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The Use of Lead Isotope Analysis to Identify Potential Sources of Lead Toxicosis in a Juvenile Bald Eagle (Haliaeetus leucocephalus) With Ventricular Foreign Bodies.

Abstract: A male juvenile bald eagle (Haliaeetus leucocephalus) was admitted to the Wildlife Center of Virginia with a left humeral fracture a large quantity of anthropogenic debris in the ventriculus, a blood lead level of 0.616 ppm, and clinical signs consistent with chronic lead toxicosis. Because of the poor prognosis for recovery and release, the eagle was euthanatized. Lead isotope analysis was performed to identify potential anthropogenic sources of lead in this bird. The lead isotope ratios in the eagle's femur (0.8773), liver (0.8761), and kidneys (0.8686) were most closely related to lead paint (0.8925), leaded gasoline (0.8450), and zinc smelting (0.8240). The lead isotope ratios were dissimilar to lead ammunition (0.8179) and the anthropogenic debris in the ventriculus. This case report documents foreign body ingestion in a free-ranging bald eagle and demonstrates the clinical utility of lead isotope analysis to potentially identify or exclude anthropogenic sources of lead poisoning in wildlife patients.

Key words: lead, foreign body, isotope, avian, bald eagle, Haliaeetus leucocephalus

Clinical Report

A male juvenile (3- to 4-months old) bald eagle (Haliaeetus leucocephalus) was admitted to the Wildlife Center of Virginia after it was found on the ground unable to fly in York County, Virginia. On initial presentation, the bird was weak, depressed, and in poor body condition (estimated body condition score, 2/5) with a body weight of 2.46 kg (in-house weight range of healthy juvenile male bald eagles in Virginia, 2.8-3.75 kg). The bird was bradycardic (80 beats per minute; in-house reference range, 170-220 beats per minute), and a distal left humeral fracture was palpable, with subcutaneous emphysema surrounding the fracture. Results of radiographs revealed a long oblique, comminuted, distal diaphyseal to distal metaphyseal fracture of the left humerus with moderate displacement and a large butterfly fragment, as well as a linear metallic object and multiple soft tissue to mineral opacity foreign objects of varying sizes and shapes in the ventriculus (Fig 1). In-house blood tests showed a low normal packed cell volume (33% reference interval: 28.8-57.9%), (1) a low normal total protein (2.6 g/dL; reference interval: 2.4-5.1 g/dL), (1) and a moderately elevated blood lead (Pb) level (0.616 ppm [61.6 [micro]g/dL]; LeadCare II Blood Lead Test System, Magellan Diagnostics, North Billerica, MA, USA). Both the clinical presentation and the blood lead levels were consistent with chronic lead toxicosis. (2) The distal, comminuted, long oblique nature of the humeral fracture with a displaced butterfly fragment, along with the debilitated and juvenile status of the patient, carried a guarded prognosis for successful repair and recovery to release. Therefore, euthanasia was elected because of the severity of the fracture and evidence of clinical lead toxicosis.

Preliminary gross postmortem examination revealed a wide variety of anthropogenic debris in the ventriculus, including 2 rubber balloons, paper, multiple plastic particles, a thumbtack, and an aluminum soda can tab. The carcass was sent to the University of Minnesota Veterinary Diagnostic Laboratory for a full postmortem diagnostic investigation; results showed no additional gross or microscopic lesions. To determine the source of lead poisoning, the foreign ventricular contents along with samples of kidney, liver, and proximal femur were sent to the Michigan State University Diagnostic Center for Animal and Population Health (Lansing, MI, USA) for lead concentration and isotope analysis. In brief, tissues were digested in nitric acid and nebulized, and lead concentration was measured as parts per million (ppm) with a mass spectrometer. Lead isotopes were determined as counts per second by isotope ratio mass spectrometry. (3)

