Craniopharyngiomas are benign epithelial tumors of the. Malignant Craniopharyngioma
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1 Malignant Craniopharyngioma Theresa Kristopaitis, MD; Chinnamma Thomas, MD; Guy J. Petruzzelli, MD, PhD; John M. Lee, MD, PhD Craniopharyngiomas are histologically and cytologically benign epithelial tumors of the central nervous system that may be locally aggressive and tend to recur after excision. Malignant change in craniopharyngiomas is extremely rare; we found only 4 such reports in the literature. In this report, we describe a case of squamous cell carcinoma arising in a previously benign craniopharyngioma in a 42-yearold woman. The patient was diagnosed with craniopharyngioma in 1982; during the subsequent 15 years she experienced 7 tumor recurrences, for which surgical resections and 3 courses of radiotherapy were performed. In 1998, the tumor recurred with involvement of the nasal cavity and sphenoid and ethmoid sinuses. Histologic evaluation revealed foci of typical adamantinomatous craniopharyngioma associated with a moderately differentiated squamous cell carcinoma. The transition of typical craniopharyngioma to squamous cell carcinoma was well demonstrated, suggesting that carcinoma arose from the underlying craniopharyngioma. Radiation may have been a contributing factor to carcinogenesis in this case. (Arch Pathol Lab Med. 2000;124: ) Craniopharyngiomas are benign epithelial tumors of the central nervous system that characteristically arise in the infundibulohypophyseal axis in the sellar and suprasellar areas. They comprise approximately 3% of all intracranial tumors and have a bimodal age distribution; the majority of these tumors occur during the first 2 decades of life, and a small proportion occur in the seventh and eighth decades. 1 These generally slow-growing tumors may reach large sizes before becoming clinically symptomatic. Although benign, craniopharyngiomas may be locally aggressive, invading into neighboring tissue and adhering to blood vessels and nerves. In turn, they have a well-recognized propensity to recur after surgical excision, particularly if the resection is incomplete. 2 Both locally aggressive and recurrent craniopharyngiomas are histologically and cytologically benign. Malignant change in craniopharyngiomas is distinctly rare. There has been one such report of malignant transfor- Accepted for publication January 4, From the Departments of Pathology (Drs Kristopaitis, Thomas, and Lee) and Otolaryngology (Dr Petruzzelli), Loyola University Medical Center, Maywood, Ill. Presented as a poster at the Annual Meeting of the American Association of Neuropathology, Portland, Ore, June 19, Reprints: John M. Lee, MD, PhD, Department of Pathology, Loyola University Medical Center, EMS Building, 2nd Floor, 2160 S First Ave, Maywood, IL mation to squamous cell carcinoma in the English literature and 3 reports in the Japanese literature. 3 5 In addition, there is a single case report in the veterinary literature of a spontaneously occurring, metastasizing, malignant craniopharyngioma in an albino rat, an event as uncommon in animals as it is in humans. 6 We report a case of craniopharyngioma with multiple recurrences and subsequent malignant transformation 15 years after the initial diagnosis. REPORT OF A CASE In 1982, at 27 years of age, the patient presented with bilateral hemianopsia and underwent transphenoidal resection of a typical craniopharyngioma. Three years later the craniopharyngioma recurred. Open craniotomy was performed with subtotal removal of the tumor and cyst drainage. External beam radiation (52 Gy in 30 fractions) was delivered to the pituitary/suprasellar region. In 1988, the patient underwent craniotomy followed by transphenoidal resection for recurrence. In 1992, intracranial stereotactically guided iodine 125 implants delivered a radiation dose to the tumor of cgy over 87 days. Despite radiotherapy the craniopharyngioma progressed, and the patient underwent an extensive craniofacial resection in Three years later, stereotactic radiosurgery was performed. In 1996, at 40 years of age, the patient developed temporal lobe seizures secondary to recurrence of typical craniopharyngioma. At age 42 years in 1998, the patient displayed complications resulting from multiple craniopharyngioma recurrences and resections, including panhypopituitarism, blindness in her right eye, a residual visual field defect in her left eye, and temporal lobe seizures. Magnetic resonance imaging showed a mass bilaterally in the nasopharynx and the sphenoid sinuses (Figure 1). The clivus on the right side and centrally was also destroyed by tumor. The tumor displaced the inferior limb of the right carotid siphon. Tumor was endoscopically resected. PATHOLOGIC FINDINGS Tissue sections submitted from the previous resections in 1994 