Abstract

In response to recent precipitous declines of vulture populations in the Indian subcontinent, the Peregrine Fund established the Asian Vulture Crisis Project. This collaborative project with the Ornithological Society of Pakistan, documented adult and subadult mortality as high as 86% and estimated population declines of 34–95% at breeding colonies in Punjab Province of Pakistan between 2000 and 2003¹ (Gilbert, recent unpublished data). Visceral gout (uric acid precipitation on visceral surfaces) was the significant finding in 219 of 259 (85%) vultures necropsied.³ Most of the vultures with visceral gout were in good body condition, suggesting the vultures were foraging well and the disease condition was of short duration prior to death. Microscopic examination confirmed urate deposition with associated necrosis in kidney, liver, spleen, lung, heart, adrenal gland, parathyroid gland, skin, fascia of skeletal muscle, as well as urate deposition on visceral surfaces. Renal damage in vultures was severe, acute, and throughout the sections of kidney. There was minimal inflammation and no evidence of repair of renal tubules. When renal architecture could be identified in kidneys with less extensive lesions, the proximal renal tubular epithelium was preferentially damaged without urate deposition, and the collecting tubules and glomeruli were relatively spared. Kidneys with more “chronic” lesions had necrosis of almost all renal epithelium with extensive urate deposition both in dilated renal tubules and interstitium. With the exception of early gouty tophi in the kidneys with more advanced stages of renal disease, there was no consistent inflammation. Because kidneys with early lesions had acute renal tubular necrosis without evidence of urate deposition, the renal failure was considered the primary problem and cause of visceral urate deposition, rather than urate deposition causing the renal failure. Because kidneys in early stages of disease had necrosis of epithelium of proximal tubules and not collecting or distal convoluted tubules, the likelihood of an ascending nephrosis due to disease and subsequent obstruction of the ureter was unlikely. Published reports of dehydration-induced renal pathology that would have been consistent with the severity and distribution of that seen in these vultures could not be found. The most likely cause of acute renal tubular necrosis of this magnitude and uniformity, without inflammation was considered to be a nephrotoxic compound.

Vultures dying with extensive visceral gout have been reported throughout much of the Indian subcontinent,⁴ suggesting that a nephrotoxic agent would need to be available over a large geographic area. Extensive tissue analysis for infectious agents, metals, and contaminants did not identify a likely etiology.³ The primary food source for Oriental white-backed vultures in Pakistan is discarded carcasses of domestic animals. A survey of veterinarians and pharmaceutical retailers in Pakistan conducted by Oaks and Gilbert³ in the Fall of 2002 identified widespread use of diclofenac, a non-steroidal anti-inflammatory drug, in domestic livestock. Non-steroidal anti-inflammatory drugs are potentially nephrotoxic, although reports of adverse effects associated with their use in birds are not common.^2,5 Subsequent analysis of vulture tissues identified diclofenac residues in all of the Oriental white-backed vultures that had necropsy evidence of visceral urate deposition and severe renal damage microscopically. Diclofenac residues were not found in Oriental white-backed vultures dying from other causes.³

Captive, non-releasable Oriental white-backed vultures that were either directly treated with diclofenac or fed livestock that were treated with therapeutic doses of diclofenac before euthanasia confirmed the acute toxicity of diclofenac in these birds and strengthened the hypothesis that Oriental white-backed vulture could be exposed to lethal levels of diclofenac by scavenging disposed domestic animals treated with diclofenac before death. Severe renal lesions, indistinguishable from those seen in the 26 Oriental white-backed vultures examined from the wild, were seen in the experimental vultures both directly and indirectly exposed to diclofenac. The impact of this non-steroidal anti-inflammatory drug on the population of Oriental white-backed vulture in Pakistan makes diclofenac an important consideration when looking for the cause of mortality in other populations of vultures on the Indian subcontinent with identifiable visceral gout or renal failure. Risk to populations of scavenging raptors in other parts of the world would depend on species sensitivity and availability to scavengers of exposed carcasses treated with diclofenac.

Literature Cited

1.  Gilbert M, Virani MZ, Watson RT, Oaks JL, Benson PC, Khan AA, et al. Breeding and mortality of Oriental white-backed vulture Gyps bengalensis in Punjab Province, Pakistan. Bird Conservation International. 2002;12:311–326.

2.  Klein PN, Charmatz K, Langenberg J. The effect of flunixin meglumine (Banamine®) on the renal function in the northern bobwhite (Colinus virginianus): an avian model. In: Proceedings from the American Association of Zoo Veterinarians. 1994;128–131.

3.  Oaks JL, Gilbert M, Virani MZ, Watson RT, Meteyer CU, Rideout BA, et al. Diclofenac residues as the cause of vulture population decline in Pakistan. Nature. 2003;427:630–633.

4.  Pain D. Causes and effects of temporospatial declines of Gyps vultures in Asia. Conservation Biology. 2003;17:661–671.

5.  Paul-Murphy J. Ludders JW. Avian Analgesia. In: Veterinary Clinics of North America Exotic Animal Practice: Analgesia and Anesthesia. Philadelphia, PA: WB Saunders; 2001;4:35–45.