Next Article in Journal
Impact of the Madden–Julian Oscillation on North Indian Ocean Cyclone Intensity
Next Article in Special Issue
Review on Atmospheric Ozone Pollution in China: Formation, Spatiotemporal Distribution, Precursors and Affecting Factors
Previous Article in Journal
Characteristics of Chlorine Releasing from Coal-Fired Power Plant
Previous Article in Special Issue
Regional Air Pollutant Characteristics and Health Risk Assessment of Large Cities in Northeast China
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Atmosphere
Volume 12
Issue 12
10.3390/atmos12121552
atmosphere-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Impact of Air Pollution (PM2.5) on Atherogenesis in Modernizing Southern versus Northern China

by
Kamsang Woo
1,*,
Changqing Lin
2,
Yuehui Yin
3,
Dongshuang Guo
4,
Ping Chook
1,
Timothy C. Y. Kwok
1 and
David S. Celermajer
5
1
Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, China
2
Division of Environment and Sustainability, The Hong Kong University of Science and Technology, Hong Kong, China
3
Second Hospital of Chongqing Medical University, Chongqing 400010, China
4
Department of Medicine, Yu County Provincial Hospital, Yangquan 045100, China
5
Faculty of Medical and Health Science, The University of Sydney, Sydney, NSW 2006, Australia
*
Author to whom correspondence should be addressed.
Atmosphere 2021, 12(12), 1552; https://doi.org/10.3390/atmos12121552
Submission received: 29 September 2021 / Revised: 5 November 2021 / Accepted: 8 November 2021 / Published: 24 November 2021
(This article belongs to the Special Issue Air Pollution in China)
Browse Figures
Versions Notes

Abstract

:
To evaluate the impact of PM2.5 air pollution on atherogenic processes in modernizing Southern versus Northern China, we studied 1323 asymptomatic Chinese in Southern and Northern China in 1996–2007. PM2.5 exposure and metabolic syndrome (MS) were noted. Brachial flow-mediated dilation (endothelial function FMD) and carotid intima-media thickness (IMT) were measured by ultrasound. Although age and gender were similar, PM2.5 was higher in Northern China than in Southern China. The Northern Chinese were characterized by lower lipids, folate and vitamin B12, but higher age, blood pressures, MS and homocysteine (HC) (p = 0.0015). Brachial FMD was significantly lower and carotid IMT was significantly greater (0.68 ± 0.13) in Northern Chinese, compared with FMD and IMT (0.57 ± 0.13, p < 0.0001) in Southern Chinese. On multivariate regression, for the overall cohort, carotid IMT was significantly related to PM2.5, independent of location and traditional risk factors (Model R2 = 0.352, F = 27.1, p < 0.0001), while FMD was inversely related to gender, age, and northern location, but not to PM2.5. In Southern Chinese, brachial FMD was inversely correlated to PM2.5, independent of age, whereas carotid IMT was significantly related to PM2.5, independent of age and gender. In Northern Chinese, brachial FMD was inversely related to gender only, but not to PM2.5, while carotid IMT was related to traditional risk factors. Despite a higher PM2.5 pollution in Northern China, PM2.5 pollution was more significantly associated with atherogenic surrogates in Southern compared to Northern Chinese. This has potential implications for atherosclerosis prevention.

1. Introduction

Atherosclerotic diseases (stroke and heart attack CVS) are currently the most important global health hazard, including for mainland China, which is now in a rapid phase of modernization [1,2]. Traditional atherosclerosis risk factors, including smoking, hypertension, diabetes mellitus, hyperlipidemia, obesity and physical inactivity, have been implicated [3]. Recently the detrimental association of air pollution (AP) with CVS in modernized society has been realized. In particular, small particulate matter less than 2.5 µm in diameter (PM2.5) has been associated with cardiovascular morbidity and mortality [4,5,6]. Of the 7 million premature deaths each year linked to air pollution (PM2.5), 34% were related to ischemic heart disease, 26% to respiratory disease and 20% were due to stroke [7].
The pathobiology of PM2.5-related atherosclerotic disease may involve direct effects of PM2.5 on cardiovascular system and/ or indirect effects of PM2.5 mediated by oxidative stress and vascular inflammation [8,9]. In other words, PM2.5 can act as a trigger in susceptible persons, or it can contribute to long-term atherogenic processes. On this issue, we and others have previously documented the negative impact of long-term PM2.5 exposure on atherosclerosis surrogates (brachial endothelial dysfunction FMD and carotid intima-media thickening IMT), which are closely linked to cardiovascular and stroke outcome [10,11,12].
In the past three decades, China has been undertaking a process of rapid economic development and modernization [13]. This started from the Southern seashore region and the greater Pearl Delta Bay area, and later moved to the Northern parts of the country, with different PM2.5 pollution exposure. The present study aimed to evaluate the impact of PM2.5 pollution on atherogenic process in Southern compared with Northern China.

