Article pubs.acs.org/JAFC
Accumulation Potentials of Perfluoroalkyl Carboxylic Acids (PFCAs) and Perfluoroalkyl Sulfonic Acids (PFSAs) in Maize (Zea mays) Johanna Krippner,† Sandy Falk,§ Hubertus Brunn,‡ Sebastian Georgii,§ Sven Schubert,† and Thorsten Stahl*,§ †
Institute of Plant Nutrition, Interdisciplinary Research Centre (IFZ), Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany § Hessian State Laboratory, Glarusstr. 6, 65203 Wiesbaden, Germany ‡ Hessian State Laboratory, Schubertstr. 60, 35392 Giessen, Germany S Supporting Information *
ABSTRACT: Uptake of perfluoroalkyl acids (PFAAs) by maize represents a potential source of exposure for humans, either directly or indirectly via feed for animals raised for human consumption. The aim of the following study was, therefore, to determine the accumulation potential of perfluoroalkyl carboxylic acids (PFCAs) and perfluoroalkyl sulfonic acids (PFSAs) in maize (Zea mays). Two different concentrations of PFAAs were applied as aqueous solution to the soil to attain target concentrations of 0.25 mg or 1.00 mg of PFAA per kg of soil. Maize was grown in pots, and after harvesting, PFAA concentrations were measured in the straw and kernels of maize. PFCA and PFSA concentrations of straw decreased significantly with increasing chain length. In maize kernels, only PFCAs with a chain length ≤ C8 as well as perfluorobutanesulfonic acid (PFBS) were detected. The highest soil-to-plant transfer for both straw and kernels was determined for short-chained PFCAs and PFSAs. KEYWORDS: carryover, translocation, short-chain PFAAs, soil-to-plant transfer factors
■
INTRODUCTION Due to their use in diverse areas of industry and in many household products perfluoroalkyl acids (PFAAs) have become ubiquitous throughout the environment. The class of substances of the PFAAs comprises both perfluoroalkyl carboxylic acids (PFCAs) and perfluoroalkyl sulfonic acids (PFSAs). The use and circulation of perfluoro-octanesulfonic acid (PFOS) and its derivatives have been greatly restricted in the EU as a result of this substance being evaluated as PBT (persistent, bioaccumulative, and toxic). Exceptions for use apply for photoresists or antireflective coatings for photolithography processes; photographic coatings applied to films, papers, or printing plates; mist suppressants for non-decorative hard chromium(VI) plating; and wetting agents for use in controlled electroplating systems and hydraulic fluids for aviation. Use of fire-fighting foam containing PFOS was only allowed in Germany until June 27, 2011.1 PFAAs have been identified in numerous matrices such as soil, sewage sludge, sediment, and ground and surface water as well as in plants, animals, and human tissue.2−4 The European Food Safety Authority (EFSA) has derived tentative tolerable daily intake (TDI) recommendations for PFOS (150 ng kg−1 d−1) and PFOA (1500 ng kg−1 d−1) for risk assessment of human exposure to these substances based on toxicological data.5 Possible entry and distribution paths of PFAAs have been identified and verified in both the environment and in the food chain.6,7 As a result of their relatively high degree of aqueous solubility, it can be assumed that their distribution takes place primarily via the water pathway.8−11 Another possible path of entry into the environment is the discharge of effluents from © 2015 American Chemical Society
industrial processes in municipal sewage treatment plants. Due to their persistence, PFAAs are apparently not degradable and therefore pass through sewage plants untransformed.12 Furthermore, the application of sewage sludge to agricultural lands as fertilizer and the legal disposal of PFAA containing waste in landfills as well as the illegal disposal of waste or mixed waste products may result in substantial contamination of the soil. PFAA concentrations in these so-called “hot-spot regions” may reach levels many times higher than the ubiquitous background soil contamination.13−16 Plants can take up PFAAs from contaminated soil. Both of the so-called key compounds, perfluorooctanoic acid (PFOA) and perfluoro-octanesulfonic acid (PFOS), undergo this type of uptake by various plant species and are translocated to various plant parts.17−21 Because of this uptake, PFAAs can therefore lead to human contamination, either directly by human consumption of PFAA-contaminated food or indirectly via carryover of PFAAcontaminated fodder fed to animals raised as food for humans.22−24 The uptake of PFAAs dependent upon chain length and pH value in maize was previously determined in a nutrient solution experiment.25 Chain length-dependent uptake was confirmed by Felizeter et al.26 in further nutrient solution experiments on tomatoes, cabbage, and zucchini plants. Nutrient solution experiments, however, do not accurately reflect the natural conditions in the field. Sorption of PFAAs Received: Revised: Accepted: Published: 3646
January 2, 2015 March 25, 2015 March 27, 2015 March 27, 2015 DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Article
Journal of Agricultural and Food Chemistry
