Organic Contaminants in Chinese Sewage Sludge - ACS Publications

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Organic Contaminants in Chinese Sewage Sludge: A Meta-Analysis of the Literature of the Past 30 Years Xiang-Zhou Meng,*,† Arjun K. Venkatesan,‡ Yi-Lin Ni,†,§ Joshua C. Steele,‡ Ling-Ling Wu,† Anders Bignert,∥ Åke Bergman,⊥ and Rolf U. Halden‡

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†

State Key Laboratory of Pollution Control and Resources Reuse, College of Environmental Science and Engineering, Tongji University, 1239 Siping Road, Shanghai 200092, China ‡ Biodesign Center for Environmental Security, The Biodesign Institute, Global Security Initiative and School of Sustainable Engineering and the Built Environment, Arizona State University, 781 E. Terrace Mall, Tempe 85287, United States § Department of Civil & Environmental Engineering, Imperial College London, London SW7 2AZ, U.K. ∥ Department of Environmental Research and Monitoring, Swedish Museum of Natural History, Bo 50007, Stockholm 104 05, Sweden ⊥ Swedish Toxicology Sciences Research Center (Swetox), Forskargatan 20, Södertälje 151 36, Sweden S Supporting Information *

ABSTRACT: The production of sewage sludge is increasing in China but with unsafe disposal practices, causing potential risk to human health and the environment. Using literature from the past 30 years (N = 159), we conducted a meta-analysis of organic contaminants (OCs) in Chinese sludge. Most data were available from developed and populated regions, and no data were found for Tibet. Since 1987, 35 classes of chemicals consisting of 749 individual compounds and 1 mixture have been analyzed, in which antibiotics and polycyclic aromatic hydrocarbons (PAHs) were the most targeted analytes. For 13 classes of principal OCs (defined as chemicals detected in over five studies) in sludge, the median (expressed in nanograms per gram dry weight) was the highest for phthalate esters (27 900), followed by alkylphenol polyethoxylates (12 000), synthetic musks (5800), antibiotics (4240), PAHs (3490), ultraviolet stabilizers (670), bisphenol analogs (160), organochlorine pesticides (110), polybrominated diphenyl ethers (100), pharmaceuticals (84), hormones (69), perfluorinated compounds (21), and polychlorinated biphenyls (15). Concentrations of PAHs in sludges collected between 1998 and 2012 showed a decreasing trend. Study findings suggest the need for a Chinese national sewage sludge survey to identify and regulate toxic OCs, ideally employing both targeted as well as nontargeted screening approaches.

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disposal. In 1986, the European Union (EU) issued its first sludge directive (86/278/EEC) to protect agricultural soils receiving sludge applications. Limits were established only for seven heavy metals. Similarly, based on the assessment method of 14 major exposure pathways and the extensive survey of sludge production, the United States developed “The Standards for the Use or Disposal of Sewage Sludge” (known as Part 503 Biosolids Rule) in 1993 to regulate heavy metals, pathogens, and vector attraction.14 Standards of OCs were not included in the Part 503 Biosolids Rule. China also issued the first regulation in 1984: Control Standards of Pollutants in Sludges from Agricultural Use (GB 4284-84); nevertheless, the human health and ecological risk assessment of OCs in sludge for land application is insufficient.15 Recently, concerns over OCs in

INTRODUCTION Sewage sludge, hereafter referred to as sludge, is a byproduct of wastewater treatment and a sink of many wastewater-borne organic contaminants (OCs). Meanwhile, sludge is a source of OCs to the environment. Significantly higher concentrations of OCs were frequently found in sludge-amended soils compared to reference soils,1−4 with a fraction of them accumulating in plant5,6 and animal tissues.7 Besides application on land, disposal options for sludge such as landfilling8 and incineration9 can also release sludge-borne OCs into the surrounding environment. As new chemicals have been introduced and chemical monitoring has intensified, more and more OCs have been detected in sludge in recent yearsthese contaminants are representative of synthetic and high-production volume organic chemicals used in consumer products and/or transformation products formed during wastewater treatment.10−13 Regulations on pollutants in sludge/biosolids have been set forth worldwide since 1980s, seeking to limit the risk to human health and the environment during sludge land application and © 2016 American Chemical Society

Received: Revised: Accepted: Published: 5454

November 12, 2015 April 24, 2016 May 4, 2016 May 4, 2016 DOI: 10.1021/acs.est.5b05583 Environ. Sci. Technol. 2016, 50, 5454−5466

