Organic Contaminants in Chinese Sewage Sludge: A Meta-Analysis of

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Organic Contaminants in Chinese Sewage Sludge: A Meta-Analysis of Literature of the Past 30 Years Xiang-Zhou Meng, Arjun K. Venkatesan, Yi-Lin Ni, Joshua C. Steele, Ling-Ling Wu, Anders Bignert, Ake Bergman, and Rolf U Halden Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 04 May 2016 Downloaded from http://pubs.acs.org on May 4, 2016

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Organic Contaminants in Chinese Sewage Sludge:

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A Meta-Analysis of Literature of the Past 30 Years

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Xiang-Zhou Meng†,*, Arjun K. Venkatesan‡, Yi-Lin Ni†,§, Joshua C. Steele‡, Ling-Ling Wu†,

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Anders Bignert║, Åke Bergman¥, Rolf U. Halden‡

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†

Science and Engineering, Tongji University, 1239 Siping Road, Shanghai 200092, China

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State Key Laboratory of Pollution Control and Resources Reuse, College of Environmental

‡

Center for Environmental Security, The Biodesign Institute, Global Security Initiative and

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School of Sustainable Engineering and the Built Environment, Arizona State University,

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781 E. Terrace Mall, Tempe 85287, USA

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§

2AZ, UK

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║

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Department of Environmental Research and Monitoring, Swedish Museum of Natural History, Bo 50007, Stockholm104 05, Sweden

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Department of Civil & Environmental Engineering, Imperial College London, London SW7

¥

Swedish Toxicology Sciences Research Center (Swetox), Forskargatan 20, Södertälje 151 36, Sweden

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1


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ABSTRACT: The production of sewage sludge is increasing in China but with unsafe

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disposal practices, causing potential risk to human health and the environment. Using

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literature from the past 30 years (N = 159), we conducted a meta-analysis of organic

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contaminants (OCs) in Chinese sludge. Most data were available from developed and

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populated regions, and no data were found for Tibet. Since 1987, 35 classes of chemicals

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consisting of 749 individual compounds and one mixture have been analyzed, in which

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antibiotics and polycyclic aromatic hydrocarbons (PAHs) were the most targeted analytes.

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For 13 classes of principal OCs (defined as chemicals detected in over five studies) in sludge,

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the median (expressed in ng/g dry weight) was the highest for phthalate esters (27,900),

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followed by alkylphenol polyethoxylates (12,000), synthetic musks (5800), antibiotics (4240),

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polycyclic aromatic hydrocarbons (3490), ultraviolet stabilizers (670), bisphenol analogs

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(160), organochlorine pesticides (110), polybrominated diphenyl ethers (100),

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pharmaceuticals (84), hormones (69), perfluorinated compounds (21), and polychlorinated

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biphenyls (15). The concentrations of PAHs in samples taken since 1998 featured a

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decreasing trend. Study findings suggest the need for a Chinese national sludge survey to

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identify and regulate toxic OCs, ideally employing both targeted as well as non-targeted

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screening approaches.

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INTRODUCTION

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Sewage sludge, hereafter referred to as sludge, is a byproduct of wastewater treatment

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and a sink of many wastewater-borne organic contaminants (OCs). Meanwhile, sludge is a

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source of OCs to the environment. Significantly higher concentrations of OCs were

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frequently found in sludge-amended soils compared to reference soils,1-4 with a fraction of

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them accumulating in plant5,6 and animal tissues.7 Besides application on land, disposal

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options for sludge such as landfilling8 and incineration9 can also release sludge-borne OCs

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into the surrounding environment. As new chemical introduction and intensified chemical

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monitoring, more and more OCs have been detected in sludge in recent years – these

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contaminants are representative of synthetic and high-production volume organic chemicals

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used in consumer products and/or transformation products formed during wastewater

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treatment.10-13

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Regulations on pollutants in sludge/biosolids have been set forth worldwide since 1980s,

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seeking to limit the risk to human health and the environment during sludge land application

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and disposal. In 1986, the European Union (EU) issued its first sludge directive

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(86/278/EEC) to protect soil environment when sludge is used in agriculture. The low limits

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were established only for seven heavy metals. Similarly, adopted the pre-cautionary principle

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and based on the assessment method of 14 major exposure pathways and the extensive survey

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of sludge production, the United States developed “The Standards for the Use or Disposal of

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Sewage Sludge” (known as Part 503 Biosolids Rule) in 1993 to regulate heavy metals,

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pathogens, and vector attraction.14 The standards of OCs were excluded from the Part 503

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Biosolids Rule considering their low concentrations in sludge and no significant risks to 3


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public health or the environment. China also issued the first regulation in 1984: Control

