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ORIGINAL ARTICLE
Year : 2021  |  Volume : 24  |  Issue : 12  |  Page : 1785-1792

Gastrointestinal stromal tumors of the stomach: A 10-year experience of a single-center


Department of General Surgery, Kartal Dr Lütfi Kırdar City Hospital, Istanbul, Turkey

Date of Submission08-Sep-2020
Date of Acceptance17-Jun-2021
Date of Web Publication09-Dec-2021

Correspondence Address:
Dr. H Uzunoglu
Department of General Surgery, Istanbul Kartal Dr Lütfi Kırdar City Hospital
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_558_20

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   Abstract 


Background: Gastrointestinal tract stromal tumors (GIST) are the most common mesenchymal tumors in the gastrointestinal tract (GIS). GISTs may cause significant morbidity and mortality rates. Aim: In this study, it was aimed to evaluate 10 years of gastric GIST cases followed in our hospital, and to analyze the prognostic factors. Subjects and Methods: In this single-center retrospective study, a total of 64 patients who were operated between May 2010 and May 2020 due to gastric GIST tumor were reviewed. Clinical and pathological features, risk classifications, overall survival (OS) and disease-free survival (DFS) were evaluated. Results: According to the risk classification, 18.8% of the patients were in the high-risk group. The overall 5-year OS and DFS rates were 85.7%. The mean OS of the patients was 47.9 SD36.2 months, and the duration of DFS was 45.5 months. Patients with a 5-year OS rate above 5 cm in diameter (P = 0.024), with a mitotic index above 5/50 high power field (HPF) (P = 0.038), and those with a high-risk group (P = 0.011) were significantly lower than the other group. In the correlation analysis, it was found that tumor diameter correlated significantly with OS (P = 0.034; r = -0.317). Tumor diameter and mitotic index were found to be inversely correlated with DFS duration (P = 0.004; r = -0.425 and P = 0.035; r = -0.316, respectively). Conclusion: Our findings showed that in gastric GIST cases, as the primary tumor diameter and mitotic index increase, correlate with survival rates and the mean overall and disease-free survival times decrease.

Keywords: CD117, gastric GIST, Gastrointestinal system stromal tumors, immunochemical markers, mitotic index, tumor diameter


How to cite this article:
Uzunoglu H, Tosun Y, Akinci O, Baris B. Gastrointestinal stromal tumors of the stomach: A 10-year experience of a single-center. Niger J Clin Pract 2021;24:1785-92

How to cite this URL:
Uzunoglu H, Tosun Y, Akinci O, Baris B. Gastrointestinal stromal tumors of the stomach: A 10-year experience of a single-center. Niger J Clin Pract [serial online] 2021 [cited 2022 Jan 25];24:1785-92. Available from: https://www.njcponline.com/text.asp?2021/24/12/1785/332084




   Introduction Top


Gastrointestinal tract stromal tumors (GIST) are the most common mesenchymal tumors in the gastrointestinal tract (GIT). GISTs, which have the characteristics of subepithelial lesion and can be malignant, may occur anywhere in the entire GIT, but are most common in the stomach.[1],[2],[3],[4],[5]

GISTs mostly involve elderly individuals. GIST cases, which are mostly manifested by bleeding and chronic abdominal pain, are detected by computed tomography (CT), magnetic resonance imaging (MRI), and endoscopy. Some GIST cases are detected incidentally at the time of diagnosis or during surgery of a different primary tumor.[6],[7],[8] Immunohistochemical markers such as Cluster of Differentiation-117 (CD117), Cluster of Differentiation-34 (CD34) and Discovered on GIST-1 (DOG1) are used to differentiate GISTs from some other GIT tumors, such as leiomyoma.[9],[10]

GISTs are amongst the significant causes of morbidity and mortality. Therefore, determining the prognosis as well as the early diagnosis of GIST is critical.[5],[6],[7] For this purpose, a malignancy risk classification is made based on components such as the diameter of the primary tumor, mitotic activity index and localization of the tumor. This risk classification is divided into high, medium, low and very low risk groups.[2],[11],[12],[13]

In gastric GIST cases, mostly wedge resection or total or subtotal gastrectomy is performed. The aim of the surgery is to achieve a complete resection (R0) with no tumor residue. It has been reported that complete resection affects prognosis. In some cases with high risk and with metastasis at the time of diagnosis, the addition of imatinib therapy as an adjuvant may also have a positive effect on prognosis.[1],[2],[3],[14],[15],[16]

In this study, it was aimed to analyze 10 years of gastric GIST cases followed in our hospital, and to analyze prognostic factors.