cartridges. Ammonium hydroxide, A.C.S. reagent for eluting PFAAs from cartridges, was obtained from Sigma-Aldrich. Unless otherwise noted, all chemicals and solvents were from Merck, Darmstadt, Germany and from Sigma-Aldrich, Taufkirchen, Germany of the quality, “purum” or “suprapur”.25 Spiking Solution. The soil for cultivation of maize was spiked by first creating a 1 L stock solution with 10 different PFAAs at a concentration of 200 mg/L of each individual substance. The stock solution was made up of seven perfluoroalkyl carboxylic acids (PFBA, PFPeA, PFHxA, PFHpA, PFOA, PFNA, PFDA) as well as three perfluoroalkyl sulfonic acids (PFBS, PFHxS, PFOS). To improve the solubility of the substances, 220 mL of PFAA-free absolute ethanol (purity 100%) was added to the stock solution, and the PFASs were then dissolved individually beginning with the longer-chain followed by the shorter-chain molecules. PFAA-free ethanol was also added to all of the treatments in order to ensure the same physiological conditions for cultivation of all plants.25 Study Design. Maize (Zea mays L. cv. Amadeo, Kleinwanzlebener Saatzucht, German plant breeding company) was chosen for the pot experiment. This maize hybrid is suitable for use as grain maize and silage as well as a substrate for biogas plants and has been established as an experimental plant for plant physiology studies by the Institute of Plant Nutrition (Justus Liebig University Giessen, Germany). Each maize plant was cultivated in 12 kg of nutrient-poor subsoil in 12 L Ahr pots. The soil used in the experiment did not contain any PFAAs above the limit of quantification (LOQ) of 1 μg/kg soil and had the following properties: pH 7.2 (in 0.01 M CaCl2), 18% clay, 34% silt, 48% sand (Supporting Information, Table S1). The soil was air-dried at room temperature for 5 days before use, sieved to a particle size 0.32) were considerably higher than those reported by Stahl et al.19 (Table 2). Possible explanations for the differences in PFOA and PFOS in maize straw are differences in maize cultivars and varying cultivation conditions as well as differences in the soil composition.21 In the present study, just as described by Stahl et al.,19 only a minimal transfer of PFOA and PFOS into the kernels was observed. PFOS concentrations of the generative organs of the plants were never above the LOQ at either spiking concentration. For PFOA, it was only possible to calculate a transfer factor in the kernels (TFkernels) of 0.002 at the 1.00 mg spiking concentration (Table 3) because the amounts of PFOA in the 0.25 mg samples were below the LOQ of 1 μg/kg DW (Figure 2A). From pot experiment results, Lechner and Knapp18 calculated transfer factors (TF = [PFAA]plant (wet substance)/[PFAA]soil (dry weight)) of PFOA and PFOS in carrots, 3651
DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Article
Journal of Agricultural and Food Chemistry finally the uptake via roots and the distribution of PFAAs in maize plants. Altogether, the results from the present study and the other studies cited here show that PFAAs accumulate to a greater degree in vegetative plant parts and only to a small degree in generative organs. Genotypic and culture-specific differences occur in regard to accumulation in vegetative and generative plant parts. However, the transfer factors for PFOA and PFOS in the generative organs of zucchini are higher than the transfer factors in maize kernels. Analysis of the results of the present study with different spiking concentrations can be summarized as follows: • The fingerprints of both spiking levels show that shorterchain PFAAs predominate both in maize straw as well as in the kernels and are found at the significantly higher concentrations compared to longer-chain molecules. • A comparison of the spiking concentration levels shows that a 4-fold increase in spiking (1.00 mg of the individual substances/kg soil versus 0.25 mg/kg soil) leads to a 4-fold higher concentration of PFCAs with chain lengths ≥ C6 (PFHxA, PFHpA, PFOA, PFNA, PFDA) and PFSAs with a chain length ≥ C6 (PFHxS, PFOS) in the straw of maize plants. • In contrast, a 4-fold increase in spiking concentration does not lead to a 4-fold increase of PFBA, PFPeA, or PFBS in the straw, but only to a 2-fold increase. • For PFOS, however, a 4-fold increase in spiking concentration leads to an 8-fold increase in concentration of the straw. • Significant differences in concentrations of maize kernels dependent upon spiking concentration could only be shown for PFPeA, PFHxA, and PFBS. • Regardless of spiking concentration, PFAA concentrations were always significantly lower in the kernels than in the straw. • Shorter-chain PFAAs (≤C7) have the highest accumulation potentials in above-ground plant parts with transfer factors of >1.00 in straw and >0.01 in kernels. • Of all the PFAAs tested, PFPeA showed the highest accumulation potential in maize kernels. The results presented here confirm the results of previous nutrient solution experiments inasmuch as they also show that short-chain PFAAs are particularly mobile under the influence of soil. Shorter-chain PFAAs are preferentially taken up by maize plants from the soil and are stored in above-ground vegetative as well as in generative plant parts. Those molecules consequently exhibit the highest accumulation potentials in maize. Uptake and storage of these substances in above-ground plant parts of maize depend not only on chain length (C4 to C10) but also on the functional group: carboxylate or sulfonate. Significantly lower concentrations of PFCAs and PFSAs are observed with increasing chain length, and as a consequence, short-chain molecules have the highest transfer factors in maize straw and kernels. In addition, PFCAs are always found in higher concentrations than PFSAs in maize. In addition to different rates of uptake, this may be the result of different transport mechanisms for PFCAs and PFSAs from root to kernels, which will be the subject of future studies.
