Polybrominated diphenyl ethers and decabromodiphenyl ethane in paired hair/serum and nail/serum from corresponding chemical manufacturing workers and their correlations to thyroid hormones, liver and kidney injury markers
Graphical abstract
Introduction
Brominated flame retardants (BFRs) are a class of chemical additives that are normally blended into various products, such as building and ornamental materials, electronic components, and assorted rubber or fiber products, to delay or terminate burning. Polybrominated diphenyl ethers (PBDEs) used to be the most commonly used BFRs throughout the world because of their excellent performance. Commercial PBDEs are divided into three categories: penta-BDE, octa-BDE and deca-BDE. The first two categories have been listed as persistent organic pollutants (POPs) under the Stockholm Convention since 2009 by virtue of their potential threats to the environment and human health (http://chm.pops.int/TheConvention/ThePOPs). According to the announcement issued by the Ministry of Ecology and Environment of China, the production, import, export and use of penta- and octa-BDE have been completely banned nationwide since 2014 (http://www.mee.gov.cn). However, the production and use of deca-BDE are still permitted in China at present, even though this compound has also been listed as a POP under the 2017 Stockholm Convention (http://chm.pops.int/TheConvention/ThePOPs). Deca-BDE (primarily BDE-209) has been found to be ubiquitous in both environmental media such as the atmosphere, soil and natural water (Chao et al., 2014; Li et al., 2016; Song et al., 2004) and biological matrices such as breast milk, blood, urine and the placenta (Chen et al., 2014; Dassanayake et al., 2009; Shi et al., 2017a, Shi et al., 2017b). The health effects of deca-BDE are also a matter of great concern. Recent studies have indicated that BDE-209 interferes with glycolipid metabolism and thyroid function, and it causes damage to the liver and reproductive system (Liang et al., 2019; Sarkar et al., 2019; Sun et al., 2020; Wang et al., 2019b; Zhu et al., 2019).
On pace with the prohibition of legacy BFRs such as PBDEs, a series of novel BFRs considered to have superior flame retardancy and lower toxicity have come onto the market. Decabromodiphenyl ethane (DBDPE) is a commonly used novel BFR that was introduced to the Chinese market in 2005. DBDPE has a similar bromine content and thermal stability as those of BDE-209. More importantly, there is no ether bond in the DBDPE molecule, and thus no highly toxic compounds, such as polybrominated dibenzo-p-dioxins/furans (PBDD/Fs), will be produced during combustion (Liu et al., 2016b). For this reason, DBDPE is regarded as the best substitute for BDE-209, and is has taken over the market rapidly. However, the environmental and human health risks of DBDPE have also generated great concern, even if it is considered as a quality alternative to BDE-209 with lower toxicity (Cristale et al., 2019; Li et al., 2019). Previous studies showed that DBDPE has become the most abundant novel BFR in both food and human milk in China, with its huge and soaring production and use (Chen et al., 2019a; Shi et al., 2018). In addition, although toxicology research has shown that DBDPE might be less toxic than BDE-209, its potential health effects, such as its cardiovascular toxicity, hepatotoxicity and endocrine disrupting effects, should not be neglected yet (Jing et al., 2019; Sun et al., 2020; Wang et al., 2019b).
To date, internal and external exposures to BFRs in the general population have been assessed in quite a few studies, whereas studies involving “occupational populations” such as e-waste recyclers, are much less common (Eguchi et al., 2015; Sjodin et al., 2019), and exposure assessments of BFR manufacturing workers is rather scarce. According to our previous research, deca-BDE and DBDPE manufacturing workers are facing much higher BFR exposure than ordinary residents or e-waste recyclers, which has resulted in the disruption of their serum thyroid hormones (Chen et al., 2018; Chen et al., 2019b; Wang et al., 2019a).
