0016·5107/90/3604·0342$02.00
GASTROINTESTINAL ENDOSCOPY Copyright © 1990 by the American Society for Gastrointestinal Endoscopy
Endoscopic ultrasonography for the evaluation of smooth muscle tumors in the upper gastrointestinal tract: an experience with 42 cases T. L. Tio, MD, PhD G. N. J. Tytgat, MD, PhD F. C. A. den Hartog Jager, MD Amsterdam, The Netherlands
Before surgery, 12 patients with suspected leiomyoma and 12 patients with suspected leiomyosarcoma were studied by endoscopic ultrasonography (EUS), computed tomography (CT), endoscopy, and barium swallow. The results were correlated with surgery and histology. Ten leiomyomas, one benign gastric ulcer, one carcinoid metastasis, eight leiomyosarcomas, two leiomyoblastomas, one mucus secreting adenocarcinoma, and one bronchial carcinoma were diagnosed. Eighteen additional patients suspected to have benign submucosal lesions by endoscopy and barium meal were treated non-surgically, and studied by EUS and CT. EUS was superior to other imaging techniques in the detection, staging, and follow-up of submucosal smooth muscle tumors because of clear imaging of the intramural abnormality and adjacent lymph nodes. (Gastrointest Endosc
1990;36:342-350)
Submucosal gastrointestinal tumors are usually detected by single or double-contrast barium swallow demonstrating a smoothly marginated filling defect in the barium column or a double contour. Distinction between a benign and malignant lesion may be difficult or impossible.l-5 Endoscopy can visualize a submucosal neoplasm as a bulge covered with normal mucosa or occasionally associated with a central ulcer. 6 ,7 Endoscopic biopsy is not always helpful in ascertaining the diagnosis because the lesion cannot always be reached with a standard biopsy forceps except when special techniques are used. B, 9 Computed tomography (CT) may identify a submucosal tumor as a hypodense lesion immediately adjacent to the lumen or as a thickening of the gastrointestinal wall after filling the lumen with contrast. 1O- l5 Endoscopic ultrasonography (EUS) is accurate in the detection and staging of gastrointestinal Received July 20, 1989. For revision September 26, 1989. Accepted November 27, 1989. From the Academic Medical Center, Department of Gastro-EnteroHepatology, Amsterdam, The Netherlands. Reprint requests: T. L. Tio, MD, Department of Gastro-Entero-Hepatology, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands.
342
neoplasms by directly approaching the target lesion with a high frequency real-time ultrasonic beam via the gastrointestinal lumen. 16- 26 Endoscopic ultrasonography (EUS) has been reported to be more accurate than endoscopy, barium meal, and CT in the detection and staging of smooth muscle tumors in the upper gastrointestinal tract. 27 A more extended series than our previously published data was performed to assess the accuracy and limitations of EUS in the detection, staging, and followup of smooth muscle tumors in the upper gastrointestinal tract by comparing EUS findings to those of CT, endoscopy, barium swallow, and histology of resected tissue. Moreover, application of EUS-guided aspiration cytology is described. MATERIALS AND METHODS
Between December 1983 and April 1988, EUS was performed in 42 patients in whom a smooth muscle tumor was suspected after endoscopic and radiographic examination. CT scan was performed before or after EUS examination. Interpretation of EUS images was made prospectively without knowledge of the results of other investigations. The patients were divided into three groups. The first group GASTROINTESTINAL ENDOSCOPY
(group 1) consisted of 12 patients undergoing surgery for a large lesion or a bleeding tumor thought to be benign because initial endoscopic biopsies were negative for malignancy. The second group (group 2) consisted of 12 patients who underwent surgery because of suspected malignancy. The timing of surgery was approximately 4 weeks after EUS and CT examination. The third group (group 3) consisted of 18 patients with smaller, sharply delineated lesions, thought to
Figure 1. A prototype Olympus video echoendoscope (VUM2) with a small echoprobe (e) attached to the tip of a sideviewing videoendoscope.