2. Subjects and Methods

A total of 1323 asymptomatic Chinese adults (mean age 47.1 ± 11.7 years and 47.5% male) in Southern China (Hong Kong, Macau, Pan Yu, n = 395) and Northern China (Yu County in Shanxi and Three Gorges Territories of Yangtze River, n = 928) were studied in 1996–2007, as part of the international collaborative Chinese Atherosclerosis in the Aged and Young Project (CATHAY Study). The study protocol and some related findings have been reported previously [14,15,16,17,18].
All recruited subjects were apparently healthy. They were not known to have hypertension, diabetes mellitus or metabolic syndrome, had no major vascular, hepatic or renal disease, and were not taking any regular medications, including vitamin supplementation. Nearly all subjects (>95%) were local born residents and the other migrated to the county for over 10 years. After fasting for 14 h and signing written informed consent, their cardiovascular risk profiles, including smoking, body mass index (BMI), waist circumference, waist hip ratio (WHR), systolic and diastolic blood pressure (SBP, DBP) were measured. On recruitment, blood was taken once for fasting lipid profile (total, high and low lipoprotein cholesterol, TC, HDL-C, LDL-C and triglycerides TG), creatinine, vitamin B12, folate, and fasting total homocysteine (HC). Fasting glucose was measured by haemstix and HC was evaluated on stored frozen sample by enzymatic immune assay (Abbott IMX analyses, Abbott Peak, IL, USA). Blood was assayed in batches at the The Hospital Central Corde de Januarie, Macau, and The Prince of Wales Hospital, Hong Kong, currently accredited by the USA laboratory centres. MTHFR genotypes were evaluated by PCR technique at the Li Hysan research laboratory of the Chinese University of Hong Kong. Metabolic Syndrome (MS) was diagnosed according to International Diabetes Federation (IDF) criteria [19,20].
Our research study and informed consent form were reviewed and approved by our institutional research ethics committee of The Chinese University of Hong Kong (CREC 2000-108). This study complied with the 1995 and 2003 Helsinki Declaration for human studies.

2.1. PM2.5 Air Pollution Exposure

The yearly mean PM2.5 concentration over China was assessed by using the satellite remote sensing technology. Firstly, spectral data from the two moderate resolution imaging spectroradiometer (MODIS) instruments aboard the Terra and Aqua satellites were used to build aerosol optical depth (AOD) data at a resolution of 0.01° × 0.01°, over China [21]. Secondly, an observational data-driven algorithm, which took the ground-observed visibility and relative humidity data as inputs, was developed to derive the yearly mean ground-level PM2.5 concentration from the AOD [22]. Evaluation of the long-term satellite-derived PM2.5 concentration against the ground observations demonstrated a correlation coefficient of >0.9 and a mean absolute percentage error within ±20% [23]. The mean concentration of PM2.5 over a single year was registered, corresponding to the study year of each subject.

2.2. Arterial Ultrasound Studies

Atherosclerotic surrogate markers, flow-mediated dilation (FMD) of brachial artery, and carotid intima-media thickness (IMT), were studied once on recruitment using high resolution ultrasound as reported previously [24,25]. Briefly, forearm tourniquet cuff placement was applied to induce reactive hyperemia on deflation, and percentage of dilation in vessel diameter (from baseline) was computed, as indicator of endothelium-dependent dilation, in comparison with dilation after sublingual glyceryltrinitrate (endothelium-independent dilation GTN). Similarly carotid IMT was measured by using a standard scanning protocol for both carotid arteries as described by Salonen and Salonen, Bots and Touboul et al. [26,27,28]. Images of the far wall of the distal 10 mm of the common carotid artery were used. All scans were evaluated off-line by a verified automatic edge-detecting software device. The intra-observer variability for mean IMT was 0.03 ± 0.01 mm (coefficient of variation 1%, R = 0.99).

2.3. Statistical Analyses

The group mean values, standard deviation and 95% confidence intervals (CI) when appropriate were computed. Standard testing of normality of distribution was used for the assessment of normal distribution. Possible intergroup differences were identified with independent samples Students’ test and a one-way ANCOVA model. The primary study endpoints were carotid IMT and brachial FMD, whereas other outcome variables were compared after Bonferroni adjustment for multiple comparisons. On the assumption of mean carotid IMT being 0.61±0.14 mm and brachial FMD being 8% ± 1% in the subjects, we estimated that enrolment of 350 subjects in Southern China and 600 subjects in Northern China would result in adequate power (80%) to detect a 18% difference in carotid IMT and an 8% difference in brachial FMD, between the two location groups at 2p < 0.05 significance level [29]. Linear multivariate regressions were performed to assess the major determinants of IMT and FMD, including age, gender, smoking status, BMI, metabolic syndrome, LDL-C, PM2.5, southern and northern locations. The variables with significant standardized beta coefficients (beta value with 2p < 0.05) as an indicator of the contribution to the model, were identified, and insignificant variables (2p > 0.05) were removed subsequently. Group differences with an error probability of 5% (2p < 0.05) were considered statistically significant. Analyses were performed with SPSS version 25.

