Surgical Resection of a Mature Teratoma on the Head of a Young Cat

Introduction

Teratomas are complex tumors composed of multiple tissues foreign to the part of the body in which they arise.¹ They originate from pluripotent germ cells that undergo somatic differentiation into two or usually three embryonic germ cell layers, and a variety of mature tissues are arranged chaotically throughout the tumor.² Any combination of ectodermal (skin and appendages), mesodermal (osseous, cartilaginous, adipose, or muscle structures), and endodermal tissues (glandular tissues) can be seen.^3–5

Very few feline teratomas have been reported.^1,2,4,6–10 They most commonly originate from the ovary or testicle because of their germ cell origin.² To the authors’knowledge, only two cases of an extragonadal teratoma have previously been reported in cats. Chénier et al described a kitten with an intracranial teratoma.⁸ Location and secondary lesions prohibited surgical treatment, and euthanasia was elected. Wray et al described a cat with a retrobulbar teratoma that was successfully treated by surgical excision.⁹

This article describes the successful excision of a mature extragonadal teratoma located on the skull of a 4-month-old kitten.

Case Report

A 3-month-old, domestic shorthair kitten was presented for examination of a soft mass, measuring 5 × 6 × 3 cm, on the head over the temporal area near the base of the left ear [Figure 1]. The mass had reportedly been present 2 weeks prior to presentation when this stray kitten was found and adopted by the current owner. At that time, the mass was approximately 2 cm in diameter. Radiographs revealed a soft tissue swelling on the left side of the cranium, with a heterogeneous opacity including areas of mineralization [Figure 2]. On cytological examination of a fine-needle aspirate, keratinocytes were observed along with keratinaceous debris on an amorphous background. Further diagnostic options (i.e., computed tomography [CT] scan and biopsy) were recommended to the owner but were not pursued at that time.

Because the mass continued to grow, the kitten was reevaluated 1 month later. The soft tissue mass extended from the lateral commissure of the eye to the caudal extent of the skull and completely enveloped the ear base and pinna (10 × 15 × 8 cm). Further staging of the disease was performed. Regional lymph node aspirates and thoracic radiographs did not show any signs of metastasis. Cytological examinations of aspirates of the tumor at various locations were performed. These revealed the same hypocellular material that was again considered nondiagnostic. The owner declined a biopsy procedure, and the decision was made to perform CT scans to determine tumor margins and invasiveness and then to remove the tumor as an excisional biopsy [Figure 3].

The kitten was given xylazine^a (1 mg/kg intramuscularly) and induced with propofol^b (4 mg/kg intravenously [IV] to effect). An endotracheal tube was placed, and anesthesia was maintained with isoflurane in oxygen, using a semi-closed rebreathing system.^c Prior to surgery, the kitten received amoxicillin^d (10 mg/kg IV) and carprofen^e (4 mg/kg IV). During surgery, fentanyl^f was administered at 5 μg/kg per hour.

The mass was removed according to commonly recognized principles of oncological surgery.¹¹ An attempt was made to perform local wide excision; however, at some locations the plane of dissection was close to the tumor’s pseudocapsule (marginal resection)¹² [Figure 4]. Superficial cutaneous and auricular muscles were transected. The temporal fascia was incised along the left side of the external sagittal crest. Dorsal to the zygomatic process, the temporal and masseter muscles were transected. The ear canal was resected at the external auditory meatus. The facial nerve was sacrificed because of its entry into the mass. After tumor resection, the entire parietal and part of the temporal bones were exposed [Figure 5]. To prevent drooping of the lateral eye commissure, the orbicularis oculi muscles were attached to the remaining muscle fascia at the external sagittal crest with two horizontal mattress sutures (polypropylene 4-0)^g [Figure 6]. In the same manner, the auricular muscles from the right side were reattached to this medial ridge. A single pedicle advancement flap from the neck was used to close the skin defect [Figure 7]. The subcutaneous tissues were apposed with simple interrupted sutures (polydioxanone 3-0),^h and the skin was closed with a continuous intradermal suture (polyglecaprone 4-0).ⁱ

Postoperatively, a pressure bandage was placed around the skull (in a figure-of-eight pattern around the contralateral ear) for the first 48 hours. The left eye was lubricated with hypromellosum.^j Analgesia was provided with morphine^k (0.3 mg/kg per hour for 19 hours) and carprofen (4 mg/kg orally q 24 hours for 3 days).

The mass was fixed in neutral-buffered formalin (10%) and processed for paraffin sectioning, and 5-μm sections were stained with hematoxylin and eosin according to standard techniques. Microscopic examination revealed the following: cystic cavities that were lined by stratified epithelium and often filled with keratinized squamous cells and hair shafts; cysts lined by pseudostratified ciliated epithelium; numerous hair follicles and hair bulbs; multifocal islands of hyaline cartilage; adipose tissue; and spindle cell proliferation [Figure 8]. These findings are consistent with the diagnosis of a teratoma. Surgical margins were evaluated and considered to be free of abnormal cells.

