Skip to main content
Log in

Evaluating a Rapid Field Assessment System for Anticoagulant Rodenticide Exposure of Raptors

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Anticoagulant rodenticides (ARs) are commonly used to control rodent pests. However, worldwide, their use is associated with secondary and tertiary poisoning of nontarget species, especially predatory and scavenging birds. No medical device can rapidly test for AR exposure of avian wildlife. Prothrombin time (PT) is a useful biomarker for AR exposure, and multiple commercially available point-of-care (POC) devices measure PT of humans, and domestic and companion mammals. We evaluated the potential of one commercially available POC device, the Coag-Sense® PT/INR Monitoring System, to rapidly detect AR exposure of living birds of prey. The Coag-Sense device delivered repeatable PT measurements on avian blood samples collected from four species of raptors trapped during migration (Intraclass Correlation Coefficient > 0.9; overall intra-sample variation CV: 5.7%). However, PT measurements reported by the Coag-Sense system from 81 ferruginous hawk (Buteo regalis) nestlings were not correlated to those measured by a one-stage laboratory avian PT assay (r = − 0.017, p = 0.88). Although precise, the lack of agreement in PT estimates from the Coag-Sense device and the laboratory assay indicates that this device is not suitable for detecting potential AR exposure of birds of prey. The lack of suitability may be related to the use of a mammalian reagent in the clotting reaction, suggesting that the device may perform better in testing mammalian wildlife

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AR:

Anticoagulant rodenticides

PT:

Prothrombin time

POC:

Point-of-care

SGAR:

Second generation anticoagulant rodenticides

References

  • Abernathy EV, Hull JM, Fish AM, Briggs CW (2018) Secondary anticoagulant rodenticide exposure in migrating juvenile red-tailed hawks (Buteo jamaicensis) in relationship to body condition. J Raptor Res 52:225–230. https://doi.org/10.3356/JRR-17-39.1

    Article  Google Scholar 

  • Berlin N, Kelmer E, Segev G, Aroch I, Kelmer G (2019) Assessment of the CoaguChek-XS portable prothrombin time point-of-care analyzer for horses. J Vet Diagn Investig 31:448–452. https://doi.org/10.1177/1040638719832340

    Article  CAS  Google Scholar 

  • Berny P, Esther A, Jacob J, Prescott C (2018) Development of resistance to anticoagulant rodenticides in rodents. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (eds) Anticoagulant rodenticides and wildlife. Springer, New York, pp 259–286

    Chapter  Google Scholar 

  • Bloom PH, Clark WS, Kidd JW (2007) Capture techniques. In: Bird D, Bildstein K (eds) Raptor research and management techniques. Hancock House Publishers Ltd, Surrey, BC, pp 193–219

    Google Scholar 

  • Cox P, Smith RH (1992) Rodenticide ecotoxicology: pre-lethal effects of anticoagulants on rat behaviour. In: Borrecco JE, Marsh RE (eds) Proceedings of the 15th vertebrate pest conference. University of California, Davis, California, USA, pp 165–170

  • Dickson AJ (2020) Prevalence of anticoagulant rodenticides in ferruginous hawk nestlings and evaluation of a novel method to rapidly assess exposure. M.S. Thesis, Boise State University, Boise, Idaho, USA

  • Doerr JA, Wyatt RD, Hamilton PB (1975) Investigation and standardization of prothrombin times in chickens. Poult Sci 54:969–980. https://doi.org/10.3382/ps.0540969

    Article  CAS  Google Scholar 

  • Doolittle RF, Feng DF (1987) Reconstructing the evolution of vertebrate blood coagulation from a consideration of the amino acid sequences of clotting proteins. Cold Spring Harb Symp Quant Biol 52:869–874. https://doi.org/10.1101/SQB.1987.052.01.095

    Article  CAS  Google Scholar 

  • Elliott JE, Rattner BA, Shore RF, Van Den Brink NW (2016) Paying the pipers: mitigating the impact of anticoagulant rodenticides on predators and scavengers. Bioscience 66:401–407. https://doi.org/10.1093/biosci/biw028