and 1996 and from the most recent resection in 1998 for histologic examination were reviewed. The 1994 and 1996 resections showed histopathologic features characteristic of a classic adamantinomatous craniopharyngioma (Figure 2). Loose collections of polygonal epithelial cells were arranged in anastomosing nests and trabeculae. A palisading basal layer of small cells with darkly staining nuclei surrounded the nests. In the center of the epithelial nests were laminated layers and whorls of squames recognized as wet keratin. There was background connective tissue stroma. The mitotic count was less than 1 per 10 high-power fields. No cytologically atypical features 1356 Arch Pathol Lab Med Vol 124, September 2000 Malignant Craniopharyngioma Kristopaitis et al
2 Figure 1. Magnetic resonance imaging of the brain reveals tumor in the nasopharynx and skull base in the clivus and sphenoid sinus regions. In addition, the image shows bifrontal encephalomalacia, most likely secondary to the previous craniotomies. were noted. Fragments of bone showed tumor invasion, a finding not unusual in typical craniopharyngiomas. In the 1998 resection, there were areas of typical adamantinomatous craniopharyngioma. However, the majority of lesion showed hypercellular areas composed of squamous cells with nuclear pleomorphism, increased nuclear-cytoplasmic ratios, and hyperchromatism. An increased number of mitotic figures, which ranged up to 5 per high-power field and included atypical mitotic figures, was present. Pearls of wet keratin were present both within the foci of typical craniopharyngioma and within areas with squamous cell carcinoma (Figure 3). Transformation zones consisting of adjacent foci of squamous cell carcinoma and craniopharyngioma were demonstrated (Figure 4). The final diagnosis was a moderately differentiated squamous cell carcinoma arising in a craniopharyngioma. Immunohistochemical staining for p53 (Dako Corporation, Carpinteria, Calif, 1:50 dilution) was performed on paraffin-fixed tissue. Focal squamous cell carcinoma nuclei were strongly positive for p53; in some areas up to 75% of the nuclei displayed immunoreactivity. Within the areas of typical craniopharyngioma, p53 was expressed in fewer than 10% of the nuclei (Figure 5). CLINICAL FOLLOW-UP An extensive clinical workup showed no evidence of metastatic squamous cell carcinoma. Palliative systemic chemotherapy (paclitaxel and carboplatin) was administered. After 3 cycles, there was significant reduction in the unresected portion of the mass; however, residual tumor did remain in the right infratemporal fossa, extending up to the level of the floor of the right middle cranial fossa and in the right petrous bone. Six months after the diagnosis of squamous cell carcinoma was rendered, followup magnetic resonance imaging scans of the head showed growth and extension of the tumor. Pathologic examination of the incompletely resected mass demonstrated typical adamantinomatous craniopharyngioma with foci of necrotic material but no evidence of squamous cell carcinoma. COMMENT Patients with craniopharyngiomas generally present with 3 major clinical syndromes related to (a) increased intracranial pressure, (b) endocrine dysfunction caused by compression of the hypothalamic-hypophyseal axis, or (c) visual problems resulting from direct compression of the optic pathways by the tumor, secondary intracranial hypertension, or both. 1,2 Craniopharyngiomas are hypothesized to develop from remnants of Rathke s pouch and in a strict sense are malformative, trapped elements of nonneoplastic tissue of the central nervous system with linear growth curves. 7 There are 2 recognized histologic variants of craniopharyngioma, the adamantinomatous type like that seen in this case and the papillary variant. A mixture of both types is frequently present. Grossly, the adamantinomatous variant is characterized by cysts, calcification, and cholesterol droplets, giving a motor oil content. Papillary craniopharyngiomas lack motor oil contents and are more typically solid rather than cystic. The papillary variant is formed microscopically of well-differentiated, stratified, squamouslike epithelium and an anastomosing fibrovascular stroma, resulting in the formation of prominent papillae. 8 While adamantinomatous craniopharyngiomas are poorly circumscribed and frequently exhibit an infiltrative growth pattern, the papillary types are well-circumscribed and do not adhere to local structures. In turn, some authors have observed that the papillary variant may be more amenable to complete surgical resection and may have a more favorable outcome, but this issue is still being debated in the literature One of the most challenging aspects in the treatment of craniopharyngiomas is prevention of recurrence. After gross total resection, the recurrence rate is approximately 20%, but tumors incompletely resected have recurrence rates up to 60%. 