Environment International 134 (2020) 105300

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Environment International
journal homepage: www.elsevier.com/locate/envint

Removal of triclosan during wastewater treatment process and sewage T

sludge composting—A case study in the middle reaches of the Yellow River
⁎
Guodi Zhenga,b, , Bao Yua,b, Yuewei Wanga,b, Chuang Mac, Tongbin Chena,b
a
Center for Environmental Remediation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
b
College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
c
Department of Material and Chemical Engineering, Zhengzhou University of Light Industry, Zhengzhou 450002, China

A R T I C LE I N FO A B S T R A C T

Handling Editor: Adrian Covaci Triclosan (TCS) is widely used as an antibacterial disinfectant in personal care products, especially in rapidly-
Keywords: urbanizing countries, such as China. Almost all TCS enters wastewater treatment plants (WWTPs), but the fate of
Triclosan the TCS in the WWTPs is unclear. TCS may be present in sewage sludge or in effluent, and the discharge of TCS
Biodegradation into an ecosystem can pose environmental risks. In the present study, influent, effluent, and sewage sludge were
Sewage sludge collected from four typical urban WWTPs, and the fate of TCS in the plants was investigated. The study was
Compost conducted in Zhengzhou, a city in the middle reaches of the Yellow River in China. The sewage sludge was used
Aeration for aerobic composting to study the influences of different ventilation treatments on the biodegradation effects of
TCS and the changes in the microbial community during the composting process. The results showed that the
mean concentration of TCS in the influent of the four typical WWTPs was 397.1 ng/L. The mean level of TCS in
the effluent was 8.0 ng/L. The mean concentration of TCS in the sewage sludge was 814.4 ng/g. For the four
WWTPs, the percentages of TCS removal were 97.6% (Nansanhuan), 97.6% (Xinzheng), 98.8% (Wulongkou),
and 97.9% (Chenyu), respectively. The sewage sludge enrichment rates for TCS ranged between 36.4% and 49%.
Therefore, there is a need to focus on the environmental risks from sewage sludge. During aerobic composting,
the TCS was effectively degraded under three ventilation strategies. Thus, improved ventilation could enhance
the degradation rate of TCS. Moreover, TCS degradation occurred in the mesophilic period and in the early stage
of the thermophilic phase period. Finally, the degradation rates of TCS in sewage sludge samples composted with
low-, medium-, and high-ventilation treatments were 48.1%, 59.0%, and 59.5%, respectively. Thus, high ven-
tilation could provide enough oxygen for the pile and enhanced microorganism activity, benefiting the de-
gradation of TCS. In addition, the microbial communities change during the composting process, and a diversity
index of the changes can help explain the composting process.

1. Introduction
Triclosan (TCS) is a broad-spectrum antibacterial agent, and is
widely used in pharmaceutical and personal care products (PPCPs). TCS
has a fungicidal effect on a variety of bacteria and fungi (Armstrong
et al., 2019; Chen et al., 2018a). However, TCS has a far-reaching in-
fluence on the ecological environment, owing to its usage (Lindström
et al., 2002). Previous investigations have indicated that TCS has a high
detection rate in the environment. In the United States of America, the
detection rate of TCS in 139 rivers was 57.6% (Kolpin et al., 2002); in
China, the detection rate of TCS in the aquatic environment of the
Dongjiang River basin was 90% (Chen et al., 2014). TCS has been found
to accumulate in a variety of organisms, including algae, snails,
starlings, and kestrels (Coogan and Point, 2008; Sherburne et al., 2016).
TCS may affect the growth of organisms in terrestrial and aquatic en-
vironments, and may even cause health risks to human beings that are
exposed to these environments (Butler et al., 2012; Sherburne et al.,
2016). Unfortunately, TCS has also been detected in human bodies. Iyer
et al. (2017) collected 430 samples of human urine from countries in
Asia and the United States of America for investigating urinary levels of
TCS, and TCS was detected in 355 samples (83%). Chen et al. (2018b)
found that the detection rate of TCS in urine samples collected from
children in South China was 95%, with the highest concentration being
21.9 μg/L.
TCS inhibits algal photosynthesis, affecting the growth of aquatic
plants, and also exhibits toxicity and endocrine disruption effects on

⁎
Corresponding author at: Center for Environmental Remediation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences,
Beijing 100101, China.
E-mail address: zhenggd@igsnrr.ac.cn (G. Zheng).

