HYPERTENSIVE HEART DISEASE AND ENCEPHALOPATHY IN A CENTRAL BEARDED DRAGON (POGONA VITTICEPS) WITH SEVERE ATHEROSCLEROSIS AND FIRST-DEGREE ATRIOVENTRICULAR BLOCK

Abstract

A 0.5 kg, 5-yr-old male bearded dragon (Pogona vitticeps) presented with a 2-mo history of lethargy, anorexia, and impaired locomotion. Upon physical examination, bradyarrhythmia (heart rate: 20 beats/min) and balance disorders were noted. Electrocardiography revealed a first-degree atrioventricular block (P-R interval: 360 ms). On echocardiography, all cardiac chambers were slightly above normal ranges. Complete blood count, blood biochemistry, and T4 were unremarkable except for mildly elevated aspartate aminotransferase. Adenovirus testing was negative by polymerase chain reaction. Following euthanasia, necropsy revealed marked thickening of the arterial trunks and histopathology confirmed multifocal atherosclerosis of efferent heart vessels, arteriosclerosis of cerebral arterioles, and multifocal spongiosis of brain tissue, more pronounced in the optic chiasma. Owing to its severity, atherosclerosis may have contributed to chronic arterial hypertension with damages to the heart, brain vessels, and brain tissue-optic chiasma.

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HYPERTENSIVE HEART DISEASE AND ENCEPHALOPATHY
IN A CENTRAL BEARDED DRAGON (POGONA VITTICEPS)
WITH SEVERE ATHEROSCLEROSIS AND FIRST-DEGREE
ATRIOVENTRICULAR BLOCK
Authors: Lionel Schilliger, Clément Paillusseau, Frédéric Gandar, Isabelle
Desprez, William Claude, et. al.
Source: Journal of Zoo and Wildlife Medicine, 50(2) : 482-486
Published By: American Association of Zoo Veterinarians
URL: https://doi.org/10.1638/2018-0178
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Journal of Zoo and Wildlife Medicine 50(2): 482– 486, 2019
Copyright 2019 by American Association of Zoo Veterinarians
HYPERTENSIVE HEART DISEASE AND ENCEPHALOPATHY IN A
CENTRAL BEARDED DRAGON (POGONA VITTICEPS)WITH
SEVERE ATHEROSCLEROSIS AND FIRST-DEGREE
ATRIOVENTRICULAR BLOCK
Lionel Schilliger, D.V.M., Dipl. E.C.Z.M. (Herpetology), D.A.B.V.P. (Reptile and Amphibian
Practice), Cle
´ment Paillusseau, D.V.M., Fre
´de
´ric Gandar, D.V.M., Isabelle Desprez, D.V.M., William
Claude, D.V.M., Peggy Passavin, D.V.M., Vittorio Saponaro, D.V.M., Ph.D., Marine Roche-Catholy,
D.V.M., Alexandra Nicolier, D.V.M., Dipl E.C.V.P., Jean-Louis Pouchelon, D.V.M., Ph.D., and Vale
´rie
Chetboul, D.V.M., Ph.D., Dipl. E.C.V.I.M. (Cardiology).
Abstract: A 0.5 kg, 5-yr-old male bearded dragon (Pogona vitticeps) presented with a 2-mo history of lethargy,
anorexia, and impaired locomotion. Upon physical examination, bradyarrhythmia (heart rate: 20 beats/min) and
balance disorders were noted. Electrocardiography revealed a first-degree atrioventricular block (P-R interval:
360 ms). On echocardiography, all cardiac chambers were slightly above normal ranges. Complete blood count,
blood biochemistry, and T4 were unremarkable except for mildly elevated aspartate aminotransferase. Adenovirus
testing was negative by polymerase chain reaction. Following euthanasia, necropsy revealed marked thickening of
the arterial trunks and histopathology confirmed multifocal atherosclerosis of efferent heart vessels,
arteriosclerosis of cerebral arterioles, and multifocal spongiosis of brain tissue, more pronounced in the optic
chiasma. Owing to its severity, atherosclerosis may have contributed to chronic arterial hypertension with
damages to the heart, brain vessels, and brain tissue-optic chiasma.