Critical Review

Environmental Science & Technology sludge are growing, as a result of the increasing number and production of synthetic organic chemicals and the potential coincident exposure to multiple compounds, which usually were overlooked in previous risk assessments.16,17 Understanding levels and trends of OCs in sludge is necessary for assessing the potential risk to human health and the environment. The United States Environmental Protection Agency (USEPA) has conducted four nationwide surveys in 1982, 1988, 2001, and 2006−2007, with the purpose of identifying and quantifying contaminants in sludge.18 The latest survey investigated 4 polycyclic aromatic hydrocarbons (PAHs), 2 semivolatiles, 11 flame retardants, 72 pharmaceuticals, and 25 steroids and hormones in 84 sludge samples collected from 74 selected publicly owned treatment works (POTWs) in 35 states. In 2011, the European Commission’s Joint Research Centre screened European sludges for 92 OCs, including ingredients of personal care products and pharmaceuticals; the 63 samples examined mostly had been taken as grab samples and originated from 15 European countries.19 Similar work also has been done in the United Kingdom,20 Denmark,21 and Australia.22 However, no national survey on pollutants in sludge has been carried out in China yet. With the rapid economic development in China and its status as the world’s most populous nation, the discharge of treated wastewater has increased considerably. In 1990, the volume of wastewater was 35.4 billion metric tons, including 24.9 billion metric tons industrial wastewater and 10.5 billion metric tons domestic wastewater. However, the total volume of wastewater in 2013 reached to 69.5 billion metric tons, generating 6.25 million dry metric tons of sludge equivalent to ∼4.5 kg/person·y.23 However, over 80% of this sludge has not been disposed of safely in China, which poses a potential, currently ill-defined threat to both human health and the environment.23,24 Moreover, industrial wastewater is commonly combined with domestic wastewater prior to treatment, contributing as much as 35% of the total wastewater discharge.24 Compared to heavy metals,25 less attention has been paid to OCs in Chinese sludge. Relevant studies are scattered and there is no clear understanding of the organic contamination burden in sludge from China, given that the production amount is vast and most sludges are handled and disposed of unsafely. Finally, some of the data were published exclusively in the Chinese language, making it largely unavailable to international readers. In this study, we present the first systematic review and a meta-analysis of OCs in Chinese sludge based on the literature published over the past 30 years. The objectives were to (i) examine the temporal and spatial distributions of all previous work, (ii) reveal the identity and concentration of important and abundant OCs in Chinese sludge, and (iii) assess the potential need for conducting a Chinese national sewage sludge survey.

Table 1. Classes of Organic Contaminants (OCs) Analyzed in Chinese Sewage Sludge over the Past 30 Yearsa compound class antibiotics alkylphenol polyethoxylates aromatic amines azole antifungals bisphenol analogs chlorinated hydrocarbons dechlorane plus hexabromocyclododecanes hormones hydroxylated polybrominated diphenyl ethers methoxylated polybrominated diphenyl ethers nitrogen-heterocyclic compounds novel brominated flame retardants organochlorine pesticides organometals organophosphate esters parabens perfluorinated compounds pharmaceuticals phenolic compounds phthalate esters polybrominated diphenyl ethers polychlorinated biphenyls polychlorinated dibenzo-p-dioxins and dibenzofurans polychlorinated naphthalenes polycyclic aromatic hydrocarbons quaternary ammonium compounds short chain chlorinated paraffins siloxanes substituted polycyclic aromatic hydrocarbons synthetic musks synthetic phenolic antioxidants triclosan and triclocarban ultraviolet stabilizers volatile aromatic hydrocarbons a

abbreviation

N

n

antibiotics APEOs AAs AAFs BPAs CHCs DPs HBCDs hormones OH-PBDEs

25 14 2 4 11 2 2 2 12 1

86 27 31 7 13 6 7 4 40 9

MeO-PBDEs

1

9

NHCs N-BFRs OCPs organometals OPs parabens PFCs pharmaceuticals PCs PAEs PBDEs PCBs PCDD/Fs

1 1 7 1 2 1 12 9 1 9 15 10 4

34 12 17 5 7 4 59 22 16 16 48 43 17

PCNs PAHs QACs SCCPs siloxanes S-PAHs

4 24 2 3 3 2

75 17 27 mixture 19 13

SMs SPAs TCS + TCC UV stabilizers VAHs

16 1 3 5 3

9 15 2 20 13

N: number of studies. n: number of compounds in each class of OCs.

