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Diagnosticimagingof Reproductivetract Disordersinreptiles: Michaela Gumpenberger
Diagnosticimagingof Reproductivetract Disordersinreptiles: Michaela Gumpenberger
R e p ro d u c t i v e Tr a c t
D i s o rd e r s i n R e p t i l e s
Michaela Gumpenberger, Dr med vet
KEYWORDS
Reproductive tract Radiography Ultrasonography Computed tomography
Chelonian Snake Lizard Reptile
KEY POINTS
Radiographs serve as a cheap and widely available imaging tool for getting an overview of
the general condition in reptiles. Mineralized egg shells are differentiated in most species.
Sonography allows the evaluation of the whole reproductive tract in lizards and snakes;
however, the examination of chelonians is limited by the shell.
Computed tomography is the perfect imaging tool for the visualization of all organ systems
in chelonians.
Diagnosis of dystocia should always be supported by diagnostic imaging, especially in
chelonians where the shell hampers proper palpation.
Diagnostic imaging of the reptilian reproductive tract may be helpful for determining
gender (particularly in monomorphic species),1 for evaluating the breeding status,2
for finding pathologic conditions, and for supervising treatment.3 This article demon-
strates the most commonly used imaging techniques, including their advantages and
disadvantages (Table 1). Physiologic appearance and pathologic findings of male and
female reproductive tract are described and illustrated.
Table 1
Comparison of the value of radiography, sonography, and plain computed tomography in
differentiating various reproductive conditions
Lizards, Iguanas,
Chelonians, Turtles Chameleons Snakes
RX US CT RX US CT RX US CT
Ovary 0 1 11 0 1/11 1/11 0 1 1
Follicles, eggs with 0/1 11/111 111 11 111 111 1/11 111 111
noncalcified shells
Eggs, poorly 11 111 111 11 111 111 11 111 111
calcified shells
Eggs, well- 111 1 111 111 11 111 111 111 111
mineralized shells
Salpinx 0 1/11 111 0 1 1 0 0/11 n.i.
Testes 0 11 1/11 0 1/11 1/11 0 1 n.i.
main interest for diagnosing respiratory tract disorders. Lateral views in turtles should
be performed in horizontal view to minimize organ displacement and to ensure sym-
metric views. The animal is placed on a wooden block or a paper box for proper posi-
tioning (Fig. 1A). Small lizards should be done in a similar way, but rather be confined
in a radiolucent box (Fig. 1B). Manual restraint in tiny species might hurt the patient
and result in compromised images because of superimposition. Chameleons may
be offered a kind of (preferably radiolucent) perch (Fig. 1C, D). For larger lizards and
snakes either horizontal or vertical beam imaging is applied. Usually large lizards
are restrained and positioned in a similar way to dogs or cats.4
One disadvantage of radiology is artifacts caused by superimposition. This can at
least to some extent be overcome by always performing two radiographs in perpen-
dicular directions. Restricting oneself to only one view results in considerable loss
of information (discussed later).
Another disadvantage in reptile radiography is the lack of coelomic fat between the
organs. Therefore differentiation of ovaries, follicles, or testes is difficult or even
completely impossible, especially in chelonians. Mineralized egg shells are usually
defined when proper imaging techniques are used. Superimposition of the shell ham-
pers the visualization of eggs with poorly mineralized shells, especially in underex-
posed images. The easily applicable digital radiography might tempt to an
excessive use of milliampere and/or kilovolt to overcome this problem, which is
certainly unacceptable for reasons of radiation protection.
Sonography
Sonography may be used more often in diagnosing reproductive disorders than radi-
ography, particularly in snakes and lizards (eg, iguanas).5 The main advantage of so-
nography is the possibility to evaluate the inner architecture of soft tissues.
Sonography is therefore a perfect supplement to radiography.3 Although radiographs
serve the purpose of being documents that are evaluated anytime, sonographic diag-
noses are made during the examination of patients. Even if videos are taken it is diffi-
cult to form a trustworthy second opinion about somebody else’s images. Thorough
training and detailed knowledge of different species and their sometimes unique anat-
omy are therefore prerequisites for performing sonography.