On follow-up examination 2 weeks later, the wound had healed unremarkably. As was expected, no blinking of the left eyelids nor a palpebral reflex were observed. Opening of the mouth during eating or yawning was neither limited nor painful. Eye medication had previously been discontinued without consequence. Digital photographs [Figure 9] sent in by the owner and a telephone consultation 3 years later revealed that the cat had a normal quality of life without any signs of recurrence.

Discussion

This report describes an extragonadal teratoma in a 4-month-old kitten. A literature review found only nine other cases of teratomas in the cat.^1,2,4,6–10 The median age of these nine cats was 3 years (range 4 months to 17 years). The young age at presentation in this case is most likely due to the extragonadal location, where tumors are more easily recognized by the owner. This is reflected in the different presentation ages between cats with gonadal (mean 3 years, median 4.9 years) and extragonadal teratomas (mean and median 1.7 years).

Few conclusions can be made regarding the location of the teratoma in the present case, because the incidence of this tumor in cats is low (0.7% to 3.6%).³

In humans, extracranial teratomas of the head and neck region are rare.^13,14 Most are diagnosed around birth and during the first 3 months of life.¹⁴ Complete surgical excision has the lowest relapse rate¹⁴ and the highest probability for event-free survival.¹⁵

In animals, teratomas are most common in horses, and rare cases of temporal teratomas (i.e., open mass-like lesions or cystic tumors of the temporal bone occurring inferior to the ear canal) have been described only in horses.^16,17 In small animals, Lambrechts et al described a 1.5-year-old dog with a mandibular teratoma originating from the salivary gland.¹³ Seven months after treatment, this dog was clinically normal. More recently, Wray et al described a 3-year-old cat with a small retrobulbar teratoma. The mass was successfully removed surgically, but no data regarding follow-up were presented.⁹

Although cytology is a common method for diagnosing tumors, in this case cytological examination was not sufficient to diagnose the tumor type. The presence of several cell types and an amorphous background are considered typical of a (mature) teratoma. In some cases, however, one of these elements may dominate the cytological picture.¹⁸ Findings in this case were a moderately cellular sample that yielded only keratin debris and mature keratinocytes with pyknotic nuclei. Further evidence of a teratoma was not found, and the sample was considered to be nondiagnostic. This corresponds with the two other clinical case reports of lateral teratomas (i.e., feline retrobulbar teratoma and canine salivary gland teratoma), which both described inconclusive cytology results.^9,13

Before surgical tumor excision is performed, a definitive diagnosis obtained via biopsy is typically recommended.¹¹ The information gathered can help predict prognosis prior to surgery and guide the surgeon with regard to the extent of surgical resection (e.g., intralesional, marginal, wide and en-bloc resection).¹⁹ In this case, an anesthetic procedure to perform an incisional biopsy was suggested to the owner but was declined. Since further staging at a later date did not confirm the presence of metastasis, it was felt that surgical excision, although very invasive, provided a chance for local tumor control.

The extent of surgery was determined based on the CT scan. A heterogeneous tumor was shown to be connected to the dorsolateral structures of the skull (i.e., pinna, ear canal, parotid gland) and was limited to these soft tissues with no invasion into the neurocranium. Because of the young age of the animal, the fast growth rate of the tumor, and an undefined tumor type, an aggressive local tumor excision was believed to provide the best chance for long-term local tumor control.¹²

The original goal of performing a local wide excision was not achieved. During manipulation of the tumor (because of the loose adherence of the overlying skin), the tumor pseudocapsule became visible. Also, the location of the ear base lacked a deep fascial plane, which is required to achieve a local wide excision. Since part of the dissection was close to the tumor pseudocapsule, this surgery can only be considered as a marginal resection. Nevertheless, complete tumor-free margins were achieved. In this kitten, marginal resection would still have resulted in removal of the ear and the facial nerve; however, a marginal resection would have allowed the preservation of large parts of the temporal and masseter muscles and the overlying skin.

Techniques for the reconstruction for head wounds include local flaps, indirect flaps, axial pattern flaps, free skin grafts, and free tissue transfer. The technique used depends on the availability of local skin, the size of the defect, and location.¹⁹ An axial pattern flap technique was not used, because both the superficial temporal and the caudal auricular arteries and veins were sacrificed during tumor resection, leaving only the more distant omocervical vessels. A local single pedicle advancement flap was chosen because of the abundant amount of loose skin available in the neck. This technique is straightforward and is esthetically preferable, because it maintains the direction of hair growth and creates smaller “dog ears.” An advancement flap is limited in the amount of tissue it brings in, and it is susceptible to tension; therefore, it should be used cautiously close to the eyelids.¹⁹

