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Apparent Tolerance of Turkey Vultures (<I>Cathartes Aura</I>) To

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Apparent Tolerance of Turkey Vultures (<I>Cathartes Aura</I>) To University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln USGS Staff -- ubP lished Research US Geological Survey 2008 Apparent Tolerance Of Turkey Vultures (Cathartes Aura) To The on-SN teroidal Anti-Inflammatory Drug Diclofenac Barnett A. Rattner U.S. Geological Survey, [email protected] Maria A. Whitehead The Center for Birds of Prey Grace Gasper The Center for Birds of Prey Carol U. Meteyer U.S. Geological Survey William A. Link U.S. Geological Survey See next page for additional authors Follow this and additional works at: http://digitalcommons.unl.edu/usgsstaffpub Part of the Geology Commons, Oceanography and Atmospheric Sciences and Meteorology Commons, Other Earth Sciences Commons, and the Other Environmental Sciences Commons Rattner, Barnett A.; Whitehead, Maria A.; Gasper, Grace; Meteyer, Carol U.; Link, William A.; Taggart, Mark A.; Meharg, Andrew A.; Pattee, Oliver H.; and Pain, Deborah J., "Apparent Tolerance Of Turkey Vultures (Cathartes Aura) To The on-SN teroidal Anti- Inflammatory Drug Diclofenac" (2008). USGS Staff -- Published Research. 967. http://digitalcommons.unl.edu/usgsstaffpub/967 This Article is brought to you for free and open access by the US Geological Survey at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USGS Staff -- ubP lished Research by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Barnett A. Rattner, Maria A. Whitehead, Grace Gasper, Carol U. Meteyer, William A. Link, Mark A. Taggart, Andrew A. Meharg, Oliver H. Pattee, and Deborah J. Pain This article is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/usgsstaffpub/967 Environmental Toxicology and Chemistry, Vol. 27, No. 11, pp. 2341–2345, 2008 ᭧ 2008 SETAC Printed in the USA 0730-7268/08 $12.00 ϩ .00 Short Communication APPARENT TOLERANCE OF TURKEY VULTURES (CATHARTES AURA) TO THE NON-STEROIDAL ANTI-INFLAMMATORY DRUG DICLOFENAC BARNETT A. RATTNER,*† MARIA A. WHITEHEAD,‡ GRACE GASPER,‡ CAROL U. METEYER,§ WILLIAM A. LINK,† MARK A. TAGGART,࿣#ANDREW A. MEHARG,࿣ OLIVER H. PATTEE,† and DEBORAH J. PAIN†† †Patuxent Wildlife Research Center, U.S. Geological Survey, ࡆBeltsville Agricultural Research Center-East, Building 308, 10300 Baltimore Avenue, Beltsville, Maryland 20705 ‡The Center for Birds of Prey, P.O. Box 1247, Charleston, South Carolina 29402, USA §National Wildlife Health Center, U.S. Geological Survey, 6006 Schroeder Road, Madison, Wisconsin 53711 ࿣School of Biological Sciences, Department of Plant and Soil Science, University of Aberdeen AB24 3UU, Aberdeen, United Kingdom #Instituto de Investigacio´n en Recursos Cinege´ticos, Consejo Superior de Investigaciones Cientificas, Universidad de Castilla, La Mancha, Junta de Comunidades de Castilla, La Mancha, Ronda de Toledo s/n, 13005, Ciudad Real, Spain ††Royal Society for the Protection of Birds, The Lodge Sandy, Bedfordshire SG19 2DL, United Kingdom (Received 12 March 2008; Accepted 22 April 2008) Abstract—The nonsteroidal anti-inflammatory drug diclofenac is extremely toxic to Old World Gyps vultures (median lethal dose ϳ0.1–0.2 mg/kg), evoking visceral gout, renal necrosis, and mortality within a few days of exposure. Unintentional secondary poisoning of vultures that fed upon carcasses of diclofenac-treated livestock decimated populations in the Indian subcontinent. Because of the widespread use of diclofenac and other cyclooxygenase-2 inhibiting drugs, a toxicological study was undertaken in turkey vultures (Cathartes aura) as an initial step in examining sensitivity of New World scavenging birds. Two trials were conducted entailing oral gavage of diclofenac at doses ranging from 0.08 to 25 mg/kg body weight. Birds were observed for 7 d, blood samples were collected for plasma chemistry (predose and 12, 24, and 48 h and 7 d postdose), and select individuals were necropsied. Diclofenac failed to evoke overt signs of toxicity, visceral gout, renal necrosis, or elevate plasma uric acid at concen- trations greater than 100 times the estimated median lethal dose reported for Gyps vultures. For turkey vultures receiving 8 or 25 mg/kg, the plasma half-life of diclofenac was estimated to be 6 h, and it was apparently cleared after several days as no residues were detectable in liver or kidney at necropsy. Differential sensitivity among avian species is a hallmark of cyclooxygenase-2 inhibitors, and despite the tolerance of turkey vultures to diclofenac, additional studies in related scavenging species seem warranted. Keywords—Diclofenac Scavenging birds Species sensitivity Vultures INTRODUCTION gout (grossly visible urate deposits on internal organs) that is Diclofenac is a nonsteroidal anti-inflammatory drug the result of kidney failure [1]. Acute necrosis of the proximal (NSAID) used by veterinarians for the treatment of inflam- convoluted tubules in affected individuals is severe [7]. Di- mation, fever, and pain in domestic livestock. This drug ap- clofenac is known to be a potent inhibitor of cyclooxygenase- pears to have been the principal cause of a population crash 2 and prostaglandin synthetase. From a mechanistic perspec- of Old World vultures (genus Gyps) in India, Pakistan, and tive, it has been hypothesized that impaired production of pros- Nepal [1–5]. Vultures unintentionally ingested diclofenac taglandins E 2 and I2 may alter smooth muscle control of the when scavenging carcasses of livestock that had been treated renal portal valve and shunt blood from the renal cortex; this with this drug shortly before death. This is perhaps the only would result in ischemia and necrosis of the proximal con- well-documented instance of a veterinary or human drug re- voluted tubules [7]. Similar pathology has also been reported sulting in an adverse population-level response in nontarget in domestic fowl (Gallus gallus), although they seem to be free-ranging wildlife. considerably more tolerant to diclofenac (median lethal dose Based upon observational and experimental data, the me- estimate of 9.8 mg/kg when administered intramuscularly) [8]. dian lethal dose (LD50) of diclofenac in Oriental white-backed Although veterinary use of diclofenac in India is being vulture (Gyps bengalensis) was estimated to be 0.098 mg/kg phased out and an alternative that is not toxic to Gyps vultures body weight (95% CI, 0.027–0.351 mg/kg), and 0.225 mg/kg has been identified (meloxicam [9]), widespread sale and vet- (95% CI, 0.117–0.432 mg/kg) when an outlier was excluded erinary and human use of diclofenac continues on a global [1,6]. Oral dosing of Eurasian (G. fulvus) and African (G. scale [10,11] (http://www.birdlife.org/news/news/2007/11/ africanus) vultures with diclofenac at 0.8 mg/kg body weight africa࿞diclofenac.html; accessed 19 December 2007). At pres- has been shown to evoke a substantial increase in plasma uric ent there are no data on diclofenac-induced mortality in free- acid, which is indicative of altered renal function, and dosed ranging birds of prey in North and South America. While New birds succumb within 48 h [6]. Based upon lethality data, and Old World vultures are not closely related, data on diclo- diclofenac can be categorized as extremely toxic to Gyps vul- fenac toxicity to New World vultures is warranted for several tures. Pathological signs in affected vultures include visceral reasons. Notably, simple extrapolation of diclofenac toxicity data for Gyps vultures (order Falconiformes family Accipitri- * To whom correspondence may be addressed ([email protected]). dae) may not adequately assess risk in New World vultures Published on the Web 5/13/2008. (order Ciconiiformes family Cathartidae) due to taxonomic and 2341 2342 Environ. Toxicol. Chem. 27, 2008 B.A. Rattner et al. genetic distinctions; diclofenac is easy to manufacture, inex- activities, but was ultimately included in trial 2 as plasma pensive, and readily accessible in many undeveloped countries enzyme activities had declined substantially. for treatment of livestock; seven species of vultures are found in North and South America and numerous reports in devel- Diclofenac-dosing solutions oped countries document poisoning of raptors that fed on an- Because of difficulties in the importation of the veterinary imal carcasses treated with veterinary drugs (barbiturates) or formulation of diclofenac used in the Indian subcontinent, exposed to pesticides [12–16]; carcass burial and disposal technical grade sodium diclofenac (2-[(2,6-dichlorophen- practices are less sophisticated on ranches with large open yl)amino]benzeneacetic acid sodium salt; Ͼ99% purity; Chem- range, in remote regions, and in undeveloped countries, in- ical Abstract Service no. 15307-79-6) was purchased from creasing the likelihood of exposure; modeling studies suggest Sigma-Aldrich (St. Louis, MO, USA). A 2.5 mg/ml stock so- that even the rare presence of contaminated carcasses can have lution was prepared by dissolving sodium diclofenac in dis- significant population effects on vultures [5]; comparative tox- tilled water on a stirring hot plate at 30ЊC. Dosing solutions icological aspects of nonsteroidal anti-inflammatory drugs are were prepared by addition of various quantities of this stock poorly known in birds [11,17–19]; and there is growing con- into distilled water in volumetric flasks. Nominal concentra- cern for the ecotoxicological effects of veterinary pharmaceu- tions ranged from 0.16 to 25 mg sodium diclofenac/ml, and ticals released from animal feed lot operations into streams were analytically verified (recovery averaged 104.9%; meth- and estuaries [20,21]. Finally, other currently used NSAIDs, ods described below). Solutions were administered in a volume including carprofen and flunixin, have been associated with of 0.5 ml/kg body weight, and nominal doses ranged from 0.08 mortality, gout, and/or renal failure in some scavenging birds to 12.5 mg/kg body weight. Due to limits of solubility, the outside of the Gyps genus [11], and thus their toxicity would greatest dose, 25 mg/kg body weight, was administered in also merit urgent investigation should diclofenac prove ex- twice the volume (1 ml/kg body wt). tremely toxic to New World vultures.
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