Keywords: atherosclerosis, bearded dragon, bradycardia, first-deg ree atrioventricular block, hypertensive
encephalopathy, Pogona vitticeps.
BRIEF COMMUNICATION
A 0.5 kg, 5-yr-old, male, captive-born, inland
bearded dragon (Pogona vitticeps) presented with a
2-mo history of lethargy, anorexia, and impaired
locomotion. The animal was purchased in a pet
store and was kept alone in a terrarium. Upon
questioning, the owner described adequate hus-
bandry in terms of temperature gradients, humid-
ity, photoperiod, UVB exposure, and substrate.
No deficiencies were identified with the diet,
which consisted of daily vegetables (romaine
lettuce, escarole, beet greens, spinach, dandelion)
and twice-weekly crickets (Acheta domestica).
The animal was lethargic and displayed a
delayed righting reflex with postural abnormali-
ties. Cardiac auscultation revealed bradyarrhyth-
mia (heart rate: 20 beats/min; reference range, 24–
170).
7
No heart murmur was detected.
Electrocardiography (ECG) was performed and
recorded with the use of a digital ECG recorder
(MAC 5500, General Electric Medical Systemt,
Waukesha, WI 53186, USA). Atraumatic alligator
clip electrodes were applied to the skin using a
modified Einthoven triangle as described for
squamata.
2,7
The cranial electrodes were placed
in the lateral cervical region on a line ventral to
the ear scale (red lead on the right, yellow lead on
the left) and the caudal electrodes were placed on
the lateral body wall at a point just cranial to the
stifle (green lead on the left, black on the right)
(Fig. 1A). Coupling gel was applied to the skin a
few minutes before recording to improve skin
contact. Recording of the ECG started 30 sec after
the lizard had settled into a relaxed position and
had become inactive. One minute of six-lead
(bipolar I, II, III and augmented unipolar aVR,
aVL, aVF) ECG recordings were taken. Brady-
cardia was confirmed (heart rate: 20 beats/min)
and a first-degree atrioventricular (AV) block was
diagnosed, indicated by a prolonged P-R interval
From the Veterinary Clinic of Auteuil Village, 35 rue
Leconte de Lisle, 75016 Paris, France (Schilliger, Paillus-
seau, Gandar); Exotics Medicine Service, National Veter-
inary School of Alfort, 7 avenue du ge
´ne
´ral de Gaulle,
94704 Maisons-Alfort cedex, France (Desprez, Claude);
Alfort Cardiology Unit (UCA), Centre Hospitalier Uni-
versitaire Ve
´te
´rinaire d’Alfort (CHUVA), National Veter-
inary School of Alfort, 7 avenue du ge
´ne
´ral de Gaulle,
94704 Maisons-Alfort cedex, France (Passavin, Saponaro,
Roche-Catholy, Pouchelon, Chetboul); Veterinary Pathol-
ogy Laboratory Vetdiagnostics, 14 avenue Rockefeller,
69008 Lyon, France (Nicolier); and INSERM U955,
E
´quipe 03, 51 avenue du mare
´chal de Lattre de Tassigny,
94010 Cre
´teil cedex, France (Chetboul). Correspondence
should be directed to Dr. Schilliger (Dr.L.Schilliger@
club-internet.fr).
482
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(360 ms; reference range, 75–253) (Fig. 1B).
7
On
echocardiography, heart size was slightly above
normal range (left atrium: 1.05 cm, reference
range 0.81–0.96 cm; right atrium: 1.32 cm,
reference range 1.03–1.25 cm; total atrial diame-
ter: 2.37 cm, reference range 1.89–2.17 cm;
ventricular longitudinal diastole: 2.0 cm, refer-
ence range 1.36–1.58 cm; ventricular longitudinal
systole: 1.46 cm, reference range 1.03–1.23 cm).
13
Minor pericardial effusion, considered as a nor-
mal finding in more than 60
%
of healthy bearded
dragons, was also visible.
13
Whole blood was
collected by venipuncture of the ventral tail vein.
Complete blood count did not show any abnor-
malities.
