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Ultrasonographic imaging of loggerhead sea turtles (Caretta caretta)

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Papers & Articles

Ultrasonographic imaging of loggerhead sea

turtles (Caretta caretta)
A. L. Valente, M. L. Parga, Y. Espada, S. Lavin, F. Alegre, I. Marco, R. Cuenca

Twenty live and five dead juvenile and subadult loggerhead sea turtles were examined ultrasonographically.
Ten soft tissue areas of the integument were used as acoustic windows: cervical-dorsal and cervical-ventral,
left and right cervicobrachial, left and right axillary, left and right prefemoral and left and right postfemoral
windows. Anatomical cross-sections were performed on the dead turtles to provide reference data. The
fourth and fifth cervical vertebrae, the spinal cord, and the venous sinuses of the external jugular vein
were clearly visible through the cervical-dorsal acoustic window, and the oesophagus and the heart were
imaged through the cervical-ventral acoustic window. The stomach was more frequently visible through the
left axillary acoustic window. The liver could be imaged through both sides, but the right axillary acoustic
window was better for visualising the gall bladder. The large and small intestines and the kidneys were
visible through the right and left prefemoral acoustic windows; the kidneys were easily identified by their
intense vasculature.

THE loggerhead sea turtle (Caretta caretta) is the MATERIALS AND METHODS
most common species accidentally captured by fisheries
in the western Mediterranean Sea. Juvenile and subadult A total of 25 loggerhead sea turtles with minimum straight
animals are those most often captured. According to the carapace lengths ranging from 26·0 to 58·5 cm and weigh-
IUCN (2004) the species is listed as endangered (EN A1abd), ing 3·5 to 26·8 kg were used; 20 of them, eight juveniles and
and it is estimated that more than 20,000 subadult log- 12 subadults, were alive and used for the ultrasound examin-
gerhead sea turtles are captured accidentally every year ations, and five dead juvenile turtles were used to provide
along the Spanish Mediterranean coast (Aguilar and Pastor the anatomical information. The turtles were measured by
1995). The captured turtles are usually released back to the the techniques described by Bolten (1999); turtles with a
sea with a fish hook still in place, and it is estimated that
between 20 per cent and 30 per cent of them may die as
a result of the lesions caused by the hook (Aguilar and Cervical dorsal (A)
Pastor 1995). The main reason for sea turtles to be admit-
ted to rescue centres is the ingestion of fishhooks; other
reasons include lesions caused by entanglement in fishing Cervical ventral (B)
nets, collisions with boat propellers and the ingestion of
garbage. As in other chelonian species, the shell severely
limits the examination of the internal organs, and any diag- Cervicobrachial (C)
nosis based only on a clinical examination is usually very
poor.
Ultrasonography is well established as a rapid, non-
invasive and inexpensive method for assessing soft tis-
sues, and it can therefore be useful for clinical diagnosis
in the rehabilitation of turtles. Its main disadvantage is Axillary (D)
the lack of established ultrasonographic standards for sea
turtles. Although general considerations for ultrasound Veterinary Record (2007)
in reptiles were found in some wildlife medicine books Prefemoral (E)
161, 226-232
(Jackson and Sainsbury 1992, Silverman and Janssen 1996,
Whitaker and Krum 1999, Wilkinson and others 2004) A. L. Valente, DVM, MSc,
and papers (Sainsbury and Gili 1991, Gaudron and others S. Lavin, DVM, PhD,
2001, Schumacher and Toal 2001), few of them systemati- I. Marco, DVM, PhD,
cally describe the normal appearance and the best way to R. Cuenca, DVM, PhD,
visualise the organs (Penninck and others 1991, Martorell Servei d’Ecopatologia de
Postfemoral (F)
and others 2004). Furthermore, anatomical differences Fauna Salvatge,
between species of turtles may affect the ease of scan- Y. Espada, DVM, PhD,
FIG 1: Acoustic windows used for ultrasound scanning
ning. The reproductive tracts of adult female Olive Ridley of loggerhead sea turtles (Caretta caretta). C, D, E and
Department de Medicina
turtles (Lepidochelys olivacea) and Kemp’s Ridley turtles F were scanned on both the right- and left-hand sides. i Cirurgia Animal,
(Lepidochelys kempii) have been studied by Rostal and Corresponding echo accesses: A Echoes pass obliquely Facultat de Veterinària,
others (1989, 1990, 1994). They recommended ultrasound cranial to the edge of the carapace (nuchal scute), B Echoes Universitat Autònoma
as a good technique for evaluating the structure of the pass in parallel dorsally to the plastron, between the cranial de Barcelona,
gonads, the development of the eggs and the presence of edge (epiplastron bone), medial ends of coracoid bones and 08193-Bellaterra,
atretic follicles. To the authors’ knowledge, no data about ventral face of the cervical vertebra, C Echoes pass between Barcelona, Spain
the coracoid bone and the acromion process of the scapula, M. L. Parga, DVM, MSc,
the normal ultrasonography of the loggerhead sea turtle
D Echoes pass between the shoulder joint and the cranial
are available. F. Alegre, DVM,
border of the bridge joining the carapace and the plastron,
This paper describes the normal ultrasonographic E Echoes pass between the caudal border of the bridge
Centre de Recuperació
appearance of the cervical structures and coelomic organs joining the carapace and the plastron and cranial face of the d’Animals Marins, Camí
of loggerhead sea turtles and provides images of frozen cross- femur, F Echoes are limited dorsally by the carapace and the Ral, 239-08330 Premià de
sections for anatomical reference. proximal end of the femur Mar, Barcelona, Spain

