Source: MICHIGAN STATE UNIV submitted to
MECHANISTIC UPTAKE OF CHEMICALS OF EMERGING CONCERN BY VEGETABLE CROPS FROM WATER AND SOIL
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
AFRI COMPETITIVE GRANT
Reporting Frequency
Annual
Accession No.
1008020
Grant No.
2016-67017-24514
Project No.
MICL08514
Proposal No.
2015-05691
Multistate No.
(N/A)
Program Code
A1331
Project Start Date
Nov 1, 2015
Project End Date
Oct 31, 2019
Grant Year
2016
Project Director
Li, H.
Recipient Organization
MICHIGAN STATE UNIV
(N/A)
EAST LANSING,MI 48824
Performing Department
Plant, Soil and Microbial Sci
Non Technical Summary
Background. Consumption of pharmaceutical-tainted fresh produce, especially raw vegetables, represents a direct route of human exposure to chemicals of emerging concern (CECs). The major sources for human and veterinary pharmaceuticals that accumulated in vegetables can be tracked to the agricultural lands and irrigation water containing CECs. Land application of biosolids derived from livestock manures and sewage sludges, and agricultural irrigation with reclaimed water, are the major practice responsible for the accumulation of pharmaceuticals in fresh produce including vegetables. Although the pharmaceuticals typically found in fresh produce are usually below acceptable levels for daily intake, consumption of agricultural produce containing antibiotics could plausibly increase the populations of antibiotic resistant bacteria in the intestinal tracks of human and animals. Mitigating the accumulation of antibiotics in fresh produce during agricultural production is a crucial first step in improving food safety, which surely reduces human exposure to antibiotics. However, currently it is unclear how pharmaceuticals move into vegetables during growth, and the extent to which they accumulate. A better understanding the mechanism of vegetable uptake and accumulation of pharmaceuticals from soil and water will enable the development of scientifically-informed management practice that can help vegetable producers ensure food safety by minimizing or eliminating pharmaceuticals in fresh produce.Overall Hypothesis. The overarching objective is to elucidate the mechanism of pharmaceutical uptake by vegetables growing in water-soil systems. We hypothesize that pharmaceutical translocation to vegetables is controlled water flow in both soils and plants. Pharmaceutical accumulation depends on vegetable type, interaction of pharmaceuticals with plant tissue constituents, and the growth conditions.Specific Aims. (1) Screen and rank the uptake of multiple representative human and veterinary pharmaceuticals by selected vegetables (carrot, celery, cucumber and lettuce). (2) Evaluate sorption by vegetables and growth factors influencing the rate and magnitude of pharmaceutical uptake and accumulation in vegetables. (3) Assess the influence of pharmaceutical sorption/desorption in soils on the uptake by vegetable roots. (4) Investigate novel soil management and irrigation practices designed to minimize pharmaceutical accumulation in vegetables.Approaches. Vegetable uptake of representative pharmaceuticals will be investigated using both hydroponic and soil-pot experiments. Pharmaceuticals in plant tissues, soil and water will be extracted and quantitated by LC-MS/MS using the methods developed and used in our laboratory. The kinetics and magnitude of pharmaceutical uptake will be measured, and related to physicochemical properties of the pharmaceuticals, sorption by plant constituents, and with water flow in both soils and vegetables. In the pot experiments soils with different sorptive constituents (e.g. organic matter, clays) and textures will be used to delineate the role of sorption and water flow in influencing pharmaceutical accumulation in vegetables.Potential Impact and Expected Outcomes. New fundamental understanding is needed for mitigating uptake and accumulation of pharmaceuticals in fresh produce and vegetables. The results from this research project will be published in peer-reviewed journals, presented at conferences and outreach events in order to effectively transfer the knowledge to scientific communities, food producers, industries, policy makers, and the general public. Such knowledge helps guide vegetable producers to develop scientifically informed management practices that ensure food safety during the production phase, and ultimately to minimize chemical hazards in the fresh produce delivered to the public.
Animal Health Component
0%
Research Effort Categories
Basic
60%
Applied
30%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
1020110200030%
1020210200030%
1021499200040%
Knowledge Area
102 - Soil, Plant, Water, Nutrient Relationships;

Subject Of Investigation
1499 - Vegetables, general/other; 0110 - Soil; 0210 - Water resources;

