Ambient Air Pollution Increases the Risk of Cerebrovascular and Neuropsychiatric Disorders through Induction of Inflammation and Oxidative Stress
Abstract
:1. Introduction
2. Air Pollution Mixtures and Sources
3. Pathophysiology of Air-Pollution-Induced Disorders
4. Evidence from Human and Animal Studies
4.1. Human Observational/Epidemiological Studies
4.1.1. Cerebrovascular Events
4.1.2. Dementia
4.1.3. Parkinson’s Disease
4.1.4. Cognitive Decline
4.1.5. Headache and Migraine
4.1.6. Epilepsy
4.1.7. Neurodevelopmental Disorders
4.1.8. Mental Disorders
4.2. Animal Experimental Studies
5. Neurological Complications of Coronavirus Disease 2019 (COVID-19) and Air Pollution
6. Conclusions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
3NT | 3-nitrotyrosine |
4-HNE | 4-hydroxynonenal |
8-oxoG | 8-hydroxyguanosine |
Aβ | amyloid beta peptide |
ACE2 | angiotensin-converting enzyme 2 |
BBB | blood–brain barrier |
CD68 | cluster of differentiation 68—also macrosialin |
CI | confidence interval |
CNS | central nervous system |
COVID-19 | coronavirus disease 2019 |
COX-2 | inducible cyclooxygenase (isoform 2) |
DEP | diesel exhaust particles |
EC | elemental or black carbon |
γ-H2AX | H2A histone family member X |
GBD | Global Burden of Disease |
GEMM | Global Exposure-Mortality Model |
gp91phox | catalytic subunit of the phagocytic NADPH oxidase (isoform 2)—also NOX-2 |
H3K9me2/me3 | histone 3 lysine 9 di- and trimethylation (epigenetic marks) |
HR | hazard ratio |
ICAM-1 | intercellular adhesion molecule 1 |
INF-γ | interferon gamma |
IHME | Institute for Health Metrics and Evaluation |
IL-1β | interleukin-1β |
iNOS | inducible nitric oxide synthase |
IQR | interquartile range |
Ly6g | lymphocyte antigen 6 complex locus G6D |
MCP-1 | monocyte chemoattractant protein-1—also CCL2 |
MyD88 | myeloid differentiation primary response 88 protein |
NFκB | nuclear factor ‘kappa-light- chain-enhancer’ of activated B-cells |
NOx | oxides of nitrogen |
NOX-2 | catalytic subunit of the phagocytic NADPH oxidase (isoform 2)—also gp91phox |
OC | organic carbon |
OR | odds ratio |
oxLDL | oxidized low density lipoprotein |
p47phox | regulatory subunit of the phagocytic NADPH oxidase (isoform 2) |
PAHs | polycyclic aromatic hydrocarbons |
PCBs | polychlorinated biphenyls |
PM0.1 | particulate matter < 0.1 µm (ultrafine particles) |
PM2.5 | particulate matter < 2.5 µm (fine particles) |
PM10 | particulate matter with a diameter between 2.5 and 10 µm (coarse particles) |
RANTES | chemokine (C-C motif) ligand 5—also CCL5 |
ROS | reactive oxygen species |
RR | relative risk |
SARS-CoV-2 | severe acute respiratory syndrome coronavirus 2 |
SNS | sympathetic nervous system |
TLR4 | Toll-like receptor 4 |
TNFα | tumor necrosis factor alpha |
TNFR2 | tumor necrosis factor receptor type 2 |
UK | United Kingdom |
US | United States |
VOCs | volatile organic compounds |
WHO | World Health Organization |
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Studies and Major Outcomes | Ref. |
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Stroke (cerebral ischemia) | |
Seasonal variation in air particulate matter (PM10) exposure-induced ischemia-like injuries in the rat brain was attributed to varying toxin (PAHs) loading of the particles | [118] |
SO2 inhalation contributes to the development and progression of ischemic stroke in the rat brain by enhanced endothelin-1 activity and inflammation (iNOS, COX-2, and ICAM-1 mRNA) followed by activation of caspase-3 and higher cerebral infarct volume | [119] |
Air pollutants (PM generated by different engines and aluminum sulfate aerosols) caused cortical selective neuronal loss, nuclear pyknosis, karyolysis and karyorrhexis as well as activation of microglia and astrocytes (also features of stroke and other neurological disease) as revealed by magnetic resonance imaging | [120] |
Stroke damage is aggravated by nano-size particulate matter in mice, secondary to more pronounced DNA damage (8-hydroxyguanosine) and oxidative stress (gp91phox, p47phox) as well as higher number of inflammatory cells (CD68 and Ly6g positive) | [121] |
Glutamatergic neurons in rodent models respond to nanoscale particulate urban air pollutants (PM0.2) in mice, suggesting additive effects of air pollution and ischemic stroke on cerebral damage | [122] |
Astrocyte activation plays a role in fine particulate matter (PM2.5)-dependent aggravation of ischemic stroke in male rats | [123] |
Dementia (Alzheimer’s disease) | |
Diesel engine exhaust accelerates amyloid β42 plaque formation in the 5X Familial AD mouse model of Alzheimer’s disease, although no additive effects on spatial working memory deficits (assessed by Y-maze and X-maze tests) and markers of inflammation (IL-1β, RANTES and MCP-1) were observed | [124] |
Central role of Toll-like receptor 4 for glial inflammatory responses (higher TLR4, MyD88, TNFα, and TNFR2 mRNA) to air pollution (PM0.2) in rats leading to a neuroinflammatory, accelerated cognitive aging and dementia-like phenotype | [125] |