Imaging of the Reproductive Tract in Reptiles 329
Transducers should always feel comfortable for the examiner. In general, microcon-
vex transducers with a high frequency (7.5–12 MHz) and superior spatial resolution are
the best choice for smaller turtles up to 5 kg body weight, whereas larger species may
require convex or linear transducers (3.5–5 MHz). The frequency depends on actual
patient size and the organ of main interest. Sonography in turtles is usually performed
through the natural shell openings (mediastinale, axillary, and inguinal window) but can
sometimes be performed through the shell, when the plastron lacks proper minerali-
zation. Most aquatic species have large inguinal windows (also known as prefemoral
fossa) so that the genital tract is more easily accessible.
Lizards and snakes are usually scanned with high-frequency linear transducers (the
author still prefers a microconvex transducer). Images do not need to be “pretty,” but
should rather be diagnostic. Hence there is hardly a restriction in transducer choice.
Sometimes the use of several transducers in one animal is legitimate to achieve
desired results.
It is crucial to aim for good transducer-skin contact in all sonographic examinations,
which is achieved by the use of sonographic gel. Dysecdysis may compromise sono-
graphic imaging as soon as gas is entrapped between transducer and skin. This is
330 Gumpenberger
partially overcome by soaking the patient in warm water. However, performing sonog-
raphy during soaking often results in undesirable movements and splashing as soon
as the animal starts to struggle and is therefore considered less advisable.
A simple stand-off pad, made from a gel-filled finger of an examination glove, can be
helpful for sonography performed via the prefemoral window in turtles (Fig. 2A). In tiny
patients the stand-off pad is also useful for obtaining proper imaging of superficial or-
gans whenever an adequate high-frequency transducer is not available. In general, all
patients are restrained only as much as necessary and in the most comfortable way
possible (Fig. 2B, C).
Computed Tomography
Computed tomography (CT) is a radiographic, cross-sectional imaging method that
overcomes superimposition artifacts of plain radiographs. Reading CT images is
comparatively easier to learn than reading MR images , because the different tissue
densities resemble those of radiographs. Some advantages are the opportunity to
do multiplanar and three-dimensional reconstructions, volumetry, densitometry, or vir-
tual endoscopy. CT examinations are admittedly more expensive than radiography or
sonography and require special equipment and premises. That is why CT is still not
available for all veterinarians. Nevertheless, if available and used in complement to
radiography and sonography valuable information is gained that leads to a better un-
derstanding of all imaging techniques.
Usually chelonian species need no anesthesia. Lizards and snakes are restrained in
cardboard boxes and plastic rolls. For rapid multislice CT machines, sedation is
increasingly dispensable. In general there is no need for intravenous contrast media
application for further evaluation of the reproductive tract. If needed a dosage of
600 mg iodine/kg body weight should be administered intravenously.6
MRI
In general all soft tissues can be evaluated perfectly with MRI. Because of their
different signal even their quality is evaluated further. T2-weighted images highlight
fluid and are therefore often addressed as “pathology scans,” whereas T1-weighted
images offer further details on anatomy in which fluid appears hypointense and fat
hyperintense. Variations of these sequences help to differentiate between liquor, hem-
orrhage, and plain cysts. Solid bone and air appear in all sequences dark without a
signal. Because MRI examinations are easily depreciated by movement artifacts,
sedation is usually necessary.
Fig. 2. Sonographic examination of a (A) Hermann’s tortoise (Testudo hermanni) and (B, C)
two Bearded dragons (Pogona vitticeps). The examiner tries to place the patient in a most
convenient and physiologic position. (A) A simple stand-off pad, made from a gel-filled
finger of a glove, is used to achieve optimal skin contact within the prefemoral window.
(Courtesy of Michaela Gumpenberger, Dr med vet, Austria.)