Field Of Science
2000 - Chemistry;
Goals / Objectives
Our overarching objective is to elucidate the mechanism(s) governing the uptake of pharmaceuticals from water and soil by vegetables. This knowledge will facilitate the development of best management practices to mitigate the accumulation of CECs in vegetable fresh produce. The proposed project directly addressesphysical or molecular mechanisms that allow foodborne hazards of pharmaceuticals to internalize into fresh produce. Consumption of pharmaceutical-tainted fresh produce, especially raw vegetables, represents a direct route of human exposure to CECs. The trace levels of pharmaceutical mixtures in fresh vegetable produce might adversely affect human health. Moreover, antibiotics (one major class of pharmaceuticals proposed for study) could exert selective pressure on native antibiotic resistant populations of bacteria in human and animal gastrointestinal tracks hence accelerating the development and proliferation of antibiotic resistance. Reducing uptake of CECs by vegetables during agricultural production is a key step in improving food safety. Surely, reduced uptake by vegetables reduces human exposure to pharmaceuticals in natural environments.Little is known about the mechanism of pharmaceuticals movement into vegetables from soil and water. Here, our central hypothesis is that water flow in soils and vegetables is the major process by which pharmaceuticals translocate from soil and water to vegetables. The accumulation of pharmaceuticals depends on vegetable types, plant tissue constituents and growth condition, physicochemical properties of CECs, and soil properties. Mitigating uptake of CECs by vegetables could be achieved by reducing CEC concentrations in soil water flowing into vegetables. To test this hypothesis, and to achieve our overall research goals, we propose the following four specific aims:(1) Quantify and rank the uptake of multiple representative human and veterinary pharmaceuticals by selected vegetables (carrot, celery, cucumber and lettuce)(2) Evaluate which vegetable organs (roots, leaves etc.) and growth factors most significantly influence the rate and magnitude of pharmaceutical uptake and accumulation in vegetables(3) Assess the influence of pharmaceutical sorption/desorption by soils on their uptake via vegetable roots(4) Discover and investigate novel soil management and irrigation practices that minimize pharmaceutical accumulation in vegetables.
Project Methods
We will integrate hydroponic studies and greenhouse soil-pot experiments with advanced analytical measurements that can quantify CECs at very low environmentally relevant concentrations to understand the mechanistic determinants of vegetable uptake of CECs. To achieve Research Objective #1, we will quantify and rank the uptake and accumulation of a wide array of CECs in several representative types of vegetables. The selected vegetables include carrot (root vegetable), celery (stem vegetable), cucumber (fruit vegetable) and lettuce (leaf vegetable). The selection of carrot represents the worst case scenario of direct contact between pharmaceuticals in soil water and the consumed vegetable fraction, which may accentuate the harmful impacts to human health. We select fifteen pharmaceuticals based on consideration of the (large) amounts used for humans and animals, the reported (high) frequencies found in land applied biosolids and in reclaimed water, and the largest hazard quotient values. Hydroponic experiments to measure the uptake and accumulation of CECs in vegetable roots, stems, leaves and fruits as a function of time. The pharmaceuticals in the nutrient solution, vegetable roots, stems, leaves and fruits will be extracted using the QuEChERS method, and quantified by our new state-of-the-art LC-MS/MS system. The results will be systematically analyzed to identify and evaluate any relation(s) between uptake by vegetables and pharmaceutical properties.For Research Objective #2, we hypothesize that transpiration flow is the driving force for the translocation of pharmaceuticals in vegetables. The accumulation of pharmaceuticals is controlled by vegetable types, plant tissue constituents, and physicochemical properties of CECs. Importantly, sorption of CECs by vegetable roots diminishes their translocation in vegetables. To test this hypothesis, we will test vegetable uptake of 15 pharmaceuticals from water as a function of exposure time. In parallel, we will also measure sorption of CECs from nutrient solution by dry vegetable roots, stems, leaves and fruits of the selected vegetables to establish sorption affinity to these structural components. The comparison results could verify our hypothesis that pharmaceuticals strongly sorbed by vegetable roots will have diminished accumulation in the upper compartments of the vegetables such as in stems, leaves, and fruits. The vegetable fractions with strong affinity for pharmaceuticals should lead to greater accumulation in that compartment. To elucidate the role of transpiration flow in translocating CECs to vegetable upper compartments, we will conduct hydroponic experiments quantifying pharmaceutical uptake by vegetables at changing transpiration flows. Plant hormone abscisic acid (ABA) will be applied to vegetables via root uptake to reduce stomata conductance hence diminish transpiration water flow. The uptake and accumulation of target pharmaceuticals in vegetable fractions will be measured, along with their concentration in nutrient solution. By comparing these results with the controls without ABA application, the effects of water transpiration stream on vegetable uptake and accumulation of pharmaceuticals can be evaluated.Under Research Objective #3, we will assess the influence of pharmaceutical sorption and desorption by soils on their uptake via vegetable roots. We will conduct soil-pot experiments to quantify pharmaceutical uptake by vegetables from different types of soils. Pharmaceutical concentrations in vegetable roots, stems, leaves and fruits, as well as in the surrounding soils will be quantified including soil pore water. The pharmaceutical concentration and speciation in soil pore water could provide more insight into their bioavailability for vegetable uptake than the total soil concentration. We will examine how pharmaceutical speciation (neutral, cation and anion) in soil pore water, and soil properties influence pharmaceutical uptake by vegetable roots, and potential relations between accumulation and pharmaceutical characteristics in the soil pore solution. These results are expected to provide insights into how soil properties/processes impact plant uptake.Under Research Objective #4, we will evaluate pharmaceutical uptake by the vegetables grown under surface drip irrigation vs. overhead sprinkler irrigation, simulating the common irrigation scenarios employed with reclaimed water. We will irrigate the vegetable crops with tap water containing the selected CECs by surface drip and overhead sprinkler irrigations using our in-house irrigation system. Among the overhead irrigation treatments, one sub-set of soil pots will have the soil surface covered by a water-impermeable plastic film, and the openings in the middle will be sealed to the vegetable stems with silicone sealant. The other sub-set of overhead irrigation treatments allows the irrigation water to drain directly onto the soil surfaces. By doing so, we will be able to discern the extent of foliar and root uptake for the test pharmaceuticals, and to evaluate the influence of pharmaceutical hydrophilic/lipophilic property on their accumulation in vegetables via foliar uptake.

Progress 11/01/18 to 10/31/19

Outputs
Target Audience:The results gained from this project have been disseminated primarily through publications in peer-reviewed journals and presentations at national and international conferences to scientists, graduate students and policy makers. The results are also reported to the general public who are interested in the relevant issues. In addition, the research and related results are used in the PIs' teaching courses to graduate students and undergraduates at Michigan State University. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided many opportunities to train postdoctoral research associates and graduate students who have been benefited from this research by improving their laboratory skills, critical thinking, data analysis, manuscript writing, and problem solving. These trainings have helped them to advance their professional development and careers. PhD student Ya-Hui Chuang grdautated in 2018, and currently assumed a faculty position at National Chung Hsing University, Taiwan. MS studentGemini Bhalsod graduated in 2017, and current assumed a position at University of Illinois Extension. Postdoctoral research trainee Yuanbo Li is hired as a senior faculty position at Chinese Acedemy of Agricultural Sciences. How have the results been disseminated to communities of interest?The results from this project have been disseminated primarily through publications in leading peer-reviewed journals in environmental science and food sciences, and presentations in national and international professional conferences to scientists and policy makers. The results are also reported to the general public who are interested in the relevant issues, and have been incorporated in several grduate- and undergraduate-level courses taught by PIs at Michigan State University. What do you plan to do during the next reporting period to accomplish the goals?This is the final project report. We are still working on three manuscripts, and hope to publish them in the next year.