https://doi.org/10.1016/j.envint.2019.105300
Received 30 July 2019; Received in revised form 21 October 2019; Accepted 30 October 2019
Available online 11 November 2019
0160-4120/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
G. Zheng, et al.
amphibians and mammals (Ricart et al., 2010; Shi et al., 2017). Lin
et al. (2010) found that TCS induced an increase in the activity of su-
peroxide dismutase (SOD) in earthworms. Moreover, TCS was identified
as a “possible toxicant” associated with reproductive and develop-
mental health (Johnson et al., 2016). Another study revealed that
prenatal TCS exposure had potential impacts on reproductive hormones
in cord blood mediated by a steroidogenic enzyme (Wang et al., 2018).
TCS has also affected the function of soil, such that a soil nitrogen cycle
was severely damaged when the TCS concentration in the soil was more
than 5 mg/kg (Svenningsen et al., 2011). Therefore, more attention
should be paid to the fate and risks of TCS in the environment.
As most TCS is discharged into wastewater treatment plants
(WWTPs) with wastewater, it is important to develop urban wastewater
treatment strategies for providing better aquatic environments (Tohidi
and Cai, 2017). Wastewater treatment rates generally increase as a
country develops, and since 2014, the wastewater treatment rates for
metropolitan areas in China have exceeded 90%, according to assess-
ment results (Zhu et al., 2018). After a series of physical and chemical
changes, pollutants are decomposed during the wastewater treatment
process, and are released into the environment with the treated effluent
or sewage sludge. Different treatment processes affect the removal ef-
ficiency of TCS during the wastewater treatment process. Although
there have been many studies on the presence of TCS in WWTPs, there
is scant research on the fate of TCS in wastewater treated by different
treatment processes, and/or on a regional scale. (Tohidi and Cai, 2017)
studied the fate of TCS using three different types of wastewater
treatments, and the results indicated that the removal rates of the TCS
were different. During the wastewater treatment process, most of the
TCS was removed through biodegradation or adsorption (Armstrong
et al., 2018; Lozano et al., 2013). During wastewater and biosolid
treatment processes, Lozano et al. (2013) found that over 97% of the
TCS was removed, and that 64% of the TCS was transferred to sewage
sludge.
Owing to the hydrophobic lipophilicity of TCS, sewage sludge has
an apparent adsorption effect on TCS (Dann and Hontela, 2011; Tohidi
and Cai, 2017). Land application is one of the primary disposal methods
of sewage sludge; direct application would cause a large amount of TCS
to discharge into farmlands, destroying the soil structure and con-
taminating the environment, and leading to the flow of TCS into river
water (Alvarenga et al., 2015; Butler et al., 2012; Healy et al., 2017). As
such, the environmental risks of TCS in sewage sludge should be em-
phasized. Composting has been the primary method for ensuring the
safe utilization of sewage sludge (Pujara et al., 2019). Thus, the beha-
vior of TCS during the composting process has been studied. Under
aerobic conditions, microorganisms in sewage sludge can decompose
organics into small molecule inorganics, or into stable humus. Studies
have found that many types of organisms can degrade TCS (Tohidi and
Cai, 2017; Yu et al., 2019). Yu et al. (2019) studied the removal and
risks of TCS in sewage sludge and indicated that 65.2% of the TCS in the
study was biodegraded during sewage sludge composting with high
ventilation. In this regard, the microbial community plays a decisive
role in organic contaminate degradation during the sewage sludge
composting process (Alves et al., 2019). To study different methods for
improving a composting process, some studies have altered parameters
such as the ventilation, choice of conditioner, or adjustment ratio of
carbon/nitrogen (C/N). As TCS leads to environmental and health risks,
it is important to investigate whether TCS can be degraded during the
sewage sludge composting process, and to study ways to accelerate TCS
degradation.
The Bohai Sea Ring Area and the regions around the Yellow Sea are
rapidly-developing areas of China. Moreover, the Yellow River dis-
charges most of its flow into the Bohai Sea. A decrease in the con-
centration of TCS in the water discharged to the Bohai Sea will there-
fore decrease the concentration of TCS in the Bohai Sea. Therefore, it is
particularly important to understand the fate of TCS in the upper
reaches of the Bohai Sea. The Yellow River is the second largest river in
2
Environment International 134 (2020) 105300
China, and ultimately flows into the Bohai Sea. Zhengzhou, which is the
capital of the Henan Province, is the most important city in the Yellow
River basin, with a population of 10.1 million. Zhengzhou was chosen
as the location for studying the fate of TCS in WWTPs and in the
composting process. The present study sampled water and sewage
sludge from four representative WWTPs in Zhengzhou and analyzed the
fate of TCS during the wastewater treatment process and composting
process. This study emphasized the degradation rule of TCS and ad-
justed some technological parameters during the composting process.
The purpose of this study was to accurately evaluate the abatement
process of TCS during the wastewater treatment and composting pro-
cesses, and to reduce the environmental risks in land application. The
results can provide some information for countries and other entities in
regard to wastewater and sewage sludge treatment and pollution pre-
vention.
2. Materials and methods
2.1. Chemical analysis
All analytical solvents, including dichloromethane, methanol,
acetone, and n-hexane (high-performance liquid chromatography
(HPLC) grade), were purchased from Sigma-Aldrich (St. Louis, USA).
The TCS was obtained from Aladdin (Shanghai, China). Solid-phase
extraction columns (Oasis hydrophilic/lipophilic balanced (HLB), 6 mL,
500 mg) were purchased from Waters (Milford, USA). The stock solu-
tion of TCS was prepared at a concentration of 1000 mg/L in methanol.
2.2. Sampling
The sampling was conducted from June–July 2018. The influent,
effluent, and sewage sludge samples of four WWTPs with different
treatment processes were collected in Zhengzhou to study the fate of
TCS. The different treatment processes were: preposition anaerobic
phase +A2/O (Nansanhuan WWTP), Carrousel oxidation ditch
(Xinzheng WWTP), modified oxidation ditch (Wulongkou WWTP), and
modified A2/O (Chenyu WWTP of the Zhengzhou airport zone). The
four WWTPs are large and discharge their final effluents into the tri-
butaries of the Yellow River and the Huai River.
Wastewater samples were collected in three replicates using clean
brown glass bottles (500 mL) and without considering the flow rate.
These samples were preserved using nitric acid (pH 2–3). Sewage
sludge samples were collected in three replicates using sealed poly-
ethylene (PE) bags. After collection, the samples were transported on
ice to the laboratory, then stored in a freezer at 4 °C until extraction.
The wastewater samples were extracted within a week. The sewage
sludge samples were dried in a low-pressure freeze dryer (Labconco
Freezone, Kansas, USA), then were fully ground in a mill (IKA A11
BASIC, Staufen, Germany) and sieved through 60 meshes.
2.3. Sample preparation
The extraction and analysis for all of the samples were performed in
triplicate. The wastewater samples were filtered through 0.45 μm glass
fiber filters. Furthermore, the wastewater samples were passed through
the HLB columns, which were preconditioned using 10 mL methanol
and 10 mL Milli-Q water (pH 2–3). The HLB columns were dried using a
vacuum pump, and the target compounds were eluted from them using
a dichloromethane and methanol mixture (4:1, 10 mL). The extracts
were dried with nitrogen gas, and then were dissolved to 1 mL in me-
thanol for HPLC-mass spectrometry (MS) analysis.
The target compounds in the sewage sludge were extracted using an
accelerated solvent extractor (ASE 350, Dionex, Sunnyvale, USA). Each
sewage sludge sample was weighed and placed in an extraction pool
with 34 mL of the extraction solvent (dichloromethane:acetone = 1:1)
(Zheng et al., 2018). The samples were extracted once at 100 °C and
G. Zheng, et al. Environment International 134 (2020) 105300

