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Characterization of Natural and Affected Environments

Fertilizers as a Source of Melamine and Cyanuric Acid in Soils: A Nationwide Survey in China Hongkai Zhu, Yu Wang, Hongwen Sun, and Kurunthachalam Kannan Environ. Sci. Technol. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.estlett.8b00711 • Publication Date (Web): 17 Jan 2019 Downloaded from http://pubs.acs.org on January 18, 2019

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Fertilizers as a Source of Melamine and Cyanuric Acid in Soils: A Nationwide Survey in

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China

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Hongkai Zhu,† Yu Wang,† Hongwen Sun,§ and Kurunthachalam Kannan*,†,‡

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†Wadsworth

Center, New York State Department of Health, and Department of Environmental

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Health Sciences, School of Public Health, State University of New York at Albany, Empire State

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Plaza, P.O. Box 509, Albany, New York 12201-0509, United States

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§MOE

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Environmental Science and Engineering, Nankai University, Tianjin 300071, China

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‡Biochemistry

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Key Laboratory of Pollution Processes and Environmental Criteria, College of

Department, Faculty of Science and Experimental Biochemistry Unit, King Fahd

Medical Research Center, King Abdulaziz University, Jeddah 21589, Saudi Arabia

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*Corresponding author at: Wadsworth Center, Empire State Plaza, P.O. Box 509, Albany, NY

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12201-0509, United States

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Phone: +1 518 4740015; Fax: +1 518 473 2895; e-mail: [email protected]

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Graphic Abstract

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■ ABSTRACT

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The use of melamine and cyanuric acid in agriculture, industry, and consumer products has led to

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their ubiquitous environmental distribution. Nevertheless, little is known about the contamination

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of soils by melamine and cyanuric acid. Contamination of soils with melamine can lead to plant

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uptake and food chain transfer of these chemicals. In this study, concentrations of melamine and

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its three derivatives (cyanuric acid, ammeline and ammelide) were determined in 98 surface soils

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and 16 fertilizers collected across China in 2017. Elevated concentrations of ∑Melamine (sum of

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melamine and its three derivatives) were found in soils at concentrations that ranged from 8.67 to

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2020 ng/g dry weight (dw), with an average value of 213 ng/g dw. Melamine accounted for 63%

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of the total concentrations in soils, which was followed by cyanuric acid (28%). Elevated

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concentrations of melamine and cyanuric acid were found in nitrogenous fertilizers such as

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nitrolime (n = 3; mean: 284 µg/g) and urea (n = 4; mean: 3160 µg/g), respectively. The measured

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concentrations in fertilizers were 3 to 4 orders of magnitude higher than those found in soils.

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Farmland soils (mean: 545 ng/g dw) contained significantly higher concentrations of ∑Melamine

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than those of urban and background (forest) soils (92.5 ng/g dw). Our findings suggest that

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fertilizers are an important source of melamine and cyanuric acid in farm soils. Spatial distribution

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of melamine and cyanuric acid in soils showed the highest concentrations in Eastern China, which

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corresponded well with population density, industrial and agricultural activities. An ecological

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hazard assessment was performed of melamine in soils through a hazard quotient (HQ) approach.

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The mean HQ value was 0.35, and 7 of 98 surface soils had values above 1. Further studies are

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needed to discern uptake of melamine and its derivatives by crops and the fate of these chemicals

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in agricultural ecosystems.

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■ INTRODUCTION

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Melamine received worldwide attention from the pet food contamination incident in North

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America in 2007, which was followed by an adulterated milk scandal in China in 2008.1 Due to its

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high nitrogen content (67% by mass), melamine was deliberately added to milk and feed

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ingredients to increase the protein content. This incident led to exposure to melamine of over

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294,000 children in China, with at least six deaths from kidney-related diseases and kidney failure.2

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The severity of this incidence prompted global surveillance of melamine in infant formula, milk,

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and other dairy products, with measured concentrations ranging from below the limit of detection

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to 3630 ng/g.3-5 Nevertheless, melamine was reported to occur ubiquitously in human urine at

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concentrations on the order of several tens to hundreds of ng/mL,6 even in recent years (range:
150 km away from the production facility.25 That previous study was

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focused only on melamine, although other derivatives such as cyanuric acid can be present in

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soils.26 Considering that melamine can be hydrolyzed to cyanuric acid by soil bacteria, it is prudent

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that these chemicals are measured simultaneously to enable complete understanding of

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environmental transformation and fate.27

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The specific objectives of this study were to: (1) determine the concentrations and profiles of

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melamine, cyanuric acid, ammeline and ammelide in Chinese surface soils and select nitrogenous

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fertilizers; (2) elucidate sources and factors that affect melamine and cyanuric acid concentrations

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in soil; (3) examine the spatial distribution of melamine in Chinese soils; and (4) assess ecological

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risks of melamine in soils.