   Subjects and Methods Top


This study was approved by the local ethics committee (approval number: 2020.514.180.24), and was planned retrospectively. The study was conducted in accordance with the principles of the Declaration of Helsinki.

Patients and criteria

A total of 64 patients who had gastric GIST tumors and who were operated in the General Surgery Department of our hospital within the 10-year period between May 2010 and May 2020 were included in the study. Demographic information, clinical, laboratory, pathology and radiology findings of all patients were recorded. Those who refused to participate, those under the age of 18, and those who died due to a reason other than GIST tumor were not included in the study. After the collection of the data, all the contact numbers were called by phone, and it was learned whether the patients were still alive or not.

Since DOG1 test has been studied in our hospital since November 2014, no DOG1 data were available prior to this date.

The risk classification was used according the original National Institutes of Health (NIH) prognostic criteria, based on the tumor diameters and mitotic indexes of the patients.[12],[13]

The mitotic index is counted in an area of 5 mm2 on the glass side section for modern microscopes, equal to 50 high power fields for the traditional microscopes. In the present study, mitotic index has been calculated as[17]:

Mitotic index = (the number of cells undergoing mitosis per 50 high power fields)/(the total number of cells per 50 high power fields).

Statistical analysis

All the statistical analyzes in the study were done using SPSS 25.0 software (IBM SPSS, Chicago, IL, USA). Descriptive data were given as numbers and percentages. In terms of categorical variables, comparisons between groups were made with Pearson's Chi Square test and Fisher's Exact Test. Whether continuous variables are suitable for normal distribution was confirmed by the Kolmogorov-Smirnov Test. The differences between the groups in terms of continuous variables were analyzed using Student's t Test, and the comparison of mean values between multiple groups by variance analysis. The relationship between continuous variables was tested using Spearman's correlation analysis. Risk coefficient of categorical variables was evaluated by logistic regression analysis and given as “odds ratio.” The results were evaluated within the 95% confidence interval, and P < 0.05 values were considered statistically significant. Bonferroni correction was made where appropriate.


   Results Top


A total of 27 (42.2%) patients were men, and 37 (57.8%) were women. The most common symptoms in the patients were pain (59.4%), bleeding (17.2%), and 15.6% of the patients were asymptomatic. In 81.2% of the patients, the diagnosis was made as a result of the examination of the resected material, and 18.8% of them were made as a result of pre-op biopsy [Table 1].
Table 1: Distribution of symptoms, risk, tumor diameter, mitotic index groups and marker detection rates

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Tumor diameter was 5 cm and below in 56.3% of the patients. In 75% of patients, the mitotic index was 5/50 high power field (HPF) and below. According to the risk classification, 18.7% of the patients were in the very low-risk group, 29.7% in the low-risk group, 32.8% in the intermediate risk group, and 18.8% in the high-risk group respectively. Among the immunohistochemical markers, CD117 and DOG1 were detected in all patients, and CD34 in 98.4% [Table 1].

Gastric wedge resection was performed in 41 (64.1%) of the patients, and subtotal or total gastrectomy was performed in 23 (35.9%). Metastasis was detected in five patients (7.8%) at the time of diagnosis, and metastasis or recurrence was detected in the computer tomography (CT) and/or Positron Emission Tomography examinations during the follow-up in five patients (7.8%). Eight (12.6%) of the patients had a second primary tumor other than gastric GIST. Gastric GIST tumor was detected incidentally in 14 patients (21.9%), seven of whom were during the mentioned operation of the second primary tumor. Two patients (3.1%) died within post-op 30 days, and six patients (9.4%) died during the follow-up period. The 5-year overall survival (OS) and disease-free survival (DFS) rates were 85.7% in the patients whose 5-year-follow-up were complete. The morbidity rate was 20.3%. Imatinib was given as an adjuvant treatment to 31.3% of the patients. Complete resection (R0) was achieved in 93.8% of the patients. None of the patients had synchronous GIST [Table 2].
Table 2: Surgical method, metastasis and distribution of some variables of tumor

