Abstract
Previous research has found relationships between some single metals and lung function parameters. However, the role of simultaneous multi-metal exposure is poorly understood. The crucial period throughout childhood, when people are most susceptible to environmental dangers, has also been largely ignored. The study aimed to evaluate the joint and individual associations of 12 selected urinary metals with pediatric lung function measures using multi-pollutant approaches. A total of 1227 children aged 6–17 years from the National Health and Nutrition Examination Survey database of the 2007–2012 cycles were used. The metal exposure indicators were 12 urine metals adjusted for urine creatinine, including arsenic (As), barium (Ba), cadmium (Cd), cesium (Cs), cobalt (Co), mercury (Hg), molybdenum (Mo), lead (Pb), antimony (Sb), thallium (Tl), tungsten (Tu), and uranium (Ur). The outcomes of interest were lung function indices, including the 1st second of a forceful exhalation (FEV1), forced vital capacity (FVC), forced expiratory flow between 25 and 7% of vital capacity (FEF25–75%), and peak expiratory flow (PEF). Multivariate linear regression, quantile g-computation (QG-C), and Bayesian kernel machine regression models (BKMR) were adopted. A significantly negative overall effect of metal mixtures on FEV1 (β = − 161.70, 95% CI − 218.12, − 105.27; p < 0.001), FVC (β = − 182.69, 95% CI − 246.33, − 119.06; p < 0.001), FEF25–75% (β = − 178.86 (95% CI − 274.47, − 83.26; p < 0.001), and PEF (β = − 424.17, 95% CI − 556.55, − 291.80; p < 0.001) was observed. Pb had the largest negative contribution to the negative associations, with posterior inclusion probabilities (PIPs) of 1 for FEV1, FVC, and FEF25–75%, and 0.9966 for PEF. And Pb’s relationship with lung function metrics showed to be nonlinear, with an approximate “L” shape. Potential interactions between Pb and Cd in lung function decline were observed. Ba was positively associated with lung function metrics. Metal mixtures were negatively associated with pediatric lung function. Pb might be a crucial element. Our findings highlight the need for prioritizing children’s environmental health to protect them from later respiratory disorders and to guide future research into the toxic mechanisms of metal-mediated lung function injury in the pediatric population.
Similar content being viewed by others
Abbreviations
- FEV1 :
-
1st second of a forceful exhalation
- FVC:
-
Forced vital capacity
- FEF25–75% :
-
Forced expiratory flow between 25 and 75% of vital capacity
- PEF:
-
Peak expiratory flow
- As:
-
Arsenic
- Ba:
-
Barium
- Be:
-
Beryllium
- Cd:
-
Cadmium
- Cs:
-
Cesium
- Co:
-
Cobalt
- Hg:
-
Mercury
- Mo:
-
Molybdenum
- Pb:
-
Lead
- Pt:
-
Platinum
- Sb:
-
Antimony
- Tl:
-
Thallium
- Tu:
-
Tungsten
- Ur:
-
Uranium
- NCHS:
-
National Center for Health Statistics
- NHANES:
-
National Health and Nutrition Examination Survey
- ATS:
-
American Thoracic Society
- PIR:
-
Income-to-poverty ratio
- BMI:
-
Body mass index
- ICP-MS:
-
Inductively coupled plasma–mass spectrometry
- ICP-DRC-MS:
-
Inductively coupled plasma dynamic reaction cell–mass spectrometry
- LOD:
-
Limit of detection
- SD:
-
Standard deviation
- QG-C:
-
G-computation model
- WQS:
-
Weighted quantile sum
- BKMR:
-
Bayesian kernel machine regression
- MCMC:
-
Markov chain Monte Carlo
- PIP:
-
Posterior inclusion probabilities
- CI:
-
Confidence interval
- PAH:
-
Polycyclic aromatic hydrocarbon
- ROS:
-
Reactive oxygen species
- MDA:
-
Malonaldehyde
References
Agustí, A., Noell, G., Brugada, J., & Faner, R. (2017). Lung function in early adulthood and health in later life: A transgenerational cohort analysis. The Lancet Respiratory Medicine, 5, 935–945. https://doi.org/10.1016/s2213-2600(17)30434-4