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Standards of Pollutants in Sludges from Agricultural Use (GB 4284-84); nevertheless, the

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human health and ecological risk assessment of OCs in sludge for land application is

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insufficient.15 Recently, concerns on OCs in sludge are growing, as a result of the increasing

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number and production of synthetic organic chemicals and the potential coincident exposure

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to multiple compounds, which usually were overlooked in the previous risk assessment.16,17

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Understanding levels and trends of OCs in sludge is necessary for assessing the potential

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risk to human health and the environment. The United States Environmental Protection

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Agency (USEPA) has conducted four nationwide surveys in 1982, 1988, 2001, and

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2006-2007, with the purpose of identifying and quantifying contaminants in sludge.18 The

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latest survey investigated four polycyclic aromatic hydrocarbons (PAHs), two semi-volatiles,

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11 flame retardants, 72 pharmaceuticals, and 25 steroids and hormones in 84 sludge samples

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collected from 74 selected publicly owned treatment works (POTWs) in 35 states. In 2011,

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the European Commission’s Joint Research Centre screened European sludges for 92 OCs,

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including ingredients of personal care products and pharmaceuticals; the 63 samples

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examined mostly had been taken as grab samples and originated from 15 European

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countries.19 Similar work also has been done in the United Kingdom,20 Denmark,21 and

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Australia.22

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However, no national survey on pollutants in sludge has been carried out in China at

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present. With the rapid economic development in China and its status as the world’s most

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populous nation, the discharge of treated wastewater has increased considerably. In 1990, the

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volume of wastewater was 35.4 billion metric tons, including 24.9 billion metric tons 4



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industrial wastewater and 10.5 billion metric tons domestic wastewater. However, the total

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volume of wastewater in 2013 reached to 69.5 billion metric tons, generating 6.25 million dry

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metric tons of sludge equivalent to ~4.5 kg/person/year.23 However, over 80% of this sludge

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has not been disposed of safely in China, which poses a potential, currently ill-defined threat

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to both human health and the environment.23,24 Moreover, industrial wastewater is commonly

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combined with domestic wastewater prior to treatment, contributing as much as 35% of the

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total wastewater discharge.24 Compared to heavy metals,25 less attention has been paid to

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OCs in Chinese sludge. Relevant studies are scattered and there is no clear understanding of

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the organic contamination burden in sludge from China, given that the production amount is

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vast and most sludge are handled and disposed of unsafely. Finally, some of the data were

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published exclusively in the Chinese language, causing it unavailable to international readers.

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In this study, we present the first systematic review and a meta-analysis of OCs in

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Chinese sludge based on literature published over the past 30 years. The objectives were to (i)

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examine the temporal and spatial distributions of all previous work; (ii) reveal the identity

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and concentration of important and abundant OCs in Chinese sludge, and (iii) assess the

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potential need for conducting a Chinese national sludge survey.

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METHODOLOGY

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Search strategy. Frequently detected OCs in the environment were categorized into 35

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classes for this study. The full names and abbreviations of contaminants considered are

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shown in Table 1. The literature survey was conducted via searching of the Web of

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Knowledge (WoK) publications database (http://apps.isiknowledge.com/) and the China

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Academic Journal Network Publishing Database (CAJD; http://oversea.cnki.net/) until 5


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September 30, 2015. The detailed search terms and strategy were presented in the Supporting

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Information (SI). The initial search yielded 1679 publications, of which 536 and 1143

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publications were found in the WoK database and the CAJD, respectively. Subsequently, we

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examined these publications individually and further eliminated the duplicate and irrelevant

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articles, such as the studies focusing on industrial sludge, removal technologies of

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contaminants in sludge, and sludge disposal processes. In the end, 159 relevant papers were

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selected for the meta-analysis. Data were extracted from the selected papers to develop a

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database, including compound name, sampling location, concentration, and reference

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information, which can be obtained upon request.

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Data analysis. Table 1 summarized the names and abbreviations for 35 classes of

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compounds. More detailed information can be obtained from Table S1. The class of

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pharmaceuticals refers to all kinds of drugs used to improve human and animal health with

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the notable exception of antibiotics. Generally, mean concentrations were either provided by

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authors or calculated as needed using original data. Both non-detects and concentrations

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below detection limit were assigned a value of zero due to inconsistent detection limits

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reported, even for the same compound in different studies. Depending on the concentration

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range of each compound, levels were recorded in the database as either ng/g or µg/g on a dry

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weight (dw) basis.

