FOLLICULAR CELL CARCINOMA OF THE THYROID

GLAND IN THREE CAPTIVE AGED RACCOON DOGS

(NYCTEREUTES PROCYONOIDES)
Author(s): Nobuhide Kido, D.V.M., Dipl. J.C.Z.W.M., Dipl. A.C.C.M., Ph.D.,
Iori Itagaki, D.V.M., Dipl. J.C.V.P., Kaori Ono, D.V.M., Tomoko Omiya,
D.V.M., and Rei Matsumoto, D.V.M., Dipl. J.C.Z.W.M.
Source: Journal of Zoo and Wildlife Medicine, 46(4):889-894.
Published By: American Association of Zoo Veterinarians
DOI: http://dx.doi.org/10.1638/2015-0013.1
URL: http://www.bioone.org/doi/full/10.1638/2015-0013.1

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 Journal of Zoo and Wildlife Medicine 46(4): 889–894, 2015
Copyright 2015 by American Association of Zoo Veterinarians

FOLLICULAR CELL CARCINOMA OF THE THYROID GLAND IN

THREE CAPTIVE AGED RACCOON DOGS (NYCTEREUTES
PROCYONOIDES)

Nobuhide Kido, D.V.M., Dipl. J.C.Z.W.M., Dipl. A.C.C.M., Ph.D., Iori Itagaki, D.V.M., Dipl. J.C.V.P.,
Kaori Ono, D.V.M., Tomoko Omiya, D.V.M., and Rei Matsumoto, D.V.M., Dipl. J.C.Z.W.M.

Abstract: The clinical and histologic features of thyroid carcinoma in raccoon dogs have not been previously
reported. Three of four raccoon dogs (Nyctereutes procyonoides) over 8 yr of age at the Nogeyama Zoological
Gardens developed thyroid follicular cell carcinomas that were detected at necropsy. The affected raccoon dogs
were rescued from the wild and were housed at the Nogeyama Zoological Gardens for 8 yr 8 mo, 8 yr 10 mo, and
10 yr 3 mo, respectively. Although all of them appeared lethargic and developed partial alopecia or desquamation
of their skin, they did not display any other specific clinical signs associated with a thyroid lesion. Serum thyroid
hormone values were examined in two of the affected raccoon dogs and the average and standard deviation values
(free-thyroxin [FT4]: 0.078 6 0.077 pM/L and 0.062 6 0.0039 pM/L; free-triiodothyronine [FT3]: 3.261 6 0.765
pM/L and 3.407 6 0.919 pM/L) were lower than the reference range (FT4: 0.141 6 0.117 pM/L; FT3: 5.139 6
2.412 pM/L) derived from a clinically normal raccoon dog. On necropsy, the thyroid lobes were markedly enlarged
bilaterally. Histopathologically, the neoplastic cells in the thyroid gland appeared round or oval and columnar or
cuboidal with minimal heteromorphism. Moreover, mostly small (but occasionally large) follicles were identified,
and the neoplastic cells had infiltrated into the surrounding capsule and blood vessels. The histopathologic
features of the thyroid tumors in the raccoon dogs revealed that the tumors were derived from follicular cells.
Key words: Follicular cell carcinoma, hypothyroid, Nyctereutes procyonoides, raccoon dog, serum thyroid
hormone, thyroid glands.