Impacts
What was accomplished under these goals? Irrigation with treated wastewater and application of biosolids introduce numerous pharmaceutical and personal care products (PPCPs) into agro-production systems. These PPCPs could enter vegetables and food crops with water flow from soil to plant roots and then shoots. We modified QuEChERS extraction method to analyze PPCPs in plants tissue. Then, we conducted hydroponic studies for uptake of PPCPs by lettuce and radish from water. PPCPs enter plants from roots, and transport to upper fractions. We examined the uptake of thirteen commonly used PPCPs by lettuce. PPCP sorption by lettuce roots was measured in order to evaluate the influence on PPCP transport from roots to shoots. Small-sized pharmaceuticals e.g., caffeine and carbamazepine have smaller molecular weight (MW) <300 g/mol and a low affinity to lettuce roots (sorption coefficient Kp < 50 L/kg) manifested substantial transport to shoots. Small-sized molecules lamotrigine and trimethoprim had a relatively strong affinity to lettuce roots (Kp > 12000 L/kg) and demonstrated a reduced transport to shoots. The accumulation of small-sized PPCPs in plant shoots increased with increasing transpiration stream. Large-sized pharmaceuticals (e.g. MW >400 g/mol) including lincomycin, monensin sodium, and tylosin could be excluded from cell membranes during a short period of uptake (e.g. 6 days), resulting in the predominant accumulation in lettuce roots. Large-sized oxytetracycline existed as zwitterionic species that could slowly enter lettuce roots; however, the relatively strong interaction with lettuce roots limits the transport to shoots. The mass balance analysis revealed that acetaminophen, β-estradiol, carbadox, estrone and triclosan were readily metabolized in lettuce with> 90% loss during 144-h exposure period. A scheme was proposed to describe PPCP uptake and transport in plants, which could reasonably elucidate many literature-reported results. Molecular size, reactivity and ionic speciation of pharmaceuticals, as well as plant physiology, collectively determine their uptake, transport and accumulation in plants. We also conducted pot experiments in greenhouse study. Currently, it is not very clear whether pore water is the carrier facilitating plant uptake of PPCPs from soils. The fate, uptake and distribution of fifteen commonly used pharmaceuticals in soil-water-radish systems were investigated to elucidate the relationship between the accumulation and their physicochemical processes in soils, soil pore water in the study. The results indicate that the distribution of PPCPs between soil and pore water, as well as their biodegradation, combined to govern the bioavailability of PPCPs to plant uptake. Fourteen out of 15 pharmaceuticals could enter radish tissues in which the accumulation varied. Comparison of bioconcentration factors (BCFs) on the basis of PPCP concentration in bulk soil vs. in pore water implies that pharmaceuticals present in soil pore water are the major bioavailable fractions to plant uptake. The pore water-based BCFs exhibited a positive linear relationship with log Dow for the PPCPs with >90% as neutral species in soil pore water, while such relationship was not observed between bulk soil-based BCFs and log Dow mainly due to sorption by soil. Other than hydrophobicity, the dissociation of ionic pharmaceuticals in soil pore water and (or) root cells may lead to the "ion trap" effects and thus influence the uptake and translocation process. The large molecular-size pharmaceuticals (e.g., tylosin) manifested a minimum uptake due plausibly to the limited permeability of cell membranes. Metabolism of pharmaceuticals in plants is important to evaluate their fate and accumulation in vegetables, and subsequently the risks to human health. However, limited knowledge is available to evaluate metabolism of pharmaceuticals in plants due to the lack of appropriate research approaches. We investigated metabolism of PPCPs in intact plants (in vivo) growing in hydroponic solution and in plant tissue enzyme extracts (in vitro). For caffeine, six phase-I demethylation metabolites were identified in the intact radish plant and lettuce. More work is needed to identify and quantify metabolites in plant tissues.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Qiuguo Fu, Tomer Malchi, Laura J. Carter, Hui Li, Jay Gan, Benny Chefetz, 2019, Pharmaceutical and Personal Care Products: From Wastewater Treatment into Agro-Food Systems, Environmental Science and Technology, 53: 14083-14090.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Ya-Hui Chuang, Cheng-Hua Liu, J. Brett Sallach, Raymond Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2019, Mechanistic Study on Uptake and Transport of Pharmaceuticals in Lettuce from Water, Environment International, 131, 104976.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Hui Li, 2019, Uptake, Accumulation and Metabolism of Pharmaceuticals in Soil-Water-Plant Systems. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), San Antonio, Texas. November 10-13. (invited)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Yike Shen, Wei Zhang, Hui Li, Elliot T. Ryser, 2019, Uptake and Accumulation of Antibiotics and Associated Impact on Bacterial Microbiome and Salmonella Survival in Greenhouse Lettuce, International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), San Antonio, Texas. November 10-13.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd and Hui Li, 2019, Relation of Plant Physiological Processes and Compound Physicochemical Properties to Lettuce Uptake of Pharmaceuticals. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), San Antonio, Texas. November 10-13.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Zhirui Qin, Zhenhua Zhao, Liling Xia, Abduelrahman Adam, Yong Li, Deqiang Chen, Sara Margaret Mela, and Hui Li, 2019, The Dissipation and Risk Alleviation Mechanism of PAHs and Nitrogen in Constructed Wetlands: The Role of Submerged Macrophytes and their Biofilms-leaves, Environment International, 131, 104940.


