Abstract
Several studies have shown the effects of PM2.5 exposure on respiratory and cardiovascular systems. However, there is no cohort study evidence of adverse effects of PM2.5 exposure on survival in patients with hepatocellular carcinoma (HCC) in China. This study is aimed at evaluating this association. This cohort study included 1440 HCC patients treated at the Third Central Clinical College of Tianjin Medical University from September 2013 to December 2018. We collected patient information, including demographic data, medical history, lifestyle characteristics, and disease characteristics. Based on PM2.5 concentrations measured at monitoring stations, the inverse distance weighted (IDW) method was used to assess the individuals’ exposure during their survival period. Survival status was analysed by the Kaplan–Meier method. Restricted cubic splines and Cox proportional hazards models were used to estimate the relationship between PM2.5 and mortality, and potential confounders were adjusted for. The mortality rate of HCC patients exposed to PM2.5 ≥ 58.56 μg/m3 was significantly higher than that of HCC patients living in environments with PM2.5 < 58.56 μg/m3 (79.0% vs 50.7%, P < 0.001). The restricted cubic spline model showed a linear relationship between the PM2.5 concentration and mortality risk (P overall-association < 0.0001 and P nonlinear-association = 0.3568). Cox regression analysis showed that after adjusting for confounding factors, for every 10-μg/m3 increase in atmospheric PM2.5, the risk of death for HCC patients increased by 44% [hazard ratio (HR) = 1.44, 95% confidence interval (CI) 1.34, 1.56; P < 0.001]. Compared with patients exposed to PM2.5 <58.56 μg/m3, those exposed to PM2.5 ≥ 58.56 μg/m3 had a 1.55-fold increased risk of death. Stratified analysis results showed that the effects of PM2.5 on HCC mortality were more significant in patients aged ≥60 years or patients living in central urban areas. We found that exposure to elevated PM2.5 after HCC diagnosis may affect survival, with a higher concentration corresponding to a greater effect.
Similar content being viewed by others
Availability of data and materials
All the data used to support the findings of this study are available on reasonable request from the corresponding author.
References
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2016) Outdoor air pollution. Iarc Monogr Eval Carcinog Risks Hum 109:9–444
Deng H, Eckel SP, Liu L, Lurmann FW, Cockburn MG, Gilliland FD (2017) Particulate matter air pollution and liver cancer survival. Int J Cancer 141(4):744–749
Gores GJ (2014) Decade in review-hepatocellular carcinoma: HCC-subtypes, stratification and sorafenib. Nat Rev Gastroenterol Hepatol 11(11):645–647
Harris PS, Hansen RM, Gray ME, Massoud OI, McGuire BM, Shoreibah MG (2019) Hepatocellular carcinoma surveillance: an evidence-based approach. World J Gastroenterol 25(13):1550–1559
Kim JW, Park S, Lim CW, Lee K, Kim B (2014) The role of air pollutants in initiating liver disease. Toxicol Res 30(2):65–70
Lee CH, Hsieh SY, Huang WH, Wang IK, Yen TH (2019) Association between ambient particulate matter 2.5 exposure and mortality in patients with hepatocellular carcinoma. Int J Environ Res Public Health 16(14)
Liu C, Chen R, Sera F, Vicedo-Cabrera AM, Guo Y, Tong S, Mszs Coelho PHN, Saldiva E, Lavigne P, Matus NV, Ortega SO, Garcia M, Pascal M, Stafoggia M, Scortichini M, Hashizume Y, Honda M, Hurtado-Díaz J, Cruz B et al (2019) Ambient particulate air pollution and daily mortality in 652 cities. N Engl J Med 381(8):705–715
Llovet JM, Brú C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19(3):329–338
Luo J, Liu H, Hua S, Song L (2022) The correlation of PM2.5 exposure with acute attack and steroid sensitivity in asthma. Biomed Res Int 2022:2756147
Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R (1973) Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 60(8):646–649
Rumgay H, Ferlay J, de Martel C, Georges D, Ibrahim AS, Zheng R, Wei W, Lemmens V, Soerjomataram I (2022) Global, regional and national burden of primary liver cancer by subtype. Eur J Cancer 161:108–118
Schneider KM, Mohs A, Gui W, Galvez EJC, Candels LS, Hoenicke L, Muthukumarasamy U, Holland CH, Elfers C, Kilic K, Schneider CV, Schierwagen R, Strnad P, Wirtz TH, Marschall HU, Latz E, Lelouvier B, Saez-Rodriguez J, de Vos W et al (2022) Imbalanced gut microbiota fuels hepatocellular carcinoma development by shaping the hepatic inflammatory microenvironment. Nat Commun 13(1):3964
Shiina S, Tateishi R, Imamura M, Teratani T, Koike Y, Sato S, Obi S, Kanai F, Kato N, Yoshida H, Omata M, Koike K (2012) Percutaneous ethanol injection for hepatocellular carcinoma: 20-year outcome and prognostic factors. Liver Int 32(9):1434–1442