Imaging of the Reproductive Tract in Reptiles 331
Although the author has access to MRI, all diagnoses are perceived to be gained
much faster with CT for the reproductive tract in reptiles (sometimes complemented
with sonography). Because MRI examinations are more time consuming, require
sedation, and are much more expensive, the author’s clinic prefers other imaging
methods for diagnosing reproductive tract disorders.
Fig. 3. Sonography of testes (T) of a (A) Hermann’s tortoise (Testudo hermanni, sagittal
view) and a (B) Bearded dragon (Pogona vitticeps, transverse view, comparing left and right
organ). The spherical to oval testicles have a homogenous parenchyma. (Courtesy of Mi-
chaela Gumpenberger, Dr med vet, Austria.)
332 Gumpenberger
Fig. 4. Lateral radiograph of an adult female Red Eared Slider turtle (Trachemys scripta el-
egans). The lung fields are narrowed. The borderline between the lung and the other
coelomic organs has risen to caudally (arrows). A vast number of follicles was identified so-
nographically as cause. (Courtesy of Michaela Gumpenberger, Dr med vet, Austria.)
follicles and eggs may be differentiated as roundish or oval soft tissue opacity objects,
often accumulating in a grapelike manner in lizards.8,9 Mineralized shells should
appear of similar shape, size, and density in one clutch, although number, size, shape,
and shell density are species-dependent (Fig. 5). For example, Box turtles produce
exceptionally large eggs. Tortoises have radiographically denser shells than most
aquatic species. However, the shell of the two large eggs (in comparison with body
size) is hardly visible in leopard geckos (Fig. 6). A clear visibility of the shell indicates
dystocia in these geckos.4
The visibility of poorly mineralized egg shells in chelonians significantly depends on
proper image settings. If the shell is not penetrated on dorsoventral views, the thin
shells cannot be differentiated (see Fig. 5A). Differentiation of follicles or thin-shelled
eggs on radiographs of lizards and snakes is easier due to lack of a bony shell.
Fig. 5. Dorsoventral radiographs of two Hermann’s tortoises (Testudo hermanni). (A) Two
thin-shelled eggs that are barely visible (arrows). (B) On a follow-up examination 5 days
later those eggs are not fully but better mineralized. The shell is mildly demineralized. (C)
Shell and skeleton are perfectly mineralized in another individual. Five fully mineralized
eggs of similar shape and size are visible. Radiographically the clutch appears normal
(and was delivered on the next day). (Courtesy of Michaela Gumpenberger, Dr med vet,
Austria.)
Imaging of the Reproductive Tract in Reptiles 333
Fig. 6. Dorsoventral (A) and lateral (B) radiograph of a Leopard gecko (Eublepharis macular-
ius) showing relatively poor mineralization of the skeleton. Nevertheless, two thin shells are
visible (arrows), partially superimposed by ingesta and some radiopaque material of un-
known origin (there was no history of contrast media application). This female showed dif-
ficulties in delivering the eggs, which might be caused by mineral imbalances. (Courtesy of
Michaela Gumpenberger, Dr med vet, Austria.)
Fig. 7. Coronal CT in soft tissue window of a Bearded dragon (Pogona vitticeps) at the level
of the ovaries. Unremarkable, hyperdense follicles (asterisks) with a less dense center are
visible. The animal suffered from obstipation, which was not related to the follicles. (Cour-
tesy of Michaela Gumpenberger, Dr med vet, Austria.)
334 Gumpenberger
Fig. 8. Coronal CT in soft tissue window of a Hermann’s tortoise (Testudo hermanni). Several
normal-shaped eggs of unremarkable density and structure are present. The liver (L) is
mildly enlarged (not clearly seen at this level) and shows decreased density (lipidosis). (Cour-
tesy of Michaela Gumpenberger, Dr med vet, Austria.)
than 2.2–2.4 cm are prone to ovulation).10 Premordial follicles may undergo atresia.
