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Radiographic anatomy and barium sulfate contrast transit time of the gastrointestinal tract of bearded dragons (Pogona vitticeps)

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  • Université de Montréal - Faculté de médecine vétérinaire

Abstract and Figures

The positive contrast gastrointestinal study is a common non-invasive diagnostic technique that does not require anesthesia and enables good visualization of the digestive tract. Radiographic anatomy and reference intervals for gastrointestinal contrast transit time in inland bearded dragons (Pogona vitticeps) were established using seven animals administered 15 ml/kg of a 35% w/v suspension of barium by esophageal gavage. Dorso-ventral and lateral radiographic views were performed at 0, 15, 30 min, 1, 2, 4, 6, 8, 12 h, and then every 12 h up to 96 h after barium administration. Gastric emptying was complete at a median time of 10 h (range 4–24 h). Median jejunum and small intestinal emptying times were 1 h (range 30 min–2 h) and 29 h (range 24–48 h), respectively. Median transit time for cecum was 10 h (range 8–12 h). Median time for contrast to reach the colon was 31 h (range 12–72 h) after administration. Results were compared to those obtained in other reptilian species. This technique appeared safe in fasted bearded dragons and would be clinically applicable in other lizard species.
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RADIOGRAPHIC ANATOMY AND BARIUM SULFATE CONTRAST
TRANSIT TIME OF THE GASTROINTESTINAL TRACT OF BEARDED
DRAGONS (Pogona vitticeps)
CLAIRE GROSSET,LISE DANIAUX,DAV I D SANCHEZ-MIGALLON GUZMAN,ERNEST SCOTT WEBERIII, ALLISON
ZWINGENBERGER,JOANN E PAU L-MURPHY
The positive contrast gastrointestinal study is a common non-invasive diagnostic technique that does not require
anesthesia and enables good visualization of the digestive tract. Radiographic anatomy and reference intervals
for gastrointestinal contrast transit time in inland bearded dragons (Pogona vitticeps) were established using
seven animals administered 15 ml/kg of a 35% w/v suspension of barium by esophageal gavage. Dorso-ventral
and lateral radiographic views were performed at 0, 15, 30 min, 1, 2, 4, 6, 8, 12 h, and then every 12 h up to 96 h
after barium administration. Gastric emptying was complete at a median time of 10 h (range 4–24 h). Median
jejunum and small intestinal emptying times were 1 h (range 30 min–2 h) and 29 h (range 24–48 h), respectively.
Median transit time for cecum was 10 h (range 8–12 h). Median time for contrast to reach the colon was 31 h
(range 12–72 h) after administration. Results were compared to those obtained in other reptilian species. This
technique appeared safe in fasted bearded dragons and would be clinically applicable in other lizard species.
C2014 American College of Veterinary Radiology.
Key words: bearded dragon (Pogona vitticeps), barium, contrast, gastrointestinal transit time.
Introduction
INLAND BEARDED DRAGONS (Pogona vitticeps) are rep-
tiles commonly kept as companion animals in North
America, Australia, and Europe.1Approximately 500,000
juvenile bearded dragons are produced annually in the
United States.2Gastrointestinal disorders are a com-
mon clinical presentation in bearded dragons often as-
sociated with several clinical signs including anorexia.
Causes are various and include phytobezoars secondary to
dehydration,3obstruction by foreign bodies secondary to
substrate ingestion,4parasites,3and neuroendocrine gas-
tric carcinoma.5,6 Ileus or constipation can also be sec-
ondary to anatomic malformation of the pelvis or spine,3
follicular stasis, renomegaly, or other organomegaly.3Con-
trast studies offer a noninvasive technique to investigate
gastrointestinal transit in reptiles, as previously described
in green iguanas (Iguana iguana),7ball pythons (Python
regius),8leopard tortoises (Testudo pardalis),9Mediter-
ranean tortoises (Testudo hermanni),10 hawsbill sea tur-
tles (Erethmochelys imbricata),11 loggerhead sea turtles
(Caretta caretta),12 and red-eared slider turtles (Trache-
William R. Pritchard Veterinary Medical Teaching Hospital (Grosset,
Daniaux) the Departments of Medicine and Epidemiology (Guzman,
Weber, Paul-Murphy) Surgical and Radiologic Sciences (Zwingenberger)
School of VeterinaryMedicine, University of California , Davis, CA 95616.
