Abstract
Anticoagulant rodenticides are used worldwide to control commensal rodents for hygienic and public health reasons. As anticoagulants act on all vertebrates, risk is high for unintentional poisoning of terrestrial and aquatic wildlife. Causative associations have been demonstrated for the unintended poisoning of terrestrial nontarget organisms. However, behavior and fate of anticoagulant rodenticides in the aquatic environment have received minimal attention in the past despite considerable acute toxicity of several anticoagulants to aquatic species such as fish. In light of recent regulatory developments in the European Union concerning rodenticides, we critically review available information on the environmental occurrence, fate, and impact of anticoagulant rodenticides in the aquatic environment and identify potential risks and routes of exposure as well as further research needs. Recent findings of anticoagulant rodenticides in raw and treated wastewater, sewage sludge, estuarine sediments, suspended particulate matter, and liver tissue of freshwater fish in the low ng/L and µg/kg range, respectively, demonstrate that the aquatic environment experiences a greater risk of anticoagulant rodenticide exposure than previously thought. While the anticoagulant’s mechanism of action from the molecular through cellular levels is well understood, substantial data gaps exist regarding the understanding of exposure pathways and potential adverse effects of chronic exposure with multiple active ingredients. Anticoagulants accumulating in aquatic wildlife are likely to be transferred in the food chain, causing potentially serious consequences for the health of wildlife and humans alike.
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Ajo P, Preis S, Vornamo T, Mänttäri M, Kallioinen M, Louhi-Kultanen M (2018) Hospital wastewater treatment with pilot-scale pulsed corona discharge for removal of pharmaceutical residues. J Environ Chem Eng 6:1569–1577. https://doi.org/10.1016/j.jece.2018.02.007
Alomar H, Chabert A, Coeurdassier M, Vey D, Berny P (2018) Accumulation of anticoagulant rodenticides (chlorophacinone, bromadiolone and brodifacoum) in a non-target invertebrate, the slug, Deroceras reticulatum. Sci Total Environ 610–611:576–582. https://doi.org/10.1016/j.scitotenv.2017.08.117
Andre C, Guyon C, Guillaume YC (2004) Rodenticide-humic acid adsorption mechanisms and role of humic acid on their toxicity on human keratinocytes: chromatographic approach to support the biological data. J Chromatogr, B: Anal Technol Biomed Life Sci 813:295–302. https://doi.org/10.1016/j.jchromb.2004.10.028
Andre C, Guyon C, Thomassin M, Barbier A, Richert L, Guillaume YC (2005) Association mechanism between a series of rodenticide and humic acid: a frontal analysis to support the biological data. J Chromatogr, B: Anal Technol Biomed Life Sci 820:9–14. https://doi.org/10.1016/j.jchromb.2005.02.020
Barnes KK, Kolpin DW, Furlong ET, Zaugg SD, Meyer MT, Barber LB (2008) A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States - I) groundwater. Sci Total Environ 402:192–200. https://doi.org/10.1016/j.scitotenv.2008.04.028
Barten R (2014) New approaches from the view of industry. In: Esther A et al (eds) Rodenticide resistance. Julius Kühn Institute, Federal Research Centre for Cultivated Plants, Braunschweig, pp 50–54
Battersby SA (2015) Rodents as carriers of disease. In: Buckle AP, Smith RH (eds) Rodent pests and their control. CABI, Oxfordshire, pp 81–100
Bayen S, Estrada ES, Juhel G, Kelly BC (2015) Direct injection of tissue extracts in liquid chromatography/tandem mass spectrometry for the determination of pharmaceuticals and other contaminants of emerging concern in mollusks. Anal Bioanal Chem 407:5553–5558. https://doi.org/10.1007/s00216-015-8760-9)
Beklova M, Krizkova S, Supalkova V et al (2007) Determination of bromadiolone in pheasants and foxes by differential pulse voltammetry. Int J Environ Anal Chem 87:459–469. https://doi.org/10.1080/03067310601170472
Berny PJ, Buronfosse T, Buronfosse F, Lamarque F, Lorgue G (1997) Field evidence of secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone, a 4-year survey. Chemosphere 35:1817–1829. https://doi.org/10.1016/S0045-6535(97)00242-7
Berny P, Velardo J, Pulce C, D’Amico A, Kammerer M, Lasseur R (2010) Prevalence of anticoagulant rodenticide poisoning in humans and animals in France and substances involved. Clin Toxicol (Phila) 48:935–941. https://doi.org/10.3109/15563650.2010.533678
Bidny S, Gago K, David M, Duong T, Albertyn D, Gunja N (2015) A validated LC-MS-MS method for simultaneous identification and quantitation of rodenticides in blood. J Anal Toxicol 39:219–224. https://doi.org/10.1093/jat/bku175
Booth LH, Ogilvie SC, Eason CT (2010) Persistence of sodium monofluoroacetate (1080), pindone, cholecalciferol, and brodifacoum in possum baits under simulated rainfall. N Z J Agric Res 42:107–112. https://doi.org/10.1080/00288233.1999.9513359