Then they become heterogenous with hypoechoic to anechoic zones.10 As soon as
follicles are ovulated they are hyperechoic and tend to elongate, especially in lizards
and snakes.8 A small peripheral anechoic rim is built, representing the albumen (see
Fig. 9E). A poorly mineralized shell appears as curvilinear echoic thin line. The better
mineralized the shell the more hyperechoic it becomes (see Fig. 14A). Well-
mineralized shells even cause distal shadowing, depending on species and grade
of mineralization. Then the albumen and yolk can no longer be differentiated and
the eggs superimpose each other in sonography. Therefore using sonography, espe-
cially in chelonians, it is impossible to count the eggs or give proper information
about their position. Visibility of follicles or eggs in chelonians not only depends on
the size of the inguinal acoustic window, but also on bowel loop contents and, espe-
cially in larger individuals, on the cooperation of the patient. Radiography and CT are
less or not at all hampered by the previously mentioned circumstances. However, so-
nography can easily detect cardiac action in fetus in viviparous snakes (Fig. 10) and
lizards.
Depending on the species and developmental status horizontal and concentric
layering of various intensities is observed in follicles and eggs in reptiles in MRI.
The preovulatory follicles of lizards appear hyperintense in T2-weighted
sequences. In case of eggs, the albumen appears hyperintense, the yolk hypoin-
tense, and the calcified shell very hypointense in T2-weighted sequences,
whereas in T1-weighted images the yolk appears of similar intensity as
muscle.3,11
Imaging of the Reproductive Tract in Reptiles 335
Salpinx
The salpinx cannot be visualized radiographically, but it is clearly seen as a narrow
folded, tubular, hyperechoic or hyperdense structure in the caudal part of the shell
in turtles in sonography and CT, respectively (Fig. 11). In lizards and snakes it is hardly
visible when nonaffected and not filled with fluid.
Fig. 10. Sonographic images of various breeding status in snakes. (A) Small hypoechoic fol-
licles (F) are present on the normal ovary in a Tiger python (Python molurus). (B) Normal egg
with a barely distinguishable shell (arrows) and hyperechoic contents of a Tiger python (P
molurus). Measuring points indicate the size (4.7 3 cm). (C) A hockey-stick linear trans-
ducer was used for this examination. The vertebrae and spine (arrows), surrounded by
soft tissues, of a fetus in a Garter snake (Thamnophis sirtalis) are visible. In live view the
heartbeat proved this animal to be alive. (D) In the dead fetus inside a Dumeril boa (Acran-
tophis dumerili) there is no need to find a heartbeat because of the obviously degenerated
status. (Courtesy of Michaela Gumpenberger, Dr med vet, Austria.)
Fig. 11. (A) Sonography of a Red Eared Slider turtle (Trachemys scripta elegans). The hyper-
echoic follicle (F) measures more than 2.4 cm in diameter and may ovulate soon. Distal
shadowing is present, which is typical for large follicles in chelonians. Right next to the
follicle some part of the unremarkable urinary bladder is visible. In the near field the hy-
perechoic, tubular, serpentine salpinx (S) is seen. (B) Right lateral sagittal CT in soft tissue
window of a Hermann’s tortoise (Testudo hermanni), the head is to the left. Small hyper-
dense follicles (f) and large ones with a hypodense peripheral rim (F) are present. The sal-
pinx is a hyperdense tubular structure folded between them (S). (Courtesy of Michaela
Gumpenberger, Dr med vet, Austria.)
Imaging of the Reproductive Tract in Reptiles 337
Fig. 12. Lateral (A) and dorsoventral (B) radiograph of a Hermann’s tortoise (Testudo her-
manni). One egg has already entered the pelvis but could not pass the shell opening. This
is only seen on the lateral radiograph. Another indication for dystocia is the different den-
sity of the shells; the egg that got stuck in the cloaca has a much denser shell than the other
eggs. (Courtesy of Michaela Gumpenberger, Dr med vet, Austria.)
