Craniopharyngiomas are locally aggressive lesions of
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1 CASE REPORT Recurrent papillary craniopharyngioma with BRAF V600E mutation treated with dabrafenib: case report Benjamin T. Himes, MD, 1 Michael W. Ruff, MD, 2 Jaimie J. Van Gompel, MD, 1 Sean S. Park, MD, PhD, 3 Evanthia Galanis, MD, 4 Timothy J. Kaufmann, MD, 5 and Joon H. Uhm, MD 2,4 Departments of 1 Neurological Surgery, 2 Neurology, 3 Radiation Oncology, 4 Oncology, and 5 Radiology, Mayo Clinic, Rochester, Minnesota The authors present the case of a man with a papillary craniopharyngioma, first diagnosed at 47 years of age, who experienced multiple recurrences. Review of the pathologic specimen from his first resection demonstrated the BRAF V600E mutation. With his most recent recurrence following previous surgery and radiotherapy, at 52 years of age, the decision was made to initiate treatment with the BRAF V600E inhibitor dabrafenib. Imaging following initiation of dabrafenib demonstrated reduction in tumor size. He remained on dabrafenib therapy for approximately 1 year and continued to demonstrate a good clinical result. At that time the decision was made to discontinue dabrafenib therapy and follow up with serial imaging. After more than 1 year of follow-up since stopping dabrafenib, the patient has continued to do well with no radiographic evidence of tumor progression and continues to be monitored with frequent interval imaging. KEYWORDS papillary; craniopharyngioma; dabrafenib; BRAF V600E; oncology Craniopharyngiomas are locally aggressive lesions of the suprasellar space that occur in two distinct histopathological subtypes. Adamantinomatous craniopharyngiomas tend to occur in a bimodal distribution, with peaks in childhood and middle age, while papillary craniopharyngiomas develop in adults. 3,11,12 Papillary craniopharyngiomas represent a distinct minority of cases, as few as 11% in some series. 11 Both histologies exhibit a similar clinical course, with frequent recurrences despite aggressive local resection and subsequent radiation. 6 These lesions can present with a morbid clinical picture due to compression of the optic chiasm, pituitary stalk, and hypothalamus. Adherence to these critical structures can limit the ability of the surgeon to completely resect the lesion, placing patients at risk for recurrence. In circumstances in which there is a persistent lesion despite aggressive resection and subsequent radiation treatment (the current standard of care), there is a need to explore additional therapeutic avenues to improve longterm disease control while minimizing treatment-related morbidities. Papillary craniopharyngiomas frequently carry a mutation in the BRAF gene, of which the V600E mutation is a common alteration, affecting as many as 95% of tumors. 2,8 This mutation results in constitutive activation of the gene and the associated downstream MAP kinase pathway, leading to increased cellular proliferation. 2,7 The biological importance of the BRAF V600E mutation and targeted therapies directed toward the mutant protein have been pioneered in melanoma, 5 and one reported case of treatment of a papillary craniopharyngioma with inhibitors SUBMITTED September 22, ACCEPTED November 10, INCLUDE WHEN CITING Published online April 27, 2018; DOI: / JNS AANS 2018, except where prohibited by US copyright law J Neurosurg April 27,
2 of BRAF V600E (dabrafenib) and MAP kinase pathway (trametinib) resulted in an 85% reduction in tumor volume following treatment. 1 In this report we present a case of a patient with a recurrent papillary craniopharyngioma who previously underwent surgery and radiotherapy, which was salvaged with dabrafenib and led to a radiographic response that was sustained through 1 year of therapy. The patient has remained free of tumor progression for more than 1.5 years since discontinuing dabrafenib. Case Report History and Examination A 47-year-old man with a remote history of non-hodgkin lymphoma presented with visual loss and color blindness, as well as symptoms of diabetes insipidus. Magnetic resonance imaging revealed a cystic suprasellar lesion concerning for a craniopharyngioma (Fig. 1A and B). He underwent resection of the lesion through a right pterional craniotomy at an outside institution. Histopathological analysis at the time confirmed the lesion to be a papillary craniopharyngioma. He suffered panhypopituitarism