3. Results

The demographic and clinical characteristics of the southern/ northern groups were tabulated (Table 1). While their gender, mean age, BMI and fasting glucose were similar, smoking status, SBP, DBP, metabolic syndrome and homocysteine were significantly lower, but their LDL-C, vitamin B12 and folate were significantly higher in Southern Chinese compared with the Northern Chinese (p < 0.0015). PM2.5 exposure in Southern China (44.0 ± 6.8 µg/m3) (Figure 1A,B) was significantly lower than in Northern China (71.1 ± 15.8 µg/m3), p < 0.0015. (Figure 2A,B).

3.1. Vascular Parameters

Brachial FMD and carotid IMT were normally distributed. Brachial FMD was significantly lower (7.5 ± 18, 95% CI 7.3–7.7%, p < 0.001), but carotid IMT was significantly greater (0.68 ± 0.13, 95% CI 0.67–0.69 mm, p < 0.0001) in Northern Chinese, compared with their Southern counterparts (8.1 ± 3.0, 95% CI 7.8–8.5% and 0.57 ± 0.13, 95% CI 0.56–0.58 mm, respectively) (Table 2). The GTN responses of the two groups were similar.

3.2. Determinants of Risk Factors for Impaired Brachial FMD

On multivariate regression analyses, in Southern Chinese, brachial FMD was inversely related to PM2.5 (beta = −0.274, p = 0.001), age (beta= −0.238, p < 0.005), but not to gender, smoking status, BMI, MS, homocysteine, LDL-C or MTHFR. (Model R2 = 0.202, F = 4.026, p < 0.0001) (Table 3). In Northern Chinese, brachial FMD was related to gender (beta = −0.329, p = 0.009), but not to other traditional risk factors (Model R2 = 0.211, F = 3.802, p < 0.0001). In the overall 1323 Chinese cohort, lower brachial FMD was related to older age, male gender and northern location, but not to PM2.5 (Model R2 = 0.190, F = 7.802, p < 0.0001).
On multivariate regression analyses, carotid IMT in Southern Chinese was significantly related to PM2.5 (beta = 0.334, p < 0.0001), independent of age (beta = 0.393, p < 0.0001) and gender (beta = 0.146, p = 0.043) (Model R2 = 0.451, F = 13.3, p < 0.0001) (Table 4). In Northern Chinese, carotid IMT was related to age (beta = 0.385, p < 0.0001), smoking status (beta = 0.157, p = 0.01), MS (beta = 0.110, p = 0.039), homocysteine (beta = 0.137, p = 0.014) and LDL-C (beta = 0.145, p = 0.0003), but not to PM2.5 (beta = 0.033, p = 0.471). For the overall cohort, carotid IMT was related to PM2.5 (beta = 0.368, p < 0.0001), independent of other atherosclerotic risk factors including age, male gender, BMI, MS, HC, LDL-C and northern location (beta = 0.206, p = 0.002) (Model R2 = 0.362, F = 27.1, p < 0.0001). No PM2.5 and age (beta = 0.305, p = 0.125), or PM2.5 and location (beta = 0.093, p = 0.056) interactions were identified.

4. Discussion

The present report further confirms the detrimental impact of PM2.5 air pollution on atherogenic processes in modernizing China, independent of traditional atherosclerotic risk factors [12,18,30]. Specifically, Northern Chinese were more prone to higher carotid IMT and worse arterial endothelial dysfunction, compared with Southern Chinese. This may be attributed to more smoking, higher SBP, DBP, homocysteine, PM2.5 exposure and metabolic syndrome rates, and lower (unfavorable) vitamin B12 and folate levels. Metabolic syndrome includes the impact of several atherosclerotic risk factors i.e., blood pressure, waist circumference, HDL and LDL-cholesterol and fasting glucose. We and others have documented its detrimental impact on atherogenesis, independent of PM2.5 [18,31].
Multivariate regression of the overall cohort suggested that PM2.5 exposure and location were important determinants of carotid IMT, independent of homocysteine and other traditional vascular risk factors. Higher homocysteine presumably could be related to unique Northern dietary pattern of low folate and vitamin B12 intakes, the formal documentation of which is awaited with interest. On this issue, we have previously confirmed the beneficial effects of vitamin B12 and folate supplementations on atherogenic process (FMD and IMT) in 207 Northern Chinese adult subjects with subnormal nutritional status [32].
Greater carotid IMT is an important prognostic atherosclerosis surrogate related to later risk of stroke and cardiovascular diseases [33]. We have previously shown that increased carotid IMT is a marker of subclinical atherosclerosis in westernized as compared with rural Southern Chinese [15]. To contextualize the magnitude of the IMT difference (19.3%, 0.11 mm), a 0.16 mm increase in carotid IMT has been associated with 41% increase in stroke and 43% increase in acute myocardial infarction over a follow up period of 2–7 years [33]. The 19.3% difference in carotid IMT in the present study was far greater than the kind of difference between diabetic and non-diabetic Chinese adults [17].

