Intracranial Metastasis from an Esophageal Gastrointestinal Stromal Tumor
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1 CASE REPORT Intracranial Metastasis from an Esophageal Gastrointestinal Stromal Tumor Satoshi Hamada 1, Atsushi Itami 2, Go Watanabe 2, Shinya Nakayama 2, Eiji Tanaka 2, Masato Hojo 3, Akihiko Yoshizawa 4, Seiichi Hirota 5 and Yoshiharu Sakai 2 Abstract We report the case of a woman with intracranial metastasis from an esophageal gastrointestinal stromal tumor (GIST) with the mutation site in the 3 end of exon 11. Frontal craniotomy was performed with complete resection of the mass, followed by postoperative stereotaxic radiotherapy (SRT). Intracranial metastasis from GISTs is extremely rare; we found only seven case reports in the literature. Key words: gastrointestinal stromal tumor, brain metastasis, imatinib, mutation analysis (Inter Med 49: , 2010) () Introduction Gastrointestinal stromal tumors (GISTs) account for at least 80% of all mesenchymal tumors of the gastrointestinal tract, where they arise from precursors of the interstitial cells of Cajal (1). Clinically, GISTs are usually diagnosed on the basis of KIT (CD117) expression on immunohistochemical analysis (2). About 70% of the GISTs are located in the stomach, 20% in the small bowel, and 5% in the rectum (3). Smaller portions of GISTs occur in the esophagus or outside the gastrointestinal tract. Recurrent disease arises mainly in the original site or via hematogenous metastasis or peritoneal dissemination. Intracranial metastasis is extremely rare, and our review of the literature revealed only seven reports (4-10). The gain of function of the c-kit or platelet-derived growth factor receptor alpha (PDGFRA) genes plays a critical oncogenic role in GISTs (2, 11). Around 70% of mutations in c-kit gene are detected within exon 11, particularly the 5 end. Some investigations of the relationship between the c-kit mutation site and clinical outcome have been reported (12-17). Imatinib mesylate is a competitive inhibitor of multiple tyrosine kinases, including KIT and PDGFRA. The clinical effectiveness of imatinib mesylate for advanced GISTs has been documented (18). We report the case of a woman with intracranial metastasis from an esophageal GIST with the mutation site in the 3 end of exon 11, and systemic disease progression appeared to be controlled for two years after stopping imatinib mesylate prescribed for liver metastasis. Case Report A 54-year-old right-handed woman presented with an abnormality on a chest X-ray film at a routine medical checkup in July The chest X-ray showed loss of the descending aorta border. Abdominal computed tomography scan (CT) revealed a large complex lower esophagus mass (Fig. 1), and esophagography reveals no stenosis. Esophagectomy using a thoracotomy approach was performed, and the 11 7 cm mass was resected. Histopathological examination demonstrated a spindle-shaped cell tumor with a mitotic index of 2-3 per 10 high power fields (HPF). Immunohistochemical analysis was positive for c-kit, and the tumor was identified as a GIST. The patient subsequently remained well, but multiple hepatic masses were detected on follow up abdominal CT in October Histopathological examination of the liver lesions revealed metastatic GISTs. Consequently, systemic Department of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Department of Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Department of Neurosurgery, Graduate School of Medicine, Kyoto University, Kyoto, Department of Diagnostic Pathology, Kyoto University, Kyoto and Department of Surgical Pathology, Hyogo College of Medicine, Nishinomiya Received for publication November 9, 2009; Accepted for publication January 12, 2010 Correspondence to Dr. Atsushi Itami, itami@kuhp.kyoto-u.ac.jp 781
2 Figure1. ChestCTimage.AxialchestCTimageshowinga 11cm heterogeneouslesionintheloweresophagus. Figure3. FDG-PETimage.FDG-PETshowingnoFDG uptakeincludingintheliver. Figure2. BrainCTimage.AxialbrainCTimageshowing a5cm heterogeneouslesionintheleftfrontallobewithsig nificantperifocaledemaandmidlineshift. Figure4. Immunohistochemicalstainofcerebralmetastasis. ImmunohistochemicalstainforCD117(c-kit)showingstainingofthecelmembrane( 400). treatment with imatinib mesylate 400 mg per day was administered from December The effectiveness of the drug was revealed by the change of tumor density on CT (data not shown). The dose was reduced to 300 mg per day in September 2005 because of adverse effects, including fatigue and edema. Eventually, the patient decided to stop treatment in December The patient complained about new onset memory disturbance, communication difficulties, and other neurological symptoms around August These symptoms were slowly progressive and the patient was hospitalized in October CT of the brain revealed a 5 cm heterogeneous lesion in the left frontal lobe with significant perifocal edema and midline shift (Fig. 2). T1-weighted magnetic resonance imaging (MRI) of the head showed an isointense mass with ring enhancement. 