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Association of criteria pollutants with plasma hemostatic/inflammatory markers: a population-based study
Abstract
To elucidate the health effects of air pollution, the short-term association of criteria pollutants (particles <10 microm in diameter [PM(10)], O(3), CO, NO(2), and SO(2)) with hemostatic and inflammatory markers were examined using a population-based sample of 10,208 middle-age males and females of the biracial cohort of Atherosclerosis Risk in Communities (ARIC) study. For each participant, we calculated the following pollutant exposures 1-3 days prior to the randomly allocated cohort examination date: PM(10), CO, NO(2), and SO(2) as 24-h averages, and O(3) as an 8-h average of the hourly measures. The hemostatic/inflammatory factors included fibrinogen, factor VIII-C, von Willebrand factor (vWF), albumin, and white blood cell count (WBC). Linear regression models were used to adjust for cardiovascular disease (CVD) risk factors, demographic and socioeconomic variables, and relevant meteorological variables. One standard deviation (SD) increment of PM(10) (12.8 microg/m(3)) was significantly (P < 0.05) associated with 3.93% higher of vWF among diabetics and 0.006 g/dl lower of serum albumin among persons with a history of CVD. One SD increment of CO (0.60 p.p.m.) was significantly (P < 0.01) associated with 0.018 g/dl lower of serum albumin. Significant curvilinear associations, indicative of threshold effects, for PM(10) with factor VIII-C, O(3) with fibrinogen and vWF, and SO(2) with factor VIII-C, WBC, and serum albumin were found. This population-based study suggest that the hemostasis/inmflammation markers analyzed, which are linked to higher risk of CHD, are associated adversely with environmentally relevant ambient pollutants, with the strongest associations in the upper range of the pollutant distributions, and in persons with a positive history of diabetes and CHD.
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“Increased exposure to ambient ozone has been associated with increased levels of hemostatic markers, including fibrinogen (48–50), von Willebrand factor (49), and plasminogen activator inhibitor-1 (48).”
From Ozone pollution: A Major health hazard worldwide (2019) · cites this paper as [49]
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“An examination of biomarkers in individuals with diabetes who were exposed to PM revealed mixed results, including an increase in von Willebrand factor (Liao et al. 2005), an increase in thiobarbituric acid but no increases in CRP or tumor necrosis factorα (Liu et al.”
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“…of inflammatory pathways (Baccarelli et al. 2007b; Liao et al. 2004; Peters et al. 2001), alterations in blood coagulation (Baccarelli et al. 2007a; Liao et al. 2005), endothelial injury and dysfunction (Brook et al. 2002; Ikeda et al. 1998), and alterations in the autonomic control of the heart…”
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InfluentialGIS Approaches for the Estimation of Residential-Level Ambient PM Concentrations
Liao, D., Peuquet, D. J., Duan, Y., Whitsel, E. A., Dou, J., Smith, R. L., Lin, H.-M., Chen, J., & HEISS, G. M. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9169 · Cited by 164
Short-Term Exposure to Ambient Air Pollution and Biomarkers of Systemic Inflammation
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Effects of particulate matter on inflammatory markers in the general adult population
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ResultMechanisms of Inhaled Fine Particulate Air Pollution–Induced Arterial Blood Pressure Changes
Bartoli, C. R., Wellenius, G. A., Diaz, E. A., Lawrence, J. E., Coull, B. A., Akiyama, I., Lee, L. M., Okabe, K., Verrier, R. L., & Godleski, J. J. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11573 · Cited by 137
“…exposure was associated with increased arterial blood pressure changes is consistent with most (Auchincloss et al. 2008; Ibald-Mulli et al. 2001; Linn et al. 1999; Urch et al. 2005; Zanobetti et al. 2004) but not all (Harrabi et al. 2006; Ibald-Mulli et al. 2001, 2004; Linn et al. 1999; Urch et…”
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“…air pollution and systemic inflammation arises from studies demonstrating some type of correlation between inflammatory biomarkers, and the amount of outdoor atmospheric particles and volatile gases (Diez Roux et al., 2006; Ghio et al., 2003; Liao et al., 2005; Schwartz, 2001; Seaton et al., 1999).”