The eagle had elevated lead levels in the femur (26.787 ppm), liver (6.003 ppm), and kidney (7.591 ppm). Lead isotope results from the eagle's tissues and foreign ventricular contents were compared with published values (Table 1; Fig 2).3 4 The ratios of [sup.207]Pb/[sup.206]Pb in the eagle's bone (0.8773), liver (0.8761), and kidneys (0.8686) differed by greater than 2 standard errors from the mean isotope ratios reported for lead ammunition purchased in California (0.8179). (4) The values also differed from the mean isotope ratios reported in Virginia black vultures (Coragyps atratus; 0.8272), Virginia turkey vultures (Cathartes aura; 0.8268),3 and postrelease California condors (Gymnogyps californianus; 0.8284)(4) all of which were attributed to lead ammunition. A relatively wide range in lead isotope values have been reported for ammunition. (3,4) Ammunition is frequently made from recycled lead from multiple sources, resulting in variable lead isotope ratios. (5,6) Because of the wide range of reported isotope values, the results from this eagle do fall below the maximum value (0.8706) in the range reported for ammunition. (3,4) The isotope ratios in this eagle were most closely related to lead paint (0.8925), leaded gasoline (0.8450), and zinc smelting (0.8240). The isotope ratios of the ingested anthropogenic debris were dissimilar to the bone and tissue values, aside from the plastic zip tie (0.8547). The plastic zip tie contained a small amount of lead, at 0.225 ppm, compared with 1500-247 250 ppm in lead paint chips and so was unlikely to have significantly contributed to the lead burden in this bird. (7)

Discussion

This case report describes the clinical use of lead isotope analysis to ascertain possible anthropogenic sources of lead toxicosis in a hatch-year bald eagle that ingested a significant amount of anthropogenic debris.

In the mid-20th century, the bald eagle population plummeted because of negative reproductive effects from dichlorodiphenyltrichloroethane (DDT). (8) In 1972, the US Environmental Protection Agency (EPA) issued a cancellation order for DDT based on its adverse environmental effects on wildlife, as well as its potential risks to human health (Bridge Document 11.1, The 1972 EPA DDT Cancellation Hearing Final Order). Since then, the bald eagle population has rebounded and they are no longer on the federal threatened and endangered species list. However, the species still faces significant threats from other environmental toxins, including lead. Poisoning was the most common cause of death of bald eagle carcasses submitted to the National Wildlife Health Center from 1982 to 2013, with lead poisoning occurring in 63.5% of poisoned birds. (9) Lead has many negative clinical and pathologic effects in birds. Clinical abnormalities can include neurologic signs and respiratory compromise, and pathologic abnormalities may include cardiac and renal damage. (2,3,10)

The 3 main sources of environmental lead contamination that affect wild birds are spent lead ammunition, lead sinkers and jigs, and the mining and smelting industry. (10-14) Birds are exposed to lead ammunition and sinkers and jigs primarily through direct ingestion. (3,10-14) Exposure to lead from the mining and smelting industry may be indirect, by ingestion through contaminated water sources or of prey containing lead from environmental food sources, or direct through ingestion of man-made objects containing lead.' The incidence of lead poisoning of bald eagles has been increasing despite the 1991 ban on the use of lead shot for waterfowl hunting. (8-11) Ingestion of bullet fragments from hunted mammalian carcasses is believed to be a significant source of lead exposure in bald eagles. (8-11)

Lead occurs as 4 main isotopes: [sup.208]Pb, [sup.206]Pb, and [sup.207]Pb are formed through radioactive decay, whereas 204Pb is a stable isotope. (12) The isotopic composition of lead can be expressed in ratios, with the [sup.207]Pb/[sup.206]Pb ratio used most frequently. (12) Lead isotope ratios are proposed as a means to identify the anthropogenic source of environmental lead contamination, as different sources have unique ratios. (3,4,12-15) Lead isotope analysis has been used effectively to trace sources of environmental pollution (12) and has provided valuable evidence in legal proceedings. (15)

Lead isotope analysis can also indicate potential sources of lead poisoning of wildlife. For example, most free-flying California condors, (4,14) Canadian waterfowl, and Canadian eagles (13) exposed to lead have an isotope ratio consistent with ammunition. Additionally, lead isotope analysis was used successfully to correlate lead paint with lead toxicosis of California condors (4) and Laysan albatrosses (Phoebastria immutabilis). (16)

When lead from multiple sources is combined, the resultant isotope value will reflect the average isotope ratio of the 2 or more substances, making the exact source difficult to pinpoint. (15) For example, evaluation of lead in black vultures and turkey vultures in Virginia found that all birds had evidence of chronic lead exposure, and lead isotope ratios overlapped with those of ammunition, leaded gasoline, coal emissions, and zinc smelting. (3) These results suggest that these scavengers are exposed to multiple sources of environmental lead contaminants.