Supporting Information (SI). The initial search yielded 1679 publications, of which 536 and 1143 publications were found in the WoK database and the CAJD, respectively. Subsequently, we examined these publications individually and further eliminated the duplicate and irrelevant articles, such as the studies focusing on industrial sludge, removal technologies of contaminants in sludge, and sludge disposal processes. In the end, 159 relevant papers were selected for the meta-analysis. Data were extracted from the selected papers to develop a database, including compound name, sampling location, concentration, and reference information, which can be obtained upon request. Data Analysis. Table 1 summarized the names and abbreviations for 35 classes of compounds. More detailed information can be obtained from Table S1. The class of pharmaceuticals refers to all kinds of drugs used to improve human and animal health with the notable exception of antibiotics. Generally, mean concentrations were either provided by authors or calculated as needed using original

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METHODOLOGY Search Strategy. Frequently detected OCs in the environment were categorized into 35 classes for this study. The full names and abbreviations of contaminants considered are shown in Table 1. The literature survey was conducted via searching of the Web of Knowledge (WoK) publications database (http:// apps.isiknowledge.com/) and the China Academic Journal Network Publishing Database (CAJD; http://oversea.cnki.net/) until September 30, 2015. The detailed search terms and strategy were presented in the 5455

DOI: 10.1021/acs.est.5b05583 Environ. Sci. Technol. 2016, 50, 5454−5466

Critical Review

Environmental Science & Technology

Figure 1. Number of publications on organic contaminants in Chinese sewage sludge per year. (inset) Percentages of publications in English and Chinese during 1987−2015. (*) The number of publications of the full year of 2015 was estimated based on the count in the first 9 months.

Figure 2. National distribution of (a) the number of studies detecting at least one organic contaminant in Chinese sewage sludge, (b) the gross regional product (GRP; USD/y per capita and RMB/y per capita), and (c) the population density (people per square kilometer) by province or municipality in China.

data. Both nondetects and concentrations below detection limit were assigned a value of zero due to inconsistent detection limits reported, even for the same compound in different studies. Depending on the concentration range of each compound, levels were recorded in the database as either nanograms per gram (ng/g) or micrograms per gram (μg/g) on a dry weight (dw) basis.

Data on the number of wastewater treatment plants, the discharge of wastewater, the gross domestic product (GDP), the gross regional product (GRP), and the total investment on environmental production were extracted from the Annual Report of the Ministry of Housing and Urban-Rural Development of China, China Statistical Yearbook on Environment, 5456


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pattern of distribution (Figure 2). Beijing, Shanghai, and Guangdong Province, three of the most developed and populated areas of China, have the largest number of studies (i.e., 66, 46, and 46, respectively). Generally, fewer sludge samples were collected from the northern, southern, and western regions than those from the east and central regions of China. For example, only three or four studies were conducted in Jilin Province, the Guangxi Zhuang Autonomous Region, Hainan Province, Guizhou Province, and the Ningxia Hui Autonomous Region. To date, no sludge has been sampled from the Tibet Autonomous Region, although due to its high elevation it has fundamental significance to the environment of China, Asia, and the world.31 The Tibet Autonomous Region built its first WWTP in 2011 with a daily sewage treatment capacity of 50 000 m3. For the 2 Special Administrative Regions of China, 11 studies were conducted in Hong Kong, whereas no samples have been analyzed from Macau. The study distribution, per capita GRP, and population density throughout China were compared to find patterns (Figure 2). Provinces or municipalities along the coastal areas of China (eastern region), such as Shanghai, Jiangsu Province, Zhejiang Province, and Guangdong Province, have the highest GRP and population density and the greatest number of sludge studies. In contrast, the sparsely populated western region featured the lowest GRP and fewest number of studies performed. To further explore the relationship among the three distributions, a two-tailed Spearman correlation analysis was performed (Table S2). Hong Kong and Macau were excluded due to their different administrative systems. As expected, a positive albeit moderate relationship was found between the number of studies and the per capita GRP of all provinces and municipalities of China. The correlation coefficient (r) was 0.51 with a corresponding p value of 0.003. Similarly, a moderate but significant positive relationship was obtained between the number of studies and the population density (correlation coefficient: r = 0.59; p < 0.001). These observations suggest that continued investment in the environmental sector will foster much needed future research into the composition of and safe disposal options for sludge in China. Coverage of OCs in Sludge. Thirty-five classes of organic contaminants, including 749 individual compounds and 1 mixture (short chain chlorinated paraffins (SCCPs); generally reported in mixture), have been analyzed in Chinese sludge since 1987 (Figure 3 and Table S1). Some targeted OCs originated from the residuals of various commercial products with wide applications, such as antibiotics, pharmaceuticals,

