Article pubs.acs.org/est
Parabens in Sediment and Sewage Sludge from the United States, Japan, and Korea: Spatial Distribution and Temporal Trends Chunyang Liao,† Sunggyu Lee,‡ Hyo-Bang Moon,‡ Nobuyoshi Yamashita,§ and Kurunthachalam Kannan*,† †
Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Empire State Plaza, P.O. Box 509, Albany, New York 12201-0509, United States ‡ Department of Marine Sciences and Convergent Technology, College of Science and Technology, Hanyang University, Ansan, Gyeonggi 426-791, South Korea § National Institute of Advanced Industrial Science and Technology (AIST), 16-1 Onogawa, Tsukuba, Ibaraki 305-8569, Japan S Supporting Information *
ABSTRACT: Parabens (alkyl esters of p-hydroxybenzoic acid) are widely used in cosmetics, pharmaceuticals, and foodstuffs as broad-spectrum antimicrobial preservatives. Laboratory animal studies have shown that parabens possess weak estrogenic activity. Widespread exposure of humans to parabens has raised significant public health concerns. Despite such concern, little is known about the occurrence of parabens in the environment. In this study, six paraben analogues, methyl- (MeP), ethyl- (EtP), propyl- (PrP), butyl- (BuP), benzyl(BzP), and heptyl parabens (HepP), were determined in surface sediment and sediment core samples collected from several locations in the United States (U.S.), Japan, and Korea by high-performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Concentrations of parabens also were determined in sewage sludge collected from several wastewater treatment plants (WWTPs) in Korea. MeP was found in all samples, including surface sediment, sediment core, and sludge samples, at concentrations ranging from 0.312 to 540 ng/g dry weight (dw). PrP was detected in the majority of samples (79%), and the concentrations were, in general, 1−2 orders of magnitude lower than MeP concentrations. Significant positive correlations were found among the concentrations of paraben analogues in sediment and sludge, which suggested the existence of similar sources of origin for these compounds. The sum concentrations of six parabens (∑PBs) in sludge (geometric mean: 66.3, median: 89.5 ng/g dw) were remarkably higher than those in sediment (5.48, 5.24 ng/ g dw). Vertical profiles of parabens in sediment cores from the U.S. showed a gradual increase in concentrations in the past decade, although such a trend was not clear in sediment core from Tokyo Bay, Japan.
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INTRODUCTION
National Health and Nutrition Examination Survey (NHANES), conducted in 2005−2006, showed that 99% of 2,548 urine specimens contained at least one paraben at quantifiable concentrations (the detection rate was 99%, 42%, 93%, and 47% for MeP, EtP, PrP, and BuP, respectively).6 Parabens have been reported to occur in human breast tissues from the United Kingdom at concentrations on the order of a few tens to thousands of nanograms per gram.7,8 The estrogenic effects of parabens have been documented in both in vitro and in vivo studies.2,3 In an in vitro yeast-based assay, MeP, EtP, PrP, and BuP were found to be weakly estrogenic, and the estrogenic effect was proportional to the alkyl chain length.9 The estrogenic effect of BuP was further confirmed in an in vivo uterotrophic assay.9 Estrogenic activities
Alkyl esters of p-hydroxybenzoic acid (parabens) are added as ingredients in certain cosmetics, pharmaceuticals, and foodstuffs due to their broad-spectrum antimicrobial properties.1−3 The most commonly used parabens include methyl- (MeP), ethyl- (EtP), propyl- (PrP), butyl- (BuP), and benzyl-parabens (BzP). It has been estimated that parabens are used in over 22,000 cosmetic products, as preservatives, at concentrations of up to 0.4% for a single compound or up to 0.8% for a mixture of parabens.4 Several pharmaceuticals contain parabens, as preservatives, at concentrations varying from product to product but generally below 1%.3 Parabens have been used in foods for several decades, especially in processed vegetables, bakery products, fats and oils, seasonings, sugar substitutes, and frozen dairy products, in concentrations of up to 0.1%.5 Widespread use of parabens has resulted in ubiquitous human exposure to these chemicals. Humans are exposed to parabens through diet, cosmetics, and pharmaceuticals with cosmetics contributing, in general, to major exposures.3,4,6 The U.S. © 2013 American Chemical Society
Received: Revised: Accepted: Published: 10895