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Gawda, A., Majka, G., Nowak, B., & Marcinkiewicz, J. (2017) · Central European Journal of Immunology · doi:10.5114/ceji.2017.70975 · Cited by 113
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THE LONG-TERM DYNAMICS OF RACIAL/ETHNIC INEQUALITY IN NEIGHBORHOOD AIR POLLUTION EXPOSURE, 1990-2009
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“…and determinants of the exposure itself (c.f., Barakat-Haddad et al., 2012 ; Delfino et al., 2009 ; Diez Roux et al., 2008 ; Jerrett et al., 2009; Liao et al., 2004 ; Miller et al., 2007 ; Whitsel et al., 2009 ) or, when individual exposure is more central to the study (c.f., Crowder and Downey,…”
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Cozzi, E., Hazarika, S., Stallings, H. W., Cascio, W. E., Devlin, R. B., Lust, R. M., Wingard, C. J., & Scott, M. R. V. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01362.2005 · Cited by 102
“(33) have shown that short-term exposure to coarse PM is associated with plasma inflammatory and hemostatic risk factors for cardiovascular disease (33).”
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Goodman, J. E., Prueitt, R. L., Sax, S. N., Pizzurro, D. M., Lynch, H. N., Zu, K., & Venditti, F. J. (2015) · Critical Reviews in Toxicology · doi:10.3109/10408444.2015.1031371 · Cited by 96
“Of two large-scale, cross-sectional studies in the US, Schwartz (2001) reported a non-signifi cant, positive association between ozone and fi brinogen levels at a lag of 0 days, and Liao et al. (2005) reported a signifi cant nonlinear eff ect of ozone on fi brinogen at a lag of 1 day.”
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Long-and Short-Term Exposure To Air Pollution and Inflammatory/Hemostatic Markers in Midlife Women
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“, 2007; Lux and Pope, 2009), and on blood coagulation (Liao et al., 2005) The latter included longer-term PM effects on atherosclerosis and plaque rupture (Suwa et al.”
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Vascular Effects of Ultrafine Particles in Persons with Type 2 Diabetes
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“[59] examined data from the ARIC study that included 10,208 middle-aged people, and found ozone exposure was associated with increases in fibrinogen and vWF levels, with greater effects in people with diabetes and cardiovascular disease.”
MethodHua, Q., Meng, X., Gong, J., Qiu, X., Shang, J., Xue, T., & Zhu, T. (2024) · Fundamental Research · doi:10.1016/j.fmre.2024.02.016 · Cited by 51
“…exposure to O 3 was related to increased levels of some coagulation factors, such as fibrinogen, plasminogen activator fibrinogen inhibitor-1 (PAI-1), tissue factor, and von Willebrand factor [ 182 , 193 , 220 ], along with decreased levels of anticoagulant proteins such as thrombomodulin [221] .”
Ganesh, H. S., Seo, K., Fritz, H., Edgar, T. F., Novoselac, A., & Bâldea, M. (2020) · Journal of Building Engineering · doi:10.1016/j.jobe.2020.101552 · Cited by 48
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“These findings were counterintuitive, because the prothrombotic effects of PM (Liao et al. 2005) and estrogen (Curb et al.”
BackgroundPlasma biomarkers in carbon monoxide poisoning
Thom, S. R., Bhopale, V. M., Milovanova, T. M., Hardy, K. R., Logue, C. J., Lambert, D. S., Troxel, A. B., Ballard, K., & Eisinger, D. P. (2010) · Clinical Toxicology · doi:10.3109/15563650903468209 · Cited by 43
Effects of outdoor air pollutants on platelet activation in people with type 2 diabetes
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“Some air pollution epidemiology studies indeed suggest that diabetes confers an increased risk for health effects from air pollution (Zanobetti and Schwartz, 2002; Liao et al., 2005; Goldberg et al., 2006).”
