Urinary monohydroxylated polycyclic aromatic hydrocarbons in primiparas from Shenzhen, South China: Levels, risk factors, and oxidative stress☆
Graphical abstract
Introduction
Polycyclic aromatic hydrocarbons (PAHs) are produced by the incomplete combustion and pyrolysis of organic material (Chen et al., 2019a; Wang et al., 2012). Due to the carcinogenicity, endocrine disrupting, reproductive and developmental toxicity of PAHs, scientists and governments have acknowledged the health risks of exposure to PAHs (Kim et al., 2013; Zhang et al., 2017). Humans are exposed to PAHs mainly via air, food, and skin (Kamal et al., 2015; Lao et al., 2018; Sun et al., 2015; Yu et al., 2012). In the human body, PAHs undergo hydroxylation reactions and transfer into monohydroxylated, dihydroxylated, and tetrahydroxylated metabolites (Carmella et al., 2004; Klotz et al., 2011). These are then excreted in the urine mainly as forms of sulfate conjugates and glucuronides (Li et al., 2006). To assess human exposure to PAHs, urinary OH-PAHs (monohydroxylated metabolites of PAHs) have been widely used as biomarkers (Bortey-Sam et al., 2017; Wang et al., 2019).
Generally, the ambient atmosphere is considered one of the most important sources of PAHs, and human external exposure to PAHs via inhalation is assessed. However, internal exposure estimated by PAH metabolites in urine is more accurate than ambient detection and external exposure because it reflects an internal dose from contamination by all external exposure pathways, such as inhalation via air, ingestion through the diet, and dermal contact and absorption by skin (Lao et al., 2018; Ma and Harrad, 2015). As environmental toxicants, PAHs can lead to many adverse effects in humans. Several studies have shown that PAHs can combine with DNA and formed DNA adducts, which are potential biomarkers for estimating the degree of malignancy in cancer (Bach et al., 2003; Ewa and Danuta, 2016). 8-Hydroxyl-2′-deoxyguanosine (8-OHdG) is generally used as a biomarker to assess the harm from oxidative DNA in humans (Guo et al., 2014; Kuusimäki et al., 2004; Yang et al., 2015). As reported in the literature, human exposure to polluted air can lead to an excess of reactive oxygen species, which consequently attack the carbon atoms in the DNA molecule, leading to the production of 8-OHdG. There are many studies on the relationship between PAH exposure and 8-OHdG in occupational groups, including populations living close to e-waste recycling facilities (Kuang et al., 2013; Lu et al., 2016). However, investigations on general populations are limited, especially for primiparas.
It is known that developing fetuses are more susceptible to PAHs due to their immature physiology, weak detoxification of toxic compounds, and low metabolization (Archibong et al., 2002; Lamichhane et al., 2016; Makri et al., 2004). Many studies have demonstrated that fetuses are more sensitive to PAH-induced DNA damage than their mothers (Perera et al., 2005; Wu et al., 2010). Additionally, some studies have demonstrated that exposure to PAHs during pregnancy increases the risk of poor childbirth (Hoffman et al., 2018; Jedrychowski et al., 2017). For example, intrauterine developmental delay and reduced birth length and weight were observed because of the PAH exposure of mothers during pregnancy (Choi et al., 2006; Mu et al., 2015). Thus, an investigation of the exposure of primiparas to PAHs is very important for understanding both the maternal exposure to the pollutants and to assess potential fetal health.
Shenzhen is a national economic center and an important industrial city in China. In addition, it is the center of the Guangdong-Hong Kong-Macao Greater Bay Area linking Guangzhou, Shenzhen, with another 11 cities, as well as Macao and Hong Kong. The Greater Bay Area is an important region as its development has been a feature of one of the national strategies of China. To our knowledge, no studies have investigated the exposure of the general population to PAHs in this region. More information about the general population levels of exposure to PAHs and source apportionment in this region is needed, especially for primiparas. Therefore, the main objectives of this study were: (1) to measure the urinary concentrations of seven OH-PAHs in primiparas from Shenzhen, China; (2) to evaluate the influence factors including age, body mass index (BMI), cooking, and smoking on urinary OH-PAHs; (3) to investigate the associations of OH-PAHs with 8-OHdG in urine; and (4) to evaluate the health risks of primiparas exposed to PAHs.