Address correspondence and reprint requests to Joanne Paul-Murphy
at the above address. E-mail: paulmurphy@ucdavis.edu
Received July 2, 2013; accepted for publication September 29, 2013.
doi: 10.1111/vru.12128
mys scripta elegans).13 Digestive emptying times are typ-
ically higher in reptiles compared to mammals,12–14 and
this transit time may increase with gastrointestinal disease:
up to 40 days has been reported in loggerhead sea turtles.12
Gastrointestinal anatomy and normal digestive transit of
barium has not been evaluated in healthy bearded dragons.
The aims of this study were to evaluate contrast tran-
sit time, to describe the normal anatomy of the bearded
dragon gastrointestinal tract, and to evaluate possible ad-
verse effects of barium administration to bearded dragons.
Materials and Methods
Seven bearded dragons and four bearded dragon cadav-
ers obtained from a private breeder were used to investigate
the anatomy and imaging characteristics of the gastroin-
testinal tract. This project was approved by the Institu-
tional Animal Care and Use Committee of the University
of California, Davis.
Four adult bearded dragons, two females and two males
(weight range 150–282 gm), were used to establish the nor-
mal gross anatomic structures and topography of the gas-
trointestinal tract. Three of these bearded dragons were
preserved in 10% formalin solution after being used in an-
other experimental study, and had no digestive lesions. One
of the four bearded dragons was an adult male euthanized
due to congestive heart failure. Post mortem, the digestive
Vet Radiol Ultrasound, Vol. 00, No. 0, 2014, pp 1–10.
1
2GROSSET ET AL. 2014
tract was sutured at the level of the cardia and the cloaca,
and barium contrast was injected into the stomach with
a 20 gauge needle (Monoject, Tyco Heathcare Group LP,
Mansfield, MA) mounted on a 20 ml syringe. The digestive
tract was dissected and isolated from the body, and a radio-
graphic view was obtained to determine the radiographic
appearance of the lumen of the gastrointestinal tract.
Seven adult captive-bred bearded dragons, three females
and four males (weight range 150–297 gm), were obtained
from a private breeder (Sandfire Dragon Ranch, Bansall,
CA). Prior to this study animals were used to teach han-
dling and diagnostic techniques to veterinary students and
were housed individually in aquaria equipped with full-
spectrum fluorescent lights (Desert 50 UV B fluorescent
bulb, Zilla 20W, Franklin, WI) set on a twelve hr daily cy-
cle, with an infrared lamp (Zilla 50W, 120V, Franklin, WI.
Roche Cobas C501 Chemistry Analyzer, Roche Diagnos-
tics, Indianapolis, IN) providing a temperature gradient
ranging from 28Cto31
C. The diet consisted of dark
leafy greens, crickets (Acheta domesticus), and mealworms
(Tenebrio molitor). Physical examinations were conducted
for each animal and a 1 ml blood sample was obtained
from the ventral coccygeal vein with a 25 gauge needle
mounted on a 1 ml syringe. Physical examination, hema-
tocrit (Hematocrit tube, Fisherman scientific, Pittsburgh,
PA), biochemistry panel, and fecal parasitic examinations
by fecal flotation (Zinc sulfate 7-hydrate, Ovassay, Symbi-
otics Corporation, Pfizer Animal Health, New York City,
NY) were unremarkable and all the animals were consid-
ered healthy when enrolled in the study.
The day prior to administration of barium contrast,
bearded dragons were moved to a room adjacent to the
radiology equipment to minimize environmental tempera-
ture fluctuations during the study and decrease stress that
may be associated with transport. Ambient room temper-
ature was maintained between 28Cand33
Candtem-
perature was recorded in each terrarium to insure homo-
geneity of the environmental temperature between 28C
and 33C. Animals were housed individually in glass ter-
raria (120 cm ×35 cm ×35 cm) without physical nor
visual contact between subjects. The aquarium substrate
was newspapers, changed daily unless more frequently re-
quired. Full-spectrum fluorescent lights (Repti Glo 10.0,
Hagen Inc., Mansfield, MA) were provided, 13 h/day at a
distance of 30 cm from the animals.