China Statistical Yearbook, China Environment Bulletin, and a reference.26 A two-tailed Spearman correlation analysis was performed to determine the relationship among the study distribution, per capita GRP, and population density throughout China. Comparisons of the concentrations of PAHs in sludges sampled from different periods were examined using either Mann− Whitney U (in two groups of samples) or Kruskal−Wallis H (in more than two groups of samples), both of which are nonparametric tests. All statistical analyses were conducted using SPSS (Version 18.0, Chicago, IL, USA) with a significance level of p = 0.05. A Bonferroni-adjusted significance level of 0.0125 was applied for the repeated Mann−Whitney U test.

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RESULTS AND DISCUSSION Temporal Distribution of Sludge Studies. A total of 159 papers on OCs in Chinese sludge have been published since 1987 (Figure 1). Approximately 65% of available studies were published in English journals, a positive development facilitating sharing of information internationally. The first sludge study appeared in 1987 in a Chinese journal, identifying 35 nitrogen-heterocyclic compounds (NHCs) in five sludge samples from a secondary wastewater treatment plant (WWTP) in Beijing, in which seven compounds were quantitatively analyzed.27 For the next 13 years (1988−2000), no publications were found in our search. In 2005, a paper published in English investigated patterns and levels of six synthetic musks (SMs) in sludge from Guangdong Province, South China.28 Starting in 2004, at least two publications appeared every year with new information on contaminant levels in sludge. An increasing number of publications per year was observed, with three main periods identified: less than 5 papers annually in period I (1987−2006), approximately 10 per year in period II (2007−2010), and approximately 20 annually thereafter in period III (2011−2015). Only one paper was presented in English in period I, contributing 7% of the total in that period. However, the ratio of English papers to the total number of papers has grown significantly since 2007, increasing to 49% and 80% in periods II and III, respectively. The observed rapid increase of studies on OCs in Chinese sludge could be related to the growth of investment in environmental protection. China increased investment in environmental projects with an average annual growth rate of 19% during the last three decades, and the investment reached 951 billion Chinese Yuan (148 billion current USD) in 2013 (Figure S1). The corresponding proportion (ratio of investment to gross domestic production) has been steadily increasing, from 0.5% in 1981 to 1.6% in 2013. Improvements in analytical technologies also represent a driving force for increased publication activity. Sludge is a complicated matrix with abundant organic matter, which is a challenge for sample pretreatment and subsequent instrumental analysis. However, extensive applications of hyphenated methods in environmental analysis, including advanced gas chromatography and liquid chromatography coupled to mass spectrometry and tandem mass spectrometry (GC-MS/MS) and (LC-MS/MS), have broadened the list of formally targeted compounds, exploring nontargeted chemicals and increasing the reliability of quantitative measurements.29,30 Spatial Distribution of Sludge Sampling Sites. Among 159 studies, sludge samples were collected from different provinces and municipalities of China, showing an uneven

Figure 3. Percentages of organohalogen contaminants analyzed in Chinese sewage sludge. F-R: fluorinated compounds. Cl-R: chlorinated compounds. Br-R: brominated compounds. N: the number of individual organic contaminants analyzed. 5457