9
Blood biochemistry (calcium, liver en-
zymes, phosphate, potassium, sodium, total
cholesterol, uric acid) was unremarkable except
for elevated aspartate aminotransferase (105 IU/
L; reference range 1–53 IU/L).
14
Total T4 (12.14
nM/L) was within the reference range for other
species, although ranges are not established for
Pogona vitticeps.
3
This could somewhat rule out
hypothyroidism as a potential cause of both
bradycardia and AV block. A fecal sample was
negative for protozoal or helminthic infection.
Adenovirus testing was negative by polymerase
chain reaction.
10
Computed tomography (CT) was
also performed to explore neurological signs, but
no abnormalities of the central nervous system
could be detected.
As the dragon’s condition was rapidly deterio-
rating, the owner elected for euthanasia. On gross
examination, necropsy mainly showed a thicken-
ing of the efferent arterial trunks of the base of the
heart (Fig. 2A). Atrophy of the cerebellum was
also observed (Fig. 2B). All sampled organs
(brain, carotid arteries, jugular veins, thyroid,
aortas, pulmonary trunk, heart, lung, liver, stom-
ach, intestine, kidney, testis) were fi xed in 10
%
neutral buffered formalin, processed routinely,
embedded in paraffin, sectioned at 3–5 microns,
mounted on glass slides, and stained with hema-
toxylin and eosin. Histopathology confirmed
severe multifocal atherosclerosis of efferent heart
vessels, sometimes resulting in the subocclusion
of the arterial lumen. The lesions were character-
ized by thickening of the intima, and rarely the
media, by variable amounts of lipids, inflammato-
ry cells, connective tissue, and mucinous matrix
forming atheromatous plaques (Fig. 3A). Slight
mineralizations were also present. Examination of
the brain revealed cerebellar atrophy, mild hydro-
cephalus, and bilateral spongiosis of the white
matter, more pronounced in the optic chiasma,
the pons, and the medulla oblongata. Some
meningeal and parenchymal arterioles in the
Figure 1. Electrodes positioning (A) and D2 lead ECG tracing showing bradycardia and a first-deg ree AV
block with P-R interval of 360 ms duration (B). 1 mV ¼20 mm and paper speed ¼12.5 mm/sec.
SCHILLIGER ET AL—ATHEROSCLEROSIS IN A BEARDED DRAGON 483
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spongiotic areas showed hyaline thickening of
their wall evidenced by the trichrome stain,
compatible with arteriosclerosis. (Fig. 3B).
Based upon ECG, echocardiography, necropsy,
and histological examination, a final diagnosis of
multifocal atherosclerosis with bradycardia and
first-degree AV block, associated with cerebellar
atrophy, cerebral spongiosis, and arteriosclerosis
was established.
Although common in captive psittacines, ath-
erosclerosis is poorly documented in reptiles, and
has been reported only once in this species.
12
Additionally, to the best of the authors’ knowl-
edge, AV block has not yet been reported in
reptiles.
First-degree AV block is defined as a prolonga-
tion of the PR interval on ECG tracings, mea-
sured from the onset of atrial depolarization (P
wave) to the beginning of ventricular depolariza-
tion (qRs complex). The main challenges associ-
ated with the use of ECG in reptiles are related to
the fact that amplitudes are generally very low (,1
mV) and standard parameters are only established
for a few species.
2,7
However, a good quality ECG
tracing could be obtained in the present case,
allowing accurate measurement of the PR interval
duration which, in this case, was markedly pro-
longed (360 ms; upper normal range: 253 ms).
7
In
first-degree AV block, whereas conduction is
slowed, every atrial impulse is transmitted to the
Figure 2. Necropsy (gross examination) showing a rigid aspect and a thickening of the efferent arterial trunks
of the heart base (white circle) (A), and atrophy of the cerebellum (black circle) (B).
Figure 3. Histopathological examination showing a suboccluding atheromatous plaque in an efferent heart
artery (A), bar ¼250 lm; and arteriosclerosis in the optic chiasma (B), bar ¼100 lm). B. Masson’s trichome
inserted. Hematoxylin and eosin stain.