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■ MATERIALS AND METHODS

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Sample Collection. A total of 98 surface soil samples were collected across China during April

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to August 2017. The samples were collected at a depth of 0–10 cm using a handheld corer that was

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cleaned (in water) before and after each sample. The sampling locations are shown in Figure S1,

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and a detailed description of the sampling sites is given in Table S1 (in the Supporting Information).

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It should be noted that the sampling sites were selected randomly, primarily based on accessibility,

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and may not represent the entire geographical area. The samples consisted of soils from 5

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background, 20 rural, 47 urban, and 26 farmland locations. The background locations were remote

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forests >10 km away from any residential area. All rural and urban soils were forest, grassland,

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and roadside soils. Farmland soils were from currently cultivated agricultural lands. Soils were 5

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collected from multiple spots within a given location and then mixed thoroughly to obtain a

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representative sample. Soil samples were stored in pre-cleaned polypropylene (PP) tubes and

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transported to the laboratory, where they were air dried, sieved (< 2.0 mm), transferred into new

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PP tubes and stored at -20 °C until analysis.

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Six types of commercial nitrogenous fertilizers (n = 16) were purchased from agricultural

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chemical stores, and that include six synthetic fertilizers, four ureas, three nitrolimes, and a single

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sample of an organic fertilizer, calcium ammonium nitrate, and ammonium sulfate. All of these

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fertilizers were popular brands, commonly used by farmers as a source of nitrogen in China.

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Sample Pretreatment and Instrumental Analyses. Two different solid-liquid extraction

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methods were applied for the analysis of soil and fertilizer as described elsewhere.16, 22 Briefly, 0.1

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g of soil was extracted with 5 mL of methanol by shaking in an orbital shaker (250 oscillations/min;

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Eberbach, Ann Arbor, MI) for 6 h, after fortification with 10 ng of internal standard (ISs) mixture

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(15N3,13C3-melamine, 13C3-ammeline, 13C3-ammelide, and 15N3,13C3- cyanuric acid). Fertilizer (0.1

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g) samples were extracted with 40 mL of 5% formic acid in water (v/v), by shaking for 6 h, after

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fortification with ISs. The mixture was then centrifuged for 10 min at 4000 g (Eppendorf

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Centrifuge 5804, Hamburg, Germany), and the supernatant was transferred into another PP tube.

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For soil samples, the extraction step was repeated twice with 5 mL of 5 % formic acid in methanol

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(v/v), followed by concentration and solvent-reconstitution with 500 μL of the HPLC mobile phase

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(see below). For fertilizers, following extraction, 0.5 mL of the supernatant was diluted to 5.0 mL

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with the HPLC mobile phase. The final solutions were filtered through nylon syringe filters (pore

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size 0.2 µm; Corning, NY) directly into a glass vial for analysis by high performance liquid

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chromatography-tandem mass spectrometry (HPLC-MS/MS).

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Identification and quantification of melamine, cyanuric acid, ammeline and ammelide were

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performed on a Shimadzu LC-30AD Series HPLC system interfaced with API 5500 triple-

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quadrupole (MS/MS) mass spectrometer. Analytes were separated using acetonitrile (A) and 5

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mM ammonium formate buffer (pH 4.0; B) as mobile phases, by passing them through a Luna®

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hydrophilic-lipophilic interaction liquid chromatography column (100 mm × 3.0 mm, 3.0 μm

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particle size; Phenomenex, Torrance, CA). Two acquisition modes were used, i.e., the negative

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mode was applied for cyanuric acid and ammelide detection (0–4.5 min) and the positive mode

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was applied for melamine and ammeline detection (4.5–18 min). Compound specific MS/MS

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parameters as well as typical chromatograms of the target analytes present in samples are shown

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in Table S1 and Figure S2, respectively.