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Data on the number of sewage treatment facilities, the discharge of wastewater, the gross

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domestic product (GDP), the gross regional product (GRP), and the total investment on

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environmental production were extracted from the Annual Report of the Ministry of Housing

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and Urban-Rural Development of China, China Statistical Yearbook on Environment, China

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Statistical Yearbook, China Environment Bulletin, and a reference.26

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A two-tailed Spearman correlation analysis was performed to determine the relationship

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among the study distribution, per capita GRP, and population density throughout China.

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Comparisons of the concentrations of PAHs in sludges sampled from different periods were

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examined using either Mann-Whitney U (in two groups of samples) or Kruskal-Wallis H (in

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more than two groups of samples), both of which are nonparametric tests. All statistical

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analyses were conducted using SPSS (Version 18.0, Chicago, IL, USA) with a significance

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level of p = 0.05. A Bonferroni-adjusted significance level of 0.0125 was applied for the

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repeated Mann-Whitney U test.

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RESULTS AND DISCUSSION

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Temporal distribution of sludge studies. A total of 159 papers on OCs in Chinese

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sludge have been published since 1987 (Figure 1). Approximately 65% of available studies

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were published in English journals, a positive development facilitating sharing of information

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internationally. The first sludge study appeared in 1987 in a Chinese journal, identifying 35

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nitrogen-heterocyclic compounds (NHCs) in five sludge samples from a secondary

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wastewater treatment plant (WWTP) in Beijing, in which seven compounds were

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quantitatively analyzed.27 For the next 13 years (1988-2000), no publications were found in

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our search. In 2005, a paper published in English investigated patterns and levels of six

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synthetic musks (SMs) in sludge from Guangdong Province, South China.28 Starting in 2004,

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at least two publications appeared every year with new information on contaminant levels in

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sludge. An increasing number of publications per year was observed, with three main periods 7


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identified: less than 5 papers annually in Period I (1987-2006), approximately 10 per year in

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Period II (2007-2010), and approximately 20 annually thereafter in Period III (2011-2015).

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Only one paper was presented in English in Period I, contributing 7% of the total in that

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period. However, the ratio of English papers to the total number of papers has grown

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significantly since 2007, increasing to 49% and 80% in Periods II and III, respectively.

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The observed rapid increase of studies on OCs in Chinese sludge could be related to the

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growth of investment in environmental protection. China increased investment in

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environmental projects with an average annual growth rate of 19% during the last three

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decades, and the investment reached 951 billion Chinese Yuan (148 billion current USD) in

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2013 (Figure S1). The corresponding proportion (ratio of investment to gross domestic

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production) has been steadily increasing, from 0.5% in 1981 to 1.6% in 2013. Improvements

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in analytical technologies also represent a driving force for increased publication activity.

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Sludge is a complicated matrix with abundant organic matter, which is a challenge for sample

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pretreatment and the subsequent instrumental analysis. However, extensive applications of

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hyphenated methods in environmental analysis, including advanced gas chromatography and

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liquid chromatography coupled to mass spectrometry and tandem mass spectrometry

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(GC-MS/MS) and (LC-MS/MS), have broadened the list of formally targeted compounds,

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exploring non-targeted chemicals and increasing the reliability of quantitative

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measurements.29,30

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Spatial distribution of sludge sampling sites. Among 159 studies, sludge samples were

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collected from different provinces and municipalities of China, showing an uneven pattern of

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distribution (Figure 2). Beijing, Shanghai, and Guangdong Province, three of the most 8



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developed and populated areas of China, have the largest number of studies (i.e., 66, 46, and

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46, respectively). Generally, fewer sludge samples were collected from the northern,

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southern, and western regions than those from the east and central regions of China. For

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example, only three or four studies were conducted in Jilin Province, the Guangxi Zhuang

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Autonomous Region, Hainan Province, Guizhou Province, and the Ningxia Hui Autonomous

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Region. To date, no sludge has been sampled from the Tibet Autonomous Region, although

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due to its high elevation it has fundamental significance to the environment of China, Asia,

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and the world.31 The Tibet Autonomous Region built its first WWTP in 2011 with a daily

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sewage treatment capacity of 50,000 cubic meters. For the two Special Administrative

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Regions of China, 11 studies were conducted in Hong Kong, whereas no samples have been

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analyzed from Macau.

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The study distribution, per capita GRP, and population density throughout China were

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compared to find patterns (Figure 2). Provinces or municipalities along the coastal areas of

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China (eastern region), such as Shanghai, Jiangsu Province, Zhejiang Province, and

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Guangdong Province, have the highest GRP and population density and the greatest number

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of sludge studies. In contrast, the sparsely populated western region featured the lowest GRP

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and fewest number of studies performed. To further explore the relationship among the three

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distributions, a two-tailed Spearman correlation analysis was performed (Table S2). Hong

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Kong and Macau were excluded due to their different administrative systems. As expected, a

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positive albeit moderate relationship was found between the number of studies and the per

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capita GRP of all provinces and municipalities of China. The correlation coefficient (r) was

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0.51 with a corresponding p value of 0.003. Similarly, a moderate but significant positive 9


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relationship was obtained between the number of studies and the population density

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(correlation coefficient: r = 0.59; p < 0.001). These observations suggest that continued

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investment in the environmental sector will foster much needed future research into the

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composition of and safe disposal options for sludge in China.