4.1. Limitations

We acknowledge some limitations in our present study. Firstly, we have not explored inflammatory markers, such as fibrinogen, C-reactive protein or cytokine family, in the Northern compared with Southern Chinese. This will be valuable for confirming the hypothesis of generalized vascular inflammation in AP-induced atherogenic process. Secondly, the concentration and LDL-C happened (by chance) to be lower, but hyperemia (by ultrasound) to be higher in Northern Chinese. These, however, have not contributed to the worse FMD and IMT results, since these two factors would have been associated with better rather than worse FMD and IMT levels in the Northern Chinese. Thirdly, we have identified FMD, an early atherosclerotic surrogate, is lower in Northern Chinese on univariate analyses, but its relationship with PM2.5 concentration is borderline only on multivariate analyses. FMD in more labile and dynamic compared with carotid IMT measurement, subjected to daily fluctuation of PM2.5 concentration. This was measured once only during the study period. Perhaps more FMD measurements for individual subject over the study period may illuminate the real impact of PM2.5 on FMD. Fourthly, realtime long term PM2.5 measurement is more informative and better than yearly mean PM2.5 estimation for studying its relationship with more labile FMD measurement. This, however, has logistic and economic implications which may not be readily resolved.

4.2. General Remarks

We propose carotid IMT and brachial FMD as two surrogate targets for measuring the success of possible prevention of PM2.5-related atherogenesis in Chinese. While the nationwide adoption of PM2.5-reduction policies will be welcomed in both Northern and Southern Chinese, our present study would suggest the possible importance of micronutrient (folate and vitamin B12) deficiencies in some areas of Northern China, apart from control of vascular risk factor [31]. In addition, strategies on a more personal approach may be advisable particularly in southern China, including face-mask and filtering devices for indoor air pollution [34,35,36,37], as well as exploration of potential medical therapies to reduce the impact of atherosclerosis.

5. Conclusions

PM2.5 air pollution in China, in particular in Southern Chinese, is related to atherogenic surrogates, independent of traditional risk factors, with potential implications in both dietary and air pollution reduction strategies for atherosclerosis prevention.

Author Contributions

K.W.: Project conception and design, research administration, statistical analysis and interpretation of data, drafting and revision of the article and final approval of the version to be published. C.L.: Provision and interpretation of PM2.5 data in China, revision of the article and final approval of the version to be published. Y.Y.: Project conception, interpretation of data, revision of the article and final approval of the version to be published. D.G.: project conception and design, co-administration of the field work at Yu County, revision of the articles and final approval of the version to be published. P.C.: Project conception and design, performance of ultrasonography analysis and interpretation of data, drafting, revision of the article and final approval of the version to be published. T.C.Y.K.: Design of project, interpretation of data, revision of the article and final approval of the version to be published. D.S.C.: Project conception and design, interpretation of data, drafting and revision of the article, and final approval of the version to be published. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by The Chinese Atherosclerosis Trust, Madam Leung Kit Wah Project Fund, Dr Stanley Ho Medical Development Foundation (grant and donation), Star Industrial Company and Dr Thomas HC Cheung Trust: They provided unrestricted sponsorships for the present study, without any involvement in study design, data collection, analysis or interpretation, nor in the writing of this report or the decision to submit the paper for publication.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board.

Informed Consent Statement

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

Data Availability Statement

The research data will be available from the corresponding author to the editor and Atmosphere readers on reasonable request.