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Quality Assurance (QA)/Quality Control (QC). The carryover of target analytes between

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samples was eliminated by rinsing the autosampler syringe with a mixture of acetonitrile-water

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(50:50, v/v). Procedural blanks were analyzed by passing water through the entire analytical

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procedure. Both solvent blanks (acetonitrile) and procedural blanks were injected after every 20

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samples and no target analytes were found in blanks (Figure S2D). Quantification of target analytes

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was achieved by a ten-point calibration curve, that ranged in concentrations from 0.05 to 200

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ng/mL, and the regression coefficient of the calibration curve was >0.99. Duplicate analysis of

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randomly selected samples (n = 10) showed a coefficient variation of < 20% for the concentrations

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of target compounds measured in samples. The recoveries of target compounds (spiked at 20 and

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200 ng each) fortified into soils were between 75% and 96%. The average recoveries of ISs spiked

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into all soil samples were 81% for

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ammelide, and 70% for

15N ,13C -melamine, 3 3

15N ,13C -cyanuric 3 3

68% for

13C-ammeline,

72% for

13C-

acid. Isotope dilution method was used in the

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quantification. Limits of quantitation (LOQs; signal-to-noise ratio of 10) were 0.12 ng/g for

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melamine, 0.20 ng/g for ammeline, 0.10 ng/g for ammelide, and 0.25 ng/g for cyanuric acid.

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■ RESULTS AND DISCUSSION

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Occurrence of Melamine and Its Derivatives in Soils and Fertilizers. Melamine and its

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derivatives were found ubiquitous in surface soils, with a detection frequency (df) of 100% for

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melamine, ammelide, and cyanuric acid and 85% for ammeline (Table 1). The total concentrations

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of ∑Melamine (sum of melamine and its three derivatives) ranged from 8.67 to 2020 ng/g dry

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weight (dw), with a mean value of 213 ng/g dw and a median value of 78.3 ng/g dw. Among the

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four compounds analyzed, melamine (mean: 176 ng/g dw) was the predominant, followed by

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cyanuric acid (25.4 ng/g dw), ammeline (7.47 ng/g dw), and ammelide (4.11 ng/g dw). In an earlier

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study that focused on melamine contamination in soils near manufacturing factories, this

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compound was rarely found in farm soils >150 km away from the point sources of contamination.25

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Nevertheless, ubiquitous occurrence of melamine and its derivatives in soils in our study suggests

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the existence of major sources that contribute to contamination.

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To elucidate the sources of these compounds in Chinese surface soil, we analyzed 16

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commercially available nitrogenous fertilizers. Nitrogenous fertilizers such as urea were suspected

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as the sources of melamine/cyanuric acid, due to their similarities in chemical structure. The

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measured concentrations of melamine and its derivatives in fertilizers are shown in Table S3.

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Melamine and its derivatives were found in all fertilizers, and their concentrations ranged from

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4.37 to 483 (mean: 66.8) μg/g for melamine, from 0.206 to 26.4 (mean: 4.03) μg/g for ammeline,

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from 0.188 to 35.2 (mean: 8.49) μg/g for ammelide, and from 11 to 5260 (mean: 994) μg/g for

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cyanuric acid (Table 1). Except for cyanuric acid, the measured concentrations were below the 8

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provisional limit of 0.4% for melamine, as issued by the Food Safety and Consumer Affairs Bureau,

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Ministry of Agricultural, Forestry and Fisheries of Japan.28 Among six types of fertilizers analyzed,

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relatively high concentrations of melamine and cyanuric acid were found in nitrolime (n=3; mean:

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284 µg/g) and urea (n = 4; mean: 3160 µg/g), respectively. China is the largest producer and

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consumer of nitrogenous fertilizers and approximately 41 million tons of nitrogenous fertilizers

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were used in 2016 in China.29 These results suggest that fertilizers are the main sources of

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melamine and its derivatives found in soils in China. In addition, it should be noted that melamine

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and its derivatives can be formed from the transformation triazine-based herbicides like

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cyromazine.30 Other sources of melamine and cyanuric acid in soils include application of poultry

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manure, wastewater and sludge.20, 26, 31, 32

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Profiles and Correlations. The contribution of each target compound to the sum concentration

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of all four derivatives (∑Melamine) in soils and fertilizers is shown in Figure 1. For soils,

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melamine accounted for 63% (range: 10–99%) of the total concentrations, followed by cyanuric

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acid (range: 0.5–79%; mean: 28%), ammeline (range: 0.005–30%; mean: 6.0%), and ammelide

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(range: 0.15–13%; mean: 3%). For fertilizers, the composition of melamine and its derivatives

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varied depending on the fertilizer type. Specifically, cyanuric acid accounted for 99% of the total

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concentrations in ureas, followed by synthetic (89%) and ammonium (74%) fertilizers. In contrast,

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melamine was the most abundant compound found in nitrolime (72%). Cyanuric acid can be

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formed by thermal degradation of urea. The measured concentrations of melamine and cyanuric

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acid are impurities of these compounds formed during the fertilizer production processes.