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ventricle without affecting the ventricular rate. In
mammals, it may be secondary to increased vagal
tone, athletic training, mitral valve surgery, myo-
carditis, cardiomyopathies, electrolyte distur-
bances (e.g. hyperkalemia), AV nodal blocking
drugs (beta-blockers, calcium channel blockers,
amiodarone) or may be a normal variant. In
reptiles, the reasons for first-degree AV block
are unknown so far but may be due to myocardial
remodeling, as described in parrots with athero-
sclerosis.
2
In mammals and birds, the heart is
driven by a natural pacemaker, called the sinus
node that resides within a distinct anatomically
distinguishable structure, located at the sinoatrial
junction. In reptiles, a ring-like domain of myo-
cardium with nodal characteristics, located
around the sinoatrial junction, functions as the
dominant pacemaker of the heart and has a
molecular phenotype comparable to those of
embryonic mammals and chicken.
8
Unlike mam-
mals, reptiles maintain a sinoatrial delay of the
impulse, allowing the sinus venosus to function as
a chamber.
8
Atherosclerosis, which is a disease of large-
and medium-sized muscular arteries, character-
ized by formation of atherosclerotic plaques,
seems to be rare or at least underdiagnosed in
reptiles. Conversely, arteriosclerosis, character-
ized by ringed calcifications of the vessel walls
with aneurysmal dilatations, is more frequent in
these species.
5
In a study performed on 98
reptiles received for necropsy from English zoos
(including 59 snakes, 21 chelonians, and 10
lizards), only one specimen (a female black-
pointed tegu, Tupinambis nigropunctatus) showed
a few lipid-containing aortic nodules.
4
In another
study performed on 39 and 109 Australian
captive snakes and lizards, respectively, athero-
matous plaques were not seen in any of 148
aortas examined, this even in the presence of
considerable degrees of hypercholesterolemia.
1
It was reported only once, in a 2-yr-old male
captive bearded dragon (Pogona vitticeps),
12
and
was a fortuitous finding in a Mcdowell’s carpet
python (Morelia spilota mcdowelli) suffering from
restrictive cardiomyopathy and secondary con-
gestive heart failure.
11
Low arterial pressure in
reptiles may lead to a low prevalence of the
disease in these animals. In birds, atherosclerosis
risk factors include age, sex, species, stress,
elevated plasma cholesterol, systemic arterial
hypertension, nonnative diet, lack of antioxi-
dants, lack of exercise, and genetic factors.
2
Because this patient was neither overweight, its
diet did not include fat-rich insect larvae, and it
did not seem stressed, arterial hypertension was
suspected by a process of elimination. In birds, it
is assumed that either primary arterial hyperten-
sion can induce atherosclerosis (by injury of the
endothelium) or hypertension can be the conse-
quence of atherosclerosis owing to the related
increase in vascular resistance.
6
For technical
reasons, arterial blood pressure could not be
measured in this dragon, but the mild observed
cardiomegaly may have been induced by in-
creased afterload resulting from arterial hyper-
tension. In a high percentage of Amazon and
African g rey parrots, atheromatous lesions are
significantly and positively associated with car-
diac hypertrophy and myocardial fibrosis.
2
In this
case, no myocardial lesion was observed on
histopathology.
Ultrasound examination did not permit obtain-
ment of an antemortem diagnosis of atheroscle-
rosis because of the small size of the aortic walls
and limited access to these vascular structures
when using a left axillary window. Neither arte-
riosclerosis of brain vessels nor cerebellar atrophy
could be detected on CT.
A full neurologic examination was not per-
formed on this animal, but arteriosclerosis of the
cerebral arterioles associated with spongiosis
(which was more pronounced in the optic chias-
ma) and cerebellar atrophy strengthened the
hypothesis of hypertensive encephalopathy. Ow-
ing to its severity, atherosclerosis may have
contributed to chronic arterial hypertension with
damage to several target organs (heart, optic
chiasma, brain).
In conclusion, as atherosclerosis was reported
only once in this species, this report provides
clinical information on a vascular disease that is
significantly underrepresented in the reptile liter-
ature. To the authors’ knowledge, it is the first to
document first-degree AV block and presumed
arterial hypertension in a reptile.