Progress 11/01/15 to 10/31/19

Outputs
Target Audience:The results gained from this project have been disseminated primarily through publications in peer-reviewed journals and presentations at national and international conferences to scientists, graduate students and policy makers. The results are also reported to the general public who are interested in the relevant issues. In addition, the research and related results areused in the PIs' teaching courses to graduate students and undergraduates at Michigan State University. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided many opportunities to train postdoctoral research associates and graduate students who have beenbenefited from this research by improving their laboratory skills, critical thinking, data analysis, manuscript writing, andproblem solving. These trainings have helped them to advance their professional development and careers. PhD student Ya-Hui Chuang grdautated in 2018, and currently assumed a faculty position at National Chung Hsing University, Taiwan. MSstudent Gemini Bhalsod graduated in 2017, and current assumed a position at University of Illinois Extension. Postdoctoralresearch trainee Yuanbo Li is hired as a senior faculty memberat Chinese Acedemy of Agricultural Sciences. How have the results been disseminated to communities of interest?The results from this project have been disseminated primarily through publications in leading peer-reviewed journals inenvironmental science and food sciences, and presentations in national and international professional conferences toscientists and policy makers. The results are also reported to the general public who are interested in the relevant issues. The research hasbeen incorporated in several grduate- and undergraduate-level courses taught by PIs at Michigan State University. What do you plan to do during the next reporting period to accomplish the goals?This is the final report for this project. The previous report was submitted in Feb 2020 mistakenly as a progress report. We submitted it again (by adding new publications)as the final project. We are still seeking additional grants to further elucidate the pathways and mechanism of organic contaminants into food crops and vegetables from soil and water.

Impacts
What was accomplished under these goals? Irrigation with treated wastewater and application of biosolids introduce numerous pharmaceutical and personal care products (PPCPs) into agro-production systems. These PPCPs could enter vegetables and food crops with water flow from soil to plant roots and then shoots. We modified QuEChERS extraction method to analyze PPCPs in plants tissue. Then, we conducted hydroponic studies for uptake of PPCPs by lettuce and radish from water. PPCPs enter plants from roots, and transport to upper fractions. We examined the uptake of thirteen commonly used PPCPs by lettuce. PPCP sorption by lettuce roots wasmeasured in order to evaluate the influence on PPCP transport from roots to shoots. Small-sized pharmaceuticals e.g., caffeine and carbamazepine have smaller molecular weight (MW) <300 g/mol and a low affinity to lettuce roots (sorptioncoefficient Kp < 50 L/kg) manifested substantial transport to shoots. Small-sized molecules lamotrigine and trimethoprim had a relatively strong affinity to lettuce roots (Kp > 12000 L/kg) and demonstrated a reduced transport to shoots. The accumulation of small-sized PPCPs in plant shoots increased with increasing transpiration stream. Large-sizedpharmaceuticals (e.g. MW >400 g/mol) including lincomycin, monensin sodium, and tylosin could be excluded from cellmembranes during a short period of uptake (e.g. 6 days), resulting in the predominant accumulation in lettuce roots. Large-sized oxytetracycline existed as zwitterionic species that could slowly enter lettuce roots; however, the relatively stronginteraction with lettuce roots limits the transport to shoots. The mass balance analysis revealed that acetaminophen, beta-estradiol, carbadox, estrone and triclosan were readily metabolized in lettuce with> 90% loss during 144-h exposure period. Ascheme was proposed to describe PPCP uptake and transport in plants, which could reasonably elucidate many literature-reported results. Molecular size, reactivity and ionic speciation of pharmaceuticals, as well as plant physiology, collectively determine their uptake, transport and accumulation in plants. We also conducted pot experiments in greenhouse study. Currently, it is not very clear whether pore water is the carrier facilitating plant uptake of PPCPs from soils. The fate, uptake and distribution of fifteen commonly used pharmaceuticals in soil-water-radish systems were investigated to elucidate the relationship between the accumulation and their physicochemicalprocesses in soils, soil pore water in the study. The results indicate that the distribution of PPCPs between soil and pore water, as well as their biodegradation, combined to govern the bioavailability of PPCPs to plant uptake. Fourteen out of 15 pharmaceuticals could enter radish tissues in which the accumulation varied. Comparison of bioconcentration factors (BCFs)on the basis of PPCP concentration in bulk soil vs. in pore water implies that pharmaceuticals present in soil pore water are the major bioavailable fractions to plant uptake. The pore water-based BCFs exhibited a positive linear relationship with logDow for the PPCPs with >90% as neutral species in soil pore water, while such relationship was not observed between bulksoil-based BCFs and log Dow mainly due to sorption by soil. Other than hydrophobicity, the dissociation of ionic pharmaceuticals in soil pore water and (or) root cells may lead to the "ion trap" effects and thus influence the uptake andtranslocation process. The large molecular-size pharmaceuticals (e.g., tylosin) manifested a minimum uptake due plausibly to the limited permeability of cell membranes. Metabolism of pharmaceuticals in plants is important to evaluate their fate and accumulation in vegetables, and subsequently the risks to human health. However, limited knowledge is available to evaluate metabolism of pharmaceuticals in plants due to the lack of appropriate research approaches. We investigated metabolism of PPCPs in intact plants (in vivo) growing in hydroponic solution and in plant tissue enzyme extracts (in vitro). For caffeine, six phase-I demethylation metabolites were identified in the intact radish plant and lettuce. More work is needed to identify and quantify metabolites in plant tissues.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Qiuguo Fu, Tomer Malchi, Laura J. Carter, Hui Li, Jay Gan, Benny Chefetz, 2019, Pharmaceutical and Personal Care Products: From Wastewater Treatment into Agro-Food Systems, Environmental Science and Technology, 53: 14083-14090.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Ya-Hui Chuang, Cheng-Hua Liu, J. Brett Sallach, Raymond Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2019, Mechanistic Study on Uptake and Transport of Pharmaceuticals in Lettuce from Water, Environment International, 131, 104976.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Hui Li, 2019, Uptake, Accumulation and Metabolism of Pharmaceuticals in Soil-Water-Plant Systems. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), San Antonio, Texas. November 10-13. (invited)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Yike Shen, Wei Zhang, Hui Li, Elliot T. Ryser, 2019, Uptake and Accumulation of Antibiotics and Associated Impact on Bacterial Microbiome and Salmonella Survival in Greenhouse Lettuce, International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), San Antonio, Texas. November 10-13.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd and Hui Li, 2019, Relation of Plant Physiological Processes and Compound Physicochemical Properties to Lettuce Uptake of Pharmaceuticals. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), San Antonio, Texas. November 10-13.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Zhirui Qin, Zhenhua Zhao, Liling Xia, Abduelrahman Adam, Yong Li, Deqiang Chen, Sara Margaret Mela, and Hui Li, 2019, The Dissipation and Risk Alleviation Mechanism of PAHs and Nitrogen in Constructed Wetlands: The Role of Submerged Macrophytes and their Biofilms-leaves, Environment International, 131, 104940.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Geoff Rhodes, Ya-Hui Chuang, Raymond Hammerschmidt, Wei Zhang, Stephen A Boyd, Hui Li, 2021, Uptake of Cephalexin by Lettuce, Celery, and Radish from Water, Chemosphere, 263: 127916.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Yike Shen, Hui Li, Elliot T Ryser, Wei Zhang, 2021, Comparing Root Concentration Factors of Antibiotics for Lettuce (Lactuca sativa) Measured in Rhizosphere and Bulk Soils. Chemosphere, 262: 127677.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wenfeng Wang, Geoff Rhodes, Jing Ge, Xiangyang Yu, Hui Li, 2020, Uptake and accumulation of per-and polyfluoroalkyl substances in plants, Chemosphere, 261: 127584
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Yuanbo Li, Jianzhou He, Haonan Qi, Hui Li, Stephen A Boyd, Wei Zhang, 2020, Impact of Biochar Amendment on the Uptake, Fate and Bioavailability of Pharmaceuticals in Soil-Radish Systems. Journal of Hazardous Materials, 398: 122852.
  • Type: Journal Articles Status: Submitted Year Published: 2020 Citation: Yan Chen, Enguang Nie, Xinqiang Zheng, Qingfu Ye, Hui Li, Haiyan Wang, 2020, Uptake, Subcellular Distribution and Metabolism of 14C-Caffeine in Leafy Vegetables from Water. Water Research. Submitted