1500 psi, using dichloromethane. After extraction, the extracts were Table 1
rotary-evaporated to 1 mL and dried with nitrogen gas, then were re- Main properties of the composting materials.
dissolved using 5 mL n-hexane. The diluted extracts were then further Materials Moisture pH Organic C/N Triclosan
purified using the HLB columns that were conditioned with 3 mL me- content (%) matter (%) (TCS) (ng/g)
thanol, 3 mL acetone, 3 mL dichloromethane, and 3 mL n-hexane. The
Sewage sludge 80.0 6.2 70.9 6.7 952.3
extracts were subsequently passed through the columns, followed by
Sawdust 10.0 7.0 85.1 293.0 285.1
the leaching of 2 mL n-hexane and 4 mL dichloromethane through the Low ventilation 60.1 6.7 65.3 11.0 763.4
columns. After drying the columns for 10 min, 4 mL Milli-Q water was Medium ventilation 62.2 6.9 64.8 8.4 820.6
added to each column. Then, the columns were dried in a vacuum for High ventilation 61.7 6.6 64.0 9.7 817.1
5 min, and finally, were eluted with a methanol and acetone mixture Control check (CK) 80.0 6.2 70.9 6.7 952.3

(1:1, 6 mL). Prior to analysis, the final eluates were dried with nitrogen
gas, re-dissolved using 0.5 mL methanol, and passed through 0.22 μm
During the sewage sludge composting, the oxygen was automatically
needle-type organic filters.
monitored with a real time on-line system (Zheng et al., 2018). Sewage
sludge samples were collected at days 0, 1, 2, 4, 7, 8, 11, and 17.
2.4. Analysis
Furthermore, the physical and chemical properties of the samples were
detected, and the samples were stored at 4 °C for subsequent analysis.
The wastewater samples were analyzed using the analytical proto-
cols developed by Pintado-Herrera et al. (2016). That study contains all
2.6. Data analysis
of the information regarding the analytical standards and methods.
The sewage sludge samples were analyzed using HPLC (including a
The ash content was determined using a constant weight method. A
UV detector and autosampler, Agilent, USA). The HPLC columns (C18
crucible with mass M1 was used to weigh a certain amount of a dry
symmetry, 5.0 μm, 4.6 mm × 250 mm) were purchased from Waters
sewage sludge sample, and the total mass was M2. The sample con-
(Milford, USA). The analysis conditions were as follows: mobile phase:
tained in the crucible was placed into a muffle stove and calcined for
methanol and water (4:1); flow rate: 0.6 mL/min; sample volume:
5 h at 550 °C. The final mass of crucible and sample was M3, and the ash
50 μL; detection temperature: 30 °C; and ultraviolet detection wave-
content was calculated as follows:
length: 280 nm. The detection limit (S/N = 3, n = 6) was 0.25 mg/L,
and the recovery rate of TCS was 73.0%. M3 − M1
Ash content = × 100%
M2 − M1
2.5. Sewage sludge composting The formula for calculating the degradation rate of TCS during
sewage sludge composting is as follows:
The sewage sludge used for composting was collected from the
Wulongkou WWTP in Zhengzhou. Moreover, sawdust was obtained (Ai × C0) − (A0 × Ci )
Degradation rate(%) = × 100%
from local farms for use as a conditioner, and the proportion of sewage Ai × C0
sludge to sawdust was 4:1. The compost experiment was conducted in
where, A0 is the ash content of the original material of the compost, Ai is
bioreactors, and each bioreactor had a volume of 340 L (Fig. 1). Three
the ash content of the compost on day i, C0 is the TCS content of the
different ventilation frequencies were set for the composting experi-
original material of the compost, and Ci is the TCS content of the
ment (low ventilation; medium ventilation; high ventilation). Mean-
compost on day i.
while, the same quality of sewage sludge was directly piled as a control
check (CK). The main properties of the composting materials are shown
2.7. Microbial community diversity
in Table 1.
During the composting process, the intermittent aeration duration
The Soil Power® DNA extraction kit (MO BIO Laboratories,
for a 22 min ventilation cycle was 1 min. The compost lasted for
Carlsbad, Canada) was used to extract DNA from the compost samples
17 days, and the temperature was measured daily at 08:00 and 17:00.
(medium ventilation), as well as to select qualified DNA samples. Then,
the whole 16S regions of the DNA samples were amplified using full-
Temperature sensor Exhaust length amplification primers with barcode tags, thereby eliminating
low-quality sequences and obtaining high-quality amplified sub-
sequences. The microbial community diversity of the compost samples
was obtained using a third-generation high-throughput sequencing
Control system platform (Illumina HiSeq/MiSeq). Finally, the 16S rDNA result was
analyzed, and the microbial community information was revealed using
operational taxonomic units (OTU), principal component analysis
(PCA), and alpha diversity, as well as a heatmap of species.