Ashrap, P., Watkins, D. J., Milne, G. L., Ferguson, K. K., Loch-Caruso, R., Fernandez, J., Rosario, Z., Vélez-Vega, C. M., Alshawabkeh, A., Cordero, J. F., & Meeker, J. D. (2021). Maternal urinary metal and metalloid concentrations in association with oxidative stress biomarkers. Antioxidants (Basel). https://doi.org/10.3390/antiox10010114
Atapaththu, K. S., Rashid, M. H., & Asaeda, T. (2016). Growth and oxidative stress of brittlewort (Nitella pseudoflabellata) in response to cesium exposure. Bulletin of Environment Contamination and Toxicology, 96, 347–353. https://doi.org/10.1007/s00128-016-1736-4
Bhagat, J., Nishimura, N., & Shimada, Y. (2021). Toxicological interactions of microplastics/nanoplastics and environmental contaminants: Current knowledge and future perspectives. Journal of hazardous materials, 405, 123913. https://doi.org/10.1016/j.jhazmat.2020.123913
Bobb, J. F., Claus Henn, B., Valeri, L., & Coull, B. A. (2018). Statistical software for analyzing the health effects of multiple concurrent exposures via Bayesian kernel machine regression. Environmental Health, 17, 67. https://doi.org/10.1186/s12940-018-0413-y
Bobb, J. F., Valeri, L., Claus Henn, B., Christiani, D. C., Wright, R. O., Mazumdar, M., Godleski, J. J., & Coull, B. A. (2015). Bayesian kernel machine regression for estimating the health effects of multi-pollutant mixtures. Biostatistics, 16, 493–508. https://doi.org/10.1093/biostatistics/kxu058
Bui, D. S., Lodge, C. J., Burgess, J. A., Lowe, A. J., Perret, J., Bui, M. Q., Bowatte, G., Gurrin, L., Johns, D. P., Thompson, B. R., Hamilton, G. S., Frith, P. A., James, A. L., Thomas, P. S., Jarvis, D., Svanes, C., Russell, M., Morrison, S. C., Feather, I., … Dharmage, S. C. (2018). Childhood predictors of lung function trajectories and future COPD risk: A prospective cohort study from the first to the sixth decade of life. The Lancet Respiratory Medicine, 6, 535–544. https://doi.org/10.1016/s2213-2600(18)30100-0
Caicedo, M. S., Pennekamp, P. H., McAllister, K., Jacobs, J. J., & Hallab, N. J. (2010). Soluble ions more than particulate cobalt-alloy implant debris induce monocyte costimulatory molecule expression and release of proinflammatory cytokines critical to metal-induced lymphocyte reactivity. Journal of Biomedical Materials Research Part A, 93, 1312–1321. https://doi.org/10.1002/jbm.a.32627
Cheng, Y. J., Chen, Z. G., Li, Z. Y., Mei, W. Y., Bi, W. T., & Luo, D. L. (2021). Longitudinal change in lung function and subsequent risks of cardiovascular events: Evidence from four prospective cohort studies. BMC Medicine, 19, 153. https://doi.org/10.1186/s12916-021-02023-3
Choi, H. S., Lee, S. W., Kim, J. T., & Lee, H. K. (2020). The association between pulmonary functions and incident diabetes: Longitudinal analysis from the ansung cohort in Korea. Diabetes and Metabolism Journal, 44, 699–710. https://doi.org/10.4093/dmj.2019.0109
Ciprandi, G., & Cirillo, I. (2019). The pragmatic role of FEF(25–75) in asymptomatic subjects, allergic rhinitis, asthma, and in military setting. Expert Review of Respiratory Medicine, 13, 1147–1151. https://doi.org/10.1080/17476348.2019.1674649
Feng, X., Zeng, G., Zhang, Q., Song, B., & Wu, K. H. (2022). Joint association of polycyclic aromatic hydrocarbons and heavy metal exposure with pulmonary function in children and adolescents aged 6–19 years. International Journal of Hygiene and Environmental Health, 244, 114007. https://doi.org/10.1016/j.ijheh.2022.114007
Gelman, A. (2007). Struggles with survey weighting and regression modeling. Statistical Science, 22, 153–164.