    Article  Google Scholar 

  • Environmental Protection Agency (EPA) (2017) Restrictions on rodenticide products. https://www.epa.gov/rodenticides/restrictions-rodenticide-products. Accessed 3 Oct 2017

  • Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. Office of Prevention, Pesticides and Toxic Substances, United States Environmental Protection Agency, Washington, DC, USA

  • Frost CL, Naudé RJ, Oelofsen W, Jacobson B (1999) Comparative blood coagulation studies in the ostrich. Immunopharmacology 45:75–81. https://doi.org/10.1016/S0162-3109(99)00058-2

    Article  CAS  Google Scholar 

  • Gamer M, Lemon J, Singh P (2019) irr: various coefficients of interrater reliability and agreement. R package version 0.84.1.https://CRAN.R-project.org/package=irr

  • Gossett DN (1993) Studies of ferruginous hawk biology: I. Recoveries of banded ferruginous hawks from presumed eastern and western subpopulations. II. Morphological and genetic differences of presumed subpopulations of ferruginous hawks. III. Sex determination of nestling ferruginous hawks. M.S. Thesis, Boise State University, Boise, Idaho, USA

  • Guddorf V, Kummerfeld N, Mischke R (2014) Methodical aspects of blood coagulation measurements in birds applying commercial reagents—a pilot study. Berliner und Münchener Tierärztliche Wochenschrift 127:322–327. https://doi.org/10.2376/0005-9366-127-322

    Article  Google Scholar 

  • Hadler MR, Buckle AP (1992) Forty-five years of anticoagulant rodenticides—past, present and future trends. In: Borrecco JE, Marsh RE (eds) Proceedings of the 15th vertebrate pest conference. University of California, Davis, California, USA, pp 165–170

  • Harris LF, Castro-López V, Killard AJ (2013) Coagulation monitoring devices: past, present, and future at the point of care. Trends Anal Chem 50:85–95. https://doi.org/10.1016/j.trac.2013.05.009

    Article  CAS  Google Scholar 

  • Herring G, Eagles-Smith CA, Bedrosian B, Craighead D, Domenech R, Langner HW, Parish CN, Shreading A, Welch A, Wolstenholme R (2018) Critically assessing the utility of portable lead analyzers for wildlife conservation. Wildl Soc Bull 42:284–294

    Article  Google Scholar 

  • Hindmarch S, Rattner BA, Elliott JE (2019) Use of blood clotting assays to assess potential anticoagulant rodenticide exposure and effects in free-ranging birds of prey. Sci Total Environ 657:1205–1216. https://doi.org/10.1016/j.scitotenv.2018.11.485

    Article  CAS  Google Scholar 

  • Hull B, Bloom P (2001) The North American banders manual for raptor banding techniques. North American Banding Council, Point Reyes Station

    Google Scholar 

  • Jacob J, Buckle A (2018) Use of anticoagulant rodenticides in different applications around the world. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (eds) Anticoagulant rodenticides and wildlife. Springer, New York, pp 11–44

    Chapter  Google Scholar 

  • Kazuki T, Manago K, Nakayama SMM, Moirta A, Ikenaka Y, Ishizuka M (2020) Pharmacokinetics/dynamics analysis of anticoagulant rodenticides with Egyptian fruit bats (Rousettus aegyptiacus). In: Proceedings of the international symposium on the chemistry hazards wildlife. February 5, 2020 Hokkaido University, Japan, pp 30–31

  • Kelmer E, Segev G, Codner C, Bruchim Y, Klainbart S, Aroch I (2014) Assessment of a portable prothrombin time analyzer (CoaguChek-XS) in dogs. J Vet Emerg Crit Care 24:455–460. https://doi.org/10.1111/vec.12200

