Department of Pathology, Smithsonian National Zoological Park, Washington, DC, USA
Aluminum phosphide (AlP) is a regulated pesticide used worldwide against rodents and insects. Its main use is fumigation of grain and other agricultural products and it is also used for treatment of rodent burrows.1 Upon contact with moisture, toxic phosphine gas (hydrogen phosphide) is liberated. The liberation of phosphine is accelerated by an acidic environment such as the hydrochloric acid of the stomach following ingestion.1,2
Toxicosis associated with AlP can occur following either inhalation of phosphine gas or ingestion of the solid product leading to a subsequent release of phosphine internally. The toxic mechanism of the gas has not been fully elucidated,2 however, phosphine has been shown to block cytochrome C oxidase in rat liver preparations. The resulting blockage of electron transfer and inhibition of oxidative phosphorylation lead to an energy crisis in the cells.1 Postmortem findings in rodents and humans include cyanosis, pulmonary edema, pleural effusion and congestion of internal organs.1,2
On the morning of 11 January 2003 two previously healthy adult male red pandas (Ailurus fulgens fulgens) were found dead on the ground of their outdoor enclosure at the Smithsonian National Zoological Park (SNZP). On the previous afternoon, 1–2 aluminum phosphide pellets weighing 3 g each (Fumitoxin, Pestcon Systems, Inc. USA) were buried in each of seven rodent holes in the enclosure by a private pest control contractor; the pellets were said to have been placed approximately 60 cm deep. The treated holes were then covered with metal plates or soil. Several other rodent holes remained open and uncovered. During the placement of the AlP pellets, both red pandas were observed in a tree in the exhibit.
Full necropsies were performed under chemical hoods on both red pandas. Both animals were found to be in excellent nutritional condition with stomachs partially filled with bamboo ingesta, and normal feces in the lower digestive tract. There was no evidence of external or internal injury or trauma and no outward or systemic signs of infectious diseases. Significant gross abnormalities noted in both animals included subcutaneous dehydration, cyanosis of mucous membranes and lungs, generalized dark venous congestion, and aspiration of fluid gastric contents into the trachea and bronchi. Peri-oral staining of bilious vomitus was present in one of the animals.
Histopathologic findings in both cases were similar and included acute pulmonary edema and emphysema, degenerative changes in the liver, including eosinophilic, diastase-resistant PASpositive cytoplasmic inclusion bodies within hepatocytes, edema of the gallbladder and proteinaceous casts in the kidneys. These changes are compatible with a systemic insult by a toxic agent. Similar liver inclusion bodies have occurred in association with certain chemicals toxic to the liver in humans.4 Mild inflammatory changes were noted in the kidneys and livers of both red pandas and a few lymphocytes in the meninges of one of the animals. These changes were considered preexistent and noncontributory. Cytologic examination of abdominal fluid and heart blood were within normal limits, and cultures from abdominal fluid, heart blood, liver and feces were negative or determined to be nonpathogenic and noncontributory to any of the histopathologic changes noted.
Using gas chromatography-mass spectrometric methods (GC-MS), stomach contents and tissue samples from both red pandas were analyzed specifically for the constituents of aluminum phosphide and generally for heavy metals, pesticides, drugs and industrial chemicals by the Michigan State University Animal Health Diagnostic Laboratory. After treatment of stomach contents from each red panda with strong acid, phosphine gas was detected at 163 and 58 ppm respectively. Aluminum levels in the stomach contents of each animal were 1030 ppm and 444 ppm. Aluminum levels in their feed (bamboo and biscuit) and feces ranged from 30–147 ppm. In addition, lung levels of aluminum in both affected red pandas were 69.3 ppm and 71.3 ppm, respectively. The aluminum level in archived frozen normal lung tissue from another SNZP red panda used as a control was 5.48 ppm. Aluminum levels in kidney and liver tissues were <1 ppm in both affected red pandas.
The high phosphine gas levels and relatively high amounts of aluminum detected in the stomach contents of both red pandas indicate the digestive tract as the portal of entry, and that the animals most likely ingested the aluminum phosphide rodenticide. The increased level of aluminum in the lungs of both red pandas relative to the low level in the control red panda’s lung tissue is likely due to agonal aspiration of gastric fluid.
Red pandas are nocturnal animals and most likely descended from the tree to investigate changes in their environment the evening after their exhibit yard had been treated with the rodenticide. Physical signs of digging were not evident, and it is unlikely a red panda would be able to dig deeply enough to retrieve and ingest aluminum phosphide pellets buried 60 cm deep. However, the curious nature and chemo-sensory behavior of investigating unknown materials in their environment by tongue-tasting,3 suggests the red pandas ingested fragments of aluminum phosphide that may have escaped in the area during the rodenticide placement procedure.
1. Gupta, S. and S.K. Ahlawat. 1995. Aluminum phosphide poisoning—a review. Clinical Toxicology 33:19–24.
2. Plumlee, K.H. 1997. Toxicant use in the zoo environment. J. Zoo Wildl. Med. 28(1):20–27.
3. Roberts, M.S. and J.L. Gittleman. 1984. Ailurus fulgens, Mammalian Species, American Society of Mammologists 222:1–8.
4. Zimmerman, H.J. and K.G. Ishak. 1994. Hepatic injury due to drugs and toxins. In: Pathology of the Liver, 3rd Ed. pp 591–592, ed. MacSween R.N.M. et al. Churchill Livingstone, London UK.