Since the 1990s, the Gyps vulture populations of South Asia have collapsed by more than 99%. In 2003, scientists identified diclofenac, a non-steroidal anti-inflammatory drug (NSAID) used to treat livestock, as the leading cause behind this decline as vultures feeding on the carcasses of animals recently treated with the drug died within weeks of ingesting it. As a result of the evidence, India, Nepal and Pakistan banned the veterinary use of diclofenac in 2006 and Bangladesh followed in 2010. However, it seems that the drug residues are still present in the environment, as well as livestock and vulture carcasses.
Despite the proven adverse effects of diclofenac on vulture populations, some countries within the EU approved the use of the drug for veterinary purposes over the last ten years. In Spain, for example, home to approximately 90% of the European vulture population, the drug entered the market in 2013.
The VCF, together with other environmental groups, widely advocated for the ban of vet drug diclofenac in Europe. Following a thorough process, that included public consultation with several stakeholders, the EU has recognized that veterinary diclofenac indeed posed a risk to vultures, but considered that the current system of managing livestock in Europe would prevent the drug from entering the vulture food chain. Still, the EU asked its member states to develop further risk management measures such as regulations and veterinary controls to avoid the poisoning vultures.
Based on the findings of two recently published studies, in this research review, we will discuss the presence of NSAIDs in avian scavengers and carrion in Iberia as well as give an update on the availability of diclofenac and other NSAIDs and their impact on vultures in South Asia.
NSAIDs detected in Iberian avian scavengers and carrion after diclofenac registration for veterinary use in Spain
Following the registration and commercialization of diclofenac for veterinary use on livestock in Spain, the research team aimed to assess any related impacts on vulture and other avian scavenger populations. Furthermore, in addition to diclofenac, they evaluated the risk of exposure to nine other NSAIDs in avian scavengers across the Iberian Peninsula (Spain and Portugal).
To do so, they sampled 228 livestock carcasses from vulture feeding sites, notably, 156 pigs and 45 sheep. They also collected tissue samples of 389 avian scavenger carcasses, of which 344 were vulture species, which rely predominantly on carrion as a food resource (306 Griffon Vultures, 15 Cinereous Vultures, 11 Egyptian Vultures, 12 Bearded Vultures) and 45 other facultative scavengers. Samples were analyzed by liquid chromatography with mass spectrometry (LCMS).
According to results, seven livestock carcasses (3.07%) in Spain contained residues of the following NSAIDs: flunixin (1.75%), ketoprofen, diclofenac and meloxicam (0.44% each). These residues were only detected in sheep (4.44%) and pig (3.21%) carcasses.
Out of the avian scavenger carcasses analyzed, 14 (3.60%) had NSAID residues in kidney and liver, specifically flunixin (1.03%) and meloxicam (2.57%). Three dead Griffon Vultures may have died from Flunixin poisoning as it is associated with visceral gout and/or kidney damage.
Conclusions and Recommendations
Although diclofenac poisoning has not been recorded in Spain and Portugal so far, flunixin appears to pose an immediate and real risk. It is essential to manage carrion disposal better as well as properly label the risk associated with veterinary NSAIDs and other pharmaceuticals potentially toxic to avian scavengers to help mitigate the threat of harmful NSAIDs to avian scavengers.
The Vulture Conservation Foundation (VCF) will continue to monitor vulture carcasses to try to identify any eventual mortality due to veterinary diclofenac, which could then potentially lead to renewed calls for its ban. The VCF also considers that sufficient evidence now exists to look into the use and impacts of flunixin, and we will be discussing these findings with veterinary authorities
Furthermore, it is crucial that toxicological testing for exposure to poison baits, lead and NSAIDs is performed alongside a necropsy on allvulture carcasses found whenever possible. This would enable a continuous assessment of the scale and scope of these silent threats and help conservationists in the development and delivery of more accurate and targeted actions to protect vultures and other avian scavengers.
Trends in the availability of the vulture-toxic drug, diclofenac, and other NSAIDs in South Asia, as revealed by covert pharmacy surveys
The unintentional poisoning by the non-steroidal anti-inflammatory drug (NSAID) diclofenac caused the catastrophic declines of three Gyps vulture species in South Asia, leading them to be listed as ‘Critically Endangered’. In an attempt to protect vultures, in 2006, India, Nepal, Pakistan, followed by Bangladesh in 2010 banned its veterinary use in their countries but residues of diclofenac continued to be detected in cattle and vulture carcasses. Studies showed that meloxicam, another NSAID, is safe for vultures and was therefore promoted as a suitable alternative for treating livestock. Still, there was a need to investigate if diclofenac continued to be sold for veterinary use, whether the availability of meloxicam increased and which other NSAIDs were available.
From 2012 to 2018, a research team conducted surveys of pharmacies in India, Nepal and Bangladesh to investigate the availability and prevalence of NSAIDs for the treatment of livestock.
Results illustrated that the availability of diclofenac declined in all three countries, virtually disappearing from pharmacies in Nepal and Bangladesh. However, in India, diclofenac still accounted for 10–46% of all NSAIDs offered for sale for livestock treatment in 2017, which indicated weak enforcement of existing regulations and highlighted the continued threat this poses to vultures.
The availability of meloxicam, safe to vultures, increased in all countries and was the most common veterinary NSAID in Nepal (89.9% in 2017). Meloxicam was also the most widely available NSAID in India in 2017, but it accounted for only 32% of products offered for sale. On the other hand, meloxicam was less commonly available in Bangladesh compared to ketoprofen (toxic to vultures), amounting to 28% and 66% availability respectively in 2018. These results are even more worrying when taking into consideration the partial government ban on ketoprofen in 2016. Finally, the team recorded a total of 11 different NSAIDs, several of which are known or suspected to be toxic to vultures.
Conclusions and recommendations
In South Asia, the biggest threat to vultures continues to be the wide availability of diclofenac, despite its ban by several governments. It is urgent for stricter implementation and enforcement of these bans, especially in India. Similarly, the partial ban on ketoprofen in Bangladesh needs to be extended. The veterinary use of aceclofenac and nimesulide that are suspected to be toxic to vultures, which have growing market shares, should also be banned.
Out of the 11 different NSAIDs recorded in this study, only three have been tested for their toxicity to vultures, and so it is necessary to assess whether the rest are safe for vultures or not.
Currently, meloxicam is the only NSAID that has been established as vulture-safe. However, in this survey, up to half of the products of this drug also contained paracetamol, for which there is no information regarding its safety to vultures, hence, its toxicity also needs to be assessed.
Finally, new veterinary NSAIDs must be tested for toxicity to vultures before receiving government approval through the region.
Herrero-Villar, M., Velarde, R., Camarero, P., Taggart, M., Bandeira, V., & Fonseca, C. et al. (2020). NSAIDs detected in Iberian avian scavengers and carrion after diclofenac registration for veterinary use in Spain. Environmental Pollution, 266, 115157. https://doi.org/10.1016/j.envpol.2020.115157
Galligan, T., Mallord, J., Prakash, V., Bhusal, K., Sarowar Alam, A., & Anthony, F. et al. (2020). Trends in the availability of the vulture-toxic drug, diclofenac, and other NSAIDs in South Asia, as revealed by covert pharmacy surveys. Bird Conservation International, 1-17. https://doi.org/10.1017/s0959270920000477
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