June 10, 2013 August 8, 2013 August 28, 2013 August 28, 2013 dx.doi.org/10.1021/es402574k | Environ. Sci. Technol. 2013, 47, 10895−10902
Environmental Science & Technology
Article
Sample Collection and Preparation. Surface sediment samples (0−12 cm) from the U.S. were collected from several bodies of water from 1998 to 2012, including the Detroit River (Michigan, 1998, n = 5),29 Chesapeake Bay (Virginia, 2002, n = 5), several tributaries (such as the Niagara, Oswego, Ashtablua, and Buffalo Rivers) of Lakes Erie and Ontario (2009, n = 14), the Saginaw River watershed (including the Saginaw River, Saginaw Bay, and Tittabawassee River; Michigan, 2002 and 2004, n = 18),30,31 and the Hudson River (New York, 2012, n = 5). Surface sediment samples (0−4 cm) from Korea were collected from Lake Shihwa (an artificial saltwater lake) in 2008 (n = 34).32 Three sediment cores were collected from the Saginaw River watershed in 2004, with lengths of 150, 210, and 285 cm. These cores were cut into 0−30, 30−90, 90−150, 150−210, 210−270, and 270−285 cm sections.30,31 Two sediment cores were collected from Gratiot and Whitmore Lakes (Michigan) in 1999 and 2001, respectively. Both of these cores were sectioned at 0.5 cm increments for top 5−8 cm and at 1 cm increments thereafter (further details of the cores are presented elsewhere).33 The cores were dated using 210Pb and 137 Cs profiles, as reported earlier.33 Two sediment cores were collected from Tokyo Bay, Japan (N35°35′00″, E139°54′59″) in April 2012 at a location that was studied previously.34 Both of these cores were sectioned at 1-cm intervals for top 4 cm (12 cm for another core) and at 1.5 cm intervals thereafter. Sewage sludge samples were collected from several WWTPs throughout Korea in 2011 (n = 40). On the basis of the sources of wastewater treated by the WWTPs, sludge samples were categorized as domestic, mixed, or industrial and contained 0− 3%, 20−60%, and >70% loadings from industrial wastewater, respectively. All samples were homogenized, freeze-dried, and stored at −20 °C until analysis. The sample was extracted and analyzed by following the method described elsewhere.35,36 Briefly, a 100−500 mg sediment or sludge sample was weighed and transferred into a 15 mL polypropylene conical tube (PP tube). 13C12-MeP and 13 C12-BuP were spiked as internal standards (5 ng each). The sediment sample was extracted with a 5 mL solvent mixture of methanol and water (5:3, v/v) by shaking in an orbital shaker (Eberbach, Ann Arbor, MI) at 250 oscillations/min for 60 min. The mixture was centrifuged at 4500g for 5 min (Eppendorf Centrifuge 5804, Hamburg, Germany), and the supernatant was transferred into a glass tube. The extraction step was repeated one more time with a 3 mL solvent mixture. The pooled extracts were concentrated to ∼4 mL under a gentle nitrogen stream. The extract was diluted to 10 mL with 0.2% formic acid in water (pH 2.5), and the extracts were purified by passage through an Oasis MCX cartridge (60 mg/3 cm3; Waters, Milford, MA) using a RapidTrace SPE workstation (Caliper Life Sciences, Inc., Hopkinton, MA). The cartridge was conditioned with 5 mL of methanol and then with 5 mL of water. The extract was loaded onto the cartridge and rinsed with 15 mL of 25% methanol in water and 5 mL of water. Target analytes were eluted with 5 mL of methanol. After being concentrated to 1.0 mL, the eluate was transferred into a chromatographic vial for analysis by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Instrumental Analysis. An Applied Biosystems API 3200 electrospray triple quadrupole mass spectrometer (ESI-MS/ MS; Applied Biosystems, Foster City, CA) equipped with a Shimadzu Prominence Series LC-20AD system (Shimadzu U.S.A. Manufacturing Inc., Canby, OR) was used for the measurement of target compounds. The negative ion multiple
of parabens were assessed by estrogen-dependent proliferation of human breast cancer (MCF-7) cells;10−12 in comparison with 17-β-estradiol, parabens are 8,000−900,000-fold less estrogenic.13 Reduction in testosterone levels and in sperm counts in rats has been shown in laboratory studies.14,15 Parabens also were toxic to aquatic organisms, including fish, daphnia, and algae.1,16 Epidemiological studies have linked human exposure to parabens, including PrP and BuP, with sperm DNA damage in adult men and aeroallergen sensitization in children and adults.17,18 Although considerable controversy surrounds the health effects of parabens,1−3 assessment of the sources and pathways of these chemicals