INTRODUCTION have been reported as having T-cell lymphoma

and pheochromocytoma.14,17
The raccoon dog (Nyctereutes procyonoides) is a
Neoplasms of thyroid follicular cells are en-
native species in Japan inhabiting a wide geo-
countered most often in dogs, cats, and horses,
graphic range.16 It has also been kept in many zoos
with other species affected only infrequently.6,7,18
in Japan. Captive animals in zoos often survive
These neoplasms are classified into adenomas or
longer than animals living freely in the wild and
carcinomas, with various subtypes, based on
therefore may occasionally develop specific dis-
histopathologic or behavioral characteristics.
eases that seldom affect their wild counterparts.
Most animals with thyroid neoplasms are aged
Although the number of reported cases was the
adults. The mean age of dogs with thyroid
same between captive and free-ranging raccoon adenoma and carcinoma is reported to be 10.7
dogs, many cases of neoplasms have been report- and 9.0 yr, respectively.10 Captive raccoon dogs in
ed previously as the following: Neoplasms report- zoos usually have long lifespans, and the devel-
ed in free-ranging raccoon dogs include complex opment of neoplasia, such as thyroid neoplasms,
carcinoma of the mammary gland and nasal is possible in geriatric animals.
neuroendocrine carcinoma,9,12 and captive ones Raccoon dogs have been kept at the Nogeyama
Zoological Gardens for over 50 yr, with some of
From Nogeyama Zoological Gardens, Yokohama Green- them have survived for more than 8 yr. Histo-
ery Foundation, 63-10, Oimatsu cho, Nishi ku, Yokohama pathologic examination to determine the cause of
220-0032, Japan (Kido, Ono, Omiya, Matsumoto); and The death was carried out in four raccoon dogs that
Corporation for Production and Research of Laboratory died at over 8 yr of age. Three of these four
Primates, 1-16-2, Sakura, Tsukuba 305-0003, Japan (Itaga- animals had developed follicular cell carcinoma of
ki). Present addresses (Kido, Omiya): Kanazawa Zoological the thyroid gland. This study focused on acquiring
Gardens, Yokohama Greenery Foundation, 5-15-1, Kamar-
previously unreported information regarding thy-
iya higashi, Kanazawa Ku, Yokohama 236-0042, Japan;
(Itagaki): Research Center for Animal Life Science, Shiga roid follicular cell carcinoma in raccoon dogs.
University of Medical Science, Seta tsukiwa cho, Otsu 520- This included the clinical and histopathologic
2192, Japan. Correspondence should be directed to Dr. Kido descriptions of thyroid follicular cell carcinoma
([email protected]). in these animals.

889
890 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Table 1. Average and standard deviation values for serum thyroid-stimulating hormone (TSH), thyroxin (T4),
triiodothyronine (T3), free-thyroxin (FT4), and free-triiodothyronine (FT3) in the raccoon dogs of Case Nos. 1
and 2, and the values of three clinically normal raccoon dogs for comparison (numbers in parentheses are the
numbers of samples analyzed).

TSH (mIU/L) T4 (nM/L) T3 (nM/L) FT4 (pM/L) FT3 (pM/L)

Case 1 2.026 6 2.048 (4) 9.653 6 1.931 (2) 0.375 6 0.069 (3) 0.078 6 0.077 (4) 3.261 6 0.765 (4)
a

Case 2 0.621 6 0.361 (4) 21.017 6 12.716 (3) 0.524 6 0.265 (3) 0.062 6 0.039 (7) 3.407 6 0.919 (4)
Reference 1.044 6 1.903 (11) 43.333 6 30.579b (6) 1.357 6 0.970 (9) 0.141 6 0.117 (14) 5.139 6 2.412 (11)
a
One sample was excluded because the value was under the minimum limit of detection (,0.5).
b
Three samples were excluded because the values were under the minimum limit of detection (,0.5).

