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Summary
Chromatophoromas are tumours of pigment-producing cells of the skin and are rarely reported in reptiles.
These tumours are subclassified on the basis of the type of pigment. The present study characterizes chromatophoromas arising in 26 reptiles, including six snakes, 19 lizards and a tortoise. These include the first reports
of melanophoromas in a yellow anaconda (Eunectes notaeus), pigmy rattlesnake (Sistrurus spp.), southern water
snake (Nerodia fasciata), veiled chameleon (Chamaeleo calyptratus) and leopard gecko (Eublepharis macularius); the
first reports of benign iridophoromas in a savannah monitor (Varanus exanthematicus), veiled chameleon and
bearded dragon (Pogona vitticeps); and the first description of a malignant iridophoroma in a bearded dragon.
Additionally, in three bearded dragons a mucinous type of melanophoroma is described for the first time.
Chromatophoromas generally arose from the skin of the body and head and ranged in size from 0.2 to
2.0 cm in diameter. In six cases the animals were humanely destroyed immediately after diagnosis. Three further animals were humanely destroyed following recurrence of their tumour. Six of these nine reptiles had visceral metastases. Grossly, melanophoromas (n 20) were grey or black, while iridophoromas (n 6) were
white in colour. Microscopically, most of the tumours were composed of spindle cells with varying pigmentation and 0e2 mitoses per 10 high power fields. Six of the 20 melanophoromas were classified as malignant due
to the presence of intravascular tumour cells, visceral metastases, high pleomorphism and/or mitotic figures.
Five of the six iridophoromas were classified as benign and the one malignant tumour was defined by the presence of intravascular tumour cells and visceral metastases. Immunohistochemically, melan A and S100 were
coexpressed by all of the chromatophoromas.
2011 Elsevier Ltd. All rights reserved.
Keywords: chromatophoroma; iridophoroma; melanophoroma; reptile
Introduction
Three types of pigment cells (chromatophores) occur
within the integument of reptiles.
Tumours of pigment cells are generally referred to
as chromatophoromas and are classified according to
their specific chromatophores as: (1) melanophoromas or melanomas (melanin-producing cells), (2)
xanthophoromas (carotenoid or pteridine-producing
cells) or (3) iridophoromas (crystalline purineproducing cells containing reflecting granules of guanine, adenine, hypoxanthine or uric acid) (Bagnara,
1966; Bagnara and Hadley, 1973; Rohrlich, 1974;
Bagnara et al., 1979; Gopalakrishnakone, 1986;
Morrison, 1995).
Correspondence to: K. O. Heckers (e-mail: heckers@laboklin.de).
0021-9975/$ - see front matter
doi:10.1016/j.jcpa.2011.07.003
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Twenty-six chromatophoromas were selected for analysis from an archive of 179 reptilian tumours collected
over 9 years. The chromatophoromas arose in a number of different species of varying age (Table 1). In
each case the owners of the animals had observed
skin masses that had been present for a period of several
weeks.
In bearded dragons the chromatophoromas were
located in the skin of the shoulder/thorax (n 4), the
head (n 3), tail (n 2), leg (n 1) and in the oral
cavity (n 2). The origin was not documented in
three cases. In other reptiles (snakes, chameleons
and a savannah monitor) the chromatophoromas
were located in the skin of the thorax (n 6), abdomen
(n 3) and head (n 1) or in the oral cavity (n 1).
Most chromatophoromas were excised surgically
(n 23), fixed in 4% buffered formalin and submitted
Table 1
Frequency of chromatophoromas in the archive of
reptilian tumours
Species
Lizards
Bearded
dragons
Snakes
Tortoises and
turtles
Total number
105
51
20.0%
29.4%
13.7%
21.6%
6.3%
7.8%
61
13
9.8%
7.6%
9.8%
7.6%
e
e
179
14.5%
11.2%
3.3%
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Number of animals
15
1
1
2
1
1
1
1
1
few granules), mild (some or most cells with mild pigmentation), moderate (most cells are moderately pigmented), marked (most cells are intensely pigmented)
or dispersed.
Immunohistochemistry
Sex (n)
Female (6)
Male (3)
Unknown (6)
Male (2)
Female
Unknown
Female
Unknown
Female
Female
Female
Male
Female
Age (years)
Mean 3.7
(range 2e7)
3
1
10
5
Unknown
7
17
3
13
11
13
Melanophoroma (11)
Iridophoroma (4)
Melanophoroma
Iridophoroma
Melanophoroma
Iridophoroma
Melanophoroma
Melanophoroma
Melanophoroma
Melanophoroma
Melanophoroma
Melanophoroma
LI
Value
1
2
3
4
none
weak
moderate
strong
0
1
2
3
Statistics
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Results
Twenty of the 26 tumours were diagnosed as melanophoromas and six tumours with birefringent cytoplasmic granules were identified as iridophoromas. Six of
the melanophoromas were classified as malignant due
to the presence of intravascular neoplastic cells, visceral metastases, high pleomorphism and/or the presence of mitotic figures. Most iridophoromas were
classified as benign (n 5), with only one being considered malignant due to the presence of intravascular
neoplastic cells and neoplastic cells in the viscera.
The age of the affected animals ranged between 1
and 17 years (median 5 years; Table 2).