3. Results and discussion

Sensor probe 1.2m
3.1. Occurrence of triclosan in four wastewater treatment plants

The occurrences of TCS in the Nansanhuan WWTP, Xinzheng

WWTP, Wulongkou WWTP, and Chenyu WWTP are shown in Table 2.
Table 2 includes the concentrations and fate of TCS in influent (raw
Fan
wastewater), effluent (final effluent), and sewage sludge for each
Flowmeter WWTP.
The concentration of TCS in the influent and effluent was
Fig. 1. Schematic diagram of a biological fermentation automatic control de- 322.5 ± 22.3–467.2 ± 39.4 ng/L and 5.0 ± 4.2–11.3 ± 6.4 ng/L,
vice. respectively. This result indicated that more than 97% of the TCS was

3
G. Zheng, et al. Environment International 134 (2020) 105300

removed after through the WWTPs with different treatment processes.

Transfer to sewage sludge
Lozano et al. (2013) found that the TCS removal rates and removal
principles were different in the primary treatment stage, secondary
treatment stage, and secondary nitrification and denitrification stages.
The TCS was enriched in the sewage sludge, with a concentration of
742.1 ± 63.3–886.3 ± 104.8 ng/g. In the Nansanhuan WWTP, the
36.4%
47.5%
42.4%
49.0%

TCS concentration in the influent was 467.2 ± 39.4 ng/L; however,

after the treatment process, its concentration in the effluent was re-
duced to 11.3 ± 6.4 ng/L, and its concentration in the sewage sludge
Biodegradation

was found to be 886.3 ± 104.8 ng/g. In the Chenyu WWTP, the TCS
concentration in the influent was 378.8 ± 20.0 ng/L. However, after
61.2%
50.1%
56.4%
48.9%

treatment, its concentration in the effluent was reduced to

7.9 ± 3.7 ng/L, and its concentration in sewage sludge was determined
as 825.6 ± 30.8 ng/g. The treatment abilities of the four WWTPs were
Removal rate

120,000 tons/d (Nansanhuan), 105,000 tons/d (Xinzheng), 100,000

tons/d (Wulongkou), and 40,000 tons/d (Chenyu). The total quantities
97.6%
97.6%
98.6%
97.9%

of TCS in the wastewater of the four WWTPs were 56.1 g/d, 33.9 g/d,
42 g/d, and 15.1 g/d, respectively, and the quantities discharged into
the environment through the wastewater treatment process were 1.4 g/
Effluent (g/d)

d, 0.8 g/d, 0.5 g/d, and 0.3 g/d, respectively.

Among the four typical WWTPs, the Nansanhuan WWTP, located in
a densely-populated urban area, has the longest service time, the
1.4
0.8
0.5
0.3

highest daily wastewater treatment capacity, and the highest content of

TCS in the influent. The use of PPCPs containing TCS by humans is an
Influent (g/d)

essential cause of the influx of such compounds in wastewater and the

entry of such compounds into the environment, ultimately leading to its
exposure to humans. As compared with other countries and regions, the
56.1
33.9
42.0
15.1

concentrations of TCS in the influent of the WWTPs were found to be

lower in this study. In the mid-Atlantic region of the U.S., the con-
Sewage sludge (ng/g)

centration of TCS in the influent is approximately 8000 ng/L (Lozano

et al., 2013). This difference in the total content of TCS in the waste-
104.8
98.6
63.3
30.8

water may be caused by differences in the population of the regions, as

well as the use of related products. The concentrations of TCS in the
±
±
±
±
886.3
803.6
742.1
825.6

effluent of the four WWTPs were 11.3 ng/L, 7.9 ± 3.3 ng/L,
5.0 ± 4.2 ng/L, and 7.9 ± 3.7 ng/L, respectively, with a mean value
of 8.0 ng/L. The previous literature predicted the chronic toxicity of
Effluent (ng/L)

TCS, and they found that the no-effect concentration (PNEC) of TCS was
11.3 ± 6.4
7.9 ± 3.3
5.0 ± 4.2
7.9 ± 3.7

26 ng/L (Liu et al., 2015). The maximum concentration of TCS in the

effluent was lower than the PNEC of TCS. In addition, there are dilu-
tion, diffusion, and degradation processes when TCS is discharged into
an aquatic environment. Therefore, it is difficult for wastewater that
Influent (ng/L)

goes through the treatment process to damage the ecosystem or pose a

39.4
22.3
44.7
20.0

biological risk.
±
±
±
±

Currently, TCS has been identified as one of the top pollutants in the
467.2
322.5
419.7
378.8

national sewage sludge of certain countries (Guerra et al., 2014;

Kannan, 2015; Subedi et al., 2014). However, there are few studies
concerning China. Chen et al. (2019) studied the concentrations of TCS
Carrousel oxidation ditch
Anaerobic phase + A2/O