CASE REPORTS Gross necropsies of all three deceased raccoon

dogs revealed significant bilateral swelling of the
Three raccoon dogs, including one male (No. 1)
thyroid gland (No. 1: left, 39 3 19 3 18 mm and
and two females (Nos. 2 and 3), were rescued from
right, 40 3 16 3 14 mm; No. 2: left, 35 3 22 3 22
the wild (No. 1: Naka ku, Yokohama, in 2003; No.
mm and right, 39 3 21 3 16 mm; No. 3: left, 35 3
2: Asahi ku, Yokohama, in 2001; No. 3: Kohoku
23 mm and right, 22 3 17 mm), with apparent
ku, Yokohama, in 1999); Nos. 1 and 2 were
restriction of the trachea by the swollen thyroid
orphaned as juveniles, and No. 3 was debilitated.
gland. The thyroid glands were covered with a
The orphaned animals were estimated to be 6 mo
thick white capsule and uniformly replaced by the
in age, while the age of dog No. 3 was unclear. The
proliferative lesion (Fig. 1). In dog No. 2, the liver
three raccoon dogs were kept at Nogeyama
also was peppered by random white spots along
Zoological Gardens for exhibition for 8 yr 8 mo
(No. 1), 8 yr 0 mo (No. 2), and 10 yr 3 mo (No. 3). with a solid tumor (84 3 76 3 32 mm) in the right
At that time, the three raccoon dogs exhibited lobe. In dog No. 3, the lobar pattern of the lungs
scabrities, alopecia, and emaciation. Desquama- was accentuated. For all three cases, heart, lung,
tion along the dorsum and lumbar region also was liver, spleen, stomach, intestine, kidney, and
identified. The serum thyroid stimulating hor- thyroid gland were fixed in 10% neutral buffered
mone (TSH), thyroxin (T4), triiodothyronine formalin.
(T3), free-thyroxin (FT4), and free-triiodothyro- The formalin-fixed tissue samples of dog No.1
nine (FT3) values were determined by chemilu- were embedded in paraffin, sectioned, and stained
minescent immune assay at Showa Medical with hematoxylin and eosin (H&E) at the Corpo-
Science Co. (Tokyo) in Nos. 1 and 2, as well as ration for Production and Research of Laboratory
in three healthy raccoon dogs (one male and two Primates (Ibaraki, Japan). Histologic examination
females) used as controls. These values were revealed bilateral thyroid follicular cell carcino-
determined twice in winter and twice in summer ma, some tumor-associated reactive arterial
for dog No. 1 and twice in winter and five times in changes in multiple organs and tissues, and
summer for dog No. 2 over a period of 1.5 yr atrophic changes of hepatocytes and lymphoid
before the death of the animal. The three raccoon tissue. Thyroid follicular cell carcinoma replaced
dogs (1, 1, and 2.5 yr of age, respectively) used for almost all of the normal tissue of the right and left
comparison were exhibited in the zoo and were lobes of the thyroid gland, and non-neoplastic
clinically normal, with good body condition thyroid gland was not identified (Fig. 2). Neo-
scores; these values were determined three times plastic cells were arranged in single layers in small
in winter and once in summer in two raccoon dogs follicles or discrete follicle-like islands and had
and three times in winter and three times in clear or slightly eosinophilic cytoplasm with mild
summer in the third raccoon dog over a period of atypism. They showed malignant histologic char-
2 or 3 yr, respectively (see Table 1). Raccoon dog acteristics and were organized into two types of
No. 1 became partially anorexic and died after 1.5 histologic areas. In one type, neoplastic cells were
mo. Raccoon dog No. 2 was losing body condi- small with unclear edges. These cells proliferated
tion, and bilateral enlargement of the thyroid in solid clumps and had an average mitotic index
gland was palpated under manual restraint. of 3.4 in 10 fields. In the other type, neoplastic
Therefore, abnormality in the thyroid gland was cells had a clearly demarcated cytoplasm and
considered. The animal died 1 yr later. Raccoon proliferated in a follicular pattern. These cells had
dog No. 3 died suddenly without any specific an average mitotic index of 0.3 in 10 fields. The
clinical signs. degree of nuclear anisokaryosis was low in both
 KIDO ET AL.—FOLLICULAR CELL CARCINOMA IN RACCOON DOGS 891

Figure 1. Macroscopic assessment of the thyroid gland in the raccoon dogs (Nyctereutes procyonoides). (a) No.
1: Estimated to be 9 yr of age, male raccoon dog No. 1 became partially anorexic and died after 1.5 mo. Thyroid
gland fixed in 10% buffered formalin. Thyroid glands were bilaterally swollen and the capsule was remarkably
thick. Scale ¼ 1 mm. (b) No. 1: Sections of thyroid gland fixed in 10% buffered formalin. Thyroid glands were solid
with unclear follicular structures and clear capsule. Scale ¼ 1 mm. (c) No. 2: Estimated to be 9 yr of age, female
raccoon dog No. 2 exhibited bilateral enlargement of the thyroid gland and died 1 yr later. Sections of thyroid
glands. Thyroid glands were bilaterally swollen and solid. The scale is in centimeters. (d) No. 3: Estimated to be
greater than 10 yr of age, female raccoon dog No. 3 died suddenly without any specific clinical signs. Thyroid
glands were swollen, and the blood vessels in the surrounding capsule exhibited dilatation. Bar ¼ 3 cm.

