Neoadjuvant treatment of Dermatofibrosarcoma Protuberans of pancreas with Imatinib: case report and systematic review of literature
© Dhir et al.; licensee BioMed Central Ltd. 2014
Received: 14 May 2014
Accepted: 7 July 2014
Published: 6 August 2014
Dermatofibrosarcoma Protuberans (DFSP) is a rare skin tumor, characterized by frequent local recurrence but is seldom metastatic. It is histologically characterized by storiform arrangement of spindle cells. Cytogenetically, most tumors are characterized by translocation 17:22 leading to overexpression of tyrosine kinase PDGFB which can be targeted with tyrosine kinase inhibitor, Imatinib. We describe the first case of unresectable pancreatic metastases from DFSP treated with neoadjuvant Imatinib and subsequently R0 metastectomy. Additionally, a comprehensive systematic review of DFSP pancreatic metastases and the current published data on the use of Imatinib in DFSP is summarized.
KeywordsPancreatic metastases DFSP Imatinib Systematic review
Dermatofibrosarcoma Protuberans (DFSP) is a rare fibrohistiocytic tumor of the skin or subcutaneous tissue that is often locally infiltrative but rarely metastatic[1, 2]. Cytogenetically, DFSP is characterized by a pathognomonic translocation t(17;22) (22;q13) with fusion of the COL1A1 gene on chromosome 17 with the PDGFB gene on chromosome 22. This event results in constitutive expression of ligand PDGFB creating an autocrine stimulatory loop that drives cell proliferation and fibrosis. Clinically, it commonly presents in younger adults growing slowly over many years[2, 4]. Microsatellite instability and p53 mutations are involved in tumor progression to the fibrosarcomatous variant (DFSP-FS). Although the major recurrence risk for DFSP is local relapse, DFSP-FS subtype is associated with an aggressive clinical course, more likely to develop distant metastases[6, 7]. Several case reports in the literature have demonstrated that DFSP can metastasize to the lungs[8–10], as well as, pancreatic or retroperitoneal spaces similar to the current case[11–13]. The optimal treatment of primary and metastatic DFSP is complete surgical resection with negative margins. Over 90% of DFSPs, demonstrate a constitutive activation of platelet-derived growth factor receptor, making inhibition with a promiscuous tyrosine kinase inhibitor (TKI), Imatinib a good option for unresectable, recurrent, or metastatic disease. There have been several reports of neoadjuvant Imatinib for locally advanced primary tumors and adjuvant Imatinib for resected margin positive primary disease and metastatic disease[16–20]. There have been no published reports of neoadjuvant Imatinib for unresectable metastatic DFSP to the pancreas successfully treated and subsequently resected. Here, we present the first reported case of unresectable metastatic DFSP to the pancreas, successfully resected following neoadjuvant Imatinib. Additionally, we conducted a systematic review of the literature for pancreatic metastases of DFSP and use of Imatinib in DFSP.
The patient resumed adjuvant Imatinib for 6 months and remained free of disease for 14 months, off therapy. His imaging at 14 months revealed para-aortic nodal disease without evidence of local recurrence that responded to reinstitution of Imatinib at the same dose. The patient is now five years out from the initial diagnosis of metastatic disease and remains in remission on Imatinib.
Systematic review: Pancreatic metastasis of Dermatofibrosarcoma Protuberans
A Medline search was performed using the key words (a) “Pancreatic metastasis” AND “Dermatofibrosarcoma Protuberans” (b) “Pancreas” AND “Dermatofibrosarcoma Protuberans”. Similarly, an Embase search was performed using the key words (a) “Pancreatic metastasis” AND “Dermatofibrosarcoma Protuberans”. Medline and Embase search using strategy (a) revealed 2 articles[13, 21]. Search strategy (b) identified 3 articles[11, 13, 22]. Backward search was performed using the references from full texts of these 4 articles and no additional articles were found.
We identified 4 articles reporting pancreatic metastases from DFSP[11, 13, 21, 22]. A summary of these articles is provided in Additional file1. Two of these patients were found to have pancreatic metastases during follow up and this appeared to be the only site of metastases[13, 21]. In another patient reported by Winter et al., diagnosis was not clear preoperatively. Interestingly, all three of these patients had aggressive disease with fibrosarcomatous variant of DFSP, high mitotic counts, relatively short disease free interval and did not have local recurrence prior to development of metastatic disease. In the report by Onoda et al. a patient had multiple local recurrences with relatively more aggressive features at each recurrence and finally died of brain metastases. Patient was found to have pancreatic and other systemic metastases at autopsy. No studies described the use of Imatinib as a neoadjuvant strategy to treat the pancreatic metastases.
