Distribution and mass loads of xenoestrogens bisphenol A, 4-nonylphenol, and 4-tert-octylphenol in rainfall runoff from highly urbanized regions: A comparison with point sources of wastewater

Abstract

This study pays a special attention to three phenolic endocrine disrupting compounds (EDCs), — bisphenol A (BPA), 4-nonylphenol (4-NP), and 4-tert-octylphenol (4-t-OP) — that are present in urban environments, resultant of several anthropogenic activities that can be also carried through rainfall runoff. We investigated the distributions of BPA, 4-NP, and 4-t-OP in Pearl River basin and estimated the mass loads in rainfall runoff, wastewater treatment plant (WWTP) effluents, and industrial wastewater from urbanized Huizhou and Dongguan regions. These three phenolic EDCs were detected frequently in tributaries and mainstream of Dongjiang River with the maximum 4-NP concentrations of 14540 ng/L in surface waters and 3088 ng/g in sediments. BPA showed high concentrations in rainfall runoff samples with maximum concentrations of 5873 and 2397 ng/L in Huizhou and Dongguan regions, respectively, while concentrations for 4-NP and 4-t-OP were detected at tens to hundreds of nanograms per liter. Mass loads of phenolic EDCs from rainfall runoff were 3‒62 times higher than those of WWTP effluents, suggesting rainfall runoff is an important source of phenolic EDCs into receiving waters. Sources and tributaries showed median to high estrogenic risks, while low to median risks were found in mainstream, implying the source control should be focused.

Full text

Journal of Hazardous Materials 401 (2021) 123747
Available online 22 August 2020
0304-3894/© 2020 Elsevier B.V. All rights reserved.
Distribution and mass loads of xenoestrogens bisphenol a, 4-nonylphenol,
and 4-tert-octylphenol in rainfall runoff from highly urbanized regions: A
comparison with point sources of wastewater
Jian-Liang Zhao
a
,
b
,
*, Zheng Huang
a
,
b
, Qian-Qian Zhang
a
,
b
, Liang Ying-He
a
,
b
,
Tuan-Tuan Wang
c
, Yuan-Yuan Yang
a
,
b
, Guang-Guo Ying
a
,
b
a
SCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Theoretical
Chemistry of Environment, South China Normal University, Guangzhou 510006, China
b
School of Environment, South China Normal University, Guangzhou 510006, China
c
State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China
ARTICLE INFO
Editor: R Sara
Keywords:
Phenolic chemicals
Pearl River basin
Rainfall runoff
Mass loads
Endocrine disputing risks
ABSTRACT
This study pays a special attention to three phenolic endocrine disrupting compounds (EDCs), — bisphenol A
(BPA), 4-nonylphenol (4-NP), and 4-tert-octylphenol (4-t-OP) — that are present in urban environments, resul-
tant of several anthropogenic activities that can be also carried through rainfall runoff. We investigated the
distributions of BPA, 4-NP, and 4-t-OP in Pearl River basin and estimated the mass loads in rainfall runoff,
wastewater treatment plant (WWTP) efuents, and industrial wastewater from urbanized Huizhou and Dong-
guan regions. These three phenolic EDCs were detected frequently in tributaries and mainstream of Dongjiang
River with the maximum 4-NP concentrations of 14,540 ng/L in surface waters and 3088 ng/g in sediments. BPA
showed high concentrations in rainfall runoff samples with maximum concentrations of 5873 and 2397 ng/L in
Huizhou and Dongguan regions, respectively, while concentrations for 4-NP and 4-t-OP were detected at tens to
hundreds of nanograms per liter. Mass loads of phenolic EDCs from rainfall runoff were 3–62 times higher than
those of WWTP efuents, suggesting rainfall runoff is an important source of phenolic EDCs into receiving
waters. Sources and tributaries showed median to high estrogenic risks, while low to median risks were found in
mainstream, implying the source control should be focused.
1. Introduction
Over the past few decades, endocrine disrupting chemicals (EDCs)
have attracted increasing concerns from researchers and the public
because of their potential hormonal related effects, which might cause
endocrine disorders in wildlife and humans. Among these chemicals, the
phenolic EDCs, e.g., bisphenol A (BPA), 4-nonylphenol (4-NP), and 4-
tert-octylphenol (4-t-OP), represent common xenoestrogens that are
regularly used in various products. Approximately 95 % of the BPA
volume is used to produce polycarbonate and epoxy resins, while the
remaining 5% is used as additive agents (plasticizers, antioxidants,
rubber anti-aging agents, etc.) in a variety of products (Huang et al.,
2012). The global volumetric consumption of BPA was estimated at 7.7
million metric tons in 2015, and this amount is expected to reach 10.6
million metric tons by 2022 (Industry Expert, 2016). In China, the BPA
shares are approximately 12.5 % of the global volume, and its con-
sumption rate has increased by more than 13 %/y (Lu et al., 2013).
Alkylphenols (APs) including 4-NP and 4-t-OP are the main degradation
products of alkylphenol ethoxylates (APEOs), which are widely used in
industrial, agricultural, and household applications as detergents,
emulsiers, wetting agents, dispersants, or solubilizers (Ying et al.,
2002). The global volume consumption of APEOs exceeded 400 thou-
sand metric tons prior to 2007, of which China consumed approximately
50 thousand metric tons (Li et al., 2007).