Brakes CR, Smith RH (2005) Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. J Appl Ecol 42:118–128. https://doi.org/10.1111/j.1365-2664.2005.00997.x
Buckle AP, Eason CT (2015) Control methods: chemical. In: Buckle AP, Smith RH (eds) Rodent pests and their control. CAB International, Wallingford, pp 123–154
Buckle AP, Smith RH (eds) (2015) rodent pests and their control. CAB International, Wallingford
BVL (2012) Absatz an Pflanzenschutzmitteln in der Bundesrepublik Deutschland. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Braunschweig
BVL (2015) Absatz an Pflanzenschutzmitteln in der Bundesrepublik Deutschland. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Braunschweig
Cavanagh J-AE, Ward N (2014) Contaminants in estuarine and riverine sediments and biota in Southland. Environment Southland, Invercargill
Chen XH, Cai MQ, Ouyang XK, Jin MC (2009) Ion chromatography tandem mass spectrometry for simultaneous confirmation and determination of indandione rodenticides in serum. Biomed Chromatogr 23:1217–1226. https://doi.org/10.1002/bmc.1246
Chen M, Zhu G, Zhou L, Min J, Chen X, Jin M (2014) Analysis of trace bromadiolone and brodifacoum in environmental water samples by ionic liquid ultrasound-assisted dispersive liquid–liquid microextraction and LC-MS/MS. Anal Methods 6:5879–5885. https://doi.org/10.1039/c3ay42317d
Christensen TK, Lassen P, Elmeros M (2012) High exposure rates of anticoagulant rodenticides in predatory bird species in intensively managed landscapes in Denmark. Arch Environ Contam Toxicol 63:437–444. https://doi.org/10.1007/s00244-012-9771-6
Coeurdassier M, Riols R, Decors A et al (2014) Unintentional wildlife poisoning and proposals for sustainable management of rodents. Conserv Biol 28:315–321. https://doi.org/10.1111/cobi.12230
Colvin BA, Swift TB, Fothergill FE (1998) Control of Norway rats in sewer and utility systems using pulsed baiting methods. In: Proceedings of the 18th vertebrate pest conference, vol 36, pp 247–253
Connors KA, Du B, Fitzsimmons PN et al (2013) Comparative pharmaceutical metabolism by rainbow trout (Oncorhynchus mykiss) liver S9 fractions. Environ Toxicol Chem 32:1810–1818. https://doi.org/10.1002/etc.2240
Crouse BA, Ghoshdastidar AJ, Tong AZ (2012) The presence of acidic and neutral drugs in treated sewage effluents and receiving waters in the Cornwallis and Annapolis River watersheds and the Mill CoveSewage Treatment Plant in Nova Scotia, Canada. Environ Res 112:92–99. https://doi.org/10.1016/j.envres.2011.11.011
CRRU UK (2015) Campaign for responsible rodenticide Use UK code of best practice. Campaign for Responsible Rodenticide Use UK, Leeds
Damin-Pernik M, Espana B, Besse S et al (2016) Development of an ecofriendly anticoagulant rodenticide based on the stereochemistry of difenacoum. Drug Metab Dispos 44:1872–1880. https://doi.org/10.1124/dmd.116.071688
Damin-Pernik M, Espana B, Lefebvre S et al (2017) Management of rodent populations by anticoagulant rodenticides: toward third-generation anticoagulant rodenticides. Drug Metab Dispos 45:160–165. https://doi.org/10.1124/dmd.116.073791
Dawson A, Garthwaite D (2004) Rodenticide usage by local authorities in Great Britain 2001. Pesticide usage survey report 185. Department for Environment, Food and Rural Affairs, New York
de Solla SR, Gilroy EA, Klinck JS et al (2016) Bioaccumulation of pharmaceuticals and personal care products in the unionid mussel Lasmigona costata in a river receiving wastewater effluent. Chemosphere 146:486–496. https://doi.org/10.1016/j.chemosphere.2015.12.022
Doubkova V, Marsalek P, Vecerek V (2017) The rapid determination of bromadiolone in liver and blood plasma by in-injector pyrolysis gas chromatography—ion trap tandem mass spectrometry. J Chromatogr, B: Anal Technol Biomed Life Sci. https://doi.org/10.1016/j.jchromb.2017.10.027
Du B, Price AE, Scott WC et al (2014) Comparison of contaminants of emerging concern removal, discharge, and water quality hazards among centralized and on-site wastewater treatment system effluents receiving common wastewater influent. Sci Total Environ 466–467:976–984. https://doi.org/10.1016/j.scitotenv.2013.07.126
Eason CT, Murphy EC, Wright GR, Spurr EB (2002) Assessment of risks of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicol 11:35–48. https://doi.org/10.1023/A:1013793029831
EBPF (2015) Sustainable use of rodenticides as biocides in the EU. CEFIC-European Biocidal Products Forum, Brussels
eCA (2016a) Flocoumafen assessment report. Product-type 14 (Rodenticide) competent authority. European Union, The Netherlands
eCA (2016b) Coumatetralyl assessment report. Product-type 14 (Rodenticide) competent authority. European Union, Denmark
eCA (2016c) Brodifacoum assessment report. Product-type 14 (Rodenticide) competent authorities. European Union, The Netherlands and Italy