Gutteridge, J. M., & Halliwell, B. (2000). Free radicals and antioxidants in the year 2000. A historical look to the future. Annals of the New York Academy of Sciences, 899, 136–147. https://doi.org/10.1111/j.1749-6632.2000.tb06182.x
Hicks, R., Caldas, L. Q., Dare, P. R., & Hewitt, P. J. (1986). Cardiotoxic and bronchoconstrictor effects of industrial metal fumes containing barium. Archives of Toxicology Supplement, 9, 416–420. https://doi.org/10.1007/978-3-642-71248-7_84
Higashikawa, K., Zhang, Z. W., Shimbo, S., Moon, C. S., Watanabe, T., Nakatsuka, H., Matsuda-Inoguchi, N., & Ikeda, M. (2000). Correlation between concentration in urine and in blood of cadmium and lead among women in Asia. Science of the Total Environment, 246, 97–107. https://doi.org/10.1016/s0048-9697(99)00415-5
Hu, P., Su, W., Vinturache, A., Gu, H., Cai, C., Lu, M., & Ding, G. (2021). Urinary 3-phenoxybenzoic acid (3-PBA) concentration and pulmonary function in children: A national health and nutrition examination survey (NHANES) 2007–2012 analysis. Environmental Pollution, 270, 116178. https://doi.org/10.1016/j.envpol.2020.116178
Huang, X., **e, J., Cui, X., Zhou, Y., Wu, X., Lu, W., Shen, Y., Yuan, J., & Chen, W. (2016). Association between concentrations of metals in urine and adult asthma: A case-control study in Wuhan. China. PLoS One, 11, e0155818. https://doi.org/10.1371/journal.pone.0155818
Johnson, C. L., Paulose-Ram, R., Ogden, C. L., Carroll, M. D., Kruszan-Moran, D., Dohrmann, S. M., & Curtin, L. R. (2013). National health and nutrition examination survey. Analytic guidelines, 1999–2010. US Department of Health and Human Services.
Jomova, K., & Valko, M. (2011). Advances in metal-induced oxidative stress and human disease. Toxicology, 283, 65–87. https://doi.org/10.1016/j.tox.2011.03.001
Jonckheere, A. C., Steelant, B., Seys, S. F., Cremer, J., Dilissen, E., Boon, L., Liston, A., Schrijvers, R., Breynaert, C., Vanoirbeek, J. A. J., Ceuppens, J. L., & Bullens, D. M. A. (2022). Peribronchial inflammation resulting from regulatory T cell deficiency damages the respiratory epithelium and disturbs barrier function. The Journal of Immunology, 209, 1595–1605. https://doi.org/10.4049/jimmunol.2200416
Keil, A. P., Buckley, J. P., O’Brien, K. M., Ferguson, K. K., Zhao, S., & White, A. J. (2020). A quantile-based g-computation approach to addressing the effects of exposure mixtures. Environmental Health Perspectives, 128, 47004. https://doi.org/10.1289/ehp5838
Kuczmarski, R. J., Ogden, C. L., Guo, S. S., Grummer-Strawn, L. M., Flegal, K. M., Mei, Z., Wei, R., Curtin, L. R., Roche, A. F., & Johnson, C. L. (2002). 2000 CDC growth charts for the United States: Methods and development. Vital Health Stat, 11, 1–190.