In prior studies, population-based studies on exposure levels to environmental pollutants normally focused on determining the concentrations of specific pollutants in whole blood, serum or plasma. Only a small number of studies have explored the possibility of using hair and nails to assess internal exposure of PBDEs, DBDPE and other POPs in human beings (Alves et al., 2014; Chen et al., 2019c; Liang et al., 2016; Liu et al., 2016a). Studies on hair and nails have many advantages. First, using hair and nails is noninvasive, with easy collection and easy storage of the biomatrices. Second, their collection is more friendly to vulnerable groups (i.e., pregnant and parturient women, new-born infants, senior citizens, and the chronically ill) than blood drawing. Third, hair and nail measurements can better reflect long-term exposures to environmental pollutants due to their slow growth rate (Liang et al., 2016; Liu et al., 2015; Qiao et al., 2018; Zheng et al., 2011). In the present study, population-based research was conducted on two BFRs, deca-BDE and DBDPE, in manufacturing plants. The levels of PBDEs or DBDPE were measured in paired human hair-serum samples and nail-serum samples that were collected from the corresponding BFR manufacturing workers. Correlations between the levels of specific contaminants in hair/nail and serum samples were analyzed to determine the possibility of using hair and nails as noninvasive biomatrices to assess the occupational exposure levels to deca-BDE or DBDPE of BFR manufacturing workers. Moreover, the influencing factors (the work place, body mass index (BMI), length of service, use of personal protective equipment, etc.) on the deca-BDE or DBDPE contamination levels in the hair and nail samples were also evaluated. Additionally, correlations between the BDE-209 or DBDPE contents of the hair and nail samples and the levels of a series of clinical biochemical markers related to thyroid hormones and liver and kidney injuries in serum were explored to find if the BFR levels in hair and nails can also be used to assess the health effects of BFRs on occupational workers.
Section snippets
Study site and sampling
Sample collection was launched at two separate BFR manufacturing plants located in Shandong Province, North China, which produced deca-BDE and DBDPE. The production line of both the deca-BDE and DBDPE plants could be roughly divided into two parts, a pretreatment workshop and a posttreatment workshop. In the pretreatment workshop, production procedures including bromination, distillation and washing were performed, and the drying and packaging of BFRs were performed in the posttreatment
PBDEs in paired hair-serum samples
As shown in Table 1, the detecting frequencies (DFs) of BDE-209 reached 100% in both serum and hair. The median levels of BDE-209 in the serum and hair samples were 3.89 μg/g lipid weight (lw) (geomean: 4.78 μg/g lw) and 75.0 μg/g dry weight (dw) (geomean: 101 μg/g dw), respectively. The BFR levels in hair samples from different populations around the world in recent years are listed in Table 2. Clearly, a comparison to other studies showed that the BDE-209 level in hair samples from deca-BDE
Conclusion
In this study, the levels of PBDEs or DBDPE in the paired hair-serum and nail-serum samples collected from the corresponding BFR manufacturing plants were determined. The specific BFR levels in the serum, hair and nail samples collected from the corresponding BFR manufacturing workers were much higher than those in other populations, suggesting that the workers were heavily and continuously exposed to BFRs without proper protection, and specific protection measures should be taken to reduce the
CRediT authorship contribution statement
Xuezhen Zhao: Formal analysis, Data curation, Writing - original draft. Tian Chen: Formal analysis, Data curation, Writing - original draft. Dejun Wang: Investigation. Yinglin Du: Investigation, Formal analysis. Yan Wang: Investigation, Formal analysis. Wenwen Zhu: Formal analysis. Melikedilnur Bekir: Methodology, Validation. Dong Yu: Formal analysis, Data curation. Zhixiong Shi: Methodology, Writing - review & editing.
Declaration of competing interest
The authors declared that there is no conflict of interest.
Acknowledgements
The authors thank all the workers for their kindly donation. This study was supported by the National Natural Science Foundation of China (21777107, 21477083, 81703198, 21537001, 31770441), the National Key R&D Program of China (2017YFC1600500), the Joint funding of Beijing Natural Science Foundation and Beijing Education Commission (KZ201910025037), and Shandong Medical and Health Science and Technology Development Program (No. 2013WS0159).
References (62)
- et al.
Long-term exposure assessment to phthalates: how do nail analyses compare to commonly used measurements in urine
J. Chromatogr. B
(2016) - et al.
Serum levels of brominated flame retardants (BFRs: PBDE, HBCD) and influence of dietary factors in a population-based study on Swedish adults
Chemosphere
(2017) - et al.
Estimating uptake of phthalate ester metabolites into the human nail plate using pharmacokinetic modelling
Environ. Int.
(2017) - et al.
Atmospheric concentrations of persistent organic pollutants over the Pacific Ocean near southern Taiwan and the northern Philippines
Sci. Total Environ.
(2014) - et al.