eCA (2016d) Chlorophacinone assessment report. Product-type 14 (Rodenticide) competent authority. European Union, Spain
eCA (2016e) Bromadiolone assessment report. Product-type 14 (Rodenticide) competent authority. European Union, Italy
eCA (2016f) Warfarin Assessment report. Product-type 14 (Rodenticide) competent authority. European Union, Ireland
eCA (2016g) Difenacoum assessment report. Product-type 14 (rodenticide) competent authority. European Union, Finland
eCA (2016h) Difethialone assessment report. Product-type 14 (Rodenticide) competent authority. European Union, Norway
ECHA (2017a) Guidance on the biocidal products regulation: volume IV environment—assessment and evaluation (parts B + C). European Chemicals Agency, Helsinki
ECHA (2017b) Opinion of the Biocidal Products Committee on questions related to the comparative assessment of anticoagulant rodenticides. ECHA/BPC/145/2017. European Chemicals Agency, Helsinki
Ejhed H, Fang J, Hansen K et al (2018) The effect of hydraulic retention time in onsite wastewater treatment and removal of pharmaceuticals, hormones and phenolic utility substances. Sci Total Environ 618:250–261. https://doi.org/10.1016/j.scitotenv.2017.11.011
Elliott JE, Rattner BA, Shore RF, Van Den Brink NW (2016) Paying the pipers: mitigating the impact of anticoagulant rodenticides on predators and scavengers. Biosci 66:401–407. https://doi.org/10.1093/biosci/biw028
Empson RA, Miskelly CM (1999) The risks, costs and benefits of using brodifacoum to eradicate rats from Kapiti Island, New Zealand. N Z J Ecol 23:241–254
Endepols S (2002) Rodenticides—indispensable for safe food production. Pestic Outlook 13:231–232. https://doi.org/10.1039/b211694b
European Commission (2011) Regulation (EU) No 253/2011 of 15 March 2011 amending Regulation (EC) No 1907/2006 of the European Parliament and of the Council on the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH) as regards Annex XIII. Off J Eur Union L 69:7–12
European Commission (2016) Commission Regulation (EU) 2016/1179 of 19 July 2016 amending, for the purposes of its adaptation to technical and scientific progress, Regulation (EC) No 1272/2008 of the European Parliament and of the Council on classification, labelling and packaging of substances and mixtures. Off J Eur Union L 195:11–25
European Commission (2017a) Commission Implementing Regulation (EU) 2017/1380 of 25 July 2017 renewing the approval of bromadiolone as an active substance for use in biocidal products of product-type 14. Off J Eur Union L 194:33–38
European Commission (2017b) Commission Implementing Regulation (EU) 2017/1379 of 25 July 2017 renewing the approval of difenacoum as an active substance for use in biocidal products of product-type 14. Off J Eur Union L 194:27–32
European Commission (2017c) Commission Implementing Regulation (EU) 2017/1376 of 25 July 2017 renewing the approval of warfarin as an active substance for use in biocidal products of product-type 14. Off J Eur Union L 194:9–14
European Union (2009) Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Off J Eur Union L 309:1–50
European Union (2012) Regulation (EU) No 528/2012 of the European parliament and of the council of 22 May 2012 concerning the making available on the market and use of biocidal products. Off J Eur Union L 167:1–128
Fernandez I, Santos A, Cancela ML, Laize V, Gavaia PJ (2014) Warfarin, a potential pollutant in aquatic environment acting through Pxr signaling pathway and gamma-glutamyl carboxylation of vitamin K-dependent proteins. Environ Pollut 194:86–95. https://doi.org/10.1016/j.envpol.2014.07.015
Fisher P (2013) Environmental residues of anticoagulants used for pest animal control. Landcare Research, Lincoln
Fisher P, O’Connor C, Wright GR, Eason CT (2003) Persistence of 4 anticoagulant rodenticides in the livers of laboratory rats. Department of Conservation, Wellington
Fisher P, Funnell E, Fairweather A, Brown L, Campion M (2012) Accidental discharge of brodifacoum baits into a freshwater lake: a case study. Bull Environ Contam Toxicol 88:226–228. https://doi.org/10.1007/s00128-011-0470-1
Focazio MJ, Kolpin DW, Barnes KK et al (2008) A national reconnaissance for pharmaceuticals and other organic wastewater contaminants in the United States-II) untreated drinking water sources. Sci Total Environ 402:201–216. https://doi.org/10.1016/j.scitotenv.2008.02.021
Fourel I, Damin-Pernik M, Benoit E, Lattard V (2017a) Core-shell LC–MS/MS method for quantification of second generation anticoagulant rodenticides diastereoisomers in rat liver in relationship with exposure of wild rats. J Chromatogr B 1041–1042:120–132. https://doi.org/10.1016/j.jchromb.2016.12.028
Fourel I, Damin-Pernik M, Benoit E, Lattard V (2017b) Cis-bromadiolone diastereoisomer is not involved in bromadiolone Red Kite (Milvus milvus) poisoning. Sci Total Environ 601–602:1412–1417. https://doi.org/10.1016/j.scitotenv.2017.06.011