Modified oxidation ditch

and its conversion products in sewage sludge from urban WWTPs in 21

provinces and cities in China and found that the highest concentration
Treatment process
Occurrence of TCS in four wastewater treatment plants.

of TCS was 4870 ng/g. In this study, the maximum concentration of TCS
Modified A2/O

in the sewage sludge was 886.3 ng/g, with a mean value of 814.4 ng/g.
Moreover, the TCS concentration in the sewage sludge in China was
lower than in other countries (Chen et al., 2019; Guerra et al., 2014;
Healy et al., 2017). According to data from the US Environmental
Protection Agency (USEPA), the average concentration of TCS in urban
Wastewater treatment plants (WWTPs)

sewage sludge in the United States is 16097 ng/g. Furthermore, the

United States has begun to limit the use of TCS to decrease its con-
centrations in sewage sludge (Chen et al., 2019). The concentration of
TCS in sewage sludge in Canada was 6800 ng/g (Guerra et al., 2014).
Subedi et al. (2015) investigated the concentrations of TCS in sewage
sludge obtained from four WWTPs in India and observed a mean value
of 1133.8 ng/g. The concentration of TCS in sewage sludge in Ireland
Nansanhuan

Wulongkou

was 80 ng/g; thus, its concentration was found to be low. This could be
Xinzheng

Chenyu

owing to Ireland′s policy of limiting the amount of TCS in use and of

Table 2

phasing out TCS from the pharmaceutical industry (Healy et al., 2017).
In this study, the average concentration of TCS in the sewage sludge