Each animal was fasted and water was withdrawn 10 h
prior to barium administration. Survey radiographs were
taken 10 h before barium administration and no radio-
graphic abnormalities were identified. Three mls of barium
105% w/v suspension (Barium sulfate, E-Z-EM Canada
Inc, Lake Success, NY) were diluted with six milliliters of
tap water to obtain a 35% w/v thoroughly homogenized
suspension. Barium was administered to each lizard (15
ml/kg) into the thoracic esophagus using a 10-gauge, 15
cm (6-inch) long stainless steel blunt-tipped feeding tube in-
serted to the level of the sternal xiphoid process. Each lizard
was held vertically with the head up during the administra-
tion of the barium, and maintained in this position for an
additional 30 s postbarium administration. Radiographs
were taken immediately after barium administration, then
15, 30 min, 1, 2, 4, 6, 8, 12, 24, 36, 48, 60, 72, 84, and 96
h after contrast administration. Radiograph times were de-
termined based on a pilot study performed in one bearded
dragon not included in the study. Exposure settings were 54
kV, 160 ms and 5 mAs, with a standard focus-film distance
of 109 cm on the X-ray machine (X-ray Generator, Sedecal
model SHF-310, Sedecal, Buffalo Grove, IL; X-ray Tube,
Toshiba Rotanode model E7239X, Toshiba America In-
formation System Inc., Irvine, CA; Console Global, Sede-
cal model A-6199–01, Sedecal, Buffalo Grove, IL). Each
bearded dragon was positioned with the pelvic limbs ex-
tended caudally and restrained along the tail with ban-
daging material (Red Cross Secure-Comfort Cloth Tape,
Johnson&Johnson, Skillman, NJ). A vasovagal response
was used by applying digital pressure on the closed lids
and eyes for 10 s as described in green iguanas,7to prevent
motion artifact in less cooperative animals. Radiographs
were reviewed with a X-ray/DICOM images viewer (eFilm
2.1, Merge Healthcare, Irvine, CA). Radiographic dorso-
ventral views were taken at each time point. Based on
the pilot study, right lateral views using horizontal beam
were taken only every 12 h, as lateral views did not pro-
vide enough detail for radiographic interpretation for this
species. Lizards were monitored for signs of regurgitation,
diarrhea, and other signs of discomfort including abnor-
mal posture, increased agitation, or tenesmus, during eight
days following barium administration. A large water dish in
which the lizard could drink and soak was reintroduced 72 h
after barium administration. Food, as previously described,
was offered daily starting 96 h after barium administration.
The radiographic study was discontinued four days after
barium administration.
The relationship between the lizard’s weight and the
colon filling time was measured by linear regression and
computed Spearman’s rank correlation coefficient; the cor-
relation between the lizard gender and the colon filling time
was analyzed by a Wilcoxon–Mann–Whitney rank sum test
using a the “R” statistics software. The statistical signifi-
cance was set as P<0.05.15
Results
The radiographs obtained were of excellent quality,
demonstrating each compartment of the gastrointesti-
nal tract with complete filling and good distension. The
bearded dragon gastrointestinal tract is composed of an
esophagus, a stomach, a duodenal bulb, a short small
VOL. 00, NO.0 RADIOGRAPHIC ANATOMY AND BARIUM SULFATE 3
FIG. 1. Anatomy of the digestive tract of a bearded dragon illustrated by a digital image of the ventral view in situ after removal of all non digestive organs
(1A), and radiograph of the tract dissected from the body and filled with barium (1B).
intestine, a cecum, and a colon (Fig. 1A and B). Most
of the gastrointestinal tract organs were confined to the
mid-coelomic region caudal to the heart and liver.
The esophagus traveled dorsally along midline, joining
the stomach to the left of midline. Grossly, the esophageal
mucosa had longitudinal folds, which were visible as ra-
diopaque lines on the radiographs (Fig. 2). The stomach
of all bearded dragons was located on the left side of the
body, elongated longitudinally in a J-shape, as previously
described,16 with the small curvature oriented toward mid-
line (Fig. 3A and B). The cardia was observed as an area of
smaller diameter than the esophagus, craniomedial to the
gastric fundus (Fig. 3C). Rugal folds of the stomach mu-
cosa appeared as radiographic filling defects in the gastric
lumen. Radiographically, the pyloric antrum was visible as
a distinct narrowing of the stomach body, just proximal to
the pylorus. The pylorus was located to the left of midline,
caudomedial to the stomach body (Figs. 3A and B).
The proximal duodenum formed a segmental dilatation,
termed the duodenal bulb in the green iguana (Figs. 3A
and B).7The duodenal bulb emerging from the pylorus
appeared as an enlargement, with its lumen measuring ap-
proximately the same diameter as the pyloric antrum and
narrowing at the entry to the proximal duodenum. After
the duodenal bulb, the duodenum curved toward the left
side of the coelomic cavity, then cranially. After this cranial
curvature, the first intestinal loop following the duodenum
(termed the jejunum in this study) began medially to the
stomach and progressed cranially toward the right, before
a dorsal turn cranio-dorsally to the cecum on the right of
midline (Fig. 1A and B). The following portion of the small
intestine had a small diameter and remained dorsal to the
duodenum and cecum. Following the jejunum, the ileum
was the last transverse intestinal segment before reaching
the cecum (Fig. 4A). The ileum began medially to the stom-
ach and progressed toward the right side of the coelomic
cavity, before connecting cranially to the cecum through a
small diameter ileo-cecal junction (Figs. 1B, and 4A), which
contained a sphincter.