■
different PFAA concentrations. This material is available free of charge via the Internet at http://pubs.acs.org.
■
AUTHOR INFORMATION
Corresponding Author
*Tel.: +49 611 7608532. Fax: +49 611 7608539. E-mail: [email protected]. Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS Special thanks to our technical staff, Rosa Maria Sobel and Maria Elisabeth Ebel, for their efforts in sample preparation and analysis. We are indebted to Anna Stein for preparation of the graphical abstract. We also wish to thank Barbara Gamb for her assistance in the literature search. We would also like to express our gratitude to Corinna Alles, Helga Tripp, and Lutz Wilming of the Institute of Plant Nutrition at Justus Liebig University Giessen, Germany, for assistance in culturing and harvesting the plants.
■
REFERENCES
(1) The European Parliament and the Council of the European Union. Directive 2006/122/EC of the European Parliament and of the Council of 12 December 2006 on restrictions on the marketing and use of certain dangerous substances and preparations (perfluorooctanesulfonates). Off. J. Eur. Union 2006, 372, 32−34. (2) Zhao, Y. G.; Wonga, C. K. C.; Wonga, M. H. Environmental contamination, human exposure and body loadings of perfluorooctane sulfonate (PFOS), focusing on Asian countries. Chemosphere 2012, 89, 355−368. (3) Valsecchi, S.; Rusconi, M.; Polesello, S. Determination of perfluorinated compounds in aquatic organisms: A review. Anal. Bioanal. Chem. 2013, 405, 143−157. (4) Stahl, T.; Mattern, D.; Brunn, H. Toxicology of perfluorinated compounds. Environ. Sci. Eur. 2011, 23, 38. (5) European Food Safety Authority (EFSA). Perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and their salts. EFSA J. 2008, 653, 1−131. (6) Gellrich, V.; Brunn, H.; Stahl, T. Perfluoroalkyl and polyfluoroalkyl substances (PFASs) in mineral water and tap water. J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2013, 48, 129−135. (7) van Asselt, E. D.; Kowalczyk, J.; van Eijkeren, J. C.; Zeilmaker, M. J.; Ehlers, S.; Forst, P.; Lahrssen-Wiederholt, M.; van der Fels-Klerx, H. J. Transfer of perfluorooctane sulfonic acid (PFOS) from contaminated feed to dairy milk. Food Chem. 2013, 141, 1489−1495. (8) Hong, S.; Khim, J. S.; Park, J.; Kim, M.; Kim, W.-K.; Jung, J.; Hyun, S.; Kim, J.-G.; Lee, H.; Choi, H. J.; Codling, G.; Giesy, J. P. In situ fate and partitioning of waterborne perfluoroalkyl acids (PFAAs) in the Youngsan and Nakdong River Estuaries of South Korea. Sci. Total Environ. 2013, 445−446, 136−145. (9) Cai, M.; Zhao, Z.; Yang, H.; Yin, Z.; Hong, Q.; Sturm, R.; Ebinghaus, R.; Ahrens, L.; Cai, M.; He, J.; Xie, Z. Spatial distribution of per- and polyfluoroalkyl compounds in coastal waters from the East to South China Sea. Environ. Pollut. 2012, 161, 162−169. (10) Kwok, K. Y.; Yamazaki, E.; Yamashita, N.; Taniyasu, S.; Murphy, M. B.; Horii, Y.; Petrick, G.; Kallerborn, R.; Kannan, K.; Murano, K.; Lam, P. K. S. Transport of Perfluoroalkyl substances (PFAA) from an arctic glacier to downstream locations: Implications for sources. Sci. Total Environ. 2013, 447, 46−55. (11) Del Vento, S.; Halsall, C.; Gioia, R.; Jones, K.; Dachs, J. Volatile per− and polyfluoroalkyl compounds in the remote atmosphere of the western Antarctic Peninsula: An indirect source of perfluoroalkyl acids to Antarctic waters? Atmos. Pollut. Res. 2013, 3, 450−455.
