Case History: In March of 2021, a Bald Eagle (Haliaeetus leucocephalus) was found moribund by a deer carcass near a highway in South Dakota, USA.
Pathology Case of the Month - Bald Eagle
The bird was taken to a local facility and evaluated by a veterinarian. No signs of trauma were observed, and there was no evidence of broken bones on radiographs. There was a moderate amount of frank blood noted in the oral cavity that returned several times after being swabbed, which was suggestive of a gastrointestinal source. The eagle subsequently died and was submitted for diagnostic necropsy with a suspicion for anticoagulant rodenticide exposure.
Gross Findings: A subadult male Bald Eagle in good body condition and fair postmortem condition was examined at necropsy. Within the coelomic fat, there were multiple up to 2 cm in diameter dark red foci (hemorrhage). The coelomic cavity contained ~20 ml opaque, light red fluid and dark red clotted blood around the liver, heart, and lungs (Fig. 1A). The internal organs, especially the heart, liver, and kidneys, were pale tan. The liver had rounded margins, and the right liver lobe was partially replaced by multifocal to coalescing pockets of blood up to ~2 x 1 x 1 cm (Fig. 1B). The left liver lobe had a 10 x 2 mm area of hemorrhage with a 10 x 2 x 2 mm tear in the adjacent liver parenchyma. The crop and ventriculus contained recently ingested meat.
Diagnostic Test Results: Anticoagulant rodenticide testing on the liver using high-performance liquid chromatography performed at Michigan State University Veterinary Diagnostic Laboratory showed a brodifacoum level of 0.020 ppm (positive for exposure). The panel tests for first- and second-generation anticoagulant rodenticides, including brodifacoum, bromadiolone, chlorophacinone, difenacoum, difethialone, diphacinone, and warfarin. Liver lead screening was in the low-level background range (<3.0 ppm dry weight). Tracheal and cloacal swabs were negative for avian influenza by matrix RT-PCR.
Morphologic Diagnoses:
- Severe acute hemorrhage in the coelomic fat, coelomic cavity, liver, and lungs
- Brodifacoum exposure
Case Comment: Despite the detection of brodifacoum in the liver, the inciting cause of the hemorrhage is difficult to determine. The location of the eagle near a highway suggested a possible traumatic event, even though other signs of trauma (skeletal fractures, subcutaneous hemorrhages, etc.) were not present in this case. Based on a recent publication (see Niedringhaus et al. below), the liver brodifacoum level in this Bald Eagle is indicative of exposure at minimum, though mild trauma complicated by brodifacoum exposure could not be completely ruled out as a cause of hemorrhage given the location of the bird near a highway.
Etiology: Anticoagulant rodenticide (AR) exposure. In this case, brodifacoum, a second-generation anticoagulant rodenticide (SGAR), was identified from the liver.
Distribution: Anticoagulant rodenticides are commonly used worldwide for rodent control, and exposure to ARs can occur wherever these pesticides are used. Toxicosis in non-target wildlife caused by ARs has been reported in the United States, Canada, Europe, and New Zealand.
Host range: Rodenticides are toxic to many species of birds and mammals, including domestic animals, farm animals, and wildlife species. Birds of prey (i.e., eagles, hawks, owls) and scavengers (i.e., crows, vultures) may be at increased risk of exposure due to their diet.
Transmission: Toxicosis caused by ARs can occur from either direct ingestion of bait product (primary toxicosis) or indirectly from preying on or scavenging other animals (i.e., rodents, small mammals) that have consumed the bait (secondary toxicosis).
Pathogenesis: ARs interfere with blood clotting by inhibiting the activation of Vitamin K, a critical component in the production of blood clotting factors in the liver. Ingestion of ARs can result in interference with blood coagulation and spontaneous bleeding, either internally or externally. SGARs, including brodifacoum, bromadiolone, difenacoum, and difethiolone, are more lethal, and therefore often only require one dose, compared to first-generation anticoagulant rodenticides, such as warfarin, chlorphacinone, and diphacinone, which have a shorter elimination time and generally require multiple feedings of the bait before causing death.