Fournier-Chambrillon C, Berny PJ, Coiffier O et al (2004) Evidence of secondary poisoning of free-ranging riparian mustelids by anticoagulant rodenticides in France: implications for conservation of European mink (Mustela lutreola). J Wildl Dis 40:688–695. https://doi.org/10.7589/0090-3558-40.4.688
Fram MS, Belitz K (2011) Occurrence and concentrations of pharmaceutical compounds in groundwater used for public drinking-water supply in California. Sci Total Environ 409:3409–3417. https://doi.org/10.1016/j.scitotenv.2011.05.053
Garman GC (1991) Use of terrestrial arthropod prey by a stream-dwelling cyprinid fish. Environ Biol Fishes 30:325–331. https://doi.org/10.1007/BF02028848
Geduhn A (2015) Exposure of wildlife to anticoagulant rodenticides: how environmental drivers modulate the pathway of anticoagulant rodenticides from bait to predators. University of Münster, Münster
Geduhn A, Esther A, Schenke D, Mattes H, Jacob J (2014) Spatial and temporal exposure patterns in non-target small mammals during brodifacoum rat control. Sci Total Environ 496:328–338. https://doi.org/10.1016/j.scitotenv.2014.07.049
Geduhn A, Jacob J, Schenke D, Keller B, Kleinschmidt S, Esther A (2015) Relation between intensity of biocide practice and residues of anticoagulant rodenticides in Red Foxes (Vulpes vulpes). PLoS ONE 10:e0139191. https://doi.org/10.1371/journal.pone.0139191
Geduhn A, Esther A, Schenke D, Gabriel D, Jacob J (2016) Prey composition modulates exposure risk to anticoagulant rodenticides in a sentinel predator, the barn owl. Sci Total Environ 544:150–157. https://doi.org/10.1016/j.scitotenv.2015.11.117
Gibs J, Stackelberg PE, Furlong ET, Meyer M, Zaugg SD, Lippincott RL (2007) Persistence of pharmaceuticals and other organic compounds in chlorinated drinking water as a function of time. Sci Total Environ 373:240–249. https://doi.org/10.1016/j.scitotenv.2006.11.003
Godfrey E, Woessner WW, Benotti MJ (2007) Pharmaceuticals in on-site sewage effluent and ground water, Western Montana. Ground Water 45:263–271. https://doi.org/10.1111/j.1745-6584.2006.00288.x
Goldade DA, Primus TM, Johnston JJ, Zapien DC (1998) Reversed-phase ion-pair high-performance liquid chromatographic quantitation of difethialone residues in whole-body rodents with solid-phase extraction cleanup. J Agric Food Chem 46:504–508. https://doi.org/10.1021/jf970715u
Gómez-Canela C, Lacorte S (2016) Comprehensive characterization of anticoagulant rodenticides in sludge by liquid chromatography–tandem mass spectrometry. Environ Sci Pollut Res Int 23:15739–15748. https://doi.org/10.1007/s11356-016-6743-9
Gómez-Canela C, Barata C, Lacorte S (2014a) Occurrence, elimination, and risk of anticoagulant rodenticides and drugs during wastewater treatment. Environ Sci Pollut Res 21:7194–7203. https://doi.org/10.1007/s11356-014-2714-1
Gómez-Canela C, Vazquez-Chica A, Lacorte S (2014b) Comprehensive characterization of rodenticides in wastewater by liquid chromatography–tandem mass spectrometry. Anal Bioanal Chem 406:345–358. https://doi.org/10.1007/s00216-013-7449-1
Gras LM, Patergnani M, Farina M (2012) Poison-based commensal rodent control strategies in urban ecosystems: some evidence against sewer-baiting. EcoHealth 9:75–79. https://doi.org/10.1007/s10393-012-0748-8
Guan F, Ishii A, Seno H, Watanabe-Suzuki K, Kumazawa T, Suzuki O (1999) Use of an ion-pairing reagent for high-performance liquid chromatography–atmospheric pressure chemical ionization mass spectrometry determination of anionic anticoagulant rodenticides in body fluids. J Chromatogr B Biomed Sci Appl 731:155–165. https://doi.org/10.1016/S0378-4347(99)00126-7
Gurung K, Ncibi MC, Fontmorin JM (2016) Incorporating submerged MBR in conventional activated sludge process for municipal wastewater treatment: a feasibility and performance assessment. J Membr Sci Technol. https://doi.org/10.4172/2155-9589.1000158
Hauck ZZ, Feinstein DL, van Breemen RB (2016) LC-MS-MS analysis of brodifacoum isomers in rat tissue. J Anal Toxicol 40:304–309. https://doi.org/10.1093/jat/bkw008
Hernández AM, Bernal J, Bernal JL, Martín MT, Caminero C, Nozal MJ (2013) Simultaneous determination of nine anticoagulant rodenticides in soil and water by LC–ESI-MS. J Sep Sci 36:2593–2601. https://doi.org/10.1002/jssc.201300310
Horak KE, Fisher PM, Hopkins B (2018) Pharmacokinetics of anticoagulant rodenticides in target and non-target organisms. In: van den Brink NW et al (eds) Anticoagulant rodenticides and wildlife. Springer, Cham, pp 87–108
Hosea RC (2000) Exposure of non-target wildlife to anticoagulant rodenticides in California. In: Proceedings of the 19th vertebrate pest conference, pp 6–9
Huckle KR, Hutson DH, Warburton PA (1988) Elimination and accumulation of the rodenticide flocoumafen in rats following repeated oral administration. Xenobiotica 18:1465–1479. https://doi.org/10.3109/00498258809042269
