Abstract
In French wildlife rescue centers, veterinarians or volunteers often note embedded lead projectiles in X-rayed birds of prey that are not the cause of admission. To know if embedded lead in birds of prey may result in lead poisoning, 77 individuals admitted in three wildlife rescue centers in France were X-rayed and separated into two groups and then submitted to a blood lead level analysis. Blood lead levels of birds of prey with embedded lead projectiles are significantly higher (224.2 μg/L, 95% confidence interval 197.0–251.4 μg/L) than those without (142.9 μg/L, 95% confidence interval 124.1–161.7 μg/L). Among the birds of prey included in this study, the same difference was demonstrated in two species, the common buzzard and the common kestrel, when analyzed separately. Clinical lead poisoning was not observed but birds of prey with embedded lead have a mean blood level higher than the threshold of 200 μg/L defining the risk of subclinical effect occurrences and 60% of the lead-exposed birds had blood lead concentrations above the threshold. This result suggests that embedded lead projectile may release lead and induce some long-term detrimental effects.
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Battaglia A, Ghidini S, Campanini G, Spaggiari R (2005) Heavy metal contamination in little owl (Athene noctua) and common buzzard (Buteo buteo) from northern Italy. Ecotoxicol Environ Saf 60(1):61–66. https://doi.org/10.1016/j.ecoenv.2003.12.019
Berny P, Vilagines L, Cugnasse J-M, Mastain O, Chollet J-Y, Joncour G, Razin M (2015) VIGILANCE POISON: illegal poisoning and lead intoxication are the main factors affecting avian scavenger survival in the Pyrenees (France). Ecotoxicol Environ Saf 118(C):71–82. https://doi.org/10.1016/j.ecoenv.2015.04.003
Burger J (1995) A risk assessment for lead in birds. J Toxicol Environ Health 45(3):369–396. https://doi.org/10.1080/15287399509532003
Burger J, Gochfeld M (2005) Effects of lead on learning in herring gulls: an avian wildlife model for neurobehavioral deficits. Neurotoxicology 26(4):615–624. https://doi.org/10.1016/j.neuro.2005.01.005
Cruz-Martinez L, Redig PT, Deen J (2012) Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Human Wildlife Interact 6(1):94–104
Demartini J, Wilson A, Powell JS, Powell CS (2001) Lead arthopathy and systemic lead poisoning from an intra-articular bullet. Am J Roentgenol 176(5):1144–1145. https://doi.org/10.2214/ajr.176.5.1761144
Dumoulin M (2015) Etude bibliographique et statistique des entrées d’oiseaux dans les centres de soins français pour la cause “Tir”. Veterinary Thesis, Vetagro-sup, (online http://portaildoc-veto.vetagro-sup.fr/?q=node/119) consulted on December, 2016
Finkelstein ME, George D, Scherbinski S, Gwiazda R, Johnson M, Burnett J, Brandt J, Lawrey S, Pessier AP, Clark M, Wynne J, Grantham J, Smith DR (2010) Feather lead concentrations and 207Pb/ 206Pb ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environ Sci Technol 44(7):2639–2647. https://doi.org/10.1021/es903176w
Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131(3):421–432. https://doi.org/10.1016/j.biocon.2006.02.018
Franson JC (1996) Interpretation of tissue lead residues in birds other than waterfowl. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue concentrations. SETAC special publication series, USA, pp 265–279
Franson JC & Pain DJ (2011) Lead in birds. USGS available online http://digitalcommons.unl.edu/usgsstaffpub/974/ consulted in December 2016
Gameiro VS, de Araújo GCS, & Bruno FMM (2013) Lead intoxication and knee osteoarthritis after a gunshot: long-term follow-up case report. Case Reports, 2013(June 24 1), bcr2013009404–bcr2013009404. https://doi.org/10.1136/bcr-2013-009404
Garcia-Fernandez AJ, Martinez-Lopez E, Romero D, Maria-Mojica P, Godino A, Jimenez P (2005) High levels of blood lead in griffon vultures (Gyps fulvus) from Cazorla natural park (southern Spain). Environ Toxicol 20(4):459–463. https://doi.org/10.1002/tox.20132
Geroudet P (2013) Les rapaces d’Europe diurnes et nocturnes, 7th edn. Delachaux et Niesle Eds, Paris, 446p
Greenberg SR (1990) The histopathology of tissue lead retention. Histol Histopathol 5(4):451–456
