Skip to main content

Advertisement

Log in

Associations and dose-response relationships between different kinds of urine polycyclic aromatic hydrocarbons metabolites and adult lung functions

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Associations and dose-response relationships between different kinds of urine polycyclic aromatic hydrocarbons (PAHs) metabolites and lung functions in general American adults were unknown. Data from the National Health and Nutrition Examination Survey database of the 2009–2012 cycles were used. The independent variables were urine PAHs adjusted for urine creatinine, including 1-hydroxynaphthalene (1-NAP), 2-hydroxynaphthalene (2-NAP), 3-hydroxyfluorene (3-FLU), 2-hydroxyfluorene (2-FLU), 3-hydroxyphenanthrene (3-PHE), 1-hydroxyphenanthrene (1-PHE), 2-hydroxyphenanthrene (2-PHE), 1-hydroxypyrene (1-PYR), and 9-hydroxyfluorene (9-FLU). The dependent variables were lung function indices including the forced vital capacity (FVC), the 1st second of a forceful exhalation (FEV1), the ratio of FEV1/FVC, the forced expiratory flow rate 25–75% (FEF25%-75%), and the fractional exhaled nitric oxide (FENO). Multivariate linear regression analyses and the restricted cubic splines were used. Except for 1-PHE and 9-FLU, FEF25%-75% decreased in quartile (Q) 4 of all the remaining seven PAHs; FEV1 decreased in Q4 of 2-NAP, 3-PHE, 2-PHE, and 9-FLU, with β (SE) of −121.89 (45.46), −105.21 (33.57), −143.67 (40.60), and −127.71 (37.14), respectively. FVC decreased only in Q3 of 9-FLU, with β (SE) of −142.24 (56.54); FEV1/FVC decreased in Q4 of all PAHs except for 2-FLU. Besides, FENO decreased in Q4 of all PAHs in smokers, while in non-smokers, the results were opposite. The dose-response relationships were non-linear. In conclusion, we found that urine PAHs may relate to the changes in lung functions. Besides, smoking status had a significant influence on FENO; FENO decreased in smokers while increased in non-smokers, suggesting that PAHs exposure may relate to airway inflammation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig 1
Fig 2
Fig 3
Fig 4

Similar content being viewed by others

Data availability

The datasets generated and/or analyzed during the current study are available in the [NHANES] repository [https://wwwn.cdc.gov/nchs/nhanes/Search/DataPage.aspx?Component=Laboratory

https://wwwn.cdc.gov/Nchs/Nhanes/2009-2010/SPX_F.htm].

Abbreviations

NHANES:

National Health and Nutrition Examination Survey

PAHs:

Polycyclic aromatic hydrocarbons

1-NAP:

1-hydroxynaphthalene

2-NAP:

2-hydroxynaphthalene

3-NAP:

3-hydroxyfluorene

2-FLU:

2-hydroxyfluorene

3-PHE:

3-hydroxyphenanthrene

1-PHE:

1-hydroxyphenanthrene

2-PHE:

2-hydroxyphenanthrene

1-PYR:

1-hydroxypyrene

9-FLU:

9-hydroxyfluorene

FVC :

The forced vital capacity

FEV1 :

The 1st second of a forceful exhalation

FEF25%-75% :

The forced expiratory flow rate 25–75%

FENO:

The fractional exhaled nitric oxide

References

  • Best EA, Juarez-Colunga E, James K, LeBlanc WG, Serdar B (2016) Biomarkers of exposure to polycyclic aromatic hydrocarbons and cognitive function among elderly in the United States (National Health and Nutrition Examination Survey: 2001-2002). PLoS One 11:e0147632

    Article  Google Scholar 

  • Bhatt SP, Balte PP, Schwartz JE, Cassano PA, Couper D, Jacobs DR Jr, Kalhan R, O'Connor GT, Yende S, Sanders JL, Umans JG, Dransfield MT, Chaves PH, White WB, Oelsner EC (2019) Discriminative accuracy of FEV1:FVC thresholds for COPD-related hospitalization and mortality. Jama 321:2438–2447