The cecum was very distensible, with a diameter of up
to three times the diameter of the colon, mobile, and vari-
able in shape (Fig. 4B, C, and D). The cecum was located
4GROSSET ET AL. 2014
FIG. 2. Radiographic dorso-ventral view of a bearded dragon 15 min
following gavage of 15 ml/kg 35% w/v barium suspension into the thoracic
esophagus. Contrast in the esophagus provides visualization of esophageal
folds (white arrows). The colon is gas-filled on the right of the coelomic cavity
(black arrows).
cranio-medially to the colon. The appendix of the cecum
was grossly visible, both on the serosal and mucosal surfaces
of the cecum, in the medio-cranial quadrant of the cecum
and measured approximately 5 mm in length (Fig. 4A). The
cecum connected to the colon by a small diameter muscular
junction, approximately 5 mm long, located to the right of
midline (Fig. 4A and B). Grossly, the mucosa of this ceco-
colic junction had longitudinal folds. The colon was a sim-
ple tubular structure oriented cranio-caudally, originating
from the right side of the coelomic cavity and connecting
with the cloaca on midline.
Throughout the study the bearded dragons were ac-
tive and appeared clinically healthy with exception of one
bearded dragon. Retching started two days postbarium ad-
ministration in this lizard and continued throughout the
study. However, no actual vomitus of barium was observed
in this animal. Physical examination and biochemistry re-
sults remained normal. Restraint and barium administra-
tion techniques were well tolerated by every lizard.
In four of the seven bearded dragons, barium was ob-
served in the thoracic esophagus at 15 min following con-
trast administration. In two of these lizards, barium was
also observed in the oral cavity. This was attributed to pos-
sible reflux of the contrast suspension, or alternatively to
tracking of the contrast material as the tube was with-
drawn from the caudal thoracic esophagus. No barium was
expelled out of the mouth of the lizards and no barium
aspiration was identified radiographically.
The location of the barium at the different time intervals
is presented in Table 1 and Figs. 5 and 6. Lateral views
did not provide additional information because the barium
was mostly confined to the region ventral to the lungs and
caudal to the heart, where all the digestive structures were
superimposed in the midcoelom, except the esophagus and
the colon (Figs. 3C, 7A and B). In most lizards, no radio-
graphic changes were observed between 36 and 96 h after
barium administration (Fig. 6). There was no difference in
colon filling time between males and females (P=0.56).
There was no relationship between body weight and filling
time (r=0.22, P=0.64).
On the fourth day following barium administration,
all bearded dragons had a normal appetite, passed fe-
ces of normal appearance, and displayed expected activ-
ity level for the species, including predation, exploration of
their environment,and interaction with care-takers. Barium
defecation was observed 2–5 days after barium ingestion.
However, it was sometimes difficult to distinguish urates
from barium, especially when the animals defecated in
water.
Discussion
Gastrointestinal studies with contrast agents enable de-
tection of foreign bodies, partially to completely obstruct-
ing the digestive tract, intraluminal masses originating from
the digestive tract, delayed gastric emptying, and evalu-
ation of the digestive transit time, which can vary with
core body temperature, food composition, metabolic fac-
tors, such as dehydration or hypocalcemia,3metabolic dis-
eases, and digestive infectious agents.14,17 We described the
normal anatomy and imaging characteristics of the gas-
trointestinal tract of bearded dragons, and established nor-
mal transit times in seven healthy adult bearded dragons
kept in the preferred optimal temperature range for the
species.
Barium sulfate, a noniodinated contrast medium,18 was
chosen in this study because of its excellent quality of con-
trast, its availability to clinicians and because of its inexpen-
sive cost. Alternative contrast mediums previously studied
in reptiles include iodinated water-soluble agents, such as
the ionic high-osmolarity contrast agent18 aminotrizoate
sodium and amidotrizoate megumine (Gastrografin R)10, 13
and the nonionic low-osmolarity contrast agent18 iopami-
dol (Isovue R).12 GastrografinRhas a more rapid tran-
sit time than barium in red-eared sliders, reaching the
large intestine 10 h faster than barium sulfate.13, 17 Al-
though water soluble contrast agents may be chosen in
cases where intestinal perforation is suspected12, 16, 18 po-
tential adverse effects of hyperosmolar agents include
dehydration12, 13, 17 and pulmonary edema if aspirated.18–21
Gastrografin Radministered to red-eared sliders had
VOL. 00, NO.0 RADIOGRAPHIC ANATOMY AND BARIUM SULFATE 5
FIG. 3. Anatomy of the digestive tract of a bearded dragon illustrated by a photograph of the ventral view in situ after removal of the liver only (3A) for
comparison to the radiologic views; dorso-ventral view (3C) of the same animal at 12 h postbarium administration (3B) and right lateral view at 1 h following
gavage of 15 ml/kg of a 35% w/v barium suspension into the thoracic esophagus (3C).