18F-fluorodeoxyglucose positron emission tomogram (FDG-PET) showed no FDG uptake including in the liver (Fig. 3). Frontal craniotomy was performed with complete resection of the mass, followed by postoperative stereotaxic radiotherapy (SRT). Histopathological examination of the resected mass showed a tumor with spindle-shaped cells with necrosis and a mitotic index of 1 per 50 HPF. Immunohistochemical analysis was positive for c-kit, confirming metastatic GIST (Fig. 4). Mutation analysis showed that six amino-acid residues corresponding to glutamine (Gln) followed by five amino acids codons were inserted between codon 579 and codon 580 in exon 11 (Fig. 5). This finding was consistent with the mutation site of the patient s 782
3 control TAT GAT CAC AAA TGG GAG TTT CCC AGA AAC AGG patient Amiono acid (575) (576) (577) (578) (579) TAT GAT CAA CAA CTT CCT TAT GAT CAC AAA TGG Gln Gln Leu Pro Tyr Asp Figure5. DNAsequenceofexon11ofc-kit.DNAsequenceofexon11ofc-kitofcontrol(upper) andpatient(lower).mutationalanalysisrevealedatandem duplicationbetweencodon579and 580.Sixamino-acidresiduescorrespondingtoglutamine(Gln)folowedbyfiveaminoacidscodons wereinsertedbetweencodon579andcodon580inexon11. Table. SevenCaseReportofGISTwithIntracranialMetastasis esophageal GIST. Subsequently, the patient remained well and no recurrence was found during six months of follow up after her craniotomy. Discussion We report the case of a woman with intracranial metastasis from an esophageal GIST with the mutation site in the 3 end of exon 11, and systemic disease progression appeared to be controlled for two years after stopping imatinib mesylate prescribed for liver metastasis. The original tumor diameter was more than 10 cm, putting the patient in a high risk category for recurrent or metastatic disease according to NIH criteria (19); the detection of liver metastasis 2 years after esophagectomy was consistent with this. The patient was started on imatinib mesylate. Assessment of small changes in tumor size or density on CT is a sensitive and specific technique for evaluating the response to imatinib mesylate (20). A change in density on CT was found in our patient (data not shown) and revealed that imatinib mesylate was effective in her case. Nevertheless, the patient decided to stop the drug after 2 years of treatment because of unacceptable side effects. Two years after imatinib mesylate cessation, intracranial metastasis occurred. Though the withdrawal of imatinib mesylate leads to rapid disease progression in most patients with advanced GIST (21), the present patient had stable disease (SD) for about 2 years. Mutations in the 5 end of exon 11, particularly deletions affecting codons , are associated with poor outcomes, whereas internal tandem duplications in the 3 end of exon 11 are associated with a good clinical courses (22). In our case, mutational analysis revealed a tandem duplication between codons 579 and 580. Long-term SD after imatinib mesylate termination is considered to be related to this mutation. Eventually, the patient presented with brain metastasis. Intracranial metastasis of GIST is very rare. A review of the 783
4 literature revealed only seven case reports (Table) (4-10). Of these, four were treated surgically (4, 7-9) and one of these case received radiotherapy as an additional treatment (7). Another case was treated with radiotherapy alone to relieve pain (10). Only one case of the three cases treated with imatinib mesylate responded to treatment (5). It has been reported that imatinib mesylate apparently does not effectively cross the blood blain barrier and achieve adequate concentrations in the CNS, and this has been demonstrated in cases of chronic myeloid (CML) and Philadelphia chromosome positive acute lymphoblastic leukemia (ALL) (23, 24). Therefore for the present case, we decided on surgical treatment over imatinib mesylate, in the expectation of reducing the risk of local recurrence. Although radiation therapy is not a standard therapy for GIST, we performed SRT in hope of controlling micro residual cells. Our patient remained well after surgery and postoperative radiotherapy during six months of follow-up. Nevertheless, she remains in a high risk category and recurrences can be expected. Mutational analysis of the tumor in the esophagus and in the cerebral metastasis detected