NO2 inhalation promotes Alzheimer’s disease-like progression via cyclooxygenase-2-derived prostaglandin E2 modulation, altered astrocyte and microglia function, all of which leading to deterioration of spatial learning and memory as well as aggravated amyloid β42 accumulation in wildtype C57BL/6J or Alzheimer’s disease-prone APP/PS1 mice | [126] |
Neurotoxicity of diesel exhaust nanoparticles in the rat brain is associated with increased levels of pro-inflammatory cytokines, amyloid β42, reactive oxygen species, hydrogen peroxide, nitrogen oxide metabolites and apurinic/apyrimidinic sites (DNA damage) | [127] |
Exposure of mice to particulate urban air pollution reduced the repressive epigenetic marks (H3K9me2/me3) and increased DNA damage (γ-H2AX) as well as Alzheimer’s disease hallmarks (hyperphosphorylated tau and amyloid-β plaques) in the brain | [128] |
Traffic-related air pollutants (nano-sized PM) promote neuronal amyloidogenesis (amyloid-β deposition) through oxidative damage (4-HNE, 3NT) in lipid rafts of mice | [129] |
Parkinson’s disease | |
Developmental exposure to concentrated ambient ultrafine particle air pollution (similar to the paraquat and maneb model) cause a Parkinson’s disease phenotype in male mice with locomotor dysfunction and dopaminergic and glutamatergic changes | [130] |
Cognitive and memory impairment | |
Selective memory and behavioral alterations after ambient ultrafine particulate matter exposure (using the Harvard ultrafine concentrated ambient particle system) in aged 3xTgAD Alzheimer’s disease mice | [131] |
Developmental exposure to low level concentrated ambient ultrafine particle air pollution and cognitive dysfunction in mice revealed by complementary learning (repeated learning), memory (novel object recognition, NOR), impulsive-like behavior (differential reinforcement of low rate (DRL), schedule of reward and delay of reward (DOR)), motor activity (locomotor behavior) and motivation (progressive ratio schedule) assessment assays | [132] |
Activation of NLRP3 in microglia exacerbates diesel exhaust particles-induced impairment in learning and memory in mice | [133] |
Impairment of learning and memory, induction of oxidative stress and dysregulation of monoamine neurotransmitters in the brains of mice by exposure to volatile organic compounds and carbon monoxide mixtures | [134] |
PM2.5, SO2 and NO2 co-exposure impairs neurobehavior and induces mitochondrial injuries in the mouse brain | [135] |
Effects of diesel engine exhaust origin secondary organic aerosols on novel object recognition ability and maternal behavior in mice | [136] |
Exposure to ambient dusty particulate matter impairs spatial memory and hippocampal long-term potentiation by increasing brain inflammation and oxidative stress in rats | [30] |
Mental disorders | |
Involvement of oxidative stress and mitochondrial mechanisms in air pollution (simulated vehicle exhaust)-related neurobiological impairments in rats leading to anxiety- and depression-like behavior | [137] |
Ambient PM2.5 exposure caused depressive-like responses in mice through Nrf2/NLRP3 signaling pathway and altered inflammation | [138] |
Psychological impact of vehicle exhaust exposure (CO, CO2, NO2) as revealed by anxiety- and depression-like behavior as well as impaired memory in rats | [139] |
Ozone exposure of rats (Flinders Sensitive Line translational model) caused neurobiological oxidative stress and a depression-like phenotype | [140] |
Other adverse effects on the brain (e.g., impaired BBB) | |
Early postnatal exposure to ultrafine particulate matter air pollution leads to dysregulated CNS neurotransmitters, cytokines and glial activation preferentially in male mice. In addition, lateral ventricle dilation (=ventriculomegaly) was observed in exposed male mice, which is associated with poor neurodevelopmental outcome, autism, and schizophrenia | [141] |
Exposure to traffic-generated air pollutants mediates alterations in brain microvascular integrity (disrupted blood-brain barrier) and enhanced oxidized low density lipoprotein signaling in wildtype mice on a high-fat diet, indicating additive adverse effects of obesity and air pollution on brain function | [142] |
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Hahad, O.; Lelieveld, J.; Birklein, F.; Lieb, K.; Daiber, A.; Münzel, T. Ambient Air Pollution Increases the Risk of Cerebrovascular and Neuropsychiatric Disorders through Induction of Inflammation and Oxidative Stress. Int. J. Mol. Sci. 2020, 21, 4306. https://doi.org/10.3390/ijms21124306
Hahad O, Lelieveld J, Birklein F, Lieb K, Daiber A, Münzel T. Ambient Air Pollution Increases the Risk of Cerebrovascular and Neuropsychiatric Disorders through Induction of Inflammation and Oxidative Stress. International Journal of Molecular Sciences. 2020; 21(12):4306. https://doi.org/10.3390/ijms21124306
Chicago/Turabian StyleHahad, Omar, Jos Lelieveld, Frank Birklein, Klaus Lieb, Andreas Daiber, and Thomas Münzel. 2020. "Ambient Air Pollution Increases the Risk of Cerebrovascular and Neuropsychiatric Disorders through Induction of Inflammation and Oxidative Stress" International Journal of Molecular Sciences 21, no. 12: 4306. https://doi.org/10.3390/ijms21124306