Kuiper, N., Rowell, C., Nriagu, J., & Shomar, B. (2014). What do the trace metal contents of urine and toenail samples from Qatar׳s farm workers bioindicate? Environmental Research, 131, 86–94. https://doi.org/10.1016/j.envres.2014.02.011
Kumar, S., Prasad, S., Yadav, K. K., Shrivastava, M., Gupta, N., Nagar, S., Bach, Q. V., Kamyab, H., Khan, S. A., Yadav, S., & Malav, L. C. (2019). Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review. Environment Research, 179, 108792. https://doi.org/10.1016/j.envres.2019.108792
Kuwano, K. (2007). Epithelial cell apoptosis and lung remodeling. Cellular & Molecular Immunology, 4, 419–429.
Lai, Y. L., & Diamond, L. (1992). Cigarette smoke exposure does not prevent cadmium-induced alterations in rat lungs. Journal of Toxicology and Environment Health, 35, 63–76. https://doi.org/10.1080/15287399209531594
Leung, T. F., Chan, I. H., Liu, T. C., Lam, C. W., & Wong, G. W. (2013). Relationship between passive smoking exposure and urinary heavy metals and lung functions in preschool children. Pediatric Pulmonology, 48, 1089–1097. https://doi.org/10.1002/ppul.22801
Li, S., Wang, J., Zhang, B., Liu, Y., Lu, T., Shi, Y., Shan, G., & Dong, L. (2018). Urinary lead concentration is an independent predictor of cancer mortality in the U.S. general population. Frontiers in oncology, 8, 242. https://doi.org/10.3389/fonc.2018.00242
Madrigal, J. M., Persky, V., Jackson, B. P., Bain, A., Siemer, M., Pappalardo, A. A., & Argos, M. (2021). Assessment of metal concentrations and associations with pulmonary function among children with asthma in Chicago, Illinois. International Journal of Environmental Research and Public Health. https://doi.org/10.3390/ijerph18147279
Madrigal, J. M., Persky, V., Pappalardo, A., & Argos, M. (2018). Association of heavy metals with measures of pulmonary function in children and youth: Results from the national health and nutrition examination survey (NHANES). Environment International, 121, 871–878. https://doi.org/10.1016/j.envint.2018.09.045
Mannino, D. M., Holguin, F., Greves, H. M., Savage-Brown, A., Stock, A. L., & Jones, R. L. (2004). Urinary cadmium levels predict lower lung function in current and former smokers: Data from the third national health and nutrition examination survey. Thorax, 59, 194–198. https://doi.org/10.1136/thorax.2003.012054
Meo, S. A., & Al-Khlaiwi, T. (2003). Health hazards of welding fumes. Saudi Medical Journal, 24, 1176–1182.
Miller, A. C., Bonait-Pellie, C., Merlot, R. F., Michel, J., Stewart, M., & Lison, P. D. (2005a). Leukemic transformation of hematopoietic cells in mice internally exposed to depleted uranium. Molecular and Cellular Biochemistry, 279, 97–104. https://doi.org/10.1007/s11010-005-8226-z
Miller, M. R., Hankinson, J., Brusasco, V., Burgos, F., Casaburi, R., Coates, A., Crapo, R., Enright, P., van der Grinten, C. P., Gustafsson, P., Jensen, R., Johnson, D. C., MacIntyre, N., McKay, R., Navajas, D., Pedersen, O. F., Pellegrino, R., Viegi, G., & Wanger, J. (2005b). Standardisation of spirometry. European Respiratory Journal, 26, 319–338. https://doi.org/10.1183/09031936.05.00034805
Mitra, S., Chakraborty, A. J., Tareq, A. M., Emran, T. B., Nainu, F., Khusro, A., Idris, A. M., Khandaker, M. U., Osman, H., Alhumaydhi, F. A., & Simal-Gandara, J. (2022). Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter the toxicity. Journal of King Saud University - Science, 34, 101865. https://doi.org/10.1016/j.jksus.2022.101865