2,9 Repeat surgeries may make complete surgical resection even more difficult, with each subsequent attempt having higher morbidity. 2 Radiation therapy has shown to benefit patients with incomplete surgical resection, decreasing tumor recurrence rates to about 30%. 2,9 Overall, there is an 80% 5-year survival rate for patients with these benign central nervous system lesions. 12 A distinctly rare complication of craniopharyngioma is malignant transformation. In this case, the presence of squamous cell carcinoma adjacent to and within areas showing features of a typical adamantinomatous craniopharyngioma supports that carcinoma arose from the un- Arch Pathol Lab Med Vol 124, September 2000 Malignant Craniopharyngioma Kristopaitis et al 1357
3 1358 Arch Pathol Lab Med Vol 124, September 2000 Malignant Craniopharyngioma Kristopaitis et al
4 derlying craniopharyngioma. In addition, foci of wet keratin, which are distinctive and diagnostic of craniopharyngiomas, were present in both the benign and malignant components. 8 There is little information regarding the natural history of malignant transformation of craniopharyngiomas. 3 5 Nelsonetal 3 described a 48-year-old patient who developed malignant change 35 years after initial diagnosis of craniopharyngioma; this patient died secondary to complications of upper gastrointestinal bleeding and pneumonia. Six months after diagnosis of squamous cell carcinoma, our patient s tumor increased in size, but the resected tissue was a benign craniopharyngioma. The mechanism for malignant transformation in craniopharyngioma is currently unknown. Nelson et al 3 suggested a causal relationship between radiation therapy and malignant transformation of craniopharyngiomas. The occurrence of neoplasms after radiotherapy is well documented. 13,14 Radiation therapy for craniopharyngiomas has been implicated in the development of secondary neoplasms in 5 cases In their study of the side effects of radiation therapy for benign brain tumors in adults, Al- Meftyetal 20 reported that the latency for secondary neoplasms ranges from 4 years to 30 years, with a median of 12.5 years. Our patient received multiple courses of radiation therapy over a 15-year period. Therefore, it is possible that radiation may have been a contributing factor to the development of the squamous cell carcinoma in this case. However, the vast majority of cases in which radiation has been used to prevent recurrence of craniopharyngioma have not resulted in transformation to a squamous cell carcinoma. Therefore, radiation-induced malignant transformation is a distinctly rare event. Additional evidence that radiation may have contributed to carcinogenesis in this case is the immunohistochemical expression of p53 in the squamous cell carcinoma. Animal research as well as in vitro analyses of human tumors have demonstrated that the development of delayed mutations in p53 following irradiation may be one step in the sequence leading to radiation-induced neoplasia. 21,22 The p53 tumor suppressor gene controls cellular growth after DNA damage through mechanisms involving growth arrest and apoptosis. 23 Mutation of the p53 gene can lead to loss of cell cycle control, genetic instability, and neoplastic growth. 23 The wild-type p53 protein is present in very low levels in tissue; mutations of the p53 tumor suppressor gene stabilize the p53 protein and extend its half-life, enabling detection with immunohistochemical methods The ability to detect p53 with immunohistochemistry closely correlates with the presence of a p53 gene mutation in some tumors, such as squamous cell carcinoma of the esophagus. 24,26,27 In other tumors, such as squamous cell carcinomas of the head and neck, immunohistochemical expression of p53 may not always reflect mutation of the p53 gene. 28,29 For example, Xu et al 29 demonstrated 60% concordance between immunohistochemical expression of p53 and gene mutations detected by single-strand conformational polymorphism analysis in squamous cell carcinomas of the head and neck. Although malignant transformation in craniopharyngiomas is uncommon, pathologists should be aware of its occurrence. Confusion ought not to be made with benignappearing tongues and nests of craniopharyngioma in surrounding areas of nervous tissue. Local invasion, particularly in adamantinomatous craniopharyngiomas, is characteristic and not a sign of malignancy. 1 However, dysplastic features in craniopharyngiomas, particularly in patients having had radiotherapy, should be critically examined and noted. References 1. Thapar K, Kovacs K. Neoplasms of the sellar region. In: Bigner DD, Mc- Lendon RE, Bruner J, eds. Russel and Rubinstein s Pathology of Tumors of the Nervous System. New York, NY: Oxford University Press; 1998: Samii M, Tatagiba M. Craniopharyngioma. In: Kaye AH, Laws ER, eds. Brain Tumors. London, England: Churchill Livingstone; 1995: Nelson GA, Bastian FO, Schlitt M, White RL. Malignant transformation in craniopharyngioma. Neurosurgery. 