Huerta B, Rodriguez-Mozaz S, Barcelo D (2012) Pharmaceuticals in biota in the aquatic environment: analytical methods and environmental implications. Anal Bioanal Chem 404:2611–2624. https://doi.org/10.1007/s00216-012-6144-y
Hughes J, Sharp E, Taylor MJ, Melton L, Hartley G (2013) Monitoring agricultural rodenticide use and secondary exposure of raptors in Scotland. Ecotoxicol 22:974–984. https://doi.org/10.1007/s10646-013-1074-9
Hunter K (1983a) Determination of coumarin anticoagulant rodenticide residues in animal tissue by high-performance liquid chromatography: II. Fluorescence detection using ion-pair chromatography. J Chromatogr A 270:277–283. https://doi.org/10.1016/S0021-9673(01)96372-2
Hunter K (1983b) Determination of coumarin anticoagulant rodenticide residues in animal tissue by high-performance liquid chromatography: I. Fluorescence detection using post-column techniques. J Chromatogr A 270:267–276. https://doi.org/10.1016/S0021-9673(01)96372-1
Imran M, Shafi H, Wattoo SA, Chaudhary MT, Usman HF (2015) Analytical methods for determination of anticoagulant rodenticides in biological samples. Forensic Sci Int 253:94–102. https://doi.org/10.1016/j.forsciint.2015.06.008
Jacob J, Buckle A (2018) Use of anticoagulant rodenticides in different applications around the world. In: van den Brink NW et al (eds) Anticoagulant rodenticides and wildlife. Springer, Cham, pp 11–43
Jacquot M, Coeurdassier M, Couval G et al (2013) Using long-term monitoring of red fox populations to assess changes in rodent control practices. J Appl Ecol 50:1406–1414. https://doi.org/10.1111/1365-2664.12151
Jin MC, Chen XH, Zhu Y (2007) Determination of five 4-hydroxycoumarin rodenticides in animal liver tissues by ion chromatography with fluorescence detection. J Chromatogr A 1155:57–61. https://doi.org/10.1016/j.chroma.2006.12.074
Jin MC, Chen XH, Ye ML, Zhu Y (2008) Analysis of indandione anticoagulant rodenticides in animal liver by eluent generator reagent free ion chromatography coupled with electrospray mass spectrometry. J Chromatogr A 1213:77–82. https://doi.org/10.1016/j.chroma.2008.08.100
Jin MC, Cai MQ, Chen XH (2009) Simultaneous measurement of indandione-type rodenticides in human serum by liquid chromatography-electrospray ionization- tandem mass spectrometry. J Anal Toxicol 33:294–300. https://doi.org/10.1093/jat/33.6.294
Jones A (1996) HPLC determination of anticoagulant rodenticide residues in animal livers. Bull Environ Contam Toxicol 56:8–15. https://doi.org/10.1007/s001289900002
Kammerer B, Kahlich R, Ufer M, Schenkel A, Laufer S, Gleiter CH (2005) Stereospecific pharmacokinetic characterisation of phenprocoumon metabolites, and mass-spectrometric identification of two novel metabolites in human plasma and liver microsomes. Anal Bioanal Chem 383:909–917. https://doi.org/10.1007/s00216-005-0113-7
Kasprzyk-Hordern B (2010) Pharmacologically active compounds in the environment and their chirality. Chem Soc Rev 39:4466–4503. https://doi.org/10.1039/c000408c
Kinney CA, Furlong ET, Werner SL, Cahill JD (2006) Presence and distribution of wastewater-derived pharmaceuticals in soil irrigated with reclaimed water. Environ Toxicol Chem 25:317–326. https://doi.org/10.1897/05-187R.1
Koivisto E, Koivisto P, Hanski IK et al (2016) Prevalence of anticoagulant rodenticides in non-target predators and scavengers in Finland. Finnish Safety and Chemicals Agency, Helsinki
Kolpin DW, Furlong ET, Meyer MT et al (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211. https://doi.org/10.1021/es011055j
Kolpin DW, Skopec M, Meyer MT, Furlong ET, Zaugg SD (2004) Urban contribution of pharmaceuticals and other organic wastewater contaminants to streams during differing flow conditions. Sci Total Environ 328:119–130. https://doi.org/10.1016/j.scitotenv.2004.01.015
Kopanke JH, Horak KE, Musselman E et al (2018) Effects of low-level brodifacoum exposure on the feline immune response. Sci Rep 8:8168. https://doi.org/10.1038/s41598-018-26558-3
Kostich MS, Lazorchak JM (2008) Risks to aquatic organisms posed by human pharmaceutical use. Sci Total Environ 389:329–339. https://doi.org/10.1016/j.scitotenv.2007.09.008
Kostich MS, Batt AL, Lazorchak JM (2014) Concentrations of prioritized pharmaceuticals in effluents from 50 large wastewater treatment plants in the US and implications for risk estimation. Environ Pollut 184:354–359. https://doi.org/10.1016/j.envpol.2013.09.013
Kotthoff M, Rüdel H, Jürling H et al (2018) First evidence of anticoagulant rodenticides in fish and suspended particulate matter: spatial and temporal distribution in German freshwater aquatic systems. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-018-1385-8
Krüger G, Solas H (2010) Nachbarn im Kanalnetz - Ergebnisse einer Fragebogenaktion zur Rattenbekämpfung. Korrespondenz Abwasser, Abfall 57:430–435