BackgroundWu, X., Basu, R., Malig, B. J., Broadwin, R., Ebisu, K., Gold, E. B., Qi, L., Derby, C. A., & Green, R. (2017) · Environment International · doi:10.1016/j.envint.2017.07.004 · Cited by 41
“2000), although the findings have been inconsistent across studies (Liao et al. 2005; Rückerl et al. 2007).”
BackgroundResultAmbient Air Pollutants and Risk of Fatal Coronary Heart Disease Among Kidney Transplant Recipients
Spencer-Hwang, R., Knutsen, S. F., Soret, S., Ghamsary, M. G., Beeson, W. L., Oda, K., Shavlik, D. J., & Jaipaul, N. (2011) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2011.05.017 · Cited by 40
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“ANC has been used as a sensitive inflammation biomarker in studies examining physiological consequences of environmental exposures (Frost-Pineda et al., 2011; Liao et al., 2005; Yang et al., 2009).”
BackgroundControlled human exposures to ambient pollutant particles in susceptible populations
Huang, Y.-C. T., & Ghio, A. J. (2009) · Environmental Health · doi:10.1186/1476-069x-8-33 · Cited by 29
“PM10 levels were associated positively with increased von Willebrand factor (vWF) only in person with a history of diabetes [34].”
BackgroundJiang, M., Li, Y., Zhang, B., Zhou, A., Zhu, Y., Li, J., Zhao, H., Chen, L., Hu, J., Wu, C., et al. (2018) · Environment International · doi:10.1016/j.envint.2018.07.021 · Cited by 29
Air Pollution and Other Environmental Modulators of Cardiac Function
Gorr, M. W., Falvo, M. J., & Wold, L. E. (2017) · Comprehensive physiology · doi:10.1002/cphy.c170017 · Cited by 30
Weight-of-evidence evaluation of long-term ozone exposure and cardiovascular effects
Prueitt, R. L., Lynch, H. N., Zu, K., Sax, S. N., Venditti, F. J., & Goodman, J. E. (2014) · Critical Reviews in Toxicology · doi:10.3109/10408444.2014.937855 · Cited by 26
The Association of White Blood Cells and Air Pollutants—A Population-Based Study
Hung, S.-C., Cheng, H.-Y., Yang, C., Lin, C.-I., Ho, C., Lee, W.-H., Cheng, F., Li, C.-J., & Chuang, H. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18052370 · Cited by 25
“Our finding is in line with previous studies [42,47].”
BackgroundResultInfluentialGondalia, R., Holliday, K. M., Baldassari, A., Justice, A. E., Stewart, J. D., Liao, D., Yanosky, J. D., Engel, S. M., Jordahl, K. M., Bhatti, P., et al. (2020) · Environmental Health Perspectives · doi:10.1289/ehp5360 · Cited by 26
Singh, S. K., Goel, I., Tripathi, S., Ahirwar, A. K., Kumar, M., Rana, A., Dhar, R., & Karmakar, S. (2024) · Environmental Science and Pollution Research · doi:10.1007/s11356-024-35016-9 · Cited by 26
“…a threat to health as it causes coughing and sore throat, breathing difficulty, chest pain, inflamed airways, susceptibility to infection, and aggravates respiratory disorders (G. C. Chuang et al. 2009; Day et al. 2017; Liao et al. 2005; Nuvolone et al. 2018; Paffett et al. 2015; Xia et al. 2018).”
Morabia, A., Zhang, F. F., Deyssenroth, M. A., Flory, J. D., Mirer, F., Santella, R. M., Wolff, M. S., & Markowitz, S. B. (2012) · Preventive Medicine · doi:10.1016/j.ypmed.2012.01.019 · Cited by 24
“Short-term (Liao et al., 2005; Schwartz, 2001) and long-term (Chen and Schwartz, 2008) elevation of ambient PM10 is associated with increased levels of inflammatory markers (Peters et al.”