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Coverage of OCs in sludge. Thirty-five classes of organic contaminants, including 749

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individual compounds and one mixture (short chain chlorinated paraffins (SCCPs); generally

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reported in mixture), have been analyzed in Chinese sludge since 1987 (Figure 3 and Table

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S1). Some targeted OCs originated from the residuals of various commercial products with

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wide applications, such as antibiotics, pharmaceuticals, personal care products, pesticides,

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flame retardants, plasticizers, antioxidants, solvents, surfactants, and thermal stabilizers.

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Others, including hydroxylated polybrominated diphenyl ethers (OH-PBDEs), methoxylated

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polybrominated diphenyl ethers (MeO-PBDEs), polychlorinated dibenzo-p-dioxins and

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dibenzofurans (PCDD/Fs), PAHs, and substituted polycyclic aromatic hydrocarbons

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(S-PAHs), were generated unintentionally during the manufacture, usage, and disposal of

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commercial products, and even in household cooking.

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Excluding SCCPs, approximately 54% of analytes contain at least one halogen atom

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(chlorine, bromine, or fluorine), and can be categorized as organohalogen contaminants

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(OHCs). As global environmental pollutants, the OHCs have raised concern because they can

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be highly persistent, bioaccumulative, and have adverse effects on humans and wildlife.32

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Although the production and usage of several old OHCs (e.g., polychlorinated biphenyls

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(PCBs) and organochlorine pesticides (OCPs)) were banned almost four decades ago, they

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still remain ubiquitous in the environment worldwide, including remote regions.33,34 10



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Moreover, new OHCs (e.g., polybrominated diphenyl ethers (PBDEs) and perfluorinated

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compounds (PFCs)) continue to be discovered in aquatic and terrestrial ecosystems and have

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recently been considered as emerging OCs.32-34 In Chinese sludge, 228 chlorinated, 103

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brominated, and 83 fluorinated OHCs have been screened in sludge in the past three decades,

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accounting for 30%, 13%, and 11% of the total analytes, respectively (Figure 3). Twelve

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OHCs have two different halogen atoms. For example, an alternative to

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perfluorooctanesulfonate in the electroplating industry, 6:2 chlorinated polyfluorinated ether

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sulfonate (6:2 Cl-PFAES) as well as its homologues 8:2 and 10:2 Cl-PFAESs were recently

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identified in municipal sludge samples of China.35

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Over the past 30 years, antibiotics36-60 and PAHs61-84 were the most commonly studied

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OCs in Chinese sludge with 25 and 24 publications, respectively (Figure 4 and Tables S1 and

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S3). Antibiotics are a group of emerging OCs that have received considerable attention in

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recent years. Alkylphenol polyethoxylates (APEOs),62,85-97 bisphenol analogs

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(BPAs),62,86,90,92,96-102 hormones,90,92,96-100,102-106 OCPs,62,65,67,81,107-109 PFCs,35,110-120

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pharmaceuticals,45,49,53-55,57,98,121,122 phthalate esters (PAEs),62,123-130 PBDEs,109,131-144

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PCBs,62,65,67,77,80,81,107,145-147 SMs,28,78,148-161 and ultraviolet stabilizers (UV stabilizers),2,162-165

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were each found in more than five studies. However, some OCs have been monitored

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infrequently, with only one or two studies being available on the occurrence in Chinese

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sludge of chlorinated hydrocarbons (CHCs),131,166 OH-PBDEs,137 MeO-PBDEs,137 NHCs,27

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novel brominated flame retardants (N-BFRs),167 organometals,168 organophosphate esters

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(OPs),169,170 parabens,98 phenolic compounds (PCs),96,171 quaternary ammonium compounds

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(QACs),172,173 and S-PAHs.82,174 11


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PAHs and antibiotics were first detected in sludge in 200161 and 200736, respectively.