On the basis of available reports of lead isotope ratios, possible anthropogenic sources of lead in this eagle are lead paint, zinc smelting, or leaded gasoline. However, it is likely this bird was exposed to several sources of lead or to a source not previously identified. Because of the cumulative nature of lead isotopes, confirming a single, primary source of lead exposure is not possible. The lead isotope results and the timing of this case do not support lead ammunition as the primary source of poisoning of this bird. This bird was admitted to the rehabilitation center in June and had hatched the previous March or April; Virginia hunting and trapping seasons occur in the fall of the year. Bald eagles will frequently eat fish; thus exposure to lead sinkers through prey ingestion is possible. Lead isotope ratios collected from the tissues of common loons (Gavia immer) diagnosed with lead toxicosis secondary to lead sinker ingestion were comparable to ratios of ammunition. (13) However, the lead isotope ratios of lead sinkers have not been directly measured and published.

The bone (26.787 ppm), liver (6.003 ppm), and kidney (7.591 ppm) lead levels in this juvenile eagle were several orders of magnitude higher than the blood lead level (0.616 ppm). Blood and soft tissue lead levels reflect recent lead exposure or leaching from bone stores, whereas bone lead levels reflect chronic lead exposure. (3,10,14) Although recent exposure to large quantities of lead cannot be ruled out, the amount of lead required to reach such high levels in the bone and tissues would likely have caused death if ingested at a single time point. Chronic, low-level lead exposure is more likely in this case and may have started with food fed in the nest and continued after fledging. Additionally, the clinical abnormalities noted in this bird, including loss of body condition, weakness, low hematocrit, and low total protein concentration, are consistent with the clinical changes generally seen in birds with chronic lead toxicosis." Birds with acute lead toxicosis are usually in good body condition, have more severe neurologic signs, and have higher blood lead levels ranging between 1.0 and 4.0 ppm. (2)

Why this individual bird ingested such a large amount and variety of anthropogenic debris is not known. Possible scenarios include pica from neurologic abnormalities associated with lead toxicosis, direct foreign body ingestion at a landfill, (17) ingestion of a prey species that contained the debris, or opportunistic ingestion because of the inability to fly and locate food. The ventricular foreign bodies were initially considered a potential source of toxicity, but the isotope analysis suggested otherwise. Although juvenile bald eagles are reported to ingest anthropogenic debris, (17) documentation of anthropogenic foreign bodies in the ventriculus of a free-ranging bald eagle has not been published to date.

This clinical case report documents a high degree of chronic lead exposure in a young bald eagle. The lead isotope ratios in this individual are dissimilar to lead ammunition, suggesting that environmental sources other than ammunition may be contributing to lead poisoning in this species. However, additional research is needed to evaluate further all potential sources of lead toxicosis in this species. Lead isotope analysis in combination with evaluation of gastrointestinal contents can provide an effective method for wildlife veterinarians to identify or exclude potential sources of lead poisoning. However, clinicians should use caution when interpreting lead isotope results in chronic cases where animals have likely been exposed to multiple sources of environmental lead. Additional publications that provide positive correlation between the lead isotope ratios present in ingested lead sources and the isotope ratios present in the bone and soft tissues will provide further evidence to support the use of lead isotope analysis in wildlife species.

Acknowledgments: We thank Dr Amo Wuenschmann from the University of Minnesota's Diagnostic Laboratory for performing the complete postmortem examination, Dr. Megan Kirchgessner for providing the US Geological Survey internal review, and Dr Patrick T. Redig for providing professional review. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

References

(1.) Teare JA. Haliaeetus leucocephalus. Physiological Data Reference Values [CD-ROM], Eagan, MN: International Species Information System; 2013.