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The mean age of diagnosis of the patients was 58.8 SD11.2 years (age range: 30-81 years). The mean tumor diameter was 5.8 SD5.1 cm (range: 0.3-27.0 cm). The mean mitotic index was 6.7 SD15.0/50 HPF (range: 0-110/HPF). The mean follow-up time of the patients was 50.6 SD36.6 months (3-125 months). The mean general OS of the patients was 47.9 SD36.2 months, and the mean DFS was 45.5 SD37.2 months [Table 3].
Table 3: Mean values of age of diagnosis, tumor diameter, mitotic index and survival variables.

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No statistically significant difference was found between the patients that died and the survived ones in terms of distribution rates of genders, risk groups, tumor diameters and mitotic indices (P > 0.05 for each). There was no significant difference between the groups in terms of necrosis, rupture, complete resection, second primary tumor and recurrence/metastasis rates (P > 0.05 for each). In the risk analysis, it was determined that patients in the high-risk group had a 2.398-fold increased risk of mortality (Odds ratio; 0.385-14.925). Patients with second primary tumors had a 4.333-fold increased risk (Odds ratio; 0.651-28.86), those with recurrence/metastasis had a 2.7-fold increased risk (Odds ratio; 0.251-29.032), those with tumors larger than 5 cm had a 1.319-fold increased risk (Odds ratio; 0.224-7.092) and those with a higher mitotic index of 5/50 HPF had a 1.572-fold (Odds ratio; 0.26-9.524) increased risk of mortality [Table 4].
Table 4: Comparison and risk analysis in terms of mortality

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The 5-year OS ratio was significantly lower in the patients with a tumor diameter over 5 cm than those with tumors below 5 cm (P = 0.024), in those with a mitotic index above 5/50 HPF than those with a mitotic index below 5/50 HPF (P = 0.038), and in those with a high-risk group than those with non-high-risk group (P = 0.011) [Table 5].
Table 5: Comparison of mean survival times by tumor diameter, mitotic index and risk groups

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Men and women were similar in terms of the mean OS (P = 0.282) and DFS (P = 0.112). The mean OS (P = 0.005) and DFS (P = 0.004) of the tumors with a diameter of more than 5 cm were significantly lower than the patients with 5 cm or less. The mean OS (P = 0.023) and DFS (P = 0.008) were significantly lower in the patients with a mitotic index higher than 5/50 HPF. The mean OS (P = 0.012) and DFS (P < 0.001) were also significantly lower in the high-risk group in comparison to those in the non-high group [Table 5].

In the correlation analysis, it was found that tumor diameter correlated significantly with OS (P = 0.034; r = -0.317). In addition, tumor diameter and mitotic index were found to be inversely correlated with DFS (P = 0.004; r = -0.425 and P = 0.035; r = -0.316, respectively).


   Discussion Top


Gastrointestinal tract stromal tumors can be seen in the entire GIS canal. In most of the studies, especially gastric and intestinal GIST cases were reviewed together.[18],[19],[20] In this study, only gastric GIST cases were reviewed in order to reach more specific data. It is very important to predict the prognosis and survival in gastric GIST cases. For this purpose, risk classifications are used.[2],[11],[12],[13] In this study, it was determined that tumor diameter, mitotic index and risk classification provided important information in predicting the prognosis and the survival.

It has been reported that there is no significant difference between the genders in gastric GIST cases.[1],[2],[3],[21],[22] In this study, no significant difference was found between the genders in terms of mortality rate, and also no significant difference was found between the genders in terms of OS (P = 0.282) and DFS (P = 0.112). These findings show that men and women have a similar rate of disease, and that mortality, disease-free survival time and overall survival time do not differ between genders.

Gastric GISTs mostly involve older people.[3],[4],[5],[21],[22],[23] The mean age was reported to be between 60.0-68.8 years.[21],[22],[23],[24] In this study, the mean age of patients at the time of diagnosis was determined as 58.8 years. These findings show that gastric GIST cases are more frequent especially after the 6th decade.