Because of the widespread use of phenolic EDCs in various industrial
and domestic applications, industrial wastewater and municipal
wastewater treatment plant (WWTP) efuents are important point
sources for phenolic EDCs in receiving rivers. Although industrial
wastewater and domestic sewage are generally treated before discharge,
phenolic EDCs are still detected regularly in efuents and receiving
* Corresponding author at: SCNU Environmental Research Institute, South China Normal University, 378 Waihuanxi Road, Panyu, Guangzhou 510006, China.
E-mail address: jianliang.zhao@m.scnu.edu.cn (J.-L. Zhao).
Contents lists available at ScienceDirect
Journal of Hazardous Materials
journal homepage: www.elsevier.com/locate/jhazmat
https://doi.org/10.1016/j.jhazmat.2020.123747
Received 28 March 2020; Received in revised form 12 August 2020; Accepted 15 August 2020

Journal of Hazardous Materials 401 (2021) 123747
2
waters because of their incomplete removal in most treatment facilities
(H¨
ohne and Püttmann, 2008). For example, 4-NP was detected (260
ng/L) in textile wastewater from Belgium and Italy (Loos et al., 2007;
Berardi et al., 2019); furthermore, BPA can be found at concentrations
over 1900 ng/L in efuents from paper mills (Balabaniˇ
c et al., 2017) and
ne chemical factories (Fang et al., 2012). In municipal WWTPs of
Germany and Greece, concentrations were found to have reached to tens
of micrograms per liter for BPA and thousands of nanograms per liter for
4-t-OP (H¨
ohne and Püttmann, 2008; Pothitou and Voutsa, 2008; Care-
ghini et al., 2015). Beginning in 2005, the European Union (EU) has
legislated restrictions on the sale and use of products that contain more
than 0.1 % of 4-nonylphenol ethoxylates or 4-NP (EC, 2003). At present,
this is the only relevant legislation related to the use of this chemical,
although the U.S. Environmental Protection Agency is proposing a rule
for signicant new uses of NP and nonylphenol ethoxylates (USEPA,
2014). In conjunction with earlier legislation, the EU has issued a leg-
islative act for priority substances in water including 4-NP that stipulates
a maximum allowable concentration of 2.0
μ
g/L in surface water (EC,
2013). Regulations for BPA also have been enacted in different countries
in terms of the production and usage in various products such as textiles,
infant feeding bottles, food containers, and cosmetics (CFDA, 2015;
Usman and Ahmad, 2016). However, these partial usage limitations
seem to have not resulted in widespread reductions in environmental
exposures to phenolic EDCs. BPA, 4-NP, and 4-t-OP still can be regularly
detected in various waterbodies (Peng et al., 2008; Li et al., 2019), and
further, bioaccumulation of such chemicals is occurring in wild sh
around the world (Lee et al., 2015; Diao et al., 2017; Lv et al., 2019).
Rainfall runoff from cities and land is probably a signicant non-
point source for phenolic EDCs in the environment. For example, BPA
is a raw material for phenolic resin synthesis, and phenolic resin insu-
lation board has been widely installed in exterior walls of buildings in
cities, especially in large public buildings. Alkylphenol ethoxylates have
been used as detergents for the cleaning of private automobiles, building
walls, glassware, and so forth. Hence, during rain events, the runoff
probably contains BPA and alkylphenols, and this runoff may represent
an obvious mass input for receiving rivers. So far, data on the occurrence
and fate of phenolic EDCs in rainfall runoff are very limited (Maduka
Ignatius et al., 2010; Wilkinson et al., 2016; Fairbairn et al., 2018).
Wilkinson et al. (2016) reported BPA concentrations of 511 and 2410
ng/L at two sites receiving street runoff prior to entering rivers. Other
studies have reported that the concentrations of BPA and 4-NP in road
runoff were 552 and 359 ng/L, respectively, which were correlated with
high levels of local production (Gasperi et al., 2014) and trafc-related
sources (Lamprea et al., 2018). In general, the discharge of such runoff
probably poses risks for receiving waters.
The Pearl River system is the main source of potable water for resi-
dents in the Pearl River Delta area, and this is a developed region with a
high density of industrial activity and high urbanization rates, as well as
a large population size. Hence, the rainfall runoff could be a potentially
important input source for phenolic EDCs in the environment compared
with point sources such as, WWTPs and industrial wastewater. The ob-
jectives of this study were as follows: (1) to evaluate the levels and
distribution of phenolic EDCs in surface waters, sediments, rainfall
runoff, and WWTP and industrial efuents in the Pearl River region; (2)
to estimate the mass loads from different sources, especially from rain-
fall runoff; and (3) to assess the potential estrogenic risks contributed by
phenolic EDCs. The present study will help us to understand the
importance and risks of rainfall runoff as a potential discharge source for
phenolic EDCs in receiving surface waters.
2. Materials and methods
2.1. Materials
Standards of BPA and 4-t-OP were both obtained from Supelco
(Bellefonte, PA, USA). The 4-NP standard (technical mixture) was
obtained from Dr. Ehrenstorfer GmbH (Augsburg, Germany). The purity
was above 95 % for all of the compounds. The isotope-labeled internal
standard BPA-d16 for BPA was purchased from Supelco, and 4-n-NP
used as the internal standard for 4-NP and 4-t-OP were obtained from Dr.
Ehrenstorfer GmbH. Their basic physicochemical properties are listed in
Table S1 (Supplementary material). Individual and stock solutions for
standards and internal standards were prepared with methanol in amber
glass bottles and stored at −18 ◦C in a freezer for later use. All of the
solvents and reagents used for extraction and analytical measurements
were of HPLC grade. Methanol and acetonitrile were purchased from
Merck (Darmstadt, Germany). Dichloromethane, ethyl acetate, and n-
hexane were obtained from CNW Technologies (Germany).