decreased opacity when the contrast reached the colon.13
Since digestive obstructions in bearded dragons can oc-
cur in the distal digestive tract, secondary to renomegaly,
barium was chosen in this study, to obtain high contrast
opacity in the caudal part of the digestive tract.7,13 An-
other alternative in cases of cloacal obstruction would
be to perform cloacography, as described in loggerhead
sea turtles.12 Based on the results of this study, cloacog-
raphy is recommended to investigate a distal obstruction
in bearded dragons due to the delay of approximately 29
h before barium enters the colon. In some cases, barium
was defecated within 12 h after reaching the colon, requir-
ing frequent radiographic imaging to assess the lumen of
the colon. Conversely, barium has been reported to cause
digestive obstruction in chelonians, which is not the case
of water-soluble hyperosmolar agents.4, 10, 13 Barium sulfate
can become desiccated in the digestive tract and result in
digestive obstruction, especially if a large volume of con-
trast medium is used and remains in the digestive tract for
an extended period of time, due to dehydration, or preex-
isting ileus.22 However, digestive obstruction secondary to
barium administration has not been reported in bearded
dragons or in other lizards,7and was not observed in these
animals.
In a previous study performed in red-eared sliders, re-
gurgitation was observed in 43% of the animals follow-
ing rapid administration into the stomach of 8 ml of 30%
w/v barium per kg.13 In these turtles, regurgitation into
the oral cavity was grossly visible during administration of
the barium whereas in our study reflux was only visible
6GROSSET ET AL. 2014
FIG. 4. Comparison between the ventral anatomic view (4A) and the
digital image of the radiologic dorso-ventralviews (4B, 4C, 4D) of the bearded
dragon. On the anatomic image (4A), the cecum has been pulled toward the
right and its ventral surface is exposed; the cecum is full and the ileum
and the colon are empty. Note the varied radiographic appearance of the
ceco-colic junction (black arrows 4B, 4C, 4D) of three bearded dragons 12
h following gavage of 15 ml/kg of a 35% w/v barium suspension into the
caudal esophagus. In 4B the ceco-colic junction is filled with barium, in
4C the ceco-colic junction is not visible, and in 4D the ceco-colic junction
is visible between the cecum filled with barium and the colon. Note the
varied radiologic appearance of the distensible cecum (white arrows 4B, 4C,
4D), which should not be confused with the stomach (not visible on these
radiographic views) when the cecum is displaced toward the left (4D).
radiographically. The same dose was appropriate when the
contrast medium was administered over a period of 20 s.13
In ball pythons, a dose of 25 ml/kg was associated with
regurgitation in four of 18 snakes.8In green iguanas, a dose
of 25 ml/kg of 25% w/v barium resulted in regurgitation
in three out of five animals and a smaller dose was rec-
ommended by the authors.7In the current study, a dose
of 15 ml/kg was elected and provided appropriate disten-
sion of the gastrointestinal tract, despite more than half
of the animals showing reflux into the cranial esophagus.
Some of the contrast appearing in the esophagus could also
be associated with tracking of the contrast material as the
tube was withdrawn from the caudal thoracic esophagus. In
red-eared sliders, a concentration of 30% w/v barium sul-
fate was recommended,13 in ball pythons a concentration
of 35% w/v was preferred compared to either 25% or 45%
w/v,8whereas in green iguanas, a dilution of 25% w/v was
considered more appropriate than nondiluted 105% w/v
barium sulfate.7Similarly, in the bearded dragons of the
study presented here, good quality images of the digestive
tract were obtained with a concentration of 35% w/v, and
excellent distension of each portion of the gastrointestinal
tract was obtained.
The storage compartment located between the small in-
testine and the colon was called the cecum in this study.
To the authors’ knowledge, digestive anatomy of healthy
bearded dragons has not been described in detail previ-
ously. A recent study described bearded dragons’ coelomic
organs, referring to the nomenclature established in green
iguanas.16 However, this study was performed in four
bearded dragons euthanized due to advanced clinical con-
ditions and not in healthy animals.16 The current study
combined anatomic description and radiographic gastroin-
testinal positive contrast information, to identify and con-
firm gastrointestinal tact segments based on their function.