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Environmental Science & Technology personal care products, pesticides, flame retardants, plasticizers, antioxidants, solvents, surfactants, and thermal stabilizers. Others, including hydroxylated polybrominated diphenyl ethers (OH-PBDEs), methoxylated polybrominated diphenyl ethers (MeO-PBDEs), polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), PAHs, and substituted polycyclic aromatic hydrocarbons (S-PAHs), were generated unintentionally during the manufacture, usage, and disposal of commercial products, and even in household cooking. Excluding SCCPs, approximately 54% of analytes contain at least one halogen atom (chlorine, bromine, or fluorine), and can be categorized as organohalogen contaminants (OHCs). As global environmental pollutants, the OHCs have raised concern because they can be highly persistent, bioaccumulative, and have adverse effects on humans and wildlife.32 Although the production and usage of several old OHCs (e.g., polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs)) were banned almost four decades ago, they still remain ubiquitous in the environment worldwide, including remote regions.33,34 Moreover, new OHCs (e.g., polybrominated diphenyl ethers (PBDEs) and perfluorinated compounds (PFCs)) continue to be discovered in aquatic and terrestrial ecosystems and have recently been considered as emerging OCs.32−34 In Chinese sludge, 228 chlorinated, 103 brominated, and 83 fluorinated OHCs have been screened in sludge in the past three decades, accounting for 30%, 13%, and 11% of the total analytes, respectively (Figure 3). Twelve OHCs have two different halogen atoms. For example, an alternative to perfluorooctanesulfonate in the electroplating industry, 6:2 chlorinated polyfluorinated ether sulfonate (6:2 Cl-PFAES) as well as its homologues 8:2 and 10:2 Cl-PFAESs were recently identified in municipal sludge samples of China.35 Over the past 30 years, antibiotics36−60 and PAHs61−84 were the most commonly studied OCs in Chinese sludge with 25 and 24 publications, respectively (Figure 4 and Tables S1 and S3). Antibiotics are a group of emerging OCs that have received considerable attention in recent years. Alkylphenol polyethoxylates (APEOs), 6 2, 85 −97 bisphenol analogs (BPAs), 6 2 , 8 6 , 9 0 , 9 2 , 9 6 − 1 0 2 hormones, 9 0 , 9 2 , 9 6 − 1 0 0 , 1 0 2 − 1 0 6 OCPs, 62 , 6 5 , 67 , 8 1, 1 0 7 −1 0 9 PFCs, 3 5, 1 1 0 −1 20 pharmaceuticals,45,49,53−55,57,98,121,122 phthalate esters (PAEs),62,123−130 PBDEs,109,131−144 PCBs,62,65,67,77,80,81,107,145−147 SMs,28,78,148−161 and ultraviolet stabilizers (UV stabilizers)2,162−165 were each found in more than five studies. However, some OCs have been monitored infrequently, with only one or two studies being available on the occurrence in Chinese sludge: chlorinated hydrocarbons (CHCs),131,166 OHPBDEs,137 MeO-PBDEs,137 NHCs,27 novel brominated flame retardants (N-BFRs),167 organometals,168 organophosphate esters (OPs), 169,170 parabens, 98 phenolic compounds (PCs),96,171 quaternary ammonium compounds (QACs),172,173 and S-PAHs.82,174 PAHs and antibiotics were first detected in sludge in 200161 and 2007,36 respectively. Since then, they have been investigated in Chinese sludge almost every year, indicating their frequent detection and researchers’ concern for them (Table S3). The occurrence of other old pollutants, such as APEOs,85 BPAs,62 OCPs,131 PAEs,123 PCBs,62 PCDD/Fs,62 and polychlorinated naphthalenes (PCNs),131 were reported before the year 2006. Since 2010, numerous emerging OCs have raised attention, including dechlorane plus (DPs),64 hexabromocyclododecanes (HBCDs),175 N-BFRs,167 OPs,169 parabens,98 PFCs,110 pharmaceuticals,121 PBDEs,131 QACs,173

Figure 4. Concentrations of organic contaminants (OCs) detected in Chinese sewage sludge (median and 95% confidence interval; ng/g dry weight (dw)). The first and second numbers in parentheses indicate the counts of studies and compounds of each class of OCs, respectively. ppm: parts per million. ppb: parts per billion. ppt: parts per trillion; −: mixture.

SCCPs, 176 siloxanes, 177 synthetic phenolic antioxidants (SPAs),178 triclosan and triclocarban (TCS + TCC),179 UV stabilizers,162 and metabolites of PBDEs137 and PAHs.174 Level and Profile of OCs in Sludge. Based on median concentrations, 34 classes of contaminants were ranked in decreasing order, as shown in Figure 4. MeO-PBDEs were excluded due to a lack of detection in 36 sludge samples from 27 cities throughout China.137 The medians of 16 classes of contaminants, including antibiotics, APEOs, aromatic amines (AAs), azole antifungals (AAFs), CHCs, organometals, PCs, PAEs, PAHs, QACs, SCCPs, siloxanes, S-PAHs, SMs, SPAs, and TCS + TCC were higher than 1 μg/g dw (parts per million or ppm). For the other 16 classes, BPAs, DPs, HBCDs, hormones, NHCs, N-BFRs, OCPs, OPs, parabens, PFCs, pharmaceuticals, PBDEs, PCBs, PCNs, UV stabilizers, and volatile aromatic hydrocarbons (VAHs) the levels fall into a range from lower ng/g dw (parts per billion; ppb) to μg/g dw (ppm). OH-PBDEs and PCDD/Fs were frequently detected in sludge, while occurring in relatively lower concentrations of less than 1 ng/g dw. Notably large variations in concentrations were found (expressed as 95% confidence intervals) for most of the compounds, which could be related to the limited number of studies, inconsistent targets, different sampling strategies and/ or different sampling times (Figure 4). Thirteen classes of contaminants found in over five studies were chosen as “principal OCs” in Chinese sludge. Table 2 5458