Progress 11/01/17 to 10/31/18

Outputs
Target Audience:The results gained from this project have been disseminated primarily through publications in peer-reviewed journals and presentations at national and international conferences to scientists, graduate students and policy makers. The results are also reported to the general public who are interested in the relevant issues. In addition, the research and related results are used in the PIs' teaching courses to graduate students and undergraduates at Michigan State University. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided many opportunities to train postdoctoral research associates and graduate students who have beenbenefited from this research by improving their laboratory skills, critical thinking, data analysis, manuscript writing, andproblem solving. These trainings have helped them to advance their professional development and careers. PhD student Ya-Hui Chuang grdautated in December 2017. After one-year postdoctorate training at the Ohio State University, she moved to Taiwan as an assistant professor at National Chung Hsing University. How have the results been disseminated to communities of interest?The results from this project have been disseminated primarily through publications aspeer-reviewed journal articles andpresentations in national and international professional conferences to scientists and policy makers. The results are also reported to the general publicwho are interested in the relevant issues, and have been incorporated in several grduate- and undergraduate-level coursestaught by PIs at Michigan State University. What do you plan to do during the next reporting period to accomplish the goals?We have conducted experiments described in Objective 1, 2 and 3, and collected sufficient data for several publications inpeer-reviewed journals. During this reporting period, five manuscripts have been published in major agricultural and environmental science journals. We have requested one-year no-cost extension. During the next peirod of time, we will continueto do conduct the experiments to further evaluate the uptake mechanism of pharmaceuticals in vegetables. At the same time, we will drafttwo more manuscripts, and submitted themfor publication.