Some discrepancies were observed between our results and
those previously published.16 An “ascending stomach” was
described medial to the gastric fundus, with the pylorus lo-
cated distal to this segment; however in our study, when
combining radiographic and anatomic views, the pylorus
was localized caudal to the gastric fundus, as noted on
Fig. 5. Therefore we would call the previously termed “as-
cending stomach” a duodenal bulb, since it is aboral to the
pyloric sphincter.
In addition, an ascending and a transverse colon were
described in the same study,16 which were not observed
in the bearded dragons of the study presented here. No
cecum was described in bearded dragons in this compara-
tive study about bearded dragons, green iguanas, and black
VOL. 00, NO.0 RADIOGRAPHIC ANATOMY AND BARIUM SULFATE 7
TABLE 1. Barium Contrast Agent Transit Time (h) in the Digestive Tract of Bearded Dragons (n=7) with the Weight (g) and Gender of each Bearded
Dragon Recorded (One Individual per Column and Median in the First Column): Time (h) When Barium First Entered (Arrival, h) and Had
Completely Emptied (Exit, h, If Applicable) each Segment of the Gastrointestinal Tract
Animalnumber: Median1234567
Animal weight (in g) 150 294 256 163 282 262 297
Animal gender N/A M M M F F F M
Oral cavity (arrival, h) N/A 0.25 0
(exit, h) N/A 0.5 0.25
Esophagus (arrival, h) N/A 0.25 000000
(exit, h) 0.68 0.5 0.5 1 0.25 0.25 2 0.25
Stomach(arrival,h) 0 0000000
(exit, h) 10 4 24 6 6 12 6 12
Pylorus (arrival, h) 0.14 0 0 0.25 0.5 0.25 0 0
(exit,h) 9 62466648
Duodenum (arrival, h) 0.4 0.25 0.25 0.25 0.5 0.5 0.25 1
(exit,h) 13 636246648
Jejunumandileum(arrival,h)1.40.5112221
(exit, h) 29 24 36 48 24 24 24 24
Cecum (arrival, h) 10 12 8 12 8 8 8 12
(exit, h) N/A 96 48
Colon (arrival, h) 31 24 24 24 36 24 12 72
and white tegu (Tupinambis merianae) coelomic organs.16
Furthermore, the appendix was not described,16 contrary
to what is reported in the present study (see Fig. 4A).
The gastro-intestinal anatomy of closely related species
has been described, including the common agama (Agama
agama),23 and Uromastyx spp.24 In these species, a cecum
has been described with a homologous position as what
is observed in bearded dragons.23 The tip of the cecum
has been called “appendix”24 and contains individual lym-
phatic follicles.25 Natural diet is not the only predictor
of the occurrence and size of a cecum in reptiles.26,27 In
Iguanidae lizards, a homologous compartment of the di-
gestive tract has been called alternatively “large colon,”7,28
or “cecum.”23 In lizards, the cecum histologic morphology
is thought to be identical to the histologic morphology of
the colon,25 therefore the designation of the storage com-
partment is a convention. In the eleven bearded dragons in
this study, the distension of the compartment cranial to the
colon was highly variable and its diameter was sometimes
the same as the diameter of the colon. Therefore it was des-
ignated as the cecum in this study. Whether fermentation
occurs in the bearded dragon cecum is beyond the scope
of this study, however contrast was stored in the cecum for
up to 96 h (Table 1). It is relevant to know that the ce-
cum can be highly distensible and mobile in the coelomic
cavity, and the cecum should not be mistaken for a dila-
tion of the digestive tract proximal to an obstruction. Most
of the Iguanidae lizards display one to eleven transversal
valves in their proximal colon.29 Some lizards of the family
Aguamidae, such as Agama stellio,Gonyocephalus sp. and
Physignathus leseuri do not have any colic valves,23 which
was also the case in bearded dragons. Conversely, the lizards
of the genus Uromastyx sp., which belong to the Agamidae
family, display colic partition.23
In reptiles, barium gastrointestinal transit is influenced
by environmental temperature,7exercise, health status, diet
items,17,29 and the stage of digestion.8In this study, lizards
were fasted for 106 h, beginning 10 h before barium ad-
ministration. This experimental protocol was intended to
reduce individual variability due to variable food inges-
tion, and to reproduce the common clinical situation for
a bearded dragon presented with anorexia. Recommended
feeding frequency for adult bearded dragons varies between
once a day to twice a week,1therefore a four and a half-
day fasting period was considered compatible and within
the range of the species normal captive husbandry recom-
mendations. In previous studies in green iguanas, food, and
water were available at all times, which made the interpre-
tation of the study results challenging for application to ill
lizards.7
Bearded dragon gastric emptying time was 10 h in this
study, which is similar to the green iguana,7however the in-
dividual variability was higher in bearded dragons, respec-
tively, 4–24 h vs. 6–12 h in iguanas.7In comparison leopard
geckos have been shown to keep mealworms for up to 52
h in their stomach.30 Compared to the green iguana that
displays a U-shaped stomach centrally positioned,7, 28 the
stomach of bearded dragons was J-shaped and was lateral-
ized on the left coelomic cavity as previously described.16
In some cases when the stomach did not contain any bar-
ium, the cecum could easily be confused as the stomach
(Fig. 4D). However, the stomach was always more lateral
than the cecum on the left side of the coelomic cavity. Given
the small diameter of this sphincter and the normal disten-
sion of the cecum, this could be misinterpreted as a partial
obstruction of the digestive tract when reviewing radio-
graphs, but it is anatomically normal in bearded dragons.