Acknowledgments

We wish to acknowledge the valuable support of the Chinese Atherosclerosis Trust, Leung Kit Wah Project Fund, Stanley Ho Medical Development Foundation Trust, The Star Industrial Company Fund of The Chinese University of Hong Kong and Thomas HC Cheung Trust in sponsoring the study. We also acknowledge The Macau Heart Foundation, for helping recruitment of subjects, and the Pathology Department of Centro Hospitalar Conde de Sao Januario in Macau for the blood assays. We acknowledge the superb statistical analyses and clerical work of Guo Cui of the School of Public Health, Mikki Wong and Chu Pui Yan, Daphne, of The Chinese University of Hong Kong.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lloyd-Jones, D.; Adams, R.; Carnethon, M.; de Simone, G.; Ferguson, T.B.; Flegal, K.; Ford, E.; Furie, K.; Go, A.; Greenlund, K.; et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics—2009 update: A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2009, 119, 480–486. [Google Scholar] [PubMed]
  2. Roth, G.A.; Johnson, C.; Abajobir, A.; Abd-Allah, F.; Abera, S.F.; Abyu, G.; Ahmed, M.; Aksut, B.; Alam, T.; Alam, K.; et al. Global regional and national burden of cardiovascular diseases for 10 causes, 1990-2015. J. Am. Coll. Cardiol. 2017, 70, 1–25. [Google Scholar] [CrossRef] [PubMed]
  3. Danaei, G.; Ding, E.L.; Mozaffarian, D.; Taylor, B.; Rehm, J.; Murray, C.J.L.; Ezzati, M. The preventable causes of death in the United States: Comparative risk assessment of dietary, lifestyle, and metabolic risk factors. PLoS Med. 2009, 6, e1000058. [Google Scholar] [CrossRef] [PubMed]
  4. Rajagopalan, S.; Al-Kini, S.G.; Brook, R.D. Air pollution and cardiovascular disease. J. Am. Coll. Cardiol. 2018, 72, 2054–2070. [Google Scholar] [CrossRef] [PubMed]
  5. Liang, F.; Liu, F.; Huang, K.; Yang, X.; Li, J.; Xiao, Q.; Chen, J.; Liu, X.; Cao, J.; Shen, C.; et al. Longterm exposure to fine particulate matter and cardiovascular disease in China. J. Am. Coll. Cardiol. 2020, 75, 707–717. [Google Scholar] [CrossRef]
  6. Brook, R.D.; Rajagopalan, S.; Pope, C.A., 3rd; Brook, J.R.; Bhatnagar, A.; Diez-Roux, A.V.; Holguin, F.; Hong, Y.; Luepker, R.V.; Mittleman, M.A.; et al. American Heart Association Council on Epidemiology and Prevention, Council on the Kidney in Cardiovascular Disease, and Council on Nutrition, Physical Activity and Metabolism. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation 2010, 121, 2331–2378. [Google Scholar]
  7. Jasarevic, T.; Thomas, G.; Osseiran, N. 7 Million Premature Deaths Annually Lined to Air Pollution. WHO Media Centre 2014. Available online: https://www.who.int/mediacentre/news/releases/2014/air-pollution/en/ (accessed on 25 March 2014).
  8. Arden Pope, C., 3rd; Burnett, R.T.; Thurston, G.D.; Thun, M.J.; Calle, E.E.; Krewski, D.; Godleski, J.J. Cardiovascular mortality and long-term exposure to particular air pollution – Epidemiological evidence of general pathophysiological pathways of disease. Circulation 2004, 109, 71–77. [Google Scholar] [CrossRef] [Green Version]
  9. Pepine, C.J. The effects of angiotensin-converting enzyme inhibition on endothelial dysfunction: Potential role in myocardial ischemia. Am. J. Cardiol. 1998, 82, 23S–27S. [Google Scholar] [CrossRef]
  10. Roux, A.V.D.; Auchincloss, A.H.; Franklin, T.G.; Raghunathan, T.; Barr, R.G.; Kaufman, J.; Astor, B.; Keeler, J. Long-term exposure to ambient particulate matter and prevalence of subclinical atherosclerosis in the Multi-Ethnic Study of Atherosclerosis. Am. J. Epidemiol. 2008, 167, 667–675. [Google Scholar] [CrossRef] [Green Version]
  11. Bauer, M.; Moebus, S.; Möhlenkamp, S.; Dragano, N.; Nonnemacher, M.; Fuchsluger, M.; Kessler, C.; Jakobs, H.; Memmesheimer, M.; Erbel, R.; et al. HNR Study Investigative Group. Urban particulate matter air pollution is associated with subclinical atherosclerosis: Results from the HNR (Heinz Nixdorf Recall) study. J. Am. Coll. Cardiol. 2010, 56, 1803–1808. [Google Scholar] [CrossRef] [Green Version]
  12. Woo, K.S.; Chook, P.; Hu, Y.J.; Lao, X.Q.; Lin, C.Q.; Lee, P.; Kwok, C.; Wei, A.N.; Guo, D.S.; Yin, Y.H.; et al. The Impact of Particulate Matter Air Pollution (PM2.5) on Atherosclerosis in Modernizing China: The report from CATHAY Study. Int. J. Epid. 2020, 50, 1–11. [Google Scholar] [CrossRef]