Fig. 13. (A) Dorsoventral radiograph of a Corn snake (Pantherophis guttatus). The egg posi-
tioned at the cloaca (arrows) seems a little bit larger than the others. Moreover, a swelling
was found at the cloaca during physical examination, most likely responsible for the
dystocia. (B) Lateral radiograph of a Mandarin Rat snake (Euprepiophis mandarinus) that
was pregnant with a single egg (arrows) and showed symptoms of dystocia. (Courtesy of
the Section of Reptiles and Birds, Vetmeduni Vienna, Austria.)
338 Gumpenberger
Fig. 14. Sonography of a Red Eared Slider turtle (Trachemys scripta elegans) (A) and a
Hermann’s tortoise (Testudo hermanni) (B). Two eggs (E) of the Red Eared Slider turtle are
clearly positioned outside of the urinary bladder (UB). Even a thin bladder wall is visible.
In (B) shell fragments (arrows) are present within the urinary bladder. This egg-
displacement was caused by improper manual therapy resulting in shell fracture and in addi-
tional pneumoperitoneum and peritonitis, which was fatal for the patient. Compare with
Fig. 15A, B. Note that in a poorly mineralized shell the yolk (hyperechoic) and albumen (hy-
poechoic) are seen (A). The shell is represented by a thin hyperechoic curvilinear reflex (A).
As soon as the shell is fully mineralized only the surface of the shell is visualized (B). (Cour-
tesy of Michaela Gumpenberger, Dr med vet, Austria.)
Fig. 15. Transverse (A) and sagittal (B) CT of a Hermann’s tortoise (Testudo hermanni), modi-
fied soft tissue window. The animal is suffering from dystocia. The shell and skeleton show
poor mineralization and deformation. One egg shell (E) is severely deformed and positioned
within the urinary bladder (UB). Another shell is obstructing the pelvis and has a mildly
thickened shell and a gas cap (not visible in these levels). Compare with Fig. 14A, B. (Cour-
tesy of Michaela Gumpenberger, Dr med vet, Austria.)
Fig. 16. Transverse CT (soft tissue window) in the middle of the coelomic cavity of a 60-year-
old Spur-thighed tortoise (Testudo graeca). Multiple follicles (F) of various sizes and
densities cause severe lung compression. Some show horizontal layering with a hypodense
dorsal cap. The connective tissue in between the follicles is hypodense with irregular hyper-
dense areas, indicating coelomitis. Surgery proved severe follicular stasis with peritonitis
and multiple adhesions. (Courtesy of Michaela Gumpenberger, Dr med vet, Austria.)
Imaging of the Reproductive Tract in Reptiles 339
Fig. 17. (A) Transverse CT image (soft tissue window) of a Hermann’s tortoise (Testudo her-
manni). A normally calcified shell with an unremarkable yolk is seen. A tiny dorsal gas cap
suggests dystocia (asterisk). Adjacent to the egg some follicles (F) are visible. One small fol-
licle (f) shows a hypodense peripheral rim indicating atrophy. (B) Sagittal CT image (bony
window) of another Hermann’s tortoise. A thickened egg-shell (being denser than the skel-
eton) with a rough spiculated surface is positioned within the pelvis. The egg is wider than
the maximal diameter of the shell opening near the cloaca. Chronic dystocia is not only indi-
cated because of the egg-shell formation but also by the loss of proper egg contents, a gas
cap within the egg-shell, and multiple gas pockets around the egg-shell. Surgery proved se-
vere inflammation and adhesion of the egg-shell to the oviduct (compare Fig. 22). Note the
thickened heterogenous shell and the pyramid-shaped neural bony plates indicating long-
standing mineral imbalances and improper feeding and keeping. (Courtesy of Michaela
Gumpenberger, Dr med vet, Austria.)