2.2. Sample collection
Highly urbanized regions, namely, the cities of Huizhou and Dong-
guan, in the middle and lower reaches of the Dongjiang River basin were
selected in this study. These regions are located in the eastern part of the
Pearl River Delta Economic Zone, South China. The Dongjiang River is
the second tributary of the Pearl River system, with a drainage area of
32,275 km
2
, and it is the main source of potable water for nearly 40
million people in the cities of Huizhou, Heyuan, Guangzhou, Dongguan,
Shenzhen, and Hong Kong (Chen et al., 2014).
The sampling sites for the Dongjiang River, rainfall runoff, and
WWTP efuents are shown in Fig. 1. For water and sediments of the
Dongjiang River, sampling campaigns were carried out in March (dry
season) and July 2015 (wet season). There were 13 sampling sites, with
4 sites located in the mainstream of the Dongjiang River (DJ-1, DJ-4, DJ-
8, and DJ-13) and 9 sites situated in the tributaries. The basic infor-
mation (e.g., geographical location, ow rate, site characteristics) for
each site is presented in Table S2. The surface water samples (0–10 cm)
were collected from the middle and both sides of a river section at each
site, and samples were mixed to a nal volume of 1 L with three repli-
cates. Surface sediments (about 0–5 cm) were collected with a stainless
steel sampler from two positions of the section, which were located
10–20 m off the river bank.
For rainfall runoff, samples were collected from the cities of Huizhou
and Dongguan during the period of June to December in 2015. Col-
lecting weirs were setup in the designed drainage ditches for courtyards,
streets, and farmland to collect the converged water before each rainfall
event. During each rain event, the runoff (rst ush) samples (1 L each,
three replicates) were collected. In Huizhou, there was one courtyard
site at a middle school (HZ-A), two street sites in commercial districts
(HZ-B and HZ-C), and one farmland site in a paddy eld (HZ-D).
Meanwhile in Dongguan, there was one courtyard site at a government
building (DG-A), one street site in a commercial district (DG-B), and one
farmland site in a vegetable plantation (DG-C). The basic information (e.
g., geographical location, sampling time, and sampling date) for the
sampling sites is presented in Table S3.
For municipal WWTP efuents, the water samples were collected
during the period of September and October of 2015. Two sites in
Huizhou (WWTP-A and WWTP-B) and two sites in Dongguan (WWTP-C
and WWTP-D) were selected. The basic information for WWTPs is listed
in Table S4. For industrial wastewater, efuents from industrial waste-
water treatment facilities were collected with the representative indus-
trial types consisting of dyeing, electroplating, and papermaking
efuents. Each industrial type was derived from six plants located in the
Dongguan or Huizhou regions. The detailed information for industrial
wastewater is listed in Table S5. Time-integrated composite efuents
(three replicates for each) from the WWTPs and industrial factories were
collected in 1 L amber glass bottles on two consecutive days.
After sampling, all of the water samples for surface water, runoff, and
efuents stored in 1 L amber glass bottle were immediately adjusted to
pH 3 by using 4 M H
2
SO
4
. Methanol (5% v/v) was added to inhibit
microbial activity. Then, the samples were transported to the laboratory
in coolers. River sediment samples were stored in 200 mL glass bottles
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
3
and preserved by the addition of 0.4 g sodium azide to inhibit microbial
activity. Upon arrival at the laboratory, the water samples were stored at
4 ◦C in a cold room and then used within 48 h. The sediment samples
were rst stored at −20 ◦C, and then, samples were freeze-dried within a
week, passed through a 60-mesh standard sieve, and stored at −18 ◦C in
the dark until extraction. Meanwhile, the basic quality parameters of the
surface water and sediment samples of the Dongjiang River basin were
determined. The results for the water quality parameters are shown in
Fig. S1, while the results for the sediment quality parameters are given
in Table S6.
2.3. Sample extraction and instrumental analysis
The three target phenolic EDCs in surface water, rainfall runoff,
wastewater, suspended particulate matter (SPM), and sediment samples
were extracted according to our previous methods with a few modi-
cations (Zhao et al., 2011).
Briey, water samples (1 L each) were ltered through glass ber
lters (Whatman GF/F, 0.7
μ
m). Particles loaded on glass ber lters
were separately stored as SPM samples. The water phase was then mixed
with 100
μ
L of the internal standard mixture (1 mg/L of 4-n-NP and BPA-
d16). Then, the samples were extracted with the solid phase extraction
(SPE) method by using HLB cartridges (500 mg, 6 mL), which were
consecutively preconditioned by using 10 mL methanol and 10 mL Milli-
Q water. The ltered water samples were passed through the pre-
conditioned SPE cartridges at an approximate speed of 5–10 mL/min.
Then, the cartridges were dried for 1 h under vacuum. The target
compounds in each cartridge were eluted by using 7 mL methanol and 5
mL dichloromethane, and the extracts were nally reconstituted in 1 mL
methanol and stored at −18 ◦C prior to the instrumental analysis.
The homogenized sediment samples (5.0 g each) were weighed
accurately into a 30 mL centrifuge tube and spiked with 100
μ
L of the
internal standard mixture (1 mg/L each). Then, the samples were
manually mixed and stored at 4 ◦C overnight. On the second day, these
samples were individually extracted by using 10 mL of ethyl acetate and
vortex mixing and ultrasonicating the samples. Then, the tubes were
centrifuged and the supernatant was transferred into stock tubes. The
extraction step was repeated twice, and the combined extracts were
Fig. 1. Sketch map showing the sampling area and sites in the Dongjiang River basin.