Miyata, R., & van Eeden, S. F. (2011). The innate and adaptive immune response induced by alveolar macrophages exposed to ambient particulate matter. Toxicology and Applied Pharmacology, 257, 209–226. https://doi.org/10.1016/j.taap.2011.09.007
Moitra, S., Blanc, P. D., & Sahu, S. (2013). Adverse respiratory effects associated with cadmium exposure in small-scale jewellery workshops in India. Thorax, 68, 565–570. https://doi.org/10.1136/thoraxjnl-2012-203029
Moitra, S., Chakraborty, K., Bhattacharyya, A., & Sahu, S. (2015). Impact of occupational cadmium exposure on spirometry, sputum leukocyte count, and lung cell DNA damage among Indian goldsmiths. American Journal of Industrial Medicine, 58, 617–624. https://doi.org/10.1002/ajim.22449
Nie, L., Chu, H., Liu, C., Cole, S. R., Vexler, A., & Schisterman, E. F. (2010). Linear regression with an independent variable subject to a detection limit. Epidemiology, 21(Suppl 4), S17-24. https://doi.org/10.1097/EDE.0b013e3181ce97d8
NIfHSCN. CfDCaP (2011) National health and nutrition examination survey (nhanes) respiratory health spirometry procedures manual.: by G Atlanta).
Nordberg, G. F., Fowler, B. A., & Nordberg, M. (2014). Handbook on the toxicology of metals. Academic press.
O’Brien, K. M., Upson, K., Cook, N. R., & Weinberg, C. R. (2016). Environmental chemicals in urine and blood: Improving methods for creatinine and lipid adjustment. Environmental Health Perspectives, 124, 220–227. https://doi.org/10.1289/ehp.1509693
Pan, Z., Guo, Y., **ang, H., Hui, Y., Ju, H., Xu, S., & Li, L. (2020). Effects of lead, mercury, and cadmium co-exposure on children’s pulmonary function. Biological Trace Element Research, 194, 115–120. https://doi.org/10.1007/s12011-019-01772-w
Pandya, C. D., Pillai, P. P., & Gupta, S. S. (2010). Lead and cadmium co-exposure mediated toxic insults on hepatic steroid metabolism and antioxidant system of adult male rats. Biological Trace Element Research, 134, 307–317. https://doi.org/10.1007/s12011-009-8479-6
Peana, M., Medici, S., Dadar, M., Zoroddu, M. A., Pelucelli, A., Chasapis, C. T., & Bjørklund, G. (2021). Environmental barium: Potential exposure and health-hazards. Archives of Toxicology, 95, 2605–2612. https://doi.org/10.1007/s00204-021-03049-5
Plataki, M., Koutsopoulos, A. V., Darivianaki, K., Delides, G., Siafakas, N. M., & Bouros, D. (2005). Expression of apoptotic and antiapoptotic markers in epithelial cells in idiopathic pulmonary fibrosis. Chest, 127, 266–274. https://doi.org/10.1378/chest.127.1.266
Qin, R., An, J., **e, J., Huang, R., **e, Y., He, L., Xv, H., Qian, G., & Li, J. (2021). FEF(25–75)% Is a More sensitive measure reflecting airway dysfunction in patients with asthma: A comparison study using FEF(25–75)% and FEV(1). The Journal of Allergy and Clinical Immunology. in Practice, 9, 3649-3659.e3646. https://doi.org/10.1016/j.jaip.2021.06.027
Rokadia, H. K., & Agarwal, S. (2013). Serum heavy metals and obstructive lung disease: Results from the national health and nutrition examination survey. Chest, 143, 388–397. https://doi.org/10.1378/chest.12-0595
Sallsten, G., Ellingsen, D. G., Berlinger, B., Weinbruch, S., & Barregard, L. (2022). Variability of lead in urine and blood in healthy individuals. Environmental Research, 212, 113412. https://doi.org/10.1016/j.envres.2022.113412
Sedman, R. M., Polisini, J. M., & Esparza, J. R. (1994). The evaluation of stack metal emissions from hazardous waste incinerators: Assessing human exposure through noninhalation pathways. Environmental Health Perspectives, 102(Suppl 2), 105–112. https://doi.org/10.1289/ehp.94102105