4
G. Zheng, et al.
Fig. 2. Fate of triclosan in four wastewater treatment plants.
was at a medium level compared to the global average concentration,
demonstrating that there was room for improvement.
3.2. Fate of triclosan in four wastewater treatment plants
The fate of the TCS in the four WWTPs are shown in Fig. 2. The
biodegradation rates of the TCS in the four WWTPs of Nansanhuan,
Xinzheng, Wulongkou, and Chenyu were 61.2%, 50.1%, 56.4%, and
48.9%, respectively. The enrichment percentage of the TCS in the
sewage sludge of the four WWTPs were 36.4%, 47.5%, 42.4%, and
49.0%, respectively. Finally, no more than 2.4% of TCS existed in the
effluent. Most of the TCS was degraded or enriched in the sewage
sludge, and only a small percentage was discharged into the environ-
ment along with the final effluent. The total removal rate of TCS in the
wastewater was high (more than 97%), and nearly half of the TCS was
concentrated in the sewage sludge. Similar results have been obtained
in previous research (Heidler et al., 2006; Lozano et al., 2013). Based on
these results, sewage sludge could be considered as a new contamina-
tion source which poses a threat to environmental safety and human
health. After wastewater treatment, the next key step was to control the
TCS in the sewage sludge. Butler et al. (2012) conducted a 12-month
experiment to explore the persistence and mobility of TCS in soil. The
experimental results showed that some of the TCS migrated to the deep
soil, whereas 49.4–83.5% of the TCS remained in the soil as morpho-
logical or methyl TCS. Therefore, proper disposal of sewage sludge
before application to agricultural land is essential to eliminate the en-
vironmental risks of new organic pollutants. As such, enhanced TCS
biodegradation during the wastewater treatment process and sewage
sludge disposal process are two directions for future research.
More than 97% of the TCS was removed through different methods,
and different treatment technologies were effective for reducing the
TCS environmental risk. However, the biodegradation rate is different
in different treatment processes. The preposition anaerobic phase +A2/
O treatment technique was found to have the highest degradation rate,
followed by the improved oxidation ditch treatment; however, the
modified A2/O treatment had the lowest degradation rate. The pre-
position anaerobic phase +A2/O treatment process had the best overall
degradation effect on TCS, probably owing to proper anaerobic diges-
tion. However, the modified A2/O treatment process did not aid in the
biodegradation of TCS but enhanced the enrichment of the TCS in the
sewage sludge. Moreover, the modified Carrousel oxidation ditch could
enhance the biodegradation of TCS during the wastewater treatment
process. Thus, all four different treatment processes could effectively
remove TCS (Tohidi and Cai, 2017). The fate of TCS is not only de-
termined by the biological processes of the WWTPs but is also affected
5
Environment International 134 (2020) 105300
by the primary sedimentation process and secondary sedimentation
process, the microorganisms′ activity, sedimentation, and adsorption.
Each of these factors is important for determining the final fate of the
TCS. For the four WWTPs, the percentages of TCS removal were 97.6%
(Nansanhuan), 97.6% (Xinzheng), 98.8% (Wulongkou), and 97.9%
(Chenyu), respectively. In addition, the TCS in the effluent did not pose
a risk to the basin. However, sewage sludge has an apparent adsorption
effect on TCS, owing to the hydrophobic lipophilicity of TCS, and the
enrichment rate of TCS in the sewage sludge was more than 36%. The
TCS could therefore still pose an ecological risk to the terrestrial en-
vironment and aquatic environment (through runoff) after sewage
sludge land application. Therefore, the ecological risks of sewage sludge
require more attention (Armstrong et al., 2018; Chen et al., 2019;
Chevillot et al., 2018).
3.3. Temperature and oxygen content changes during composting
The temperature changes in the three different ventilation compost
treatments are shown in Fig. S1. The composting period can be divided
into three stages, namely the mesophilic phase (0–2 days), thermophilic
phase (3–11 days), and cooling and ripening phase (12–17 days). In this
study, during composting, the thermophilic phase was more than
3 days, ensuring the sterilization effect of the compost and the stability
of the compost products, and thereby meeting the sanitary standards for
composting (Yan et al., 2016). The temperature of the compost is clo-
sely related to the life activity of microorganisms, heat production, and
the heat dissipation of the composting device, with the temperature
affecting the activity, abundance, and community structure of the mi-
croorganisms (Yu et al., 2019; Zheng et al., 2018).
At the beginning of the compost, the temperature increased rapidly,
and entered the thermophilic phase. After two days, the temperatures in
the composts with low-, medium-, and high-ventilation treatments were
63.1 °C, 73.4 °C, and 75.9 °C, respectively. The thermophilic phase
lasted more than 11 days, and the highest temperature reached was
approximately 70 °C. On the 14th day of the compost, the temperature
decreased, indicating that the composting had entered the cooling and
ripening stage. Furthermore, the temperature dropped slowly to
29.1 °C, which is close to the ambient temperature. Thus, composting
can effectively reduce the potential pathogenic bacteria in sewage
sludge. It can be seen from Fig. 3 that the warming effect from the high-
ventilation composting treatment is significantly better than that in the
other two experimental groups (Yan et al., 2018; Yu et al., 2019). Yan
et al. (2018) researched the effects of different ventilation strategies
(no-aeration intermittent aeration, and continuous aeration) on the
composting of cattle manure, and observed that sufficient oxygen was
necessary to obtain a good quality compost. Improving the ventilation
conditions of compost piles could therefore increase the effective ac-
cumulated temperature and benefit the degradation of TCS.
Ventilation treatments not only affect the compost temperature, but
Fig. 3. Changes in triclosan degradation rates in each group under different
aeration conditions.
G. Zheng, et al.
Table 3
The slope of the fitted straight line in each group under different aeration conditions.
Ventilation Slope (K) of fitting line of TCS degradation /d−1
Mesophilic phase Thermophilic phase Cooling phase
Low 0.15 0.03 0.01
Medium 0.14 0.03 0.03
High 0.20 0.05 0.02
also affect the oxygen content of the compost piles, thereby influencing
the activities of the microbes that participate in the composting process.
The changes in the oxygen content inside the compost piles with the
three different ventilation treatments are shown in Table 3.
The oxygen content of the low-, medium-, and high-ventilation
composts before ventilation were 7.3%, 7.5%, and 8.2%, respectively.
Once ventilation began, the oxygen content increased rapidly, reaching
up to 10.4%, 13.9%, and 15.7%, respectively. The enhanced ventilation
could effectively increase the oxygen content, as the oxygen content
increased 33.7% and 51.0% in the compost piles with medium and high
ventilation, respectively, as compared to those with low ventilation.
After the end of ventilation, the oxygen content in the low-ventilation
treatment gradually decreased to 7.2%, whereas the oxygen content for