Fig. 19. Dorsoventral (A) and lateral (B) radiograph of a Green iguana (Iguana iguana) Mul-
tiple soft tissue–dense oval structures (E) indicate pregnancy. Poor serosal detail would be
normal under these circumstances. Sonographic examination (C) of the same animal shows
normal, thin-shelled eggs, causing some distal shadowing surrounded by free fluid (FF). As-
cites in combination with typical clinical symptoms led to the diagnosis of dystocia. (Cour-
tesy of Michaela Gumpenberger, Dr med vet, Austria.)
several layers may appear, depending on the duration of the disorder. Retained folli-
cles often become friable and can rupture, leading to egg yolk coelomitis.13 Free fluid
is therefore an indicator for aggravation of the process (Fig. 21). In the post-ovulatory
stage the ova should appear more elliptical and of increased echogenicity.3,9,14 Ac-
cording to the author’s experience, these two conditions may sometimes be difficult
to differentiate. Actually, no matter if there is a preovulatory or postovulatory follicular
stasis, surgery is usually the therapy of choice.
Salpingitis
In rare circumstances one may be able to identify a fluid-filled salpinx in sonography
(Fig. 22) or CT (or MRI if used) that is most likely caused by salpingitis. An inflammation
Fig. 20. Sonography of follicles and eggs in various Bearded dragons (Pogona vitticeps). (A)
Normal, hypoechoic, mildly layered, seemingly ovulated follicles. (B–D) Cases suffering from
follicular stasis that were proved surgically. Mild peritoneal effusion is present (arrows in C).
(D) Different densities and sizes of layered follicles. (Courtesy of Michaela Gumpenberger,
Dr med vet, Austria.)
Imaging of the Reproductive Tract in Reptiles 341
Fig. 21. Lateral radiograph (A) and sonography (B) of a Bearded dragon (Pogona vitticeps).
Ascites may be better seen on horizontal lateral radiographs than on dorsoventral views.
Note the small and compressed lung fields (L). The abdominal organs appear as a broadened
homogeneous soft tissue density. Sonographically the easily detectable fluid (FF) surrounds
the layered, hyperechoic ova, which appear mildly oval and deformed. Although the shape
and inner architecture of the ova already indicate follicular stasis, the ascites (especially
when containing hyperechoic particles) is indicative for an inflammatory process most of
the time. In addition, the appearance of the follicles has hardly changed in several
follow-up examinations whereas ascites has progressed. (Courtesy of Michaela Gumpen-
berger, Dr med vet, Austria.)
Fig. 22. Sonographic image of the same animal shown in Fig. 17B. The right salpinx (S) is
fluid filled, indicating salpingitis. It is differentiated from the bowel loops because of posi-
tion and different wall-layering. A hyperechoic egg shell with multiple spicules (arrows) is
seen in the far field. (Courtesy of Michaela Gumpenberger, Dr med vet, Austria.)
342 Gumpenberger
or firm manual palpation (especially in snakes) may cause rupture of the oviduct, which
can lead to egg yolk coelomitis.13 In sonography free fluid additionally to degenerated
follicles and eggs is seen. In CT the contours of follicles and eggs may become
blurred. The connective tissue appears heterogenous and often of increased density
(see Fig. 16).
SUMMARY
CT provides the most thorough information of the reproductive tract in chelonian spe-
cies. The salpinx and all reproductive products can clearly be seen. Nevertheless, ra-
diographs are much easier and cheaper to obtain and therefore remain the preferred
first choice imaging technique for a first overview. In lizards and snakes sonography
seems to be the most appropriate imaging technique. Being quick and noninvasive,
it enables satisfying diagnoses and can be applied anywhere, whereas radiography
and CT are restricted to dedicated locations. Still, more experience is needed to
correctly interpret sonographic images with the additional difficulty of getting second
opinions on found diagnoses.
ACKNOWLEDGMENT
The author thanks the team of the Section for Reptiles and Birds of the Clinical
Department for Small Animals and the team of the Department for Pathology and
Forensic Medicine of the University of Veterinary Medicine in Vienna (Vetmeduni
Vienna), Austria for their great cooperation and support.
REFERENCES
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patterns associated with the reproductive cycle in female veiled chameleons
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in reptile medicine & surgery. 1st edition. St Louis (MO): Elsevier Saunders; 2014.
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