Laasko S, Suomalainen K, Koivisto S (2010) Literature review on residues of anticoagulant rodenticides in non-target animals. Nordic Council of Ministers, Copenhagen
Lambert O, Pouliquen H, Larhantec M, Thorin C, L’Hostis M (2007) Exposure of raptors and waterbirds to anticoagulant rodenticides (difenacoum, bromadiolone, coumatetralyl, coumafen, brodifacoum): epidemiological survey in Loire Atlantique (France). Bull Environ Contam Toxicol 79:91–94. https://doi.org/10.1007/s00128-007-9134-6
Lao W, Gan J (2012) Enantioselective degradation of warfarin in soils. Chirality 24:54–59. https://doi.org/10.1002/chir.21023
Larsen J (2003) Emission scenario document for biocides used as rodenticides. Danish EPA, Copenhagen
Lemarchand C, Rosoux R, Berny P (2010) Organochlorine pesticides, PCBs, heavy metals and anticoagulant rodenticides in tissues of Eurasian otters (Lutra lutra) from upper Loire River catchment (France). Chemosphere 80:1120–1124. https://doi.org/10.1016/j.chemosphere.2010.06.026
Lemarchand C, Rosoux R, Talon C, Berny P (2014) Flagship species conservation and introduced species invasion: toxic aspects along Loire River (France). In: pesticides—toxic aspects, pp 53–79. InTech
Lewis RJ, Trager WF, Chan KK et al (1974) Warfarin stereochemical aspects of its metabolism and the interaction with phenylbutazone. J Clin Investig 53:1607–1617. https://doi.org/10.1172/jci107711
Lin Y, Shen X, Yuan Q, Yan Y (2013) Microbial biosynthesis of the anticoagulant precursor 4-hydroxycoumarin. Nat Commun 4:2603. https://doi.org/10.1038/ncomms3603
Liphatech (2013) The veterinarian’s guide to accidental rodenticide ingestion by dogs & cats. Liphatech Inc., Milwaukee
Liu J, Xiong K, Ye X, Zhang J, Yang Y, Ji L (2015) Toxicity and bioaccumulation of bromadiolone to earthworm Eisenia fetida. Chemosphere 135:250–256. https://doi.org/10.1016/j.chemosphere.2015.04.058
López-Perea JJ, Camarero PR, Molina-López RA et al (2015) Interspecific and geographical differences in anticoagulant rodenticide residues of predatory wildlife from the Mediterranean region of Spain. Sci Total Environ 511:259–267. https://doi.org/10.1016/j.scitotenv.2014.12.042
Lund M (2015) Commensal rodents. In: Buckle AP, Smith RH (eds) Rodent pests and their control. CABI, Oxfordshire, pp 19–32
Magiera S, Pardylla A, Baranowska I (2015) Effects of various factors of ultrasonic treatment on the extraction recovery of drugs from fish tissues. Ultrason Sonochem 26:388–398. https://doi.org/10.1016/j.ultsonch.2015.03.005
Mandel F, Wendt J, Vistocco R, Bachmann C (2000) Development of an LC/MS method for the analysis of rodenticides. Application note 5989-8440EN. Agilent Technologies, Waldbronn
Marek LJ, Koskinen WC (2007) Multiresidue analysis of seven anticoagulant rodenticides by high-performance liquid chromatography/electrospray/mass spectrometry. J Agric Food Chem 55:571–576. https://doi.org/10.1021/jf061440y
Market Data Forecast (2017) Europe rodenticides market by type (non-anticoagulant, anticoagulant), by mode of application (pellets, powders, sprays), by end user (agricultural fields, urban centres, warehouses, pest control companies, household consumers), and by region-Industry analysis, size, share, growth, trends, and forecasts (2016–2021). Market Data Forecast Inc., Hyderabad
Marsalek P, Modra H, Doubkova V, Vecerek V (2015) Simultaneous determination of ten anticoagulant rodenticides in tissues by column-switching UHPLC-ESI-MS/MS. Anal Bioanal Chem. https://doi.org/10.1007/s00216-015-8954-1
Maruya KA, Dodder NG, Tang C, Lao W, Tsukada D (2015) Which coastal and marine environmental contaminants are truly emerging? Environ Sci Pollut Res 22:1644–1652. https://doi.org/10.1007/s11356-014-2856-1
Masuda BM, Fisher P, Beaven B (2015) Residue profiles of brodifacoum in coastal marine species following an island rodent eradication. Ecotoxicol Environ Saf 113:1–8. https://doi.org/10.1016/j.ecoenv.2014.11.013
McDonald RA, Harris S, Turnbull G, Brown P, Fletcher M (1998) Anticoagulant rodenticides in stoats (Mustela erminea) and weasels (Mustela nivalis) in England. Environ Pollut 103:17–23. https://doi.org/10.1016/S0269-7491(98)00141-9
McLeod L, Saunders G (2013) Pesticides used in the management of vertebrate pests in australia: a review. NSW Department of Primary Industries, New South Wales
Medvedovici A, David F, Sandra P (1997) Determination of the rodenticides warfarin, diphenadione and chlorophacinone in soil samples by HPLC-DAD. Talanta 44:1633–1640. https://doi.org/10.1016/S0039-9140(97)00068-4
Morrison SA, Sieve KK, Ratajczak RE, Bringolf RB, Belden JB (2016) Simultaneous extraction and cleanup of high-lipid organs from white sturgeon (Acipenser transmontanus) for multiple legacy and emerging organic contaminants using QuEChERS sample preparation. Talanta 146:16–22. https://doi.org/10.1016/j.talanta.2015.08.021
