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Israel Journal of Veterinary Medicine  Vol. 69 (3)  September 2014 163 Acute Lead Poisoning in a Grifon Vulture
INTRODUCTION
Te Israeli Wildlife Hospital (IWH), established in 2005,
treats over 2,400 injured and sick birds brought in by civilians
and Israel’s Nature and Park Authority (NPA) rangers every
year. Finding birds that are still alive with lead poisoning is
extremely rare in Israel (1); the IWH typically receives only
about two of such cases per year. Toxic blood lead levels are
most often attributed to digestion of gunshot pellets in the
stomach, where the toxic metal is broken down by the strong
acidity and further absorbed into the blood stream (2). Te
bird, however, may not be a direct target of the gunshot,
but rather sufer from lead poisoning after ingesting bullets
remaining in carcasses left in hunted animals (2, 3, 4).
General clinical symptoms of lead toxicity include weak-
ness, lethargy, and weight loss. Gastrointestinal signs often
present as dark green or black diarrhea, ileus of the upper
gastrointestinal tract, and crop stasis with resulting disten-
sion and regurgitation. Neurological signs include head tilt
and tremors, paresis, and paralysis (4, 5). Hematological signs
include erythrocyte fragility and anemia due to the adhesion
of lead to erythrocytes in the blood stream (3).
Because of a dearth of literature regarding the toxic blood
lead levels of diferent bird species, the clinical standards of
toxicity commonly used are those established for other rap-
tors such as those reported on the Bald Eagle (Haliaeetus
leucocephalus) population by Redig (1984) at the University
of Minnesota (6, 7, 8, 9). According to these thresholds, there
are four stages of lead exposure measured in the blood: back-
ground (<20 µg/dL), subclinical exposure (20-59 µg/dL),
clinical exposure (60-99 µg/dL), and acute exposure (>100
Acute Lead Poisoning in a Grifon Vulture (Gyps fulvus) in Israel
Horowitz, I.H.,
1
* Yanco, E.,
2
Nadler, R. V.,
2
Anglister, N.,
2
Landau, S.,
2
Elias, R.,
2
Lublin, A.,
3
Perl, S.,
4
Edery, N.
4
and Rosenzweig, A.B.
1
1
Zoological Center Tel Aviv-Ramat Gan & Israeli Wildlife Hospital at the Zoological Center Tel Aviv-Ramat Gan, 1 HaTsvi
Ave., Ramat Gan 52109, Israel.
2
Israeli Wildlife Hospital at the Tel Aviv-Ramat Gan Zoological Center, 1 Hatsvi Ave., Ramat Gan 52109, Israel.
3
Division of Avian & Fish Diseases, Kimron Veterinary Institute, POB 12, Bet Dagan 50250, Israel.
4
Department of Pathology, Kimron Veterinary Institute, POB 12, Bet Dagan 50250, Israel.
* Corresponding Author: Dr. Igal Horowitz DVM, Zoological Center Tel Aviv-Ramat Gan, 1 Hatsvi Ave., Ramat Gan 52109, Israel. P.O. Box 984.
Tel: +972-3-6305318, Mobile: +972-54-4650000, Fax: +972-3-6305303, Email: igal@safari.co.il
ABSTRACT
A free-ranging Grifon Vulture (Gyps fulvus) found lying in a feeding station in the Golan Heights region of
Israel was admitted to the Israeli Wildlife Hospital in Ramat Gan, Israel. Te adult female vulture presented
weak, cachectic, and standing on her tarsometatarsi. She had green diarrhea on her feathers and around
her cloaca, a distended crop, and dropped head. X-ray images showed a circular radio-opaque object in
the proventriculus and gastric lavage resulted in the regurgitation of a 9 mm lead bullet. Te vulture was
diagnosed with suspected lead toxicity, which was later confrmed with a blood lead level of 804.8 µg/dL. On
day 7, a blood assay showed a lead level of 341.7 µg/dL, an overall marked decrease though still extremely
toxic. Crop stasis and distension persisted despite chelation therapy and supportive care and the vulture died
7 days after hospital admission, prior to ingluviotomy. To the best knowledge of the authors, this is the most
toxic case of lead poisoning discovered and published to date of a Grifon Vulture in the Palearctic Zone.