ASSOCIATED CONTENT
S Supporting Information *
Detailed description of the properties of the subsoil used in this study as well as the results of the statistical comparison between concentrations of PFAAs of maize after spiking the soil with 3652
DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Article
Journal of Agricultural and Food Chemistry (12) Zhang, W.; Zhang, Y.; Taniyasu, S.; Yeung, L. W. Y.; Lam, P. K. S.; Wang, J.; Li, X.; Yamashita, N.; Dai, J. Distribution and fate of perfluoroalkyl substances in municipal wastewater treatment plants in economically developed areas of China. Environ. Pollut. 2013, 176, 10−17. (13) Stahl, T.; Gellrich, V.; Brunn, H. PFC contamination of groundwater and drinking water. Water Waste, Special Edition, 2012, 18−20. (14) Gomez-Canela, C.; Barth, J. A. C.; Lacorte, S. Occurrence and fate of perfluorinated compounds in sewage sludge from Spain and Germany. Environ. Sci. Pollut. Res. 2012, 19, 4109−4119. (15) Kim, S. K.; Im, J. K.; Kang, Y. M.; Jung, S. Y.; Kho, Y. L.; Zoh, K. D. Wastewater treatment plants (WWTPs)-derived national discharge loads of perfluorinated compounds (PFCs). J. Hazard. Mater. 2012, 201−202, 82−91. (16) Lin, A. Y.; Panchangam, S. C.; Ciou, P. S. High levels of perfluorochemicals in Taiwan’s wastewater treatment plants and downstream rivers pose great risk to local aquatic ecosystems. Chemosphere 2010, 80, 1167−1174. (17) Felizeter, S.; McLachlan, M. S.; de Voogt, P. Uptake of perfluorinated alkyl acids by hydroponically grown lettuce (Lactuca sativa). Environ. Sci. Technol. 2012, 46, 11735−11743. (18) Lechner, M.; Knapp, H. Carryover of perfluorooctanoic acid (PFOA) and perfluorooctanesulfonate (PFOS) from soil to plant and distribution to the different plant compartments studied in cultures of carrots (Daucus carota ssp. sativus), potatoes (Solanum tuberosum), and cucumbers (Cucumis sativus). J. Agric. Food Chem. 2011, 59, 11011− 11018. (19) Stahl, T.; Heyn, J.; Thiele, H.; Hüther, J.; Failing, K.; Georgii, S.; Brunn, H. Carryover of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from soil to plants. Arch. Environ. Contam. Toxicol. 2009, 57, 289−298. (20) Stahl, T.; Riebe, R. A.; Falk, S.; Failing, K.; Brunn, H. A longterm lysimeter experiment to investigate the leaching of perfluoroalkyl substances (PFAAs) and the carryover from soil to plants − Results of a pilot study. J. Agric. Food Chem. 2013, 61, 1784−1793. (21) Zhao, H.; Chen, C.; Zhang, X.; Chen, J.; Quan, X. Phytotoxicity of PFOS and PFOA to Brassica chinensis in different Chinese soils. Ecotoxicol. Environ. Saf. 2011, 74, 1343−1347. (22) Kowalczyk, J.; Ehlers, S.; Forst, P.; Schafft, H.; LahrssenWiederholt, M. Transfer of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from contaminated feed into milk and meat of sheep: Pilot study. Arch. Environ. Contam. Toxicol. 2012, 63, 288−298. (23) Kowalczyk, J.; Ehlers, S.; Oberhausen, A.; Tischer, M.; Forst, P.; Schafft, H.; Lahrssen-Wiederholt, M. Absorption, distribution, and milk secretion of the perfluoroalkyl acids PFBS, PFHxS, PFOS, and PFOA by dairy cows fed naturally contaminated feed. J. Agric. Food Chem. 2013, 61, 2903−2912. (24) Van Asselt, E. D.; Kowalczyk, J.; van Eijkeren, J. C.; Zeilmaker, M. J.; Ehlers, S.; Forst, P.; Lahrssen-Wiederholt, M.; van der FelsKlerx, H. J. Transfer of perfluorooctane sulfonic acid (PFOS) from contaminated feed to dairy milk. Food Chem. 2013, 141, 1489−1495. (25) Krippner, J.; Brunn, H.; Falk, S.; Georgii, S.; Schubert, S.; Stahl, T. Effects of chain length and pH on the uptake and distribution of PFAAs in maize (Zea mays). Chemosphere 2014, 94, 85−90. (26) Felizeter, S.; McLachlan, M. S.; de Voogt, P. Root uptake and translocation of perfluorinated alkyl acids by three hydroponically grown crops. J. Agric. Food Chem. 2014, 62, 3334−3342. (27) Higgins, C. P.; Luthy, R. G. Sorption of perfluorinated surfactants on sediments. Environ. Sci. Technol. 2006, 40, 7251−7256. (28) Weinfurtner, K.; Kördel, W.; Bücking, M. Untersuchungen zum Ü bergang aus PFT-belasteten Böden in Pflanzen. Bodenschutz 2008, 3/08, 88−92. (29) State Agency for Nature, Environment and Consumer Protection in North Rhine-Westphalia. Perfluorinated tenside soil testing of crop land exposed to the “GW Umwelt” waste mixture in North RhineWestphalia. (http://www.lanuv.nrw.de/boden/pft_boden.htm) (accessed 2/28/2015).
(30) Hessian State Office of the Environment and Geology (HLUG). Perfluorinated Chemicals (PFC) in Hesse. Research program of the HLUG; HLUG: Wiesbaden, Germany, 2010; ISBN 978-3-89026-3639. (31) Press information: Department of the Environment BadenWürttemberg. Perfluorinated tensides (PFT) in effluent sludge in Baden-Württemberg − Background − Results − Perspectives. Press conference from August 3, 2007, Stuttgart. (32) Anastassiades, M.; Lehotay, S. J.; Stajnbaher, D.; Schenck, F. J. Fast and easy multiresidue method employing acetonitrile extraction/ partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J. AOAC Int. 2003, 86, 412− 431. (33) Yoo, H.; Washington, J. W.; Jenkins, T. M.; Ellington, J. J. Quantitative determination of perfluorochemicals and fluorotelomer alcohols in plants from biosolid-amended fields using LC/MS/MS and GC/MS. Environ. Sci. Technol. 2011, 45, 7985−7990.