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In our earlier studies, we showed that melamine (59% of total) was the most abundant compound,

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followed by cyanuric acid (38%) in indoor dust samples.16 In contrast, cyanuric acid (68–82%)

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was the major compound found in infant formulas, dairy products, and human urine.8, 33 These 9

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results suggest a compositional shift from melamine to cyanuric acid from environmental (e.g. soil

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and dust) to biological samples (e.g. food, urine). Melamine was the dominant compound in

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environmental matrices, whereas cyanuric acid was the prevalent compound in biological samples.

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Biotransformation of melamine to cyanuric acid in soils and by microbial cultures has been

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reported earlier.27, 34, 35 Further studies are needed to understand the fate of melamine and cyanuric

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acid in the food chain, especially in agricultural ecosystems.

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A significant correlation (Spearman correlation; 0.406 < r < 0.578, p < 0.01) existed between

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the concentrations of melamine and ammeline/ammelide (Table S4), which indicated a common

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source of origin for these three compounds. These results are consistent with the fact that ammeline

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and ammelide are intermediates formed during environmental and biological transformation of

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melamine or are present as impurities in melamine-based products.36 A significant (Spearman

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correlation; p < 0.01), but weak correlation (r = 0.261), however, was found between melamine

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and cyanuric acid (Table S4), which suggested the existence of multiple sources for these two

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compounds. On the one hand, cyanuric acid can be formed from the hydrolysis of melamine. On

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the other hand, cyanuric acid by itself is used in a variety of applications. As a hydrolysate of

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chloroisocyanurates (e.g., sodium dichloroisocyanurate and potassium dichloroisocyanurate),

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cyanuric acid is used in dishwashing detergents, sanitizing solutions, and drinking water treatment

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products.37

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Geographical Distribution of Melamine and Its Derivatives in Surface Soils. The spatial

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distribution of ∑Melamine in Chinese surface soils was examined on the basis of land-use pattern,

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administrative divisions, latitude, and longitude (Figure 2). The sampling locations were classified

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into four land-use categories, i.e. farmland, urban, rural and background; six administrative

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divisions namely, East China (EC), Northeast China (NE), Southwest China (SW), Northwest 10

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China (NW), South Central China (SC), and North China (NC).38 Depending on the economic

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development and climate, latitude and longitude were divided into three subgroups, i.e., [< 30oN,

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30–38oN, >38oN] and [120oE].

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Soil samples collected from farmlands (mean: 545 ng/g dw) contained significantly higher

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∑Melamine concentrations than those from urban (114 ng/g dw), rural (61.1 ng/g dw), and

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background (16.4 ng/g dw) areas (Independent sample t-test; p < 0.001; Figure 2A). High

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concentrations in farm soils suggest exposure to melamine and cyanuric acid found in nitrogenous

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fertilizers. In comparison to rural soils, significantly higher ∑Melamine concentrations were found

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in urban soils (Independent sample t-test; p < 0.05), which suggests the existence of other potential

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sources in the urban environment. Melamine is used in products such as paints, dinnerware,

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plastics and flooring. Remarkable spatial variation was found in ∑Melamine concentrations among

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the six administrative divisions. Surface soil collected from EC contained the highest

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concentrations of ∑Melamine (mean: 320 ng/g dw), followed by those from NE (281 ng/g dw),

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SW (270 ng/g dw), NW (225 ng/g dw), SC (103 ng/g dw), and NC (84 ng/g dw) (Figure 2B). This

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spatial distribution pattern aligns with the application rates of nitrogenous fertilizers across

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China.39 The concentrations of ∑Melamine in soils were enriched in eastern part (> 120 oE; mean:

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381 ng/g dw) at low latitudes (< 30 oN; mean: 273 ng/g dw) (Figure 2C and D). This region is also

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known for its intensive industrial and e-waste recycling operations in China.40,

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geographical pattern of contamination was reported for brominated flame retardants, perchlorate,

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and per- and poly-fluoroalkyl substances.38,

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production of melamine-formaldehyde resin which is used in the manufacture of plastics,

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kitchenware, and dishware.44 In addition, melamine and cyanuric acid are used as flame retardants

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in furnishings, intumescent paints, textiles, and electrical appliances.45

42, 43

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A similar

Melamine and its derivatives are used in the

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Hazard Assessment. Potential hazards of melamine contamination in soil were evaluated through a hazard quotient (HQ) approach, as shown in Eq (1): HQ = PECsoil/PNECsoil

(1)

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where PECsoil is the melamine concentration in soil (ng/g dw). PNECsoil is the predicted no-

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effect concentration (ng/g dw). A PNEC value of 500 ng/g soil was adapted from a study that

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measured growth of four plants, Hordeum vulgare, Tritium aestivum, Raphanus sativus, and

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Lepidum sativum in melamine contaminated soil.18 This value was derived from the LC50 value

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(median lethal concentration), which was then divided by a safety factor of 1000. However,

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PNECsoil values were not available for ammeline, ammelide and cyanuric acid and therefore HQs

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were not calculated for these three compounds. A HQ value of ≥ 1 indicates a potential risk; 0.1 ≤

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HQ ≤ 1 indicates a moderate to low risk; and 0.01 ≤ HQ ≤ 0.1 indicates minimal to negligible risk.