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
4
dried. Then, the extracts were puried by passing the material through a
silica gel column followed by elution with 6 mL of n-hexane, 6 mL of
ethyl acetate, and 6 mL of methanol in sequence. The ethyl acetate phase
was collected and dried and reconstituted in 1 mL of methanol; these
samples were stored at −18 ◦C prior to instrumental analysis.
The SPMs loaded on the lter membranes were freeze-dried. Then,
the lter membranes were cut into small pieces by using stainless scis-
sors. These small pieces were transferred into 30 mL centrifuge tubes
and spiked with 100
μ
L internal standard (1 mg/L each) for each sample.
Then, the SPMs were extracted by the same procedure as that used for
the sediment samples.
Target phenolic EDCs in the nal extracts were analyzed by an
ultrahigh-performance liquid chromatograph (Agilent 1200, USA)
coupled to a triple quadrupole mass spectrometer (Agilent 6460, USA)
with electrospray ionization under negative ionization modes (UPLC-
ESI-MS/MS). The chromatographic separation was performed on an
Agilent SB-C18 column (3.0 ×100 mm, 1.8
μ
m) with an in-line lter kit
(4.6 mm, 0.2
μ
m lter) (Germany). The column temperature was
maintained at 40 ◦C. The detailed operating parameters can be found in
our previous study (Chen et al., 2011) and are also described in Text S1.
Strict quality assurance and quality control (QA/QC) procedures
were performed. The QA/QC procedures are described in Text S2. In
water samples, the range of limit of detection (LOD), limit of quanti-
cation (LOQ), and average recoveries (spiking at 100 ng/L) were 0.3–2.0
ng/L, 1.0–7.0 ng/L, and 82–112 %, respectively. In SPM samples, the
range of LOD, LOQ, and average recoveries (spiking at 100 ng/L) were
0.1‒0.2 ng/L, 0.3‒0.6 ng/L, and 88–108 %, respectively. In sediment
samples, the range of LOD, LOQ, and average recoveries (spiking at 20
ng/g) were 0.5–1.3 ng/g, 1.6–4.3 ng/g, and 89–103 %, respectively. The
relative standard deviations for all of the matrices were below 15 %. The
range of concentrations used for the quantication of the three com-
pounds in the extracted sample vials was 0.1–20,000
μ
g/L. The detailed
relative recoveries, LOD, and LOQ for each target compound in water,
SPM, and sediment are listed in Table S7.
2.4. Calculation of annual mass loads from different sources
The estimated mass loads of phenolic EDCs per year from rainfall
runoff and efuents of WWTPs and industrial wastewater treatment
facilities were calculated by the following equations:
Mrunoff =k1×Crunoff ×A×P×10−6
Meffluents =Ceffluent ×Q
109
where M
runoff
(kg/y) is the estimated annual emissions of phenolic EDCs
in each city; k
1
represents the average runoff coefcients, with values of
0.543 used for the middle reach of the Pearl River (Huizhou) and 0.587
used for the lower reach of the Pearl River (Dongguan) (He et al., 2014);
C
runoff
(ng/L) is the mean concentration of phenolic EDCs in all of the
rainfall runoff samples from Huizhou or Dongguan; A (km
2
) is the area
of Huizhou or Dongguan; P (mm/y) is the annual precipitation in
Huizhou or Dongguan in 2015; M
efuents
(kg/y) is the estimated annual
emissions of phenolic EDCs in each city; C
efuent
(ng/L) is the average
concentrations of phenolic EDCs in WWTP efuents in Huizhou or
Dongguan; and Q (m
3
/y) represents the average total daily water ow
for each type of efuent. The values of A, P, and Q are listed in
Tables S3‒S4.
2.5. Estrogenic risk assessment
The total 17β-estradiol (E
2
) equivalents (EEQ) contributed by the
three phenolic EDCs in the water phase of each site were calculated
according to the following equation:
∑EEQ =∑(Ci×EEFi)
where C
i
refers to the concentration of each compound in the water
samples; and EEF
i
(estradiol equivalent factor) represents the ratio of the
median effective concentration (EC
50
) of E
2
and the EC
50
of the com-
pound. The EEF values for the phenolic EDCs were obtained from the
literature (Nakada et al., 2004) as shown in Table S1.
The potential estrogenic risk of the water from each site in the Pearl
River system was assessed based on the risk quotient (RQ), which was
computed as the ratio of the ΣEEQ value of each site to the predicted no-
effect concentration (PNEC) of E
2
. A PNEC for E
2
of 1.5 ng/L in the water
phase was applied (Zhao et al., 2011). The levels of risk were classied
as high risk (RQ ≥1), median risk (0.1 ≤RQ <1), and low risk (RQ <
0.1).
2.6. Data analysis
Because of the small dry weight of the SPM content loaded on glass
lters, the concentrations of phenolic EDCs in SPM were expressed as the
equivalent volume of the water phase; hence, the unit of concentration
in the SPM is expressed as ng/L. Differences in the concentrations from
various sites were examined with nonparametric Kruskal–Wallis tests
(K–W test). A p value of <0.05 was considered to be statistically sig-
nicant, and a p value of <0.01 was deemed highly signicant.
Descriptive statistics were computed with Microsoft Excel software, and
distribution gures were constructed with Sigma Plot software.
3. Results
3.1. Occurrences of phenolic EDCs in the riverine environment
Because of the low concentrations of phenolic EDCs in most of the
river SPM samples, the concentration value of each sample with regard
to each replicate was added to its corresponding surface water sample
and data were then displayed as a whole surface water concentration.