When all 179 reptilian tumours were considered,
chromatophoromas (n 26) were the most frequent,
followed by adenocarcinomas of different organs
(n 23), squamous cell carcinomas (n 18), fibrosarcomas (n 18), lymphomas (n 11), papillomas
(n 11), osteochondrosarcomas (n 9) and lipomas
(n 9). In lizards, chromatophoromas (n 19) were
the most frequent tumours followed by squamous cell
carcinomas (n 14), fibrosarcomas (n 10), adenocarcinomas of different organs (n 9), lymphomas (n 6)
and papillomas (n 5). The most common tumours of
snakes were adenocarcinomas of different organs
(n 13), fibrosarcomas (n 8), chromatophoromas
(n 6), lymphomas (n 6) and osteochondrosarcomas
(n 5). In the group of tortoises and turtles the most frequent tumours were papillomas (n 3) and squamous
cell carcinomas (n 3).
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Shape of cells
Pleomorphism
Bearded dragon
n 11
Spindle shaped, n 11
Mild, n 4
Moderate, n 6
Marked, n 1
Veiled chameleon
Leopard gecko
Garter snake 1
Garter snake no. 2
Yellow anaconda
Pigmy rattlesnake
Boa constrictor
Southern water snake
Hermanns tortoise
Spindle shaped
Epithelioid
Spindle shaped, n 2
Marked
Marked
Moderate, n 2
Spindle shaped
Spindle shaped
Spindle shaped
Spindle shaped
Spindle shaped
Moderate
Mild
Moderate
Mild
Moderate
Mitotic figures/HPF
Degree of pigmentation
Metastases
0, n 4
1, n 6
2, n 1
Amelanotic, n 2
Mild, n 3
Marked, n 1
Dispersed, n 5
Dispersed
Dispersed
Dispersed, n 2
Yes
Yes
Yes
No
Dispersed
Marked
Dispersed
Marked
Dispersed
Yes
No
No
No
Yes
3
11
0, n 1
1, n 1
2
0
0
0
2
amount of basophilic, PAS-positive, mucinous interstitial matrix. The cells were arranged in interlacing
bundles and loose whorls. The cells were mostly amelanotic with dispersed foci of moderate to marked pigmentation. The nuclei had a mildly dispersed
chromatin pattern. The mean number of mitoses
was 0e1 per HPF. The growth was invasive into the
dermis and musculature in all cases, but tumour cell
emboli in lymphatic or blood vessels and metastases
were not found (Fig. 4).
Birefringence was not exhibited by any of the melanophoromas. Mild inflammatory infiltration was
seen in seven tumours. Heterophils were the dominant inflammatory cells, but some lymphocytes,
plasma cells and histiocytes were also present.
Metastatic melanophoromas had a significantly
greater pleomorphism (P 0.047) than those tumours without metastases. The number of nucleoli
Fig. 4. Mucinous type of dermal melanophoroma from a 7-yearold bearded dragon. Loosely-arranged tumour cells lie
within large amounts of basophilic mucinous stroma. HE.
Bar, 10 mm.
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Melanophoromas were present in the viscera in addition to the skin in five cases, including three lizards,
one snake and one tortoise (Table 4) and these metastatic lesions affected 18 different tissues. Neoplastic
foci occurred predominately in the kidney, liver,
lung, intestine and abdominal fat bodies as well as
in the stomach and heart. In four of five cases multiple
organs were affected. In two cases the dermal tumours
showed intravascular tumour cells and during necropsy examination, visceral metastases were seen. In
three cases no tumour cell emboli were found in dermal neoplasms, but visceral metastases were located.
In general, the morphological features of the metastatic tumours corresponded to that described for the
dermal neoplasms, but some differences are notable.
In the veiled chameleon and the leopard gecko the
primary tumours showed a higher number of mitotic
figures and a higher degree of cellular atypia than the
visceral metastases. The primary oral tumour of the
leopard gecko was amelanotic, while the neoplastic
cells in the lungs were moderately pigmented. In the
yellow anaconda with recurring tumours the cellular
differentiation changed from epithelioid (first dermal
lesion) to spindle shaped (first recurrence in skin, second recurrence in skin and visceral metastases). At
first, the nuclei showed a homogenous chromatin pattern that changed to a mildly dispersed and finally to
a vacuolated pattern.
Clinical Outcome of Reptiles with Melanophoromas
Table 4
Characteristics of metastatic chromatophoromas
Species
Primary location
Bearded dragon
Skin
Melanophoroma
Skin
Iridophoroma
Bearded dragon
Veiled chameleon 1
Skin
Melanophoroma
Leopard gecko
Oral cavity
Melanophoroma
Skin
Melanophoroma
Carapace
Melanophoroma
Yellow anaconda
Hermanns tortoise
Metastasis
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Discussion
Chromatophoromas appear to be relatively common
tumours in reptiles. In bearded dragons melanophor-
Table 5
Summary of microscopical findings of iridophoromas
Species
Bearded dragon
n4
Veiled chameleon 2
Savannah monitor
Shape of cells
Spindle shaped,
n4
Spindle shaped
Spindle shaped
Pleomorphism
Mild, n 2
Moderate, n 2
Moderate
Mild
Mitotic figures/HPF
Degree of pigmentation
Intravascular growth
0, n 2
1, n 2
0
0
Marked, n 4
Yes
Marked
Marked
No
No
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003
10
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doi:10.1016/j.jcpa.2011.07.003
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Please cite this article in press as: Heckers KO, et al., Melanophoromas and Iridophoromas in Reptiles, Journal of Comparative Pathology (2011),
doi:10.1016/j.jcpa.2011.07.003