  13. Yang, J.; Siri, J.G.; Remais, J.V.; Cheng, Q.; Zhang, H.; Chan, K.K.Y.; Sun, Z.; Zhao, Y.; Cong, N.; Li, X.; et al. The Tsinghua-lancet commission on healthy cities in China: Unlocking the power of cities for a healthy China. Lancet 2018, 391, 2140–2184. [Google Scholar] [CrossRef] [Green Version]
  14. Woo, K.S.; Robinson, J.T.; Chook, P.; Adams, M.R.; Yip, G.; Mai, Z.J.; Lam, C.W.; Sorensen, K.E.; Deanfield, J.E.; Celermajer, S.D. Differences in the effect of cigarette smoking on endothelial function in Chinese and white adults. Ann. Int. Med. 1997, 127, 372–375. [Google Scholar] [CrossRef]
  15. Woo, K.S.; Chook, P.; Raitakari, O.T.; McQuillan, B.; Feng, J.Z.; Celermajer, D.S. Westernization of Chinese adults and increased subclinical atherosclerosis. Arter. Thromb. Vasc. Biol. 1999, 19, 2487–2493. [Google Scholar] [CrossRef] [Green Version]
  16. Thomas, G.N.; Chook, P.; Qiao, M.; Huang, X.S.; Leong, H.C.; Celermajer, D.S.; Woo, K.S. Deleterious impact of “high normal” glucose levels and other metabolic syndrome components on arterial endothelial function and intima-media thickness in apparently healthy Chinese subject: The CATHAY study. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 739–743. [Google Scholar] [CrossRef] [Green Version]
  17. Woo, K.S.; Chook, P.; Yu, C.W.; Sung, R.Y.T.; Qiao, M.; Leung, S.S.F.; Lam, C.W.K.; Metreweli, C.; Celermajer, D.S. Effects of diet and exercise on obesityrelated vascular dysfunction in children. Circulation 2004, 109, 1981–1986. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Woo, K.S.; Timothy, K.C.Y.; Chook, P.; Hu, Y.J.; Yin, Y.H.; Lin, C.Q.; Lau, K.H.A.; Lee, P.W.A.; Celermajer, D.S. Independent Effects of Metabolic Syndrome and Air Pollution (PM2.5) on Atherosclerosis in Modernizing China. Austin J. Public Health Epidemiol. 2021, 8, 1097. [Google Scholar]
  19. Zimmet, P.; Alberti, K.; George, M.M.; Rios, M.S. A new International Diabetes Federation (IDF) worldwide definition of the metabolic syndrome: The rationale and the results. Rev. Esp. Cardiol. 2005, 58, 1371–1376. [Google Scholar] [CrossRef]
  20. Woo, K.S.; Hu, Y.J.; Chook, P.; Wei, A.N.; Chan, R.; Yin, Y.H.; Celermajer, D.S. A Tale of Three Gorges in the Yangtze River: Comparing the Prevalence of Metabolic Syndrome According to ATP III, WHO, and IDF Criteria and the Association with Vascular Health in Modernizing China. Metab. Syndr. Relat. Disord. 2019, 17, 137–142. [Google Scholar] [CrossRef]
  21. Li, C.; Lau, A.K.H.; Mao, J.; Chu, D.A. Retrieval, validation, and application of the 1-km aerosol optical depth from MODIS measurements over Hong Kong. IEEE Trans. Geosci. Remote Sens. 2005, 43, 2650–2658. [Google Scholar]
  22. Lin, C.Q.; Li, Y.; Yuan, Z.B.; Lau, A.K.H.; Li, C.C.; Fung, J.C.H. Using satellite remote sensing data to estimate the high-resolution distribution of ground-level PM2.5. Remote Sens. Environ. 2015, 156, 117–128. [Google Scholar] [CrossRef]
  23. Lin, C.Q.; Liu, G.; Lau, A.K.H.; Li, Y.; Li, C.C.; Fung, J.C.H.; Lao, X.Q. High-resolution satellite remote sensing of provincial PM2.5 trends in China from 2001 to 2015. Atmos. Environ. 2018, 180, 110–116. [Google Scholar] [CrossRef]
  24. Celermajer, D.S.; Sorensen, K.; Gooch, V.; Spiegelhalter, D.J.; Miller, O.I.; Sullivan, I.D.; Lloyd, J.K.; Deanfield, J.E. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992, 340, 1111–1115. [Google Scholar] [CrossRef]
  25. Woo, K.S.; Chook, P.; Yu, C.W.; Sung, R.Y.T.; Qiao, M.; Leung, S.S.F.; Lam, C.W.K.; Metreweli, C.; Celermajer, D.S. Overweight in children is associated with arterial endothelial dysfunction and intima-media thickening. Int. J. Obes. 2004, 28, 852–857. [Google Scholar] [CrossRef] [Green Version]
  26. Salonen, J.T.; Salonen, R. Ultrasonographically assessed carotid morphology and the risk of coronary heart disease. Arterioscler. Thromb. Vasc. Biol. 1991, 11, 1245–1249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Bots, M.L.; Hoes, A.W.; Koudstaal, P.J.; Hofman, A.; Grobbee, D.E. Common carotid intima-media thickness and risk of stroke and myocardial infarction: The Rotterdam Study. Circulation 1997, 96, 1432–1437. [Google Scholar] [CrossRef] [Green Version]