In addition, the ceco-colic junction was free of barium in
8GROSSET ET AL. 2014
FIG. 5. Contrast-enhanced dorso-ventral radiographic images and asso-
ciated schematic drawings of bearded dragons immediately following gavage
of 15 ml/kg of a 35% w/v barium suspension into the caudal esophagus to
12 h postadministration.
most of the views and should not be mistaken for a foreign
body.
In bearded dragons, time for barium to reach the duo-
denal bulb was longer, that is 15 min, compared to im-
mediately after contrast administration in green iguanas.7
Jejunum transit time was quicker in the bearded dragons
from this study than in green iguanas, respectively, 1.4 h
vs. 4 h. Small intestine emptying time was almost twice
as long in bearded dragons (median 29 h) compared to
green iguanas (median 16 h).7This could be due to the
different gastrointestinal anatomy or differences in natu-
ral dietary requirements between the green iguana and the
bearded dragon, with the cecum having a storage function
in bearded dragons, or it could be associated with fast-
ing the bearded dragons in this study whereas the green
iguanas had access to food.7However, this should not
have affected the gastric emptying time because gastric
tone is generally unchanged during the fast.31 Overall, lit-
tle information was gained from lateral views in healthy
bearded dragons, however, these additional views may be
helpful in diseased lizards to visualize and characterize a
potential lesion. Bearded dragon and green iguana gas-
trointestinal transit times appear to be different, which
would be expected since they belonging to distinct lizard
families, that is Iguanidae and Agamidae, which differ by
many anatomic features.32 Moreover green iguanas and
bearded dragons have different husbandry and dietary re-
quirements, adult bearded dragons being omnivorous1and
green iguanas being herbivorous from birth.31, 33 Gastroin-
testinal transit time in carnivorous lizards species has been
reported to be shorter than in herbivorous species.17 Ju-
venile bearded dragon are more omnivorous than adults,1
therefore results obtained from our study may not apply to
younger animals eating more insects. In addition, bearded
dragons originate from arid to semi-arid environments in
Australia,1whereas green iguanas come from more humid
environments in America.33 Green iguanas tend to favor
food items with high water content, such as flowers, dur-
ing dry season, whereas vegetables higher in protein are
consumed during rainy season.29 Various food items have
been shown to be associated with various transit times.29
Whether longer transit time in bearded dragon is associated
with increased water reabsorption would require further in-
vestigation. Similar study design with fasted animals would
be necessary to accurately compare gastrointestinal transit
of various lizard species and ages.
Interindividual variability was observed among bearded
dragons (Table 1), although care was taken to standardize
the ambient temperature. Interindividual variability was
not associated with the gender of the lizard and the transit
time did not correlate with the body weight of the ani-
mals. This may have been due to physiologic causes or to
various gastrointestinal digestive phases when the study
was started, although the lizards were fasted for ten hours
VOL. 00, NO.0 RADIOGRAPHIC ANATOMY AND BARIUM SULFATE 9
FIG. 6. Contrast-enhanced dorso-ventral radiographic imagesfrom a bearded dragon 24–96 h following gavage of 15 ml/kg of a 35% w/v barium suspension
into the caudal esophagus (* =cecum, C =colon). Three views were selected during the time period because of the lack of progression of the contrast medium.