    Article  Google Scholar 

  • Boada LD, Henríquez-Hernández LA, Navarro P, Zumbado M, Almeida-González M, Camacho M, Álvarez-León EE, Valencia-Santana JA, Luzardo OP (2015) Exposure to polycyclic aromatic hydrocarbons (PAHs) and bladder cancer: evaluation from a gene-environment perspective in a hospital-based case-control study in the Canary Islands (Spain). Int J Occup Environ Health 21:23–30

    Article  CAS  Google Scholar 

  • Bougard N, Nekoee H, Schleich F, Guissard F, Paulus V, Donneau AF, Louis R (2020) Assessment of diagnostic accuracy of lung function indices and FeNO for a positive methacholine challenge. Biochem Pharmacol 179:113981

    Article  CAS  Google Scholar 

  • Cao L, Zhou Y, Tan A, Shi T, Zhu C, Xiao L, Zhang Z, Yang S, Mu G, Wang X, Wang D, Ma J, Chen W (2020) Oxidative damage mediates the association between polycyclic aromatic hydrocarbon exposure and lung function. Environ Health : a global access science source 19:75

    Article  CAS  Google Scholar 

  • Centers for Disease Control and Prevention. (2020a) National Health and Nutrition Examination Survey. Spirometry. [accessed 2020-12-20]. https://wwwn.cdc.gov/Nchs/Nhanes/2009-2010/SPX_F.htm

  • Centers for Disease Control and Prevention. (2020b) National health and nutrition examination survey. Urine Polycyclic Aromatic Hydrocarbons. [accessed 2020-12-20]. https://wwwn.cdc.gov/nchs/nhanes/Search/DataPage.aspx?Component=Laboratory&CycleBeginYear=2013.

  • Centers for Disease Control and Prevention. (2020c) National Health and Nutrition Examination Survey. Weighting. [accessed 2020-12-20]. https://wwwn.cdc.gov/nchs/nhanes/tutorials/module3.aspx.

  • Chen L, Hu G, Fan R, Lv Y, Dai Y, Xu Z (2018) Association of PAHs and BTEX exposure with lung function and respiratory symptoms among a nonoccupational population near the coal chemical industry in Northern China. Environ Int 120:480–488

    Article  CAS  Google Scholar 

  • Chen Z, Cui L, Cui X, Li X, Yu K, Yue K, Dai Z, Zhou J, Jia G, Zhang J (2019) The association between high ambient air pollution exposure and respiratory health of young children: a cross sectional study in Jinan, China. Sci Total Environ 656:740–749

    Article  CAS  Google Scholar 

  • Cheng YJ, Chen ZG, Li ZY, Mei WY, Bi WT, Luo DL (2021) Longitudinal change in lung function and subsequent risks of cardiovascular events: evidence from four prospective cohort studies. BMC Med 19:153

    Article  CAS  Google Scholar 

  • Doiron D, de Hoogh K, Probst-Hensch N, Fortier I, Cai Y, De Matteis S, Hansell AL (2019): Air pollution, lung function and COPD: results from the population-based UK Biobank study. Eur Respir J 54

  • Fanucchi MV, Day KC, Clay CC, Plopper CG (2004) Increased vulnerability of neonatal rats and mice to 1-nitronaphthalene-induced pulmonary injury. Toxicol Appl Pharmacol 201:53–65

    Article  CAS  Google Scholar 

  • Fielding S, Pijnenburg M, de Jongste JC, Pike KC, Roberts G, Petsky H, Chang AB, Fritsch M, Frischer T, Szefler S, Gergen P, Vermeulen F, Vael R, Turner S (2019) Change in FEV(1) and FENO measurements as predictors of future asthma outcomes in children. Chest 155:331–341

    Article  Google Scholar 

  • Gibbs K, Collaco JM, McGrath-Morrow SA (2016) Impact of tobacco smoke and nicotine exposure on lung development. Chest 149:552–561

    Article  Google Scholar 

  • Grigg J (2020) Air pollution and suppression of lung function growth: a triumph for epidemiology. Am J Respir Crit Care Med 201:400–401