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Environmental Science & Technology Table 2. Concentrations of Principal Organic Contaminants in Chinese Sewage Sludge (ng/g dry weight)a

a

compound class

N

minimum

mean

median

maximum

ref

antibiotics alkylphenol polyethoxylates (APEOs) bisphenol analogs (BPAs) hormones organochlorine pesticides (OCPs) perfluorinated compounds (PFCs) pharmaceuticals phthalate esters (PAEs) polybrominated diphenyl ethers (PBDEs) polychlorinated biphenyls (PCBs) polycyclic aromatic hydrocarbons (PAHs) synthetic musks (SMs) ultraviolet stabilizers (UV stabilizers)

25 14 11 12 7 12 9 9 15 10 24 16 5

0.83 ND 34.6 ND 9.0 ND ND 680 3.46 3.14 100 ND 288

8390 887000 10500 178 327 796 482 48400 1020 81 15900 8320 1040

4240 12000 160 69 110 21 84 27900 100 15 3490 5800 670

38700 33810000 127000 981 3200 9980 4460 282000 7100 1400 170000 33200 2330

36−60 62, 85−97 62, 86, 90, 92, 96−102 90, 92, 96−100, 102−106 62, 65, 67, 81, 107−109 35, 110−120 45, 49, 53−55, 57, 98, 121, 122 62, 123−130 109, 131−144 62, 65, 67, 77, 80, 81, 107, 145−147 61−84 28, 78, 148−161 2, 162−165

N: number of studies. ND: not detected.

summarized their detailed concentration information. The levels of PAEs were the highest, with a median in units of ng/g dw of 27 900, followed by APEOs (12 000), SMs (5800), antibiotics (4240), PAHs (3490), UV stabilizers (670), BPAs (160), OCPs (110), PBDEs (100), pharmaceuticals (84), hormones (69), PFCs (21), and PCBs (15). As for the individual compounds, di(2-ethylhexyl) phthalate (6630) and dibutyl phthalate (1180) were two predominant PAEs. Similarly, the abundant and representative compounds were determined for eight other principal OCs: 4-nonylphenol monoethoxylate (6830) and 4-nonylphenol (3140) for APEOs, galaxolide (3860), and tonalide (1400) for SMs, phenanthrene (280) and fluoranthene (260) for PAHs, 2-[3′,5′-bis(1-methyl1-phenylethyl)-2′-hydroxyphenyl]benzotriazole (340) and 2(2-hydroxy-3,5-dipenryl-phenyl)benzotriazole (310) for UV stabilizers, bisphenol A (160) for BPAs, p,p′-dichlorodiphenyldichloroethylene (52) and hexachlorobenzene (17) for OCPs, decabromodiphenyl ether (78) and 2,2′,4,4′,5-pentabromodiphenyl ether (4.6) for PBDEs, and 2,4,4′-trichlorobiphenyl (5.4) and 2,2′,5,5′-tetrachlorobiphenyl (0.4) for PCBs. Here no abundant compounds were shown for antibiotics, pharmaceuticals, hormones, and PFCs because of the large variety of analytes in different studies. Variation of PAH Concentrations and Regulations. Due to limited data for most OCs in Chinese sludge, the variation of concentrations in different years was examined only for PAHs. Among all studies concerning PAHs (N = 24), 20 of them targeted 16 priority pollutants specified by the USEPA and subsequently were selected to study the temporal variation.61−64,66,68,69,71,72,74−84 The sum concentration of these 16 PAHs was compiled into four periods per the sampling years mentioned above (Figure 5). If the sampling time was not provided in the paper, it was assumed that the samples were collected three years before the publication date of the paper. It is interesting to note that a significant difference was observed among samples collected from the four periods (Kruskal−Wallis H test; p = 0.001). Overall, the median PAH concentration in Chinese sludge showed a decreasing trend: from 15 700 ng/g dw in 1998−2000, 13 100 ng/g dw in 2001− 2005, 2360 ng/g dw in 2006−2010, to 3000 ng/g ng in 2011− 2012. Moreover, the sludge sampled from 2006 to 2010 contained significantly lower PAHs than those from the periods of 1998−2000 and 2001−2005 (Mann−Whitney U test; p = 0.005 and 0.001, respectively). However, no significant changes of PAHs were found in samples from other periods, including

Figure 5. Concentrations of polycyclic aromatic hydrocarbons (PAHs) in Chinese sewage sludge sampled from different years (median and 95% confidence interval; ng/g dry weight (dw)). Classes A and B refer to the sludge with different disposals classified by the Chinese Standard (CJ/T 309-2009). The blue and red dash lines refer to the maximum tolerance concentration (MTC) of PAHs for Class A (5000 ng/g dw) and Class B sludge (6000 ng/g dw), respectively. Medians with different letters are significantly different (p < 0.05). N: number of studies.