(2.) Redig PT, Arent LR. Raptor toxicology. Vet Clin North Am Exot Anim Pract. 2008; 11(2):261-282.

(3.) Behmke S, Fallon J, Duerr AE, et al. Chronic lead exposure is epidemic in obligate scavenger populations in eastern North America. Environ Int. 2015; 79:51-55.

(4.) Finkelstein ME, Doak DF, George D, et al. Lead poisoning and the deceptive recovery of the critically endangered California condor. Proc Natl Acad Sci USA. 2012; 109(28): 11449-11454.

(5.) Koons RD, Grant DM. Compositional variation in bullet lead manufacture. J Forensic Sci. 2002;47(5): 950-958.

(6.) U.S. ammunition industry to survive closure of lead smelter. National Rifle Association Institute for Legislative Action Web site, https://www.nraila.org/ articles/201 31205/us-ammunition-industry-tosurvive-closure-of-lead-smelter. Accessed January 7, 2017.

(7.) Sileo L, Fefer SI. Paint chip poisoning of Laysan albatross at Midway Atoll. J Wildl Dis. 1987;23(3): 432-437.

(8.) Fisher IJ, Pain DJ, Thomas VG. A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv. 2006;131:421-432.

(9.) Russell RE, Franson JC. Causes of mortality in eagles submitted to the national wildlife health center 1975-2013. Wildl Soc Bull. 2014;38(4):697 704.

(10.) Scheuhammer AM, Norris SL. The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology. 1996;5(5):279-295.

(11.) Cruz-Martinez L, Redig PT, Deen J. Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Hum Wildl Interact. 2012;6(1):94 104.

(12.) Komarek M, Ettler V, Chrastny V, Mihaljevic M. Lead isotopes in environmental sciences: a review. Environ Int. 2008;34(4):562 577.

(13.) Scheuhammer AM, Templeton DM. Use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology. 1998;7:37-42.

(14.) Church ME, Gwiazda R, Risebrough RW, et al. Ammunition is the principal source of lead accumulated by California condors re-introduced to the wild. Environ Sci Technol. 2006;40(19):6143-6150.

(15.) Gulson B. Korsch M, Winchester W, et al. Successful application of lead isotopes in source apportionment, legal proceedings, remediation and monitoring. Environ Res. 2012;112:100-110.

(16.) Finkelstein ME, Gwiazda RH. Smith DR. Lead poisoning of seabirds: environmental risks from leaded paint at a decommissioned military base. Environ Sci Technol. 2003;37(15):3256-3260.

(17.) Elliot KH, Duffe J, Lee SL, et al. Foraging ecology of bald eagles at an urban landfill. Wilson J Ornithol. 2006; 118(3):380-390.

Dana Franzen-Klein, DVM, David McRuer, MSc, DVM, Dipl ACVPM, Vincent A. Slabe, MS, and Todd Katzner, PhD

From the Wildlife Center of Virginia, The Raptor Center, 1800 South Delphine Avenue, PO Box 1557, Waynesboro, VA 22980, USA (Franzen-Klein, McRuer); West Virginia University, Division of Forestry and Natural Resources, 355 Oakland Street, 322 Percival Hall. Morgantown, WV 26506, USA (Slabe); and the US Geological Survey, Forest and Rangeland Ecosystem Science Center, 970 Lusk Street. Boise, ID 83706, USA (Katzner). Present address 1920 Fitch Avenue, St Paul, MN 55108, USA (Franzen-Klein); Atlantic Veterinary College, Department of Pathology and Microbiology. 550 University Avenue, Charlottetown, PE CIA 4P3, Canada (McRuer).

Caption: Figure 1. Radiographs of a juvenile male bald eagle that that was presented to the Wildlife Center of Virginia after being found on the ground unable to fly. Images include a ventrodorsal whole-body view (a), a right lateral whole-body view (b), and a caudal-cranial view of the left proximal wing (c). The arrows identify a long oblique, comminuted, distal diaphyseal to distal metaphyseal fracture of the left humerus with moderate displacement and a large butterfly fragment. The circle identifies the foreign debris visible in the ventriculus, including a linear metallic opacity (*), as well as multiple foreign objects of varying shapes with a soft tissue to mineral opacity.

