Abstract
Exposure to polycyclic aromatic hydrocarbons (PAHs) has been associated with many adverse health outcomes. However, the evidence on such associations with the liver function was not reviewed systemically. Therefore in this study, we systemically reviewed the observational studies on exposure to PAHs and liver function. The MOOSE guidelines were applied to perform this review. We systematically searched Scopus, PubMed, and Web of Science for all relevant articles published in English until 10 September 2022. The quality of retrieved studies was evaluated based on the Gascon et al. method. We retrieved a total of 3927 citations through the initial search, of which an overall of five articles (n = 6994 participants) was included in our final review. The quality assessment indicated that three studies had excellent, one had good, and one had fair quality. Three reviewed studies reported a significant negative association between exposure to PAHs and liver function. One study reported a significant correlation between urinary metabolites of PAHs with serum g-glutamyltransferase (GGT), two studies reported that there was an increase in the risk of hepatocellular carcinoma (HCC) related exposure to PAH-albumin adducts as well as benzo[a]pyrene (BPDE)-DNA adducts in the blood, and two studies indicated that higher levels of urinary metabolites of PAHs were associated with higher risk of abnormal levels of alanine transaminase (ALT), aspartate transaminase (AST) and GGT enzymes. Overall, our review indicated that exposure to PAHs has an adverse impact on human liver function.
Similar content being viewed by others
Data availability
This is a review and all data is publicly available.
References
Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25:107–123
Alazawi W, Mathur R, Abeysekera K, Hull S, Boomla K, Robson J, Foster GR (2014) Ethnicity and the diagnosis gap in liver disease: a population-based study. Br J Gen Pract 64:e694-702
Astell-Burt T, Maynard MJ, Lenguerrand E, Whitrow MJ, Molaodi OR, Harding S (2013) Effect of air pollution and racism on ethnic differences in respiratory health among adolescents living in an urban environment. Health Place 23:171–178
Autrup H, Daneshvar B, Dragsted LO, Gamborg M, Hansen M, Loft S, Okkels H, Nielsen F, Nielsen PS, Raffn E, Wallin H, Knudsen LE (1999) Biomarkers for exposure to ambient air pollution–comparison of carcinogen-DNA adduct levels with other exposure markers and markers for oxidative stress. Environ Health Perspect 107:233–238
Bauer AK, Velmurugan K, Plöttner S, Siegrist KJ, Romo D, Welge P, Brüning T, Xiong K-N, Käfferlein HU (2018) Environmentally prevalent polycyclic aromatic hydrocarbons can elicit co-carcinogenic properties in an in vitro murine lung epithelial cell model. Arch Toxicol 92:1311–1322
Bortey-Sam N, Ikenaka Y, Akoto O, Nakayama SMM, Asante KA, Baidoo E, Obirikorang C, Saengtienchai A, Isoda N, Nimako C, Mizukawa H, Ishizuka M (2017) Oxidative stress and respiratory symptoms due to human exposure to polycyclic aromatic hydrocarbons (PAHs) in Kumasi, Ghana. Environ Pollut 228:311–320
de Keijzer C, Gascon M, Nieuwenhuijsen MJ, Dadvand P (2016) Long-term green space exposure and cognition across the life course: a systematic review. Curr Environ Health Rep 3:468–477
Dobaradaran S, Schmidt TC, Lorenzo-Parodi N, Jochmann MA, Nabipour I, Raeisi A, Stojanović N, Mahmoodi M (2019) Cigarette butts: an overlooked source of PAHs in the environment? Environ Pollut 249:932–939
