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Trends in the availability of the vulture-toxic drug, diclofenac, and other NSAIDs in South Asia, as revealed by covert pharmacy surveys

  • TOBY H. GALLIGAN (a1) (a2), JOHN W. MALLORD (a1), VIBHU M. PRAKASH (a3), KRISHNA P. BHUSAL (a4), A. B. M. SAROWAR ALAM (a5), FERGUS M. ANTHONY (a3), RUCHI DAVE (a3), ALKA DUBE (a3), KARTIK SHASTRI (a3), YOGESH KUMAR (a3), NIKITA PRAKASH (a3), SACHIN RANADE (a3), ROHAN SHRINGARPURE (a3), DEVENDRA CHAPAGAIN (a4), ISHWARY P. CHAUDHARY (a4), ANKIT B. JOSHI (a4), KHADANANDA PAUDEL (a4), TARIK KABIR (a5), SAKIB AHMED (a5), KAZI Z. AZMIRI (a5), RICHARD J. CUTHBERT (a1) (a6), CHRISTOPHER G. R. BOWDEN (a7) and RHYS E. GREEN (a1) (a8)...

Summary

The catastrophic declines of three species of ‘Critically Endangered’ Gyps vultures in South Asia were caused by unintentional poisoning by the non-steroidal anti-inflammatory drug (NSAID) diclofenac. Despite a ban on its veterinary use in 2006 (India, Nepal, Pakistan) and 2010 (Bangladesh), residues of diclofenac have continued to be found in cattle carcasses and in dead wild vultures. Another NSAID, meloxicam, has been shown to be safe to vultures. From 2012 to 2018, we undertook covert surveys of pharmacies in India, Nepal and Bangladesh to investigate the availability and prevalence of NSAIDs for the treatment of livestock. The purpose of the study was to establish whether diclofenac continued to be sold for veterinary use, whether the availability of meloxicam had increased and to determine which other veterinary NSAIDs were available. The availability of diclofenac declined in all three countries, virtually disappearing from pharmacies in Nepal and Bangladesh, highlighting the advances made in these two countries to reduce this threat to vultures. In India, diclofenac still accounted for 10–46% of all NSAIDs offered for sale for livestock treatment in 2017, suggesting weak enforcement of existing regulations and a continued high risk to vultures. Availability of meloxicam increased in all countries and was the most common veterinary NSAID in Nepal (89.9% in 2017). Although the most widely available NSAID in India in 2017, meloxicam accounted for only 32% of products offered for sale. In Bangladesh, meloxicam was less commonly available than the vulture-toxic NSAID ketoprofen (28% and 66%, respectively, in 2018), despite the partial government ban on ketoprofen in 2016. Eleven different NSAIDs were recorded, several of which are known or suspected to be toxic to vultures. Conservation priorities should include awareness raising, stricter implementation of current bans, bans on other vulture-toxic veterinary NSAIDs, especially aceclofenac and nimesulide, and safety-testing of other NSAIDs on Gyps vultures to identify safe and toxic drugs.