the compost piles with medium- and high-ventilation treatments de-
creased rapidly, from 13.9% and 15.7% to 7.6% and 8.1%, respectively.
According to the oxygen content changes, the microorganisms have
greater activity in compost piles with more ventilation. For compost
piles, the oxygen consumption rate decreased with a decrease in the
ventilation frequency. Low ventilation does not provide sufficient
oxygen, thereby weakening the microbial respiration and degradation
of TCS. High ventilation could provide enough oxygen for the compost
piles, and the oxygen was consumed quickly, owing to the higher mi-
croorganism activity in high ventilation. Torrent et al. (2017) also
concluded that hypoventilation inhibits the activity of microorganisms
in a compost. Therefore, increasing the ventilation frequency appro-
priately and increasing the oxygen content of the compost are con-
ducive to the degradation of TCS. During the entire ventilation cycle,
the oxygen content of each of the three experimental groups was above
7%, i.e., they did not enter the anaerobic state (Jiang et al., 2016;
Oazana et al., 2018).
3.4. Effect of aeration on the degradation of triclosan during composting
The degradation rates of TCS in compost piles with different ven-
tilation treatments are shown in Fig. 3. The initial concentrations of TCS
in the low-, medium-, and high-ventilation treatments were 763.4 ng/g,
820.6 ng/g, and 817.1 ng/g, respectively. During the composting pro-
cess, the concentration of TCS decreased remarkably. The degradation
of TCS mainly occurred in the mesophilic phase and in the early stage of
the thermophilic phase, especially in the first four days. On the 4th day,
the biodegradation rates in three compost piles were 37.1%, 35.1%, and
44.4%, respectively. At the end of composting, the TCS concentrations
decreased to 416.4 ng/g, 352.9 ng/g, and 327.4 ng/g with the low-,
medium-, and high-ventilation treatments, respectively. The final de-
gradation rates of the TCS in the compost piles with the low-, medium-,
and high-ventilation treatments were 48.1%, 59.0%, and 59.5%, re-
spectively. The highest TCS degradation rate was observed in the high-
ventilation composting treatment, followed by the medium-ventilation
treatment. The degradation percentage of TCS was enhanced by 22.7%
and 23.1% in the compost piles with medium and high ventilation,
respectively, as compared to those with low ventilation. Considering
the ventilation cost, the medium-ventilation strategy was considered to
be the best choice for TCS biodegradation during sewage sludge com-
posting. The lowest TCS degradation rate was observed in the low-
ventilation treatment group. There was no significant decrease in TCS
in the CK, proving that sewage sludge, without a composting treatment,
6
Environment International 134 (2020) 105300
Change in O2 content
Maximum O2 content /% O2 consumption/% Rate constant/K
10.4 3.2 0.16
13.9 6.3 0.27
15.7 7.6 0.32
could not effectively degrade TCS. TCS was barely degraded under
anaerobic conditions, as the microbial activity in the compost was
limited. This proves that insufficient oxygen supply in a compost is not
conducive to the degradation of TCS. Sadef et al. (2015) pointed out
that hypoxic conditions limited the biodegradation of micro-pollutants.
Yu et al. (2019) revealed that enhancing or prolonging ventilation fa-
cilitated the biodegradation of pollutants in sewage sludge during
composting.
To better understand the degradation of TCS during a composting
process, it is necessary to analyze the degradation rate of TCS at dif-
ferent periods of compost treatments with different ventilation.
Therefore, a scatter plot of the TCS concentration Ln (C/C0) with time
and a linear fit of the composting period is generated. The slope K of the
fitted straight line reflects the degradation rate. The K values of the
different composting periods in the different ventilation composting
treatments are significantly different. The slopes of the fitted straight
line in each period of the different ventilation composting treatments
are shown in Table 3.
The slopes of the Ln (C/C0)-t of TCS in the low-ventilation group
were 0.15 d−1, 0.03 d−1, and 0.01 d−1 in the mesophilic period,
thermophilic period, and cooling period, respectively. The slopes of the
linear fitting in the medium-ventilation group were 0.14 d−1, 0.03 d−1,
and 0.03 d−1, respectively. The slopes of the linear fitting in the high-
ventilation treatment group were 0.2 d−1, 0.05 d−1, and 0.02 d−1,
respectively. However, the degradation rate of TCS in the mesophilic
phase was higher, and this phase lasted for a short duration; the de-
gradation rate of TCS in the thermophilic phase was lower, and this
phase lasted for a long duration. The degradation of TCS in the three
compost groups mainly occurred during the mesophilic period and in
the early stage of the thermophilic period, and the degradation rate
decreased during the later stages of the thermophilic period and cooling
period (Yu et al., 2019; Zheng et al., 2018). As the activity of micro-
organisms and their reproduction is higher in the mesophilic period, the
degradation of TCS, which is related to the microorganisms, sig-
nificantly increased in the mesophilic period. Moreover, the degrada-
tion rate is different even within the mesophilic period, which is the
main reason for the different rates of TCS degradation in the different
ventilation treatment composts. However, as the mesophilic period it-
self is shorter, enhanced microorganism activity during the mesophilic
period or a prolonged thermophilic period were both feasible for im-
proving the degradation efficiency of TCS during a composting process.
Armstrong et al. (2018) showed that increasing the sewage sludge re-
sidence time and compost temperature would increase the degradation
rate of TCS in a sewage sludge reactor. It can be seen from the tem-
perature data that increasing the ventilation frequency of the compost
prolongs the duration of the thermophilic period, increases its tem-
perature, and increases the degradation rate of TCS in the sewage
sludge to a certain extent.
3.5. Relationship between microbial community change and triclosan
degradation in compost
During the sewage sludge composting process, samples were ob-
tained at 0, 1, 2, 4, 7, 11, and 17 days. The microbial community di-
versity of the compost samples is shown in Table S1. The coverage of
the compost samples was 0.86–0.94. This 16S rDNA analysis could
G. Zheng, et al.
Fig. 4. Principle component analysis of microbial community of medium ven-
tilation compost at different times.
cover most microbial changes, and the determined data of the microbial
community were credible. The observed species (sobs) of the compost
samples were 533–793, based on a 97% sequence similarity. The sobs
changed during composting and reached the peak (7 9 3) on the 4th
day. Chao1, Ace, Shannon, and Simpson were used as the microbial
community diversity indexes. Chao1 (807.78–1377.03) and Ace
(907.97–1882.14) were used as abundance indexes; Shannon
(4.16–5.57) was used as the species diversity index; and Simpson
(0.01–0.07) was used as the evenness index.
According to these indexes of microbial community diversity, the
microbial community changed during the sewage sludge composting
process, and the microbial diversity and abundance reached their peak
on the 4th day. The microorganisms′ characteristic changes were con-
