The submucosal tumor (SMT), or subepithelial tumor (SET), is clinically common protuberant lesions or lumps covered with intact mucosa (1). The origin and characteristics of most SMTs cannot easily be confirmed by gastrointestinal endoscopy or other radiological examinations. These SMTs can be divided into mesenchymal tumors and non-tumorous submucosal lesions (2). And the mesenchymal tumors include benign, borderline malignant and malignant tumors (3). The majority of SMTs seldom cause symptoms, but are detected incidentally by endoscopic or radiologic examinations (4).
As is known to all, gastrointestinal stromal tumor (GIST) has been already widely studied. There are relatively reliable guidelines for the diagnosis and treatment of gastric GISTs in Western and Asian countries, such as the clinical guidelines of GISTs published by the National Comprehensive Cancer Network (NCCN) in 2004 (5), and by the European Society of Medical Oncology (ESMO) in 2014 (6). However, excluding GISTs, for those other gastric SMTs, most of which are deemed benign, the necessity and timing of intervention has been ignored.
For reference, this paper will focus on the malignancy of gastric SMTs which are generally considered benign.
Heterotopic pancreas is defined as pancreatic tissue abnormally situated, which is anatomically characterized by the separation of pancreatic tissue from glands, without neurological or vascular continuity (7). The most common site of gastrointestinal heterotopic pancreas is the stomach (25–62%), followed by the duodenum (25–35%), and jejunum (16%) (8). The clinical manifestations of heterotopic pancreas is asymptomatic or non-specific, such as epigastric pain, nausea, vomiting and so on. Therefore, it is usually detected by endoscopy examination or autopsy incidentally (9).
The malignant tumors of gastric heterotopic pancreas are comparatively rare but need to be alarmed. There were 1,724 cases reported in the literature, which were composed of newborn to 89 years old patients. The sex ratio (M/F) was about 0.9. The tumor size ranged from 0.4 to 12.5 cm. Of all the 1,724 cases reported from 1980 to 2018, we found 29 cases with malignant features (Table 1). For a carcinoma to be described as arising from heterotopic pancreatic tissue, three criteria have been proposed: (I) the tumor must be found within, or close to, the ectopic pancreatic tissue; (II) transition between pancreatic structures and carcinoma must be observed (i.e., duct-cell dysplasia and/or carcinoma in situ); (III) the non-neoplastic pancreatic tissue must include at least fully developed acini and duct structures. The lesion in this case met all three criteria (10). The 29 cases were confirmed pathologically originated from gastric heterotopic pancreas. Among the 29 malignant cases, most of them were adenocarcinoma (21/29), and other pathological types included papillary cystadenocarcinoma, mucinous cystadenocarcinoma, neuroendocrine carcinoma, acinar cell carcinoma and so on. Mean age of the cases was 58.4±15.6 [27–86] years old and the male to female ratio was 14/15. The tumor size ranged from 1.7 to 12.5 cm (Table 2).
In addition to malignant cases of heterotopic pancreas, pancreatic intraepithelial neoplasia (PanIN) and intraductal papillary mucinous neoplasms (IPMN) have also been found in heterotopic pancreas. In 1,724 cases, 47 PanINs/IPMNs were found. Based on the mathematical analysis by Yachida et al. (75), it takes about 12 years for PanIN-1 to transform into PanIN-3, which can cause pancreatic ductal adenocarcinomas. According to the study by Jun et al. (76), PanINs/IPMNs were more frequently found in heterotopic pancreas of large size, deep location and infiltrative growth pattern. And most PanINs/IPMNs associated with heterotopic pancreas were low-grade, so progression to ductal adenocarcinoma during a short follow-up period is unlikely.
Therefore, although the malignant cases are rare in gastric heterotopic pancreas, we also need to be cautious when we find gastric heterotopic pancreas.
Leiomyoma is the most common SMT of upper gastrointestinal tract (77). Until the 1980s, GIST was not significantly different from a leiomyoma. It was not until 1983 when Mazur and Clark (78) proposed the concept of stromal tumors that their differences were gradually noticed. And in 1998, Hirota et al. (79) confirmed the pathogenic effect of Kit (CD117) proto-oncogene activating mutation on GISTs. Subsequently, GISTs were confirmed to have the characteristics of Cajal interstitial cells, which more specifically differ leiomyoma from GIST. So in order to get more reliable data, we only searched literatures between 2008–2018.
