Article Cite This: Environ. Sci. Technol. XXXX, XXX, XXX−XXX
pubs.acs.org/est
Neonicotinoid Residues in Fruits and Vegetables: An Integrated Dietary Exposure Assessment Approach Chensheng Lu,†,‡ Chi-Hsuan Chang,‡ Cynthia Palmer,§ Meirong Zhao,† and Quan Zhang*,†,‡ †
Key Laboratory of Microbial Technology for Industrial Pollution Control of Zhejiang Province, College of Environment, Zhejiang University of Technology, 18 Chaowang Road, Hangzhou, Zhejiang 310032, PR China ‡ Department of Environmental Health, Harvard T. H. Chan School of Public Health, Boston, Massachusetts 02215, United States § American Bird Conservancy, Washington, District of Columbia 20008, United States S Supporting Information *
ABSTRACT: Neonicotinoids have become the most widely used insecticides in the world since introduced in the mid 1990s, yet the extent of human exposure and health impacts is not fully understood. In this study, the residues were analyzed of seven neonicotinoids in fruit and vegetable samples collected from two cross-sectional studies: the U.S. Congressional Cafeteria study (USCC) and the Hangzhou China (HZC) study. We then employed a relative potency factor method to integrate all neonicotinoids in each food sample using the respective reference dose values as the basis for summation. The findings were compared with data published by the U.S. Department of Agriculture Pesticide Data Program (USDA/PDP). Imidacloprid and thiamethoxam were the most commonly detected neonicotinoids in fruits and vegetables with 66 and 51% detection in the HZC study and 52 and 53% detection in the USCC study, respectively. The overall frequency of detection for neonicotinoids in the USDA/PDP samples was much lower than those reported here for the USCC or HZC studies, with imidacloprid being the most frequently detected neonicotinoid at 7.3%. The high frequencies of neonicotinoid detection in fruits and vegetables in the USCC and HZC studies give us a snapshot of the ubiquity of neonicotinoid use in global agriculture and make it clear that neonicotinoids have become part of the dietary staple, with possible health implications for individuals.
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contaminated by at least one neonicotinoid,10 a finding which may be related to the phenomenon of honey bee colony collapse disorder worldwide.11 Besides potential exposure to nontarget organisms like bees and birds, human beings could also be frequently exposed to neonicotinoids through ingesting neonicotinoid-contaminated foods and water, respectively. Sanchez-Bayo reported individual seeds of crops treated with neonicotinoids usually contained 1−17 mg/kg neonicotinoids, and 2−20% of neonicotinoids were taken up by the plants, with approximately 80−98% of neonicotinoids on the seeds releasing directly into the soil or groundwater.12 These results suggest that neonicotinoids may be ubiquitous in the environment. Several studies have reported that neonicotinoids were detected in children’s urine in China and Japan.13,14 However, limited studies have identified the sources of neonicotinoids to which human beings could be exposed, regardless of the increasing trend of neonicotinoids use around the world.
INTRODUCTION Neonicotinoids have quickly become the most widely used insecticides in the world since their introduction in the mid 1990s. They are commonly applied as insect controls in agricultural settings, particularly in seed treatments for crops, such as corn, soybeans, cereals, and oilseed rape.1−4 It is estimated that more than 4 million pounds (about 1.8 million kilograms) of neonicotinoid active ingredients have been used on 140−200 million acres (about 567−809 000 km2) of farmland annually in the United States,5 accounting for more than 20% of the world insecticide market6 and valued at approximately $1.4 billion to the U.S. economy.7 Because of their systemic properties, neonicotinoids can be absorbed by roots and then translocated to almost every tissue of the plants, including leaves, flowers, pollen, nectar, and crops grown by those plants once applied.8,9 Therefore, from the pest control perspective, neonicotinoids and other systemic pesticides have what sound like beneficial attributes. However, the adverse ecological, environmental, and public health implications of neonicotinoid residues in pollen, nectar, crops, and fruits can also be problematic and should be examined. Recent studies have shown that approximately 73% of pollen and honey collected from bees and their hives were © XXXX American Chemical Society
Received: Revised: Accepted: Published: A
November 1, 2017 January 25, 2018 January 30, 2018 January 30, 2018 DOI: 10.1021/acs.est.7b05596 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
were processed and analyzed in the College of Environment at Zhejiang University of Technology in Hangzhou, following the same procedures (described below) as were used at the Harvard T. H. Chan School of Public Health. We also obtained neonicotinoid residue data for fruits and vegetables from USDA/Pesticide Data Program (PDP) for 6 neonicotinoids (nitenpyram was not analyzed), measured in 22 fruits and 29 vegetable commodities from 2011 to 2014 for a total of 39 159 data points. USDA/PDP was initiated in 1991 to analyze pesticide residue in foods, and the data have been used primarily by the U.S. Environmental Protection Agency (EPA) for dietary exposure and risk assessments for the review of maximum residue limits (pesticide tolerances). USDA/PDP commodity samples were selected to reflect the highest U.S. consumption with an emphasis on foods consumed by infants and children. Commodities were collected at terminal markets and large chain store distribution centers from which food commodities are supplied to supermarkets and grocery stores that are typically available to the consumers. Commodities selected by USDA/PDP are cycled through approximately every 5 years. In the USCC study, we collected vegetable and fruit samples for the purpose of detecting the residues of neonicotinoids. We selected these cafeterias to obtain samples because they are run by a food service company that publicly recognizes its corporate commitment to sustainability, as well as social and environmental