be benign, who did not have surgery but were followed with EUS, endoscopy, and CT when available. The results of EUS were correlated with the results of endoscopy, barium swallow, CT scan, and detailed histological examination of resected specimens and/or long-term follow-up. The interpretation of the gastrointestinal wall structure was based upon the results obtained by detailed examination of fresh autopsy materials and resected specimens. The normal gastrointestinal wall was visualized as a five-layer structure, which showed a close correlation with microanatomy.17-20,26 A diagnosis of benign tumor was made with EUS when a sharply demarcated hypoechoic (echo poor) homogeneous mural tumor, without evidence of penetration into surrounding tissue or lymph node involvement was recognized. Penetration was defined as extension of the mural hypoechoic pattern into the adjacent structures with total destruction of the normal gastrointestinal wall architecture. A diagnosis of malignancy was considered when an irregularly demarcated hypoechoic inhomogeneous mass lacking clear margins was found, or when a clearly demarcated hypoechoic and inhomogeneous tumor penetrated into adjacent structures was visualized. Associated central ulcerative defect within the hypoechoic mass or fistula, with or without evidence of lymph node involvement, may be found. 27 Analysis of accuracy of EUS interpretation was based on the histology of resected specimens, transmural biopsy at surgery or long-term follow-up.
Table 1. Results of endoscopy, barium swallow, CT, EUS, and histology of the resection specimens (group 1) Size No. of of patients tumor (cm)
Localization
Endoscopy
Barium swallow
CT
Hypodense tumor
3
3
Esophagus
Bulge with normal mucosa
Filling defect
1
3
Esophagus
Bulge with normal mucosa
Filling defect
1
4
Stomach
No abnormality
2
5
Stomach
Bulge with normal mucosa
No abnormality Filling defect
2
3
Stomach
Bulge with normal mucosa
Filling defect
2
4
Stomach
Bulge with an ulcer
Filling defect
1
3
Stomach
Bulge with an ulcer
Filling defect
VOLUME 36, NO.4, 1990
EUS
Sharply demarcated homogeneous hypoechoic lesion (N = 2) or local thickening of the muscularis propria (N = 1) Hypodense tumor Sharply delineated hypoechoic tumor in the submucosa Aortic aneurysm Sharply demarcated hypoechoic tumor Hypodense tumor Sharply demarcated hypoechoic tumor with anechoic ductular structures Thickening of Local thickening of the the wall (N = muscularis propria 1) Hypodense tumor Sharply demarcated hypoechoic mass with a central ulcer protruding into the gastric lumen No abnormality Sharply demarcated hypoechoic lesion in the submucosa adjacent to an ulcerative lesion
Histology
Leiomyoma
Carcinoid metastasis Leiomyoma Leiomyoma with blood vessels
Leiomyoma
Leiomyoma
Benign ulcer with extensive nodular margins
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Studies were routinely performed with a prototype Olympus echoendoscope (EU-M1) or a commercially available model (EU-M2) in which a small mechanical sector echoprobe was attached to a side-viewing endoscope. The length of the rigid tip was 4.2 cm and the diameter of the echoprobe was 13 mm. 17- 26 The frequency of the transducer was 7.5 MHz with a penetration depth of approximately 10 cm and an axial resolution of 0.2 mm. Axial resolution was defined as the ability of the echoprobe to distinguish between two points within the direction of a transmitted wave. A prototype Olympus echoendoscope with a frequency of 10 MHz was also used. The penetration depth of ultrasound was 5 cm with an axial resolution of 0.15 mm. Recently, an Olympus echoendoscope with a switchable frequency of 7.5 MHz and 12 MHz and a biopsy channel for ultrasonic guided puncture or biopsy (EU-M3) became available. Currently, we use a videoechoendoscope for simultaneous recording of endoscopic and ultrasonic images (Fig. 1). The echoprobe was routinely covered with a water-filled balloon to improve ultrasonic images. This water-filled balloon method was particularly useful for the investigation of the esophagus, cardia, and the pyloric region. Filling the gastric lumen with water facilitated clear visualization of the gastric wall. Lesions which could not be adequately coated with water were investigated using both methods. 21 • 22 Duration of EUS examination was approximately 15 to 20 min. No complications occurred during EUS examination in this study. RESULTS