Strak M, Weinmayr G, Rodopoulou S, Chen J, de Hoogh K, Andersen ZJ, Atkinson R, Bauwelinck M, Bekkevold T, Bellander T, Boutron-Ruault MC, Brandt J, Cesaroni G, Concin H, Fecht D, Forastiere F, Gulliver J, Hertel O, Hoffmann B et al (2021) Long term exposure to low level air pollution and mortality in eight European cohorts within the ELAPSE project: pooled analysis. BMJ 374:n1904
Su J, Sze NN, Bai L (2021) A joint probability model for pedestrian crashes at macroscopic level: roles of environment, traffic, and population characteristics. Accid Anal Prev 150:105898
Sun Y, Wu L, Zhong Y, Zhou K, Hou Y, Wang Z, Zhang Z, Xie J, Wang C, Chen D, Huang Y, Wei X, Shi Y, Zhao Z, Li Y, Guo Z, Yu Q, Xu L, Volpe G et al (2021) Single-cell landscape of the ecosystem in early-relapse hepatocellular carcinoma. Cell 184(2):404–21.e16
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 71(3):209–249
Thangavel P, Park D, Lee YC (2022) Recent insights into particulate matter (PM2.5)-mediated toxicity in humans: an overview. Int J Environ Res Public Health 19(12)
Villanueva A (2019) Hepatocellular carcinoma. N Engl J Med 380(15):1450–1462
VoPham T, Bertrand KA, Tamimi RM, Laden F, Hart JE (2018) Ambient PM2.5 air pollution exposure and hepatocellular carcinoma incidence in the United States. Cancer Causes Control 29(6):563–572
Wang Z, Li Z, Ye Y, Xie L, Li W (2016) Oxidative stress and liver cancer: etiology and therapeutic targets. Oxid Med Cell Longev 2016:7891574
Wong CM, Tsang H, Lai HK, Thomas GN, Lam KB, Chan KP, Zheng Q, Ayres JG, Lee SY, Lam TH, Thach TQ (2016) Cancer mortality risks from long-term exposure to ambient fine particle. Cancer Epidemiol Biomarkers Prev 25(5):839–845
Wu F, Kong S, Yan Q, Wang W, Liu H, Wu J, Zheng H, Zheng S, Cheng Y, Niu Z, Liu D, Qi S (2020) Sub-type source profiles of fine particles for fugitive dust and accumulative health risks of heavy metals: a case study in a fast-developing city of China. Environ Sci Pollut Res Int 27(14):16554–16573
Yin P, Brauer M, Cohen AJ, Wang H, Li J, Burnett RT, Stanaway JD, Causey K, Larson S, Godwin W, Frostad J, Marks A, Wang L, Zhou M, Murray CJL (2020) The effect of air pollution on deaths, disease burden, and life expectancy across China and its provinces, 1990-2017: an analysis for the Global Burden of Disease Study 2017. Lancet Planet Health 4(9):e386–ee98
Zhang H, Li Z (2019) MicroRNA-16 Via Twist1 inhibits EMT induced by PM2.5 exposure in human hepatocellular carcinoma. Open Med (Wars) 14:673–682
Zhang Q, Luo Q, Yuan X, Chai L, Li D, Liu J, Lv Z (2017) Atmospheric particulate matter(2.5) promotes the migration and invasion of hepatocellular carcinoma cells. Oncol Lett 13(5):3445–3450
Zhang Z, Hu S, Fan P, Li L, Feng S, Xiao H, Zhu L (2021) The roles of liver inflammation and the insulin signaling pathway in PM2.5 instillation-induced insulin resistance in Wistar rats. Dis Markers 2021:2821673
Zheng Z, Zhang X, Wang J, Dandekar A, Kim H, Qiu Y, Xu X, Cui Y, Wang A, Chen LC, Rajagopalan S, Sun Q, Zhang K (2015) Exposure to fine airborne particulate matters induces hepatic fibrosis in murine models. J Hepatol 63(6):1397–1404
Funding
This work was supported by Tianjin Key Medical Discipline (Specialty) Construction Project (No. TJYXZDXK-034A) and the Natural Science Foundation of Tianjin Science and Technology Bureau (No. 21JCQNJC01460).
Author information
Authors and Affiliations
Contributions
Conceptualization, writing—original draft, and resources were performed by Hao Cui. Conceptualization and writing—original draft—were performed by Ye Qi. Visualisation and formal analysis were performed by Chunyue Guo. Writing-review and editing and supervision were performed by Naijun Tang.
Corresponding author
Ethics declarations
Ethics approval
This retrospective cohort study was conducted in accordance with the Declaration of Helsinki and was approved by the ethics committee of the Third Central Clinical College of Tianjin Medical University.
Consent to participate
We obtained participants’ informed consent before we began data collection.
Consent for publication
The authors give their consent to publish all submitted material.
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.
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.
About this article
Cite this article
Cui, H., Qi, Y., Guo, C. et al. The effect of PM2.5 exposure on the mortality of patients with hepatocellular carcinoma in Tianjin, China. Environ Sci Pollut Res 30, 78632–78640 (2023). https://doi.org/10.1007/s11356-023-28039-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-28039-1