Smith, E., Gancarz, D., Rofe, A., Kempson, I. M., Weber, J., & Juhasz, A. L. (2012). Antagonistic effects of cadmium on lead accumulation in pregnant and non-pregnant mice. Journal of Hazardous Materials, 199–200, 453–456. https://doi.org/10.1016/j.jhazmat.2011.11.016
Sobel, M., Navas-Acien, A., Powers, M., Grau-Perez, M., Goessler, W., Best, L. G., Umans, J., Oelsner, E. C., Podolanczuk, A., & Sanchez, T. R. (2022). Environmental-level exposure to metals and metal-mixtures associated with spirometry-defined lung disease in American Indian adults: Evidence from the Strong Heart Study. Environment Research, 207, 112194. https://doi.org/10.1016/j.envres.2021.112194
Song, S., Han, Y., Zhang, Y., Ma, H., Zhang, L., Huo, J., Wang, P., Liang, M., & Gao, M. (2019). Protective role of citric acid against oxidative stress induced by heavy metals in Caenorhabditis elegans. Environmental Science and Pollution Research International, 26, 36820–36831. https://doi.org/10.1007/s11356-019-06853-w
Statistics NCfH (2017) National health and nutrition examination survey, Vol. 2021: Questionnaires, datasets, and related documentation. https://wwwn.cdc.gov/nchs/nhanes/Default.aspx
Surolia, R., Karki, S., Kim, H., Yu, Z., Kulkarni, T., Mirov, S. B., Carter, A. B., Rowe, S. M., Matalon, S., Thannickal, V. J., Agarwal, A., & Antony, V. B. (2015). Heme oxygenase-1-mediated autophagy protects against pulmonary endothelial cell death and development of emphysema in cadmium-treated mice. American Journal of Physiology Lung Cellular and Molecular Physiology, 309, L280-292. https://doi.org/10.1152/ajplung.00097.2015
Suwazono, Y., Kido, T., Nakagawa, H., Nishijo, M., Honda, R., Kobayashi, E., Dochi, M., & Nogawa, K. (2009). Biological half-life of cadmium in the urine of inhabitants after cessation of cadmium exposure. Biomarkers, 14, 77–81. https://doi.org/10.1080/13547500902730698
Tantucci, C., Duguet, A., Giampiccolo, P., Similowski, T., Zelter, M., & Derenne, J. P. (2002). The best peak expiratory flow is flow-limited and effort-independent in normal subjects. American Journal of Respiratory and Critical Care Medicine, 165, 1304–1308. https://doi.org/10.1164/rccm.2012008
Thompson González, N., Ong, J., Luo, L., & MacKenzie, D. (2022). Chronic community exposure to environmental metal mixtures is associated with selected cytokines in the navajo birth cohort study (NBCS). International Journal of Environmental Research and Public Health. https://doi.org/10.3390/ijerph192214939
Ueha, R., Nativ-Zeltzer, N., Sato, T., Goto, T., Yamauchi, A., Belafsky, P. C., & Yamasoba, T. (2020). The effects of barium concentration levels on the pulmonary inflammatory response in a rat model of aspiration. European Archives of Oto-Rhino-Laryngology, 277, 189–196. https://doi.org/10.1007/s00405-019-05666-4
Wang, X., Dockery, D. W., Wypij, D., Fay, M. E., & Ferris, B. G., Jr. (1993). Pulmonary function between 6 and 18 years of age. Pediatric Pulmonology, 15, 75–88. https://doi.org/10.1002/ppul.1950150204
Wei, W., Wu, X., Bai, Y., Li, G., Feng, Y., Meng, H., Li, H., Li, M., Zhang, X., He, M., & Guo, H. (2020). Lead exposure and its interactions with oxidative stress polymorphisms on lung function impairment: Results from a longitudinal population-based study. Environmental Research, 187, 109645. https://doi.org/10.1016/j.envres.2020.109645
White, A. J., O’Brien, K. M., Jackson, B. P., & Karagas, M. R. (2018). Urine and toenail cadmium levels in pregnant women: A reliability study. Environment International, 118, 86–91. https://doi.org/10.1016/j.envint.2018.05.030