3653
DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Accumulation Potentials of Perfluoroalkyl Carboxylic Acids (PFCAs) and Perfluoroalkyl Sulfonic Acids (PFSAs) in Maize (Zea mays) Johanna Krippner,† Sandy Falk,§ Hubertus Brunn,‡ Sebastian Georgii,§ Sven Schubert,† and Thorsten Stahl*,§ †
Institute of Plant Nutrition, Interdisciplinary Research Centre (IFZ), Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany § Hessian State Laboratory, Glarusstr. 6, 65203 Wiesbaden, Germany ‡ Hessian State Laboratory, Schubertstr. 60, 35392 Giessen, Germany S Supporting Information *
ABSTRACT: Uptake of perfluoroalkyl acids (PFAAs) by maize represents a potential source of exposure for humans, either directly or indirectly via feed for animals raised for human consumption. The aim of the following study was, therefore, to determine the accumulation potential of perfluoroalkyl carboxylic acids (PFCAs) and perfluoroalkyl sulfonic acids (PFSAs) in maize (Zea mays). Two different concentrations of PFAAs were applied as aqueous solution to the soil to attain target concentrations of 0.25 mg or 1.00 mg of PFAA per kg of soil. Maize was grown in pots, and after harvesting, PFAA concentrations were measured in the straw and kernels of maize. PFCA and PFSA concentrations of straw decreased significantly with increasing chain length. In maize kernels, only PFCAs with a chain length ≤ C8 as well as perfluorobutanesulfonic acid (PFBS) were detected. The highest soil-to-plant transfer for both straw and kernels was determined for short-chained PFCAs and PFSAs. KEYWORDS: carryover, translocation, short-chain PFAAs, soil-to-plant transfer factors
■
INTRODUCTION Due to their use in diverse areas of industry and in many household products perfluoroalkyl acids (PFAAs) have become ubiquitous throughout the environment. The class of substances of the PFAAs comprises both perfluoroalkyl carboxylic acids (PFCAs) and perfluoroalkyl sulfonic acids (PFSAs). The use and circulation of perfluoro-octanesulfonic acid (PFOS) and its derivatives have been greatly restricted in the EU as a result of this substance being evaluated as PBT (persistent, bioaccumulative, and toxic). Exceptions for use apply for photoresists or antireflective coatings for photolithography processes; photographic coatings applied to films, papers, or printing plates; mist suppressants for non-decorative hard chromium(VI) plating; and wetting agents for use in controlled electroplating systems and hydraulic fluids for aviation. Use of fire-fighting foam containing PFOS was only allowed in Germany until June 27, 2011.1 PFAAs have been identified in numerous matrices such as soil, sewage sludge, sediment, and ground and surface water as well as in plants, animals, and human tissue.2−4 The European Food Safety Authority (EFSA) has derived tentative tolerable daily intake (TDI) recommendations for PFOS (150 ng kg−1 d−1) and PFOA (1500 ng kg−1 d−1) for risk assessment of human exposure to these substances based on toxicological data.5 Possible entry and distribution paths of PFAAs have been identified and verified in both the environment and in the food chain.6,7 As a result of their relatively high degree of aqueous solubility, it can be assumed that their distribution takes place primarily via the water pathway.8−11 Another possible path of entry into the environment is the discharge of effluents from © 2015 American Chemical Society
industrial processes in municipal sewage treatment plants. Due to their persistence, PFAAs are apparently not degradable and therefore pass through sewage plants untransformed.12 Furthermore, the application of sewage sludge to agricultural lands as fertilizer and the legal disposal of PFAA containing waste in landfills as well as the illegal disposal of waste or mixed waste products may result in substantial contamination of the soil. PFAA concentrations in these so-called “hot-spot regions” may reach levels many times higher than the ubiquitous background soil contamination.13−16 Plants can take up PFAAs from contaminated soil. Both of the so-called key compounds, perfluorooctanoic acid (PFOA) and perfluoro-octanesulfonic acid (PFOS), undergo this type of uptake by various plant species and are translocated to various plant parts.17−21 Because of this uptake, PFAAs can therefore lead to human contamination, either directly by human consumption of PFAA-contaminated food or indirectly via carryover of PFAAcontaminated fodder fed to animals raised as food for humans.22−24 The uptake of PFAAs dependent upon chain length and pH value in maize was previously determined in a nutrient solution experiment.25 Chain length-dependent uptake was confirmed by Felizeter et al.26 in further nutrient solution experiments on tomatoes, cabbage, and zucchini plants. Nutrient solution experiments, however, do not accurately reflect the natural conditions in the field. Sorption of PFAAs Received: Revised: Accepted: Published: 3646
January 2, 2015 March 25, 2015 March 27, 2015 March 27, 2015 DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Article
Journal of Agricultural and Food Chemistry
