First Report of Lymphoid Neoplasia in a Loggerhead Sea Turtle (Caretta caretta)
J. Orós1, A. Torrent1, P. Calabuig1, S. Déniz1,
J. Sicilia1, A. B. Casal1, S. Tucker1, and E. R. Jacobson2; 1College of Veterinary Medicine, University of Las Palmas de Gran Canaria,
Trasmontaña s/n. 35416 Arucas (Las Palmas), Spain; 2College of Veterinary Medicine, University of Florida, Gainesville, FL 32610,
USA
Abstract. A juvenile female loggerhead sea turtle (Caretta caretta),
stranded in Gran Canaria, was submitted for necropsy. At necropsy, the thymus was enlarged
and formed by two white firm nodules. White nodules similar to those described in thymus
also were observed in the plastron, thyroid gland, heart, aorta, left lung, spleen, liver,
kidneys, stomach and small intestine. Histopathology revealed a neoplastic proliferation
of round cells identified as lymphoid cells. Ultrastructurally the neoplastic cells were
consistent with lymphoblastic cells. Viruses were not detected. The diagnosis was
multicentric lymphoblastic lymphoma. This is the first report of a lymphoid neoplasm in a
sea turtle.
Key words: Caretta caretta; lymphoblastic lymphoma; neoplasia; reptile;
sea turtle.
Introduction
Except for fibropapillomatosis, neoplastic disease is very infrequently seen in sea
turtles. Within the class Reptilia, lymphoid neoplasms are more frequently found in snakes
(Effron et al., 1977; Jacobson et al., 1981), although there are also
descriptions in lizards (Romagnano et al., 1996; Schultze et al., 1999), and
terrestrial chelonians (Ippen, 1972; Harshbarger, 1974; Frye, 1994;Rideout et al.,
1993). This report describes the macroscopic, cytologic, histopathologic, and
ultrastructural findings in a loggerhead sea turtle (Caretta caretta) with
multicentric lymphoblastic lymphoma.
Case report
A juvenile (straight carapace length 34 cm; weight 5 kg) female loggerhead sea turtle
stranded in Gran Canaria was submitted to the College of Veterinary Medicine, University
of Las Palmas of Gran Canaria, for necropsy. At necropsy the turtle was extremely
cachectic. The ventral aspect of the plastron was infiltrated with white and firm
irregular masses, ranging in size from 2 to 4 cm. The thymus was formed by two white and
firm nodules (Figure 1), weighed 25 g and appeared to be larger than that of previous
turtles we had necropsied.
 |
| Figure 1. Thymus. Notice its enlarged
size. |
White nodules similar to those described in the thymus were observed in the thyroid
gland. Several irregularly shaped, sharply demarcated, white foci up to 2 cm in diameter
were present in the ventral pectoral muscles. Similar masses were observed in the coelomic
wall.
The liver was friable with rounded edges and numerous firm white nodules, ranging in
diameter from 2 mm to 1 cm, throughout its parenchyma. Three similar masses were observed
in the ventricle, left atrium and aortic arch. The spleen was enlarged and numerous small
white nodules were observed when sectioned. The left lung had three white firm nodules, 1
cm in diameter, that were elevated on the pleural surface. The kidneys contained numerous
poorly defined white foci of small size (3-5 mm in diameter) that effaced its architecture
on section. Variable sized nodules also were observed in the serosa and mucosa of the
stomach (Figure 2) and small intestine. The mucosa of the stomach and small intestine
contained a few depressed ulcers with reddened rims and coated by fibrinonecrotic exudate. No parasites were observed in blood vessels nor digestive tract.
 |
| Figure 2. The serosa of the stomach showed
several neoplastic nodules. |
Representative tissues from all organs were fixed in neutral-buffered 10% formalin,
embedded in paraffin, sectioned at 5 µm for light microscopy,
and stained with hematoxylin and eosin (HE), periodic acid-Schiff (PAS), and Giemsa
stains. Selected samples from thymus and epicardium were routinely processed for
transmission electron microscopy and embedded in epoxy resin. Ultrathin sections were
mounted on grids, stained with uranyl acetate and lead citrate and examined with a Zeiss
910 microscope.