postoperatively, requiring replacement with desmopressin, hydrocortisone, and levothyroxine. Subsequent imaging revealed some residual enhancement along the pituitary stalk (Fig. 1C and D). He was followed closely with serial imaging, and an increase in the size of solid tumoral suprasellar enhancement was noted in 2012 (Fig. 1E and F). The patient was clinically asymptomatic from this radiographic recurrence. Complicating his history in the prior year was a diagnosis of stage III colon cancer, treated with partial colectomy and chemotherapy with folinic acid, fluorouracil, and oxaliplatin beginning in January 2012 for 4 cycles. He presented to our institution at this time for a second opinion regarding management of his recurrent craniopharyngioma. Given that his vision was intact despite his disease progression, and due to concern for adhesion between the lesion and the optic chiasm, especially given his prior surgery, the patient underwent radiotherapy in March 2012 consisting of a total dose of 36 Gy in 12 fractions (plan shown in Fig. 2). PET/MRI performed in March demonstrated a metastatic liver lesion and increased uptake in mediastinal lymph nodes, so to facilitate the delivery of adjuvant chemotherapy for his colon cancer he was transitioned to folinic acid, fluorouracil, irinotecan, and bevacizumab; this regimen was later simplified to bevacizumab and capecitabine in late 2012, with continuation of capecitabine alone in December Dabarfenib Therapy and Follow-Up The patient tolerated radiation therapy well and was once again followed with serial imaging. He initially responded well to radiation therapy, with a reduction in the size of the lesion to a 4 5-mm remaining enhancing suprasellar nodule that remained stable for more than 2 years (Fig. 1G and H). He did experience progression of his colon cancer; hypermetabolic left supraclavicular lymph nodes were treated with radiation in late He had no further evidence of disease progression, and ongoing therapy with capecitabine was halted in December However, in early 2015 enlargement of the craniopharyngioma FIG. 1. Axial (left column) and coronal (right column) postcontrast T1- weighted MR images at initial presentation showing a solid enhancing suprasellar mass involving the optic chiasm and hypothalamus (A and B) and after resection (C and D). Subsequent solid enhancing recurrence was noted more than 2 years later (E and F), as well as substantial response following fractionated radiation therapy (G and H). tumor was again noted (Fig. 3A and B). This patient s case was discussed in a neurooncology multidisciplinary board meeting and both surgery and re-irradiation options were not recommended due to the high risk of treatment-related morbidity. He once again remained clinically asymptomatic beyond his hypopituitarism. The fixed tumor specimens from his original resection were obtained to assess for the BRAF V600E mutation. Presence of the mutation was confirmed in his original lesion, and treatment with 2 J Neurosurg April 27, 2018
3 B. T. Himes et al. FIG. 2. Radiotherapy plan for recurrent craniopharyngioma, represented by a sagittal image of CT simulation (A) and a T1weighted post-gadolinium MR image (B). Hypofractionated radiotherapy (36 Gy in 12 fractions) was delivered to facilitate the patient s chemotherapy treatments for his metastatic colon cancer. Radiotherapy was delivered using 6-MV photon 9-field static intensity-modulated radiation therapy to the planning target volume (magenta) with a TrueBeam Linear Accelerator (Varian Medical Systems). Planning target volume coverage was limited by the optic apparatus (cyan), which received a maximum dose of 32.5 Gy. White, green, and blue lines correspond to 100%, 95%, and 90% isodose lines, respectively. Figure is available in color online only. dabrafenib was initiated at 150 mg twice daily. Shortly after the start of dabrafenib therapy, the patient reported joint pain, and the decision was made to reduce the dosage of dabrafenib to 150 mg daily. He tolerated this reduced dose well, and after several weeks the dose was increased to 225 mg daily, which he continued to tolerate well. Imaging obtained approximately 2 months following the initiation of dabrafenib demonstrated enlargement of the cystic component of the tumor, but the volume of the solid enhancing portion had decreased (Fig. 3C and D). Given that the patient s visual fields