Table 1 summarizes the results of endoscopy, barium swallow, CT, EUS, and histology of resected specimens (group 1). Endoscopy and barium swallow identified a bulging lesion with normal mucosa or a smooth filling defect suspicious for a benign smooth muscle tumor in 11 of 12 patients. CT revealed a clearly delineated hypodense tumor adjacent to the contrast-filled lumen in 10 of 12 patients. EUS imaged a well-circumscribed homogeneously hypoechoic tumor (diameter, 3 to 5 em) protruding into the esophagogastric lumen (Fig. 2) or extending into the perigastric tissue in 9 of 12 patients. In the remaining three patients, local thickening of the muscularis propria was recognized. In addition, anechoic duct-like patterns, presumably vascular structures, were found in 2 of 12 patients. The histology of resected specimens confirmed the diagnosis of leiomyoma in 10 patients. A carcinoid tumor of the bronchus penetrating into the esophageal wall was found in one patient and a benign gastric ulcer with extensive nodular margins in one patient. The accuracy rate of EUS was 83%. The sensitivity was 90%. Table 2 summarizes the results of endoscopy, barium swallow, EUS, and CT in the evaluation of maligFigure 2. A, EUS photograph shows a polypoid well-deline-
ated tumor mass (t) without penetration into the surrounding tissues, adjacent to the aorta (ao). b, water-filled balloon covering the echoprobe. B, CT scan shows a hypodense, 344
clearly delineated tumor mass (t) adjacent to the esophageal lumen (I). ao, aorta. C, Barium swallow photograph shows five smoothly marginated filling defects with sharply demarcated margins. GASTROINTESTINAL ENDOSCOPY
Table 2. Results of endoscopy, barium swallow, CT, EUS, and histology of the specimens (group 2) No. of patients
Size of tumor (cm)
Localization
Endoscopy
Barium swallow
CT
EUS
Histology
Bizarrely (lack of marginations) demarcated inhomogenous mass with or without hyperechoic structures (air) Hypoechoic mass adjacent to the transducer with suspicious adjacent lymph nodes Unsharply delineated mass adjacent to the liver or spleen Clearly demarcated hypoechoic mass with a central ulcerative lesion Clearly demarcated hypoechoic mass with suspicious lymph nodes Clearly demarcated hypoechoic mass with a central ulcerative lesion Clearly demarcated hypoechoic mass with a central ulcerative lesion
Leiomyosarcoma with or without a fistula
2
4 9
Esophagus
Ulcerative tumor with or without a fistula
Tumor with or without a deep fistula
Hypodense mass
1
5
Esophagus
Bulge covered with normal mucosa
Filling defect
Hypodense mass adjacent to the lumen
2
8
Stomach
Bulge covered with normal mucosa
Double contrast
3
5
Stomach
Bulge with an ulcer
Double contour mass with a central ulcer
Hypodense mass directly adjacent to the liver or spleen Not performed
2
Stomach
Bulge with a central ulcer
Double contour with a central ulcer
Hypodense mass
1
6
Stomach
Bulge with a central ulcer
Double contour with a central ulcer
Hypodense mass
1
4
Stomach
Bulge with a central ulcer
Double contour with a central ulcer
Hypodense mass
5/12
5/10
Correct diagnosis EUS/ histology
6/12
nant smooth muscle tumors (group 2). The tumors were proven to be non-resectable at surgery in three patients. In the remaining nine patients, resection was performed. In the non-resectable cases endoscopy and barium swallow recognized an extensive tumor in the esophagus and stomach in three patients suspicious for malignancy because of rigidity, displacement, and tortuosity of the involved organ. CT scan revealed a hypodense mass adjacent to the esophageal or gastric lumen without further clarification. EUS visualized a deeply penetrating hypoechoic, inhomogeneous tumor adjacent to the bronchus in one patient, infiltrating into the liver in a second patient and into the spleen in another. Adjacent lymph nodes were strongly suspicious of malignancy. The histology of the transmural biopsy of the tumor at the time of surgery confirmed the diagnosis of bronchogenic carcinoma in one patient and leiomyosarcoma in two patients. Endoscopy and barium swallow recognized a muVOLUME 36, NO.4, 1990