Copyright

Corresponding author

*Author for correspondence; email: john.mallord@rspb.org.uk

References

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Anon (2012) Regional Declaration on the Conservation of South Asia’s Critically Endangered Vulture Species. Governments of Bangladesh, India, Nepal and Pakistan, Delhi, May 2012.
Chaudhry, J. M. I., Ogada, D. L., Malik, R. N., Virani, M. Z. and Giovanni, M. D. (2012) First evidence that populations of the critically endangered Long-billed Vulture Gyps indicus in Pakistan have increased following the ban of the toxic veterinary drug diclofenac in South Asia. Bird Conserv. Internatn. 22: 389397.
Cuthbert, R. J., Dave, R., Chakraborty, S. S., Kumar, S., Prakash, S., Ranade, S. P. and Prakash, V. (2011) Assessing the ongoing threat from veterinary non-steroidal anti-inflammatory drugs to critically endangered Gyps vultures in India. Oryx 45: 420426.
Cuthbert, R. J., Taggart, M. A., Prakash, V., Chakraborty, S. S., Deori, P., Kulkarni, M., Ranade, S., Saini, M., Sharma, A.K, Shringarpure, R. and Green, R. E. (2014a) Avian scavengers and the threat from veterinary pharmaceuticals. Phil. Trans. Roy. Soc. B 20130574.
Cuthbert, R. J., Paudel, S., Chaudhary, A., Kaphle, K., Thapa, J., Subedi, T. R. and Taggart, M. A. (2014b) Aligning species conservation with animal welfare: formulation of vulture-safe meloxicam manufactured in South Asia and the reaction of goats to its administration. Sandy, Bedfordshire, UK: Royal Society for the Protection of Birds. (RSPB Research Report No. 52).
Cuthbert, R. J., Taggart, M. A., Saini, M., Sharma, A., Das, A., Kulkarni, M. D., Deori, P., Ranade, S., Shringarpure, R., Galligan, T. H. and Green, R. E. (2015) Continuing mortality of vultures in India associated with illegal veterinary use of diclofenac and a potential threat from nimesulide. Oryx 50: 104112.
Cuthbert, R. J., Taggart, M. A., Mohini, S., Sharma, A., Das, A., Kulkarni, M. D., Deori, P., Ranade, S., Shringarpure, R. N., Galligan, T. H. and Green, R. E. (2016) Continuing mortality of vultures in India associated with illegal veterinary use of diclofenac and a potential threat from nimesulide. Oryx 50: 104112.
Eleni, C., Neri, B., Giannetti, L., Grifoni, G., Meoli, R., Stravino, F., Friedrich, K. G., Scholl, F., Di Cerbo, P. and Battisti, A. (2019) Death of captive-bred vultures caused by flunixin poisoning in Italy. Environ. Toxicol. Pharm. 68: 9193.
Galligan, T. H., Taggart, M. A., Cuthbert, R. J., Svobodova, D., Chipangura, J., Alderson, D., Prakash, V. M. and Naidoo, V. (2016) Metabolism of aceclofenac in cattle to vulture-killing diclofenac. Conserv. Biol. 30: 11221127.
Galligan, T. H., Bhusal, K. P., Paudel, K., Chapagain, D., Joshi, A. B., Chaudhary, I. P., Chaudhary, A., Baral, H. M., Cuthbert, R. J. and Green, R. E. (2019) Partial recovery of Critically Endangered Gyps vulture populations in Nepal. Bird Conserv. Internatn. doi:10.1017/S0959270919000169.
Green, R. E., Newton, I., Shultz, S., Cunningham, A. A., Gilbert, G., Pain, D. J. and Prakash, V. (2004) Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. J. Appl. Ecol. 41: 793800.
Green, R. E., Taggart, M. A., Senacha, K. R., Raghavan, B., Pain, D. J., Jhala, Y. and Cuthbert, R. (2007) Rate of decline of the Oriental White-Backed Vulture population in India estimated from a survey of diclofenac residues in carcasses of ungulates. PloS ONE 2: e686.
Herrero-Villar, M., Velarde, R., Camarero, P. R., Taggart, M. A., Bandeira, V., Fonseca, C., Marco, I. and Mateo, R. In press. NSAIDs detected in Iberian avian scavengers and carrion after diclofenac registration for veterinary use in SpainEnviron. Pollut.
Naidoo, V., Wolter, K., Cromarty, D., Diekman, M., Duncan, N., Meharg, A. A., Taggart, M. A., Venter, L. and Cuthbert, R. (2010) Toxicity of non-steroidal anti-inflammatory drugs to Gyps vultures: a new threat from ketoprofen. Biol. Lett. 6: 339341.