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Overall, the calculated HQ values in Chinese soils ranged from 0.0025 to 4.02 with mean value

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of 0.351. These HQ values were 1~2 orders of magnitude higher than those reported for soils from

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a melamine factory in China (3.5 × 10-4 to 1.1 × 10-2).18 The HQ values were < 0.1 for 47% of soil

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samples, which suggested a minimal/negligible risk from melamine contamination (Figure 3). A

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moderate to low risk was found for 46% of the soil samples analyzed (HQ: 0.1–1). The HQ values

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were above 1 for 7 of 98 surface soil samples, indicating a potential for risk from melamine

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contamination. Another study reported a soil PNEC value of 2500 ng/g for earthworm.46 The calculated HQ values

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based on earthworm reproduction were 0.0005–0.804 with a mean value of 0.070. It should be noted that there exists

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considerable uncertainty in PNEC values for soil melamine. Further studies are needed to assess the effects of cyanuric

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acid in combination with melamine in soil ecosystems.

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Previous studies have reported uptake of melamine by crop plants.25, 47, 48 Melamine was also

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found in farm animal tissues (e.g., pigs, ruminants, fish, and poultry) and products (e.g., eggs and

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milk).25, 49-53 Our study provides evidence that residual melamine and its derivatives present in 12

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nitrogenous fertilizers contribute to contamination of farm soils, which results in food chain

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transfer and human exposures. Environmental fate of melamine in agricultural ecosystems requires

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further studies.

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■ ASSOCIATED CONTENT

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Supporting Information

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Details of analytical materials/reagents, instrumental analysis, and data analysis. Tables

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containing multiple reaction monitoring (MRM) transitions of target chemicals (Table S1),

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information on soils and fertilizers as well as corresponding target chemical concentrations (Table

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S2 and S3) and correlation analysis (Table S4). Figures showing sampling locations (Figure S1)

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and typical chromatograms of target chemicals in soil and fertilizers (Figure S2). This information

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is available free of charge on the ACS Publications website.

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■ AUTHOR INFORMATION

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Corresponding Authors

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*Phone: +1 518 474 0015; fax: +1 518 473 2895; e-mail:

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[email protected].

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Notes

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The authors declare no competing financial interest.

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Table 1. Concentrations of melamine, cyanuric acid, ammeline and ammelide in surface soils (ng/g dw) and fertilizers (µg/g) collected from China

Soil (n=98; ng/g dw)

Fertilizer (n=16; µg/g)

Min-Max Mean Median df/% Min-Max Mean Median df/%

Melamine 1.23–2010 176 55.9 100 4.37–483 66.8 9.04 100

Ammeline nd–96.1 7.47 3.44 85 0.206–26.4 4.03 1.54 100

Ammelide 0.106–54.7 4.11 1.91 100 0.188–35.2 8.49 2.99 100

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Cyanuric acid 3.68–211 25.4 17.0 100 11–5255 994 250 100

∑Melamine 8.67–2020 213 78.3 100 17.4–5600 1070 458 100

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Figure 1. Composition profiles of melamine and its derivatives in surface soil and fertilizer samples collected from China. SF: synthetic fertilizer; Others: including organic fertilizer, calcium ammonium nitrate, and ammonium sulfate.

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Figure 2. Mean ∑melamine (sum of melamine and its three derivatives; error bars for 95% confidence intervals) concentrations stratified by land use pattern (A), administrative divisions (B), latitude (C), and longitude (D) of surface soil samples collected from mainland China. FL: farmland; UR: urban; RU: rural; BG: background. EC: East China; NE: Northeast China; SW: Southwest China; NW: Northwest China; SC: South Central China; NC: North China. *: p < 0.05; ***: p < 0.001.

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Figure 3. Distribution of hazard quotients of melamine in surface soils collected from China. The HQ values displayed here were calculated from the reference value available for plants (500 ng/g soil) from the OECD report in 1998.

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