The occurrences and distribution characteristics of the three phenolic
EDCs in surface water (including SPM) and sediments of the river system
are shown in Fig. 2. The detailed concentrations of the three phenolic
EDCs in surface water, SPM, and sediments at each sampling site and in
each season, as well as the summarized concentration proles (range,
mean, median, and detection frequency), are listed in Table S8.
In surface water (including SPM), the three phenolic EDCs were
detected with detection frequencies of 100 %, which indicates that these
compounds were ubiquitous in the riverine environment. The maximum
concentrations of BPA, 4-NP, and 4-t-OP were 1889, 14,540, and 758
ng/L, respectively, while 4-NP showed the highest level in both wet and
dry seasons (Table S8). The spatial distributions of the three compounds
displayed obvious differences along the sampling sites (p <0.05)
(Fig. 1). Concentrations at the sites (DJ-1, DJ-4, DJ-8, and DJ-13)
located in the mainstream were generally lower than those at the
adjacent tributary sites. For example, the 4-NP concentration was
ranked in the following order: DJ-2 (Danshui River) >DJ-3 (Xizhijiang
River) >DJ-4 (Dongjiang River in the Huizhou section) (p <0.05) in
both dry and wet seasons. For BPA, sites DJ-11 and DJ-12 showed higher
concentrations than the other sites, while for 4-NP and 4-t-OP, sites DJ-
10 and DG-11 showed higher concentrations than the other sites,
especially during the dry season. These ndings revealed that the
phenolic EDCs from the tributaries were a signicant input source to the
mainstream. Meanwhile, seasonal variations were also found at some
sites. For example, the concentrations of BPA at site DJ-11 during the
wet season were 4 times higher than those in the dry season (p <
0.0001).
In sediments, the detection frequencies for BPA and 4-NP were both
100 % in the two sampling campaigns, while the detection frequencies
for 4-t-OP were only 8% in the dry season and 51 % in the wet season.
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
5
The maximum concentrations of BPA, 4-NP, and 4-t-OP ranged up to
757, 3088, and 76.1 ng/g, respectively. Similar to surface water, 4-NP
was present at higher concentrations than BPA and 4-t-OP when
comparing the mean and median values both in dry and wet seasons
(Table S8). The spatial distributions of the three compounds displayed
obvious differences along the sampling sites (p <0.05). Sites DG-2, DJ-
10, and DJ-11 showed higher concentrations of the three compounds
than the other sites.
3.2. Occurrences of phenolic EDCs in the rainfall runoff
During half of the year in the rainy season, all of the three phenolic
EDCs were detected in the rainfall runoff from the cities of Huizhou and
Dongguan in the Pearl River Delta region. The proles of BPA, 4-NP, and
4-t-OP in the water phase and SPM of rainfall runoff in the Huizhou and
Dongguan regions are shown in Fig. 3. The detailed concentration data
for BPA, 4-NP, and 4-t-OP in the water phase and SPM of rainfall runoff
are listed in Table S9.
During all rain events, the detection frequencies of BPA, 4-NP, and 4-
t-OP were almost 100 % in the water and SPM of runoff samples from
both the Huizhou and Dongguan regions. Except for the detection fre-
quency of 4-t-OP, the value was 53 % for the water phase (Table S9). For
the total concentrations of water and SPM, BPA was present at higher
maximum and mean concentrations than 4-NP and 4-t-OP in both the
Huizhou and Dongguan regions. The maximum (mean) values of total
concentrations for BPA were 5873 (968) and 2397 (629) ng/L in the
Huizhou and Dongguan regions, respectively. The maximum (mean)
values of total concentrations for 4-NP and 4-t-OP were only at the tens
to hundreds of nanograms per liter level in both the Huizhou and
Dongguan regions. Runoff samples were collected during the ush of
surfaces at specic locations during rain events, and thus, high contents
of particulate matter were usually found in the runoff samples, espe-
cially for the road samples. As shown in Fig. 3, the concentration per-
centages of 4-NP and 4-t-OP in the SPM phase were approximately 50 %
and 75 % of the total concentrations at most sites during rain events,
respectively, while the percentage of BPA was less than 10 % at most
sites. These data suggest that BPA was primarily distributed in the water
phase, while alkylphenols were distributed in both the SPM and water
Fig. 2. Distribution of phenolic endocrine disrupting chemicals in surface water together with suspended particulate matter (A) and sediments (B) collected from the
Dongjiang River. DW: dry weight.
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
6
phases.
Concentrations of BPA, 4-NP, and 4-t-OP in runoff from courtyards,
streets, and farmland of Huizhou and Dongguan regions are also shown
in Fig. 3. In both the Huizhou and Dongguan regions, the total con-
centrations (water +SPM) of BPA and 4-t-OP in street runoff samples
were generally higher than those in courtyard and farmland samples.
For example, the mean concentrations of BPA in road runoff were
5.2–8.8 (p <0.01) times higher than those in courtyard runoff and
5.0–87 (p <0.01) times higher than those in farmland runoff in the two
regions; the mean concentrations of 4-t-OP in road runoff were 1.9–4.2
(p <0.05) times higher than those in courtyard runoff and 4.2–83 (p <
0.01) times higher than those in farmland runoff. However, for 4-NP, the
mean values for the runoff types had the following order: farmland >
roads >courtyards; the mean concentrations showed no statistical dif-
ferences between the different runoff types (p >0.05).