Bronchus carcinoma
Non-resectable leiomyosarcoma
Leiomyoblastoma (N = 4) leiomyosarcoma (N
=
1) Leiomyosarcoma with adjacent lymph node metastasis Mucous-secreting adenocarcinoma with a fistula Leiomyoblastoma
10/12
cosal bulge with a periesophageal fistula (N = 1) or a central ulcerative lesion in the resectable cases. CT scan revealed a hypodense tumor adjacent to the gastric lumen. EUS visualized a clearly demarcated hypoechoic mass (diameter, 4 to 6 em) beyond the mucosa with a fistula or with an ulcerating defect or with smooth mucosa. Suspicious adjacent lymph nodes were found in two of these patients. Histology of resected specimens confirmed the size, configuration, and site of tumors obtained with EUS. Leiomyosarcoma was found in four, leiomyoblastoma in two 27- 33 (Fig. 3), mucoid secreting adenocarcinoma in one, and metastatic lymph nodes in two. During the follow-up period after surgical resection (from 9 to 36 months) in five patients, only EUS detected mural and nodal abnormalities. In the patient with a previous fistula in the distal esophagus, EUS demonstrated a submucosal deeply penetrating hypoechoic mass adjacent to the hilum of the liver with suspicious 345
B
Figure 5. A, EUS photograph shows a sharply delineated Figure 3. A, EUS photograph shows the transverse section
of an extensive tumor (t) with central ulcer (u). lu, lumen; b, balloon. B, Corresponding histology of the resection specimen reveals a leiomyoblastoma (t) with ulceration (u). C, Endoscopy reveals a tumor mass with a central ulcer carrying necrotic materials.
hypoechoic lesion (t) directly adjacent to the balloon (b) compatible with leiomyoma. B, Corresponding CT scan photograph shows a hypodense polypoid lesion (t) protruding into the esophageal lumen (Iu) ao, aorta. C, Corresponding endoscopic photograph shows bulging of the wall covered with normal mucosa.
regional lymph nodes. Cytology of the percutaneous ultrasonic guided puncture compared with the previous histology of the resected specimen ascertained the diagnosis of recurrent leiomyosarcoma. 34 ,35 In the
patient with adenocarcinoma EUS-guided aspiration cytology with a gastric aspiration biopsy needle was obtained. Malignant cells compatible with adenocarcinoma were found. 34
346
GASTROINTESTINAL ENDOSCOPY
Table 3 summarizes the results of endoscopy, barium swallow, ES, and CT (group 3). Endoscopy and barium swallow revealed a bulge covered with smooth overlying mucosa in the esophagus in 6 patients, in the stomach in 13 patients, and in the duodenum in 2 patients suspected of having a leiomyoma (Fig. 4). CT scan revealed wall thickening in the esophagus in four patients, in the stomach in three of five patients, and no abnormalities in the duodenum. Initial EUS imaged a sharply demarcated hypoechoic lesion with similar echodensity to the muscle layer in eight patients (Fig. 5) or local thickening of the muscularis propria beyond the normal overlying mucosa and submucosa (Fig. 6) suggestive of leiomyoma in seven patients. In the remaining three patients, EUS visualized a serpiginous duct-like anechoic structure adjacent to the esophageal wall suspicious for paraesophageal varices in one patient. A fine granular hyperechoic pattern in the submucosa without continuity to the muscularis propria, which appeared more hyperechoic compared with the muscle layer, was suspicious for a lipoma in two patients. A central duct-like echopattern with a hypoechoic rim localized to the posterior wall of the antrum suspicious of an ectopic pancreas was found in two patients. During follow-up of these patients (range, 1 to 3 years) EUS revealed no change in size, boundaries, and echopattern of the lesions.