in the environment is limited. Due to the endocrine-disrupting potential of some of the parabens, these substances have been restricted in the European Union, and a national ban has been implemented in Denmark. Parabens have been reported to occur in drinking water, surface water, sewage, and wastewater treatment plant (WWTP) effluent at concentrations in the range of 15−400 ng/L.19−21 Parabens can be introduced into the aquatic environment through wastewater discharges 22 and subsequently pose health risk to aquatic organisms.13 MeP and EtP were reported in indoor and outdoor air samples at concentrations in the range of 2.4−313 ng/m3 (MeP) and 1.8−117 ng/m3 (EtP), respectively.23 Elevated concentrations of parabens have been found in indoor dust, and the total concentrations of six parabens (MeP, EtP, PrP, BuP, BzP, and heptyl paraben [HepP]), were on the order of several hundreds to thousands of nanograms per gram.24 A few pilot studies (sample size of 0.99. The reported concentrations were corrected for the recoveries of internal standards (13C6-MeP for MeP and EtP; 13C6-BuP for PrP, BuP, BzP, and HepP). The recoveries of internal standards spiked into all samples were 105 ± 20% for 13C6-MeP and 88 ± 35% for 13C6-BuP. A procedural blank, containing water in place of sediment/sludge, was analyzed with each batch of 20 samples as a check for interferences or laboratory contamination. MeP (approximately 0.291 ng/g), EtP (0.019 ng/g) and PrP (0.022 ng/g) were found in procedural blanks, and the concentrations measured in sediment/sludge were subtracted from the mean value found in procedural blanks from each batch of analysis. The recoveries of parabens (10 ng each) spiked into procedural blanks were between 90 ± 9% (mean ± SD; BzP) and 101 ± 7% (BuP), and those (10 ng each) spiked into sample matrices were between 81 ± 16% (HepP) and 119 ± 28% (PrP) (Table S2; Supporting Information). Duplicate analysis of randomly selected samples (n = 4 for each batch) showed a coefficient variation of 1000 tons/year. Based on an Internet search, it appears that paraben production has shifted mainly to China and India. The sediment cores collected in Michigan in the 1990s showed an increasing trend toward paraben concentrations that coincided with high production in the U.S. in those years. Relatively low concentrations in sediment cores also reflect high water solubility and rapid biodegradation of parabens. Further studies should include environmental fate of parabens in the aquatic environment. In summary, concentrations and profiles of six paraben analogues were investigated in sediments collected from several locations in the U.S., Japan, and Korea and in sewage sludge collected from several WWTPs in Korea. All samples contained at least one of the six parabens analyzed, and elevated concentrations of parabens (range: 4.63−545, GM: 66.3 ng/g dw) were found in sewage sludge samples. MeP was the dominant analogue and contributed to 88%−92% of the total paraben concentrations. Concentrations of parabens increased gradually from bottom to surface layers of sediment cores from the U.S., suggesting a recent increase in the input of these compounds. Considering the high consumption and continuous introduction of parabens into the environment, further studies are needed to assess the risks of paraben analogues in aquatic ecosystems.
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ASSOCIATED CONTENT
S Supporting Information *
Additional information as noted in the text (two tables and four figures). This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*Phone: 1-518-474-0015. Fax: 1-518-473-2895. E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This study was funded by a grant (1U38EH000464-01) from the Centers for Disease Control and Prevention (CDC, Atlanta, GA) to the Wadsworth Center, New York State Department of Health. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the CDC. We thank Dr. Sachi Taniyasu and Ms. Eriko Yamazaki (AIST) for sample collection in Japan. We also thank Dr. Guem-Ju Song for sludge sample collection in Korea. Gratiot and Whitmore lake sediments were collected as a part of the project supported by the Michigan Department of Environmental Quality during 2000-2001, and extracts from those earlier studies were used for paraben analysis. We thank Dr. David T. Long (Michigan State University) for these samples.
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REFERENCES
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