DOI: 10.1148/radiol.2312030248
(Radiology 2004;231:421-426.)
© RSNA, 2004
Scirrhous Gastric Carcinoma: Endoscopy versus Upper Gastrointestinal Radiography1
Mi-Suk Park, MD,
Hyun Kwon Ha, MD,
Byung Se Choi, MD,
Kyoung Won Kim, MD,
Seung-Jae Myung, MD,
Ah Young Kim, MD,
Tae Kyoung Kim, MD,
Pyo Nyun Kim, MD,
Nam-Ju Lee, MD,
Jeong Kyung Lee, MD,
Moon-Gyu Lee, MD and
Jin Ho Kim, MD
1 From the Departments of Diagnostic Radiology (M.S.P., H.K.H., B.S.C., K.W.K., A.Y.K., T.K.K., P.N.K., N.J.L., J.K.L., M.G.L.) and Internal Medicine (S.J.M., J.H.K.), Asan Medical Center, University of Ulsan College of Medicine, 388–1 Poongnap Dong, Songpa-Ku, Seoul 138–040, South Korea; and Department of Diagnostic Radiology, YongDong Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea (M.S.P.). Received February 24, 2003; revision requested May 16; final revision received September 16; accepted September 29. Address correspondence to H.K.H. (e-mail: hkha@www.amc.seoul.kr).
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ABSTRACT
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PURPOSE: To compare the accuracy of upper gastrointestinal (UGI) series and endoscopic examination in the diagnosis and localization of scirrhous gastric carcinoma.
MATERIALS AND METHODS: Seventy-two patients with pathologically proved scirrhous gastric carcinoma in surgical specimens were included. Preoperative reports at UGI series and endoscopic examination, which included impressions on the location and extent of the tumor, were compared with pathology reports, and the accuracy of the preoperative reports was calculated. Two gastrointestinal radiologists retrospectively reviewed the appearance of mucosa at UGI series.
RESULTS: Preoperative diagnoses at endoscopy were Borrmann type IV carcinoma in 28 patients (39%), type III carcinoma in 29 (40%), early gastric carcinoma in seven (10%), lymphoma in six (8%), atrophic gastritis in one (3%), and type II carcinoma in one (3%). Preoperative diagnoses at UGI series were type IV carcinoma in 44 patients (61%), type III carcinoma in 25 (35%), lymphoma in two (3%), and early gastric carcinoma in one (1%). Pathology reports were compared with the preoperative reports, and tumor location and extent were correct in the endoscopic examination reports of 24 patients (33%) and the UGI series reports of 49 patients (68%). In 68 patients, UGI series revealed thickened and irregular folds in 62 (91%), ulceration in 42 (62%), and nodularity in 22 (32%) at consensus review. Endoscopic biopsy samples were positive for malignancy in 66 patients (93%).
CONCLUSION: UGI series is superior to endoscopic examination in the diagnosis and localization of scirrhous gastric carcinoma.
© RSNA, 2004
Index terms: Endoscopy, 72.123 • Gastrointestinal tract, radiography, 72.1231 • Stomach, neoplasms, 72.321
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INTRODUCTION
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The macroscopic appearance of advanced gastric carcinoma varies and was classified by Borrmann as fungating (type I), excavated (type II), ulcerated and infiltrating (type III), and diffusely thickened or scirrhous (type IV) (1,2). Type IV carcinoma, or scirrhous gastric carcinoma, represents diffuse infiltrating adenocarcinoma—which is predominantly poorly differentiated and shows no circumscribed lesion (1). When the entire stomach wall is involved with type IV gastric carcinoma, the condition is called linitis plastica (1).
In contrast with usual cases of gastric cancers, scirrhous gastric carcinoma tends to spread over the peritoneum with rapid growth and early metastasis (3–8). Thus, the prognosis is poor in patients with this disease, and the 5-year survival rate is low (3–8). In general, the tumor cells in patients with scirrhous gastric cancer are located predominantly in the submucosa and are separated by large areas of abundant connective tissue (4,7,9,10). Sometimes these unique tumor growth patterns make it difficult for radiologists or endoscopists to detect the tumor with upper gastrointestinal (UGI) series or endoscopic examinations. In fact, the tumor cells are not easily detected in frozen sections of the surgical specimens. Negative findings at endoscopic biopsy or brushing cause a substantial delay in the diagnosis and treatment of these tumors (5,9); therefore, it is clinically important to diagnosis scirrhous gastric carcinoma before planning the treatment.
Endoscopic examination is generally considered to be more reliable than UGI series in the diagnosis of gastric carcinoma; however, some reports indicate that UGI series is more accurate than endoscopic examination in the diagnosis of scirrhous gastric carcinoma (7,9,10). To our knowledge, only one report has compared radiology with endoscopy in the diagnosis of scirrhous carcinoma of the stomach (9). Thus, the purpose of our study was to compare the accuracy of UGI series and endoscopic examination in the diagnosis and localization of scirrhous gastric carcinoma.
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MATERIALS AND METHODS
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Patients
A computerized search of medical records identified 2,114 patients with advanced gastric carcinoma who underwent surgery at our institution between January 1997 and December 1999. We also searched the pathology records for the subtype of gastric carcinoma and found that 112 patients had scirrhous carcinoma. Of these patients, 72 underwent both UGI series and endoscopic examination prior to surgery (25 patients underwent UGI series prior to endoscopic examination and 47 underwent endoscopic examination prior to UGI series), and these patients constituted our study group. Our study group consisted of 45 men (mean age, 49 years; age range, 39–76 years) and 27 women (mean age, 46 years; age range, 31–68 years). We analyzed the difference in age distribution between men and women with the 
2 test. There was no significant statistical difference for age distribution between groups (P = .056). The interval between UGI series and endoscopic examination was 1–21 days (mean, 4.5 days). All 72 patients underwent surgery, with performance of total gastrectomy in 38, subtotal gastrectomy in 22, and palliative gastrojejunostomy without gastrectomy in 12. The institutional review board at Asan Medical Center approved our study and did not require informed consent.
Imaging and Interpretation
All single- and double-contrast UGI series were performed after oral administration of 200–250 mL of 220% wt/vol barium suspension. Oral administration of an effervescent powder was used to establish adequate gastric distention. Multiple spot radiographs were obtained with fluoroscopic observation after adequate mucosal coating. Of our 72 patients, four underwent only a single-contrast barium examination because food material remained in the gastric lumen; the remaining 68 patients underwent a single- and a double-contrast barium examination. All preoperative diagnoses were assigned with UGI series by two attending experienced gastrointestinal radiologists (H.K.H. and A.Y.K., with 24 and 11 years of experience, respectively) in consensus without knowledge of the endoscopic findings. If advanced gastric carcinoma was suspected, the tumors were classified according to the Borrmann system (2). The location and extent of the tumor were recorded.
Two board-certified gastrointestinal radiologists (K.W.K. and N.J.L., with 6 and 5 years of experience, respectively) retrospectively reviewed preoperative radiographic findings in the same room at the same time and focused on the appearance of the mucosa (eg, fold effacement, ulcer, and mucosal nodularity). The reviewers were blinded to the descriptive findings in the surgery and pathology reports. Final conclusions were reached by means of consensus.
Endoscopy
Endoscopy with directed biopsy and cytology was performed by two gastroenterologists (J.H.K. and S.J.M., with 25 and 14 years of experience, respectively). End-viewing fiberoptic panendoscopes were used in all patients. Directed biopsy and brush cytology specimens were obtained in all patients, with the exception of one patient who had coagulation defects. Five biopsy specimens were obtained per patient. Preoperative diagnoses were made at endoscopy by the same physicians in consensus, without knowledge of the radiographic findings. The tumors were classified with the Borrmann system if advanced gastric carcinoma was suspected. The location and extent of the tumor were also described.
Data Analysis
The pathology reports of endoscopic biopsy specimens were reviewed. The location and extent of the tumor, as described in the pathology report, were evaluated and compared with those described in the original preoperative reports at UGI series and at endoscopic examination. The accuracy of the preoperative diagnoses at UGI series and at endoscopic examination was calculated. The accuracy of UGI series and endoscopic examination in the assessment of the location and extent of the tumor was also calculated.
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RESULTS
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The preoperative diagnosis of scirrhous gastric carcinoma in the original preoperative reports of endoscopic examination and UGI series is summarized in the Table. A correct visual diagnosis of type IV carcinoma was made in 28 of our 72 patients (39%) at endoscopic examination and in 44 (61%) at UGI series. The preoperative impression at endoscopic examination was type IV carcinoma in 28 patients (39%) (Figs 1, 2), type III carcinoma in 29 (40%), early gastric carcinoma in seven (10%) (Fig 3), lymphoma in six (8%), atrophic gastritis in one (3%) (Fig 4), and type II carcinoma (Fig 5) in one (3%). The preoperative impression at UGI series was type IV advanced gastric carcinoma in 44 patients (61%), type III carcinoma in 25 (35%), lymphoma in two (3%), and early gastric carcinoma in one (1%).
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Figure 1a. Scirrhous gastric carcinoma involving the entire body and antrum of the stomach in a 48-year-old woman. The preoperative impression was type IV gastric carcinoma at UGI series and endoscopic examination. (a) Compression image obtained with single-contrast barium examination shows diffuse narrowing of the stomach from the high body to the antrum. (b) Double-contrast barium image obtained in the supine position shows loss of distensibility with effacement of folds (arrows) at the entire body and the antrum. (c) Photograph obtained during endoscopy shows enlarged gastric rugae (arrows) with hyperemic change. The stomach was not fully distended, despite air insufflation.
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Figure 1b. Scirrhous gastric carcinoma involving the entire body and antrum of the stomach in a 48-year-old woman. The preoperative impression was type IV gastric carcinoma at UGI series and endoscopic examination. (a) Compression image obtained with single-contrast barium examination shows diffuse narrowing of the stomach from the high body to the antrum. (b) Double-contrast barium image obtained in the supine position shows loss of distensibility with effacement of folds (arrows) at the entire body and the antrum. (c) Photograph obtained during endoscopy shows enlarged gastric rugae (arrows) with hyperemic change. The stomach was not fully distended, despite air insufflation.
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Figure 1c. Scirrhous gastric carcinoma involving the entire body and antrum of the stomach in a 48-year-old woman. The preoperative impression was type IV gastric carcinoma at UGI series and endoscopic examination. (a) Compression image obtained with single-contrast barium examination shows diffuse narrowing of the stomach from the high body to the antrum. (b) Double-contrast barium image obtained in the supine position shows loss of distensibility with effacement of folds (arrows) at the entire body and the antrum. (c) Photograph obtained during endoscopy shows enlarged gastric rugae (arrows) with hyperemic change. The stomach was not fully distended, despite air insufflation.
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Figure 2a. Scirrhous gastric carcinoma in the body and proximal antrum of the stomach in a 43-year-old man. The preoperative impression was type IV gastric carcinoma at UGI series and either type IV carcinoma or lymphoma at endoscopic examination. The biopsy specimen was negative for malignancy. (a) Double-contrast barium image obtained with the patient in the supine position shows thickened and irregular folds with relatively mild loss of distensibility in the body. (b) Photograph obtained during endoscopy reveals circumferentially infiltrating lesion with erythematous mucosal change in the body of the stomach.
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Figure 2b. Scirrhous gastric carcinoma in the body and proximal antrum of the stomach in a 43-year-old man. The preoperative impression was type IV gastric carcinoma at UGI series and either type IV carcinoma or lymphoma at endoscopic examination. The biopsy specimen was negative for malignancy. (a) Double-contrast barium image obtained with the patient in the supine position shows thickened and irregular folds with relatively mild loss of distensibility in the body. (b) Photograph obtained during endoscopy reveals circumferentially infiltrating lesion with erythematous mucosal change in the body of the stomach.
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Figure 3a. Scirrhous gastric carcinoma involving the greater curvature side of the fundus and body of the stomach in a 39-year-old woman. The preoperative impression was type IV carcinoma at UGI series and early gastric carcinoma at endoscopic examination. (a) Double-contrast barium image obtained with the patient in the supine position shows thickened and irregular folds (arrowheads) with stiffness at the greater curvature side of the entire body. A small ulceration (arrow) is also seen. The gastric antrum is spared. (b) Photograph obtained during endoscopy reveals a small irregular ulcer (arrow) with mucosal convergence on the greater curvature side of the body. Enlarged gastric rugae are also seen.
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Figure 3b. Scirrhous gastric carcinoma involving the greater curvature side of the fundus and body of the stomach in a 39-year-old woman. The preoperative impression was type IV carcinoma at UGI series and early gastric carcinoma at endoscopic examination. (a) Double-contrast barium image obtained with the patient in the supine position shows thickened and irregular folds (arrowheads) with stiffness at the greater curvature side of the entire body. A small ulceration (arrow) is also seen. The gastric antrum is spared. (b) Photograph obtained during endoscopy reveals a small irregular ulcer (arrow) with mucosal convergence on the greater curvature side of the body. Enlarged gastric rugae are also seen.
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Figure 4a. Scirrhous gastric carcinoma of the body and proximal antrum of the stomach in a 63-year-old woman. The preoperative impression was type IV carcinoma at UGI series and atrophic gastritis with benign ulcer at endoscopic examination. (a) Left posterior oblique double-contrast barium image shows irregular mucosal nodularity (arrow) with relatively mild loss of distensibility of the stomach. (b) Compression image obtained with a single-contrast barium examination shows irregular mucosal nodularity (white arrows) with multiple small ulcerations (black arrows) of the antrum. (c) Photograph obtained during endoscopy shows diffuse atrophic change of the mucosa, with multiple ulcerations (arrows) at the body and antrum.
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Figure 4b. Scirrhous gastric carcinoma of the body and proximal antrum of the stomach in a 63-year-old woman. The preoperative impression was type IV carcinoma at UGI series and atrophic gastritis with benign ulcer at endoscopic examination. (a) Left posterior oblique double-contrast barium image shows irregular mucosal nodularity (arrow) with relatively mild loss of distensibility of the stomach. (b) Compression image obtained with a single-contrast barium examination shows irregular mucosal nodularity (white arrows) with multiple small ulcerations (black arrows) of the antrum. (c) Photograph obtained during endoscopy shows diffuse atrophic change of the mucosa, with multiple ulcerations (arrows) at the body and antrum.
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Figure 4c. Scirrhous gastric carcinoma of the body and proximal antrum of the stomach in a 63-year-old woman. The preoperative impression was type IV carcinoma at UGI series and atrophic gastritis with benign ulcer at endoscopic examination. (a) Left posterior oblique double-contrast barium image shows irregular mucosal nodularity (arrow) with relatively mild loss of distensibility of the stomach. (b) Compression image obtained with a single-contrast barium examination shows irregular mucosal nodularity (white arrows) with multiple small ulcerations (black arrows) of the antrum. (c) Photograph obtained during endoscopy shows diffuse atrophic change of the mucosa, with multiple ulcerations (arrows) at the body and antrum.
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Figure 5. Scirrhous gastric carcinoma involving the region from the esophagus to the proximal antrum of the stomach in a 29-year-old man. The preoperative impression was type IV carcinoma at UGI series and type II carcinoma at endoscopic examination. A, Full-column image obtained with the patient in the semiupright prone position shows diffuse narrowing and irregular contour of the stomach from the cardia to the antrum. A large ulcer (arrow) is seen at the lesser curvature side of the body. B, Double-contrast barium image obtained with the patient in the supine position shows a loss of distensibility and thickened and irregular folds. A large ulcerated mass (arrow) is seen. C, Photograph obtained during endoscopy reveals a large ulcer (arrow) with widely thickened folds on the posterior wall of the upper body.
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Tumors were located in the fundus and body in eight surgical specimens (11%); the body alone in eight (11%); the fundus, body, and antrum in 14 (19%); the body and antrum in 27 (38%); and the antrum alone in 15 (21%). Thus, the antrum was involved in 56 patients (78%). In our 72 patients, lesions extended to the esophagus in five and to the duodenum in one.
When compared with the pathology reports of the surgical specimens, the preoperative endoscopy reports of the location and extent of the tumor were correct in 24 patients (33%), overestimated in 10 (14%), underestimated in 33 (46%), and incorrect in five (7%). On the other hand, the original preoperative reports at UGI series were correct in 49 patients (68%), overestimated in 15 (21%), underestimated in seven (10%), and incorrect in one (1%).
The pathology reports of endoscopic biopsy samples and/or brushings were negative for malignancy in five of our 71 patients (7%) (Fig 2). The initial biopsy results were inconclusive because of material insufficiency in two patients, but results obtained several days later at repeat biopsy were positive for carcinoma.
In four of our 72 patients, the mucosal fold changes could not be evaluated with consensus review at UGI series because food material remained in the gastric lumen due to obstruction of the gastric outlet. At consensus review, UGI series revealed thickened and irregular mucosal folds in 62 of 68 patients (91%), ulceration in 42 (62%), and mucosal nodularity in 22 (32%).
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DISCUSSION
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Gastric carcinoma has been divided into various subtypes by Borrmann, Lauren, Ming, Mulligan and Rember, and the World Health Organization (1,2,12). The relationship between the various classifications and prognoses has been controversial, however, and none of these classifications has gained acceptance as the common or standard classification (1,2,13). Borrmann classified advanced gastric carcinoma into four types according to the direction of tumor growth and whether the carcinoma is demarcated or diffusely infiltrative (1,2). The Borrmann system has been used in the classification of gastric carcinoma at UGI series and endoscopic examination, especially in Germany and the Far East. The value of this classification system has been debated because of the relationship between the classification and the prognosis. It has been proved, however, that differentiation of type III and type IV carcinoma is worse than that of type I and type II carcinoma (1).
With the advent of endoscopy, accuracy in the diagnosis of gastric carcinoma has undoubtedly improved. When combined with biopsy and brushing cytology, endoscopy has an overall sensitivity of 95%–98% in the detection of gastric cancer (14,15). Nevertheless, endoscopy has a wide range of accuracy according to the gross tumor growth pattern and anatomic tumor location (10). In patients with linitis plastica, endoscopy has been reported to have a sensitivity of only 33%–73% (6,9–11). Endoscopists often have difficulty recognizing these lesions, as the tumors are located predominantly in the submucosa; therefore, the overlying mucosa appears normal. Furthermore, the tumor cells of scirrhous gastric carcinoma are often dispersed within a dense fibrous matrix and tend to be far apart. In some instances, pathologists encounter difficulty in detecting tumor cells in biopsy specimens and frozen sections (7,10); therefore, they are obliged to examine this material carefully to find cancer cells between the gastric crypts if scirrhous carcinoma is suspected. Thus, preoperative type-specific diagnosis and exact localization of the tumor extent are more important in the diagnosis of type IV gastric carcinoma than in the diagnosis of other types of gastric carcinoma.
In our study, endoscopic biopsy samples and/or brushings were positive for carcinoma in 66 of 72 patients (92%), which is a very high sensitivity compared with that of previous reports (6,9–11). This discrepancy may be related to the fact that at our institution, type IV gastric carcinoma is not synonymous with linits plastica, as is often the case in the West. At our institution, pathologists consider linitis plastica as part of type IV carcinoma when the entire stomach wall is involved with type IV carcinoma. Thus, desmoplastic reaction or fibrosis might be less prominent in some of our patients than linitis plastica in the classic sense.
Our results show that endoscopic examination led to the correct diagnosis in only 39% of our patients, whereas UGI series led to a correct diagnosis in 61%. In 14 of our 72 patients (19%), early gastric carcinoma, lymphoma, or atrophic gastritis was diagnosed at endoscopy. In such instances, serious deleterious consequences might have ensued if scirrhous gastric carcinoma had not been diagnosed preoperatively, because clinicians would have selected improper treatment methods, such as mucosectomy, chemotheraphy, or other surgical methods. Moreover, tumor localization was correct in 33% of our patients at endoscopic examination and in 68% of our patients at UGI series. These results clearly demonstrate the known limitation of endoscopy in the diagnosis of scirrhous gastric carcinoma (9–11,15). The main reason for the poor sensitivity of endoscopy in the detection of scirrhous gastric cancer is that the overlying mucosa often appears to be normal in these patients; therefore, the tumor extent is easily underestimated. In contrast, the fluoroscopist can get a sense of the distensibility and mobility of the gastric wall in real time and has no limitation of field of view, thus improving the detectability of type IV gastric carcinoma.
Although the classic form of scirrhous gastric carcinoma is defined as an infiltrating tumor that spares the superficial mucosal layer, the most common preoperative impression at both endoscopic examination and UGI series in our patients was type III gastric carcinoma (eg, ulceroinfiltrative lesion). In fact, mucosal changes, such as fold thickening or effacement (91%), ulceration (62%), and/or mucosal nodularity (32%), were seen more frequently than we had expected. Occasionally, UGI sereis depicted the thickened lesions with irregular folds and/or mucosal nodularity and without severe luminal narrowing or rigidity, thereby leading to a misdiagnosis of lymphoma or early gastric cancer.
Levine et al (9) reported that the radiologic appearance of scirrhous gastric carcinoma is somewhat different from the appearance that is classically known. They reported that localized scirrhous tumors often involve the proximal portion of the stomach and spare the antrum in 38% of patients. In our study, 22% of the patients had localized lesions in the gastric fundus and/or body with sparing of the antrum. One of the interesting results of our study is that the number of tumors involving the esophagus (n = 5) was greater than the number involving the duodenum (n = 1). Thus, our results were in agreement with the suggestion of Levine et al (9) that a significant percentage of patients with scirrhous tumors have localized lesions that involve the proximal stomach rather than the classic form of linitis plastica that involves the distal stomach.
The limitation of our study is that it is retrospective, so the results depend on the original preoperative reports at UGI series and endoscopic examination. Thus, information regarding tumor location and extent was evaluated according to the common sense of the radiologist, mucosal change, rigidity at fluoroscopy, and narrowing.
In conclusion, UGI series is definitely superior to endoscopic examination in correct tumor localization and diagnosis of scirrhous gastric carcinoma.
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ACKNOWLEDGMENTS
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We thank Bonnie Hami, MA, for her editorial assistance in preparing this manuscript.
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FOOTNOTES
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Abbreviation: UGI = upper gastrointestinal
Author contributions: Guarantor of integrity of entire study, H.K.H.; study concepts, H.K.H.; study design, M.S.P., H.K.H.; literature research, M.S.P.; clinical studies, A.Y.K., S.J.M., J.H.K.; data acquisition, B.S.C.; data analysis/interpretation, K.W.K., N.J.L.; statistical analysis, J.K.L.; manuscript preparation, M.S.P.; manuscript definition of intellectual content, T.K.K., P.N.K., M.G.L.; manuscript editing, M.S.P.; manuscript revision/review and final version approval, H.K.H.
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ABSTRACT
INTRODUCTION