In the gastric GIST cases, the most common symptoms were reported as bleeding (17.2-40%) and abdominal pain or discomfort (22.5-59.4%), and asymptomatic patient rate was reported between 30-33%.[21],[22],[23],[24] In this study, the most common symptoms in the patients were pain (59.4%) and bleeding (17.2%), and 15.6% of patients were found to be asymptomatic. These findings indicate that GIST diagnosis should be considered in those with bleeding and abdominal pain, but it should be kept in mind that gastric GIST cases may also be asymptomatic.

In the gastric GIST cases, gastric wedge resection or total or subtotal gastrectomy is performed mostly.[14],[15] In this study, gastric wedge resection was performed in 64.1%, and gastrectomy in 35.9%. The complete resection rate was 93.8%.

Gastric GIST is an important cause of mortality.[1],[2],[3] We found the post-op 30-day mortality rate as 3.1%, the total mortality rate as 12.5%, the mean OS as 47.9 months. In our study, the 5-year OS and DFS rates were the same, and were 85.7%. In this study, the mean OS and DFS were 47.9 and 45.5 months, respectively. These findings show that the 5-year overall and disease-free survival rates are high, and that the mean survival time is acceptable in gastric GIST cases.

Determination of primary tumor diameter in gastric GIST cases is critical in terms of both determining the surgical approach, classification of risk, and predicting prognosis.[11],[12],[13],[21] In this study, the mean tumor diameter was determined as 5.8 SD5.1 cm, and tumor diameter was found to be 5 cm and below in 56.3% of the patients.

In this study, the mean OS was found to be 50.1 months in patients with a tumor diameter over 5 cm. This difference may have resulted from the inclusion of patients whose 5-year follow-up was not completed in this study. In this study, the mean OS and DFS were found to be significantly lower in the patients with tumor diameter greater than 5 cm. In the correlation analysis performed in this study, tumor diameter was found to be inversely correlated with OS (P = 0.034; r = -0.317) and DFS (P = 0.004; r = -0.425, respectively). All these data show that the size of 5 cm for tumor diameter in gastric GIST cases is a good threshold value in terms of determining the prognosis, that the duration of survival decreases significantly in patients with primary tumor over 5 cm, and that the expectation of survival decreases as the tumor diameter increases.

In this study, the 5-year OS rate was 87.5% in patients with a tumor diameter of 5-10 cm, and was 25% in those with a diameter of 10 cm. In addition, the 5-year OS rate was found to be significantly lower in the patients with a tumor above 5 cm than those with a tumor diameter of 5 cm and below (P = 0.024). In the risk analysis performed in this study, it was determined that those with a tumor diameter greater than 5 cm had a 1.319-fold increased risk of mortality (Odds ratio; 0.246-7.092). All these findings show that the 5-year survival expectancy decreases significantly in those with primary tumors over 5 cm, and that the 5-year survival expectation is very low in those whose tumor diameter exceeds 10 cm. These data support that tumor diameter is a good predictor for survival in gastric GIST cases.

The high mitotic index indicates that the mitotic activity, and thus the tumor activity is also high. In gastric GIST cases, determination of mitotic index in the primary tumor is also important in terms of surgery, risk classification and prognosis.[11],[12],[13],[21] The mitotic index less than 5/50 HPF was reported between 75.878.6%.[21],[24] In this study, 75% of the patients had a mitotic index of 5/50 HPF and below. In this study, the mean mitotic index was found to be 6.7/50 HPF (range: 0-110/HPF).

In this study, the mean OS was 37.5 months (approximately 3.1 years) in those with a mitotic index above 5/50 HPF. In this study, the mean OS (P = 0.023) and DFS (P = 0.008) in patients with a higher mitotic index of 5/50 HPF were found to be significantly lower compared to patients with 5/50 HPF and below. In the correlation analysis performed in this study, it was determined that the mitotic index was inversely correlated with DFS (P = 0.035; r = -0.316). All these data show that in gastric GIST cases, as the mitotic index increases, overall and disease-free survival times decrease significantly.