areas. Neoplastic cells occasionally invaded into Formalin-fixed tissue samples of dogs No. 2
the surrounding capsule and adjacent preexisting and 3 were sent to Marupi Lifetech Co., Ltd.
small vessels (Fig. 3). However, no metastasis was (Osaka, Japan) for histopathologic examinations.
found in other organs. In the lungs and heart, In dog No. 2, thyroid follicular cell carcinoma was
there were some reactive changes due to direct identified bilaterally and occupied almost the
airway compression by the tumor masses and entire thyroid gland. Round or columnar-shaped
related compromised circulation. The lung tissue small epithelial cells resembling follicular epithe-
was partially reconstructed with fibrous thicken- lial cells were proliferated throughout the en-
ing of the interstitium and multilayered hyper- larged thyroid gland, creating small lobules. Large
plastic growth of bronchiolar and type II alveolar neoplastic ducts contained colloid-like substance.
epithelial cells. The endocardium of the cardiac Despite their mild atypical appearance, the neo-
valves had developed papillary-like structures plastic cells invaded into the capsule of the
associated with a large atrial thrombus, and some thyroid gland. Hepatocellular carcinoma was also
arterial walls in the lungs were extremely thick- identified in the liver of dog No. 2. Hepatocyte-
ened with multilayered endothelial hyperplasia like epithelial cells had proliferated in trabecular
and resultant obstruction of blood flow. form. Neoplastic cells were smaller than preex-
892 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 2. Estimated to be 9 yr of age, male raccoon Figure 3. Estimated to be 9 yr of age, male raccoon
dog (Nyctereutes procyonoides) No. 1 became partially dog (Nyctereutes procyonoides) No. 1 became partially
anorexic and died after 1.5 mo. Thyroid follicular cell anorexic and died after 1.5 mo. Thyroid follicular cell
carcinoma in the raccoon dog. Follicular epithelial cells carcinoma in the raccoon dog. Neoplastic cells infil-
proliferated in the entire thyroid gland, obliterating any trated into the capsule and the blood vessels. Bar ¼ 50
normal thyroid tissue. The neoplasm was covered with lm.
a thick capsule. Bar ¼ 500 lm.

