pISSN 1598-298X
J Vet Clin 30(3) :214-217 (2013)
214
Cytologic Aspects of Oral Squamous Cell Carcinoma in a Captive African Hedgehog ( Altelerix albiventris)
Hyang Mi Cho, Ul Soo Choi and Hae Beom Lee1
College of Veterinary Medicine, Chonbuk National University, Jeonju-si, Jeollabuk-do 561-756, Korea (Accepted: June 07, 2013)
Abstract : A 3-year-old intact female hedgehog (Atelerix albiventris) was presented for evaluation of mandibular swelling. Fine needle aspiration of swollen mandibular was performed and smears were stained with Romanowsky type stain for cytological evaluation. Smears were highly cellular with predominance of variably shaped keratinized or non keratinized squamous cells with low numbers of spindloid to abnormally elongated cells. Cytologic impression was squamous cell carcinoma. The mass was surgically removed for histological examination. Microscopically tortuous and anastomosing delicate to broad pegs and nests of neoplastic squamous epithelial cells were supported by a moderate collagenous and spindloid fibroblast stroma. Tumor cells had moderate anisocytosis and mild anisokaryosis and range from moderately to well keratinized, with areas of intratumoral acantholysis accompanied by mixed stromal lymphoplasmacytic, neutrophilic inflammation. The mitotic index is 2-3 per high-power field. Tumor cells were expanding the subcutis subjacent to the layer of skeletal muscle and incorporating the osseous tissue fragments. The final diagnosis was squamous cell carcinoma. The patient survived three months after surgery without any further medical treatments.
Key words : squamous cell carcinoma, cytology, spindloid cells, hedgehog.
Introduction.
Squamous cell carcinoma (SCC) is a malignant tumor of epidermal cells in which the cells show differentiation to keratinocyte (4). Oral squamous cell carcinoma is the third most common tumor of the hedgehog (6,7). Affected animals may be male or females, and their reported age has ranged from 2 to 5.5 years (6,7,10). Squamous cell carcinoma in hedgehogs is slow to metastasize, with local lymph node and pulmonary metastasis present in a few cases (6,7). There were no reports describing effective treatment of oral squa- mous cell carcinoma in the hedgehog (6). The optimal treat- ment would be complete surgical excision (6). Cytologic examination typically reveals numerous neoplastic squamous cells, often polyhedral to elongated (spindloid), with a mod- erate to abundant amount of cytoplasm, and perinuclear small clear vacuoles or pallor (7). Because oral squamous cell car- cinoma are commonly ulcerated, suppurative inflammation may be prominent. It is difficult to differentiate squamous cell carcinoma from chronic hyperplasic gingivitis cytologi- cally (7).
This report describes a case of an oral squamous cell carci- noma in a hedgehog with an emphasis on cytological features of this tumor and discusses the cytological pitfalls in evaluat- ing this kind of tumor.
Case
A 3-year-old captive African hedgehog (Atelerix albiven- tris) was presented for evaluation of mandibular swelling (Fig 1). Physical examination revealed a mass in oral cavity and tooth loss, and swelled mandibular. Skull radiography revealed a soft tissue density mass in 3 cm diameter. For cytological evaluation, fine needle aspiration was performed using 23 g needle, smears fixed in methanol for one minute, and stained with Diff-Quik stain. The cytologic preparations were highly cellular and predominant cell population was
1Corresponding author.
E-mail: seatiger76@jbnu.ac.kr Fig 1. Mandibular swelling of the hedgehog (arrow).
Cytologic Aspects of Oral Squamous Cell Carcinoma in a Captive African Hedgehog (Altelerix albiventris) 215
round to polygonal squamous cells either individualized or in groups with marked anisocytosis and pleomorphism (Fig 2).
Cytoplasm was moderate to abundant and dark blue to pale blue. Low numbers of cells had small amount of deeply basophilic cytoplasm showing high N:C ratio. Occasional spindloid cells and tadpole cells were also noted with elon- gated or filamentous cytoplasm (Fig 3). Nuclei tended to be round with marked anisokaryosis and rare gigantic nuclei (upto four times the diameter of an erythrocyte). Occasional cells were binucleated or multinucleated. Chromatin was dis- persed and nucleoli were difficult to visualize. Emperipolesis (presence of one cell type within the cytoplasm of another) of neutrophils was commonly found (Fig 4). The cytologic im- pression was squamous cell carcinoma.