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Since then, they have been investigated in Chinese sludge almost every year, indicating their

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frequent detection and researchers’ concern for them (Table S3). The occurrence of other old

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pollutants, such as APEOs,85 BPAs,62 OCPs,131 PAEs,123 PCBs,62 PCDD/Fs,62 and

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polychlorinated naphthalenes (PCNs),131 were reported before the year 2006. Since 2010,

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numerous emerging OCs have raised attention, including dechlorane plus (DPs),64

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hexabromocyclododecanes (HBCDs),175 N-BFRs,167 OPs,169 parabens,98 PFCs,110

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pharmaceuticals,121 PBDEs,131 QACs,173 SCCPs,176 siloxanes,177 synthetic phenolic

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antioxidants (SPAs),178 triclosan and triclocarban (TCS +TCC),179 UV stabilizers,162 and

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metabolites of PBDEs137 and PAHs174.

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Level and profile of OCs in sludge. Based on median concentrations, 34 classes of

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contaminants were ranked in decreasing order, as shown in Figure 4. MeO-PBDEs were

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excluded due to a lack of detection in 36 sludge samples from 27 cities throughout China.137

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The medians of 16 classes of contaminants, including antibiotics, APEOs, aromatic amines

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(AAs), azole antifungals (AAFs), CHCs, organometals, PCs, PAEs, PAHs, QACs, SCCPs,

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siloxanes, S-PAHs, SMs, SPAs, and TCS + TCC were higher than 1 µg/g dw

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(parts-per-million or ppm). For the other 16 classes, BPAs, DPs, HBCDs, hormones, NHCs,

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N-BFRs, OCPs, OPs, parabens, PFCs, pharmaceuticals, PBDEs, PCBs, PCNs, UV

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stabilizers, and volatile aromatic hydrocarbons (VAHs) the levels fall into a range from lower

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ng/g (parts-per-billion or ppb) to µg/g (ppm). OH-PBDEs and PCDD/Fs were frequently

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detected in sludge, while occurring in relatively lower concentrations of less than 1 ng/g dw.

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Notably large variations in concentrations were found (expressed as 95% confidence 12



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intervals) for most of the compounds, which could be related to the limited number of

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studies, inconsistent targets, different sampling strategies and/or different sampling times

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(Figure 4).

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Thirteen classes of contaminants found in over five studies were chosen as “principal

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OCs” in Chinese sludge. Table 2 summarized their detailed concentration information. The

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levels of PAEs were the highest, with a median in units of ng/g dw of 27,900, followed by

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APEOs (12,000), SMs (5800), antibiotics (4240), PAHs (3490), UV stabilizers (670), BPAs

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(160), OCPs (110), PBDEs (100), pharmaceuticals (84), hormones (69), PFCs (21), and PCBs

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(15). As for the individual compounds, di(2-ethylhexyl) phthalate (6630) and dibutyl

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phthalate (1180) were two predominant PAEs. Similarly, the abundant and representative

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compounds were determined for eight other principal OCs: 4-nonylphenol monoethoxylate

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(6830) and 4-nonylphenol (3140) for APEOs, galaxolide (3860) and tonalide (1400) for SMs,

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phenanthrene (280) and fluoranthene (260) for PAHs,

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2-[3',5'-bis(1-methyl-1-phenylethyl)-2'-hydroxyphenyl]benzotriazole (340) and

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2-(2-hydroxy-3,5-dipenryl-phenyl) benzotriazole (310) for UV stabilizers, bisphenol A (160)

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for BPAs, p,p'-dichlorodiphenyldichloroethylene (52) and hexachlorobenzene (17) for OCPs,

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decabromodiphenyl ether (78) and 2,2’,4,4’,5-pentabromodiphenyl ether (4.6) for PBDEs,

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and 2,4,4’-trichlorobiphenyl (5.4) and 2,2’,5,5’-tetrachlorobiphenyl (0.4) for PCBs. Here no

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abundant compounds were shown for antibiotics, pharmaceuticals, hormones, and PFCs

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because of the large variety of analytes in different studies.

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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 13


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PAHs. Among all studies concerning PAHs (N = 24), 20 of them targeted 16 priority

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pollutants specified by the USEPA and subsequently were selected to study the temporal

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variation.61-64,66,68,69,71,72,74-84 The sum concentration of these 16 PAHs was compiled into four

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periods per the sampling years mentioned above (Figure 5). If the sampling time was not

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provided in the paper, it was assumed that the samples were collected three years before the

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publication date of the paper. It is interesting to note that a significant difference was

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observed among samples collected from the four periods (Kruskal-Wallis H test; p = 0.001).