Impacts
What was accomplished under these goals? Pharmaceuticals in agricultural soils originating from irrigation with treated wastewater and land applied biosolids can enter field crops. However, little is known about the role of pore water in plant uptake of pharmaceuticals from soils. In this study, the fate, uptake and distribution of fifteen commonly used pharmaceuticals in soil-water-radish systems were investigated to examine the relationship between the accumulation and their physicochemical processes in soils. The results indicate that the distribution of pharmaceuticals between soil and pore water, as well as their biodegradation, combined to govern the bioavailability of pharmaceuticals to plant uptake. Fourteen out of 15 pharmaceuticals could enter radish tissues in which the accumulation ranged from 2.1 to 14080 ng/g. Comparison of bioconcentration factors (BCFs) on the basis of pharmaceutical concentration in bulk soil vs. in pore water implies that pharmaceuticals present in soil pore water are the major bioavailable fractions to plant uptake. The pore water-based BCFs exhibited a positive linear relationship with log Dow for the pharmaceuticals with >90% as neutral species in soil pore water, while such relationship was not observed between bulk soil-based BCFs and log Dow mainly due to sorption by soil. Other than hydrophobicity, the dissociation of ionizable pharmaceuticals in the soil pore water and (or) root cells may lead to the "iontrap" effects and thus influence the uptake and translocation process. The large molecular-size pharmaceuticals (e.g., tylosin) manifested a minimum uptake due plausibly to the limited permeability of cell membranes. Metabolism of pharmaceuticals in plants is important to evaluate their fate and accumulation in vegetables, and subsequently the risks to human health. However, limited knowledge is available to evaluate metabolism of pharmaceuticals in plants due to the lack of appropriate research approaches. In this study, radish was selected as a model plant to investigate metabolism of pharmaceuticals in intact plants (in vivo) growing in hydroponic solution and in plant tissue enzyme extracts (in vitro). For caffeine, six phase-I demethylation metabolites identified in the intact radish plant were also found in the plant enzyme extracts. After 7 days of in vivo exposure, the amount of the identified metabolites was about >5X greater than the parent compound caffeine in radish roots. Furthermore, the metabolism potential of fifteen pharmaceuticals in radish was evaluated on the basis of mass balance. After 7 days of hydroponic exposure, oxytetracycline, trimethoprim, carbamazepine, lincomycin, monensin and tylosin manifested relatively less extent of metabolism with the mass recoveries ranging from 52.3 to 78.2%. In contrast, 17 beta-estradiol, sulfamethoxazole, sulfadiazine, estrone, triclosan, acetaminophen, caffeine, carbadox and lamotrigine underwent extensive metabolism with only 3.0 to 32.1% of the parent compound recovered. In the in vitro system, 17 beta-estradiol, estrone, triclosan, oxytetracycline, acetaminophen, sulfadiazine and sulfamethoxazole were readily metabolized in radish root enzyme extracts with 1.8 to 34.0% remaining after 96-h exposure. While in the leaf enzyme extracts, only triclosan was rapidly metabolized with 49.2% remaining, and others pharmaceuticals were 60%, indicating that the varying extents of metabolism occurred in different plant parts. This study highlights the importance of pharmaceutical metabolism in plants, and suggests that plant tissue enzyme extracts could serve as an alternative tool to assess pharmaceutical metabolism in plants. Pharmaceuticals can be metabolized after being taken up by plants. The metabolites could manifest similar or equivalent bioactivity to the parent compound, promoting the critical need to understand the metabolism in plants. Caffeine has been frequently detected in agriculture produce; however, little attention is given to its metabolites in vegetables. We examined uptake and metabolism of caffeine in lettuce in a hydroponic lettuce system. Caffeine and its metabolites in aqueous solution and lettuce were identified and quantified using a liquid chromatography coupled to a QTrap tandem mass spectrometry instrument. After 144 h, over 50% of applied caffeine dissipated in the hydroponic lettuce system, and eight caffeine metabolites were identified primarily in the shoots. Caffeine underwent step-by-step demethylation reactions, which were confirmed with authentic standards. The total amount of demethylation metabolites accounted for 20% of the initially applied caffeine. Other metabolism pathways included oxidation and hydroxylation, and the amount of metabolites increased over uptake time.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Yuanbo Li, Cary T Chiou, Hui Li, and Jerald L Schnoor, 2019, Improved Prediction of the Bioconcentration Factors of Organic Contaminants from Soils into Plant/Crop Roots by Related Physicochemical Parameters. Environment International. 126:46-53.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Yuanbo Li, J. Brett Sallach, Wei Zhang, Stephen A. Boyd, and Hui Li, 2019, Insight into the Distribution of Pharmaceuticals in Soil-Water-Plant Systems, Water Research, 152: 38-46.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Raymond Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2018, Metabolic Demethylation and Oxidation of Caffeine during Uptake by Lettuce. Journal of Agricultural and Food Chemistry, 66:7907-7915.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Yuanbo Li, Ya-Hui Chuang, J. Brett Sallach, Wei Zhang, Stephen A. Boyd, and Hui Li, 2018, Potential Metabolism of Pharmaceuticals in Radish: Comparison of in vivo and in vitro Exposure. Environmental Pollution, 242:962-969.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Gemini D. Bhalsod, Ya-Hui Chuang, Sangho Jeon, Wenjun Gui, Hui Li, Elliot T. Ryser, Andrey K. Guber, and Wei Zhang, 2018, Uptake and Accumulation of Pharmaceuticals in Overhead- and Surface-Irrigated Greenhouse Lettuce. Journal of Agricultural and Food Chemistry. 66: 822-830.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Geoff Rhodes, Ya-Hui Chuang, Wei Zhang, Stephen A. Boyd, and Hui Li, 2019, Uptake of Cephalexin from Water to Three Vegetables, International Soil Meeting (Soil Science Society of America, Soil Science Society of Canada, and Soil Science Society of Mexico), San Diego, California. January 6-9.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Yuanbo Li, J. Brett Sallach, Wei Zhang, Stephen A. Boyd and Hui Li, 2019, Insight into the Distribution of Pharmaceuticals in Soil-Water-Plant System. International Soil Meeting (Soil Science Society of America, Soil Science Society of Canada, and Soil Science Society of Mexico), San Diego, California. January 6-9.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Hui Li, Ya-Hui Chuang, Cheng-Hua Liu, J. Brett Sallach, Wei Zhang, Ray Hammerschmidt, and Stephen Boyd, 2018, Uptake, Accumulation and Metabolism of Pharmaceuticals in Vegetables. International Symposium on Agro-Environmental Quality, Nanjing, China, November 3-5. (invited)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Hui Li, Yuanbo Li, J. Brett Sallach, Wei Zhang, and Stephen A. Boyd, 2018, Uptake of Pharmaceuticals by Plant from Soils: Role of Soil Pore Water. 2018 International Conference on Agro-Food Safety and Nutrition, Nanjing, Jiangsu, China, October 20-23, 2018. (invited)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Hui Li, 2018, Uptake, Accumulation and Metabolism of Chemicals of Emerging Concern in Lettuce, Peking University, Beijing, China, July 3. (invited)
  • Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Ya-Hui Chuang, 2017, Uptake, Accumulation and Metabolism of Chemicals of Emerging Concern in Vegetables, PhD Dissertation, Department of Plant, Soil and Microbial Sciences, Michigan State University, December 2017.