BackgroundTian, L., Chu, N., Yang, H., Yan, J., Lin, B., Zhang, W., Li, K., Lai, W., Bian, L., Liu, H., et al. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.128838 · Cited by 24
Su, T., Hwang, J., Yang, Y., & Chan, C. (2017) · Epidemiology · doi:10.1097/ede.0000000000000715 · Cited by 24
Yang, Y., Wu, H., Zeng, Y., Xu, F., Zhao, S., Zhang, L., An, Z., Li, H., Li, J., Song, J., et al. (2024) · BMC Public Health · doi:10.1186/s12889-024-19116-2 · Cited by 23
“Whether these discrepancies in WBC effect were due to the curvilinear association of SO 2 with WBC counts remains unclear [31].”
BackgroundParticulate Air Pollutants, Brain Structure, and Neurocognitive Disorders in Older Women.
Jc, C., Wang, X., Serre, M. L., Cen, S., Franklin, M., & Espeland, M. A. (2017) · PubMed Central · Cited by 21
Westberg, H., Hedbrant, A., Persson, A., Bryngelsson, I., Johansson, A., Ericsson, A., Sjögren, B., Stockfelt, L., Särndahl, E., & Andersson, L. (2019) · International Archives of Occupational and Environmental Health · doi:10.1007/s00420-019-01446-z · Cited by 21
Michikawa, T., Okamura, T., Nitta, H., Nishiwaki, Y., Takebayashi, T., Ueda, K., Kadota, A., Fujiyoshi, A., Ohkubo, T., Ueshima, H., et al. (2016) · Environmental Pollution · doi:10.1016/j.envpol.2016.02.051 · Cited by 19
Jaafari, J., Naddafi, K., Yunesian, M., Nabizadeh, R., Hassanvand, M. S., Shamsipour, M., Ghozikali, M. G., Shamsollahi, H. R., Nazmara, S., & Yaghmaeian, K. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.139417 · Cited by 19
Circulating adhesion molecules after short-term exposure to particulate matter among welders
Fang, S. C., Eisen, E. A., Cavallari, J. M., Mittleman, M. A., & Christiani, D. C. (2009) · Occupational and Environmental Medicine · doi:10.1136/oem.2008.043794 · Cited by 18
Elvidge, T., Matthews, I. P., Gregory, C. J., & Hoogendoorn, B. (2013) · Journal of Environmental Science and Health Part C · doi:10.1080/10590501.2013.763575 · Cited by 19
Airborne environmental injuries and human health
Borchers, A. T., Chang, C., Keen, C. L., & Gershwin, M. E. (2006) · Clinical Reviews in Allergy & Immunology · doi:10.1385/criai:31:1:1 · Cited by 17
“CRIAI_31_Final Appl 7/17/06, 1:47 PM10”
BackgroundWang, K., Wang, W., Lei, L., Lan, Y., Liu, Q., Ren, L., & Wu, S. (2022) · Environmental Research · doi:10.1016/j.envres.2022.114210 · Cited by 16
Weight-of-evidence evaluation of short-term ozone exposure and cardiovascular effects
Goodman, J. E., Prueitt, R. L., Sax, S. N., Lynch, H. N., Zu, K., Lemay, J. C., King, J. M., & Venditti, F. J. (2014) · Critical Reviews in Toxicology · doi:10.3109/10408444.2014.937854 · Cited by 16
“Seven of these studies were from the ISA (Anderson et al. 2010, Dockery et al. 2005a, Metzger et al. 2007, Rich et al. 2005, 2006a,b, Sarnat, et al. 2006, and 13 were from our literature search (Peters et al. 2000, Rich et al. 2004, Dockery et al. 2005b, Peel et al. 2007, 2011, Chiu and Yang 2009, Halonen et al. 2010,…”
BackgroundMethodInfluentialFrampton, M. W., Balmes, J. R., Bromberg, P. A., Stark, P. C., Arjomandi, M., Hazucha, M. J., Rich, D. Q., Hollenbeck-Pringle, D., Dagincourt, N., Alexis, N. E., et al. (2017) · PubMed · Cited by 14
Das, P., & Chatterjee, P. (2015) · Journal of Exercise Science & Fitness · doi:10.1016/j.jesf.2015.08.001 · Cited by 14
“Short-term elevation of ambient PM is associated with increased levels of inflammatory markers such as WBC count.(29,30) This increase in WBC count following exposure to high concentrations of air pollutants might be due to their tissue-damaging effects and rise of antibody production in response to the exposure.”