Sampling also showed timely variations in the total concentrations
for target compounds at the same sites during half of the year (Fig. 3). At
courtyard sites (site A in Huizhou and Dongguan), the concentration of
BPA slightly increased from the wet season to dry season, but the
opposite trend was observed for 4-NP. For BPA, the highest concentra-
tion (A1) was 2.08 times higher than the lowest concentration (A5) in
Huizhou and 5.10 times variation was found in courtyard samples in
Dongguan. At roadway sites (site B and C in Huizhou, and site B in
Dongguan), the highest concentration of BPA was 6.41–44.9 and 3.77
times the lowest concentrations in Huizhou and Dongguan, respectively.
Similar trends were also found for 4-NP and 4-t-OP.
3.3. Occurrences of phenolic EDCs in the WWTP and industrial efuents
The concentrations proles of phenolic EDCs in the four WWTP ef-
uents, six dyeing wastewater samples, six electroplating wastewater
samples, and six papermaking wastewater samples are illustrated in
Fig. 4, and the detailed concentration data (mean ±standard deviation)
are listed in Table S10.
It can be seen that all of the three phenolic EDCs in the samples were
detected at detection frequencies of 100 % in all of the WWTP efuents
and dyeing, electroplating, and papermaking wastewaters. In WWTP
efuents, the mean concentrations were at hundreds of nanograms per
liter for BPA, thousands of nanograms per liter for 4-NP, and several
nanograms per liter for 4-t-OP (Table S10). In industrial wastewater, the
concentrations of the three phenolic EDCs varied largely among the
wastewater types and plants (Fig. 4). The maximum concentration of
BPA was 9074 ng/L in papermaking wastewater, while the maximum
concentrations of 4-NP and 4-t-OP were 125,400 and 1694 ng/L,
respectively, in dyeing wastewater. In general, the concentrations for
BPA in different wastewater types followed the order of papermaking >
dyeing ~ electroplating, while the concentrations for 4-NP and 4-t-OP in
different wastewater types followed the order of dyeing >papermaking
Fig. 3. Distribution of phenolic endocrine disrupting chemicals in rainfall runoff in the Huizhou (A) and Dongguan (B) regions.
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
7
~ electroplating.
3.4. Mass loads of phenolic EDCs from different sources
The estimated mass loads of the three phenolic EDCs in the rainfall
runoff and different point sources in the Huizhou and Dongguan regions
in 2015 are listed in Table 1. The annual mass loads of BPA, 4-NP, and 4-
t-OP in the rainfall runoff were 5222, 1024, and 123 kg/y, respectively,
together in the Huizhou and Dongguan regions. Meanwhile, the annual
mass loads of BPA, 4-NP, and 4-t-OP in the efuents of municipal
WWTPs were 83.9, 304, and 0.49 kg/y, respectively, together in the
Huizhou and Dongguan regions. It can be seen that the mass loads of 4-
NP in rainfall runoff were 3.4 times higher than those of WWTP efu-
ents, while the mass loads of BPA and 4-t-OP in rainfall runoff were far
more than 10 times higher than those of WWTP efuents. Hence, the
ndings indicated that the input of phenolic EDCs from rainfall runoff to
the riverine environment of the Dongjiang River basin was not a negli-
gible factor.
The annual mass loads of BPA, 4-NP, and 4-t-OP in industrial
wastewater treatment facilities varied largely from 7.07 kg/y (4-t-OP in
electroplating wastewater) to 3857 kg/y (4-NP in dyeing wastewater).
For BPA, the mass load in papermaking wastewater was 8–9 times
higher than that in dyeing and electroplating wastewater. For 4-NP and
4-t-OP, the mass loads in dyeing wastewater were 2–9 times higher than
those in electroplating and papermaking wastewater. The mass loads of
the three phenolic EDCs also showed large differences between the
Huizhou and Dongguan regions. For example, the mass load of BPA in
papermaking wastewater in the Dongguan region (384 kg/y) was 16
times higher than that in the Huizhou region (24.2 kg/y). Additionally,
the mass load of 4-NP in dyeing wastewater in the Dongguan region
(2970 kg/y) was 3.3 times higher than that in the Huizhou region (887
kg/y).
4. Discussion
During the past two decades, many studies have reported widespread
detections of BPA, 4-NP, and 4-t-OP in surface waters, sediments, and
biota in riverine environments around the world (Kuch and
Fig. 4. Concentrations of phenolic endocrine disrupting chemicals in different efuents of municipal wastewater treatment plants (WWTPs) and three types of
industrial wastewater treatment facilities.
Table 1
The estimated annual mass loads (kg/y) of three phenolic endocrine disrupting chemicals in the rainfall runoff and efuents of municipal wastewater treatment plants
and industrial wastewater treatment facilities in the Huizhou and Dongguan regions during 2015.