cartridges. Ammonium hydroxide, A.C.S. reagent for eluting PFAAs from cartridges, was obtained from Sigma-Aldrich. Unless otherwise noted, all chemicals and solvents were from Merck, Darmstadt, Germany and from Sigma-Aldrich, Taufkirchen, Germany of the quality, “purum” or “suprapur”.25 Spiking Solution. The soil for cultivation of maize was spiked by first creating a 1 L stock solution with 10 different PFAAs at a concentration of 200 mg/L of each individual substance. The stock solution was made up of seven perfluoroalkyl carboxylic acids (PFBA, PFPeA, PFHxA, PFHpA, PFOA, PFNA, PFDA) as well as three perfluoroalkyl sulfonic acids (PFBS, PFHxS, PFOS). To improve the solubility of the substances, 220 mL of PFAA-free absolute ethanol (purity 100%) was added to the stock solution, and the PFASs were then dissolved individually beginning with the longer-chain followed by the shorter-chain molecules. PFAA-free ethanol was also added to all of the treatments in order to ensure the same physiological conditions for cultivation of all plants.25 Study Design. Maize (Zea mays L. cv. Amadeo, Kleinwanzlebener Saatzucht, German plant breeding company) was chosen for the pot experiment. This maize hybrid is suitable for use as grain maize and silage as well as a substrate for biogas plants and has been established as an experimental plant for plant physiology studies by the Institute of Plant Nutrition (Justus Liebig University Giessen, Germany). Each maize plant was cultivated in 12 kg of nutrient-poor subsoil in 12 L Ahr pots. The soil used in the experiment did not contain any PFAAs above the limit of quantification (LOQ) of 1 μg/kg soil and had the following properties: pH 7.2 (in 0.01 M CaCl2), 18% clay, 34% silt, 48% sand (Supporting Information, Table S1). The soil was air-dried at room temperature for 5 days before use, sieved to a particle size 0.32) were considerably higher than those reported by Stahl et al.19 (Table 2). Possible explanations for the differences in PFOA and PFOS in maize straw are differences in maize cultivars and varying cultivation conditions as well as differences in the soil composition.21 In the present study, just as described by Stahl et al.,19 only a minimal transfer of PFOA and PFOS into the kernels was observed. PFOS concentrations of the generative organs of the plants were never above the LOQ at either spiking concentration. For PFOA, it was only possible to calculate a transfer factor in the kernels (TFkernels) of 0.002 at the 1.00 mg spiking concentration (Table 3) because the amounts of PFOA in the 0.25 mg samples were below the LOQ of 1 μg/kg DW (Figure 2A). From pot experiment results, Lechner and Knapp18 calculated transfer factors (TF = [PFAA]plant (wet substance)/[PFAA]soil (dry weight)) of PFOA and PFOS in carrots, 3651
DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Article
Journal of Agricultural and Food Chemistry finally the uptake via roots and the distribution of PFAAs in maize plants. Altogether, the results from the present study and the other studies cited here show that PFAAs accumulate to a greater degree in vegetative plant parts and only to a small degree in generative organs. Genotypic and culture-specific differences occur in regard to accumulation in vegetative and generative plant parts. However, the transfer factors for PFOA and PFOS in the generative organs of zucchini are higher than the transfer factors in maize kernels. Analysis of the results of the present study with different spiking concentrations can be summarized as follows: • The fingerprints of both spiking levels show that shorterchain PFAAs predominate both in maize straw as well as in the kernels and are found at the significantly higher concentrations compared to longer-chain molecules. • A comparison of the spiking concentration levels shows that a 4-fold increase in spiking (1.00 mg of the individual substances/kg soil versus 0.25 mg/kg soil) leads to a 4-fold higher concentration of PFCAs with chain lengths ≥ C6 (PFHxA, PFHpA, PFOA, PFNA, PFDA) and PFSAs with a chain length ≥ C6 (PFHxS, PFOS) in the straw of maize plants. • In contrast, a 4-fold increase in spiking concentration does not lead to a 4-fold increase of PFBA, PFPeA, or PFBS in the straw, but only to a 2-fold increase. • For PFOS, however, a 4-fold increase in spiking concentration leads to an 8-fold increase in concentration of the straw. • Significant differences in concentrations of maize kernels dependent upon spiking concentration could only be shown for PFPeA, PFHxA, and PFBS. • Regardless of spiking concentration, PFAA concentrations were always significantly lower in the kernels than in the straw. • Shorter-chain PFAAs (≤C7) have the highest accumulation potentials in above-ground plant parts with transfer factors of >1.00 in straw and >0.01 in kernels. • Of all the PFAAs tested, PFPeA showed the highest accumulation potential in maize kernels. The results presented here confirm the results of previous nutrient solution experiments inasmuch as they also show that short-chain PFAAs are particularly mobile under the influence of soil. Shorter-chain PFAAs are preferentially taken up by maize plants from the soil and are stored in above-ground vegetative as well as in generative plant parts. Those molecules consequently exhibit the highest accumulation potentials in maize. Uptake and storage of these substances in above-ground plant parts of maize depend not only on chain length (C4 to C10) but also on the functional group: carboxylate or sulfonate. Significantly lower concentrations of PFCAs and PFSAs are observed with increasing chain length, and as a consequence, short-chain molecules have the highest transfer factors in maize straw and kernels. In addition, PFCAs are always found in higher concentrations than PFSAs in maize. In addition to different rates of uptake, this may be the result of different transport mechanisms for PFCAs and PFSAs from root to kernels, which will be the subject of future studies.
■
different PFAA concentrations. This material is available free of charge via the Internet at http://pubs.acs.org.