BackgroundBelz, D. C., Woo, H., Putcha, N., Paulin, L. M., Koehler, K., Fawzy, A., Alexis, N. E., Barr, R. G., Comellas, A. P., Cooper, C. B., et al. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.154694 · Cited by 13
Pollution de l’air et pathologie athérothrombotique cardiaque et cérébrale
Zeller, M., Giroud, M., Royer, C., Bénatru, I., Besancenot, J., Rochette, L., & Cottin, Y. (2006) · La Presse Médicale · doi:10.1016/s0755-4982(06)74844-8 · Cited by 13
Jhun, I., Kim, J.-A., Cho, B. S., Gold, D. R., Schwartz, J. D., Coull, B. A., Zanobetti, A., Rice, M. B., Mittleman, M. A., Garshick, E., et al. (2019) · Journal of the Air & Waste Management Association · doi:10.1080/10962247.2019.1596994 · Cited by 12
“positive (Ghio et al. 2003; Liao et al. 2005), or null associations (Baccarelli et al.”
BackgroundWu, J. T., & Wu, L. (2007) · Journal of Biomedical & Laboratory Sciences · doi:10.30046/jbls.200703.0001 · Cited by 12
“Population-based studies suggest that the appearance of inflammation markers and the risk of coronary heart disease (CHD) are associated adversely with environmentally relevant pollutants [14].”
BackgroundAndersson, L., Hedbrant, A., Persson, A., Bryngelsson, I., Sjögren, B., Stockfelt, L., Särndahl, E., & Westberg, H. (2021) · Biomarkers · doi:10.1080/1354750x.2021.1941260 · Cited by 14
Johannesson, S., Andersson, E. M., Stockfelt, L., Barregård, L., & Sällsten, G. (2014) · Inhalation Toxicology · doi:10.3109/08958378.2013.856968 · Cited by 11
“The coagulation factor VIII in plasma (normally mainly bound in a stable complex to von Willebrand factor) can be considered a marker of both systemic inflammation and hemostasis (Liao et al., 2005).”
BackgroundProspective Study of Metal Fume-Induced Responses of Global Gene Expression Profiling in Whole Blood
Wang, Z., Neuberg, D. S., Su, L., Kim, J. Y., Chen, J., & Christiani, D. C. (2008) · Inhalation Toxicology · doi:10.1080/08958370802192874 · Cited by 11
“It has been proposed that inhaled particulates from air pollution may cause systemic alterations, in addition to effects on the autonomic nervous system, by releasing inflammatory cytokines subsequent to pulmonary inflammation (Magari et al., 2001; Liao et al., 2005).”
BackgroundDi, N., He, W., Zhang, K., Cui, J. T., Chen, J., Cheng, J., Chu, B., Li, S., Xie, Y., Xiang, H., et al. (2021) · Environmental Research Letters · doi:10.1088/1748-9326/abd9f3 · Cited by 9
Li, G., Zhao, H., Hu, M., He, J., Yang, W.-J., Zhang, H., Zhu, Z., Zhu, J., & Huang, F. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-21128-7 · Cited by 8
Day, D. B., Clyde, M. A., Xiang, J., Li, F., Cui, X., Mo, J., Gong, J., Weschler, C. J., Zhang, Y., & Zhang, J. J. (2018) · Journal of Thoracic Disease · doi:10.21037/jtd.2018.06.135 · Cited by 7
“Of the aforementioned circulating hemostatic factors that are known to be increased with age, ambient O3 levels have been associated with fibrinogen (28-30), VWF (29), and PAI-1 (28) in humans, though these associations have also been nonsignificant in other human studies evaluating the same biomarkers (31-33).”
