IN the 1990s and 2000s, a non-steroidal anti-inflammatory drug (NSAID) called diclofenac was widely used in veterinary palliative care for cattle. What was not known at the time was that the carcasses of cattle dosed on diclofenac would be fatal to the vultures that ate them. It was only in 2003 that scientists found that diclofenac is nephrotoxic to Gyps vultures, but by then a huge environmental disaster had already taken place.
More than 40 million vultures had died from ingesting cattle carcasses that contained diclofenac. There was a catastrophic slide in the population of the three Gyps vulture species endemic to the subcontinent: the white-rumped vulture (G. bengalensis), the Indian vulture (G. indicus) and the slender-billed (G. tenuirostris) vulture. The decline was estimated to be 99.9 per cent of the population. Pushed to the brink of extinction, the birds were classified as “Critically Endangered” on the Red List of the International Union for Conservation of Nature (IUCN).
To save the birds, India, Nepal and Pakistan banned the manufacture of veterinary formulations of diclofenac in 2006. Bangladesh banned it in 2010. But the birds showed no significant signs of recovery. This was because diclofenac was still in use.
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An undercover investigation led by a group of researchers from many Indian and international environmental organisations and universities—including the Royal Society for the Protection of Birds (RSPB) Centre for Conservation Science, Sandy, England; the Bombay Natural History Society (BNHS), Mumbai; Bird Conservation Nepal, Kathmandu; IUCN Bangladesh Country Office, Dhaka; and the Conservation Science Group, Department of Zoology, University of Cambridge, England—found that cattle carcasses across India continued to have high levels of diclofenac and the same was found in dead vultures. The team set out to find which NSAIDs were being sold for veterinary use. From 2012 to 2017, members of the research team visited pharmacies pretending they needed drugs to treat their injured cows and bought the first drug that was offered. Their findings have been published in the journal Bird Conservation International.
The authors wrote: “In this study, we undertook covert (undercover) surveys of pharmacies selling veterinary drugs in India, Nepal, and Bangladesh to determine which NSAIDs are being sold for use in cattle.” Dr John Mallord, senior conservation scientist for the RSPB and the lead author of the study, said: “As the sale of diclofenac for veterinary use is illegal, if we were open about the reasons for the survey, and that we were vulture conservationists, pharmacists would be unlikely to offer us diclofenac. We had to pretend to be livestock owners so we could get an unbiased picture of its availability.”
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The team was at pains to explain the covert operation: “Covert interactions and deceit are important tools for data collection in conservation science, particularly when investigating illegal behaviour.
“Both are justified because obtaining accurate data would otherwise not be possible. Further, illegal behaviour is a concern of the public, and public rights take priority over individual rights in such circumstances (Spicker 2011). In this case, the conservation of vultures and the ecosystem services that they provide are concerns of the public, and the sale of diclofenac and the killing of vultures in Bangladesh, India and Nepal are crimes and thereby concerns of the public.
“The aims of the study were to assess (1) how effective the ban on veterinary diclofenac has been, (2) whether the only known vulture-safe drug, meloxicam, has taken over from diclofenac as a preferred drug, and (3) what other NSAIDs are currently available.”
Trends in sales of NSAIDs
That diclofenac was still available for veterinary use was proved beyond question. On the findings of the study, Chris Bowden of the RSPB and programme manager of the Saving Asia’s Vultures from Extinction consortium said: “In India, trends in sales of different NSAIDs varied between the different regions surveyed. In the first year [of the study, 2012], diclofenac was still the most commonly offered NSAID. Whilst sales of diclofenac declined in some States, elsewhere there were actually increases. In the five Indian States surveyed in the final year, 2017, diclofenac was still being offered by 10 to 46 per cent of pharmacists.”