DISCUSSION
Smooth muscle tumors of the upper gastrointestinal tract are rare. Historically, such diseases were often described by surgeons because the diagnosis was difficult to establish prior to surgery. Endoscopy and barium swallow can often detect a bulge, which is in all probability only the tip of the iceberg. EUS improves the detection and staging of smooth muscle tumors in the upper gastrointestinal tract as illustrated in the tables and figures of this study. Imaging of intestinal wall architecture and identification of local extension of lesions can be quite precise. Criteria allowing identification of a leiomyoma are local thickening of the muscularis propria or the presence of a hypoechoic mass with clearly marginated boundaries beyond normal overlying mucosa and/or submucosa. Occasionally, a central ulcer or blood vessel within the extensive mass can be found, particularly when the size of the tumor is more than 4 em. This may be caused by a reduction of blood supply. Such lesions may lead to inhomogeneity of the echopattern, which may suggest the presence of malignancy. Lipoma, ectopic pancreas, and para-esophageal varices can be distinguished from leiomyoma based upon the echopattern, the site of origin, and the configuration. A cystic lesion adjacent to the papilla of Vater can readily be distinguished from a duodenal
Table 3. Results of endoscopy, barium swallow, CT scan, EUS initial, and follow-up (group 3) Diagnosis
No. of patients
Leiomyoma
4
Paraesophageal varices
1
Leiomyoma
8
Lipoma
Ectopic pancreas
2
Leiomyoma
2
VOLUME 36, NO.4, 1990
Localization Esophagus
Endoscopy
Barium swallow
Bulge with normal Filling defect mucosa
CT
EUS initial
Local thickening Sharply demarcated of the wall (N hypoechoic pat= 2) No abtern (N = 2), 10normalities (N cal thickening of = 2) the muscularis propria (N = 2) Esophagus Bulge with normal Filling defect No abnormality Serpentine anemucosa choic duct-like structure in the adventitia Stomach Bulge with normal Double contour Wall thickening Sharply demarcated mucosa hypoechoic patin 3 out of 5 patients tern (N = 6), local thickening of the muscularis propria (N = 3) Stomach Bulge with normal Filling defect No abnormality Hyperechoic patmucosa tern in the submucosa Posterior wall Bulge with a small Filling defect Not performed Hypoechoic rim of antrum central excavawith a central tion ductular like structure Duodenum Bulge with normal Filling defect No abnormality Local thickening of (1) mucosa the muscularis No abnormalpropria (N = 2) ity (1)
Follow-up No changes in size and echopattern
No changes in size and echopattern
No changes in size and echopattern
No changes in size and echopattern No changes in size and echopattern
No changes in size and echopattern
347
findings such as invasion into surrounding tissue or the presence of suspicious lymph nodes are helpful in distinguishing the malignant nature of the lesion. Carcinoma of the bronchus invading the esophageal wall and mucoid secreting adenocarcinomas with central ulceration cannot be distinguished from a leiomyosarcoma or leiomyoblastoma based solely on echopattern. EUS-guided cytological puncture (aspiration cytology) may become helpful in further ascertaining the correct diagnosis. 35,3? This appears to be important
Figure 4. A, EUS shows a hypoechoic well-delineated tumor without penetration into the surrounding tissues. B, Barium swallow shows a smooth double contour (arrows) in the descending duodenum.
tumor because of its pathognomonic anechoic pattern beyond the normal overlying mucosa. 36 In our series, carcinoid did simulate leiomyoma due to a similar echopattern, particularly by its circumscribed localization in the submucosa. Leiomyosarcoma or leiomyoblastoma are visualized as an inhomogeneous hypoechoic large mass with sharply demarcated boundaries or irregular margins, occasionally associated with a central ulcer or fistulous tract. Although tumor size and the occurrence of gross necrosis or fistulization are suggestive of malignancy, only the biological behavior of the process (frank local infiltration or remote metastasis) defines true malignancy in those submucosal tumors. Supplementary 348
Figure 6. A, EUS photograph shows a local thickening (t) of the muscularis propria (mp) extending into the submucosa (sm) covered with normal mucosa (m) bulging into the lumen (arrows) compatible with leiomyoma. B, Barium swallow photograph shows smoothly marginated double contour (arrows).