sistent with the law of TCS degradation. The degradation of organic
matter in compost mainly depends on the metabolic activities of mi-
croorganisms. Therefore, the content of the TCS was correlated with the
change of the microbial community during composting.
To analyze the influential factors for microbial community char-
acteristics, the results of a principal component analysis (PCA) of the
microbial communities presented in the nine samples are depicted in
Fig. 4. PCA is a technology that can be used to simplify microbial data,
and it can effectively determine the main elements and structure. The
differences in various samples were obtained through PCA, and the
distance between two points on the PCA represents the degree of their
similarity (Wang et al., 2012; Zhao et al., 2018).
The microbial communities are significantly different, according to
the separation of points on Fig. 4. The two principal components (PC1
and PC2) for the accumulated variance contribution rates only occupied
57.9%. Through analysis of the samples′ sources, PC1 and PC2 are re-
presentative of the composting time and compost temperature, these
two factors only explain 57.9% of the differences. In same compost pile,
and for a microbial community in a compost sample that is sampled at
different time, there are many factors that can influence the outcome.
These 7 samples were placed in 4 groups: 0th day and 1st day; 2nd day;
4th day, 7th day, and 11th day; and 17th day. The microbial commu-
nity characteristics on 2nd day had greatly changed as compared with
those on the 0th and 1st day; the 2nd day was a transition stage. The
differences in the microbial community on the 4th day, 7th day, and
7
Environment International 134 (2020) 105300
11th day were small, indicating that the microbial community was
stable during this period. The changes of microbial community char-
acteristics were consistent with the temperature change and TCS de-
gradation law during the composting process.
A heatmap of the microbial communities (at the genus level) in the
seven samples is shown in Fig. 5. In the initial compost sample, the
dominant genera included Levilinea (22.92%), Stenotrophomonas
(7.64%), Amycolatopsis (6.16%), Kribbella (4.64%), Acinetobacter
(4.45%), Longilinea (2.82%), Emergencia (2.30%), Aciditerrimonas
(2.23%), and Terrimonas (2.19%). As the composting process began, the
microbial communities also changed. The dominant genera in the 1st
day compost sample were Stenotrophomonas (34.95%), Levilinea
(16.23%), Acinetobacter (15.51%), Petrimonas (6.25%), Thauera
(3.46%), Christensenella (1.52%), Longilinea (1.27%), and Amycolatopsis
(1.19%); and the dominant genera observed in the 2nd day compost
sample were Levilinea (14.47%), Tissierella (8.33%), Alkaliphilus
(4.58%), Pusillimonas (4.35%), Bacillus (3.62%), Massilibacterium
(2.29%), Comamonas (2.15%), Emergencia (1.97%), and Aciditerrimonas
(1.83%). The dominant genera and relative abundance in the 2nd day
compost sample were significantly different from those in the 0th day
and 1st day compost samples. In the 0–2 day phase (mesophilic period),
the microbial community was not stable; however, the degradation rate
of the TCS in this stage was higher. Therefore, the activity and abun-
dance of TCS degradation microorganisms were increased. The relative
abundance of Tissierella, Lascolabacillus, Alkalilimnicola, and Pusilli-
monas increased, and this effect was likely related to the degradation of
organic matter (including TCS). The degradation of TCS mainly oc-
curred in the mesophilic period, and in the early stage of the thermo-
philic period. The dominant microorganisms in the mesophilic period
are different from those of the thermophilic period. The dominant
genera in the 4th day compost sample were Levilinea (18.06%), Ae-
quorivita (6.15%), Tissierella (5.30%), Pusillimonas (4.98%), Dyadobacter
(3.38%), Truepera (3.32%), Lascolabacillus (3.25%), Emergencia
(2.99%), and Lutispora (2.77%). The microbial communities in the 4th
day compost sample had better diversity and abundance. The microbial
community characteristics showed few changes in the next period (7th
day and 11th day), after which the microbial community significantly
changed, as the composting process entered the cooling and ripening
stage (17th day). The changes in the relative abundance of Tissierella,
Lascolabacillus, Alkalilimnicola, and Pusillimonas were consistent with
the TCS degradation during the sewage sludge composting process; they
were considered as TCS degradation microorganisms in this study.
According to previous studies, Sphingomonas, Pseudomonas, and Novo-
sphingobium are found in sewage sludge, and they degrade TCS (Mulla
et al., 2016; Thelusmond et al., 2019). Pseudomonas was found in the
compost samples in this research, with relative abundances of 0.074%,
0.549%, 2.16%, 6.69%, and 0.347% on the 0th day, 2nd day, 7th day,
11th day, and 17th day, respectively. The relative abundance changed
with the compost process. The composting process benefited the en-
richment of Pseudomonas and enhanced the biodegradation of TCS.
Generally, there are many microorganisms that can degrade TCS. As the
organic components in sewage sludge are complex, there are many
microorganisms that could degrade organic matters, by means of direct
biodegradation or co-substrates. Different sources of sewage sludge
contain different degradation microorganisms for TCS. During the
composting process, the abundance of the dominant bacteria decreased
significantly in the cooling and ripening stage, indicating that they were
closely related to the degradation of organic matters (including TCS).
Thus, to determine the microorganisms related to TCS degradation, an
analysis of the functional genetics is necessary.
4. Conclusions
TCS was effectively removed through the different wastewater
treatment processes. Furthermore, sewage sludge became the new
pollutant source, as 36.4–49% of the TCS was transferred to the sludge.
G. Zheng, et al. Environment International 134 (2020) 105300

Fig. 5. Heatmap of microbial communities of medium ventilation compost at different times.

TCS in the sewage sludge may cause environmental pollution if applied Declaration of Competing Interest
to farmland; therefore, sewage sludge treatment is required before land
application. Aerobic composting was found to be an effective way to The authors declared that there is no conflict of interest.
degrade TCS in sewage sludge. It effectively sterilized and inactivated
TCS in the long thermophilic phase, thus ensuring the stability and Acknowledgments
safety of the compost products (within the national health standards).
The TCS was effectively degraded under different aeration conditions, This work was supported by the National Natural Science
and the degradation rate increased slightly with an increase in the Foundation of China (Grant Nos. 41371455 & 41101463) and the
aeration amount, owing to the enhancement of the oxygen content. National Science and Technology Major Project (2016ZX05040002-
Moreover, the composting process benefited the microbial activity, and 005-001).
increased the relative abundance of TCS-degrading microorganisms.
Future research is required on the functional microorganisms related to
Appendix A. Supplementary material
TCS degradation.

Supplementary data to this article can be found online at https://

doi.org/10.1016/j.envint.2019.105300.

8
G. Zheng, et al.
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