Polybrominated diphenyl ethers (PBDEs) in human samples of mother-newborn pairs in South China and their placental transfer characteristics
Environ. Int.
(2014) - et al.
Disruption of thyroid hormone levels by decabrominated diphenyl ethers (BDE-209) in occupational workers from a deca-BDE manufacturing plant
Environ. Int.
(2018) - et al.
Polybrominated diphenyl ethers and novel brominated flame retardants in human milk from the general population in Beijing, China: occurrence, temporal trends, nursing infants’ exposure and risk assessment
Sci. Total Environ.
(2019) - et al.
Thyroid function and decabromodiphenyl ethane (DBDPE) exposure in Chinese adults from a DBDPE manufacturing area
Environ. Int.
(2019) - et al.
Novel and legacy flame retardants in paired human fingernails and indoor dust samples
Environ. Int.
(2019) - et al.
Occurrence of flame retardants in landfills: a case study in Brazil
Environ. Res.
(2019)
Serum measures of hexabromocyclododecane (HBCDD) and polybrominated diphenyl ethers (PBDEs) in reproductive-aged women in the United Kingdom
Environ. Res.
Different profiles of anthropogenic and naturally produced organohalogen compounds in serum from residents living near a coastal area and e-waste recycling workers in India
Environ. Int.
Residue profiles of organohalogen compounds in human serum from e-waste recycling sites in North Vietnam: association with thyroid hormone levels
Environ. Res.
Simulating long-term occupational exposure to decabrominated diphenyl ether using C57BL/6 mice: biodistribution and pathology
Chemosphere
Dermal uptake and percutaneous penetration of ten flame retardants in a human skin ex vivo model
Chemosphere
Cardiovascular toxicity of decabrominated diphenyl ethers (BDE-209) and decabromodiphenyl ethane (DBDPE) in rats
Chemosphere
Occurrence of dechlorane compounds and polybrominated diphenyl ethers (PBDEs) in the Korean general population
Environ. Pollut.
Occurrence and levels of polybrominated diphenyl ethers (PBDEs) in house dust and hair samples from Northern Poland; an assessment of human exposure
Chemosphere
Brominated flame retardants in the surrounding soil of two manufacturing plants in China: occurrence, composition profiles and spatial distribution
Environ. Pollut.
Halogenated flame retardants in the sediments of the Chinese Yellow Sea and East China Sea
Chemosphere
Establishment of a human embryonic stem cell-based liver differentiation model for hepatotoxicity evaluations
Ecotoxicol. Environ. Saf.
Analysis of polybrominated diphenyl ethers and emerging halogenated and organophosphate flame retardants in human hair and nails
J. Chromatogr. A
Lab-scale thermal analysis of electronic waste plastics
J. Hazard. Mater.
Elevated concentrations of polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans and polybrominated diphenyl ethers in hair from workers at an electronic waste recycling facility in eastern China
J. Hazard. Mater.
Accumulation of brominated flame retardants and polychlorinated biphenyls in human breast milk and scalp hair from the Philippines: levels, distribution and profiles
Sci. Total Environ.
Brominated flame retardant (BFRs) and dechlorane plus (DP) in paired human serum and segmented hair
Ecotoxicol. Environ. Saf.
Exposure to polybrominated diphenyl ethers among workers at an electronic waste dismantling region in Guangdong, China
Environ. Int.
Maternal BDE-209 exposure during lactation causes testicular and epididymal toxicity through increased oxidative stress in peripubertal mice offspring
Toxicol. Lett.
Dietary exposure assessment of Chinese population to tetrabromobisphenol-A, hexabromocyclododecane and decabrominated diphenyl ether: results of the 5th Chinese Total Diet Study
Environ. Pollut.
A national survey of tetrabromobisphenol-A, hexabromocyclododecane and decabrominated diphenyl ether in human milk from China: occurrence and exposure assessment
Sci. Total Environ.
Legacy and emerging brominated flame retardants in China: a review on food and human milk contamination, human dietary exposure and risk assessment
Chemosphere
Cited by (28)
A meta-analysis highlighting the increasing relevance of the hair matrix in exposure assessment to organic pollutants
2024, Science of the Total EnvironmentHuman hair as a noninvasive matrix to assess exposure to micro-organic contaminants: State of the art review
2023, Science of the Total Environment
- 1
Xuezhen Zhao and Tian Chen contributed equally to this study.