Wu, L., Cui, F., Ma, J., Huang, Z., Zhang, S., **ao, Z., Li, J., Ding, X., & Niu, P. (2022). Associations of multiple metals with lung function in welders by four statistical models. Chemosphere, 298, 134202. https://doi.org/10.1016/j.chemosphere.2022.134202
Wu, S., Deng, F., Hao, Y., Shima, M., Wang, X., Zheng, C., Wei, H., Lv, H., Lu, X., Huang, J., Qin, Y., & Guo, X. (2013). Chemical constituents of fine particulate air pollution and pulmonary function in healthy adults: The healthy volunteer natural relocation study. Journal of Hazardous Materials, 260, 183–191. https://doi.org/10.1016/j.jhazmat.2013.05.018
Yoon, J. H., Kim, I., Kim, H. R., Won, J. U., Bae, K. J., Jung, P. K., & Roh, J. (2015). The association between blood cadmium level and airflow obstruction in Korean men. Annals of Human Biology, 42, 569–575. https://doi.org/10.3109/03014460.2014.990512
Zeng, X., Xu, X., Boezen, H. M., Vonk, J. M., Wu, W., & Huo, X. (2017). Decreased lung function with mediation of blood parameters linked to e-waste lead and cadmium exposure in preschool children. Environmental Pollution, 230, 838–848. https://doi.org/10.1016/j.envpol.2017.07.014
Zhang, L., Fang, B., Wang, H., Zeng, H., Wang, N., Wang, M., Wang, X., Hao, Y., Wang, Q., & Yang, W. (2023). The role of systemic inflammation and oxidative stress in the association of particulate air pollution metal content and early cardiovascular damage: A panel study in healthy college students. Environ Pollut, 323, 121345. https://doi.org/10.1016/j.envpol.2023.121345
Zheng, G., Xu, X., Li, B., Wu, K., Yekeen, T. A., & Huo, X. (2013). Association between lung function in school children and exposure to three transition metals from an e-waste recycling area. Journal of Exposure Science & Environmental Epidemiology, 23, 67–72. https://doi.org/10.1038/jes.2012.84
Funding
This work was supported by National Natural Science Foundation of China [82273651, 81874266], the public health sub-project of the construction of high-level local colleges and universities project (E1-2602-21-201006-6) from College of Public Health, Shanghai University of Medicine and Health Science.
Author information
Authors and Affiliations
Contributions
YC was involved in conceptualization, methodology, software, data curation, writing—original draft, and writing—reviewing and editing. AZ was responsible for software, writing—original draft, and writing—reviewing and editing. RL contributed to formal analysis and Software. WK participated in visualization and software. JW carried out the formal analysis. YY took part in software and resources. ST was involved in methodology and writing—reviewing and editing. SL was responsible for funding acquisition, conceptualization, methodology, and writing—reviewing and editing. JC contributed to funding acquisition, methodology, and writing—reviewing and editing. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethics approval
This study was approved by the National Center for Health Statistics Research Ethics Review Board.
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
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
Chen, Y., Zhao, A., Li, R. et al. Independent and combined associations of multiple-heavy-metal exposure with lung function: a population-based study in US children. Environ Geochem Health 45, 5213–5230 (2023). https://doi.org/10.1007/s10653-023-01565-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-023-01565-0