Section snippets
Chemicals and materials
OH-PAH isomers, including 2-hydroxynathalene (2-OHN), 1-hydroxynathalene (1-OHN), 1-hydroxyphenanthrene (1-OHPhe), 2-hydroxyfluorene (2-OHF), 3-hydroxyphenanthrene (3-OHPhe), 2-hydroxyphenanthrene (2-OHPhe), and 1-hydroxypyrene (1-OHP), were bought from Dr. Ehrenstorfer (Augsburg, Germany). 8-OHdG was obtained from Sigma-Aldrich (St. Louis, MO, USA). The internal standards including D8-2-OHN, 13C6-3-OHPhe, 13C6-1-OHP, D9-2-OHF, and 15N5-8-OHdG, were purchased from Cambridge Isotope Laboratories
Levels of urinary OH-PAHs
The OH-PAH concentrations and detection frequencies in the urine of primiparas are shown in Table 1. 2-OHF, 2-OHPhe, 1-OHN, 2-OHN, and 2+3-OHPhe were detectable in almost all urine samples with detection frequencies higher than 95%, while 1-OHPhe and 1-OHP were detectable only in some samples (82% and 66%, respectively). The high urinary OH-PAH detection frequencies indicated the extensive presence of PAHs in the environment and the wide exposure of local residents to PAHs in the regions. The
Levels of urinary OH-PAHs
Urinary concentrations of Σ7OH-PAHs in primiparas in the present study were in line with those in a USA general population in 2013–2014 (6.13 ng/mL) and Hanoi (6.84 ng/mL) (Table S3) (CDC, 2015; Thai et al., 2015), but much higher than those in Malaysia (2.26 ng/mL) and Germany (3.22 ng/mL) (Guo et al., 2013; Myers et al., 2008). However, compared with those residents from areas surrounding e-waste dismantling sites in Qingyuan (20 ng/mL), Vietnam (8.56 ng/mL), and Korea (9.34 ng/mL), and coke
Conclusion
The levels of OH-PAHs in primiparas from Shenzhen were measured and the association with 8-OHdG was analyzed. The high detection frequencies of OH-PAHs indicated the ubiquitous occurrence of human exposure to PAHs. The urinary OH-PAH concentration in Shenzhen primiparas fell to a moderate level, compared with other countries and areas. There was no significant correlation between the metabolites and other factors, such as age, weight, and lifestyle. However, a statistically significant
CRediT authorship contribution statement
Mengmeng Peng: Formal analysis, Writing - original draft. Shaoyou Lu: Supervision. Yingxin Yu: Methodology. Shan Liu: Formal analysis. Yang Zhao: Formal analysis. Chun Li: Formal analysis. Shengtao Ma: Writing - review & editing.
Declaration of competing interest
Compliance with ethical standards.
The authors declare no conflict of interest.
Acknowledgements
This research was financially supported by the National Natural Science Foundation of China (No. 21677094), the 100 Top Talents Program of Sun Yat-sen University, Shenzhen Municipal Government Research Projects (No. JCYJ20160428143348745), and Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (2017BT01Z032). We also thank Shenzhen Center for Disease Control and Prevention for these urine sample collection.
References (56)
- et al.
Alteration of pregnancy related hormones and fetal survival in F-344 rats exposed by inhalation to benzo(a)pyrene
Reprod. Toxicol.
(2002) - et al.
Screening for lung cancer: a review of the current literature
Chest
(2003) - et al.
Oxidative stress and respiratory symptoms due to human exposure to polycyclic aromatic hydrocarbons (PAHs) in Kumasi, Ghana
Environ. Pollut.
(2017) - et al.