The report pointed out that a 2011 study “surveyed pharmacies selling veterinary drugs in India and found that many were stocking and selling human formulations of diclofenac for illegal use in cattle. This misuse was made more practical by the manufacture and distribution to veterinary pharmacies, by some Indian pharmaceutical companies, of human formulations of diclofenac in large vials containing enough of the drug to dose cattle. This explained why many cattle carcasses were still found with diclofenac residues (Cuthbert et al. 2014a), dead vultures were still found with diclofenac residues and visceral gout (Cuthbert et al. 2015), and vulture populations had not recovered strongly (Prakash et al. 2017). The prevalence of diclofenac in cattle carcasses before and after bans in Bangladesh, Nepal and Pakistan was not measured.
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“However, population surveys of vultures in Nepal and Pakistan have shown a reversal of declines since the bans on veterinary diclofenac (Chaudhry et al. 2012, Galligan et al. 2019). In 2015, the Government of India strengthened its regulations on diclofenac by banning the manufacture of human formulations in vials larger than a single human dose (3 ml). Two Indian pharmaceutical companies immediately challenged the ban, but it was upheld in the High Court of Madras in 2017…. Given the influence of India’s pharmaceutical industry in the region and the far-ranging movements of vultures, this enhancement of the ban is expected to have a positive effect on vultures in neighbouring countries as well.”
The study also acknowledged some positive findings. Sales of diclofenac declined in Bangladesh, India and Nepal over the course of the survey, although there were variations across regions. Diclofenac virtually disappeared from pharmacies in Nepal, with the vulture-safe NSAID meloxicam becoming the drug of choice for treating cattle there. In Bangladesh, the vulture-toxic drug ketoprofen was always more commonly sold than meloxicam, despite also being illegal and banned.
Comparing diclofenac use
Comparing the use of diclofenac in the three countries, the report noted: “In contrast to the situation in India, diclofenac virtually disappeared from pharmacies in both Nepal and Bangladesh. This may have been due to effective advocacy and education, as well as strong government support, especially in promoting meloxicam in Nepal. However, the fact that most diclofenac is manufactured by Indian companies may contribute significantly. The one Nepali company found to be manufacturing 30-ml vials of diclofenac for human use during the first ‘Human’ pharmacy survey voluntarily stopped after being asked to do so by conservationists.
“Diclofenac could still find its way into cattle via importation across the long, permeable borders with India, where it is more easily obtainable (K. Paudel, unpubl. data), although the rapid partial recovery of white-rumped vulture populations in Nepal since 2013 (Galligan et al. 2019) suggests that this is not happening on a large scale. Meanwhile, the recent strengthening of the ban in India will also reduce the risk of diclofenac imports and benefit vultures in Nepal and Bangladesh. Meloxicam is the only NSAID that has been shown through safety testing (Swan et al. 2006b; Swarup et al. 2007) to be non-toxic to Gyps vultures at doses they are likely to be exposed to in the wild. It has therefore been promoted to pharmacists and cattle-owners by conservationists across South Asia. Such advocacy has been particularly successful in Nepal. There are a number of other NSAIDs in use and many have been found to be toxic to vultures.”
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Dr Vibhu Prakash, deputy director of the BNHS, said: “Although diclofenac, which is the most toxic drug to vultures, has been the main focus of our advocacy work, our study recorded eleven different NSAIDs, of which five are already known to be toxic to vultures. Where there is robust scientific evidence that drugs are toxic to vultures, governments within vulture range countries should implement bans on their veterinary use. This will require extensive safety testing of a range of drugs… [to] discover further vulture-safe NSAIDs, which will give farmers and veterinarians a choice, in addition to meloxicam.”
Bowden summed up by saying: “The importance of these results is emphasised by the most recent published nationwide population surveys of vultures in India and Nepal. In Nepal there is evidence that vulture populations have begun to recover, but in India they either continue to decline or, at best, are stable but at low levels and not yet showing signs of a recovery.” The Indian government needs to step in and ensure that one of Asia’s most iconic bird species does not die out because of poor implementation of the law.