Progress 11/01/16 to 10/31/17

Outputs
Target Audience:The results from this project have been disseminated primarily through publications in peer-reviewed journals and presentations at professional conferences to scientists, graduate studentsand policy makers. The results are also reported to the general public who are interested in the relevant issues. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided many opportunities to train postdoctoral research associates and graduate students who have been benefited from this research by improving their laboratory skills, critical thinking, data analysis, manuscript writing, and problem solving. These trainings have helped them to advance their professional development and careers. How have the results been disseminated to communities of interest?The results from this project have been disseminated primarily through publications in peer-reviewed journal articles and presentations in professional conferences to scientists and policy makers. The results are also reported to the general public who are interested in the relevant issues, and have been incorporated in several grduate and undergraduate-level courses taught at Michigan State University. What do you plan to do during the next reporting period to accomplish the goals?We have conducted experiments described in Objective 1, 2 and 4, and collected sufficient data for several publications in peer-reviewed journals. During this reporting period, two manuscripts have been submitted for review. We still have data for a few more papers. In the next reporting period, we will focus more on manuscript writing and publication. We will conduct the experiments described under Objective 3 to evaluate the impact of pharmaceutical sorption/desorption by soils to their uptake byvegetables. In fact, we startedtheseexperiments during this reporting period, more data will be collected during the next reporting period, and plan to draft manuscript(s) on this topic for publication.

Impacts
What was accomplished under these goals? Mechanism underlying plant uptake of pharmaceuticals from soil and water remains largely unknown, thus impeding the development of effective measures to mitigate contamination of food crops by pharmaceuticals. In this study, uptake of thirteen commonly used pharmaceuticals by lettuce from water was investigated. Pharmaceutical sorption by lettuce roots was also measured to evaluate its influence on the transport of pharmaceuticals to shoots. Small-sized pharmaceuticals with molecular weight (MW) < 300 g mol−1 entered lettuce via symplast pathway, and those pharmaceuticals with low affinity to lettuce roots manifested substantial transport to shoots which included caffeine and carbamazepine. Small-sized lamotrigine and trimethoprim had relatively high affinity to lettuce roots, which reduced the amount of transport to shoots. Large-sized pharmaceuticals (MW > 400 g mol−1) including lincomycin, monensin sodium, and tylosin could be excluded from cell membranes and moved primarily in apoplast pathway, resulting in predominant accumulation in lettuce roots. Large-sized oxytetracycline existed as zwitterionic species that could slowly enter lettuce via the symplast pathway; however, the relatively strong interaction with lettuce roots limited its transport to shoots. The mass balance analysis indicated that acetaminophen, β-estradiol, carbadox, estrone, and triclosan were readily metabolized in lettuce with ≥ 90% loss during the 144-h exposure period. Molecular size and ionic state of pharmaceuticals, as well as their sorption to root constituents, collectively determine their uptake, transport, and accumulation in plants. Understanding the uptake and accumulation of pharmaceuticals in vegetables under typical irrigation practices is critical to risk assessment of crop irrigation with reclaimed water. This study investigated the pharmaceutical residues in greenhouse lettuce under overhead and soil-surface irrigations using pharmaceuticals-contaminated water. Compared to soil-surface irrigation, overhead irrigation substantially increased the pharmaceutical residues in lettuce shoots. The increased residue levels persisted even after washing for trimethoprim, monensin sodium, and tylosin, indicating their strong sorption to the shoots. The post-washing concentrations in fresh shoots varied from 0.05 ± 0.04 μg/kg for sulfadiazine to 345 ± 139 μg/kg for carbamazepine. Root concentration factors ranged from 0.04 ± 0.14 for tylosin to 19.2 ± 15.7 for sulfamethoxazole. Translocation factors in surface-irrigated lettuce were low for sulfamethoxalzole, trimethoprim, monensin sodium, and tylosin (0.07-0.15), but high for caffeine (4.28 ± 3.01) and carbamazepine (8.15 ± 2.87). Carbamazepine was persistent in soil and hyperaccumulated in shoots.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2017 Citation: Gemini D. Bhalsod, Ya-Hui Chuang, Sangho Jeon, Wenjun Gui, Hui Li, Elliot T. Ryser, Andrey K. Guber, and Wei Zhang, 2017, Uptake and Accumulation of Pharmaceuticals in Overhead- and Surface-Irrigated Greenhouse Lettuce.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Yuanbo Li, Jonathan Brett Sallach, Wei Zhang, Stephen A. Boyd, and Hui Li, 2017, Uptake of Pharmaceuticals by Radish from Soil, The 4th International Symposium on the Environmental Dimension of Antibiotic Resistance (EDAR), Lansing, Michigan. August 1317.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2017, Influence of transpiration stream on lettuce uptake of pharmaceuticals. AEESP Research and Education Conference, Ann Arbor, Michigan. June 20-22.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Jonathan Brett Sallach, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2017, Uptake, accumulation and metabolization of caffeine in lettuce. The 14th Annual LC-MS/MS Workshop on Environmental and Food Safety, Buffalo, New York. June 11-12.
  • Type: Theses/Dissertations Status: Published Year Published: 2016 Citation: Gemini D. Bhalsod, Uptake and Accumulation of Pharmaceuticals in Surface and Overhead Irrigated Lettuce
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Jonathan Brett Sallach, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2017, Uptake and Metabolization of Caffeine in Lettuce. The 4th International Symposium on the Environmental Dimension of Antibiotic Resistance (EDAR), Lansing, Michigan. August 1317.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Ya-Hui Chuang, Cheng-Hui Liu, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2016, Accumulation and Metabolism of Caffeine in Lettuce. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), Phoenix, Arizona, November 6-9.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Ya-Hui Chuang, Cheng-Hui Liu, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2016, Influence of Transpiration Stream on Plant Uptake and Translocation of Pharmaceuticals. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), Phoenix, Arizona, November 6-9.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Wei Zhang, Gemini D. Bhalsod, Ya-Hui Chuang, Sangho Jeon, Wenjun Gui, and Hui Li, 2016, Assessing and Managing Impact of Pharmaceuticals in Irrigation Water on Fresh Produce Safety. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), Phoenix, Arizona, November 6-9.
  • Type: Journal Articles Status: Under Review Year Published: 2017 Citation: Ya-Hui Chuang, Cheng-Hua Liu, J. Brett Sallach, Raymond Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2017, Mechanism of Uptake and Accumulation of Pharmaceuticals by Lettuce from Water.