    Article  Google Scholar 

  • Guo H, Huang K, Zhang X, Zhang W, Guan L, Kuang D, Deng Q, Deng H, Zhang X, He M, Christiani D, Wu T (2014) Women are more susceptible than men to oxidative stress and chromosome damage caused by polycyclic aromatic hydrocarbons exposure. Environ Mol Mutagen 55:472–481

    Article  CAS  Google Scholar 

  • Habre R, Zhou H, Eckel SP, Enebish T, Fruin S, Bastain T, Rappaport E, Gilliland F (2018) Short-term effects of airport-associated ultrafine particle exposure on lung function and inflammation in adults with asthma. Environ Int 118:48–59

    Article  CAS  Google Scholar 

  • Hou J, Yin W, Li P, Hu C, Xu T, Cheng J, Li T, Wang L, Yu Z, Yuan J (2020) Joint effect of polycyclic aromatic hydrocarbons and phthalates exposure on telomere length and lung function. J Hazard Mater 386:121663

    Article  CAS  Google Scholar 

  • Kharitonov SA, Robbins RA, Yates D, Keatings V, Barnes PJ (1995) Acute and chronic effects of cigarette smoking on exhaled nitric oxide. Am J Respir Crit Care Med 152:609–612

    Article  CAS  Google Scholar 

  • Liu X, Wu J (2020) Update on clinical application of fractional exhaled nitric oxide. Int J Respir 40:1183–1189

    Google Scholar 

  • Lukic KZ, Coates AL (2015) Does the FEF25-75 or the FEF75 have any value in assessing lung disease in children with cystic fibrosis or asthma? Pediatr Pulmonol 50:863–868

    Article  Google Scholar 

  • Marie-Desvergne C, Maître A, Bouchard M, Ravanat JL, Viau C (2010) Evaluation of DNA adducts, DNA and RNA oxidative lesions, and 3-hydroxybenzo(a)pyrene as biomarkers of DNA damage in lung following intravenous injection of the parent compound in rats. Chem Res Toxicol 23:1207–1214

    Article  CAS  Google Scholar 

  • McSharry CP, McKay IC, Chaudhuri R, Livingston E, Fraser I, Thomson NC (2005) Short and long-term effects of cigarette smoking independently influence exhaled nitric oxide concentration in asthma. J Allergy Clin Immunol 116:88–93

    Article  CAS  Google Scholar 

  • Moorthy B, Chu C, Carlin DJ (2015) Polycyclic aromatic hydrocarbons: from metabolism to lung cancer. Toxicol Sci : an official journal of the Society of Toxicology 145:5–15

    Article  CAS  Google Scholar 

  • Mortamais M, Pujol J, van Drooge BL, Macià D, Martínez-Vilavella G, Reynes C, Sabatier R, Rivas I, Grimalt J, Forns J, Alvarez-Pedrerol M, Querol X, Sunyer J (2017) Effect of exposure to polycyclic aromatic hydrocarbons on basal ganglia and attention-deficit hyperactivity disorder symptoms in primary school children. Environ Int 105:12–19

    Article  CAS  Google Scholar 

  • Paranjape SM, Barnes LA, Carson KA, von Berg K, Loosen H, Mogayzel PJ Jr (2012) Exercise improves lung function and habitual activity in children with cystic fibrosis. J Cyst Fibros : official journal of the European Cystic Fibrosis Society 11:18–23

    Article  Google Scholar 

  • Plataki M, Koutsopoulos AV, Darivianaki K, Delides G, Siafakas NM, Bouros D (2005) Expression of apoptotic and antiapoptotic markers in epithelial cells in idiopathic pulmonary fibrosis. Chest 127:266–274

    Article  Google Scholar 

  • Riley CM, Wenzel SE, Castro M, Erzurum SC, Chung KF, Fitzpatrick AM, Gaston B, Israel E, Moore WC, Bleecker ER, Calhoun WJ, Jarjour NN, Busse WW, Peters SP, Teague WG, Sorkness R, Holguin F (2015) Clinical implications of having reduced mid forced expiratory flow rates (FEF25-75), independently of FEV1, in adult patients with asthma. PLoS One 10:e0145476