identical mutations, not a second mutation. One reason for the resistance to imatinib mesylate is a second mutation (25). Imatinib mesylate may, therefore, be effective as an adjuvant therapy in the event of a new recurrence. The present case is very rare and interesting, both in terms of the metastasis and the mutation site. Analyzing the mutation site of GIST may help clinicians estimate the prognosis and select treatment. Acknowledgement The authors thank Dr. Toshiro Nishida for evaluating the sequence analysis of the esophageal and brain masses. References 1. Chen H, Hirota S, Isozaki K, et al. Polyclonal nature of diffuse proliferation of interstitial cells of Cajal in patients with familial and multiple gastrointestinal stromal tumors. Gut 51: , Hirota S, Isozaki K, Moriyama Y, et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279: , Miettinen M, Majidi M, Lasota J. Pathology and diagnostic criteria of gastrointestinal stromal tumors (GISTs). Euro J Cancer 38: S39-S51, Hughes B, Yip D, Goldstein D, Waring P, Beshay V, Chong G. Cerebral relapse of metastatic gastrointestinal stromal tumor during treatment with imatinib mesylate: Case report. BMC Cancer 4: 74, Brooks BJ, Bani JC, Fletcher CDM, Demetri GD. Challenges in oncology. Case 4. Response of metastatic gastrointestinal stromal tumor including CNS involvement to imatinib mesylate (STI-571). J Clin Oncol 20: , Kajikawa M, Ishiyama S, Sawada K, Ono K, Suzuki Y. Multiple gastrointestinal stromal tumors of duodenum and jejunum accompanied by lymph node and brain metastasis: Report of a case. Jpn J Gastroenterol Surg 38: , Puri T, Gunabushanam G, Malik M, et al. Mesenteric gastrointestinal stromal tumour presenting as intracranial space occupying lesion. World J Surg Oncol 4: 78, Kaku S, Tanaka T, Ohtuka T, et al. Perisacral gastrointestinal stromal tumor with intracranial metastasis. Neurol Med Chir (Tokyo) 46: , Inage Y, Yamabe K, Yamamoto T, et al. Resection for pulmonary metastasis of gastrointestinal stromal tumor of the stomach at 10 years after gastrectomy: Report of a case. Kyobu Geka 55: , Akiyama K, Numaga J, Kagaya F, et al. Case of optic nerve involvement in metastasis of a gastrointestinal stromal tumor. Jpn J Ophthalmol 48: , Heinrich CM, Corless CL, Duensing A, et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299: , Taniguchi M, Nishida T, Hirota S, et al. Effect of c-kit mutation on prognosis of gastrointestinal stromal tumors. Cancer Research 59: , Andersson J, Bumming P, Meis-Kidblom JM, et al. Gastrointestinal stromal tumors with KIT exon 11 deletions are associated with poor prognosis. Gastroenterology 130: , Martin J, Poveda A, Llombart-Bosch A, et al. Deletions affecting codon of the c-kit gene indicate a poor prognosis in patients with completely resected gastrointestinal stromal tumors: A study by the Spanish group for sarcoma research (GEIS). J Clin Oncol 23: , Hassan I, You YN, Shyyan R, et al. Surgically managed gastrointestinal stromal tumors: A comparative and prognostic analysis. Ann Surg Oncol 15: 52-59, Miettinen M, Makhlouf H, Sobin LH, Lasota J. Gastrointestinal stromal tumors of the jejunum and ileum. Am J Surg Pathol 30: , Singer S, Rubin BP, Lux ML, et al. Prognosis value of KIT mutation type, mitotic activity, and histologic subtype in gastrointestinal stromal tumors. J Clin Oncol 20: , Demetri GD, Von Mehren M, Blanke CD, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 347: , Fletcher CDM, Berman JJ, Corless C, et al. Diagnosis of gastrointestinal stromal tumors: A consensus approach. Hum Pathol 33: , Choi H, Charnsangavej C, Faria SC, et al. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: Proposal of new computed tomography response criteria. J Clin Oncol 25: , Blay JY, Le Cesne A, Ray-Coquard I, et al. Prospective multicentric randomized phase III study of imatinib in patients with advanced gastrointestinal stromal tumors comparing interruption versus continuation of treatment beyond 1 year: The French sarcoma group. J Clin Oncol 25: , Lasota J, Dansonka-Mieszkowska A, Stachura T, et al. Gastrointestinal stromal tumors with internal tandem duplication in 3 end of KIT juxtamembrane domain occur predominantly in stomach and generally seem to have a favorable course. Mod Pathol 16: , Petzer AL, Gunsilius E, Hayes M, et al. Low concentrations of STI571 in the cerebrospinal fluid: a case report. Br J Haematol 117: , Takayama N, Sato N, O Brien SG, Ikeda Y, Okamoto S-I. Imatinib mesylate has limited activity against the central nervous system involvement of Philadelphia chromosome-positive acute lymphoblastic leukemia due to poor penetration into cerebrospinal 784
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