For histology and treatment the mass was surgically re- moved and fixed in 10% buffered formalin. Microscopically tortuous and anastomosing delicate to bread pegs and nests of neoplastic squamous epithelial cells were supported by a moderate collagenous and spindloid fibroblast stroma (Fig 5).
Tumor cells had moderate anisocytosis and mild anisokaryo- sis and range from moderately to well keratinized, with areas of intratumoral acantholysis accompanied by mixed stromal lymphoplamacytic, neutrophilic inflammation. The mitotic index was 2-3 per high-power field. Tumor cells were expand- ing the subcutis subjacent to the layer of skeletal muscle and incorporating the osseous tissue fragments. The histologic Fig 2. Fine needle aspirate of the mandibular lesion. Note the
predominant cell population of round to spindloid to elongated squamous cells. Fully keratinized squamous cells (arrow). Diff- Quik, × 400. Bar = 150 um.
Fig 3. Fine needle aspirate of the mandibular lesion. Note the abnormally elongated cells (fiber cells) and spindloid cells. Diff-Quik, × 200.
Fig 4. Emperipolesis (arrow, a) and perinuclear vacuoles (arrow, b). Diff-Quik, × 1000.
216 Hyang Mi Cho, Ul Soo Choi and Hae Beom Lee
diagnosis was squamous cell carcinoma. The owner declined any further treatment, and the patient was discharged, which was later notified to survive three months after surgery.
Discussion
Squamous cell carcinomas in domestic animals are epithe- lial tumors commonly arising from the skin or in organs with stratified squamous epithelium, such as tongue, esophagus, pharynx, nasal septum and uterine cervix (4). In hedgehog squamous cell carcinoma is most commonly found in oral cavity and rarely in oronasal cavity and ear (2,3,6,7,9,10).
Other oral tumors than squamous cell carcinoma have been rarely described with one report of an oral fibrosarcoma in a 5-year-old male hedgehog (9).
According to one report oral squamous cell carcinoma in hedgehogs is very aggressive, with local infiltration but only a low tendency to metastasis (9), but other report documented an animal with squamous cell carcinoma of the maxillary gin- gival that metastasized to the local lymph node and lung (6).
In this patient no regional lymph nodes enlargement was noted and radiography study for evaluation of distant metasta- sis was not able to be performed. However microscopical infiltration to the adjacent subcutis and muscle was noted in this case.
Cytologically, in domestic animals squamous cell carcino- mas tend to yield a mixture of cell clusters and more mature individual cell (3,8). Cellular morphology varies from nor- mal, large, mature, squamous cells to small or medium round cells with small amount of very basophilic cytoplasm and large, round nuclei (8). Tadpole cell and keratinized blue- green hyalinized cytoplasm may be a helpful criterion in determining the cell of origin (3,8). In domestic animals, tad- pole cells with tail-like projection were found mainly in the well-differentiated squamous cell carcinoma (1,3). Some cells may also contain, small, clear vacuoles that may occasionally aggregate around the nucleus (perinuclear vacuolation) and appear to coalesce, forming a clear ring around the nuclei;
these cells are strongly suggestive of carcinoma (1,8) and these findings were also seen in our case.
A notable finding in this case is the presence of increased numbers of spindloid or abnormally elongated squamous cells. Some cells resemble tadpole cells but the cytoplasmic rim of some cells was bipolar elongated and thinned, which comprised approximately 20-30% of the total cell population.
In human medicine, these cells are squamous cells folded dur- ing smear preparation or abnormally enlongated (fiber cells) as a dysplastic or neoplastic transformation. Abnormal enlon- gation results in tadpole cells or fiber cells accompanied by dysplastic nuclei shape change, which can be found both in neoplastic and non-neoplastic conditions such as irritation, repair, atypia and other retroplastic and proplastic states. (5).