Harmata A, Restani M (2013) Lead, mercury, selenium and other trace elements in tissues of golden eagles, southwestern Montana, USA. J Wildl Dis 49(1):114–124. https://doi.org/10.7589/2012-01-004
Hernández M, Margalida A (2009) Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 109(7):837–842. https://doi.org/10.1016/j.envres.2009.05.001
Hoffman DJ, Pattee OH, Wiemeyer SN, Mulhern B (1981) Effects of lead shot ingestion on ∂-aminolevulinic acid dehydratase activity, hemoglobinconcentration, and serum chemistry in Bald eagles. J Wildl Dis 17(3):423–431. https://doi.org/10.7589/0090-3558-17.3.423
Janssen D, Osterhuis JE, Allen JL, Anderson MP, Kelts DG, Wiemeyer SN (1986) Lead poisoning in free-ranging California condor. J Am Vet Med Assoc 189(9):1115–1117
Kelly TR, Johnson CK (2011) Lead exposure in free-flying Turkey vultures is associated with big game hunting in California. PLoS One 6(4):e15350. https://doi.org/10.1371/journal.pone.0015350
Krone O, Kenntner N, Trinogga A, Nadjafzadeh M, Scolz F, Sulawa J, Totschek K, Schuck-Wersig P, Zieschank R (2009) Lead poisoning in white-tailed sea eagles: causes and approaches to solutions in Germany. In: Watson RT, Fuller M, Pokpas M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, pp 289–301
LaDouceur EEB, Kagan R, Scanlan M, Viner T (2015) Chronically embedded lead projectiles in wildlife: a case series investigating the potential for lead toxicosis. J Zoo Wildl Med 46(2):438–442. https://doi.org/10.1638/2015-0026R.1
Lehner AF, Rumbeiha W, Shlosberg A, Stuart K, Johnson M, Domenech R, Langner H (2013) Diagnostic analysis of veterinary dried blood spots for toxic heavy metals exposure. J Anal Toxicol 37(7):406–422. https://doi.org/10.1093/jat/bkt048
Madry MM, Kraemer T, Kupper J, Naegeli H, Jenny H, Jenni L, Jenny D (2015) Excessive lead burden among golden eagles in the Swiss Alps. Environ Res Lett 10(3):1–9. https://doi.org/10.1088/1748-9326/10/3/034003
Mateo R, Estrada J, Paquet J-Y, Riera X, Domniguez L, Guitart R, Martinez-Vilalta A (1999) Lead shot ingestion by marsh harriers Circus aeruginosus from the Ebro delta, Spain. Environ Pollut 104(3):435–440. https://doi.org/10.1016/S0269-7491(98)00169-9
Moazeni M, Mohammad Alibeigi F, Sayadi M, Poorya Mofrad E, Kheiri S, Darvishi M (2014) The serum lead level in patients with retained lead pellets. Arch Trauma Res 3(2):1–4. https://doi.org/10.5812/atr.18950
Nguyen A, Schaider JJ, Manzanares M, Hanaki R, Rydman RJ, Bokhari F (2005) Elevation of blood lead levels in emergency department patients with extra-articular retained missiles. J Trauma 58(2):289–299. https://doi.org/10.1097/01.TA.0000119205.24520.1D
Nore T (2004) Buse variable Buteo buteo. In: Thiollay JM, Bretagnolle V (coord) Rapaces nicheurs de France Distribution, effectifs et conservation. Delachaux et Niestlé (Eds), Paris, pp 90–95
Pain D, Amiard-Triquet C, Bavoux C, Burneleau G, Eon L, Nicoalu-Guillaumet P (1993) Lead poisoning in wild populations of marsh harrier Circus aeruginosus in the Camargue and Charente-Maritime. Ibis 135(4):379–386. https://doi.org/10.1111/j.1474-919X.1993.tb02109.x
Pain D, Bavous C, Burneleau G (1997) Seasonal blood lead concentrations in marsh harrier Circus aeruginosus from Charente-Maritime, France: relationship with the hunting season. Biol Conserv 121:603–610
Pain D, Carter I, Sainsbury A, Shore R, Eden P, Taggart M et al (2007) Lead contamination and associated disease in captive and reintroduced red kites Milvus milvus in England. Sci Total Environ 376(1–3):116–127. https://doi.org/10.1016/j.scitotenv.2007.01.062
Vaishya R, Vijay V, Singh H, & Agarwal AK (2016) Arthroscopic retrieval of bullet from knee. Apollo Med 1–2. https://doi.org/10.1016/j.apme.2016.03.004
Acknowledgements
The authors wish to thank the volunteers and staff of all bird rescue centers who participated in the study (in Isère, Aquitaine, and Vaucluse).
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Berny, P.J., Mas, E. & Vey, D. Embedded lead shots in birds of prey: the hidden threat. Eur J Wildl Res 63, 101 (2017). https://doi.org/10.1007/s10344-017-1160-z
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DOI: https://doi.org/10.1007/s10344-017-1160-z