BackgroundInfluentialSpencer-Hwang, R. (2013) · Journal of Clinical & Experimental Cardiology · doi:10.4172/2155-9880.s6-001 · Cited by 7
Pollution de l'air et pathologie athérothrombotique cardiaque et cérébrale
Zeller, M., Giroud, M., Royer, C., Bénatru, I., Besancenot, J., Rochette, L., & Cottin, Y. (2006) · La Presse Médicale · doi:10.1016/s0755-4982(06)74882-5 · Cited by 6
Carbon Monoxide Transport and Actions in Blood and Tissues
Thom, S. R. (2011) · Comprehensive physiology · doi:10.1002/cphy.c091005 · Cited by 9
Cui, F., Miao, Y., Liu, A., Deng, Y.-L., Liu, C., Zhang, M., Zeng, J.-Y., Li, Y., Liu, H.-Y., Liu, C.-J., et al. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.115741 · Cited by 5
Environmental factors in cardiovascular disease
Rosenlund, M. (2005) · Figshare · Cited by 5
Gaio, V., Roquette, R., Monteiro, A., Ferreira, J., Rafael, S. I. M., Dias, C. M., & Nunes, B. (2021) · Air Quality Atmosphere & Health · doi:10.1007/s11869-021-01007-9 · Cited by 4
“2018) but results remain controversial (Dabass et al. 2016; Liao et al. 2005) and studies on this topic are still scarce.”
Background
Metadata
- Authors
- Liao, D., Heiss, G., Chinchilli, V. M., Duan, Y., Folsom, A. R., Lin, H.-M., & Salomaa, V.
- Affiliations
- Pennsylvania State University (US)
- University of North Carolina at Chapel Hill (US)
- University of Minnesota (US)
- Finnish Institute for Health and Welfare (FI)
- Corresponding author
- Liao, Duanping
- Venue
- Journal of Exposure Science & Environmental Epidemiology
- Published
- 2004-11-10
- Volume
- 15
- Issue
- 4
- Pages
- 319-328
- ISSN
- 1559-0631 (ISSN-L)
- 1559-064X
- OpenAlex
- W1999733163
- Cited by
- 129
- References
- 55
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 4 · 2023: 1 · 2022: 4 · 2021: 5 · 2020: 6 · 2019: 7 · 2018: 2 · 2017: 11 · 2016: 4 · 2015: 6 · 2014: 7 · 2013: 5 · 2012: 6
- FWCI
- 5.75
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Exposure Science & Environmental Epidemiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01es010189-03)
- National Institute of Environmental Health Sciences (1-R01-ES10189-01)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Indoor Air Quality and Microbial Exposure
- Social Sciences › Sociology and Political Science › Environmental Justice and Health Disparities
- Keywords
- air pollution, criteria pollutants, PM10, ozone, carbon monoxide, nitrogen dioxide, sulfur dioxide, hemostatic markers, inflammatory markers, von Willebrand factor, fibrinogen, factor VIII, serum albumin, white blood cell count, diabetes mellitus, coronary artery disease, threshold effects, Atherosclerosis Risk in Communities Study
- MeSH terms
- Air Pollutants, Carbon Monoxide, Cardiovascular Diseases, Dust, Environmental Monitoring, Factor VIII, Female, Fibrinogen, Hemostasis, Humans, Inflammation, Leukocyte Count, Male, Middle Aged, Nitrogen Dioxide, Ozone, Regression Analysis, Sulfur Dioxide, von Willebrand Factor
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