The Veterinary Record, August 18, 2007

 Papers & Articles

(a) (b)

A
B C

E
D

FIG 2: Ultrasound
images of the (c) (d) A
cervical-dorsal
structures of a
loggerhead sea turtle
B B
(Caretta caretta). C
(a, b) Transverse scan. E
(c) Oblique scan of the
venous cervical-dorsal
D
sinus of the jugular
vein. (d) Anatomical
transverse
cross-section
corresponding to
the transverse scan.
Bar=1 cm. (e) Diagram (e) 90°
showing the transverse
45°
and transverse oblique
planes preferred (f)
for imaging the
cervical-dorsal sinuses.
(f) Complex of
cervical-dorsal sinuses B
seen in a 45° oblique C B
scan, showing the
cervical vertebra
(arrow). A Vertebral
vein, anastomosis point
to transversal vein,
B, C Cervical-dorsal
sinuses, D Vertebral
body, E Spinal cord

minimum carapace length of 21 to 40 cm were considered
juveniles and those with a length of 41 to 65 cm were con-
sidered subadults (Pont and Alegre 2000). Their sex could
not be determined because they were sexually immature. All
the animals were caught accidentally in pelagic long-line sets
or fishing nets along the north-west Mediterranean coast of
Spain (40°31' to 42° 26' N, 0°32' to 3°10' E) and were housed
temporarily in the rehabilitation facilities of the Rescue Centre
for Marine Animals (CRAM), Premiá de Mar. The turtles were
in good condition, on the basis of physical, radiographic and
haematological parameters, and the turtles captured in long-
lines had the hook attached superficially in the buccal cavity.
During the ultrasonographic examinations, the animals
were restrained manually in ventral recumbency on a bucket,
high enough to prevent the limbs contacting the table. No
sedation was necessary. The head, neck or limbs were
extended as needed. The eyes were covered with a mask and
the body surface was kept wet with a sopping wet towel. Ten
areas of soft tissue integument were used as acoustic windows:
cervical-dorsal and cervical-ventral, left and right cervico-
brachial, left and right axillary, left and right prefemoral and
left and right postfemoral acoustic windows (Fig 1). Colour
and pulsed Doppler techniques were applied to the large
vessels, and the ultrasonographic examinations were made
with a real-time, B-mode scanner (Computed Sonography
Siemens 128XP/10; Acuson) using sector electronic transduc-
ers and frequencies of 4·0, 5·0 and 7·0 MHz. Coupling gel
(Polaris II; GE Medical Systems) was placed on the surface of
the transducer, which was orientated mainly in the horizontal
plane, that is, parallel to the plastron and carapace. Other
planes were not used owing to size limitations of the acoustic
windows and transducer. The images were recorded on video-
tapes, and records of the ultrasound images were made with
a thermal printer.
Anatomical sections were prepared from three frozen tur-
tles, one in a sagittal plane, one in a frontal plane and one
in a transverse plane. Two other dead turtles were dissected
to improve the morphological data. Anatomical terminology
followed that of Wyneken (2001).
RESULTS
The fourth and fifth cervical vertebrae, the spinal cord, and
the venous sinuses of the external jugular vein (also called the
cervical-dorsal sinuses) were clearly visible in a transverse and
transverse-oblique scan through the cervical-dorsal acoustic
window (Figs 2a to c). The ultrasonographic contours of
the vertebrae were visible with echogenic borders followed
by acoustic shadowing due to strong reflection from the
osseous tissue. The vertebral arch and the spinal cord were
clearly recognised and could be used as markers to identify
the right and left cervical-dorsal sinuses, which lay dorso-
lateral to the vertebrae. The sinuses are broad dilatations of