1998−2000 vs 2001−2005 (p = 0.559), 1998−2000 vs 2011− 2012 (p = 0.068), 2001−2005 vs 2011−2012 (p = 0.086), and 2006−2010 vs 2011−2012 (p = 0.577) (Figure 5). Similar decreasing trends of PAHs were also reported in sediment cores taken from the East China Sea,180 the Yellow Sea, and the South China Sea, China.181 The gradual decline in levels observed in recent sludge samples may contribute to the reduction of PAH emissions due to the replacement of domestic coal and biomass combustion by natural gas or petroleum since the 1990s in China.182 In 2009, China issued a sludge standard (CJ/T 309-2009) that regulated the maximum tolerance concentration (MTC) for PAHs: 5000 ng/g dw for Class A sludge (used in agricultural soils) and Class B sludge (used in agricultural soils not for vegetable and cereal production). In 2011, another standard (CJ/T 362-2011) was established that set an MTC of 6000 ng/g dw for PAHs in sludge applied in forestland. The medians of PAHs in sludge from 1998 to 2000 and 2001−2005 would not have met the current MTC standards, but sludge 5459


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Figure 6. Timeline of regulatory standards of sewage sludge in China. GB: Mandatory National Standards. GB/T: Voluntary National Standards. CJ: Mandatory Standards issued by the Ministry of Housing and Urban-Rural Development of China. CJ/T: Voluntary Standards issued by the Ministry of Housing and Urban-Rural Development of China.

Approximately 60% of WWTPs were located in cities, and others in counties or towns (Table S6). In addition, many industrial plants were relocated from capital cities to rural areas with the rapid urbanization of China. Therefore, more and more production of industrial wastewater could be expected in rural areas (Table S7). Second, the scale of WWTPs and the treatment process employed: generally, medium-scale WWTPs (10 000−100 000 t of wastewater per day) are common in China, accounting for 75% of the total. Only 3% of superlarge-scale WWTPs (>300 000 t per day) were built in big cities.183 More than 10 different treatment processes can be found in WWTPs of China with varying chemical oxygen demand removal efficiencies, of which the oxidation ditch, the anaerobic/ anoxic/oxic and the sequencing batch reactor are the mainstream technologies.183 Third, the sample size and type: the aim of monitoring should ideally be to characterize all of the target WWTPs, and hence all the facilities in the sample frame should have a known, nonzero chance of selection. The USEPA used a probabilistic method for estimating sample size.18 A minimum sample size of 80 POTWs was determined to represent the total number of facilities in the sample frame (3337 POTWs).184 Additionally, taking sludge from different sampling points in a WWTP to form a composite sample is better than nonrepeated grab sampling, although the latter has often been used in previous studies.35,173,185 Selection of Analytes. As mentioned above, a total of 749 organic compounds and 1 mixture have been monitored in Chinese sludge to date. However, it is not possible to prioritize these chemicals based on the data derived from the previous studies. More comprehensive and comparable data are essential to make a systematic risk assessment to human health and the environment for OCs in sludge of China. Moreover, there are other chemicals that need to be considered and/or regulated, especially those being produced and consumed in large volumes. For example, PAEs are a group of industrial chemicals that have been widely used as polymer plasticizers since the early 20th century. The global annual production of PAEs was around 6.2 million metric tons in 2009, of which around 18% was produced and 24% was consumed in China.128 Di(2-ethylhexyl) phthalate (mean: 97 400 ng/g dw) and dibutyl phthalate (mean: 22 400 ng/g dw) were typically found in high concentrations in sludge samples collected from