In this study, the 5-year OS rate was found to be significantly lower in patients with a mitotic index higher than 5/50 HPF (P = 0.038). In the risk analysis conducted in this study, it was determined that those with a higher mitotic index of 5/50 HPF had a 1.572-fold increased risk of mortality (Odds ratio; 0.26-9.524). All these findings show that the high mitotic index in gastric GIST cases significantly reduces the 5-year survival expectation, and the detection of the mitotic index is a good predictor in determining the prognosis in these cases.

Malignancy risk classification, which is determined by including tumor diameter and mitotic index, provides critical information in terms of prognosis in gastric GIST cases.[11],[12],[13] In this study, 18.7% of the patients were in the very low-risk group, 29.7% in the low-risk group, 32.8% in the intermediate risk group and 18.8% in the high-risk group.

The 5-year OS rate in the high-risk group, in this study, was found to be 40.0%, and was found to be significantly lower than those in the non-high-risk groups (P = 0.011). In this study, the mean OS (P = 0.012) and DFS (P < 0.001) were found to be significantly lower in patients with high-risk group compared to those in the non-high-risk group. In addition, in the risk analysis performed in this study, it was determined that patients in the high-risk group had a 2.398-fold increased risk of mortality (Odds ratio; 0.385-14.925). These findings show that overall and disease-free survival expectations are significantly reduced, that mean survival times are significantly reduced in patients with high-risk class, and that risk classification is a good predictor that can be used to determine prognosis.

In a meta-analysis, tumor necrosis in gastric GIST cases has been reported to have a more impact on prognosis in comparison to the small intestine GISTs.[25] However in this study, it was determined that 21.9% of patients had necrosis, and 3.1% had rupture. Due to the low number of these cases, it was seen that necrosis or rupture did not affect prognosis in patients, and did not differ in terms of OS and DFS durations. Extensive studies are needed to demonstrate the effect of necrosis or rupture has on prognosis.

In this study, metastasis was detected at the time of diagnosis in five patients (7.8%), and metastasis or recurrence was detected in CT and/or PET examinations during follow-up in five patients (7.8%). In the risk analysis performed in this study, it was determined that those who had recurrence/metastasis in their follow-ups had a 2.7-fold increased mortality risk (Odds ratio; 0.251-29.032). This finding indicates that it is critical to follow up the patient for recurrence or metastasis.

Eight (12.6%) of the patients were found to have a second primary tumor other than gastric GIST in this study. Gastric GIST was detected incidentally in 14 patients (21.9%), seven of whom were during operation of the second primary tumor mentioned above. In the risk analysis performed in this study, it was determined that patients with the second primary tumor had a 4.333-fold increased risk of mortality (Odds ratio; 0.651-28.86). These data indicate that the presence of GIST should be kept in mind in patients with a different primary tumor, but the prognosis may be worse in these patients.

It was stated that positive staining of CD117, called C-kit, as the immunohistochemical staining method in patients with gastric GIST is a diagnostic marker. In cases where CD117 is negative, DOG1 antigen has been shown to have high sensitivity and specificity values in these patients.[23] CD117 rate was reported between 87.5-100%, CD34 between 80.3-88.1%, and DOG1 between 93.3-100%.[21],[22],[23] In this study, CD117 was found to be positive in all patients. DOG1 antigen, which started to be performed in our hospital in November 2014, was found positive in all patients who were tested after this date.

It has been stated that surgical treatment is sufficient in low-risk gastric GIST patients and imatinib treatment is required in residual, metastatic, recurrent or ruptured cases in accordance with the guidelines of the European Society for Medical Oncology and the National Comprehensive Cancer Network.[22],[23] In a large-scale meta-analysis, adjuvant treatment has been shown to reduce postoperative mortality and to increase resectability.[26] Adjuvant imatinib treatment rate was reported between 19.3-28.6%,[23],[24] and imatinib was given in 31.3% of patients as an adjuvant therapy in these patients.

There were some limitations in this study. Designing retrospectively and the single center are the main limitations of this study. Since patients whose 5-year follow-up has not been completed were included in this study, this situation led to low rates of overall and disease-free survival.


   Conclusion Top


Our findings show that in gastric GIST cases, as the primary tumor diameter and mitotic index increase, survival rates and the mean overall and disease-free survival times decrease. With these findings, it was found that the tumor diameter, mitotic index and the risk classification based on these parameters can be used as reliable predictors in determining the prognosis in these cases.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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