Lead toxicosis of captive vultures: case description and responses to chelation therapy

BMC Veterinary Research

Rene Kizek³  Frantisek Treml¹  Jakub Sobotka⁴  Hana Skochova⁵  Jana Sedlackova⁵  Miroslav Pohanka⁴  Jitka Osickova⁵  Karel Ondracek⁵  Jiri Kral⁵  Miroslava Beklova⁵  Vojtech Adam³  Ivana Bednarova⁵  Hana Bandouchova⁵  Pavlina Hajkova²  Jiri Pikula⁵ 

[1] Department of Infectious Diseases and Microbiology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic;Avian Veterinary Clinic Skrivany, Cesky Brod, Czech Republic;Department of Chemistry and Biochemistry, Mendel University, Brno, Czech Republic;Centre of Advanced Studies, Faculty of Military Health Sciences, University of Defence, Hradec Kralove, Czech Republic;Department of Veterinary Ecology and Environmental Protection, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

关键词: Treatment;    Reproduction impairment;    Oxidative stress;    Biochemistry;    Haematology;    Plumbism;    Neophron percnopterus;    Aegypius monachus;   

Others  :  1119627
DOI  :  10.1186/1746-6148-9-11

 received in 2012-08-06, accepted in 2013-01-09,  发布年份 2013

【 摘 要 】

Background

Lead, a serious threat for raptors, can hamper the success of their conservation. This study reports on experience with accidental lead intoxication and responses to chelation therapy in captive Cinereous (Aegypius monachus) and Egyptian (Neophron percnopterus) Vultures.

Results

Soil contamination by lead-based paint sanded off the steel aviary resulted in poisoning of eight Cinereous and two Egyptian Vultures. A male Egyptian Vulture developed signs of apathy, polydipsia, polyuria, regurgitation, and stupor, and died on the next day. Liver, kidney and blood lead concentrations were 12.2, 8.16 and 2.66 μg/g, respectively. Laboratory analyses confirmed severe liver and kidney damage and anaemia. Blood Pb levels of Pb-exposed Cinereous Vultures were 1.571 ± 0.510 μg/g shortly after intoxication, decreased to 0.530 ± 0.165 μg/g without any therapy in a month and to 0.254 ± 0.097 μg/g one month after CaNa₂EDTA administration. Eight months later, blood lead levels decreased to close to the background of the control group. Blood parameters of healthy Pb-non-exposed Cinereous Vultures were compared with those of the exposed group prior to and after chelation therapy. Iron levels in the lead-exposed pre-treatment birds significantly decreased after chelation. Haematocrit levels in Pb-exposed birds were significantly lower than those of the controls and improved one month after chelation. Creatine kinase was higher in pre-treatment birds than in the controls but normalised after therapy. Alkaline phosphatase increased after chelation. A marked increase in the level of lipid peroxidation measured as thiobarbituric acid reactive species was demonstrated in birds both prior to and after chelation. The ferric reducing antioxidant power was significantly lower in pre-treatment vultures and returned to normal following chelation therapy. Blood metallothionein levels in lead-exposed birds were higher than in controls. Reduced glutathione dropped after CaNa₂EDTA therapy, while oxidised glutathione was significantly lower in both pre- and post-treatment birds. A chick in an egg produced by a Cinereous Vulture female two months after lead toxicosis died on day 40 of artificial incubation. Lead concentrations in foetal tissues were consistent with levels causing avian mortality.

Conclusions

The reported blood parameters and reproduction impairment in captive birds may have implications for professionals dealing with lead exposure in wild birds.