  28. Touboul, P.J.; Hennerici, M.G.; Meairs, S.; Adams, H.; Amarenco, P.; Desvarieux, M.; Ebrahim, S.; Fatar, M.; Hernandez Hernandez, R.; Kownator, S.; et al. Advisory Board of the 3rd Watching the Risk Symposium 2004, 13th European Stroke Conference. Mannheim intima-media thickness consensus. Cereb. Dis. 2004, 18, 346–349. [Google Scholar] [CrossRef] [PubMed]
  29. Schulz, K.F.; Grimes, D.A. Sample size calculations in randomised trials: Mandatory and mystical. Lancet 2005, 365, 1348–1353. [Google Scholar] [CrossRef]
  30. Li, H.; Cai, J.; Chen, R.; Zhao, Z.; Ying, Z.; Wang, L.; Chen, J.; Hao, K.; Kinney, P.L.; Chen, H.; et al. Particulate matter exposure and stress hormone levels: A randomized, double-blind, crossover trial of air purification. Circulation 2017, 136, 618–627. [Google Scholar] [CrossRef] [PubMed]
  31. Maloberti, A.; Bombelli, M.; Vallerio, P.; Milani, M.; Cartella, I.; Tavecchia, G.; Tognola, C.; Grasso, E.; Sun, J.; de Chiara, B.; et al. Metabolic syndrome is related to vascular structural alterations but not to functional ones both in hypertensives and healthy subjects. Nutr. Metab. Cardiovas. Dis. 2021, 31, 1044–1052. [Google Scholar] [CrossRef]
  32. Woo, K.S.; Kwok, T.C.Y.; Celermajer, D.S. Vegan diet, subnormal vitamin B-12 status and cardiovascular health. Nutrients 2014, 6, 3259–3273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. O’Leary, D.H.; Polak, J.F.; Kronmal, R.A.; Manolio, T.A.; Burke, G.L.; Wolfson, S.K., Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. N. Engl. J. Med. 1999, 340, 14–22. [Google Scholar] [CrossRef]
  34. Baumgartner, J.; Smith, K.R.; Chockalingam, A. Reducing CVD through improvements in household energy - Implications for policy-relevant research. Global. Heart 2012, 7, 243–247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Langrish, J.; Mills, N.; Chan, J.; Leseman, D.; Aitken, R.; Fokkens, P.; Cassee, F.; Li, J.; Donaldson, K.; Newby, D.; et al. Beneficial cardiovascular effects of reducing exposure to particulate air pollution with a simple facemask. Part. Fibre Toxicol. 2009, 6, 8. [Google Scholar] [CrossRef] [Green Version]
  36. Allen, R.W.; Carlsten, C.; Karlen, B.; Leckie, S.; van Eeden, S.; Vedal, S.; Wong, I.; Brauer, M. An air filter intervention study of endothelial function among healthy adults in a woodsmoke-impacted community. Am. J. Respir. Crit. Care Med. 2011, 183, 1222–1230. [Google Scholar] [CrossRef] [PubMed]
  37. Rajagopalan, S.; Brook, R.D. Indoor-outdoor air pollution continuum and CVD burden–An opportunity for improving global health. Glob. Heart 2012, 7, 207–213. [Google Scholar] [CrossRef] [Green Version]
Atmosphere 12 01552 g001 550
Figure 1. (A) Far view of residential estates and Mount Ma On along the Shing Moon River of Shatin, Hong Kong on clear day with PM2.5 concentration of 14 µg/m3, and (B) on foggy polluted day with PM2.5 concentration of 45 µg/m3 (Woo et al. [18]).
Figure 1. (A) Far view of residential estates and Mount Ma On along the Shing Moon River of Shatin, Hong Kong on clear day with PM2.5 concentration of 14 µg/m3, and (B) on foggy polluted day with PM2.5 concentration of 45 µg/m3 (Woo et al. [18]).
Atmosphere 12 01552 g001
Atmosphere 12 01552 g002 550
Figure 2. (A) Sky view of Chongqing Garden on clear day with PM2.5 concentration of 45 µg/m3, and (B) Chongqing residence estate near riverside on a foggy day with PM2.5 concentration of 79 µg/m3 (Courtesy of Prof. YH Yin).
Figure 2. (A) Sky view of Chongqing Garden on clear day with PM2.5 concentration of 45 µg/m3, and (B) Chongqing residence estate near riverside on a foggy day with PM2.5 concentration of 79 µg/m3 (Courtesy of Prof. YH Yin).
Atmosphere 12 01552 g002
Table
Table 1. Demographic Characteristics of Southern–Northern China.
Table 1. Demographic Characteristics of Southern–Northern China.
Southern China
(n = 395)		Northern China
(n = 928)		p-Value
(Bonferroni Adjusted)
Male Gender (%)48470.719 (>0.99)
Age (yr)46.8 ± 12.847.4 ± 9.50.340 (>0.99)
Smoking Status (%)1535<0.0001 (0.0015)
BMI23.0 ± 4.023.4 ± 3.4<0.203 (>0.99)
SBP (mmHg)119.0 ± 15.7123.7 ± 17.6<0.0001 (0.0015)
DBP (mmHg)75.9 ± 9.380.2 ± 11.0<0.0001 (0.0015)
PM2.5 (µg/m3)44.0 ± 6.871.1 ± 15.8<0.0001 (0.0015)