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Overall, the median PAH concentration in Chinese sludge showed a decreasing trend: from

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15,700 ng/g dw in 1998-2000, 13,100 ng/g dw in 2001-2005, 2360 ng/g dw in 2006-2010, to

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3000 ng/g ng in 2011-2012. Moreover, the sludge sampled from 2006-2010 contained

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significantly lower PAHs than those from the periods of 1998-2000 and 2001-2005

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(Mann-Whitney U test; p = 0.005 and 0.001, respectively). However, no significant changes

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of PAHs were found in samples from other periods, including 1998-2000 vs 2001-2005 (p =

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0.559), 1998-2000 vs 2011-2012 (p = 0.068), 2001-2005 vs 2011-2012 (p = 0.086), and

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2006-2010 vs 2011-2012 (p = 0.577) (Figure 5). Similar decreasing trends of PAHs were also

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reported in sediment cores taken from the East China Sea180, the Yellow Sea, and the South

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China Sea, China.181 The gradual decline in levels observed in recent sludge samples may

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contribute to the reduction of PAH emissions due to the replacement of domestic coal and

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biomass combustion by natural gas or petroleum since the 1990s in China.182

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In 2009, China issued a sludge standard (CJ/T 309-2009) that regulated the maximum

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tolerance concentration (MTC) for PAHs: 5000 ng/g dw for Class A sludge (used in

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agricultural soils) and Class B sludge (used in agricultural soils not for vegetable and cereal 14



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production). In 2011, another standard (CJ/T 362-2011) was established that set an MTC of

300

6000 ng/g dw for PAHs in sludge applied in forestland. The medians of PAHs in sludge from

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1998-2000 and 2001-2005 would not have met the current MTC standards, but sludge from

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2006-2010 and 2011-2012 are below the MTCs, suggesting Chinese sludge currently passes

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PAH regulation (Figure 5).

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China has developed sludge standards for other OCs as well, aiming to protect human

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health and the environment (Figure 6 and Table S4). The first regulation was issued in 1984,

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in which the MTC of benzo[a]pyrene is 3 µg/g dw when sludge is applied in agricultural soils

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with an application rate of 30 metric tons/ha/yr (Table S5). In 2002, another standard (GB

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18918-2002) set MTCs not only for benzo[a]pyrene (B(a)P; 3 µg/g dw) but also for PCDD/Fs

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(100 ng TEQ/kg dw), PCBs (0.2 µg/g dw), and adsorbable organic halogens (AOX;

310

calculated by chlorine; 500 µg/g dw), given that sludge is used in agricultural soils with the

311

above application rate. Based on different sludge disposals, several specific standards have

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been issued recently (Figure 4 and Tables S4 and S5). More OCs are regulated for sludge

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applied to soil than for that used in co-landfilling as cover material and in making bricks.

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Only standards for volatile phenolic compounds (VPCs; MTC: 40 µg/g dw) were proposed in

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sludge with aims to co-landfill (CJ/T 249-2007 and GB/T 23485-2009) or make bricks (CJ/T

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289-2008 and GB/T 25031-2010). It is worthwhile to note that the scientific methodology

317

used for calculating MTCs is insufficient in China.23

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Need for a national sewage sludge survey in China. Although a significant increase in

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the number of sludge studies is observed, two aspects on OCs in Chinese sludge are rarely

320

considered. One is the sampling of sludge samples: the collection has been unsystematic in 15


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the past and lacks nationwide representativeness.56,163,168 Another is that current studies only

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target select analytes and chemicals classes at different points in time. Therefore, to

323

systemically assess the risk to human health and the environment for OCs in Chinese sludge,

324

it is necessary to conduct a national survey.

325

Representativeness of sludge samples. Several aspects should be examined when

326

choosing appropriate WWTPs to represent pollution control infrastructure in China (3802

327

WWTPs were in operation as of June 2015) (Table S6).

328

First, the geographic distribution of WWTPs: the discharge volumes of industrial and

329

domestic wastewater, and the number and treatment capacity of WWTPs are unequal in

330

different provinces and municipalities of China.183 Most WWTPs were constructed in the

331

eastern region, especially the coastal areas that have the highest GRP and the highest

332

population density. Approximately 60% of WWTPs were located in cities, and others in

333

counties or towns (Table S6). In addition, many industrial plants were relocated from capital

334

cities to rural areas with the rapid urbanization of China. Therefore, more and more

335

production of industrial wastewater could be expected in rural areas (Table S7).