    Article  Google Scholar 

  • Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropractic Med 15:155–163. https://doi.org/10.1016/j.jcm.2016.02.012

    Article  Google Scholar 

  • Laakso S, Suomalainen K, Koivisto S (2010) Literature review on residues of anticoagulants in non-target animals. Nordic Council of Ministers, Copenhagen

    Google Scholar 

  • Last JA (2002) The missing link: the story of Karl Paul Link. Toxicol Sci 66:4–6. https://doi.org/10.1093/toxsci/66.1.4

    Article  CAS  Google Scholar 

  • López-Perea JJ, Mateo R (2018) Secondary exposure to anticoagulant rodenticides and effects on predators. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (eds) Anticoagulant rodenticides and wildlife. Springer, New York, pp 159–193

    Chapter  Google Scholar 

  • Martin AGR, Kirkpatrick WE, King DR, Robertson ID, Hood PJ, Sutherland JR (1994) Assessment of the potential toxicity of an anticoagulant, pindone (2-pivalyl-l, 3-indandione), to some Australian birds. Wildl Res 21:85–93. https://doi.org/10.1071/WR9940085

    Article  Google Scholar 

  • Monks DJ, Forbes NA (2007) Hematological. In: Bird D, Bildstein K (eds) Raptor research and management techniques. Hancock House Publishers Ltd, Surrey, BC, pp 270–284

    Google Scholar 

  • Moritsch M (1985) Photographic guide for aging nestling ferruginous hawks. Bureau of Land Management, Boise

    Google Scholar 

  • Murray M (2018) Ante-mortem and post-mortem signs of anticoagulant rodenticide toxicosis in birds of prey. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (eds) Anticoagulant rodenticides and wildlife. Emerging topics in ecotoxicology (principles, approaches and perspectives). Springer, New York

    Google Scholar 

  • Murray M, Tseng F (2008) Diagnosis and treatment of secondary anticoagulant rodenticide toxicosis in a red-tailed hawk (Buteo jamaicensis). J Avian Med Surg 22:41–46. https://doi.org/10.1647/2007-012R.1

    Article  Google Scholar 

  • Nabity MB, Harr KE, Camus MS, Flatland B, Vap LM (2018) ASVCP guidelines: allowable total error hematology. Vet Clin Pathol 47:9–21. https://doi.org/10.1111/vcp.12583

    Article  Google Scholar 

  • Nakayama SMM, Morita A, Ikenaka Y, Mizukawa H, Ishizuka M (2019) A review: poisoning by anticoagulant rodenticides in non-target animals globally. J Vet Med Sci 81:298–313. https://doi.org/10.1292/jvms.17-0717

    Article  CAS  Google Scholar 

  • Newbould A, Norman E (2013) Comparison of point-of-care analysis using Coaguchek XS and standard laboratory-measured prothrombin time in dogs. N Z Vet J 61:18–24. https://doi.org/10.1080/00480169.2012.709816

    Article  CAS  Google Scholar 

  • Pelz H-J, Rost S, Hünerberg M, Fregin A, Heiberg A-C, Baert K, MacNicoll AD, Prescott CV, Walker A-S, Oldenburg J, Müller CR (2005) The genetic basis of resistance to anticoagulants in rodents. Genetics 170:1839–1847. https://doi.org/10.1534/genetics.104.040360

    Article  CAS  Google Scholar 

  • Pirmohamed M (2006) Warfarin: almost 60 years old and still causing problems. Br J Clin Pharmacol 62:509–511. https://doi.org/10.1111/j.1365-2125.2006.02806.x

    Article  Google Scholar 

  • Plesch W, Wolf T, Breitenbeck N, Dikkeschei LD, Cervero A, Perez PL, van den Besselaar AMHP (2008) Results of the performance verification of the CoaguChek XS system. Thromb Res 123:381–389. https://doi.org/10.1016/j.thromres.2008.04.021