Ferguson KK, McElrath TF, Pace GG, Weller D, Zeng L, Pennathur S, Cantonwine DE, Meeker JD (2017) Urinary polycyclic aromatic hydrocarbon metabolite associations with biomarkers of inflammation, angiogenesis, and oxidative stress in pregnant women. Environ Sci Technol 51:4652–4660
Gallegos-Gonzalez G, Pineda-García G, Serrano-Medina A, Martinez AL, Ochoa-Ruiz E (2021) Association between stress and metabolic syndrome and its mediating factors in university students. Am J Health Behav 45:1091–1102
Gascon M, Triguero-Mas M, Martínez D, Dadvand P, Rojas-Rueda D, Plasència A, Nieuwenhuijsen MJ (2016) Residential green spaces and mortality: a systematic review. Environ Int 86:60–67
Genuis SJ, Lane K, Birkholz D (2016) Human elimination of organochlorine pesticides: blood, urine, and sweat study. Biomed Res Int 2016:1624643
Giannini EG, Testa R, Savarino V (2005) Liver enzyme alteration: a guide for clinicians. CMAJ 172:367–379
Godschalk R, Nair J, van Schooten FJ, Risch A, Drings P, Kayser K, Dienemann H, Bartsch H (2002) Comparison of multiple DNA adduct types in tumor adjacent human lung tissue: effect of cigarette smoking. Carcinogenesis 23:2081–2086
Godschalk RW, Van Schooten FJ, Bartsch H (2003) A critical evaluation of DNA adducts as biological markers for human exposure to polycyclic aromatic compounds. J Biochem Mol Biol 36:1–11
Han F, Guo H, Hu J, Zhang J, Ying Q, Zhang H (2020) Sources and health risks of ambient polycyclic aromatic hydrocarbons in China. Sci Total Environ 698:134229
Harini P, Anitha R, Raghunandhakumar S, Elumalai P, Lakshmi T (2021) Cancer Activity of Cassia Oleoresin Against Liver Cancer Cell Lines. J Complement Med Res 12:24–29
Honda M, Suzuki N (2020) Toxicities of polycyclic aromatic hydrocarbons for aquatic animals. Int J Environ Res Public Health 17
Hu Z, Li Y, Yang Y, Yu W, Xie W, Song G, Qian Y, Song Z (2021) Serum lipids mediate the relationship of multiple polyaromatic hydrocarbons on non-alcoholic fatty liver disease: a population-based study. Sci Total Environ 780:146563
IARC (2010) Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum 92:853
Johnson NM, Qian G, Xu L, Tietze D, Marroquin-Cardona A, Robinson A, Rodriguez M, Kaufman L, Cunningham K, Wittmer J, Guerra F, Donnelly KC, Williams JH, Wang JS, Phillips TD (2010) Aflatoxin and PAH exposure biomarkers in a U.S. population with a high incidence of hepatocellular carcinoma. Sci Total Environ 408:6027–6031
KamilJabbar D (2022) Biochemical evaluation of antioxidant enzyme activities and lipid peroxidation level associated with liver enzymes in patients with fascioliasis. Arch Razi Inst 77:1067–1073
Kim JY, Lee SK, Kim CH, Jeon TW, Moon CK, Lee HS, Yoo SD, Lee ES, Jeong TC (2003) Effects of polycyclic aromatic hydrocarbons on liver and lung cytochrome P450s in mice. Arch Pharm Res 26:394–404
Koyama Y, Brenner DA (2017) Liver inflammation and fibrosis. J Clin Invest 127:55–64
Lachowycz K, Jones AP (2011) Greenspace and obesity: a systematic review of the evidence. Obes Rev 12:e183–e189
Lawal AT (2017) Polycyclic aromatic hydrocarbons. a review. Cogent Environ Sci 3:1339841
Lazo M, Selvin E, Clark JM (2008) Brief communication: clinical implications of short-term variability in liver function test results. Ann Intern Med 148:348–352
Lee DH, Jacobs DR (2009) Is serum gamma-glutamyltransferase an exposure marker of xenobiotics? Empirical evidence with polycylic aromatic hydrocarbon. Clin Chem Lab Med 47:860–862
Leman MA, Claramita M, Rahayu GR (2021) Predicting factors on modeling health behavior: a systematic review. Am J Health Behav 45:268–278
Mahmood RA, Abdullah RM (2022) The effect of active compounds and trace elements extracted from Artemisia fruit on some liver enzymes in humans. Arch Razi Inst.
Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E (2020) Environmental and health impacts of air pollution: a review. Front Public Health 8:14
Marris CR, Kompella SN, Miller MR, Incardona JP, Brette F, Hancox JC, Sørhus E, Shiels HA (2020) Polyaromatic hydrocarbons in pollution: a heart-breaking matter. J Physiol 598:227–247
Masarone M, Rosato V, Dallio M, Gravina AG, Aglitti A, Loguercio C, Federico A, Persico M (2018) Role of oxidative stress in pathophysiology of nonalcoholic fatty liver disease. Oxid Med Cell Longev 2018:9547613
Masoudi N, Dahmardeh Ghaleno N, Esfandiari M (2020) Investigating the impacts of technological innovation and renewable energy on environmental pollution in countries selected by the International Renewable Energy Agency: a quantile regression approach. Caspian J Environ Sci 18:97–107
Masuda M, Wang Q, Tokumura M, Miyake Y, Amagai T (2019) Simultaneous determination of polycyclic aromatic hydrocarbons and their chlorinated derivatives in grilled foods. Ecotoxicol Environ Saf 178:188–194
Min YS, Lim HS, Kim H (2015) Biomarkers for polycyclic aromatic hydrocarbons and serum liver enzymes. Am J Ind Med 58:764–772
Miri M, Alahabadi A, Ehrampoush MH, Ghaffari HR, Sakhvidi MJZ, Eskandari M, Rad A, Lotfi MH, Sheikhha MH (2018) Environmental determinants of polycyclic aromatic hydrocarbons exposure at home, at kindergartens and during a commute. Environ Int 118:266–273
Miri M, Nazarzadeh M, Alahabadi A, Ehrampoush MH, Rad A, Lotfi MH, Sheikhha MH, Sakhvidi MJZ, Nawrot TS, Dadvand P (2019) Air pollution and telomere length in adults: a systematic review and meta-analysis of observational studies. Environ Pollut 244:636–647
Mousa N, Gado M, Osman A (2020) Multimodality of human epidermal growth factor receptor-2 antagonism restores the apoptotic capacity of liver cancer cells. J Nat Sci Biol Med 11:118–118
Muqdamal AH, Abdulhameed A, Ali Mansour A (2022) Total testosterone to estradiol ratio as a predictor marker of metabolic syndrome in males. Arch Razi Inst 77:351–357
Nadali A, Leili M, Bahrami A, Karami M, Afkhami A (2021) Phase distribution and risk assessment of PAHs in ambient air of Hamadan, Iran. Ecotoxicol Environ Saf 209:111807
Neerati P, Palle S (2019) Resveratrol nanoparticle pretreatment improved the oral bioavailability of bromocriptine: involvement of liver and intestinal CYP3A enzyme inhibition. J Nat Sci Biol Med 10:209–216
Nguyen HT (2022) Effect of nutrition intervention on the prevalence of metabolic syndrome at Kon Tum General Hospital, Vietnam. J Complement Med Res 13:24–24
Nori Mater H, ManafAbd Al-Rhman R, Ibraheem SR, Shaker Mahmood M (2022) Effects of avena sativa and glycyrrhiza glabra leaves extracts on immune responses in serum cytokine and liver enzyme levels in NIH Mice. Arch Razi Inst 77:1845–1851
O’Driscoll CA, Gallo ME, Hoffmann EJ, Fechner JH, Schauer JJ, Bradfield CA, Mezrich JD (2018) Polycyclic aromatic hydrocarbons (PAHs) present in ambient urban dust drive proinflammatory T cell and dendritic cell responses via the aryl hydrocarbon receptor (AHR) in vitro. PLoS One 13:e0209690
Patel AB, Shaikh S, Jain KR, Desai C, Madamwar D (2020) Polycyclic aromatic hydrocarbons: sources, toxicity, and remediation approaches. Front Microbiol 11:562813
Pejhan A, Agah J, Adli A, Mehrabadi S, Raoufinia R, Mokamel A, Abroudi M, Ghalenovi M, Sadeghi Z, Bolghanabadi Z, Bazghandi MS, Hamidnia M, Salimi F, Pajohanfar NS, Dadvand P, Rad A, Miri M (2019) Exposure to air pollution during pregnancy and newborn liver function. Chemosphere 226:447–453
Phillips TD, Richardson M, Cheng Y-SL, He L, McDonald TJ, Cizmas LH, Safe SH, Donnelly KC, Wang F, Moorthy B, Zhou G-D (2015) Mechanistic relationships between hepatic genotoxicity and carcinogenicity in male B6C3F1 mice treated with polycyclic aromatic hydrocarbon mixtures. Arch Toxicol 89:967–977
Pirhadi M, Shariatifar N, Bahmani M, Manouchehri A (2022) Heavy metals in wheat grain and its impact on human health: a mini-review. J Chem Health Risks 12:421–426
Robinson MW, Harmon C, O’Farrelly C (2016) Liver immunology and its role in inflammation and homeostasis. Cell Mol Immunol 13:267–276
Ruíz-Vera T, Pruneda-Alvarez LG, Pérez-Vázquez FJ, Ochoa-Martínez AC, Orta-García ST, Ilizaliturri-Hernández CA, Pérez-Maldonado IN (2015) Using urinary 1-hydroxypyrene concentrations to evaluate polycyclic aromatic hydrocarbon exposure in women using biomass combustion as main energy source. Drug Chem Toxicol 38:349–354