Histologic examination revealed that numerous parenchymal organs and tissues contained
nodular, unencapsulated masses or monotonous sheets composed of hyperchromatic neoplastic
lymphoid cells (Figure 3). Larger nodules were centrally necrotic. The cells had round or
irregularly shaped hyperchromatic nuclei with coarse chromatin clumping, and moderate to
abundant basophilic cytoplasm. Cytoplasmic granules were not detected in these cells in
sections stained with PAS, Giemsa, or HE stains. Mitotic figures were not numerous and
individual cell necrosis was common.
 |
| Figure 3. Spleen. The nodule is composed
of hyperchromatic neoplastic lymphoid cells. H&E 10x |
Due to infiltrates of lymphoid cells, there was a loss of the normal architecture of
many affected organs including thymus, thyroid gland, parathyroids, spleen and kidneys. No
neoplastic lymphoid cells were observed in sections of brain, spinal cord, skin, trachea,
gall bladder, eye, salt glands, pancreas or large intestine.
Transmission electron microscopy revealed a moderately polymorphic population of round
and oval cells with central rounded or oval nuclei, peripherally clumped heterochromatin
and two or more nucleoli. Most cells had a moderate to abundant amount of cytoplasm, and a
moderate number of organelles including mitochondria, lysosomes, endoplasmic reticulum and
dilated vacuoles (Figure 4). Viruses were not detected.
 |
| Figure 4. Heart; loggerhead sea turtle (Caretta
caretta). Lymphoid cells showed central rounded or oval nuclei, peripherally clumped
heterochromatin, moderate to abundant amount of cytoplasm, and moderate number of
organelles. 7000x |
Discussion
The morphology and ultrastructural features of the neoplastic cells and the pattern of
tumor proliferation support a diagnosis of lymphoblastic lymphoma in this sea turtle. The
absence of cytoplasmic granules excluded myelogenous neoplasia while the rounded nuclei,
peripherally clumped heterochromatin, moderate to abundant amount of cytoplasm, and
moderate number of cytoplasmic organelles were consistent with lymphoid neoplasia
described in other species (Jacobson et al. , 1980; Romagnano et al., 1996).
In reptiles, lymphoid neoplasms most commonly have a multicentric distribution (Ippen,
1972; Jacobson et al., 1980; Romagnano et al., 1996; Schultze et al.,
1999). Lymphoid neoplasia is more frequent in snakes and lizards than in other reptiles. Multicentric lymphoblastic lymphoma has been reported in a male Greek land tortoise (Testudo
hermanni) and involved the liver, heart, kidneys, spleen, pancreas and intestinal
serosa (Ippen, 1972). Grey-white nodules in the liver and kidney contained large lymphoid
cells with vesiculated nuclei, but ultrastructural study was not attempted. A malignant
lymphoma was diagnosed in a Burmese star tortoise (Geochelone platynota) but there
are no detailed published pathologic descriptions of this case (Frye, 1994). Lymphoreticular neoplasia was detected in a Florida soft-shelled turtle (Trionyx ferox)
(Harshbarger, 1974). Alimentary tract lymphomas were described in several Galapagos
tortoises (Geochelone elephantopus) (Rideout et al., 1993).
Except for fibropapillomatosis, neoplasia is very uncommon in sea turtles. Green turtle
fibropapillomatosis (GTFP) is characterized by multiple cutaneous papillomas, fibromas,
and fibropapillomas, as well as occasional visceral fibromas (Herbst et al., 1999). No involvement of lymphoid organs has been described in sea turtles with GTFP. The
multicentric lymphoblastic lymphoma described in this loggerhead sea turtle is the first
lymphoid neoplasia to be reported in a sea turtle.
Acknowledgements
We are grateful to members of Viceconsejería de Medio Ambiente, Cabildo Insular de
Gran Canaria for providing the turtles. We thank Francisco Freire of the Electron
Microscopy Service, University of Las Palmas de Gran Canaria, for preparing specimens for
electron microscopy and preparation of electron photomicrographs. We thank Pedro Castro
for technical assistance.
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