Wastewater type Bisphenol A 4-Nonylphenol 4-tert-Octylphenol
Huizhou Dongguan Huizhou Dongguan Huizhou Dongguan
Rainfall runoff 3643 1579 686 338 97.5 25.2
WWTPs 32.5 51.4 77.4 227 0.14 0.35
Dyeing 10.5 35.2 887 2970 9.51 31.9
Electroplating 14.3 26.8 204 382 2.46 4.61
Papermaking 24.2 384 24.8 395 1.29 20.6
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
8
Ballschmiter, 2001; Kolpin et al., 2002; Kawahata et al., 2004; Peng
et al., 2008; Careghini et al., 2015; Wang et al., 2016; Lv et al., 2019). In
China, three phenolic EDCs were detected in numerous river basins,
including the Haihe River (Jin et al., 2004), Liao River (Wang et al.,
2011), Yellow River (Wang et al., 2012), Yangtze River (Liu et al., 2017),
Panlong River (Wang et al., 2016), and Pearl River (Gong et al., 2008;
Diao et al., 2017). The concentrations in river water were 8300 ng/L for
BPA in the Haihe River (Jin et al., 2004; Huang et al., 2012), 3352 ng/L
for 4-NP in the Pearl River (Diao et al., 2017), and 52.1 ng/L for 4-t-OP
in the Liao River (Wang et al., 2011). These detections suggest that the
contamination of phenolic EDCs is ubiquitous. High concentrations of
BPA, 4-NP, and 4-t-OP in surface waters usually can be correlated to
wastewater inputs. The reported concentrations of 4-NP and BPA in the
streams or tributary rivers of the United States (Kolpin et al., 2002),
Germany (Quednow and Puettmann, 2008), Australia (Ying et al.,
2009), and China (Zhao et al., 2011) have reached to several to tens of
micrograms per liter. However, lower concentrations are usually
detected in large rivers, with the concentrations of 4-NP being below
1000 ng/L and those of BPA being below 200 ng/L after dilution by
clean water (Heemken et al., 2001; Wang et al., 2011). Similar trends
were also found in the Pearl River system in this study. The concentra-
tions of BPA and 4-NP were up to tens of micrograms per liter in the
tributaries of the Dongjiang River, and concentrations decreased to
nanograms per liter levels with the several-fold dilution by mainstream
waters after the tributary inputs (Fig. 2; Table S2). Hence, the pollution
of phenolic EDCs in the Pearl River was correlated with
wastewater-related sources of inputs. The distribution of the phenolic
EDCs in sediment was similar as to that in surface water, in which higher
concentrations were present in tributaries than those in the mainstream.
The high detected levels in surface water and sediment suggested that
the occurrences of these compounds in the sediments were related to
water/sediment partitioning processes.
Efuents from municipal WWTPs and industrial wastewater treat-
ment facilities are known to be important sources for phenolic EDCs in
receiving rivers (H¨
ohne and Püttmann, 2008; Ying et al., 2009;
Balabaniˇ
c and Klemenˇ
ciˇ
c, 2011; Fang et al., 2012; Song et al., 2014;
Balabaniˇ
c et al., 2017). For example, research on two pulp and paper
mill efuents from Slovenia showed that the BPA concentrations were
0.72–1.77
μ
g/L and the 4-NP concentrations were 0.43–1.52
μ
g/L
(Balabaniˇ
c and Klemenˇ
ciˇ
c, 2011). The summed concentrations of
alkylphenolic substances (4-NP, 4-t-OP, NPE
1
C, etc.) ranged up to tens of
micrograms per liter in textile wastewater in Belgium and Italy (Loos
et al., 2007). The present study also veried the widespread detection of
phenolic EDCs in efuents of WWTPs and industrial wastewater treat-
ment facilities with concentrations reaching up to hundreds of micro-
grams per liter for 4-NP in dyeing wastewater (Fig. 4). High
concentrations of alkylphenols (4-NP and 4-t-OP) and BPA in industrial
efuents were due to the applications of these chemicals during pro-
duction processes. Alkylphenol and alkylphenol ethoxylates are used as
detergents and auxiliaries in the textile industry, or for surface cleaning
in the electroplating industry (Chen et al., 2013; Ho and Watanabe,
2017); BPA is an important additive used in papermaking factories, ne
chemistry facilities, and plastic industries (Chen et al., 2016). Because of
the strong estrogenic activity effects of phenolic EDCs, alkylphenol and
alkylphenol ethoxylates have been prohibited for use at concentrations
higher than 0.1 % in product formulations by the EU under the regu-
lations of REACH from 2007 onward (EC, 2003); BPA also has been
regulated in terms of its production and usage in various products such
as infant feeding bottles, food containers, and cosmetics (CFDA, 2015;
Usman and Ahmad, 2016). Regardless of the restrictions on usage in
various products, BPA, 4-NP, and 4-t-OP are still found in WWTP ef-
uents in many countries, which implies that efuent discharges are still
the major sources for these chemicals in the environment.
Presently, research on phenolic EDCs in the rainfall runoff from cities
is still limited. Wilkinson et al. (2016) reported BPA concentrations of
511 and 2410 ng/L at two sites containing street runoff prior to entering
rivers. The runoff samples in three French urban catchments were found
to contain a wide array of micropollutants including BPA, 4-NP, and
4-t-OP with concentrations ranging up to 817 ng/L (Gasperi et al.,
2014). Pesticides containing nonylphenol ethoxylate as an adjuvant
used in agriculture may have contributed to the higher concentrations of
4-NP in farmland runoff samples (Sj¨
ostr¨
om et al., 2008). Stormwater
collected at H¨
ogsbo and Skr¨
appek¨
arr waste-sorting sites in Sweden had
concentrations of phenolic EDCs ranging from 110 to 8120 ng/L (Kal-
mykova et al., 2013). The present study also detected concentrations of
BPA up to thousands of nanograms per liter and concentrations of 4-NP
up to hundreds of nanograms per liter for the water and SPM phase of
rainfall runoff combined. In China, larger cities have undergone rapid
urbanization. Extensive detections of phenolic EDCs in the rainfall
runoff implied that widespread use of products containing these chem-
icals, such as infrastructure construction materials and household
products, was related to their release into runoff initiated by rain events.
A previous leaching experiment also veried that extractable water from
building materials, automotive materials, and consumables contains the
ubiquitous presence of alkylphenols and BPA (Lamprea et al., 2018).