The facial nerve supplies motor innervation to the muscles of facial expression (including muscles of the eyelids, ear, nose, cheeks, and lips) and the caudal portion of the digastric muscle. It also supplies parasympathetic fibers to the palate, to the rostral two-thirds of the tongue for taste, and to all major exocrine glands of the head (e.g., lacrimal and salivary) except the parotid and zygomatic salivary glands. The facial nerve is also sensory to the external ear canal. Clinical manifestations of facial nerve paralysis in cats include an inability to close the eyelid, move the lips, and move the ear. Affected animals are unable to blink spontaneously or in response to visual or palpebral sensory stimulation. Drooping of the ear and lip as a result of absent muscle tone on the affected side is common.²⁰ In cats, however, the firm subcutaneous maxillary plane allows complete facial paralysis to be accompanied by an almost normal position of the lip.²¹ Keratoconjunctivitis sicca may develop following loss of facial nerve-stimulated lacrimal gland secretion.²⁰ During the nerve’s course through the facial canal in the petrosal bone, the parasympathetic and sensory fibers leave the main trunk of the facial nerve to form the tympanic nerve. The main trunk of the facial nerve exits at the stylomastoid foramen, while the tympanic nerve follows a different course and runs through the middle ear.²²

In this kitten, the facial nerve was cut after it exited the stylomastoid foramen, so only the motor branches were cut. The intact stimulation of the lacrimal gland was apparently able to compensate for the inability to blink, and this explains why it was possible to discontinue the tear drops 1 week after surgery without adverse effects. The other reason is that the retractor bulbi muscle, which is innervated by the abducens nerve, pulls the globe caudally and allows the lids and nictitans to close passively to some extent, aiding in the distribution of lubricating tears.²²

Young cats are at risk of developing middle ear disease by extension of pharyngeal viral or bacterial pathogens through the eustachian tube.²³ In this kitten, the entire external ear canal was resected, leaving the tympanic membrane intact. A lateral bulla osteotomy to remove the epithelial lining of the tympanic bulla was not performed. The normal route of drainage of middle ear epithelial secretions is through the auditory (eustachian) tube. Obstruction of this tube with concurrent otitis media can give rise to abscess formation which, because of the absence of an external ear canal, can extend into the subcutaneous space.^24,25 The owner was asked to pay specific attention to respiratory infections and swellings of the surgical site. Three years after surgery, no complications have been observed.

In the World Health Organization’s histological classification based on the cellular morphology of the tumor, human teratomas are commonly classified using the Gonzalez-Crussi grading system. According to this system, 0 or mature is benign; 1 or immature is probably benign; 2 or immature is possibly malignant; and 3 or immature is malignant. Teratomas are also classified by their content. A solid teratoma contains only tissues, perhaps including more complex structures. A cystic teratoma contains only pockets of fluid or semifluid, such as cerebrospinal fluid, sebum, or fat. A mixed teratoma contains both solid and cystic parts.²⁶

Prognosis is primarily dependent on the nature of the teratoma. Mortality in children is dictated by malignant histology and, in the case of mature teratomas, by occurrence at certain sites.¹⁵ In humans, the metastatic rate is only 5%, with the majority of tumors being local and metastasis believed to occur through the lymphatic vessels.^1,27 In dogs, the metastatic potential for an immature teratoma (terato-carcinoma) is much higher at 32%.^3,28 Local metastases have been reported in multiple abdominal sites, and distant metastases have been reported in the lungs, the cranial mediastinum, and bone. No similar data are available for cats because of the small number of cases described, but malignancy and metastasis have both been documented.^1,10 Norris (1969) describes a solid teratoma in a cat with dysgerminomas; the tumor grew invasively and extended through the abdominal wall.¹⁰ Although this tumor was considered malignant, no metastases could be documented. A later case report described a teratoma in a cryptorchid testis of a 2-year-old cat with a histologically confirmed meta-static mass in the omentum.¹ One month later, abdominal ultrasonography was performed, and findings were suggestive of abdominal metastases. Because no postmortem examination was performed, it was unclear whether metastasis occurred via lymphatics or simply by implantation.

In contrast to immature teratomas, mature (benign) teratomas only cause clinical signs in relation to their size, and the prognosis depends on the location (i.e., the feasibility of complete surgical resection). For gonadal teratomas in dogs, survival times of up to 6 years have been reported.²⁷

Conclusion

This report documents the appearance of an extragonadal mature teratoma in a kitten. It was not possible to diagnose this tumor using cytology, and an aggressive excisional biopsy was performed. Marginal surgical resection proved sufficient to completely remove the tumor. Prognosis for an extragonadal teratoma is dependent on tumor type (malignancy) and location. When complete excision of this sometimes fast-growing tumor is achieved, surgical treatment has the potential to be curative. This type of tumor, although rare, should be listed in the differential diagnosis for head and neck tumors in kittens.

Acknowledgments

The authors are grateful to Dr. Ingrid Gielen from the Medical Imaging Department for providing the radiographic and CT scan images. Our special appreciation goes to Professor Dr. Jolle Kirpensteijn, from Utrecht University, for his valuable advice during the writing of this manuscript.