■
AUTHOR INFORMATION
Corresponding Author
*Tel.: +49 611 7608532. Fax: +49 611 7608539. E-mail: [email protected]. Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS Special thanks to our technical staff, Rosa Maria Sobel and Maria Elisabeth Ebel, for their efforts in sample preparation and analysis. We are indebted to Anna Stein for preparation of the graphical abstract. We also wish to thank Barbara Gamb for her assistance in the literature search. We would also like to express our gratitude to Corinna Alles, Helga Tripp, and Lutz Wilming of the Institute of Plant Nutrition at Justus Liebig University Giessen, Germany, for assistance in culturing and harvesting the plants.
■
REFERENCES
(1) The European Parliament and the Council of the European Union. Directive 2006/122/EC of the European Parliament and of the Council of 12 December 2006 on restrictions on the marketing and use of certain dangerous substances and preparations (perfluorooctanesulfonates). Off. J. Eur. Union 2006, 372, 32−34. (2) Zhao, Y. G.; Wonga, C. K. C.; Wonga, M. H. Environmental contamination, human exposure and body loadings of perfluorooctane sulfonate (PFOS), focusing on Asian countries. Chemosphere 2012, 89, 355−368. (3) Valsecchi, S.; Rusconi, M.; Polesello, S. Determination of perfluorinated compounds in aquatic organisms: A review. Anal. Bioanal. Chem. 2013, 405, 143−157. (4) Stahl, T.; Mattern, D.; Brunn, H. Toxicology of perfluorinated compounds. Environ. Sci. Eur. 2011, 23, 38. (5) European Food Safety Authority (EFSA). Perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and their salts. EFSA J. 2008, 653, 1−131. (6) Gellrich, V.; Brunn, H.; Stahl, T. Perfluoroalkyl and polyfluoroalkyl substances (PFASs) in mineral water and tap water. J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2013, 48, 129−135. (7) van Asselt, E. D.; Kowalczyk, J.; van Eijkeren, J. C.; Zeilmaker, M. J.; Ehlers, S.; Forst, P.; Lahrssen-Wiederholt, M.; van der Fels-Klerx, H. J. Transfer of perfluorooctane sulfonic acid (PFOS) from contaminated feed to dairy milk. Food Chem. 2013, 141, 1489−1495. (8) Hong, S.; Khim, J. S.; Park, J.; Kim, M.; Kim, W.-K.; Jung, J.; Hyun, S.; Kim, J.-G.; Lee, H.; Choi, H. J.; Codling, G.; Giesy, J. P. In situ fate and partitioning of waterborne perfluoroalkyl acids (PFAAs) in the Youngsan and Nakdong River Estuaries of South Korea. Sci. Total Environ. 2013, 445−446, 136−145. (9) Cai, M.; Zhao, Z.; Yang, H.; Yin, Z.; Hong, Q.; Sturm, R.; Ebinghaus, R.; Ahrens, L.; Cai, M.; He, J.; Xie, Z. Spatial distribution of per- and polyfluoroalkyl compounds in coastal waters from the East to South China Sea. Environ. Pollut. 2012, 161, 162−169. (10) Kwok, K. Y.; Yamazaki, E.; Yamashita, N.; Taniyasu, S.; Murphy, M. B.; Horii, Y.; Petrick, G.; Kallerborn, R.; Kannan, K.; Murano, K.; Lam, P. K. S. Transport of Perfluoroalkyl substances (PFAA) from an arctic glacier to downstream locations: Implications for sources. Sci. Total Environ. 2013, 447, 46−55. (11) Del Vento, S.; Halsall, C.; Gioia, R.; Jones, K.; Dachs, J. Volatile per− and polyfluoroalkyl compounds in the remote atmosphere of the western Antarctic Peninsula: An indirect source of perfluoroalkyl acids to Antarctic waters? Atmos. Pollut. Res. 2013, 3, 450−455.
