Second Primary Tumors in Patients with Gastrointestinal Stromal Tumors: a Single-Center Experience

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Second Primary Tumors in Patients with Gastrointestinal Stromal Tumors: a Single-Center Experience medicina Article Second Primary Tumors in Patients with Gastrointestinal Stromal Tumors: A Single-Center Experience Murat Koçer 1,*, Sadık Muallao˘glu 2, Bülent Çetin 3, Hasan ¸SenolCo¸skun 4, Nermin Karahan 5 and Osman Gürdal 6 1 Medical Oncology Subdivision, Department of Internal Medicine, Antalya Training and Research Hospital, Health Sciences University, Muratpa¸sa,Antalya 07100, Turkey 2 Medical Oncology Clinic, Private Iskenderun Geli¸simHospital, Iskenderun 31200, Turkey; [email protected] 3 Medical Oncology Subdivision, Department of Internal Medicine, Süleyman Demirel University Faculty of Medicine, Isparta 32260, Turkey; [email protected] 4 Medical Oncology Subdivision, Department of Internal Medicine, Akdeniz University Faculty of Medicine, Konyaaltı, Antalya 07070, Turkey; [email protected] 5 Department of Pathology, Süleyman Demirel University Faculty of Medicine, Isparta 32260, Turkey; [email protected] 6 Department of Biostatistics and Medical Informatics, Süleyman Demirel University Faculty of Medicine, Isparta 32260, Turkey; [email protected] * Correspondence: [email protected]; Tel.: +90-542-513-9666 Abstract: Background and Objectives: In this study, we investigated the frequency and type of second primary malignant tumors (SPMTs) accompanying gastrointestinal stromal tumors (GISTs), patient and tumor characteristics, and follow-up and survival data. Materials and Methods: We included 20 patients with SPMTs from a total of 103 patients with GISTs in a single center in Turkey. At the time of GIST diagnosis, patient age, sex, presentation symptoms, localization, pathological features of the tumor, stage, recurrence risk scoring for localized disease, treatments received, time of SPMT Citation: Koçer, M.; Muallao˘glu,S.; association, follow-up times, and survival analysis were recorded for each patient. Localization, Çetin, B.; Co¸skun,H.¸S.;Karahan, N.; histopathology, and stage of SPMT accompanying GISTs were also recorded accordingly. Results: Gürdal, O. Second Primary Tumors in Patients with Gastrointestinal Stromal SPMT was detected in 19.4% of patients with GISTs. Of the patients, 50% were men and 50% were Tumors: A Single-Center Experience. women. The mean age at the time of diagnosis of GIST was 63.8 ± 10.81 years (range: 39–77 years). Medicina 2021, 57, 494. https:// Of the GISTs, 60% were localized in the stomach, 25% in the small intestine, and 70% were at low doi.org/10.3390/medicina57050494 risk. Of the SPMTs, 60% were in the gastrointestinal system. SPMTs were diagnosed as synchronous with GISTs in 50% of the patients. The mean follow-up period of the patients from the diagnosis of Academic Editor: Rinaldo Pellicano GIST was 45.6 (0.43–129.6) months. When the data were finalized, 5% died due to GIST, 35% died due to SPMT, and 15% died due to non-disease-related causes. Conclusions: SPMT was detected in Received: 4 April 2021 19.4% of patients with GISTs. GISTs were frequently located in the stomach, and most of them were Accepted: 11 May 2021 at low risk. The most common SPMTs were gastrointestinal system tumors, and their coexistence Published: 13 May 2021 was found to be synchronous. Most patients died due to SPMT during follow-up. Publisher’s Note: MDPI stays neutral Keywords: gastrointestinal stromal tumor; second primary malignant tumor; coexistence with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Gastrointestinal stromal tumors (GISTs) are the most common mesenchymal tumors of the gastrointestinal system. They are rare, constituting 1% of all sarcomas and 3–5% of Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. gastrointestinal tumors [1], and their incidence has been reported to be 10–15 per million in This article is an open access article most studies [2]. They frequently originate from the stomach (60–70%) and small intestine distributed under the terms and (25–35%), and less frequently from the colon, rectum, and appendix (5% altogether), and conditions of the Creative Commons the esophagus (2–3%). Rarely, they may be located extragastrointestinally (omentum, Attribution (CC BY) license (https:// peritoneum, or mesentery) [3]. Mutations in the KIT (75%) or PDGFRA gene (10%) play a creativecommons.org/licenses/by/ role in the pathogenesis of GISTs. Histologically, there are three types: spindle cell type 4.0/). (70%), epithelioid type (20%), and the mixed type (10%). Prognosis depends on the tumor Medicina 2021, 57, 494. https://doi.org/10.3390/medicina57050494 https://www.mdpi.com/journal/medicina Medicina 2021, 57, 494 2 of 13 size, mitosis rate, and localization [4]. The clinical presentation is variable. They may