The Veterinary Record, August 18, 2007

Papers & Articles
(a)
D
E
F
B
A FIG 3: (a, b, d)
C
(c)
J D
I D
G
K E
E latex. Bar=1 cm. A Left
F A
J
H A
B aorta, G Brachicephalic
C
the external jugular vein (Figs 2b to f) and were identified
ultrasonographically as superficial, rounded, distensible hypo-
echogenic structures connected to the venous vessels. The
connection between the left and right cervical-dorsal sinuses
was visible through the anastomosis with the vertebral vein,
which lay centrally on the vertebral arch (Fig 2b, d). The ech-
oes of the circular blood flow inside the sinuses were some-
times visible. The dimensions of the sinuses were variable
but, in general, larger than those cited by Whitaker and Krum
(1999) who stated that the cervical-dorsal sinus in a 25 kg
turtle was approximately 1 cm x 2 cm in a transverse section;
in contrast, in the present study the dimensions were approxi-
mately 2·5 cm x 3·5 cm in a 26·8 kg turtle with a minimum
carapace length of 58·5 cm, and 1·8 cm x 4·2 cm in an 8·6 kg
turtle with a 39 cm carapace. The disparity could be related
to several factors. Because reptiles are ectothermal animals,
and the sinuses are vascular structures related to thermoregu-
lation, changes in their blood flow and dimensions may be
expected in response to external temperature variation, as
occurs in the front flippers (Hochscheid and others 2002).
The turtles used in the present study were scanned in the
summer, when the ambient temperature ranged from 25°C
to 35°C, and the increase in sinus size could have been due
to a vasodilatory response. In addition, the inclination angle
of the transverse oblique scan could also have been related to
the larger size, because of the longitudinally slanted section of
the vessels, which could have increased their apparent length.
However, when compared with the anatomical sections, it
was observed that the sinuses were not a single dilation of
the jugular vein, but a complex of small cavities separated
by fine membranous walls (Figs 2d, f), which could not be
completely visualised ultrasonographically.
Through the cervical-ventral acoustic window, the heart
appeared dorsoventrally flattened and located between
the two hepatic lobes. The atria, during diastole, could be
identified as oval, anechogenic paired structures with a fine
(b)
Ultrasound images
of the heart of a
loggerhead sea turtle
(Caretta caretta)
taken through the
cervical-ventral acoustic
window. (c) Ventral
view of an anatomical
(d) dissection of the heart
of a juvenile loggerhead
sea turtle injected with
latex, the right atrium
is slightly dilated by the
atrium, B Right atrium,
C Ventricle, D Left
B subclavian artery, E Left
pulmonary artery, F Left
F C
trunk, H Pulmonary
trunk, I Right pulmonary
artery, J, Right aorta,
K Right precaval vein
echogenic wall (Fig 3a). The ventricle had a homogeneously
echogenic appearance, with a distinct thick wall with a
trabecular lining (Figs 3a, b, d). Owing to the slow heart rate,
the echoes corresponding to blood flow and atrial diastole
were easily recognised during ventricular systole. Only an
atrioventricular valve was clearly visible as a short horizontal
echogenic line placed centrally between the atria and ventri-
cle. In the juvenile specimens the best way to see the heart
was through the cervical-ventral acoustic window; all three
chambers and the large vessels on the cardiac base could be
identified on a horizontal plane. Through this window the
scan usually passed along the dorsal aspect of the heart, where
the pulmonary and subclavian arteries were visible together
with the aortic arches (Figs 3a to d).
In the subadult turtles, the right cervicobrachial acoustic
window gave partial access to the heart and the left cervico-
brachial window provided a complete visualisation of the
right and left aortic arches and pulmonary arteries.
The distal end of the oesophagus was visible through the
cervical-ventral and left cervicobrachial acoustic windows
as a coarse echogenic structure, identified as the keratinised
papillae (Fig 4a). Although recognised postmortem as a lobu-
lar structure associated with the fat around the large cardiac
vessels, the thymus could not be clearly identified owing to
the similar granular appearance of the oesophagus.
The stomach was on the left side of the coelomic cavity.
Although it was partially visible through the left cervico-
brachial, axillary and prefemoral acoustic windows, it was
more frequently imaged through the left axillary acoustic
window (Figs 4b, c). A good marker to locate the stomach was
the subscapular muscle visible in a horizontal scan as a hypo-
echogenic rounded structure followed by a fine echogenic
line, the coelomic membrane (Figs 4b to d). The stomach
was usually visible dorsal to this muscle in an oblique dorsal
scan (30° to 35°). In general, the stomach had a thin wall
with folds visible as thin hypoechogenic lines, and it pro-
duced poor images owing to the presence of intraluminal gas
and contents (Figs 4b, c).
The liver was visualised as an echogenic structure with
granular parenchyma (Fig 5a). The hepatic vessels were vis-
ible as anechogenic tubular structures either in transverse or
The Veterinary Record, August 18, 2007
 Papers & Articles