Murphy G, Oldbury DJ (2002) Rat control by local authorities within the United Kingdom. In: Proceedings of the 4th international conference on urban pests,vol 246, pp 413–420
Murray M (2011) Anticoagulant rodenticide exposure and toxicosis in four species of birds of prey presented to a wildlife clinic in Massachusetts, 2006–2010. J Zoo Wildl Med 42:88–97
Nakagawa L, de Masi E, Narciso E, Neto HM, Papini S (2015) Palatability and efficacy of bromadiolone rodenticide block bait previously exposed to environmental conditions. Pest Manag Sci 71:1414–1418. https://doi.org/10.1002/ps.3944
Newton I, Wyllie I, Freestone P (1990) Rodenticides in British barn owls. Environ Pollut 68:101–117. https://doi.org/10.1016/0269-7491(90)90015-5
Newton I, Wyllie I, Dale L (1997) Mortality causes in British Barn Owls (Tyto alba), based on 1,101 carcasses examined during 1963–1996. United States Department of Agriculture Forest Service, Winnipeg, pp 299–307
Norström K, Remberger M, Kaj L et al (2009) Results from the Swedish National Screening Programme 2008. Subreport 3. Biocides: difenacoum. IVL Swedish Environmental Research Institute, Stockholm
Ogilvie SC, Pierce RJ, Wright GRG, Booth LH, Eason CT (1997) Brodifacoum residue analysis in water, soil, invertebrates, and birds after rat eradication on Lady Alice Island. N Z J Ecol 21:195–197
Oktay E (2015) Will NOACs become the new standard of care in anticoagulation therapy? Int J Cardiovasc Acad 1:1–4. https://doi.org/10.1016/j.ijcac.2015.06.007
Ondracek K, Bandouchova H, Hilscherova K et al (2015) Mixture toxicity of microcystin-LR, paraoxon and bromadiolone in Xenopus laevis embryos. Neuro Endocrinol Lett 36:114–119
Parker R (2013) Gute Aussichten für die Zukunft. DpS 2:13–15
Pérez S, Barceló D (2008) Applications of LC-MS to quantitation and evaluation of the environmental fate of chiral drugs and their metabolites. TrAC Trends Anal Chem 27:836–846. https://doi.org/10.1016/j.trac.2008.09.003
Pieper C, Holthenrich D, Schneider H (2014) Health risks from pest control products. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 57:574–584. https://doi.org/10.1007/s00103-013-1920-1
Pitt WC, Berentsen AR, Shiels AB et al (2015) Non-target species mortality and the measurement of brodifacoum rodenticide residues after a rat (Rattus rattus) eradication on Palmyra Atoll, tropical Pacific. Biol Conserv 185:36–46. https://doi.org/10.1016/j.biocon.2015.01.008
Primus TM, Wright G, Fisher P (2005) Accidental discharge of brodifacoum baits in a tidal marine environment: a case study. Bull Environ Contam Toxicol 74:913–919. https://doi.org/10.1007/s00128-005-0668-1
Ramirez AJ, Brain RA, Usenko S et al (2009) Occurrence of pharmaceuticals and personal care products in fish: results of a national pilot study in the United States. Environ Toxicol Chem 28:2587–2597. https://doi.org/10.1897/08-561.1
Rattner BA, Mastrota FN (2018) Anticoagulant rodenticide toxicity to non-target wildlife under controlled exposure conditions. In: van den Brink NW et al (eds) Anticoagulant rodenticides and wildlife. Springer, Cham, pp 45–86
Rattner BA, Lazarus RS, Elliott JE, Shore RF, van den Brink N (2014) Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife. Environ Sci Technol 48:8433–8445. https://doi.org/10.1021/es501740n
Sage M, Fourel I, Coeurdassier M, Barrat J, Berny P, Giraudoux P (2010) Determination of bromadiolone residues in fox faeces by LC/ESI-MS in relationship with toxicological data and clinical signs after repeated exposure. Environ Res 110:664–674. https://doi.org/10.1016/j.envres.2010.07.009
Sanchez-Barbudo IS, Camarero PR, Mateo R (2012) Primary and secondary poisoning by anticoagulant rodenticides of non-target animals in Spain. Sci Total Environ 420:280–288. https://doi.org/10.1016/j.scitotenv.2012.01.028
Santos LH, Gros M, Rodriguez-Mozaz S et al (2013) Contribution of hospital effluents to the load of pharmaceuticals in urban wastewaters: identification of ecologically relevant pharmaceuticals. Sci Total Environ 461:302–316. https://doi.org/10.1016/j.scitotenv.2013.04.077
Sato S (2005) Coumarin rodenticides. In: Suzuki O, Watanabe K (eds) Drugs and poisons in humans. Springer, Heidelberg, pp 599–608
Schaff JE, Montgomery MA (2013) An HPLC-HR-MS-MS method for identification of anticoagulant rodenticides in blood. J Anal Toxicol 37:321–325. https://doi.org/10.1093/jat/bkt036
Schmolz E, Wieck S, Friesen A (2014) Nagetierbekämpfung mit Antikoagulanzien—was ändert sich durch die Biozid-Zulassung für die Praxis? UMID 2:79–86
Schwabe U, Paffrath D, Ludwig W-D, Klauber J (eds) (2017) Arzneiverordnungs-report. Springer, Heidelberg
Shore RF, Birks JDS, Afsar A, Wienburg CL, Kitchener AC (2003) Spatial and temporal analysis of second-generation anticoagulant rodenticide residues in polecats (Mustela putorius) from throughout their range in Britain, 1992–1999. Environ Pollut 122:183–193. https://doi.org/10.1016/S0269-7491(02)00297-X