from 2006 to 2010 and 2011−2012 are below the MTCs, suggesting Chinese sludge currently passes PAH regulation (Figure 5). China has developed sludge standards for other OCs as well, aiming to protect human health and the environment (Figure 6 and Table S4). The first regulation was issued in 1984, in which the MTC of benzo[a]pyrene is 3 μg/g dw when sludge is applied in agricultural soils with an application rate of 30 t/ha·y (Table S5). In 2002, another standard (GB 18918-2002) set MTCs not only for benzo[a]pyrene (B(a)P; 3 μg/g dw) but also for PCDD/Fs (100 ng TEQ/kg dw), PCBs (0.2 μg/g dw), and adsorbable organic halogens (AOX; calculated by chlorine; 500 μg/g dw), given that sludge is used in agricultural soils with the above application rate. Based on different sludge disposals, several specific standards have been issued recently (Figure 4 and Tables S4 and S5). More OCs are regulated for sludge applied to soil than for that used in co-landfilling as cover material and in making bricks. Only standards for volatile phenolic compounds (VPCs; MTC: 40 μg/g dw) were proposed in sludge with aims to co-landfill (CJ/T 249-2007 and GB/T 23485-2009) or make bricks (CJ/T 289-2008 and GB/T 25031-2010). It is worthwhile to note that the scientific methodology used for calculating MTCs is insufficient in China.23 Need for a National Sewage Sludge Survey in China. Although a significant increase in the number of sludge studies is observed, two aspects on OCs in Chinese sludge are rarely considered. One is the sampling of sludge samples: the collection has been unsystematic in the past and lacks nationwide representativeness.56,163,168 Another is that current studies only target select analytes and chemicals classes at different points in time. Therefore, to systemically assess the risk to human health and the environment for OCs in Chinese sludge, it is necessary to conduct a national survey. Representativeness of Sludge Samples. Several aspects should be examined when choosing appropriate WWTPs to represent pollution control infrastructure in China (3802 WWTPs were in operation as of June 2015) (Table S6). First, the geographic distribution of WWTPs: the discharge volumes of industrial and domestic wastewater, and the number and treatment capacity of WWTPs are unequal in different provinces and municipalities of China.183 Most WWTPs were constructed in the eastern region, especially the coastal areas that have the highest GRP and the highest population density. 5460


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Control and Treatment (No. 2012ZX07313001), the Program for New Century Excellent Talents in University (No. NCET12-0417), the China Scholarship Council, the Collaborative Innovation Center for Regional Environmental Quality, and the Virginia G. Piper Charitable Trust (LTR 05/01/12).

Shanghai compared with other pollutants like PBDEs, DPs, and PFCs (mean: 6.0−2400 ng/g dw).116,128,135,140,185 The EU proposed an MTC for di(2-ethylhexyl) phthalate (100 000 ng/ g dw) in sludge applied to soil, and that MTC is very close to the mean value found in Shanghai samples (97 400 ng/g dw). The MTC for 4-nonylphenol (50 000 ng/g dw), an abundant chemical found in Chinese sludge, was also proposed in the third draft of the EU Sludge Directive.29 By contrast, no similar initiative was implemented in China. Furthermore, using high resolution mass spectrometry combined with nontargeted screening strategy, suspected and unknown contaminants can be identified and quantified in environmental samples.186−188 For example, employing liquid chromatography coupled to a quadrupole-time-of-flight mass spectrometer (LC-QTOF-MS), Gago-Ferrero et al. tentatively identified 13 of 284 predicted and literature metabolites of selected pharmaceuticals and nicotine in influent samples from Athens, 7 of which were finally confirmed with reference standards. They also found 34 nontargeted compounds and 4 of them were confirmed.188 With the targeted and nontargeted screening, as well as the unbiased sampling, a national survey on OCs in Chinese sludge could be conducted. Subsequently, according to their production volumes, concentrations in the environment, environmental persistence, and potential toxicities, all detected compounds should be ranked in a list of Chinese priority OCs. The findings and database of this study could serve as a useful tool for researchers, policy makers, and industry professionals. By using sludge as a suitable matrix for capturing human activities and ecological impacts, more knowledge will result from monitoring geographic and temporal trends of OCs in sludge, in the environment,189,190 and ultimately in human populations.191

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b05583. Additional tables contain a summary of compounds analyzed in Chinese sewage sludge, the Spearman correlation analyses between the number of studies and per capita gross regional product and population density, the class of organic contaminants analyzed per year, regulations on sewage sludge, the maximum tolerance concentration of organic contaminants in sewage sludge, the numbers of wastewater treatment plants, and the discharge of industrial and domestic wastewater. An additional figure contains the total investment on environmental research and the proportion of investment to gross domestic product (PDF)

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*Tel./fax: +86 21 65984261. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The present study was financially supported by the National Natural Science Foundation of China (No. 21437004), the Swedish Research Council (contract Dnr. 639-2013-6913), the Major Science and Technology Program for Water Pollution 5461


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Organic Contaminants in Chinese Sewage Sludge - ACS Publications

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