Keywords: Grifon Vulture, Gyps fulvus, Crop Stasis, Lead Toxicity, Gastric Lavage.
Israel Journal of Veterinary Medicine  Vol. 69 (3)  September 2014 Horowitz, I.H. 164
µg/dL) (6). Te blood lead level of the 8 year old Grifon
Vulture upon admission to the Israeli Wildlife Hospital was
804.8 µg/dL, more than eight times the threshold for toxic
lead exposure.
CASE HISTORY
On February 17, 2014 (day 0), an adult female Grifon
Vulture (Gyps fulvus) was found unresponsive by NPA rang-
ers in a feeding station in Gamla, in the Golan Heights
region of Israel. Known to the NPA from previous popu-
lation monitoring captures, she presented extremely weak
and cachectic at 5.3 kilograms, down 2.2 kilograms from her
weight recorded in September 2007 (7.5 kg). She was imme-
diately transported to a local veterinary clinic for examina-
tion. Because of recent episodes in organophosphate-related
deaths of local wildlife scavenging on tainted livestock car-
casses, she was administered an undetermined amount of
atropine for treatment for suspected organophosphate in-
toxication. Te vulture was then transported 180 kilome-
ters to the IWH by NPA rangers for further diagnosis and
treatment.
Upon arrival to the IWH, the vulture showed signs of
cachexia, green diarrhea, and dry third eyelids. She was mod-
erately weak with her head dropping forward and balance
maintained on her tarsometatarsi, but did occasionally resist
handling. Her crop was completely full and distended and
simple palpation elicited vomiting. Temperature, pulse, and
respiration were all within normal limits. A 20G catheter
(Delta Ven 2, Delta Med Medical Devices, Viadana, Italy)
was inserted into the metatarsal vein, whole blood was col-
lected in heparinized, serum, and EDTA blood collection
tubes (Greiner Bio-One GmbH, Austria) for external labo-
ratory diagnostics (PathoVet, Ltd., Rehovot, Israel and Tel
Hashomer Hospital Toxicology Laboratory, Ramat Gan,
Israel), and parenteral fuids (Lactated Ringer’s solution
with 5% Dextrose, 30ml/hr, Teva Medical Ltd., Ashdod,
Israel) were administered intravenously. An in-house PCV/
TS test showed a packed cell volume of 40%, just under the
normal range determined for Grifon Vultures in captivity
(43 ± 2.1%), and total solids of 4 g/dL, which was within the
normal range of total protein for Grifon Vultures in captiv-
ity (4.0 ± 0.21) (10). Dorsoventral and lateral radiographic
images revealed a 9 mm round radio-opaque object in the
proventriculus (Figure 1). According to the presenting signs
and radiology, IWH veterinarians diagnosed the vulture with
suspected lead toxicity.
Hematology and biochemical results are presented in
Table 1. Hematology indicated moderate leukocytosis with
a relative heterophilia, left shift, and slight to moderate
monocytosis with no apparent toxicity of the heterophils.
Figure 1: a) A radiograph of a Grifon Vulture with suspected lead
poisoning shows a 9mm radio-opaque object in the proventriculus
(indicated with an arrow), assumed to be the source of intoxication.
Te second radio-opaque object near the right wing is a wing tag pin.
b) Gastric lavage led to the expulsion of gastric content containing a
9mm lead bullet.
a)
b)
Case Reports
Israel Journal of Veterinary Medicine  Vol. 69 (3)  September 2014 165 Acute Lead Poisoning in a Grifon Vulture
Hemoglobin levels were signifcantly decreased (11), indi-
cating severe anemia. Blood flms revealed abundant poly-
chromasia (~15%) and occasional rubricytes. All biochemical
measurements were unremarkable.
Tese fndings indicated an infammatory leukogram,
which could be associated with an infectious agent or non-
infectious condition (i.e. toxicity) or in response to environ-
mental stress (stress leukogram). Immature erythrocytes (i.e.
rubricytes) coupled with polychromasia in the blood of an
anemic bird indicate a marked erythrocyte response. In ad-
dition, these immature erythrocytes could be a sign of pre-
mature release from hematopoietic tissue due to toxicity (i.e.
lead poisoning) (12). Lead also directly interferes with the
enzymes involved in the biosynthesis of the heme group,
contributing to the fragility of red blood cells and a decrease
in hemoglobin levels (3, 13). Te efect of lead in both pro-
cesses supports the diferential diagnosis of lead poisoning
in the Grifon Vulture.