    Article  Google Scholar 

  • Schleich FN, Seidel L, Sele J, Manise M, Quaedvlieg V, Michils A, Louis R (2010) Exhaled nitric oxide thresholds associated with a sputum eosinophil count ≥3% in a cohort of unselected patients with asthma. Thorax 65:1039–1044

    Article  Google Scholar 

  • Siddens LK, Bunde KL, Harper TA Jr, McQuistan TJ, Löhr CV, Bramer LM, Waters KM, Tilton SC, Krueger SK, Williams DE, Baird WM (2015) Cytochrome P450 1b1 in polycyclic aromatic hydrocarbon (PAH)-induced skin carcinogenesis: tumorigenicity of individual PAHs and coal-tar extract, DNA adduction and expression of select genes in the Cyp1b1 knockout mouse. Toxicol Appl Pharmacol 287:149–160

    Article  CAS  Google Scholar 

  • Srogi K (2007) Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ Chem Lett 5:169–195

    Article  CAS  Google Scholar 

  • Su Z, Jiang Y, Li C, Zhong R, Wang R, Wen Y, Liang H, Chen Z, He J, Liang W (2021) Relationship between lung function and lung cancer risk: a pooled analysis of cohorts plus Mendelian randomization study. J Cancer Res Clin Oncol 147:2837–2849

    Article  Google Scholar 

  • Wang N, Li Q, Liu H, Lin L, Han W, Hao W (2019) Role of C/EBPα hypermethylation in diesel engine exhaust exposure-induced lung inflammation. Ecotoxicol Environ Saf 183:109500

    Article  CAS  Google Scholar 

  • Wang S, Bai Y, Deng Q, Chen Z, Dai J, Li X, Zhang W, Zhang X, He M, Wu T, Guo H (2016) Polycyclic aromatic hydrocarbons exposure and lung function decline among coke-oven workers: a four-year follow-up study. Environ Res 150:14–22

    Article  CAS  Google Scholar 

  • Yang K, Wu Y, Chen D, Liu S, Chen R (2020) The impact of lung function on extra-pulmonary diseases and all-cause mortality in US Adult Population with and without COPD. Clin Epidemiol 12:997–1005

    Article  Google Scholar 

  • Zhang L, Sun J, Zhang D (2021) The relationship between urine polycyclic aromatic hydrocarbons and depressive symptoms in American adults. J Affect Disord 292:227–233

    Article  CAS  Google Scholar 

  • Zhou Y, Sun H, Xie J, Song Y, Liu Y, Huang X, Zhou T, Rong Y, Wu T, Yuan J, Chen W (2016) Urinary polycyclic aromatic hydrocarbon metabolites and altered lung function in Wuhan, China. Am J Respir Crit Care Med 193:835–846

    Article  CAS  Google Scholar 

  • Zhou Y, Liu Y, Sun H, Ma J, Xiao L, Cao L, Li W, Wang B, Yuan J, Chen W (2018) Associations of urinary polycyclic aromatic hydrocarbon metabolites with fractional exhaled nitric oxide and exhaled carbon monoxide: a cross-sectional study. Sci Total Environ 618:542–550

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the National Center for Health Statistics of the Centers for Disease Control and Prevention for sharing the data.

Author information

Authors and Affiliations

Authors

Contributions

Liming Zhang: conceptualization, methodology, software, formal analysis, and writing—original draft. Jing Sun: software and formal analysis. Dongfeng Zhang: writing (review and editing), supervision, and project administration. All authors provided critical revisions of the manuscript and approved the final manuscript.

Corresponding author

Correspondence to Dongfeng Zhang.

Ethics declarations

Ethics approval and consent to participate

The protocol was approved by the NCHS Research Ethics Review Board (ERB) (Protocol Number: Protocol #2005-06; Protocol #2011-17). All adult participants provide written notice of consent.

Consent for publication

Not applicable

Competing interests

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.

Supplementary information

ESM 1

(DOC 691 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, L., Sun, J. & Zhang, D. Associations and dose-response relationships between different kinds of urine polycyclic aromatic hydrocarbons metabolites and adult lung functions. Environ Sci Pollut Res 29, 8639–8649 (2022). https://doi.org/10.1007/s11356-021-16294-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-16294-z

Keywords

Navigation