remained preserved at this time, the decision was made to continue therapy and close observation. Subsequent imaging demonstrated no further enlargement of the lesion and after 6 months of therapy began to demonstrate significant reduction in the size of the both the cystic and solid enhancing components of the lesion. After 9 months of therapy, minimal residual tumor remained, and this remained stable on serial scans until 1 year after the initiation of dabrafenib therapy (Fig. 3E and F). At that time, given the patient s stable disease on multiple imaging studies, the decision was made to transition him off of dabrafenib therapy and to a period of close observation. On subsequent imaging studies, his burden of disease remained stable, with the recent study completed just over 1 year following cessation of dabrafenib therapy (Fig. 3G and H). Discussion Given that craniopharyngiomas are locally aggressive suprasellar tumors, surgical intervention and radiotherapy can result in morbidity secondary to collateral injury to adjacent structures if the tumor is adherent and therefore unable to be removed. Hence, despite aggressive multimodal treatments that comprise the current standard of care, these tumors often recur and are recalcitrant to further treatment. Thus, craniopharyngiomas are an ideal tumor for which to use targeted therapy, as either an adjuvant or potentially up-front treatment.6 There are two main histological subtypes of craniopharyngioma with similar clinical presentation and behavior, i.e., adamantinomatous and papillary.6 The papillary subtype is more frequent in adults.8 BRAF V600E is a targetable mutation, which has recently been described in the majority of papillary craniopharyngiomas.2 BRAF is a protooncogene that encodes a serine/threonine kinase involved in growth factor signaling and regulation. Mutations in BRAF that transform the BRAF kinase into a constitutively active form result in cell proliferation and tumor growth. The BRAF V600E mutation has been described in 7% of human cancers.7 It is targeted in malignant melanoma and non small cell lung cancer using inhibitors such as vemurafenib and dabrafenib, but these agents have also been used as targeted therapy for other tumor types with BRAF V600E mutations, including pleomorphic xanthoastrocytoma, ganglioglioma, and a BRAF V600E mutant glioblastoma with systemic metastases.4,9,10 Recently, a patient with a multiply recurrent BRAF V600E mutant papillary craniopharyngioma was reported as having been treated with dabrafenib and the MEK inhibitor trametinib with an excellent result, remaining symptom-free 7 months into treatment.1 We report the longest known follow-up with a patient with BRAF V600E mutant craniopharyngioma treated with a BRAF V600E inhibitor. In contrast to the prior report, we used dabrafenib monotherapy at a dose of 225 mg daily for 1 year, and report 1 year of follow-up after treatment discontinuation. Of note, initial cystic enlargement observed on the first follow-up MRI performed 2 months following the beginning of dabrafenib treatment in our patient may have been attributable to pseudoprogression in which the initial radiographic progression noted early in treatment is then followed by lesion shrinkage, as was found in our patient. While pseudoprogression is a well-defined phenomenon early after radiation/chemotherapy treatment of patients with glioma, pseudoprogression in the context of BRAF-targeted treatment of papillary craniopharynj Neurosurg April 27,
4 consider the role of the patient s prior radiation in this apparent recurrence. Given that no further tissue sampling was obtained prior to initiation of dabrafenib therapy, it is possible this recurrence represented a late radiation-related treatment effect. However, given the appearance of this recurrence nearly 3 years after completion of radiation, the likelihood of it representing radiation-related transient pseudoprogression is very low. Furthermore, were this lesion to represent true delayed radiation necrosis, we would not anticipate it to improve spontaneously over a relatively short interval. This case lends support to the use of small-molecule inhibitors such as dabrafenib as an additional tool in the challenging treatment of papillary craniopharyngiomas. The case reported here, in conjunction with that recently reported by Brastianos et al. 1 as discussed above, demonstrates that BRAF V600E