The mass load estimations for the three phenolic EDCs from different
sources suggested that the WWTP efuents, industrial wastewater, and
rainfall runoff all contributed large amounts of these chemicals to dis-
charges into the Dongjiang River basin of the Pearl River system
(Table 1). In the present study, the mass loads of rainfall runoff were
equivalent or several times higher than those from WWTP efuents and
industrial wastewater. Nowadays in China, industrial wastewater has to
be treated in an industrial wastewater treatment facility of the factory to
satisfy national industrial emission standards. Then, the wastewater is
pumped to WWTPs in Industrial Parks for further treatment before nal
discharge into receiving rivers. Hence, high mass loads derived from
dyeing, electroplating, and papermaking plants as well as other indus-
trial activities usually do not enter into receiving rivers. Thus, the mass
loads in WWTP efuents and rainfall runoff were the most important
sources for the receiving rivers in this study. Furthermore, the mass
loads of the three phenolic EDCs from rainfall runoff were 3–62 times
higher than those of WWTP efuents (Table 1), which suggested that the
rainfall runoff was the dominant source for phenolic EDCs in the
receiving rivers. It should be noted that the present evaluation is only a
rough estimation of the contamination sources and further ne calcu-
lations involving the urban pipe network system are needed.
In light of the strong estrogenic activity of phenolic EDCs (Nakada
et al., 2004; Zhao et al., 2011), the ΣEEQ values were calculated and
estrogenic risks were assessed in surface waters and source waters. The
ranges of ΣEEQ in the rainfall runoff, WWTP efuents, industrial efu-
ents, tributaries, and mainstream of the Dongjiang River basin were
0.03–1.15, 0.15–0.68, 0.35–30.1, 0.05–3.59, and 0.07–0.42 ng E
2
/L,
respectively. The RQ distributions of estrogenic risks contributed by the
three phenolic EDCs are shown in Fig. S2. In surface water, some sites in
tributaries showed high estrogenic risk, and the highest RQ value for
surface water was detected at DJ-10 (RQ =2.39) of the Shima River.
Meanwhile, there were no high risks detected in the mainstream of the
Dongjiang River. The ndings imply that at least a dilution factor of 24
will be required when the Shima River merges into the mainstream of
the Dongjiang River to maintain lower risks in the mainstream. Street
rainfall runoff and WWTP efuents also showed higher risks than those
in mainstream. Previous studies have reported that biocides used mainly
in household products are discharged into the riverine environment
mainly via domestic wastewater, and those used in paints and render
coatings of ships enter the riverine environment via rainfall ush (Liu
et al., 2018). However, the three phenolic EDCs are used in various in-
dustries and household products, and the risks to the mainstream caused
by the two inputs can range from low to high risks. The ndings of this
study suggested that the estrogenic activity in the mainstream may have
been caused by the WWTP efuents and rainfall runoff, especially street
runoff, which partially enters the mainstream via tributary inputs. Other
than the three phenolic EDCs, many other compounds in the water
J.-L. Zhao et al.

Journal of Hazardous Materials 401 (2021) 123747
9
samples, such as phthalic acid esters, pesticides, BPA analogues, and
natural and synthetic estrogens (estrone, E
2
, and ethinyloestradiol), are
estrogenic (Van Leeuwen et al., 2019). Hence, the three compounds
probably only contributed to a portion of the total estrogenic activity in
the environmental samples. Meanwhile, risks were probably increased
as a result of the elevated combined effects caused by a cocktail of
complicated estrogenic pollutants in the environments (Li et al., 2018).
Hence, more effective measures should be taken to reduce the emissions
of all EDCs and rainfall runoff should be taken into consideration for
further treatment (e.g., stormwater retention ponds) before entering
into receiving rivers.
5. Conclusions
Three phenolic EDCs of high concern, namely, BPA, 4-NP, and 4-t-
OP, were widely detected in surface waters and sediments of the
Dongjiang River basin, a branch of the Pearl River system. In source
assessment work, these compounds were detected in the rainfall runoff,
WWTP efuents, and industrial wastewater samples collected in the
Huizhou and Dongguan regions of the Dongjiang River basin. The dis-
tribution pattern of phenolic EDCs in rainfall runoff was extremely
different from that in surface water. BPA concentrations in rainfall
runoff samples were tens to hundreds of times higher than 4-NP and 4-t-
OP concentrations, while 4-NP ranked the rst in surface water. More-
over, for the three phenolic EDCs in WWTP efuents and dyeing, elec-
troplating, and papermaking wastewaters, the concentrations varied
among wastewater types. Mass loads of the three phenolic EDCs from
rainfall runoff were generally 10 times higher than those from WWTP
efuents, which suggests that the rainfall runoff is an important source
for phenolic EDCs in the receiving rivers. The estrogenic risk assessment
indicated that high estrogenic risks were present in the tributaries of the
Dongjiang River. Additional controls on phenolic EDCs as well as other
EDCs are needed to reduce the inputs of estrogenic activity from these
sources.
CRediT authorship contribution statement
Jian-Liang Zhao: Conceptualization, Visualization, Formal analysis,
Writing - original draft, Writing - review & editing. Zheng Huang:
Investigation, Data curation. Qian-Qian Zhang: Investigation. Liang
Ying-He: Validation. Tuan-Tuan Wang: Data curation. Yuan-Yuan
Yang: Software, Formal analysis. Guang-Guo Ying: Writing - review &
editing, Funding acquisition, Resources, Supervision.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Acknowledgements
The authors would like to acknowledge the nancial support from
the National Natural Science Foundation of China (NSFC 41877360) and
the Natural Science Foundation of Guangdong Province, China (No.
2019B030301008).
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.jhazmat.2020.123747.
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