From 2008 to 2018, we reviewed 133 literatures and found 946 cases of gastric leiomyoma reported. Of the 946 cases, 16 were leiomyosarcomas. The clinical manifestations of these malignant tumors were not specific, such as epigastric pain, melena, gastric outlet obstruction and so on. The average age of these 16 cases was 52.7±20.7 [16–86] years old. The male to female ratio was 9/7. The average size of tumors was 7.06±5.60 [1–21] cm. The literature indicates that gastric leiomyosarcomas often occurs in the elderly and are typically of high grade malignancy (38). However, our review showed that some middle-aged and even young patients also suffer from this disease. And the tumor size was also extensively ranged. So neither age nor tumor size can be used as criteria for judging malignant potential. Some leiomyosarcomas had distant metastases at initial diagnosed. And liver and lungs were the most common sites.
Schwannomas of the GI tract, firstly presented by Daimaru et al. in 1988 (80), which are mostly benign tumors arising from the schwann cells of the nerve sheath. The most common site (60–70% of all GI cases) is the stomach, followed by the colon and rectum (3%). Small intestinal and esophageal schwannomas are rarely reported (81).
Malignant gastric schwannomas are extremely rare, with only a few cases reported (Table 1). Of all the 530 cases reviewed, 11 showed malignancy (Table 2). Based on these conditions, we may conclude that malignant gastric schwannoma has atypical appearance with common gastrointestinal symptoms. Among these cases, there were 6 males and 5 females. The mean age of these cases was 48.9±20.2 [10–73] years old and the mean size of tumors was 4.97±2.25 [1.9–9] cm. Although the data of all the 530 cases showed a female predominance, the sex ratio of malignant schwannoma was close to 1:1, even male patients accounted for the majority. So we speculate that the possibility of malignancy is more likely to occur in males. With the increase of malignant cases, gender preference may decrease, and we can more intuitively analyze the characteristics of malignant schwannoma.
Vascular tumors, including angiogenic tumors and lymphangiomas, are relatively rare. Angiogenic tumors include glomus tumor, hemangioendothelioma, hemangiopericytoma and so on.
Glomus tumor, which is composed of modified smooth muscle cells (82), is an arteriovenous anastomosis functioning without an intermediary capillary bed (83). Most glomus tumors are benign neoplasms that occur in the dermis or subcutis of the extremities (84). Glomus tumors of stomach are relatively rare and often lead to gastrointestinal bleeding due to ulceration of the mucosa over which it is covered (85). We reviewed 97 articles and 195 cases from 1980 to 2018. According to the literature, the ages ranged from 19 to 90. Pathologically confirmed malignancy was found in 11 cases, and potential malignancy was uncertain in 3 cases. The others were benign. Folpe et al. (62) suggested malignant criteria of glomus tumors: tumors with a deep location and a size of more than 2 cm, or atypical mitotic figures, or moderate to high nuclear grade and ≥5 mitotic figures/50 HPF. All these 11 tumor cases met the above criteria. Of the 10 cases, 5 were male and 5 were female. The gender of the remaining 1 patient was not mentioned. The average age was 59.3±9.2 [43–69] years and the average tumor size was 6.18±4.75 [1–17] cm. As mentioned above, we can conclude that malignant cases usually occur in elderly patients and the risk of distant metastases cannot be ignored. And there seems to be no correlation between tumor size and malignant potential. The clinical manifestations of malignant tumors are mostly gastrointestinal symptoms without specificity. Although malignancy is rare in glomus tumors, we still need to pay close attention to it. What’s more, due to the risk of distant metastasis, long-term follow-up is necessary.
Hemangioendotheliomas which affects various parts of the digestive system (86) is classified into four types: Epithelioid hemangioendothelioma, spindle cell hemangioendothelioma, kaposiform hemangioendothelioma and endovascular papillary hemangioendothelioma (malignant tumor known as Dabska) (87). Gastric hemangioendotheliomas were rarely reported, only 5 cases, 2 of which were malignant tumors (Table 2). The tumor size of these 2 cases was relatively large. However, due to the limited number of cases, we cannot summarize the reliable common features of their malignancies.