Systematic review: use of Imatinib in Dermatofibrosarcoma Protuberans
After completing the Medline search, an Embase search was also performed using key words “Imatinib” AND “Dermatofibrosarcoma Protuberans” which revealed 348 items including 152 review articles. After exclusion of studies already identified using Medline search, we were able to identify an additional 5 case reports[55–59] and 6 case series[60–65] (5 in abstract form[60, 61, 63–65]). There was one more case report in non-English language, describing neoadjuvant Imatinib for DFSP of the face, for which no abstract was available.
We identified 23 case reports[19, 20, 23–25, 27, 29–32, 35, 38, 39, 41, 42, 50–52],[55–59], 15 case series[16, 26, 33, 34, 36, 37, 45, 47, 53, 60–65], 6 phase II studies[18, 40, 46, 48, 49] and 4 pediatric studies[28, 43, 44, 54] where Imatinib was used for the treatment of patients with DFSP. These studies include a total of 199 patients. Additional files2,3,4 and5 provide a summary of these studies including case reports (Additional file2), case series (Additional file3), phase II studies (Additional file4) and pediatric reports/series (Additional file5). A phase II study of malignancies associated with Imatinib sensitive tyrosine kinases, by Heinrich et al. was excluded. A subset of patients with DFSP in this study were further analyzed and reported separately by McArthur et al.[40, 67].
All except one case report described some response to Imatinib. Since the response assessment criteria varied in many case series and to minimize bias, only phase II studies were used for calculation of percentage response to Imatinib. Overall combined response rate (Complete, partial or stable disease) was 65% (48/74 patients) in phase II studies. Common indications for use of Imatinib in the selected studies included locally advanced primary, primary tumor in a cosmetically sensitive location, locally recurrent tumors, positive margins or metastatic disease. Commonly used dosages include 400 mg/day, 400 mg twice daily or 800 mg/day. Some studies utilized a dose escalation strategy where patients were started on 400 mg/day and dose was gradually increased to 600 mg/day and then 800 mg/day based on tolerance and side effects. Others utilized a higher dose of 400 mg twice daily or 800 mg/day and decreased the dose depending on the side effects. Duration of adjuvant strategy varied from 2 months to 2 years whereas neoadjuvant treatment was guided by response of the tumor to the therapy.
To our knowledge, this is the first case report where an unresectable pancreatic metastasis was treated in a neoadjuvant fashion with Imatinib and an R0 resection was successfully performed. Consistent with findings observed in neoadjuvant therapy for primary cutaneous disease, when a clinical and radiographic reduction in tumor size is observed, it corresponds with the histologic findings of markedly decreased cellularity as evidenced by fewer CD34+ cells, along with significant hyalinization of dermal collagen as seen in our case (Figure 5A-C). In the current case, neoadjuvant Imatinib resolved the presenting symptoms (GI bleeding, anemia, and pain) and enabled R0 resection of an unresectable metastasis. The dose of 400 mg BID was selected based on the only published phase II study, B2225 at that time in 2007. This study reported a 100% response rate in eight locally advanced t (17;22) positive DFPS tumors with four patients (50%) exhibiting complete responses. Additionally McArthur et al. reported 7/8 (88%) patients tolerated the therapy with only one patient requiring dose reduction to 600 mg. Since B2225 three additional phase II trials (Additional file4) have been conducted evaluating 400 mg, 600 mg and 800 mg doses which have reported similar efficacy and tolerance profiles[46, 49].
In this case 400 mg BID Imatinib followed by resection facilitated excellent local control evident now 5 years post metastatectomy, 10-years from primary cutaneous diagnosis without resection bed recurrence. Although, the patient did develop distant, para-aortic nodal metastasis 14 months post-resection, metastatic disease remained Imatinib responsive and demonstrated radiographic resolution with therapy. Importantly the patient did not report any significant gastrointestinal or other side effects during neoadjuvant therapy or subsequent therapy for nodal recurrence.
In conclusion, given the intrinsic biological sensitivity of COL1A1/PDGFB positive DFSP to Imatinib, neoadjuvant therapy with this medication may not only be an important tool in managing locally advanced and recurrent cutaneous disease but equally valuable in unresectable or marginally resectable metastatic DFSP; facilitating margin negative resection, improving local control, and extending disease free and overall survival. The response observed following neoadjuvant Imatinib may also be useful as an in vivo test of tumor’s responsiveness and may be useful in determine the best post-operative adjuvant therapy. Neoadjuvant and adjuvant Imatinib is well established in Gastrointestinal Stromal Tumors (GIST), unlike in DFSP. The results from the closed clinical trial NCT00243191/SARC004 will provide insight into the value of short course therapy in cutaneous disease but additional trials are needed to address the value in the setting of metastatic DFSP. This report highlights the value of neoadjuvant Imatinib in facilitating surgical resection and the continued response of distant disease sites in a patient now over 5-years with metastatic DFSP.
“Written informed consent was obtained from the patient for publication of this Case Report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.”
Collagen 1 alpha 1
- DFSP- FS:
Dermatofibrosarcoma protuberans – fibrosarcomatous type
No evidence of disease
Platelet derived growth factor beta.
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