Veterinarians should be aware that 1) athero-
sclerosis can affect bearded dragons, 2) lethargy
and postural abnormalities can be clinical signs of
atherosclerosis and its consequences on target
organs in this species, and 3) cardiovascular
diseases, including atherosclerosis, must be in-
cluded as a differential diagnosis for neurological
presentations (e.g., ataxia) in reptiles.
Acknowledgments: Jesse Bonwitt, B.V.Sc.,
M.Sc., M.R.C.V.S., Minh Huynh, D.V.M., Dipl.
E.C.Z.M. (Avian), Dipl. A.C.Z.M., and Hugues
Beaufre
`re, D.V.M., Dipl. E.C.Z.M. (Avian), Dipl.
A.B.V.P. (Avian).
SCHILLIGER ET AL—ATHEROSCLEROSIS IN A BEARDED DRAGON 485
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LITERATURE CITED
1. Ardlie NG, Schwartz CJ. Arterial pathology in the
Australian reptile: a comparative study. J Pathol
Bacteriol. 1965;90:487–494.
2. Beaufre
`re H, Schilliger L, Pariaut R. Cardiovas-
cular system. In: Tully M, Mitchell M (eds.). Current
therapy in exotic pet practice. St. Louis (MO): Elsevier;
2016. p. 151–220.
3. Boyer TH, Steffes ZJ. Reptilian thyroid anatomy,
physiology and disease. In: Proc Assoc Reptile Amphib
Vet; 2011. p. 18–35.
4. Finlayson R, Symons C, T-W-Fiennes RN. Ath-
erosclerosis: a comparative study. Br Med J. 1962;1:
501–507.
5. Finlayson R, Woods SJ. Arterial disease of
reptiles. J Zool. 1977; 183(3):397–410.
6. Fricke C, Schmidt V, Cramer K, Krautwald-
Junghanns ME, Dorrestein M. Characterization of
atherosclerosis by histochemical and immunohisto-
chemical methods in African grey parrots (Psittacus
erithacus) and Amazon parrots (Amazonas spp.). Avian
Dis. 2009; 53:466–472.
7. Hunt D. Electrocardiography of the normal inland
bearded dragon. Thesis, Diploma in Zoological Med-
icine, 2013. Royal College of Veterinary Surgeons,
London (United Kingdom).
8. Jensen B, Vesterskov S, Boukens BJ, Nielsen JM,
Moorman AFM, Christoffels VM, Wang T. Morpho-
functional characterization of the systemic venous pole
of the reptile heart. Sci Rep [Internet]. 2017 [cited 2017
July 27];7(6644):1–12. Available from doi:10.1038/
s41598-017-06291-z
9. Raiti P. Husbandry, diseases and veterinary care
of the bearded dragon, Pogona vitticeps. In: Proc Assoc
Reptile Amphib Vet; 2011. p. 36–48.
10. Ritchie B. Virology. In: Mader DR (ed.). Reptile
medicine and surgery. St Louis (MO): Saunders
Elsevier; 2006:391–417.
11. Schilliger L, Chetboul V, Damoiseaux C, Nico-
lier A. Restrictive cardiomyopathy and secondary
congestive heart failure in a Mcdowell’s carpet python
(Morelia spilota mcdowelli). J Zoo Wildl Med. 2016;
47(4):1101–1104.
12. Schilliger L, Lemberger K, Chai N, Bourgeois A,
Charpentier M. Atherosclerosis associated with peri-
cardial effusion in a central bearded dragon (Pogona
vitticeps). J Vet Diag. 2010;22:789–792.
13. Silverman S, Sanchez-Migallon Guzman D,
Stern J, Gustavsen K, Griffiths LG. Standardization
of the two-dimensional transcoelomic echocardio-
graphic examination in the central bearded dragon
(Pogona vitticeps). J Vet Cardiol. 2016;18(2):168–178.
14. Tamukai K, Takami Y, Akabane Y, Kunazawa Y,
Une Y. Plasma biochemical reference values in clini-
cally healthy captive bearded dragons (Pogona vitticeps)
and the effects of sex and season. Vet Clin Pathol. 2011;
40(3):368–373.
Accepted for publication 17 January 2019
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