present with symptoms associated with the location of the tumor (such as abdominal pain, mass, gastrointestinal bleeding) or asymptomatic and incidental (for example, during surgical procedures for other diseases) in 20–30% of patients [5]. Surgery is the most effective treatment. Imatinib, a selective KIT tyrosine kinase inhibitor, and other tyrosine kinase inhibitors, are used as medical treatments. The use of imatinib as a neoadjuvant before surgery and as an adjuvant in patients at high risk after the operation and at the unresectable/metastatic stage, increases the response and survival rates [6–8]. Overall survival (OS) increases in GISTs treated with surgery and imatinib. Second primary tumor development may occur in patients, in addition to GISTs, with increasing life expectancy. The frequency of tumors accompanying GISTs varies depending on the number of patients in different studies, selection criteria (including benign tumors in addition to malignant tumors in some studies), and follow-up periods. Some retrospective studies, mostly case series, were conducted on secondary tumors associated with GISTs. In recent years, the number of publications showing this relationship has increased accordingly. GISTs may coexist either synchronously or metachronously in different cancers [9]. There are publications in the literature showing that the association is mostly synchronous [9–16]. Synchronous associations often coexist with gastrointestinal cancers [11,17]. The associa- tion of GIST with secondary tumors ranges from 4.5% to 33% in different series (average, 13%) [9]. In the study conducted by Kramer et al., this rate was found to be 31.9% and 42%, respectively, in two different multicenter and single-center cohorts [18]. This rate was reported to be 21% in a retrospective monocentric analysis by Comandini et al. [19]. Although varying rates have been reported in literature, the association of GISTs with sec- ondary tumors was reported to be 20% in a meta-analysis performed in 2019 [11,12]. Most studies have shown that GISTs are most commonly associated with gastrointestinal and genitourinary system tumors [11,12,14,18,20]. Further, gastrointestinal tumors frequently include stomach and colorectal cancers [10–12,14,15,18]. Among genitourinary tumors in men and women, prostate, bladder, kidney, breast, ovarian, and uterine tumors are more common [11,12,18]. In two different large-scale analyses conducted in 2019, it was reported that among SPMTs accompanying GISTs, hematological malignancies were lesser (6%) compared to gastrointestinal and genitourinary system tumors [11,12]. Lymphoma and leukemia are frequently observed in hematological tumors [12,19]. There are a limited number of studies in literature regarding the prognostic effects of SPMTs accompanying GISTs. There are publications, however, predicting shorter survival in cases of concurrent coexistence [18,19,21]. Only patients displaying second primary malignant tumor (SPMT) associations during follow-up after an initial GIST diagnosis were included in this study. We aimed to describe the frequency and type of SPMT detected in patients with GIST, the characteristics of the patients and tumors, the time of occurrence of SPMTs (pre-synchronous-post-GIST), and follow-up data for these patients. We believe that this information will accordingly contribute to the literature available on this subject. 2. Materials and Methods 2.1. Patients We included a total of 20 patients with accompanying SPMT who were histopatholog- ically diagnosed with GIST (n = 103) and admitted to the Süleyman Demirel University Medical Oncology Unit between 2002 and 2018. Patient information was retrospectively obtained from the file records. None of the patients had familial GISTs. No suspected syndromic setting was found during the follow-up. At the time of GIST diagnosis, patient age, sex, presentation symptoms, localization, pathological features of the tumor (cell type, immunostaining for c-kit, CD-34 status, SMA, desmin, S-100, tumor diameter, mitosis, Ki-67, rupture, necrosis, and ulceration), stage according to the American Joint Committee on Cancer 8th edition TNM staging system, localization of metastases, recurrence risk scoring for localized disease (Armed Forces Medicina 2021, 57, 494 3 of 13 Institute of Pathology [AFIP] criteria, modified National Institutes of Health [NIH] Con- sensus Criteria), treatments received, time of SPMT association (if tumors were diagnosed simultaneously, they were defined as synchronous tumors), follow-up time, and survival analysis were recorded for each patient. In addition, localization, histopathology, and TNM stage of SPMTs accompanying GISTs were also recorded for all the patients. Ethics Committee approval was obtained from the Süleyman Demirel University Faculty of Medicine Clinical
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