FIG. 7. Contrast-enhanced right lateral radiographic images of a bearded
dragon: 12 h (7A) and 96 h (7B) after gavage of 15 ml/kg of a 35% w/v
barium suspension: the cecum (black arrow) and colon (white arrow) are
visible on lateral views.
prior to the study. Interestingly, various distribution pat-
terns have also been observed in ball python fasted for
seven days prior to a digestive contrast study.8In leop-
ard geckos, total transit time also varied between 49 and
219 hours in lizards fed the same mealworm diet.30 Vaso-
vagal response has been suspected to influence digestive
transit due to its effects on autonomic nervous system,
but this assumption has not been demonstrated in a con-
trolled study.7A restraint method using cotton balls held in
place with a bandage around the head to apply continuous
pressure on the eyes was not used in the current study to
minimize possible influence on the gastrointestinal tract. In
this study, pressure on the lizards’ eyeballs was performed
for approximately five to ten seconds, if necessary to posi-
tion for a radiograph. Therefore we do not expect this very
rapid vaso-vagal response to have significantly influenced
the results. Moreover, in a clinical situation where the pa-
tient is not sedated or anesthetized, this method could be
used and the radiographs compared to the results of the
present study.
Conclusion
Barium administration at a dose of 15 ml/kg by gavage in
the thoracic esophagus in seven fasted bearded dragons was
appropriate to study gastro-intestinal transit time for 96 h
postcontrast administration and to evaluate the bearded
dragon gastrointestinal anatomy in detail. Inter-individual
variability was observed, therefore a possible limitation of
this study is the low number of animals included, however,
reference intervals for gastric transit were similar to a study
reported in adult green iguanas. Intestine emptying time
was longer in this bearded dragon study than in green igua-
nas, which is likely due to different anatomy, dietary and
husbandry requirements between the two species although
various study designs may have accounted for part of the
differences observed. No significant adverse clinical signs
were observed following barium the gastrointestinal con-
trast study. Therefore this technique appears both safe and
informative to evaluate the gastrointestinal tract of bearded
dragons.
ACKNOWLEDGEMENTS
The authors thank Dr. Kate Gustavsen, for her help regarding the sta-
tistical analysis, the technicians of the Small Animal Radiology Ser-
vice for their technical assistance, especially Michele Santoro, Linda
Savely, and Jennifer Lazzari, and the technicians of the Companion
Avian and Exotic Pet Medicine Service of the University of California-
Davis, especially Kristina Palmer-Holtry, Stacey Zindel, Sheri
Pendergraft, Nikki Reid for their logistical assistance and Delphine
Grosset, Visual Communication Conception Creator, for her assistance
with Fig. 5 drawing.
10 GROSSET ET AL. 2014
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The present work is the first in a series of studies aiming at establishing a connection between the food habits of aves and the anatomical, histological and histochemical structures of their alimentary canal. In this study the gross anatomy, histology and histochemistry of the alimentary canal of common quail, Coturnix coturnix, a granivorous bird, have been investigated. This study revealed that, the oesophagus is not ably long with a well developed crop; thus stomach is differentiated into a glandular proventriculus and a muscular ventritculus or gizzard. The gizzard is much more developed having a thick hard cuticle, its wall consists of two strong smooth muscles, the small intestine is divided into duodenum, jejunum and ileum and the transition from the jejunum to ileum is indicated by the vitelline (Meckel's) diverticulum, and the ileum was the longest part of the small intestine. The large intestine consists of paired well developed caeca and a short rectum. The present histological studies revealed that the alimentary tract showed the usual four laminae: serosa, musculosa, submucosa and mucosa. The oesophageal mucosa of the quail was thrown into numerous longitudinal folds. The mucosa of oesophagus is lined with stratified squamous epithelium. The proventricular glands are simple tubular to simple branched tubular glands. The mucosal surface of the ventriculus is indented by deep, broad crypts into which simple to branched tubular gastric glands open. A thick gastric keratinoid material covers the mucosa of the ventriculus. The intestinal mucosa is thrown into intestinal villi which show a marked variation in density, shape and size in the different regions of the intestine. The goblet cells gradually increase in frequency from the duodenum to the rectum. Also, the histochemical study revealed the existence of a high amount of mucopolysaccharides in the oesophageal glands, PAS and Alcian blue positive mucin granules as well (neutral and acid mucin, respectively). The ventriculus mucosa is covered by a thick keratinized laminated layer of koilin membrane which is formed of proteinous material similar to keratin and stained positive for PAS and Alcian blue indicating the presence of neutral and acid mucin within its contents. The proventriculus mucosa shows folds lined by simple columnar cells containing PAS and Alcian blue positive mucin granules. The goblet cells and crypts of Lieberkühn have acid and neutral mucopolysaccharide secretions and the luminal surface of the columnar cells and the lamina propria of the intestine contains proteins.