Hemangiopericytoma of the stomach is even rarer and we found only one benign case of gastric lipomatous hemangiopericytoma. Lipomatous hemangiopericytoma is a variant of hemangiopericytoma, which is histologically composed of benign hemangiopericytomatous and mature lipomatous components (88). This was the first case of lipomatous hemangiopericytoma that occurred in the stomach, and more data is needed to deduce the possibility of malignancy.
Lymphangiomas are relatively rare compared with hemangiomas. And the digestive tract is rarely involved (89). We found 11 cases of gastric lymphangiomas, none of which were malignant.
Granular cell tumor (GCT)
GCT, first described by Abrikosoff in 1926 (90), is a benign mesenchymal tumor originating from schwann cell (91). GCTs most commonly affect the tongue, skin and subcutaneous tissue. And, 5% to 11% of GCTs are found in the gastrointestinal tract, and they mostly affect the esophagus, colon, or stomach (92). According to Fanburg-smith, there are six histologic criteria: necrosis, spindling, vesicular nuclei with large nucleoli, increased mitotic activity (>2 mitoses/10 high-power fields at 200× magnification), high nuclear to cytoplasmic (N:C) ratio, and pleomorphism. Neoplasms that met three or more of these criteria were classified as histologically malignant; those that met one or two criteria were classified as atypical; and those that displayed only focal pleomorphism but fulfilled none of the other criteria were classified as benign (93).
From January 1st, 1980 to December 31st, 2018, we found 36 cases of gastric GCTs (Table 1). Some of these gastric GCTs may coexist with gastric carcinoma and early gastric cancer. However, the pathology of these GCTs was confirmed benign. There was only one case of malignant gastric GCT, which was reported in 1996 by Matsumoto et al. A 64-year-old female was referred to the hospital for treatment due to upper abdominal discomfort after eating and gastroscopic evidence of enlargement of a SMT which had been managed conservatively by the hospital since 5 years ago. This neoplasm consisted of two tumor masses, 5.5 and 7.0 cm in diameter, respectively, which were connected to form a dumbbell-shaped lesion. After distal partial gastrectomy, reconstruction was performed by Billroth-I Method. The pathology of this case met the following criteria mentioned above: increased mitotic activity and pleomorphism. Although it only met two of the criteria, 21 months after the operation, the tumor recurred along the inferior border of the liver, 10.5 cm × 7.5 cm × 7.5 cm. Pathological characteristics of the tumor were similar to those of the primary tumor. Thus, considering the clinical and pathological evidence of local recurrence, the neoplasm was considered malignant (74).
Gastric lipomas account for less than 1% of gastric tumors and 5% of gastrointestinal lipomas (94). Lipomas are completely benign, although there is a risk of local recurrence, less than 5% (95). Of the 141 cases reviewed, no malignancy was reported (Table 1).
Neurofibroma often occurs in neurofibromatosis and solitary neurofibromas are rare (96). Neurofibromatosis type 1 is more common, frequently involving gastrointestinal tract (97). We reviewed 13 cases of gastric neurofibroma and none of them had malignant features. However, the clinical manifestations of neurofibromatosis are various, ranging from localized microscopic proliferative lesions of autonomic nerves and interstitial cells of Cajal and diffuse microscopic ganglio/neuro/fibromatosis to grossly recognizable mass-forming neurofibromas and GIST (98). Therefore, when gastric neurofibroma is diagnosed, neurofibromatosis needs to be considered and be alert.
We reviewed literatures and analyzed cases of gastric SMTs including GCT, lipoma, schwannoma, heterotopic pancreas, leiomyoma, vascular tumor (glomus tumor, hemangioendothelioma, hemangiopericytoma, lymphangioma) and neurofibroma. In this literature, there are cases of malignancy among GCT, schwannoma, heterotopic pancreas, leiomyoma, glomus tumor and hemangioendothelioma. It suggests that although most of these gastric SMTs are considered benign, there are still possibilities of malignancy, which requires our attention, even active intervention and long-term follow-up.
Funding: Zhejiang Provincial Natural Science Foundation of China, LY17H160022.
Conflicts of Interest: The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
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