Sakshi, Haritash AK (2020) A comprehensive review of metabolic and genomic aspects of PAH-degradation. Arch Microbiol 202:2033–2058
Shnewer Mahdi Al-Turfi Z, Al-Hadrawy S, Abadi Mohammed J, ChasibJabal B (2022) Evaluation of the effect of alcoholic extract of laurus nobilis leaves on blood biochemical parameters and histological changes in the liver and kidney among female wistar rats treated with depakene (sodium valproate). Arch Razi Inst 77:981–989
Slotkin TA, Skavicus S, Card J, Giulio RTD, Seidler FJ (2017) In vitro models reveal differences in the developmental neurotoxicity of an environmental polycylic aromatic hydrocarbon mixture compared to benzo[a]pyrene: neuronotypic PC12 Cells and embryonic neural stem cells. Toxicology 377:49–56
Stroup D, Berlin J, Morton S, Olkin I, Williamson G (2000) MOOSE guidelines for meta-analyses and systematic reviews of observational studies. JAMA 283:2008–2012
Su Y, Zhao B, Guo F, Bin Z, Yang Y, Liu S, Han Y, Niu J, Ke X, Wang N, Geng X, Jin C, Dai Y, Lin Y (2014) Interaction of benzo[a]pyrene with other risk factors in hepatocellular carcinoma: a case-control study in Xiamen, China. Ann Epidemiol 24:98–103
Trefts E, Gannon M, Wasserman DH (2017) The liver. Curr Biol 27:R1147-r1151
Tretyakova V, Zhernakova N, Arisheva O, Garmash I, Tretyakov A, Gerasimov N, Ermilov O (2022) Meta-analysis of non-alcoholic fatty liver disease and electromechanical reconstruction of myocardium. Arch Razi Inst 77:123–128
Ualiyeva RM, Zhangazin SB, Altayeva IB (2022) Structural organization of vitelline cells of trematode with undifferentiated body of Azygia lucii (Muller, 1776). OnLine J Biol Sci 22.
Wang T, Song X, Xu H, Zhu Y, Li L, Sun X, Chen J, Liu B, Zhao Q, Zhang Y, Yuan N, Liu L, Fang J, Xie Y, Liu S, Wu R, He B, Cao J, Huang W (2022) Combustion-derived particulate PAHs associated with small airway dysfunction in elderly patients with COPD. Environ Sci Technol 56:10868–10878
Wu HC, Wang Q, Wang LW, Yang HI, Ahsan H, Tsai WY, Wang LY, Chen SY, Chen CJ, Santella RM (2007) Polycyclic aromatic hydrocarbon- and aflatoxin-albumin adducts, hepatitis B virus infection and hepatocellular carcinoma in Taiwan. Cancer Lett 252:104–114
Xu C, Liu Q, Liang J, Weng Z, Xu J, Jiang Z, Gu A (2021) Urinary biomarkers of polycyclic aromatic hydrocarbons and their associations with liver function in adolescents. Environ Pollut 278:116842
Yang H, Shi Z, Wang XX, Cheng R, Lu M, Zhu J, Deng W, Zeng Y, Zhao LY, Zhang SY (2019) Phenanthrene, but not its isomer anthracene, effectively activates both human and mouse nuclear receptor constitutive androstane receptor (CAR) and induces hepatotoxicity in mice. Toxicol Appl Pharmacol 378:114618
Yao Y, Wang D, Ma H, Li C, Chang X, Low P, Hammond SK, Turyk ME, Wang J, Liu S (2019) The impact on T-regulatory cell related immune responses in rural women exposed to polycyclic aromatic hydrocarbons (PAHs) in household air pollution in Gansu, China: a pilot investigation. Environ Res 173:306–317
Zhu J, Zhao LY, Wang XX, Shi Z, Zhang Y, Wu G, Zhang SY (2018) Identification of hepatotoxicity and renal dysfunction of pyrene in adult male rats. Environ Toxicol 33:1304–1311
Acknowledgements
The authors would like to thank the Deanship of Scientific Research (DSR) at King Khalid University for the guidance and technical support.
Author information
Authors and Affiliations
Contributions
All of the authors contributed to the design of the study. E., Sh.H.A, A.Z., Gh.R.L.A, S.K.Sh, completed the literature review and drafted the manuscript. A.A.R., conceived of the project and edited the manuscript. N.Sh., Y.R., Z.A., R.S.Z, Y.F.M, M.L.R revised the manuscript and recheck the reviewed papers. The paper was revised and approved by all the authors.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
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
Efriza, E., Alshahrani, S.H., Zekiy, A.O. et al. Exposure to polycyclic aromatic hydrocarbons and liver function: a systematic review of observational studies. Air Qual Atmos Health 16, 1079–1088 (2023). https://doi.org/10.1007/s11869-023-01324-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11869-023-01324-1