In animals these cells were reported more commonly in well differentiated SCCs rather than poorly differentiated SCCs, and also in Hedgehogs (1,3,7,8). Clinical significance of the presence of these tadpole cells and/or fiber cells is also unknown in animals. In diagnostic aspects the presence of these cells, especially fiber cells can be challenging, because these cells appear mesenchymal in origin and falsely lead the clinician to the diagnosis of a tumor of mesnechymal origin.
On the other hand, the presence of normal shape squamous cells along with tadpole cells, spindloid or fiber cells may be helpful to identify the tumor cells as squamous origin. In epi- thelial cells tumor cells are usually round with rare spindle or spindloid cells, which is contrary to the cellular features of SCC (1,8).
Because squamous cell carcinomas are often ulcerated with or without a secondary superficial bacterial infection, puru- lent inflammation often accompanies immature or dysplastic squamous epithelium (1,8). It is often difficult to determine squamous cell carcinoma from chronic inflammation because chronic inflammation may irritate the epithelial cells and induce dysplasia (atypia) (9). Chronic hyperplastic gingivitis associated with bacterial infection is frequent in African hedge- hogs (7). There was a report of squamous cell carcinoma and consequent otitis in a long-eared hedgehog (Hemiechinus auritus) (2). Histopathologic evaluation is mandatory for dif- ferentiation. Presence of fiber cells, tadpole cells, emperi- polesis, accumulation of vacuoles around nuclei, and large vacuoles can be found both in dysplastic and neoplastic Fig 5. Histologic sections of the lesion. Note neoplastic squa-
mous epithelial cells supported by a moderate collagenous and spindloid fibroblast stroma. Larger view of the neoplastic cells (inest). H&E, × 40; inset, × 400.
Cytologic Aspects of Oral Squamous Cell Carcinoma in a Captive African Hedgehog (Altelerix albiventris) 217
changes, and should not be relied on to determine the malig- nant transformation of the squamous cells (3,5,8).
There was no reports describing effective treatments of oral squamous cell carcinoma in the hedgehog (6). The optimal treatment would be complete surgical excision (6). In this case the mass was surgically removed and the patient survived three months after surgery. Survival times are not known in the lit- erature (2,3,6,7,9,10).
Conclusively, squamous cell carcinoma develops com- monly in oral cavity in Hedgehogs, and the presence of vary- ing numbers of spindloid cells or fiber cells along with dysplastic squamous cells is a common cytological feature of SCC. Invasiveness and regional and distant metastatic poten- tial should be addressed in evaluation of the patient. Surgical excision would be the optimal treatment option.
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고슴도치의 구강 편평상피암종의 세포학적 고찰 1증례
조향미·최을수·이해범1
전북대학교 수의과대학
요 약 : 3세령의 암컷 고슴도치(Atelerix albiventris)가 심하게 종대된 하악 병변의 평가를 위해 내원하였다. 세포학적 검사를 위해 세침흡인을 실시하였으며, 도말표본을 제작 후 로마노프스키식 염색으로 염색하였다. 세포학적 검사에서 원형을 포함한 다양한 모양의 편평상피세포가 주로 관찰되었으며, 일부 세포는 유사 방추 모양 또는 매우 길쭉한 모 양을 띄고 있었다. 세포학적 소견은 편평상피암종이었으며, 조직검사를 위해 수술적으로 제거하였다. 조직병리상 악성 편평상피암종세포들이 중등도의 콜라겐과 방추형 섬유모세포로 이루어진 간질에 둘러싸여 있었으며, 인접한 골격근과 골조직으로의 침습이 관찰되었다. 종양세포는 중등도의 세포 대소부동과 핵 대소부동을 보였으며, 중등도 이상의 각화 상태를 보였다. 종양의 중심부에서는 극세포해리가 있었으며 림프형질세포 및 호중구성 염증소견이 동반되었다. 유사 분열상은 고배율에서 2-3개가 관찰되었다. 이와 같은 소견에 기초해서 편평상피암종으로 진단하였으며, 보호자는 종괴 의 수술적 제거 후 더이상의 치료를 원치 않아 바로 퇴원하였다. 환자는 추가 처치 없이 3개월 생존 후 폐사하였다.
주요어 : 편평상피암종, 세포학, 방추 모양 세포, 고슴도치