【 授权许可】

   
2013 Pikula et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Samour J: Toxicology. In Avian Medicine. 2nd edition. Edited by Samour J. Edinburgh: Mosby Elsevier; 2008:269-281.
• [2]Fisher IJ, Pain DJ, Thomas VG: A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 2006, 131(3):421-432.
• [3]Mateo R, Taggart MA, Green AJ, Cristofol C, Ramis A, Lefranc H, Figuerola J, Meharg AA: Altered porphyrin excretion and histopathology of greylag geese (Anser anser) exposed to soil contaminated with lead and arsenic in the Guadalquivir Marshes, southwestern Spain. Environ Toxicol Chem 2006, 25(1):203-212.
• [4]Blus LJ: A review of lead poisoning in swans. Comp Biochem Physiol 1994, 108:259-267.
• [5]Degernes L, Heilman S, Trogdon M, Jordan M, Davison M, Kraege D, et al.: Epidemiologic investigation of lead poisoning in trumpeter and tundra swans in Washington state, USA, 2000–2002. J Wildlife Dis 2006, 42:345-358.
• [6]Meharg AA, Osborn D, Pain DJ, Sánchez A, Naveso MA: Contamination of Donana food-chains after the Aznacóllar mine disaster. Environ Pollut 1999, 105(3):387-390.
• [7]Mateo R, Cadenas R, Mánez M, Guitart R: Lead shot ingestion in two raptor species from Donana, Spain. Ecotox Environ Safe 2001, 48(1):6-10.
• [8]Pain DJ, Carter I, Sainsbury AW, Shore RF, Eden P, Taggart MA, Konstantinos S, Walker LA, Meharg AA, Raab A: Lead contamination and associated disease in captive and reintroduced red kites (Milvus milvus) in England. Sci Total Environ 2007, 376(1–3):116-127.
• [9]Gangoso L, Alvarez-Lloret P, Rodriguez-Navarro AAB, Mateo R, Hiraldo F, Donazar JA: Long-term effects of lead poisoning on bone mineralisation in vultures exposed to ammunition sources. Environ Pollut 2009, 157(2):569-574.
• [10]Helander B, Axelsson J, Borg H, Holm K, Bignert A: Ingestion of lead from ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden. Sci Total Environ 2009, 407(21):5555-5563.
• [11]Hernandez M, Margalida A: Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 2009, 109(7):837-842.
• [12]Kramer JL, Redig PT: Sixteen years of lead poisoning in eagles, 1980-95: an epizootiologic view. J Raptor Res 1997, 31(4):327-332.
• [13]Muller K, Altenkamp R, Brunnberg L: Morbidity of free-ranging white-tailed sea eagles (Haliaeetus albicilla) in Germany. J Avian Med Surg 2007, 21(4):265-274.
• [14]Nam D-H, Lee D-P: Abnormal lead exposure in globally threatened Cinereous vultures (Aegypius monachus) wintering in South Korea. Ecotoxicology 2009, 18(2):225-229.
• [15]Dauwe T, Janssens E, Kempenaers B, Eens M: The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit (Parus caeruleus) eggs. Environ Pollut 2004, 129(1):125-129.
• [16]Nam D-H, Lee D-P: Reproductive effects of heavy metal accumulation on breeding feral pigeons (Columba livia). Sci Total Environ 2006, 366(2–3):682-687.
• [17]Finkelstein ME, George D, Scherbinski S, Gwiazda R, Johnson M, Burnett J, Brandt J, Lawrey S, Pessier AP, Clark M, et al.: Feather lead concentrations and Pb-207/Pb-206 ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environ Sci Technol 2010, 44(7):2639-2647.
• [18]Burger J: Heavy metals in avian eggshells: Another excretion method. J Toxicol Environ Health 1994, 41(2):207-220.
• [19]Skocovska B, Hilscherova K, Babica P, Adamovsky O, Bandouchova H, Horakova J, Knotkova Z, Marsalek B, Paskova V, Pikula J: Effects of cyanobacterial biomass on the Japanese quail. Toxicon 2007, 49(6):793-803.
• [20]Pikula J, Bandouchova H, Hilscherova K, Paskova V, Sedlackova J, Adamovsky O, Knotkova Z, Lany P, Machat J, Marsalek B, Novotny L, Pohanka M, Vitula F: Combined exposure to cyanobacterial biomass, lead and the Newcastle virus enhances avian toxicity. Sci Total Environ 2010, 408(21):4984-4992.
• [21]Paskova V, Adamovsky O, Pikula J, Skocovska B, Band’ouchova H, Horakova J, Babica P, Marsalek B, Hilcherova K: Detoxification and oxidative stress responses along with microcystins accumulation in Japanese quail exposed to cyanobacterial biomass. Sci Total Environ 2008, 398(1-3):34-47.
• [22]Paskova V, Paskerova H, Pikula J, Bandouchova H, Sedlackova J, Hilscherova K: Combined exposure of Japanese quails to cyanotoxins, Newcastle virus and lead: Oxidative stress responses. Ecotox Environ Safe 2011, 74(7):2082-2090.