Atomic absorption spectroscopy at the Tel Hashomer
Hospital Toxicology and Pharmacology Laboratory (Ramat
Gan, Israel) later confrmed the lead poisoning diagnosis
with a blood lead level of 804.8 µg/dL (normal blood lead
level <20 µg/dL, subclinical exposure level 20-59 µg/dL).
Tis value is more than eight times the threshold established
by Redig (1984) for acute lead exposure in raptors.
Gastric Lavage
In preparation for removal of the radio-opaque object by
gastric lavage and treatment of lead toxicity, the vulture was
administered butorphanol (Torbugesic 10 mg/ml, 0.5 mg/
kg IM; Fort Dodge Animal Health, Fort Dodge, IO, USA)
for analgesia and midazolam (Midazolam 5 mg/ml, 0.5 mg/
kg IM; Rafa Laboratories Ltd., Jerusalem, Israel) for pre-
anesthesia sedation. Tirty minutes after administration of
butorphanol and midazolam, the vulture was anesthetized
with an isofurane mask (Terrell, Piramal Critical Care,
Bethlehem, PA, USA), intubated with a 7 mm endotra-
cheal tube (Hi-Contour, Mallinckrodt Medical, Athlone,
Ireland), and maintained under anesthesia with isofurane
via intubation.
With the vulture positioned sternally on the examination
table, a custom-made 1.2 cm PVC orogastric tube was mea-
sured to the proventriculus, lubricated with a water-based lu-
bricant (K-Y Lubricating Jelly, Johnson & Johnson, Sézanne,
France), and inserted into the proventriculus (Figure 2). Te
proximal end of the body was lifted and 200 ml of LRS was
inserted through the orogastric tube into the proventriculus.
Te distal end of the table was then lifted to a 75° angle,
directing the vulture’s head down towards the foor. Fluid
and gastric content were expelled into a bucket, but an X-ray
of these contents did not show a radio-opaque object. Te
gastric lavage procedure was repeated once again, and this
second attempt resulted in the expulsion of a 9 mm lead
bullet amid the remaining gastric content (Figure 1).
Follow-up Care
Upon completion of the 20 minute gastric lavage procedure,
the vulture was removed from isofurane, placed in an ICU
unit (1.35 m x 2.15 m), and continued on fuids and heating.
She was started on meloxicam (Meloxicam 5mg/ml, 0.5 mg/
kg IM SID for 2 days; Vetmarket, Segula, Israel), cefazolin
(Pan-Cefazolin 1g, 50 mg/kg IV SID for 8 days; Panpharma,
Table 1: Hematology results
Day 1 Day 6 Reference
Packed Cell Volume (%) 40 28 43 ± 2.1*
Total Solids (g/dL) 4 3.6 4.0 ± 0.21*
Leukocytes (estimated count 10
3
/µL***) 15.75 14.00 -
Hemoglobin (g/dL) 11.3 9.4 15.1 ± 1.9**
Heterophils (%) 91 96 57.83 ± 9.87**
Lymphocytes (%) 2 1 40.67 ± 10.52**
Monocytes (%) 7 2 0.57 ± 0.53**
Eosinophils (%) 0 1 0.86 ± 1.57**
Basophils (%) 0 0 0.00**
* Ferrer, M. et al., 1987, references provided are for PCV and total
protein.
** Polo, F. et al., 1992.
*** Method described in Campbell, T. and Ellis, C., 2007.
Figure 2: Gastric lavage preparation for a Grifon Vulture with lead
poisoning: the insertion of endotracheal and orogastric tubes.
Case Reports
Israel Journal of Veterinary Medicine  Vol. 69 (3)  September 2014 Horowitz, I.H. 166
France), vitamins B
1
and B
12
(Dodicile Veterinary, 30 mg/
kg SQ SID for 2 days; FATRO S.p.A, Bologna, Italy), and
chelating agent CaEDTA (200mg/ml, 30 mg/kg IM SID
for 5 days on, 3 days of; Hebrew University of Jerusalem
Veterinary Hospital, Rehovot, Israel) (3, 5). Tree hours later,
she was vomiting fuids and digested meat and attempted to
stand up unsuccessfully due to poor balance.