Creatinine (μmol/L)81.7 ± 16.163.2 ± 16.7<0.0001 (0.0015)
Glucose (mmol/L)5.6 ± 1.25.4 ± 6.00.004 (0.06)
LDL-C3.4 ± 1.02.56 ± 0.82<0.0001 (0.0015)
Metabolic Syndrome (%)15.024.5<0.0001 (0.0015)
B12 (pmol/L)411.7 ± 249.4156.5 ± 90.6<0.0001 (0.0015)
Folate (nmol/L)31.1 ± 15.613.1 ± 5.6<0.0001 (0.0015)
Homocysteine (umol/L)9.6 ± 4.525.0 ± 21.0<0.0001
B12: Vitamin B12. BMI: Body Mass Index. DBP: Diastolic Blood Pressure. LDL-C: Low Density Lipoprotein Cholesterol. PM2.5: Particulate Matter <2.5 um in Diameter.
Table
Table 2. Vascular Parameters in Northern–Southern China Locations.
Table 2. Vascular Parameters in Northern–Southern China Locations.
Location
SouthernNorthern p-Value
Hyperemia (%)655 ± 289715 ± 2170.006
(95% CI)(623–686)(687–743)
GTN (%)18.1 ± 4.818.2 ± 3.00.912
(95% CI)(17.6–18.7)(17.8–18.6)
FMD (%)8.1 ± 3.07.5 ± 1.8 †0.001
(95% CI)(7.8–8.5)(7.3–7.7)
Carotid IMT (mm)0.57 ± 0.130.68 ± 0.13 ††0.0001
(95% CI)(0.56–0.58)(0.67–0.69)
Compared with Southern China † p < 0.0001; †† p = 0.01. FMD: Flow-mediated Dilation. GTN: Glyceryltrinitrate Dilation. IMT: Intima-media Thickness.
Table
Table 3. Determinants of Risk Factors for Brachial FMD *.
Table 3. Determinants of Risk Factors for Brachial FMD *.
Southern Chinese *Northern Chinese **Overall Cohort ***
Risk FactorsBeta Valuep-ValueBeta Valuep-ValueBeta-Valuep-Value
Age (yr)−0.2380.005−0.1630.062−0.210<0.0001
Gender−0.1740.050−0.3290.009−0.1630.013
Smoking status −0.1540.0770.0290.802−0.1180.075
BMI−0.0360.674−0.0400.4150.0050.938
MS−0.0670.436−0.0320.741−0.0510.403
Homocysteine0.0760.374−0.1960.066−0.0250.725
LDL-C−0.0580.473−0.0570.502−0.0900.206
MTHFR −0.0970.2010.1580.114−0.0140.822
PM2.5−0.2740.0010.0110.892−0.0220.862
Location----−0.3250.005
* Model R2 = 0.202; F-value = 4.026; p < 0.0001. ** Model R2 = 0.211; F-value = 3.802; p < 0.0001. *** Model R2 = 0.190; F-value = 7.802; p < 0.0001. BMI: Body Mass Index. FMD: Flow-mediated Dilation. LDL-C: Low Density Lipoprotein Cholesterol. MTHFR: Methylenetetrahydrofolate Reductase Gene Polymorphisms. PM2.5: Particulate Matters < 2.5 um in Diameter.
Table
Table 4. Determinants of Risk Factors for Carotid IMT.
Table 4. Determinants of Risk Factors for Carotid IMT.
Southern Chinese *Northern Chinese **Overall Cohort ***
Risk FactorsBeta Valuep-ValueBeta Valuep-ValueBeta-Valuep-Value
Age (yr)0.393<0.00010.385<0.00010.396<0.0001
Gender0.1460.0430.0580.3570.1270.006
Smoking status 0.0610.3880.1570.0100.0910.053
BMI0.0740.2990.0880.1030.1210.005
MS0.1190.0950.1100.0390.0990.019
Homocysteine0.0480.5010.1370.0140.1210.010
LDL-C0.0840.2040.1450.0030.1360.004
MTHFR 0.0460.463−0.0650.223−0.0260.554
PM2.50.334<0.00010.0330.4710.368<0.0001
Location----−0.2060.002
* Model R2 = 0.451; F-value = 13.3; p < 0.0001. ** Model R2 = 0.335; F-value = 7.67; p < 0.0001. *** Model R2 = 0.362; F-value = 27.1; p < 0.0001. BMI: Body Mass Index. IMT: Intima-media thickness. LDL-C: Low Density Lipoprotein Cholesterol. MS: Metabolic Syndrome. MTHFR: Methylenetetrahydrofolate Reductase Gene Polymorphisms. PM2.5: Particulate Matters < 2.5 um in Diameter.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Woo, K.; Lin, C.; Yin, Y.; Guo, D.; Chook, P.; Kwok, T.C.Y.; Celermajer, D.S. The Impact of Air Pollution (PM2.5) on Atherogenesis in Modernizing Southern versus Northern China. Atmosphere 2021, 12, 1552. https://doi.org/10.3390/atmos12121552

AMA Style

Woo K, Lin C, Yin Y, Guo D, Chook P, Kwok TCY, Celermajer DS. The Impact of Air Pollution (PM2.5) on Atherogenesis in Modernizing Southern versus Northern China. Atmosphere. 2021; 12(12):1552. https://doi.org/10.3390/atmos12121552

Chicago/Turabian Style

Woo, Kamsang, Changqing Lin, Yuehui Yin, Dongshuang Guo, Ping Chook, Timothy C. Y. Kwok, and David S. Celermajer. 2021. "The Impact of Air Pollution (PM2.5) on Atherogenesis in Modernizing Southern versus Northern China" Atmosphere 12, no. 12: 1552. https://doi.org/10.3390/atmos12121552

APA Style

Woo, K., Lin, C., Yin, Y., Guo, D., Chook, P., Kwok, T. C. Y., & Celermajer, D. S. (2021). The Impact of Air Pollution (PM2.5) on Atherogenesis in Modernizing Southern versus Northern China. Atmosphere, 12(12), 1552. https://doi.org/10.3390/atmos12121552

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop