Original Report. Carcinoid Tumors of the Stomach: A Clinical and Radiographic Study
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1 Aaron J. Binstock 1 C. Daniel Johnson 1 David H. Stephens 1 Ricardo V. Lloyd 2 Joel G. Fletcher 1 Received July 25, 2000; accepted after revision September 29, Department of Radiology, Mayo Clinic, 200 First St. S.W., Mayo E2-B, Rochester, MN Address correspondence to J. G. Fletcher. 2 Department of Pathology, Mayo Clinic, 200 First St. S.W., Hilton 1142 D, Rochester, MN AJR 2001;176: X/01/ American Roentgen Ray Society Original Report Carcinoid Tumors of the Stomach: A Clinical and Radiographic Study OBJECTIVE. Our purpose is to describe associated and coexistent diseases of gastric carcinoid tumors, the unique biologic behavior of these tumors, the appearance of these tumors on fluoroscopic and CT images, and the radiologic management of these neoplasms. CONCLUSION. First, multiple gastric carcinoid tumors are associated with enterochromaffin-like cell hyperplasia, chronic atrophic gastritis, and pernicious anemia and have a low risk of malignancy. Second, solitary gastric carcinoid tumors, or gastric carcinoid tumors associated with multiple endocrine neoplasia type I (MEN-I) and Zollinger-Ellison syndrome, have a higher potential for metastatic disease. Third, the radiologic appearance and management of these tumors depend on the clinical background of the patient. C arcinoid tumors of the stomach are rare and exhibit unique biologic behavior that distinguishes them from their counterparts in the rest of the gastrointestinal tract. Retrospective pathologic studies have shed new light on the prognosis of patients with these tumors [1, 2]. Gastric carcinoids have been divided into three subtypes on the basis of the clinicopathologic classification scheme proposed by Bordi et al. [3], which includes assessment of comorbid conditions and the presence of enterochromaffin-like cell hyperplasia. enterochromaffin-like cells have also been implicated in the pathogenesis of poorly differentiated and highly malignant neuroendocrine carcinoma of the stomach [3], but these tumors are not included in our study. The increased use of endoscopy and advances in imaging have led to a relative increase in the detection of gastric carcinoid tumors, thereby requiring radiologists to make more management decisions. The purpose of our study was to examine our own experience regarding coexistent diseases associated with gastric carcinoid tumors, to review the clinical outcome of patients with different types of gastric carcinoid tumors, and to describe the appearance of these neoplasms on upper gastrointestinal examinations and CT scans. Subjects and Methods After we received institutional review board approval, we retrospectively reviewed the medical records and imaging studies of all 28 patients with pathologically proven carcinoid tumors of the stomach who had been examined at our institution since All patients underwent endoscopy and endoscopic biopsy. Twelve patients had radiologic studies before any intervention that were reviewed by two staff gastrointestinal radiologists (upper gastrointestinal images, five patients; CT scans, eight). Because it was retrospective, our study included a variety of imaging techniques. Three of the upper gastrointestinal imaging studies were single-contrast examinations, and two were double-contrast examinations. With the exception of one patient (for whom water had been used), all patients CT scans were obtained using oral iodinated contrast medium and were generally performed with IV contrast material (6/8). Effervescent granules and IV glucagon were not used for any CT examinations. Mean follow-up time after diagnosis was 29 months. We classified patients as having type I carcinoid tumors if they had hypergastrinemia and histologic evidence of chronic atrophic gastritis and enterochromaffin-like cell hyperplasia, with or without perni- AJR:176, April
2 Binstock et al. cious anemia. Type II patients were those who had documented multiple endocrine neoplasia type I (MEN-I) and Zollinger-Ellison syndrome. Type III patients were those who had solitary tumors not associated with hypergastrinemia or any comorbid conditions defining types I and II gastric carcinoid tumors. Results We used medical history, serology studies, and pathology to classify definitively 24 of 28 patients as having one of the three subtypes of gastric carcinoid tumors [3]. Four patients with multiple small tumors had not had sufficient serologic testing to permit accurate characterization. We classified 18 of 24 patients with type I gastric carcinoid tumors. All patients had two or more comorbid conditions associated with type I gastric carcinoid tumors, including serum hypergastrinemia (12/18), pernicious anemia (11/18), and chronic atrophic gastritis with enterochromaffin-like cell hyperplasia (14/18). Most patients (14/18) had tumors smaller than 1 cm, and all tumors were smaller than 2 cm. The majority of the patients (14/18) also had multiple gastric tumors, with 16 of 18 patients having tumors predominantly in the body and fundus (Figs. 1 and 2). All but one patient had disease localized to the mucosa or submucosa; one patient had local lymph node metastasis. We identified no tumor-related deaths or carcinoid syndrome in this group of patients. We examined one patient with a type II gastric carcinoid tumor as well as MEN-I and Zollinger-Ellison syndrome. This patient has been described previously by one of the authors of this study [4]. Double-contrast upper gastrointestinal radiographs and CT scans of this patient revealed diffuse gastric wall thickening with multiple gastric tumors of various sizes (Fig. 3). Two pancreatic islet cell tumors (i.e., gastrinomas) were also identified. This patient was treated with total gastrectomy and pancreatoduodenectomy. Local perigastric lymph node metastases were excised at surgery. After 39 months of follow-up of this patient, we found no recurrence. Solitary type III gastric carcinoid tumors were found in five patients, three of whom were men. The masses were cm, with a tendency to ulcerate. Two of five patients had lymph node or liver metastases or both. The patient with liver metastases had carcinoid syndrome (Fig. 4), and both patients died within 17 months of diagnosis. Radiologic findings of five upper gastrointestinal images and eight CT scans were correlated with the findings on endoscopy. Type I tumors appeared as small sessile polyps on upper gastrointestinal radiographs (2/3 tumors) (Fig. 2) and as small enhancing mucosal masses on CT scans (2/4 tumors). Upper gastrointestinal imaging did not show tumor multiplicity in any of the three patients who had the condition, and CT scans showed tumor multiplicity in two of four affected patients. The patient with type II gastric carcinoid tumors had multiple gastric masses on upper gastrointestinal radiographs and CT scans, with the former revealing ulcerations within several of these masses. An upper gastrointestinal image had been obtained for only one patient A with a type III carcinoid tumor. The radiograph revealed a flat ulcerating lesion along the lesser curvature of the stomach. CT scans revealed one of three of the primary tumors in type III patients. The tumor appeared as focal thickening of the gastric wall along the greater curvature (Fig. 4). Both upper gastrointestinal imaging and CT performed reasonably well in helping to detect these tumors, even though optimal technique was not always used. Upper gastrointestinal imaging was useful in identifying patients with primary lesions 3 mm or larger (4/4), and CT Fig year-old woman with hypergastrinemia and chronic atrophic gastritis. A, Contrast-enhanced CT scan obtained using oral contrast material shows small enhancing mucosal or submucosal polyp (arrow) along lesser curvature of stomach. B, Contrast-enhanced CT scan obtained at different level than A reveals another small mucosal or submucosal polyp surrounded by oral contrast material (arrow). Endoscopy showed multiple fundic and body type I gastric carcinoid tumors. Fig. 2. Double-contrast upper gastrointestinal radiograph of 60-year-old man with chronic atrophic gastritis, pernicious anemia, and type I gastric carcinoid tumors. Image shows solitary 5-mm polyp (arrow) along posterior wall of body of stomach. Endoscopy (not shown) revealed multiple small fundic and body submucosal type I gastric carcinoid tumors. B 948 AJR:176, April 2001
3 Carcinoid Tumors of the Stomach was useful in identifying patients with tumors 1 cm or larger (4/4). Tumors smaller than 1 cm were not seen on CT scans (0/4). Discussion Few reports in the radiology literature describe the appearance of gastric carcinoid tumors. Balthazar et al. [5] described the radiologic appearance in a series of eight gastric carcinoid tumors, seven of which were solitary tumors. Berger and Stephens [4] reported a case of gastric carcinoid tumor in the setting of MEN-I and Zollinger-Ellison syndrome, coexistent diseases that we included in our current series. Researchers in both of these studies examined radiologic findings before the current concepts of gastric carcinoid physiology or clinicopathologic classification were established, and, consequently, they were unable to correlate the radiologic appearance of lesions with our current pathophysiologic understanding. Gastric carcinoid tumors represent a small minority (approximately 0.3%) of gastric tumors [6] but 11 41% of all gastrointestinal endocrine tumors [1]. Clinicopathologic characterization of gastric carcinoid tumors has revealed three subtypes, each with a unique endoscopic appearance, predisposing conditions, and clinical outcomes (Fig. 5). Our study delineates the contribution of the upper gastrointestinal examinations and contrast-enhanced CT scans in these patients. A Fig year-old man with multiple endocrine neoplasia, type I, Zollinger-Ellison syndrome, and type II gastric carcinoid tumors. A, Double-contrast upper gastrointestinal image shows multiple nodular masses (arrowheads) and thickened rugal folds involving fundus and body of stomach. Duodenal sweep is displaced to right (arrows) as a result of islet cell tumor in pancreatic head. B, Unenhanced CT scan obtained using oral contrast material shows multiple polypoid gastric masses and diffuse gastric wall thickening. C, Unenhanced CT scan obtained 3.5 cm caudad to B shows densely calcified mass (arrow) in pancreatic tail, representing pancreatic islet cell tumor. Fig. 4. Contrast-enhanced CT scan (obtained without oral contrast material) of 60-year-old woman with type III (solitary) gastric carcinoid tumor reveals localized thickening of the posterior gastric wall (arrows) with diffuse liver, splenic, and perigastric lymph node metastases (arrowheads). Type I gastric carcinoid tumors represented most of the cases in this and previous studies [1, 2, 6]. Type I tumors are associated with enterochromaffin-like cell hyperplasia, hypergastrinemia, and chronic atrophic gastritis, with or without pernicious anemia. Chronic atrophic gastritis is the pathologic condition with the highest frequency of enterochromaffin-like cell carcinoids in humans. In chronic atrophic gastritis, loss of acid-secreting parietal cells in the body and fundus, frequently caused by an autoimmune destructive process, causes permanent reduction of gastric acid secretion [4]. Consequently, stimulation of antral G cells to produce gastrin is uninterrupted. Hypergastrinemia acts as a trophic factor for enterochromaffin-like cells, resulting in hyperplasia. B Several mechanisms involved in transforming enterochromaffin-like cell hyperplasia to carcinoid tumor have been hypothesized. Overexpression of bcl-2 protein enhances cell survival by blocking programmed cell death (apoptosis), thereby prolonging the period during which the effects of genetic and environmental influences may incite tumor induction [3, 7, 8]. The tumors are subsequently multicentric and invariably surrounded by enterochromaffin-like cell hyperplasia, predominately located in the fundus and body of the stomach. Tumors are mucosal or submucosal, with most measuring 1 cm or less. They are generally discovered incidentally because of nonspecific symptoms (dyspepsia, pain, nausea, or anemia). Although the findings are controversial, C AJR:176, April
4 Binstock et al. Fig. 5. Drawing shows pathophysiologic schema for development of different types of gastric carcinoid tumors. Type I carcinoid tumors are small benign tumors, arising in setting of chronic atrophic gastritis and chronic hypergastrinemia. Type II tumors can be large and polypoid; arise in patients with multiple endocrine neoplasia type I and Zollinger-Ellison syndrome; and are prone to nodal metastasis. Type III tumors, which are not associated with hypergastrinemic state, are large, sporadic, solitary tumors prone to nodal and hepatic metastases, as well as to carcinoid syndrome. some studies have reported that infection with Helicobacter pylori results in hypergastrinemia and induction of gastric carcinoid tumors in animals and, more rarely, in humans [3, 9]. Type I gastric carcinoid tumors generally represent benign disease. Nodal and hepatic metastases are very rare, occurring in 2% of the patients in the larger studies and causing no tumor-related deaths [1, 6, 10]. These patients can be treated conservatively either with endoscopic surveillance and local treatment for tumors 1 cm or smaller or with partial gastric resection (including the region of the gastrinproducing cells [antrectomy]) for tumors larger than 1 cm [10]. Radiologic studies may underestimate the number of gastric carcinoid tumors because of either the small size of the tumors or inferior radiologic technique. Type II gastric carcinoid tumors are the least common type, representing 5 10% of gastric carcinoid tumors. They are seen in the hypergastrinemic state of Zollinger-Ellison syndrome in association with MEN-I. Gastric carcinoids are rarely seen in hypergastrinemic patients with sporadic Zollinger-Ellison syndrome without MEN-I because allelic loss of the MEN-I suppressor gene is necessary to induce the transformation from enterochromaffinlike cell hyperplasia to carcinoid tumors [3]. Approximately 30% of patients with MEN-I will have gastric carcinoid tumors [2, 10]. Type II carcinoids also arise from enterochromaffin-like cells in the setting of hyperplasia. These carcinoids are multicentric and variable in size but are prone to developing local lymph node metastasis. Tumor-related death is rare, as is carcinoid syndrome. The appearance of these tumors on CT scans and upper gastrointestinal radiographs can be striking because there are multiple masses in the setting of diffuse gastric wall thickening. Treatment indications for type II gastric carcinoids are largely unknown. Modalities include total gastrectomy (as in one of our patients), surgical resection of tumors, endoscopic polypectomy, or treatment with somatostatin analogues and observation [10]. Omeprazole, a protonpump inhibitor frequently used to treat the gastric acid hypersecretion in these patients, causes hypergastrinemia and subsequent enterochromaffin-like cell hyperplasia, but it does not result in the transformation from hyperplasia to neoplasia [11]. Type III gastric carcinoid tumors are sporadic tumors and are not associated with a hypergastrinemic state. They represent about 13% of gastric carcinoid tumors [6]. Biologically, these tumors are highly proliferative and have been shown to have intense overexpression of a mutated protein called p53. The p53 protein is encoded by a tumor suppressor gene and is thought to be responsible for apoptosis of damaged cells [12]. Unlike types I and II tumors, type III gastric carcinoid tumors are large solitary tumors that may show ulceration and are more likely to be invasive with distant metastases. They appear with striking predominance in men; among patients diagnosed with type III carcinoid tumors, 80% are men [1]. Metastasis is dependent on tumor size, with fewer than 10% of single tumors smaller than 1 cm metastasizing, as opposed to 66% of tumors larger than 3 cm metastasizing [2]. The histologic type of these tumors also affects the prognosis. Carcinoid syndrome may be seen in patients with liver metastasis. The prognosis is poor, with 20% of patients surviving 5 years. Such tumors are more aggressive and should be treated with total gastrectomy with en bloc removal of regional lymph nodes when liver metastases are not present [1, 2, 10]. Systemic therapy, chemotherapy, or antitumoral therapies are recommended when liver metastases are present. Our improved understanding of gastric carcinoid tumors has important implications for the radiologic treatment of patients. When these tumors are suspected, double-contrast upper gastrointestinal imaging and contrast-enhanced CT with effervescent granules, IV glucagon, and narrow collimation should be used to detect small mucosal masses. The discovery of polyps in a patient known to have chronic atrophic gastritis should alert the radiologist to the possibility of type 1 gastric carci- 950 AJR:176, April 2001
5 Carcinoid Tumors of the Stomach noid tumors. Endoscopy will be required to confirm the presence of enterochromaffin-like csell hyperplasia and gastric carcinoid tumors, as opposed to other polyps or adenocarcinoma to which patients with pernicious anemia are predisposed [2]. The appearance of multiple polyps in the gastric body and fundus should prompt endoscopy and raise the question of gastric carcinoid tumors when serum hypergastrinemia is present in any patient. In patients with MEN-I, all gastric polyps should be endoscopically examined for possible type II gastric carcinoid tumors, which are prone to nodal metastasis and can occur with normal serum gastrin levels. Finally, CT scans are necessary to properly assess types II (MEN-I associated) and III (sporadic) gastric carcinoid tumors, given the increased predisposition for nodal and hepatic metastases. An understanding of these unique tumors explains their radiographic appearance and provides guidelines for the appropriate use of upper gastrointestinal imaging and CT in detection and management. References 1. Rindi G, Luinetti O, Cornaggia M, Capaella C, Solcia E. Three subtypes of gastric argyrophil carcinoid and the gastric neuroendocrine carcinoma: a clinicopathologic study. Gastroenterology 1993; 104: Modlin IM, Tang LH. The gastric enterochromaffin-like cell: an enigmatic cellular link. Gastroenterology 1996;111: Bordi C, D Adda T, Azzoni C, Ferraro G. Pathogenesis of ECL cell tumors in humans. Yale J Biol Med 1998;71: Berger MW, Stephens DH. Gastic carcinoid tumors associated with chronic hypergastrinemia in a patient with Zollinger-Ellison syndrome. Radiology 1996;201: Balthazar EJ, Megibow A, Bryk D, Cohen T. Gastric carcinoid tumors: radiologic features in eight cases. AJR 1982;139: Rindi G, Bordi C, Rappel S, La Rosa S, Stolte M, Solcia E. Gastric carcinoids and neuroendocrine carcinomas: pathogenesis, pathology, and behavior. World J Surg 1996;20: Korsmeyer SJ. Bcl-2 initiates a new category of oncogenes: regulators of cell death. Blood 1992; 80: Azzoni C, Doglioni C, Viale G, et al. Involvement of bcl-2 oncoprotein in the development of enterochromaffin-like cell gastric carcinoids. Am J Surg Pathol 1996;20: Hirschowitz BI. Clinical aspects of ECL-cell abnormalities. Yale J Biol Med 1998;71: Cadiot G, Cattan D, Mignon M. Diagnosis and treatment of ECL cell tumors. Yale J Biol Med 1998; 71: Solcia E, Rindi G, Havu N, Elin G. Qualitative studies of gastric endocrine cells in patients treated long-term with omeprazole. Scand J Gastroenterol 1989;24[suppl 166]: Peny MO, Donckier V, Gelin M, Haot J, Noel JC. Sporadic carcinoid of the stomach: a highly proliferative disease with a probable role for p53 protein dysregulation. Eur J Gastroenterol Hepatol 1999;11: AJR:176, April
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