First diclofenac intoxication in a wild avian scavenger in Europe

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Highlights

  • First case of diclofenac poisoning in a European vulture

  • Diclofenac intoxication has been detected for the first time in cinereous vulture.

  • The fledgling presented extended visceral gout and no signs of other pathologies.

  • Diclofenac concentrations were 26.5 ng/g in liver and 51.4 ng/g in kidney.

  • This evidences the need of close vigilance and stronger regulation on diclofenac.

Abstract

Diclofenac is a non-steroidal anti-inflammatory drug (NSAID) with a well-known toxicity for old world vultures that ingest the carrion of domestic animals treated with it. Diclofenac intoxication was directly related to the dramatic declines in the populations of three native South Asian Gyps vulture species two decades ago. In 2013, this NSAID was authorised for veterinary use in Spain, which has the largest vulture populations in Europe. One of these species is the cinereous vulture (Aegypius monachus), which is classified as “near threatened” by the International Union for Conservation of Nature (IUCN). This species has been reintroduced and monitored in Catalonia (NE Spain) since 2007, and in 2020 its current population consisted of 15 breeding pairs and a total number of 61 individuals. In September 2020, one fledgling was found dead in the nest. Post-mortem examination revealed severe generalised visceral and articular gout, which was confirmed histologically. Diclofenac was detected at average concentrations of 26.5 ng/g in the liver and 51.4 ng/g in kidney replicates (n = 3), respectively. These findings support a diagnosis of fatal gout caused by diclofenac intoxication. This is the first case of diclofenac poisoning in Spain (and in Europe), in addition to being the first report of diclofenac poisoning in cinereous vultures. This case report, therefore, supports the need to closely monitor vulture populations and carry out strict regulatory measures with which to prevent these poisonings.

Introduction

It is already well known that Asian vulture populations declined markedly between 1990 and 2000 owing to intoxication with a veterinary pharmaceutical, specifically diclofenac (Prakash et al., 2003; Oaks et al., 2004). Adult mortality was reported in the main Gyps vulture species distributed throughout South Asia: the white-rumped vulture (Gyps bengalensis), the Indian vulture (Gyps indicus) and the slender-billed vulture (Gyps tenuirostris) (Prakash et al., 2003; Gilbert et al., 2006; Prakash et al., 2012). Affected vultures were in good body condition, but exhibited severe visceral gout (Oaks et al., 2004). This lesion, together with diclofenac concentrations detected in the kidneys of vultures found dead in the field, were consistent with a diagnosis of diclofenac intoxication (Oaks and Watson, 2011). Concentrations found in the kidneys of these affected vultures ranged between 51 and 643 ng/g wet weight (ww). Toxicity thresholds were confirmed after the realisation of experimental studies, which estimated a lethal dose (LD50) in the range of 98–225 ng/g body weight (bw) in white-rumped vultures (Oaks et al., 2004; Swan et al., 2006). Moreover, in studies performed in South Asia, 11.1–13.9% of the livestock carcasses evaluated contained diclofenac residues, with levels ranging between 10 and 10,100 ng/g ww in liver (Taggart et al., 2007a, Taggart et al., 2007b, Taggart et al., 2009). These residue levels posed a significant risk to vultures, because carrion containing 7–940 ng/g of diclofenac can be lethal to vultures consuming it (Oaks et al., 2004; Swan et al., 2006). As estimated by Green et al. (2004), the presence of lethal levels of diclofenac in 0.13–0.75% of livestock carcasses would be sufficient to explain the rapid declines in vulture populations observed in South Asia. Diclofenac was consequently identified as the principal cause of declines in vulture populations and was, therefore, banned in India, Pakistan and Nepal in 2006, and in Bangladesh in 2010 (Chaudhry et al., 2012; Prakash et al., 2012; Khan, 2013; Cuthbert et al., 2016). Diclofenac continues to be detected in carrion at lethal levels, but its prevalence has decreased by approximately 50% in India (Cuthbert et al., 2011a, Cuthbert et al., 2011b). Even though, availability trends of diclofenac for veterinary use in India remain variable between states, with declines in some states and little change and persistent high levels in other states (Galligan et al., 2020). In contrast, a clear reduction of the availability has been observed in Nepal (Galligan et al., 2019). As consequence, there is a notable recovery in vulture populations in Nepal since 2012 (Galligan et al., 2019), in contrast to the slow recovery in India (Prakash et al., 2019).