Caption: Figure 2. Lead isotope ratios from the soft tissues and foreign ventricular contents of the juvenile bald eagle described in Figure 1, as well as published reference values. Tissue samples from the eagle included the liver (BE Liver), kidney (BE Kidney), and femur (BE Bone). Foreign objects sampled from the bird's ventriculus included an aluminum soda can tab (Al tab), thumbtack (tack), paper, rubber balloon (balloon), plastic zip tie (zip tie), and plastic bag. Published lead isotope ratios are also included for comparison as follows: femur samples from Virginia black vulture (BV Bone) and turkey vulture (TV Bone,3) blood samples from California condors (CC Blood,4) lead paint samples from California (paint,4) values from lead (Pb) and zinc (Zn) smelting industries, (12) coal emissions, (12) leaded gasoline (fuel,12) and lead-based ammunition (ammo).4 The following lead isotope ratios are presented: (a) [sup.207]Pb/[sup.206]Pb; (b), [sup.208]Pb/[sup.206]Pb; (c), [sup.208]Pb/[sup.204]Pb; (d), [sup.206]Pb/[sup.204]Pb. The whisker portion of each graphic reflects 2 standard errors.
Table 1. Published mean [sup.207]Pb/[sup.206]Pb isotope ratios,
including the standard error (SE) and the minimum and maximum
values obtained. The mean [sup.207]Pb/[sup.206]Pb isotope ratios
from the soft tissues and foreign ventricular contents of the
juvenile male bald eagle described in this report are also
included.

Source                       Mean [sup.207]Pb/     SE
                                [sup.206]Pb

Prerelease CA condors (a)         0.8362         0.0012
Postrelease CA condors (a)        0.8284         0.0022
CA ammunition  (a)                0.8179         0.0013
CA lead paint (a)                 0.8925         0.0054
NA leaded gasoline (b)            0.8450         0.0215
Coal emissions (b)                0.8330         0.0050
Zinc smelting (b)                 0.8240         0.0225
Lead smelting (b)                 0.7520         0.0080
BLVU femur (b)                    0.8272         0.0012
TUVU femur (c)                    0.8268         0.0039
BAEA femur (c)                    0.8773
BAEA kidney (c)                   0.8686
BAEA liver (c)                    0.8761
BAEA aluminum tab (c)             0.8118
BAEA balloon (c)                  0.8273
BAEA paper (c)                    0.8387
BAEA plastic bag (c)              0.6356
BAEA plastic zip tie (c)          0.8547
BAEA tack (c)                     0.8278

Source                       Minimum [sup.207]Pb/     Maximum
                                 [sup.206]Pb        [sup.207]Pb/
                                                    [sup.206]Pb

Prerelease CA condors (a)           0.8296             0.8483
Postrelease CA condors (a)          0.7602             0.9164
CA ammunition (a)                  0.7858             0.8706
CA lead paint (a)                   0.8734             0.9148
NA leaded gasoline (b)              0.7190             0.9620
Coal emissions (b)                  0.7990             0.8880
Zinc smelting (b)                   0.8170             0.8290
Lead smelting (b)                   0.7460             0.7630
BLVU femur (b)                      0.8055             0.8813
TUVU femur (c)                      0.8121             0.8513
BAEA femur (c)
BAEA kidney (c)
BAEA liver (c)
BAEA aluminum tab (c)
BAEA balloon (c)
BAEA paper (c)
BAEA plastic bag (c)
BAEA plastic zip tie (c)
BAEA tack (c)

Abbreviations: CA indicates California; NA, North America; BLVU,
black vulture; TUVU. turkey vulture; BAEA, bald eagle.

(a) Finkelstein et al (2012).

(b) Behrnke et al (2015).

(c) The results from the bald eagle described in this report reflect
single samples; therefore, a standard deviation and low and high
values are not presented.
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Author:Franzen-Klein, Dana; McRuer, David; Slabe, Vincent A.; Katzner, Todd
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Geographic Code:1USA
Date:Mar 1, 2018
Words:3305
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