100398

    Article  CAS  Google Scholar 

  • Underwood E (2017) The polluted brain. Science 355:342

    Article  CAS  Google Scholar 

  • Vanseea de JRD, Forlenza AS, Forlenza OV (2018) Relevance of gutmicrobiota in cognition, behaviour and Alzheimer's disease. Pharmacol Res 136:29–34

    Article  Google Scholar 

  • Wang S, Wang P, Qi Q, Wang S, Meng X, Kan H, Zhu S, Zhang H (2023) Improved estimation of particulate matter in China based on multisource data fusion. Sci Total Environ 869:161552

    Article  CAS  Google Scholar 

  • Wei P, Ning Z, Ye S, Sun L, Yang F, Wong KC, Westerdahl D, Louie PKK (2018) Impact analysis of temperature and humidity conditions on electrochemical sensor response in ambient air quality monitoring. Sensors (Basel) 18:59

    Article  Google Scholar 

  • Weuve J, Puett RC, Schwartz J, Yanosky JD, Laden F, Grodstein F (2012) Exposure to particulate air pollution and cognitive decline in older women. Arch Intern Med 172:219–227

    Article  Google Scholar 

  • Wu YC, Lin YC, Yu HL, Chen JH, Chen TF, Sun Y, Wen LL, Yip PK, Chu YM, Chen YC (2015) Association between air pollutants and dementia risk in the elderly. Alzheimers Dement 1:220–228

    Google Scholar 

  • Xu Y, Yan J, Zhou P, Li J, Gao H, **a Y, Wang Q (2012) Neurotransmitter receptors and cognitive dysfunction in Alzheimer’s disease and Parkinson’s disease. Prog Neurobiol 97:1–13

    Article  Google Scholar 

  • Zhan X, Stamova B, ** LW, DeCarli C, Phinney B, Sharp FR (2016) Gram-negative bacterial molecules associate with Alzheimer disease pathology. Neurology 87:2324–2332

    Article  CAS  Google Scholar 

  • Zhao Y, Cong L, Jaber V, Lukiw WJ (2017) Microbiome-derived lipopolysaccharide enriched in the perinuclear region of Alzheimer’s disease brain. Front Immunol 8:1064

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge support from Dr. Jun Wang from Tongchuan Center for Disease Control and Prevention, Shaanxi, China.

Funding

This research was funded by the National Natural Science Foundation of China (No. 82173526; No. 42277422) and the Key Research and Development Project in Shaanxi Province, China (No. 2022ZDLNY01-10).

Author information

Author notes

  1. Jia Yuan and Hui Tan contributed equally to this work.

Authors and Affiliations

  1. School of Public Health, Health Science Center, **’an Jiaotong University, **’an, 710061, Shaanxi, China

    Jia Yuan, Yue Cheng, **nxin Ma, Si** Jiang, **nyao Hou, Shaoru Li, Lu Shi, Pu Li, Jia Lv & Bei Han

  2. Department of Rehabilitation Medicine, the First Affiliated Hospital of **’an Jiaotong University, **’an, China

    Hui Tan

  3. Key Laboratory for Disease Prevention and Control and Health Promotion of Shaanxi Province, **’an, 710061, Shaanxi, China

    Yue Cheng, Shaoru Li, Jia Lv & Bei Han

  4. School of Energy and Power Engineering, **’an Jiaotong University, **’an, 710049, Shaanxi, China

    Hongmei Xu

  5. Key Laboratory of Environment and Genes Related to Diseases (**’an Jiaotong University), Ministry of Education, **’an, China

    Bei Han

Authors
  1. Jia Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yue Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. **nxin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Si** Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. **nyao Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shaoru Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lu Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hongmei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jia Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Bei Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, H. T. and B. H.; methodology, J. Y. and Y. C.; software, Y. C. and S. R. L.; validation, X. X. M., S. J. J., and X. Y. H.; formal analysis, P. L. and L. S.; resources, H. M. X. and B. H.; data curation, P. L.; writing-original draft preparation, J. Y. and Y. C.; writing—review and editing, H. M. X., T. H., and B. H.; visualization, J. L. and S. R. L.; supervision, B. H.; project administration, J. L. and S. R. L.; funding acquisition, B. H. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Bei Han.

Ethics declarations

Institutional Review Board statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Medical Ethics Committee of Health Science Center, **'an Jiaotong University, China with approval number of 2018-553.

Informed consent

Informed consent was obtained from all subjects involved in the study.

Conflict of interest

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.

Supplementary information

ESM 1

Figure S1. Alpha diversity analysis in NG and AD8 groups. ACE (A), Chao1 (B), Shannon (C), Simpson(D). *, P<0.05, **, P<0.01. Table S1 The relative abundance compartment between AD and NG groups at genus level. Table S2 The relative abundance compartment between FAD and FNG groups at genus level. Table S3 The core microbiota at the genus level among 120 elderly participants. (DOCX 140 kb)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, J., Tan, H., Cheng, Y. et al. Air particulate pollution exposure associated with impaired cognition via microbiota gut-brain axis: an evidence from rural elderly female in northwest China. Environ Sci Pollut Res 31, 6398–6410 (2024). https://doi.org/10.1007/s11356-023-31504-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-31504-6

Keywords

Search

Navigation