• [23]Benzie IFF, Strain JJ: The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal Biochem 1996, 239(1):70-76.
• [24]Pohanka M, Bandouchova H, Sobotka J, Sedlackova J, Soukupova I, Pikula J: Ferric reducing antioxidant power and square wave voltammetry for assay of low molecular weight antioxidants in blood plasma: Performance and comparison of methods. Sensors 2009, 9(11):9094-9103.
• [25]Vitula F, Peckova L, Bandouchova H, Pohanka M, Novotny L, Jira D, Kral J, Ondracek K, Osickova J, Zendulkova D, Rosenbergova K, Treml F, Pikula J: Mycoplasma gallisepticum infection in the grey partridge (Perdix perdix): outbreak description, histopathology, biochemistry and antioxidant parameters. BMC Vet Res 2011, 7(1):34. BioMed Central Full Text
• [26]Hynek D, Prasek J, Pikula J, Adam V, Hajkova P, Krejcova L, Trnkova L, Sochor J, Pohanka M, Hubalek J, Beklova M, Vrba R, Kizek R: Electrochemical analysis of lead toxicosis in vultures. Int J Electrochem Sc 2011, 6:5980-6010.
• [27]Hynek D, Krejcova L, Krizkova S, Ruttkay-Nedecky B, Pikula J, Adam V, Hajkova P, Trnkova L, Sochor J, Pohanka M, Hubalek J, Beklova M, Vrba R, Kizek R: Metallomics study of lead-protein interactions in albumen by electrochemical and electrophoretic methods. Int J Electrochem Sc 2012, 7:943-964.
• [28]Potesil D, Petrlova J, Adam V, Vacek J, Klejdus B, Zehnalek J, Trnkova L, Havel L, Kizek R: Simultaneous femtomole determination of cysteine, reduced and oxidized glutathione, and phytochelatin in maize (Zea mays L.) kernels using high-performance liquid chromatography with electrochemical detection. J Chromatogr A 2005, 1084:134-144.
• [29]Masarik M, Gumulec J, Hlavna M, Sztalmachova M, Babula P, Raudenska M, Pavkova-Goldbergova M, Cernei N, Sochor J, Zitka O, Ruttkay-Nedecky B, Krizkova S, Adam V, Kizek R: Monitoring of the prostate tumour cells redox state and real-time proliferation by novel biophysical techniques and fluorescent staining. Integr Biol 2012, 4(6):672-684.
• [30]Thompson LJ: Lead. In Veterinary toxicology. Basic and clinical principles. 1st edition. Edited by Gupta RC. New York: Academic; 2007:438-441.
• [31]Villegas A, Sanchez JM, Costillo E, Corbacho C: Blood chemistry and haematocrit of the black vulture (Aegypius monachus). Comp Biochem Physiol A-Mol Integr Physiol 2002, 132(2):489-497.
• [32]Bailey TA, Samour JH, Naldo J, Howlett JC: Lead toxicosis in captive houbara bustards (Chlamydotis undulata macqueenii). Vet Rec 1995, 137:193-194.
• [33]Martinez-Haro M, Green AJ, Mateo R: Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field. Environ Res 2011, 111(4):530-538.
• [34]Buekers J, Redeker ES, Smolders E: Lead toxicity to wildlife: Derivation of a critical blood concentration for wildlife monitoring based on literature data. Sci Total Environ 2009, 407(11):3431-3438.
• [35]Wernery R, Wernery U, Kinne J, Samour J: Colour Atlas of Falcon Medicine. Hannover: Schlütersche Verlagsgesellschaft mbH & Co. KG; 2004.
• [36]Chvapil M, Aronson AL, Peng YM: Relation between zinc and iron and peroxidation of lipids in liver homogenate in Ca-EDTA-treated rats. Exp Mol Pathol 1974, 20(2):216-227.
• [37]Kwong WT, Friello P, Semba RD: Interactions between iron deficiency and lead poisoning: epidemiology and pathogenesis. Sci Total Environ 2004, 330(1–3):21-37.
• [38]Braide VB: Calcium EDTA toxicity: Renal excretion of endogenous trace metals and the effect of repletion on collagen degradation in the rat. Gen Pharmacol 1984, 15(1):37-41.
• [39]Fair JM, Ricklefs RE: Physiological, growth, and immune responses of Japanese quail chicks to the multiple stressors of immunological challenge and lead shot. Arch Environ Contam Toxicol 2002, 42(1):77-87.
• [40]Mateo R, Beyer WN, Spann J, Hoffman D, Ramis A: Relationship between oxidative stress, pathology, and behavioural signs of lead poisoning in mallards. J Toxicol Env Heal A 2003, 66(14):1371-1389.
• [41]Fudge AM: Avian clinical pathology - haematology and chemistry. In Avian medicine and surgery. 1st edition. Edited by Altman RB, Clubb SL, Dorrestein GM, Quesenberry K. Philadelphia: W.B. Saunders Company; 1997:142-157.