and as a result they may develop age-related

isting non-neoplastic cells and had mild cellular disease. Thyroid follicular cell carcinoma is an
atypism (or polymorphism). There was fibrin example of a typical neoplasm that can develop
thrombus formation in the hepatic sinusoids. with age. A previous study11 described two
Congestion and extramedullary hematopoiesis captured aged raccoons that eventually developed
were observed in the liver. No metastatic lesion thyroid carcinoma. Understanding the tendency
associated with the thyroid or hepatocellular for captive wildlife to develop this disease is
carcinoma was observed in other organs or useful and important information for zoo veteri-
tissues. narians.
In dog No. 3, bilateral thyroid follicular cell The present study revealed the pathologic
carcinoma was identified, and the thyroid gland characteristics of thyroid follicular cell carcinoma
was totally replaced by the carcinoma. The in the raccoon dog. Several common pathologic
thyroid follicular epithelial cells were proliferat- observations were made in the three raccoon
ed, forming small and large follicles. The neo- dogs. The bilaterally swollen thyroid gland ap-
plastic cells were oval or cuboidal in shape, with peared to compress the trachea. Thyroid follicular
an obvious nucleolus, and varied in size with mild cell carcinoma developed bilaterally and occupied
cellular atypism (or polymorphism). They invad- the entire preexisting thyroid tissue, and nodular
ed into the adjacent dilated blood vessels. The lesions and large cysts in the thyroid gland, which
parathyroid gland, which was attached to the are characteristic of adenoma, were not observed.
thyroid gland, also contained small neoplastic The neoplastic cells had mild atypism (or poly-
lesions comprising cells of the same shape as the morphism), were round-oval or columnar-cuboi-
follicular epithelial cells. dal in shape, and were arranged in small (but
occasionally large) follicles. Direct invasion into
DISCUSSION
the surrounding capsule (dogs No. 1 and 2),
The present study revealed that aged raccoon adjacent blood vessels (dogs No. 1 and 3), or
dogs in Nogeyama Zoological Gardens frequently parathyroid (dog No. 3) was histologically evi-
developed follicular cell carcinoma of the thyroid dent. These observations in the raccoon dog were
gland, because three of the four aged raccoon similar to those for the domestic dog.3 Interest-
dogs, which were over 8 yr of age, developed the ingly, thyroid carcinoma in the raccoon dog was
disease. Therefore, thyroid follicular cell carcino- bilateral in the present study; this is an unusual
ma should be considered an important disease in observation, because unilateral thyroid carcinoma
aged raccoon dogs. Generally, captive animals in is approximately twice as frequent as bilateral
zoos survive longer than do animals in the wild, carcinoma in dogs.10 In addition, except for the
 KIDO ET AL.—FOLLICULAR CELL CARCINOMA IN RACCOON DOGS 893

adjacent parathyroid gland in dog No. 3, which noma are euthyroid.3 The present study investi-
included a small neoplastic mass resembling the gated thyroid hormone levels. Although the
thyroid tumor, there were no observable meta- chemiluminescent immune assay at Showa Med-
static lesions in other organs and tissues, partic- ical Science was designed for humans and the
ularly pulmonary metastasis, which is frequent in interspecies homology was not exactly con-
canine thyroid carcinoma but not in raccoon dog firmed, results derived from the same method
cases.2,10 To the authors’ best knowledge this is the could be compared. Reference levels of serum T4
first report that describes the histopathologic and T3 in dogs are 12.87–51.48 nM/L and 0.77–
characteristics of thyroid follicular cell carcinoma 2.31 nM/L, respectively.11 However, the present
in the raccoon dog. Although the diagnosis in the study showed that serum thyroid hormone levels
present study was based on histopathologic in dogs No. 1 and 2 were lower than this
examination, it was found that the carcinoma reference range and the range of the clinically
was clearly derived from thyroid follicular cells normal raccoon dogs. As described in a previous
and easily discriminated from the tumor of study,8 thyroid hormone levels can be affected by
thyroid C cells without specific staining because nutritional status and the season of the year. In
the carcinoma was well differentiated. However, the present study, the serum samples were
further study is required to reveal the character- determined in winter and summer seasons. In
istics of thyroid tumor in the raccoon dog by addition, although dogs No. 1 and 2 appeared
specific methods, including immunohistochemi- emaciated at the time of examination, the pres-
cal staining, electron microscopy, and genetic ence of the thyroid tumor might have adversely
techniques. affected their body condition. Therefore, the low
Animals with thyroid neoplasms are usually thyroid hormone values might have reflected
older adults.10 The ages of the raccoons reported hypothyroid in dogs No. 1 and 2, which made it
previously were 6, 9, and 11 yr.5,11 The present difficult to detect the disease based on the
study showed that three of the four raccoon dogs clinical signs alone.
that died at an age of greater than 8 yr had In conclusion, the findings of the present study
developed thyroid carcinoma. The etiology of suggest that geriatric raccoon dogs might develop
thyroid carcinoma in the study subjects remains thyroid follicular cell carcinoma; the results also
unknown. However, age appears to be one of the revealed for the first time the clinical and
important risk factors associated with thyroid histopathologic features of thyroid follicular cell
follicular cell carcinoma development. Thyroid carcinoma in the raccoon dog.
follicular cell carcinoma might be one of the
important diseases in aged raccoon dogs. A
previous study13 described that the average age LITERATURE CITED
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