(a) (b) (e)

B
C

(c) (d)

B A

C
A

A C
B

D
35°

FIG 4: Ultrasound images of the oesophagus and stomach of a loggerhead sea turtle (Caretta caretta). (a) Oesophagus, cross-sectional scan. (b, c) Stomach
taken through the left axillary acoustic window. (d) Diagram showing the oblique-image plane preferred for imaging the stomach. (e) Corresponding
frontal gross anatomical section. A Stomach lumen, B Subscapular muscle, C Coelomic membrane, D Coracoid

longitudinal sections (Fig 5a). The best access to this organ
was through either the left or right axillary acoustic windows
(Fig 5b). The right axillary acoustic window provided the best
views of the gall bladder, which had an anechogenic spheri-
cal/oval appearance within the right hepatic lobe (Figs 5a,
c). The postcava (also called the right hepatic vein) could be
identified on entering the right atrium via the venous sinus
valve (Fig 5d) through this acoustic window.
The large and small intestines were visible through
the prefemoral acoustic window from both sides. Loops of
small intestine were more frequently imaged on the right
side. The ultrasonographic image of the intestine was similar
to that of mammals (Mattoon and other 2002), and strati-
fication in four layers could be recognised. The wall of the
small intestine was thicker than that of the large intestine
(Figs 6a, b). The serosal and submucosal layers were easily
identified as echogenic lines; between them, the muscular
layer had a hypoechoic to anechoic appearance. The mucosa
was the thickest hypoechoic layer (Fig 6c). In contrast, the
wall of the large intestine did not have clearly distinguish-
able layers.
(b)

(a)

C
F
C
B
E

D A B

FIG 5: Ultrasound
images of the liver of a
loggerhead sea turtle D
(Caretta caretta).
(a) Image taken through (c)
the right axillary (d)
acoustic window and
(b) corresponding
frontal gross anatomical C
section. (c) Hepatic
parenchyma. (d) Liver
and heart. A Right B
hepatic vein (postcava), D F
B Hepatic parenchyma, A
C Subscapular muscle, G
D Gall bladder, E Right
atrium, F Sinuses of
jugular vein, G Liver