Clinical signs: Typical signs of AR toxicity are due to coagulopathy and blood loss, including bruising, inappetence, lethargy, weakness, bleeding from the nares, pale mucous membranes, vomiting blood, blood in the urine and/or feces, increased heart rate, and respiratory distress. Abrupt death can occur if bleeding is sudden and significant. Depending on the type of rodenticide and the amount consumed, development of clinical signs may be delayed.
Pathology: On gross examination, bruising on the skin and bleeding into the body cavities are often seen. Mucous membranes and visceral organs can be pale from blood loss. Ingested bait or remains of poisoned small mammal may or may not be present in the digestive tract. Microscopically, acute hemorrhages can be confirmed in multiple organs, including the liver, lungs, kidneys, brain, heart, and spleen, as well as within the lumen of the gastrointestinal tract.
Diagnosis: The diagnosis of AR toxicosis in wild animals can be challenging because there are no standard toxicity ranges established for wildlife, sublethal exposure to ARs is common in birds of prey, and effects of anticoagulant rodenticides can depend on the species (e.g., raptors may be more sensitive than other avian species), age, and nutritional condition. There are also reports of multiple ARs present in individual animals. Toxicity should be suspected in cases of spontaneous hemorrhage(s) in the body when AR is detected in the liver and there is either a history of rodenticide use in the area or absence of other cause of acute hemorrhage (such as trauma). Unlike in domestic mammals, blood tests in birds for antemortem diagnosis of AR exposure or toxicosis are not well established.
Public health concerns: Children can be at risk of consuming rodenticides that are placed in the environment or if the rodenticides are not stored safely.
Wildlife population impacts: The effects on non-target species, such as birds of prey and scavengers, should be considered when rodenticide applications are used. The effects of sub-lethal exposure to ARs are not known for most wildlife species but might include compromised immune function with increased susceptibility to disease, thought to be caused by microscopic bleeds leading to tissue ischemia and organ dysfunction.
Management: Treatment for AR toxicosis includes Vitamin K to help restore normal coagulation and supportive care. Treatment is intensive and can be required for weeks to months after exposure, which makes it unrealistic for most wildlife cases.
References:
- Cornell Wildlife Health Lab. 2018. Rodenticide Toxicity. Cornell University College of Veterinary Medicine Animal Health Diagnostic Center. https://cwhl.vet.cornell.edu/disease/rodenticide-toxicity. Accessed June 2022.
- Hommerding H. 2022. Overview of rodenticide Poisoning in Animals. Merck Veterinary Manual. https://www.merckvetmanual.com/toxicology/rodenticide-poisoning/overview-of-rodenticide-poisoning-in-animals. Accessed June 2022.
- Murray M and Tseng F. 2008. Diagnosis and treatment of secondary anticoagulant rodenticide toxicosis in a red-tailed hawk (Buteo jamaicensis). J Avian Med Surg 22(1):41-46. https://doi.org/10.1647/2007-012R.1
- Nakayama SMM, Morita A, Ikenaka Y, Mizukawa H, Ishizuka M. 2019. A review: poisoning by anticoagulant rodenticides in non-targe animals globally. J Vet Med Sci 81(2): 298–313. https://doi.org/10.1292/jvms.17-0717
- Niedringhaus KD, Nemeth NM, Gibbs S, Zimmerman J, Shender L, Slankard K, Fenton H, Charlie B, Dalton multifocal, Elsmo EJ, Poppenga R, Millsap B, Ruder MG. 2021. Anticoagulant rodenticide exposure and toxicosis in bald eagles (Haliaeetus leucocephalus) and golden eagles (Aquila chrysaetos) in the United States. PLoS ONE 16(4): e0246134. https://doi.org/10.1371/journal.pone.0246134
- Rattner BA and Harvey JJ. 2021. Challenges in the interpretation of anticoagulant rodenticide residues and toxicity in predatory and scavenging birds. Pest Manag Sci 77: 604–610. https://doi.org/10.1002/ps.6137
- Rattner BA, Lazarus RS, Elliot 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