inhibitors can have a potent effect on these uncommon tumors that harbor the BRAF V600E mutation. Further investigation is needed to determine the appropriate duration, dose, and combination of small-molecule therapeutics used. Regardless, based on our experience, the use of a targeted BRAF V600E inhibitor such as dabrafenib represents a promising therapeutic consideration in patients for whom repeat surgery presents significant risks, and who do not require an emergency decompressive procedure. If papillary craniopharyngiomas could be reliably identified preoperatively, these agents could be used as a neoadjuvant therapy to reduce the preoperative tumor volume and potentially reduce morbidity associated with surgical intervention. An ongoing cooperative group trial (Alliance A071601) is testing the combination of BRAF/MEK inhibition in patients with BRAF V600E mutant craniopharyngioma. FIG. 3. Axial (left column) and coronal (right column) postcontrast T1- weighted MR images, with the exception of panel E, in which no axial contrasted image was available and therefore a T2-weighted FLAIR sequence is shown. A and B: Tumor recurrence 3 years after completion of radiation therapy with solid enhancing and cystic components. C and D: Initial enlargement of the cystic component of the tumor after initiation of dabrafenib therapy but with diminished volume of a solid enhancing component. E and F: Substantial reduction in solid and cystic tumor volume following approximately 9 months of dabrafenib therapy. G and H: Stable imaging over 1 year following cessation of dabrafenib therapy. gioma has not previously been described and therefore may need to be considered when assessing imaging studies for response versus recurrence in upcoming clinical trials evaluating BRAF inhibitors to treat papillary craniopharyngiomas. In this context, it is also important to References 1. Brastianos PK, Shankar GM, Gill CM, Taylor-Weiner A, Nayyar N, Panka DJ, et al: Dramatic response of BRAF V600E mutant papillary craniopharyngioma to targeted therapy. J Natl Cancer Inst 108:108, Brastianos PK, Taylor-Weiner A, Manley PE, Jones RT, Dias- Santagata D, Thorner AR, et al: Exome sequencing identifies BRAF mutations in papillary craniopharyngiomas. Nat Genet 46: , Bunin GR, Surawicz TS, Witman PA, Preston-Martin S, Davis F, Bruner JM: The descriptive epidemiology of craniopharyngioma. J Neurosurg 89: , Chamberlain MC: Recurrent ganglioglioma in adults treated with BRAF inhibitors. CNS Oncol 5:27 29, Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al: Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: , Crotty TB, Scheithauer BW, Young WF Jr, Davis DH, Shaw EG, Miller GM, et al: Papillary craniopharyngioma: a clinicopathological study of 48 cases. J Neurosurg 83: , Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al: Mutations of the BRAF gene in human cancer. Nature 417: , Larkin SJ, Preda V, Karavitaki N, Grossman A, Ansorge O: BRAF V600E mutations are characteristic for papillary craniopharyngioma and may coexist with CTNNB1-mutated adamantinomatous craniopharyngioma. Acta Neuropathol 127: , J Neurosurg April 27, 2018
5 9. Leaver KE, Zhang N, Ziskin JL, Vogel H, Recht L, Thomas RP: Response of metastatic glioma to vemurafenib. Neurooncol Pract 3: , Lee EQ, Ruland S, LeBoeuf NR, Wen PY, Santagata S: Successful treatment of a progressive BRAF V600E-mutated anaplastic pleomorphic xanthoastrocytoma with vemurafenib monotherapy. J Clin Oncol 34:e87 e89, Pekmezci M, Louie J, Gupta N, Bloomer MM, Tihan T: Clinicopathological characteristics of adamantinomatous and papillary craniopharyngiomas: University of California, San Francisco experience Neurosurgery 67: , Zada G, Lin N, Ojerholm E, Ramkissoon S, Laws ER: Craniopharyngioma and other cystic epithelial lesions of the sellar region: a review of clinical, imaging, and histopathological relationships. Neurosurg Focus 28(4):E4, 2010 Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author Contributions Conception and design: Uhm, Himes, Van Gompel, Galanis. Acquisition of data: Uhm, Himes, Van Gompel, Park, Galanis. Analysis and interpretation of data: Himes, Ruff, Van Gompel, Park, Kaufmann. Drafting the article: Himes, Ruff, Park. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Uhm. Correspondence Joon Uhm: Mayo Clinic, Rochester, MN. uhm.joon@mayo.edu. J Neurosurg April 27,
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