Progress 11/01/15 to 10/31/16

Outputs
Target Audience:Scientists, policy makers, undergraduate and graduate students, as well as individuals and the general public who are interested in the relevant issues. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided many opportunities to train postdoctoral research associates and graduate students who have been benefited from this research by improving their laboratory skills, critical thinking and problem solving. This training has helped them to advance their professional development and careers. How have the results been disseminated to communities of interest?The results from this project have been disseminated primarily through publications in peer-reviewed journal articles and presentations in professional conferences to scientists and policy makers. The results are also reported to the general public who are interested in the relevant issues. In addition to the above disseminations, the research methods and results were also incorporated in the PI's courses for undergraduate and graduate students. What do you plan to do during the next reporting period to accomplish the goals?During this period of study, we focused on objectives 1 and 2:Quantify and rank the uptake of multiple representative human and veterinary pharmaceuticals by selected vegetables, andevaluate which vegetable organs (roots, leaves etc.) and growth factors most significantly influence the rate and magnitude of pharmaceutical uptake and accumulation in vegetables. In the next study period, we will publish the results from Objectives 1 and 2 in peer-review journals, and initiate the experiments onObjective 3:Assess the influence of pharmaceutical sorption/desorption by soils on their uptake via vegetable roots.

Impacts
What was accomplished under these goals? Land application of animal manure and biosolids from wastewater treatment plants to agricultural fields could supply plant nutrients for crop growth, and improve soil quality as well. Agricultural irrigation with reclaimed water mitigates the stress of insufficient fresh water supplies. However, these practices can result in the potential uptake and accumulation of pharmaceuticals in plants. Duringthis study period, an efficient and more environmental friendly QuEChERS method was validated and applied to quantify the accumulation of selected pharmaceuticals in lettuce. The extraction recovery of the QuEChERS method ranged from 91.7 to 119.2% for caffeine, carbamazepine, lamotrigine, trimethoprim, monensin and tylosin in lettuce roots, and from 86.3 to 105.3% in shoots. In the kinetic uptake study of pharmaceuticals by well-developed lettuce, the results revealed that the relatively large amounts of caffeine and carbamazepine were distributed in lettuce shoots that that in roots. Lamotrigine and trimethoprim manifested a greater accumulation in lettuce roots than in shoots. The relatively large-sized pharmaceuticals such as monensin and tylosin demonstrated a weak affinity to lettuce root constituents, but were dominantly accumulated in lettuce roots. The analysis of pharmaceutical mass balance in the systems showed that the amount of caffeine and lamotrigine in lettuce roots and shoots kept on decreasing with time, suggesting the occurrence of formation of metabolites in the lettuce. To further elucidate the metabolization processes occurred in lettuce, we developed a reasonable work flow to identify and quantify metabolites of caffeine. This method could be also extended to analyze the metabolites of other types of pharmaceuticals and agrochemicals accumulated in agricultural crops.

Publications

  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Ya-Hui Chuang, Yingjie Zhang, Wei Zhang, Stephen A. Boyd, and Hui Li, 2015, Comparison of accelerated solvent extraction and quick, easy, cheap, effective, rugged and safe method for extraction and determination of pharmaceuticals in vegetables. Journal of Chromatography A 1404:1-9.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Wei Zhang, Cheng-Hua Liu, Gemini D. Bhalsod, Yingjie Zhang, Stephen A. Boyd, Brian J. Teppen, James Tiedje, and Hui Li, 2015, Sorption, Uptake, and Translocation of Pharmaceuticals across Multiple Interfaces in Soil Environment. American Geophysical Union Fall Meeting, San Francisco, California, December 14-18.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Gemini D. Bhalsod, Ya-Hui Chuang, Sanho Jeon, Weijun Gui, Hui Li, Andrey K. Guber, Wei Zhang, 2015, Uptake and Accumulation of Pharmaceuticals in Lettuce under Surface and Overhead Irrigations. American Geophysical Union Fall Meeting, San Francisco, California, December 14-18.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Wei Zhang, Stephen A. Boyd, and Hui Li, 2015, Uptake and Accumulation of Pharmaceuticals in Vegetables. International Annual Meeting of American Society of Agronomy (ASA), Crop Science Society of America (CSSA), and Soil Science Society of America (SSSA), Minneapolis, Minnesota. November 15-18.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Ya-Hui Chuang, Cheng-Hua Liu, Ray Hammerschmidt, Wei Zhang, Stephen A. Boyd, and Hui Li, 2016, Application of QuEChERS Method to Evaluate Accumulation and Metabolism of Pharmaceuticals in Vegetables, 252nd American Chemical Society National Meeting, Philadelphia, Pennsylvania, August 22-25