Urinary profiles to assess polycyclic aromatic hydrocarbons exposure in coke-oven workers
Toxicol. Lett.
(2010) - et al.
Seasonal profiles of atmospheric PAHs in an e-waste dismantling area and their associated health risk considering bioaccessible PAHs in the human lung
Sci. Total Environ.
(2019) - et al.
Organophosphate ester and phthalate ester metabolites in urine from primiparas in Shenzhen, China: implications for health risks
Environ. Pollut.
(2019) - et al.
Human exposure to parent and halogenated polycyclic aromatic hydrocarbons via food consumption in Shenzhen, China
Sci. Total Environ.
(2013) - et al.
Urinary 1-hydroxypyrene (1-OHP) in environmental and occupational studies-A review
Int. J. Hyg Environ. Health
(2008) - et al.
Human biomonitoring of phthalate exposure in Austrian children and adults and cumulative risk assessment
Int. J. Hyg Environ. Health
(2015) - et al.
Prenatal exposure to organophosphates and associations with birth weight and gestational length
Environ. Int.
(2018)
Community level exposure to chemicals and oxidative stress in adult population
Toxicol. Lett.
Characteristics and potential health risk of rural Tibetans’ exposure to polycyclic aromatic hydrocarbons during summer period
Environ. Int.
PAH exposure biomarkers are associated with clinico-chemical changes in the brick kiln workers in Pakistan
Sci. Total Environ.
A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects
Environ. Int.
1,2-Dihydroxynaphthalene as biomarker for a naphthalene exposure in humans
Int. J. Hyg Environ. Health
Co-exposure to polycyclic aromatic hydrocarbons, benzene and toluene and their dose-effects on oxidative stress damage in kindergarten-aged children in Guangzhou, China
Sci. Total Environ.
Associations between polycyclic aromatic hydrocarbon (PAH) exposure and oxidative stress in people living near e-waste recycling facilities in China
Environ. Int.
Spatiotemporal analysis and human exposure assessment on polycyclic aromatic hydrocarbons in indoor air, settled house dust, and diet: a review
Environ. Int.
Association of polycyclic aromatic hydrocarbons with cardiometabolic risk factors and obesity in children
Environ. Int.
Cumulative health risk assessment of halogenated and parent polycyclic aromatic hydrocarbons associated with particulate matters in urban air
Ecotoxicol. Environ. Saf.
Biomonitoring of polycyclic aromatic hydrocarbons exposure in small groups of residents in Brisbane, Australia and Hanoi, Vietnam, and those travelling between the two cities
Chemosphere
Polycyclic aromatic hydrocarbons and organochlorine pesticides in fish from Taihu Lake: their levels, sources and biomagnification
Ecotoxicol. Environ. Saf.
Urinary concentrations of monohydroxylated polycyclic aromatic hydrocarbons in adults from the US population assessment of tobacco and health (PATH) study wave 1 (2013–2014)
Environ. Int.
Exposure to polycyclic aromatic hydrocarbons and missed abortion in early pregnancy in a Chinese population
Sci. Total Environ.
Transplacental transfer of polycyclic aromatic hydrocarbons in paired samples of maternal serum, umbilical cord serum, and placenta in Shanghai, China
Environ. Pollut.
Biomarker approach to measuring human dietary exposure to certain phthalate diesters
Food. Addit. Contam.
Initial Risk Assessment of Polycyclic Aromatic Hydrocarbons (PAHs) in Feed (Materials)
Analysis of phenanthrols in human urine by gas chromatography-mass spectrometry: potential use in carcinogen metabolite phenotyping
Cancer Epidemiol. Biomark. Prev.
Cited by (27)
Metabolomics perspectives into the co-exposure effect of polycyclic aromatic hydrocarbons and metals on renal function: A meet-in-the-middle approach
2024, Science of the Total EnvironmentAssociation of co-exposure to polycyclic aromatic hydrocarbons and phthalates with oxidative stress and inflammation
2024, Science of the Total Environment
- ☆
This paper has been recommended for acceptance by Jun Huang.