On day 1 after the procedure, there was no change in
the vulture’s clinical appearance. She was quiet, weak, not
standing, and continued to drop her head forward, though
vital signs remained normal. She was started on preven-
tative metronidazole (Metronidazole 10%, 30 mg/kg SQ
SID for 2 days; Vetmarket, Segula, Israel). On day 2, she
was administered a gastric stimulator metoclopramide
HCl (Pramin Tablets 10mg, 0.3 mg/kg IM SID for 6 days;
Rafa Laboratories Ltd., Jerusalem, Israel). Similar to previ-
ously reported symptoms of crop stasis, the vulture had a
strong appetite and continued to eat gazelle carcass, liver,
and small mice as normal. Tough there was the impres-
sion that a portion of the food was passing through to
the stomach, the majority of her food was lodged in the
crop. Palpation induced vomiting, and vomiting continued
for the next few days even after the removal of food. On
day 3, she was dosed preventative itraconazole (Sporonox
Capsules 100mg dissolved, 10 mg/kg PO SID for 5 days;
Janssen Cilag, Italy) and weighed 6.7 kg with a distended,
full crop.
On day 6, the vulture continued to vomit with every
handling, remained weak with her head dropped, and pre-
sented clutched talons and hypothermia (37.5°, normal
~40°). In-house PCV/TS results decreased to 28% and 3.6
g/dL, respectively, and her weight reduced to 5.2 kg af-
ter excessive vomiting. Multivitamins (Duphalyte, 1 mg/
kg IM; Fort Dodge Veterinaria, S.A., Girona, Spain) and
hydroxyethyl starch (HAES-steril 10%, 1 ml/kg/hour IV;
Fresenius Kabi, Germany) were added to her IV fuids and
another blood sample was sent to external laboratory facili-
ties for a complete blood count and lead assay. Aside from
a decrease in hemoglobin levels from 11.3 g/dL to 9.4 g/
dL (Table 1), hematology results showed fndings similar
to those of day 1.
As her condition deteriorated on day 7, the veterinary
staf at the IWH started preparations for insertion of an in-
gluviostomy tube on the morning of day 8, a procedure which
has previously been successfully implemented on California
Condors (Gymnogyps californianus) with severe lead poison-
ing. Ingluviostomy tube placement has been proven to ef-
fectively bypass crop stasis and circumvent gastrointestinal
complications induced by lead toxicity (14, 15).
On the morning of day 8 just prior to the procedure,
the Grifon Vulture was found dead. Te cause of death was
attributed to complications of severe lead toxicity. Tough
an exact cause remains unknown, death can most likely be
attributed to organ failure of the known targets of lead toxic-
ity (13).
Te lead test results returned from blood drawn on day 6
showed a blood lead level of 341.7 µg/dL, a marked decrease
though still in the acute exposure threshold (6).
Post mortem and histological results
Post-mortem analysis found very dark, almost black food
content in the proventriculus and ventriculus. Tis fnding,
along with a stable weight over the course of the week (at
day 7, 5.2 kg with empty crop), confrmed the earlier suspi-
cion that some food was passing through the crop. On gross
pathology, the vulture’s kidneys were mildly enlarged. No
other signifcant pathological or histological abnormalities
were found in the known target organs of lead poisoning
(13, 16). Tis fnding is in agreement with an experimental
lead poisoning study in Turkey Vultures (Cathartes aura), in
which no gross pathological or microscopic pathognomonic
lesions for lead intoxication were found (16). Te blood levels
of lead were clear indications of the ongoing toxicity in this
case and it appears that the pathology may not be suitable to
make a defnitive diagnosis of lead poisoning.
DISCUSSION
Tough Grifon Vultures (Gyps fulvus) are currently listed on
the International Union for Conservation of Nature (IUCN)
Red List of Treatened Species as of Least Concern (17), the
local population in Israel is experiencing a rapid state of de-
cline. Dropping from 1000 nesting pairs in the 1940’s to only
39 in 2011, only 10 chicks were successfully reared in the wild
during the 2011 breeding season (1). As part of the larger
program to reinstate the declining population, the IWH aims
to act as quickly as possible on the treatment of injured or sick
Grifon Vultures arriving at our facility. Of the 148 Grifon
Vultures treated at the IWH from 2001 to 2011, 61 were suf-
Case Reports
Israel Journal of Veterinary Medicine  Vol. 69 (3)  September 2014 167 Acute Lead Poisoning in a Grifon Vulture
fering from various kinds of poisonings or suspected poison-
ings, only 5 of which were determined to be from lead (1).