336

Second, the scale of WWTPs and the treatment process employed: generally,

337

medium-scale WWTPs (10,000−100,000 metric tons of wastewater per day) are common in

338

China, accounting for 75% of the total. Only 3% of super-large-scale WWTPs (> 300,000

339

metric tons per day) were built in big cities.183 More than 10 different treatment processes can

340

be found in WWTPs of China with varying chemical oxygen demand removal efficiencies, of

341

which the oxidation ditch, the anaerobic/anoxic/oxic and the sequencing batch reactor are the

342

mainstream technologies.183 16



343

Third, the sample size and type: the aim of monitoring should ideally be to characterize

344

all of the target WWTPs, and hence all the facilities in the sample frame should have a

345

known, non-zero chance of selection. The USEPA used a probabilistic method for estimating

346

sample size.18 A minimum sample size of 80 POTWs was determined to represent the total

347

number of facilities in the sample frame (3337 POTWs).184 Additionally, taking sludge from

348

different sampling points in a WWTP to form a composite sample is better than non-repeated

349

grab sampling, although the latter has often been used in previous studies.35,173,185

350

Selection of analytes. As mentioned above, a total of 749 organic compounds and one

351

mixture have been monitored in Chinese sludge to date. However, it is not possible to

352

prioritize these chemicals based on the data derived from the previous studies. More

353

comprehensive and comparable data are essential to make a systematic risk assessment to

354

human health and the environment for OCs in sludge of China.

355

Moreover, there are other chemicals that need to be considered and/or regulated,

356

especially those being produced and consumed in large volumes. For example, PAEs are a

357

group of industrial chemicals that have been widely used as polymer plasticizers since the

358

early 20th century. The global annual production of PAEs was around 6.2 million metric tons

359

in 2009, of which around 18% was produced and 24% was consumed in China.128

360

Di(2-ethylhexyl) phthalate (mean: 97,400 ng/g dw) and dibutyl phthalate (mean: 22,400 ng/g

361

dw) were typically found in high concentrations in sludge samples collected from Shanghai

362

compared with other pollutants like PBDEs, DPs, and PFCs (mean: 6.0−2400 ng/g

363

dw).116,128,135,140,185 The EU proposed an MTC for di(2-ethylhexyl) phthalate (100,000 ng/g

364

dw) in sludge applied to soil, and that MTC is very close to the mean value found in 17


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Shanghai samples (97,400 ng/g dw). The MTC for 4-nonylphenol (50,000 ng/g dw), an

366

abundant chemical found in Chinese sludge, was also proposed in the 3rd draft of the EU

367

Sludge Directive.29 By contrast, no similar initiative was implemented in China.

368

Furthermore, using high resolution mass spectrometry combined with non-targeted

369

screening strategy, suspected and unknown contaminants can be identified and quantified in

370

environmental samples.186-188 For example, employing liquid chromatography coupled to a

371

quadrupole-time-of-flight mass spectrometer (LC-QTOF-MS), Gago-Ferrero et al. tentatively

372

identified 13 of 284 predicted and literature metabolites of selected pharmaceuticals and

373

nicotine in influent samples from Athens, seven of which were finally confirmed with

374

reference standards. They also found 34 non-targeted compounds and four of them were

375

confirmed.188

376

With the targeted and non-targeted screening, as well as the unbiased sampling, a

377

national survey on OCs in Chinese sludge could be conducted. Subsequently, according to

378

their production volumes, concentrations in the environment, environmental persistence, and

379

potential toxicities, all detected compounds should be ranked in a list of Chinese priority

380

OCs. The findings and database of this study could serve as a useful tool for researchers,

381

policy makers, and industry professionals. By using sludge as a suitable matrix for capturing

382

human activities and ecological impacts, more knowledge will result from monitoring

383

geographic and temporal trends of OCs in sludge, in the environment,189,190 and ultimately in

384

human populations.191

385 386

ASSOCIATED CONTENT 18



387 388

Supporting Information Additional tables contain a summary of compounds analyzed in Chinese sewage sludge,

389

the Spearman correlation analyses between the number of studies and per capita gross

390

regional product and population density, the class of organic contaminants analyzed per year,

391

regulations on sewage sludge, the maximum tolerance concentration of organic contaminants

392

in sewage sludge, the numbers of wastewater treatment plants, and the discharge of industrial

393

and domestic wastewater. Additional figure contains the total investment on environmental

394

research and the proportion of investment to gross domestic product. All materials are

395

available free of charge via the Internet at http://pubs.acs.org.

396

AUTHOR INFORMATION

397

Corresponding Author

398

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

399

Notes

400

The authors declare no competing financial interest.

401

ACKNOWLEDGMENTS

402

The present study was financially supported by the National Natural Science Foundation

403

of China (No. 21437004), the Swedish Research Council (contract Dnr. 639-2013-6913), the

404

Major Science and Technology Program for Water Pollution Control and Treatment (No.

405

2012ZX07313001), the Program for New Century Excellent Talents in University (No.