• [42]Pikula J, Zukal J, Adam V, Bandouchova H, Beklova M, Hajkova P, Horakova J, Kizek R, Valentikova L: Heavy metals and metallothionein in vespertilionid bats foraging over aquatic habitats in the Czech Republic. Environ Toxicol Chem 2010, 29(3):501-506.
• [43]Fernandes D, Bebianno MJ, Porte C: Hepatic levels of metal and metallothioneins in two commercial fish species of the Northern Iberian shelf. Sci Total Environ 2008, 391:159-167.
• [44]Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS: Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquat Toxicol 2006, 76:160-202.
• [45]Vanparys C, Dauwe T, Van Campenhout K, Bervoets L, De Coen W, Blust R, Eens M: Metallothioneins (MTs) and d-aminolevulinic acid dehydratase (ALAd) as biomarkers of metal pollution in great tits (Parus major) along a pollution gradient. Sci Total Environ 2008, 401:184-193.
• [46]Trust KA, Miller MW, Ringelman JK, Orme IM: Effects of ingested lead on antibody production in mallards (Anas platyrhynchos). J Wildlife Dis 1990, 26:316-322.
• [47]Grasman KA: Assessing immunological function in toxicological studies of avian wildlife. Integr Comp Biol 2002, 42:34-42.
• [48]Sebastian MM: Role of pathology in diagnosis. In Veterinary toxicology. Basic and clinical principles. 1st edition. Edited by Gupta RC. New York: Academic; 2007:1100-1136.
• [49]Goyer RA, Mahaffey KR: Susceptibility to lead toxicity. Environ Health Perspect 1972, 2:73-80.
• [50]Ding WX, Ong CN: Role of oxidative stress and mitochondrial changes in cyanobacteria induced apoptosis and hepatotoxicity. FEMS Microbiol Lett 2003, 220:1-7.
• [51]Stohs SJ, Bagchi D: Oxidative mechanisms in the toxicity of metal ions. Free Radical Bio Med 1995, 18:321-336.
• [52]Costantini D, Moller AP: Does immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Physiol A-Mol Integr Physiol 2009, 153(3):339-344.
• [53]Finkelstein ME, Doak DF, George D, Burnett J, Brandt J, Church M, Grantham J, Smith DR: Lead poisoning and the deceptive recovery of the critically endangered California condor. P Natl Acad Sci USA 2012, 109(28):11449-11454.
• [54]Flora SJS, Pachauri V: Chelation in metal intoxication. Int J Environ Res Public Health 2010, 7:2745-2788.
• [55]Samour JH, Naldo J: Diagnosis and therapeutic management of lead toxicosis in falcons in Saudi Arabia. J Avian Med Surg 2002, 16(1):16-20.
• [56]Bauck L, LaBonde J: Toxic diseases. In Avian medicine and surgery. 1st edition. Edited by Altman RB, Clubb SL, Dorrestein GM, Quesenberry K. Philadelphia: W.B. Saunders Company; 1997:604-613.
• [57]Domingo JL: Developmental toxicity of metal chelating agents. Reprod Toxicol 1998, 12(5):499-510.
• [58]Cox CR, Goldsmith VI, Engelhardt HR: Pair Formation in California Condors. Amer Zool 1993, 33(2):126-138.
• [59]Kowalczyk DF: Clinical management of lead poisoning. J Am Vet Med Assoc 1984, 184(7):858-860.
• [60]Centers for Disease Control and Prevention: Managing Elevated Blood Lead Levels Among Young Children: Recommendations from the Advisory Committee on Childhood Lead Poisoning Prevention. Atlanta: CDC; 2002.
• [61]Fry DM: Reproductive effects in birds exposed to pesticides and industrial chemicals. Environ Health Perspect 1995, 103:165-171.
• [62]Damkova V, Sedlackova J, Bandouchova H, Peckova L, Vitula F, Hilscherova K, Paskova V, Kohoutek J, Pohanka M, Pikula J: Effects of cyanobacterial biomass on avian reproduction: a Japanese quail model. Neuroendocrinol Lett 2009, 30:205-210.
• [63]Damkova V, Paskova V, Sedlackova J, Bandouchova H, Hilscherova K, Novotny L, Peckova L, Vitula F, Pohanka M, Pikula J: Testicular toxicity of cyanobacterial biomass in Japanese quails. Harmful Algae 2011, 10(6):612-618.
• [64]Hargreaves AL, Whiteside DP, Gilchrist G: Concentrations of 17 elements, including mercury, and their relationship to fitness measures in arctic shorebirds and their eggs. Sci Total Environ 2010, 408(16):3153-3161.
• [65]Makatsch W: Die Eier der Vőgel Europas. Radebeul: Neumann Verlag; 1974. (In German)
• [66]BirdLife International IUCN Red List for birds 2012. http://www.birdlife.org webcite
• [67]Pattee OH, Carpenter JW, Fritts SH, Rattner BA, Wiemeyer SN, Royle JA, Smith MR: Lead poisoning in captive Andean condors (Vultur gryphus). J Wildlife Dis 2006, 42:772-779.