    Article  CAS  Google Scholar 

  • Rattner BA, Horak KE, Johnston JJ (2010) Comparative toxicity of diphacinone to northern bobwhite (Colinus virginianus) and American kestrels (Falco sparverius). Ecotoxicol Environ Saf 73:1159–1164. https://doi.org/10.1016/j.ecoenv.2010.05.021

    Article  CAS  Google Scholar 

  • Rattner BA, Horak KE, Lazarus RS, Goldade DA, Johnston JJ (2014) Toxicokinetics and coagulopathy threshold of the rodenticide diphacinone in eastern screech-owls (Megascops asio). Environ Toxicol Chem 33:74–81. https://doi.org/10.1002/etc.2390

    Article  CAS  Google Scholar 

  • Review Memorandum (2018) Substantial equivalence determination decision summary. http://www.accessdata.fda.gov/cdrh_docs/reviews/K093243.pdf> Accessed 17 Oct 2019

  • Rodriguez-Ramos J (2009) Lead in griffon and cinereous vultures in central Spain: Correlations between clinical signs and blood lead levels. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • van den Brink N, Elliott JE, Shore RF, Rattner BA (2018) Anticoagulant rodenticides and wildlife. Springer, New York

    Book  Google Scholar 

  • Webster K, Harr K, Bennett D, Williams T, Cheng K, Maisonneuve F, Elliott J (2015) Assessment of toxicity and coagulopathy of brodifacoum in Japanese quail and testing in wild owls. Ecotoxicology 24:1087–1101. https://doi.org/10.1007/s10646-015-1449-1

    Article  CAS  Google Scholar 

  • Wells PS, Brown A, Jaffey J, McGahan L, Poon M-C, Cimon K (2007) Safety and effectiveness of point-of-care monitoring devices in patients on oral anticoagulant therapy: a meta-analysis. Open Med 1:131–146

    Google Scholar 

Download references

Acknowledgements

The authors thank Dr. M. Brooks and A. Stablein from the Comparative Coagulation Laboratory in the Animal Health Diagnostic Center at Cornell University for assistance with prothrombin time analyses; G. Isted, B. Walker, P. Dumandan, S. Alsup, T. Jolley, J. Yurick, P. Ortiz, M. Sherman, and A. Meyer for field assistance and sample processing; and G. Herring and two anonymous reviewers for comments that improved our manuscript. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Funding

This work was supported by the United States Fish and Wildlife Service [Cooperative Agreement Award F16AC00961], the Raptor Research Center at Boise State University and the US Geological Survey.

Author information

Authors and Affiliations

Authors

Contributions

BWS, JRB, and TEK obtained funding; AJD, JRB, TEK, BWS, KAM, and BAR designed the study; AJD collected data with assistance of MJS, ZPW, and MJL; AJD and JRB analyzed the data and interpreted them with assistance from TEK and BAR, AJD led writing with assistance from JRB and TEK and all authors contributed to revisions.

Corresponding author

Correspondence to Ariana J. Dickson.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethical Approval

These studies were approved by the Boise State University Animal Care and Use Committee (protocols #006-AC18-003 and #AC17-015) and conducted under the following State and Federal permits: Colorado scientific collection license #19trb2091a, state of Idaho permits #110728 and #990121, Wyoming Chapter 33 permit #729, and USGS Bird Banding Permits #23715 and #22929. All study animals were released unharmed at original capture locations.

Availability of Data and Material

Data from this study can be found in: Dickson A (2020) Prevalence of Anticoagulant Rodenticides in Ferruginous Hawk Nestlings and Evaluation of a Novel Method to Rapidly Assess Exposure. MS thesis, Boise State University, Boise, Idaho, U.S.A.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 31 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dickson, A.J., Belthoff, J.R., Mitchell, K.A. et al. Evaluating a Rapid Field Assessment System for Anticoagulant Rodenticide Exposure of Raptors. Arch Environ Contam Toxicol 79, 454–460 (2020). https://doi.org/10.1007/s00244-020-00763-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-020-00763-6

Navigation