406

NCET-12-0417), the China Scholarship Council, the Collaborative Innovation Center for

407

Regional Environmental Quality, and the Virginia G. Piper Charitable Trust (LTR 05/01/12). 19


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1020 1021 33


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1022

Table 1. Classes of organic contaminants (OCs) analyzed in Chinese sewage sludge over the

1023

past 30 years. N: number of studies. n: number of compounds in each class of OCs. Compound class

Abbreviation

N

n

antibiotics

25

86

APEOs

14

27

Aromatic amines

AAs

2

31

Azole antifungals

AAFs

4

7

Bisphenol analogs

BPAs

11

13

Chlorinated hydrocarbons

CHCs

2

6

DPs

2

7

HBCDs

2

4

hormones

12

40

Hydroxylated polybrominated diphenyl ethers

OH-PBDEs

1

9

Methoxylated polybrominated diphenyl ethers

MeO-PBDEs

1

9

Nitrogen-heterocyclic compounds

NHCs

1

34

Novel brominated flame retardants

N-BFRs

1

12

OCPs

7

17

organometals

1

5

OPs

2

7

Parabens

1

4

PFCs

12

59

pharmaceuticals

9

22

Phenolic compounds

PCs

1

16

Phthalate esters

PAEs

9

16

PBDEs

15

48

PCBs

10

43

PCDD/Fs

4

17

Polychlorinated naphthalenes

PCNs

4

75

Polycyclic aromatic hydrocarbons

PAHs

24

17

Quaternary ammonium compounds

QACs

2

27

Short chain chlorinated paraffins

SCCPs

3

mixture

Siloxanes

siloxanes

3

19

Substituted polycyclic aromatic hydrocarbons

S-PAHs

2

13

Synthetic musks

SMs

16

9

Synthetic phenolic antioxidants

SPAs

1

15

TCS + TCC

3

2

UV stabilizers

5

20

VAHs

3

13

Antibiotics Alkylphenol polyethoxylates

Dechlorane plus Hexabromocyclododecanes Hormones

Organochlorine pesticides Organometals Organophosphate esters Parabens Perfluorinated compounds Pharmaceuticals

Polybrominated diphenyl ethers Polychlorinated biphenyls Polychlorinated dibenzo-p-dioxins and dibenzofurans

Triclosan and triclocarban Ultraviolet stabilizers Volatile aromatic hydrocarbons

34



1024 1025

Page 36 of 43

Table 2. Concentrations of principal organic contaminants in Chinese sewage sludge (ng/g dry weight). N: number of studies. ND: non-detection. Compound class

N

Minimum

Mean

Median

Maximum

Reference

Antibiotics

25

0.83

8390

4240

38,700

36-60

Alkylphenol polyethoxylates (APEOs)

14

ND

887,000

12,000

33,810,000

62,85-97

Bisphenol analogs (BPAs)

11

34.6

10,500

160

127,000

62,86,90,92,96-102

Hormones

12

ND

178

69

981

90,92,96-100,102-106

Organochlorine pesticides (OCPs)

7

9.0

327

110

3200

62,65,67,81,107-109

Perfluorinated compounds (PFCs)

12

ND

796

21

9980

35,110-120

Pharmaceuticals

9

ND

482

84

4460

45,49,53-55,57,98,121,122

Phthalate esters (PAEs)

9

680

48,400

27,900

282,000

62,123-130

Polybrominated diphenyl ethers (PBDEs)

15

3.46

1020

100

7100

109,131-144

Polychlorinated biphenyls (PCBs)

10

3.14

81

15

1400

62,65,67,77,80,81,107,145-147

Polycyclic aromatic hydrocarbons (PAHs)

24

100

15,900

3490

170,000

61-84

Synthetic musks (SMs)

16

ND

8320

5800

33,200

28,78,148-161

Ultraviolet stabilizers (UV stabilizers)

5

288

1040

670

2330

2,162-165

1026 1027 1028

35


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1029

Figure Captions

1030

Figure 1. Number of publications on organic contaminants in Chinese sewage sludge per year. The inserted plot shows the 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 nine months.

1031 1032 1033 1034 1035 1036 1037 1038 1039 1040 1041 1042 1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1054 1055 1056 1057

Figure 2. National distribution of (a) the number of studies detecting at least one organic contaminants in Chinese sewage sludge, (b) the gross regional product (GRP; USD/Year per Capita and RMB/Year per Capita), and (c) the population density (people per km2) by province or municipality in China. 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. Figure 4. Concentrations of organic contaminants (OCs) detected in Chinese sewage sludge (median and 95% confidence interval; ng/g dry weight). 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. Figure 5. Concentrations of polycyclic aromatic hydrocarbons (PAHs; median and 95% confidence interval; ng/g dry weight (dw)) in Chinese sewage sludge sampled from different years. Class 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. 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.

36



Figure 1.

37


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Figure 2.

38



Figure 3.

39


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Figure 4.

40



Figure 5.

41


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Figure 6.

42


Organic Contaminants in Chinese Sewage Sludge: A Meta-Analysis of

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