responsibility. In the HZC study, we obtained the amount of fruits and vegetables consumed from the 24 h dietary consumption questionnaires by children of ages 8−10 years from an elementary school in Hangzhou. Analysis of Neonicotinoid Residues in Fruits and Vegetables. We analyzed 64 fruit and vegetable samples collected by the USCC study for 7 neonicotinoids, including acetamiprid, clothianidin, dinotefuran, imidacloprid, nitenpyram, thiacloprid, and thiamethoxam, using a recently published analytical method by LC-MS/MS.9 A total of 134 fruit and vegetable samples collected by the HZC study were also analyzed for the same 7 neonicotinoids, plus imidaclothiz a unique neonicotinoid only manufactured and used in China, using the same method as Chen et al. with minor modifications to accommodate instrumental differences.9 Briefly, we used HPLC-grade acetonitrile and formic acid from Merck (Rahway, NJ) and QuEChERS (containing 4 g of MgSO4, 1 g of NaCl, 500 mg of disodium citrate, and 2 mL of SPE with a ceramic homogenizer containing of 25 mg of PSA, 7.5 mg of GCB, and 150 mg of MgSO4) from Agilent (Shanghai, China) for sample extraction. Then, 10 g of fruit and vegetable samples were weighed, transferred to a 50 mL centrifuge tube, and shaken for 30 s. Next, 10 mL of acetonitrile and 20 μL of internal standards solutions were added to the tube followed by treatment with one pack of QuEChERS salt and one ceramic homogenizer. The tubes were then shaken vigorously for 40 s in the shaker and centrifuged for 4 min at 4000g. Separation and detection of the neonicotinoids were achieved by the UPLC−MS/MS (Waters Corporation, Milford, MA) interfaced with a triple quadrupole mass spectrometer Xevo TQ-S (Waters Corporation) using an Acquity HSS T3 column (50 mm × 3.0 mm, 1.8 μm, Waters Corporation). The system was run in isocratic mode with the mobile phase consisting of acetonitrile and Milli-Q water (95/5 V:V) acidified with 0.01% formic acid at a flow rate of 170 μL/min. Quality assurance (QA) and quality control (QC) samples using several commodity samples were also prepared and analyzed to ensure
The extent of human health impacts resulting from neonicotinoid exposure is not yet fully understood because few exposure and toxicological data are available. Previous in vitro and in vivo studies have shown that the primary mode of action of neonicotinoids is to act on the nicotinic acetylcholine receptor (nAChRs) in the central nervous system, subsequently leading to neurobehavioral deficits and increased expression of glial fibrillary acidic protein in the motor cortex and hippocampus.15,16 U.S. EPA’s risk assessments note that in mammals, neonicotinoids are neurotoxic and are associated with liver, kidney, thyroid, testicular, and immune system effects.17 Marfo et al. reported the association between urinary N-desmethyl-acetamiprid and the symptoms by a prevalence case control study.18 Cimino et al. also confirmed sublethal effects of neonicotinoids on neurological impairments of human beings.19 Those findings on sublethal exposures are highly relevant to public health. Because of their systemic properties, neonicotinoids in foods cannot be easily removed by washing or peeling, so they could pose a dietary risk in individuals. Therefore, considering the ubiquity of neonicotinoids in the environment and foods, it is prudent to assess dietary intake of neonicotinoids at the population level so that the potential health risks can be more closely examined.20−22 In this study, we report neonicotinoid residues measured in foods that are commonly consumed in cafeterias in the United States and by a group of Chinese elementary school children living in Hangzhou, China. We then compare the findings with data published by the U.S. Department of Agriculture Pesticide Data Program (USDA/PDP). The individual, as well as the total neonicotinoid residues in foods reported here, will be essential for facilitating future dietary exposure and health risk characterization and assessments.
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MATERIALS AND METHODS Sample/Data Collections. We analyzed neonicotinoid residues in fruits and vegetables collected in repeated sampling from two cross-sectional studies: the U.S. Congressional Cafeteria study (USCC) and the Hangzhou China (HZC) study. In the USCC study, we collected 36 and 28 samples from the U.S. Congressional cafeterias in winter (January) and spring (May) of 2015, respectively. Approximately half of the samples were purchased from the House Longworth Cafeteria and half from the Senate Dirksen Cafeteria. We set out to sample as many different food items as possible from both cafeterias to ensure a representative selection of foods that people often consume. Individual food items were placed in Ziploc bags, and then shipped on ice overnight from Washington, DC, to Boston, MA, for residue analysis in the lab at Harvard T. H. Chan School of Public Health.9 In the Hangzhou China Study (HZC), we collected fruit and vegetable samples from a group of 58 children ages 8−10 years (26 male and 32 female) from an elementary school in Hangzhou, Zhejiang, China in 2015. We gave 24 h dietary consumption questionnaires for 5 consecutive weekends to each child. We gathered information about food type, the amount of food, the time of consumption, and the sources of food purchased (supermarket, conventional market, etc.). We then bought food from the actual vendors, either in a traditional market or a supermarket, patronized by the parents in a marketbasket approach, in order to better reflect neonicotinoid residues in the fruits and vegetables consumed. All the participants received approved informed consent prior to participating in the HZC study. All fruit and vegetable samples B
DOI: 10.1021/acs.est.7b05596 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
Table 1. Neonicotinoid Residues (μg/kg) in Fruits and Vegetables Collected from the U.S. Congressional Cafeteria (USCC) Study in 2015a food item
ACEb
N
LOD (μg/kg)i RfD (mg/kg/day)j prevalence of detections for each compound (%) apple 6
CLOc
DINd
IMIe
THIg
THIAh
0.03 0.07 28.1
0.03−0.15 0.01 35.9
0.03−0.15 0.02 26.6
0.03−0.15 0.06 51.6
0.03−0.15 N.A. 6.3
0.03 0.004 3.1
0.03 0.006 53.1