Naidoo, V., Taggart, M. A., Duncan, N., Wolter, K., Chipangura, J., Green, R. E. and Galligan, T. H. (2018) The use of toxicokinetics and exposure studies to show that carprofen in cattle tissue could lead to secondary toxicity and death in wild vultures. Chemosphere 190: 8089.
Oaks, J. L., Gilbert, M., Virani, M. Z., Watson, R. T., Meteyer, C. U., Rideout, B. A., Shivaprasad, H. L., Ahmed, S., Chaudhry, M. J. I., Arshad, M., Mahmood, S., Ali, A. and Khan, A. A. (2004) Diclofenac residues as the cause of population decline of vultures in Pakistan. Nature 427: 630633.
Prakash, V., Green, R. E., Pain, D. J. , Ranade, S. P., Saravanan, S., Prakash, N., Venkitachalam, R., Cuthbert, R., Rahmani, A. R. and Cunningham, A. A. (2007) Recent changes in populations of resident Gyps vultures in India. J. Bombay Nat. Hist. Soc. 104: 129135.
Prakash, V., Galligan, T. H., Chakraborty, S. S., Dave, R., Kulkarni, M. D., Prakash, N., Shringarpure, R. N., Ranade, S. P. and Green, R. E. (2017) Recent changes in populations of Critically Endangered Gyps vultures in India. Bird Conserv. Internatn. 29: 5570.
SAVE (2016) NSAID Alerts. https://save-vultures.org/alerts/ Downloaded on 20 December 2017.
Sharma, P. (2012) Aceclofenac as a potential threat to critically endangered vultures in India: A review. J. Raptor Res. 46: 314318.
Shultz, S., Baral, H. S., Charman, S., Cunningham, A. A., Das, D., Ghalsasi, G. R., Goudar, M. S., Green, R. E., Jones, A., Nighot, P., Pain, D. J. and Prakash, V. (2004) Diclofenac poisoning is widespread in declining vulture populations across the Indian subcontinent. Proc. Roy. Soc. Lond. B (Supplement) 271: S458S460.
Spicker, P. (2011) Ethical covert research. Sociology 45: 118133.
Swan, G. E., Cuthbert, R., Quevedo, M., Green, R. E., Pain, D. J. , Bartels., P., Cunningham, A. A., Duncan, N., Meharg, A. A., Oaks., L., Jones, J. M., Shultz, S., Taggart, M. A., Verdoorn, G. and Wolter, K. (2006a) Toxicity of diclofenac to Gyps vultures. Biol. Lett. 2: 279282.
Swan, G., Naidoo, V., Cuthbert, R., Green, R. E., Pain, D. J. , Swarup, D., Prakash, V., Taggart, M., Bekker, L., Das, D., Diekmann, J., Diekmann, M., Killian, E., Meharg, A., Patra, R. C., Saini, M. and Wolter, K. (2006b) Removing the threat of diclofenac to Critically Endangered Asian Vultures. PLoS Biol. 4: 396402.
Swarup, D., Patra, R. C., Prakash, V., Cuthbert, R., Das, D., Avari, D. J., Pain, D. J. , Green, R. E., Sharma, A. K., Saini, M., Das, D. and Taggart, M. (2007) Safety of meloxicam to critically endangered Gyps vultures and other scavenging birds in India. Anim. Conserv. 10: 192198.
Taggart M, A., Senacha K, R., Green R, E., Cuthbert, R., Jhala Y, V., Meharg A, A., Mateo, R. and Pain D, J. (2009) Analysis of nine NSAIDs in ungulate tissues available to Critically Endangered Vultures in India. Environ. Sci. Technol. 43: 45614566.
Zorrilla, I., Martinez, R., Taggart, M. A. and Richards, N. (2014) Suspected flunixin poisoning of a wild Eurasian griffon vulture from Spain. Conserv. Biol. 29: 587592.

Keywords

Trends in the availability of the vulture-toxic drug, diclofenac, and other NSAIDs in South Asia, as revealed by covert pharmacy surveys

  • TOBY H. GALLIGAN (a1) (a2), JOHN W. MALLORD (a1), VIBHU M. PRAKASH (a3), KRISHNA P. BHUSAL (a4), A. B. M. SAROWAR ALAM (a5), FERGUS M. ANTHONY (a3), RUCHI DAVE (a3), ALKA DUBE (a3), KARTIK SHASTRI (a3), YOGESH KUMAR (a3), NIKITA PRAKASH (a3), SACHIN RANADE (a3), ROHAN SHRINGARPURE (a3), DEVENDRA CHAPAGAIN (a4), ISHWARY P. CHAUDHARY (a4), ANKIT B. JOSHI (a4), KHADANANDA PAUDEL (a4), TARIK KABIR (a5), SAKIB AHMED (a5), KAZI Z. AZMIRI (a5), RICHARD J. CUTHBERT (a1) (a6), CHRISTOPHER G. R. BOWDEN (a7) and RHYS E. GREEN (a1) (a8)...

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