Diclofenac has, however, been authorised for veterinary use in Africa and Europe. In Spain, it was authorised in 2013, despite being the European country with the largest vulture populations (Margalida et al., 2014b). The presence of NSAIDs in carrion at supplementary feeding stations has recently been studied in Spain, and one pig carcass containing 171 ng/g of diclofenac was detected out of the 156 pig carcasses analysed (Herrero-Villar et al., 2020). Unlike flunixin, diclofenac poisoning had not yet been detected in vultures in Spain (Zorrilla et al., 2015; Herrero-Villar et al., 2020). However, when using the observed occurrence of pig carcasses with diclofenac residues (0.64%) as a basis, the annual mortality in griffon vultures (Gyps fulvus; the most abundant species) was estimated to range between 78 and 600 individuals (Herrero-Villar et al., 2020). These estimates were between those calculated by the Spanish Agency of Medicines and the Ministry of Agriculture and Environment with the theoretical occurrence values (AEMPS and MAGRAMA, 2014; 4–7 vultures), and those of Green et al. (2016; 364–4609 vultures). Despite the significant differences among these mortality estimations, all of them had already warned of the potential presence of diclofenac poisoning events in vultures in Spain.

The case presented herein confirms the first diclofenac intoxication reported in a wild avian scavenger in Europe. It is also the first time that diclofenac intoxication has been described in a cinereous vulture (Aegypius monachus). These results provide evidence that diclofenac has reached the avian scavengers' food web, which may have dramatic consequences for vulture populations in Europe.

Section snippets

The reintroduction of the cinereous vulture into NE Spain

Cinereous vulture populations in Spain have undergone a continuous decline over the last century, although they are currently increasing as a result of the conservation measures applied, such as the establishment of a network of supplementary feeding stations and specific conservation plans. One of these conservation plans is the “Proyecto Monachus”, a reintroduction plan for this species led by Autochthonous Wildlife and its Habitat Rehabilitation Group (GREFA). The data obtained revealed the

Identifying the possible site and time of diclofenac exposure

The information obtained by the GPS positions during the last five days of the fledgling's life showed that it had, on September 21st, visited a cliff 6 km away from the nest where no evidence of feeding (e. g. carcass remains) was found (Fig. 2A). On September 19th, 20th and 22nd, it had been flying around the nest and had visited some perches or cliffs, but no evidence of feeding was observed on these sites. The vulture also visited the supplementary feeding site on September 23rd between

Discussion

The main lesion found in the cinereous vulture fledging was that of visceral and articular gout, which are indicative of NSAID intoxication in vultures. The lesions found during post-mortem examination, together with the good corporal condition, formed an identical clinical picture to that described in Asian vultures intoxicated with diclofenac. Moreover, the histopathological findings indicated that the visceral gout was, in this case, caused by a toxicant, because no renal inflammatory

Conclusions and management recommendations

The results of this study confirm that there is a risk of diclofenac intoxication for vultures in Spain. This is the first case of diclofenac reported in Spain, evidencing that the regulations imposed to avoid diclofenac intoxication in vultures are not, at least in some cases, being enforced. The labels of veterinary products containing diclofenac warn of the risk that the carrion of animals treated with diclofenac may pose for vultures. However, there may be failures in these product label

Funding

The programme to reintroduce the cinereous vulture into the Catalan pre-Pyrenees has been funded by “Obra Social la Caixa” (through a contract with the “Generalitat de Catalunya”), the “Red Eléctrica de España” and the “Fundación Biodiversidad” from the Spanish Ministry of Ecological Transition and Demographic Challenge (MITECO).

CRediT authorship contribution statement

Marta Herrero-Villar: Validation, Formal analysis, Investigation, Writing – original draft, Writing – review & editing. Émilie Delepoulle: Data curation, Investigation. Laura Suárez-Regalado: Investigation. Carlos Solano-Manrique: Investigation. Carles Juan-Sallés: Investigation, Methodology, Formal analysis, Writing – original draft. Juan J. Iglesias-Lebrija: Data curation. Pablo R. Camarero: Validation, Formal analysis. Fernando González: Supervision, Project administration, Funding

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors would like to thank the autonomous government of the “Generalitat de Catalunya” (Ministry of Agriculture, Livestock, Fisheries and Food, and Ministry of Territory and Sustainability) for its promotion of the reintroduction programme for the cinereous vulture in the Catalan pre-Pyrenees. Two non-governmental organisations (GREFA and TRENCA) are in charge of assessing and executing the project, together with staff members from the National Hunting Protected Area of Boumort. The

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