Te amount of time required to confrm a diagnosis of
lead toxicity and begin treatment is often the crucial factor
between survival and mortality. Due to the indicative clinical
presentation of lead toxicity similar to those reported in nu-
merous publications across the world (2, 3, 14, 15, 16), initial
radiographic diagnostics and presenting signs were adequate
for IWH veterinarians to make a provisional diagnosis of
lead toxicity and to appropriately treat this 8 year-old female
Grifon Vulture. Gastric lavage and chelation therapy were
administered before suspected lead poisoning was confrmed
by the blood lead level laboratory diagnostics; the removal
of the source of poisoning remarkably reduced blood lead
levels by 463.1 µg/dL (804.8 µg/dl down to 341.7 µg/dL)
in only 7 days.
Te IWH maintains a full stock of diagnostic tools for
incoming lead toxicity cases. Te life or death of animals
sufering from lead poisoning depends on the availability of
these diagnostic and treatment options, which can be utilized
prior to laboratory confrmation of toxicity and minimize the
time gap between arrival and diagnosis confrmation.
Veterinarians treating suspected lead intoxication cases
should not always depend upon physical evidence for a dif-
ferential diagnosis—data estimates that only 15% of birds
sufering from lead poisoning actually contain a lead pellet in
their gut upon arrival to an animal clinic (18). In such cases,
presentation of some or all of the lead-induced clinical signs
(weight loss, lack of appetite, anemia, difculty in standing,
crop stasis, diarrhea, mild head tremors, head drooping, de-
pression, nistagmus), can indicate lead as a possible source
of intoxication (2, 3, 4, 5).
Should lead particles be present in the gastrointestinal
tract, gastric lavage and chelation therapy are clearly dem-
onstrated in these fndings to be an efective treatment that
both remove the source of toxicity and greatly lower the ex-
isting toxic components in the blood stream. Should crop
stasis and distension persist after initial chelation therapy,
ingluviotomy placement can be considered as an additional
treatment.
Te challenge in such cases is deciding when treatment
should be administered. Research in two previous publica-
tions reports that ingluviotomy tubes were inserted after 8 to
12 days after initiation of treatment, but not all cases resulted
in successful recovery (14, 15). Lead toxicity in any avian spe-
cies clearly poses a treatment challenge because of the need
to address the damage to many organ systems afected by the
consumption of lead (13).
To date, this is the most severe case of lead poisoning
that has been observed in the State of Israel and, though
the vulture died of lead toxicosis-related complications,
serves as an example of of which to build a systematic
treatment plan. A signifcant amount of data has been pub-
lished regarding lead toxicity in vultures across the world,
but to the best knowledge of the authors, this is the most
severe case of lead poisoning of a Grifon Vulture in the
Palearctic Zone.
ACKNOWLEDGMENTS
Te authors would like to extend a special thanks to the skilled staf
and volunteers who treat and manage all of the animals admitted
to our facility with passion and dedication.
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Cor rect i on
Investigation of Swine Infuenza Sub-Types H1N1, H3N2, H1N2
in Pigs Population in Israel (2002-2009).
Pozzi S. P., Aborali G., Cordioli, P. and Rosner, A. IJVM 65 (1): 11-14, 2010.
In the heading of the article published the designation of the virus types were printed incorrectly in the heading of the
article although in the abstract and body of the article the correct names were given throughout the article.
Te virus designations have been corrected from H32 to H3N2 and N1N2 has been corrected to H1N2.
Te incorrect naming of the swine infuenza strains in the heading does not refect any changes in the article itself or in
the conclusions made by the authors. Te error made in the heading was a typographical error only.
Te correct title reads:
Investigation of Swine Infuenza Sub-Types H1N1, H3N2, H1N2 in Pigs Population in Israel (2002-2009).
Te online website (www.ijvm.org.il) has been corrected both in the table of contents and in the heading of the article
itself.
Case Reports