The Veterinary Record, August 18, 2007

Papers & Articles
(a)
(c)
A (a, b) Images taken
B prefemoral acoustic
The kidneys were easily identified by their intense vascula-
ture, which could be used as a marker. They could be imaged
superficially through the respective prefemoral acoustic
windows (Fig 6d) and showed a uniformly echogenic area,
comma-like, without a distinct renal pelvis and capsule.
The great renal vein was visible cranial to the kidney (Figs
6a, b).
The urinary bladder was visible only when it was
completely filled, as an anechoic globular structure (Fig 7a,
c); it was best identified through the left prefemoral acous-
tic window (Fig 7b). Echogenic dots were visible floating
within it and they were considered normal. They may have
been related not only to the presence of urate crystals but
also to parasites or faecal material, which could have entered
as a result of its closed connection with the cloaca (Wyneken
2001). Vesical parasites were found in one of the three dis-
sected turtles.
According to Wyneken (2001), sea turtles have two small,
accessory urinary bladders connected to the urinary bladder,
each located laterally to the neck of the bladder and dorsal
to the pubis. In this study, the neck of the urinary bladder
could not be imaged owing to the acoustic shadow of the
pubic bone. These structures have not been found during
detailed dissections of dead turtles (A. L. Valente, S. Lavin,
I. Marco, R. Cuenca, Y. Espada, M. L. Parga, F. Alegre, unpub-
lished observations).
The reproductive tract, the spleen, pancreas and adrenal
glands of the turtles could not be identified. The pancreas
extends as an irregular strip along the duodenum just past the
stomach. The spleen is oval and located below the pancreas.
These organs were not accessible ultrasonographically owing
to their small size, midline location and the artifacts caused
by the intestinal loops surrounding them. They were also not
identified in a study of California desert tortoises (Xerobates
agassizi) (Penninck and others 1991).
The postfemoral acoustic windows allowed access to the
caudal end of the kidneys in only a few of the larger subadult
turtles. In the juvenile turtles only the femur and muscular
mass could be imaged through these windows, which were
considered inadequate for the ultrasonographic evaluation
of any coelomic structures.
(b)
A
B D
FIG 6: Ultrasound
images of the kidney
and intestines of a
(d)
loggerhead sea turtle
C
(Caretta caretta).
B through the right
window. (c) Image
of the kidney and
longitudinal section
of small intestine.
(d) Frontal anatomical
E A section. Inset: Dorsal
view of the imaged
area. A Kidney, B Loop
of small intestine,
C Section of large
intestine, D Blood
supply of the kidney,
E Renal vein
DISCUSSION
Ultrasound imaging has been used to evaluate the repro-
ductive status of many reptilian and mammalian species
(Küchling 1989, Owens and Kraemer 1990, Casares and others
1997, Rostal and others 1998, Brook and others 2000, 2004).
Some species of reptiles are not sexually dimorphic, and in
these cases the ultrasonographic imaging of the gonads is a
reliable and inexpensive method for determining the sex of
the animals and selecting them for reproductive programmes
(Morris and Allison 1996). In general, loggerhead sea turtles
do not have differentiated external sexual characteristics until
they reach adult size, with a carapace of more than 65 cm long,
when they are more than 20 years old (Bjorndal and others
2001). This study shows that the sex of subadult turtles can
not be determined by ultrasonographic imaging. The small
undeveloped gonads may be mistaken for renal parenchyma,
and the tubular structures, such as the oviduct and defer-
ent canals, are not visible. The same limitation was found in
Kemp’s Ridley sea turtles, in which only ovarian follicles more
than 5 mm in diameter, and oviducts with eggs, could be
recognised ultrasonographically (Rostal and others 1990).
A knowledge of normal anatomy is essential for the inter-
pretation of diagnostic techniques. Chelonians have well-pro-
tected internal viscera, and the few body parts not covered by
the carapace or plastron are limited internally by the bones of
the proximal end of the limbs (scapular and pelvic girdles),
which usually limit scanning to one plane. Poor image quality
could also be a result of the great size of the turtle in relation to
the frequency of the transducer, the amount of fat tissue and
the degree of emptiness of the gastrointestinal tract. The high-
frequency transducers used in this study (7 MHz) were suitable
for assessing in detail superficial structures such as the cervi-
cal-dorsal venous sinuses, stomach, intestines and kidneys. In
the juvenile turtles, this probe provided good images of the
kidneys and the heart when the latter was viewed through the
cervical-ventral acoustic window. In the subadult animals the
The Veterinary Record, August 18, 2007

(a)
B
A reviewed the English. They would also like to thank the
(b)
B Marine Specialist Group Publication 4. Eds K. L. Eckert, K. A. Bjorndal, F. A.
A
(c)
FIG 7: Ultrasound
images of the kidney
and urinary bladder of
a loggerhead sea turtle
(Caretta caretta).
(a) Urinary bladder (A)
and kidney (B).
(b) Corresponding gross
anatomy of the scanned
area. (c) Full urinary
bladder with echogenic
dots
5 MHz transducer was more frequently used, and it provided
a good balance between penetration and resolution. The
4 MHz transducer was used infrequently because of its low
resolution. The prefemoral acoustic windows provided direct
access to the kidneys, and, as in other chelonian species,
they could be used to perform ultrasound-guided biopsies.
The hepatic and renal parenchymas were easily imaged and
could be evaluated for changes in shape and size, and for the
presence of neoplasia, cysts, abscesses and papillomas.
Owing to the slow digestive transit time, the presence of
food in the gastrointestinal tract of turtles that had fasted for
24 to 48 hours produced multiple artifacts and poor images,
mainly of the stomach. However, obstructive processes due to
garbage ingestion or severe mucosal damage caused by fish-
ing hooks (accordion effect) could be diagnosed.
In mammals it is known that low-level echoes are returned
from fat in certain areas of the body (Nyland and others
2002); low-resolution images are also obtained from some
turtles with larger amounts of fat, mainly through the cervi-
cobrachial acoustic windows.
The results of this study show that ultrasonography can be
a useful tool for the diagnosis of internal lesions in juvenile
and subadult loggerhead sea turtles. It is inexpensive, safe and
easy to use, and with practice most of the internal organs can
be located and examined.
The Veterinary Record, August 18, 2007
Papers & Articles
ACKNOWLEDGEMENTS
The authors thank Rosa Novellas and the CRAM volun-
teers for their help with this work, and the native English-
speaking teacher from the University of Barcelona who
anonymous reviewers.
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