1988;22: Akachi K, Takahashi H, Ishijima B, et al. Malignant changes in a craniopharyngioma. No Shinkei Geka. 1987;15: Suzuki F, Konuma I, Matsumoto M, Aoki M, Hayakawa I. Craniopharyngioma with malignant transformation: a report of two cases. Gan No Rinsho. 1989; 35: Pace V, Heider K, Persohn E, Schaetti P. Spontaneous malignant craniopharyngioma in an albino rat. Vet Pathol. 1997;34: Powers JM, Horoupian DS. Central nervous system. In: Damjanov I, Linder J, eds. Anderson s Pathology. 10th ed. St Louis, Mo: Mosby; 1996: Burger PC, Scheithauer BW, Vogel FS, eds. Surgical Pathology of the Nervous System and Its Coverings. 3rd ed. New York, NY: Churchill Livingstone; 1991: Weiner HL, Wisoff JH, Rosenberg ME, et al. Craniopharyngiomas: a clinicopathological analysis of factors predictive of recurrence and functional outcome. Neurosurgery. 1994;6: Eldevik OP, Blaivas M, Gabrielsen TO, Hald JK, Chandler WF. Craniopharyngiomas: radiologic and histologic findings and recurrence. AJNR Am J Neuroradiol. 1996;17: Adamson TE, Wiestler OD, Kleihues P, Yasargil MG. Correlation of clinical and pathological features in surgically treated craniopharyngiomas. J Neurosurg. 1990;73: Bunin GR, Surawica TS, Witman PA, et al. The descriptive epidemiology of craniopharyngioma. J Neurosurg. 1998;89: Kohn HI, Fry RJM. Radiation carcinogenesis. N Engl J Med. 1984;310: Levitt SH. Secondary malignancies after radiotherapy. In: Dunst J, Sauer R, eds. Late Sequelae in Oncology. Berlin, Germany: Springer-Verlag; 1995: Komaki S, Komaki R, Choi H, Correa-Raz F. Radiation- and drug-induced intracranial neoplasm with angiographic demonstration. Neurol Med Chir. 1977; 17: Matt-Schieman MLC, Bots GTAM, Thomeer RTWM, Vielvoye GJ. Malignant astrocytoma following radiotherapy for craniopharyngioma. Br J Radiol. 1986;58: Sogg RL, Donaldson SS, Yorkee CH. Malignant astrocytoma following radiotherapy of a craniopharyngioma. J Neurosurg. 1978;48: Ushio Y, Arita N, Yoshimine T, Nagatani M, Mogami H. Glioblastoma after radiotherapy for craniopharyngioma: a case report. Neurosurgery. 1987;21: Figure 2. Typical adamantinomatous craniopharyngioma consisting of trabeculae with a palisading basal layer surrounding loosely cohesive squamous cells and nodules of wet keratin (hematoxylin-eosin, original magnification 40). Figure 3. Squamous cell carcinoma with cells exhibiting nuclear pleomorphism, increased nuclear-cytoplasmic ratio, mitoses, and the presence of wet keratin (hematoxylin-eosin, original magnification 400). Figure 4. Transformation of typical craniopharyngioma composed of squamous cells separated by stellate reticulum adjacent to squamous cell carcinoma (left) (hematoxylin-eosin, original magnification 400). Figure 5. Strong nuclear immunohistochemical expression of p53 in squamous cell carcinoma (top) in contrast to typical craniopharyngioma, in which few nuclei show p53 expression (original magnification 400). Arch Pathol Lab Med Vol 124, September 2000 Malignant Craniopharyngioma Kristopaitis et al 1359
5 19. Waga S, Handa H. Radiation-induced meningioma: with review of literature. Surg Neurol. 1976;5: Al-Mefty A, Kersh JE, Routh A, Smith RR. The long-term side effects of radiation therapy for benign brain tumors in adults. J Neurosurg. 1990;73: Kemp CJ, Wheldon T, Balmain A. p53-deficient mice are extremely susceptible to radiation-induced tumorigenesis. Nature Genet. 1994;8: Nakanishi H, Tomita Y, Myoui A, et al. Mutation of the p53 gene in postradiation sarcoma. Lab Invest. 1998;78: Velculescu VE, El-Deiry WS. Biological and clinical importance of the p53 tumor suppressor gene. Clin Chem. 1996;42: Ullrich RL, Ponnaiya B. Radiation-induced instability and its relation to radiation carcinogenesis. Int J Radiat Biol. 1998;74: Raybaud-Diogene H, Tetu B, Morency R, Fortin A, Monteil RA. p53 overexpression in head and neck squamous cell carcinoma: review of the literature. Eur J Cancer B Oral Oncol. 1996;32B: Lane DP, Benchimol S. p53: oncogene or anti-oncogene? Genes Dev. 1990;4: Wagata T, Shibagaki I, Imamura M, et al. Loss of 17p, mutation of the p53 gene, and overexpression of p53 protein in esophageal squamous cell carcinoma. Cancer Res. 1993;53: Nylander K, Nilsson P, Mehle C, Roos G. p53 mutations, protein expression and cell proliferation in squamous cell carcinomas of the head and neck. Br J Cancer. 1995;71: Xu L, Chen YT, Huvos AG, et al. Overexpression of p53 protein in squamous cell carcinomas of head and neck without apparent gene mutations. Diagn Mol Pathol. 1994;3: Arch Pathol Lab Med Vol 124, September 2000 Malignant Craniopharyngioma Kristopaitis et al
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