Siers SR, Shiels AB, Goldade DA et al (2016) Wake atoll fish tissue sampling and analysis three years after an island wide rodenticide application. Unpublished Report QA 2241, USDA, APHIS, WS, National Wildlife Research Center, Hilo, HI, USA
Smith LL, Liang B, Booth MC, Filigenzi MS, Tkachenko A, Gaskill CL (2017) Development and validation of quantitative ultraperformance liquid chromatography-tandem mass spectrometry assay for anticoagulant rodenticides in liver. J Agric Food Chem 65:6682–6691. https://doi.org/10.1021/acs.jafc.7b02280
Steffen D (2014) Orientierende Untersuchungen niedersächsischer Oberflächengewässer auf aktuell in Deutschland zugelassener Pflanzenschutzmittel und auf Stoffe der sog. Metaboliten-Liste. Niedersächsischer Landesbetrieb für Wasserwirtschaft, Küsten-und Naturschutz (NLWKN), Hannover-Hildesheim, Germany
Streit B (1998) Bioaccumulation of contaminants in fish. In: Braunbeck T, Hinton DE, Striet B (eds) Fish ecotoxicology. Birkhäuser, Basel
Tosh DG, McDonald RA, Bearhop S et al (2011) Does small mammal prey guild affect the exposure of predators to anticoagulant rodenticides? Environ Pollut 159:3106–3112. https://doi.org/10.1016/j.envpol.2011.03.028
Tosh DG, McDonald RA, Bearhop S, Llewellyn NR, Montgomery WI, Shore RF (2012) Rodenticide exposure in wood mouse and house mouse populations on farms and potential secondary risk to predators. Ecotoxicology 21:1325–1332. https://doi.org/10.1007/s10646-012-0886-3
Townsend MG, Entwisle P, Hart ADM (1995) Use of two halogenated biphenyls as indicators of non-target exposure during rodenticides treatments. Bull Environ Contam Toxicol 54:526–533. https://doi.org/10.1007/BF00192595
UBA (2011) Identifizierung und Bewertung ausgewählter Arzneimittel und ihrer Metaboliten (Ab- und Umbauprodukte) im Wasserkreislauf. Texte 46/2011, Umweltbundesamt, Dessau-Roßlau
UBA (2014) Authorisation of anticoagulant rodenticides in Germany—risk mitigation measures, best practice code and FAQs. Umweltbundesamt, Dessau-Roßlau
van den Brink NW, Elliott JE, Shore RF, Rattner BA (eds) (2018) Anticoagulant rodenticides and wildlife. Springer, Cham
Vudathala D, Cummings M, Murphy L (2010) Analysis of multiple anticoagulant rodenticides in animal blood and liver tissue using principles of QuEChERS Method. J Anal Toxicol 34:273–279. https://doi.org/10.1093/jat/34.5.273
Walker LA, Turk A, Long SM, Wienburg CL, Best J, Shore RF (2008) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392:93–98. https://doi.org/10.1016/j.scitotenv.2007.10.061
Walker LA, Llewellyn NR, Pereira MG et al (2010) Anticoagulant rodenticides in predatory birds 2007 and 2008: a Predatory Bird Monitoring Scheme (PBMS) report. Center for Ecology and Hydrology, Lancaster
Wardlaw J, Hughes J, Monie C, Reay G (2016) Pesticide usage in Scotland—rodenticide use by local authorities 2015. Science and Advice for Scottish Agriculture, Edinburgh
Wardlaw J, Hughes J, Monie C, Reay G (2017) Pesticide usage in Scotland—rodenticides on arable farms 2016. Science and Advice for Scottish Agriculture, Edinburgh
Watkins CD, Winemiller KO, Mora MA et al (2014) Assessment of mosquitofish (Gambusia affinis) health indicators in relation to domestic wastewater discharges in suburbs of Houston, USA. Bull Environ Contam Toxicol 93:13–18. https://doi.org/10.1007/s00128-014-1248-z
Weigt S, Huebler N, Strecker R, Braunbeck T, Broschard TH (2012) Developmental effects of coumarin and the anticoagulant coumarin derivative warfarin on zebrafish (Danio rerio) embryos. Reprod Toxicol 33:133–141. https://doi.org/10.1016/j.reprotox.2011.07.001
Wode F, van Baar P, Dunnbier U et al (2015) Search for over 2000 current and legacy micropollutants on a wastewater infiltration site with a UPLC-high resolution MS target screening method. Water Res 69:274–283. https://doi.org/10.1016/j.watres.2014.11.034
Wong LT, Solomonraj G (1980) Biliary and urinary excretion of [14C]warfarin in rabbits. Xenobiotica 10:201–210. https://doi.org/10.3109/00498258009033746
Zielinska A, Lichti CF, Bratton S et al (2008) Glucuronidation of monohydroxylated warfarin metabolites by human liver microsomes and human recombinant UDP glucuronosyltransferases. J Pharmacol Exp Ther 324:139–148. https://doi.org/10.1124/jpet.107.129858
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Support of this study was provided by the German Environment Agency through Grant FKZ 3716 67 403 0.
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Regnery, J., Friesen, A., Geduhn, A. et al. Rating the risks of anticoagulant rodenticides in the aquatic environment: a review. Environ Chem Lett 17, 215–240 (2019). https://doi.org/10.1007/s10311-018-0788-6
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DOI: https://doi.org/10.1007/s10311-018-0788-6