ASSOCIATED CONTENT
S Supporting Information *
Detailed description of the properties of the subsoil used in this study as well as the results of the statistical comparison between concentrations of PFAAs of maize after spiking the soil with 3652
DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
Article
Journal of Agricultural and Food Chemistry (12) Zhang, W.; Zhang, Y.; Taniyasu, S.; Yeung, L. W. Y.; Lam, P. K. S.; Wang, J.; Li, X.; Yamashita, N.; Dai, J. Distribution and fate of perfluoroalkyl substances in municipal wastewater treatment plants in economically developed areas of China. Environ. Pollut. 2013, 176, 10−17. (13) Stahl, T.; Gellrich, V.; Brunn, H. PFC contamination of groundwater and drinking water. Water Waste, Special Edition, 2012, 18−20. (14) Gomez-Canela, C.; Barth, J. A. C.; Lacorte, S. Occurrence and fate of perfluorinated compounds in sewage sludge from Spain and Germany. Environ. Sci. Pollut. Res. 2012, 19, 4109−4119. (15) Kim, S. K.; Im, J. K.; Kang, Y. M.; Jung, S. Y.; Kho, Y. L.; Zoh, K. D. Wastewater treatment plants (WWTPs)-derived national discharge loads of perfluorinated compounds (PFCs). J. Hazard. Mater. 2012, 201−202, 82−91. (16) Lin, A. Y.; Panchangam, S. C.; Ciou, P. S. High levels of perfluorochemicals in Taiwan’s wastewater treatment plants and downstream rivers pose great risk to local aquatic ecosystems. Chemosphere 2010, 80, 1167−1174. (17) Felizeter, S.; McLachlan, M. S.; de Voogt, P. Uptake of perfluorinated alkyl acids by hydroponically grown lettuce (Lactuca sativa). Environ. Sci. Technol. 2012, 46, 11735−11743. (18) Lechner, M.; Knapp, H. Carryover of perfluorooctanoic acid (PFOA) and perfluorooctanesulfonate (PFOS) from soil to plant and distribution to the different plant compartments studied in cultures of carrots (Daucus carota ssp. sativus), potatoes (Solanum tuberosum), and cucumbers (Cucumis sativus). J. Agric. Food Chem. 2011, 59, 11011− 11018. (19) Stahl, T.; Heyn, J.; Thiele, H.; Hüther, J.; Failing, K.; Georgii, S.; Brunn, H. Carryover of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from soil to plants. Arch. Environ. Contam. Toxicol. 2009, 57, 289−298. (20) Stahl, T.; Riebe, R. A.; Falk, S.; Failing, K.; Brunn, H. A longterm lysimeter experiment to investigate the leaching of perfluoroalkyl substances (PFAAs) and the carryover from soil to plants − Results of a pilot study. J. Agric. Food Chem. 2013, 61, 1784−1793. (21) Zhao, H.; Chen, C.; Zhang, X.; Chen, J.; Quan, X. Phytotoxicity of PFOS and PFOA to Brassica chinensis in different Chinese soils. Ecotoxicol. Environ. Saf. 2011, 74, 1343−1347. (22) Kowalczyk, J.; Ehlers, S.; Forst, P.; Schafft, H.; LahrssenWiederholt, M. Transfer of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from contaminated feed into milk and meat of sheep: Pilot study. Arch. Environ. Contam. Toxicol. 2012, 63, 288−298. (23) Kowalczyk, J.; Ehlers, S.; Oberhausen, A.; Tischer, M.; Forst, P.; Schafft, H.; Lahrssen-Wiederholt, M. Absorption, distribution, and milk secretion of the perfluoroalkyl acids PFBS, PFHxS, PFOS, and PFOA by dairy cows fed naturally contaminated feed. J. Agric. Food Chem. 2013, 61, 2903−2912. (24) Van Asselt, E. D.; Kowalczyk, J.; van Eijkeren, J. C.; Zeilmaker, M. J.; Ehlers, S.; Forst, P.; Lahrssen-Wiederholt, M.; van der FelsKlerx, H. J. Transfer of perfluorooctane sulfonic acid (PFOS) from contaminated feed to dairy milk. Food Chem. 2013, 141, 1489−1495. (25) Krippner, J.; Brunn, H.; Falk, S.; Georgii, S.; Schubert, S.; Stahl, T. Effects of chain length and pH on the uptake and distribution of PFAAs in maize (Zea mays). Chemosphere 2014, 94, 85−90. (26) Felizeter, S.; McLachlan, M. S.; de Voogt, P. Root uptake and translocation of perfluorinated alkyl acids by three hydroponically grown crops. J. Agric. Food Chem. 2014, 62, 3334−3342. (27) Higgins, C. P.; Luthy, R. G. Sorption of perfluorinated surfactants on sediments. Environ. Sci. Technol. 2006, 40, 7251−7256. (28) Weinfurtner, K.; Kördel, W.; Bücking, M. Untersuchungen zum Ü bergang aus PFT-belasteten Böden in Pflanzen. Bodenschutz 2008, 3/08, 88−92. (29) State Agency for Nature, Environment and Consumer Protection in North Rhine-Westphalia. Perfluorinated tenside soil testing of crop land exposed to the “GW Umwelt” waste mixture in North RhineWestphalia. (http://www.lanuv.nrw.de/boden/pft_boden.htm) (accessed 2/28/2015).
(30) Hessian State Office of the Environment and Geology (HLUG). Perfluorinated Chemicals (PFC) in Hesse. Research program of the HLUG; HLUG: Wiesbaden, Germany, 2010; ISBN 978-3-89026-3639. (31) Press information: Department of the Environment BadenWürttemberg. Perfluorinated tensides (PFT) in effluent sludge in Baden-Württemberg − Background − Results − Perspectives. Press conference from August 3, 2007, Stuttgart. (32) Anastassiades, M.; Lehotay, S. J.; Stajnbaher, D.; Schenck, F. J. Fast and easy multiresidue method employing acetonitrile extraction/ partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J. AOAC Int. 2003, 86, 412− 431. (33) Yoo, H.; Washington, J. W.; Jenkins, T. M.; Ellington, J. J. Quantitative determination of perfluorochemicals and fluorotelomer alcohols in plants from biosolid-amended fields using LC/MS/MS and GC/MS. Environ. Sci. Technol. 2011, 45, 7985−7990.
3653
DOI: 10.1021/acs.jafc.5b00012 J. Agric. Food Chem. 2015, 63, 3646−3653