GASTROINTESTINAL ENDOSCOPY
because leiomyosarcoma or leiomyoblastoma has a more favorable prognosis than gastric adenocarcinoma. 30 The EUS pattern of non-Hodgkin lymphomas 19 ,22,25,27 may be similar to that of leiomyosarcoma, leiomyoblastoma, or mucoid secreting adenocarcinoma. EUS appears to be superior to other presently available imaging methods not only in the detection and staging of smooth muscle tumors but also superior during the follow-up of benign lesions and post-surgically resected malignant diseases. 27 The CT scan is often inadequate for the detection of an intramural lesion because the individual layer of gastrointestinal wall cannot be imaged. Thus, the site of origin of tumor may be difficult to identify.14 Most difficult for CT is distinguishing between a necrotic gastric leiomyosarcoma and an abscess, pseudocyst, or necrotic neoplasm arising in a perigastric organ or space. 13 Blood vessels within or adjacent to the mass can be difficult to distinguish from the primary lesion with a CT scan because of the static character of the procedure, except when intravenous contrast is added. Conversely, the real-time properties of EUS provide accurate differentiation between solid lesions such as tumor mass or lymph nodes and blood vessels without the use of contrast. The capability of endoscopic maneuvering of the transducer allows accurate assessment of lesions by employing cross-sectional, longitudinal, and oblique sections. Therefore, the maximal extent of gastrointestinal tumor can more accurately be assessed with EUS than CT. This is caused by the uni-cross sectional images of CT. The superiority of EUS as compared with CT in the staging of esophageal carcinoma has been reported elsewhere. 38 Postsurgical changes do not hamper EUS investigation because of the ability to visualize the transition between normal and pathological structures. By contrast' CT images are often hindered by the presence of post-surgical changes. The disadvantages of EUS over conventional imaging modalities include difficulties in operator interpretations of ultrasonic images because of inadequate positioning of the echoprobe due to luminal stenosis or because of difficulty in positioning the echoendoscope near the target lesion. In addition, because of the small field of image area secondary to limited penetration depth of high frequency ultrasound, and difficult topographic anatomical orientation, interpretation of EUS images may become complicated. The operator must have extensive experience in endoscopy particularly with side-viewing instruments as well as abdominal ultrasonography.17 We believe an optimal investigation can be performed by one operator with experience in both techniques in order to reduce the time required and to avoid higher cost related to examination by two operators. Technical improvements such as reduction of the length of the rigid tip and enlargement of the biopsy channel for EUSVOLUME 36, NO.4, 1990
guided cytological puncture or biopsy are necessary. Recently, a 20-MHz ultrasonic probe, which can be passed through the biopsy channel of an endoscope, has been reported. 39 However, the circumscribed penetration depth of this instrument limits its clinical application to the evaluation of superficial mural lesions. Recently available prototype echovideoendoscopy may become useful for teaching and demonstrating both endoscopic and ultrasonic images. There is easier passage through the pylorus due to the small echoprobe. In our experience EUS is helpful in planning the strategy of treatment. Submucosal tumors with a diameter of less than 4 cm without evidence of bleeding, obstruction, or malignancy at endoscopy and on EUS can be followed at intervals of 3 months. Extensive tumors with evidence of malignancy on EUS, with or without suspicious adjacent lymph nodes, should undergo EUS-guided aspiration puncture for cytology or biopsy. Negative results, however, do not exclude the possibility of malignancy. Therefore, follow-up EUS at intervals of 4 weeks is recommended. During the follow-up period, if there is detection of changes in echopatterns, boundaries, and size of tumors, surgery is recommended. Tumors with evidence of involvement of the surrounding tissue and lymph nodes should be treated surgically, e.g., local excision, partial or total resection of the involved organ. In this manner, we believe that this technique will become an important new diagnostic procedure available to gastroenterologists and surgeons as an aid in the clinical management of smooth muscle tumors of the upper gastrointestinal tract. ACKNOWLEDGMENTS
The authors thank all of the physicians, gastroenterologists, and surgeons of the Academic Medical Center and regional hospitals for referring the patients. REFERENCES 1. Baker HL, Good CA. Smooth muscle tumors of the alimentary tract. Their roentgen manifestations. AJR 1955;74:246-54. 2. Phillips JC, Lindsay JW, Kendall JA. Gastric leiomyosarcoma: roentgenologic and clinical findings. Am J Dig Dis 1970;15:23946. 3. Fargenburg D, Farman J, Dallemand S, et al. Leiomyoblastoma of the stomach. Report of 9 cases. Radiology 1975; 117:297-300. 4. Welch JP. Smooth muscle tumors of the stomach. Am J Surg 1975;130:279-85. 5. Nauert TC, Zornoza J, Ordonez N. Gastric leiomyosarcomas. AJR 1982;139:291-7. 6. Faivre J, Bory R, Moulinier B. Benign tumors of eosophagus: value of endoscopy. Endoscopy 1978;10:264-8. 7. Papazian A, Gineston JL, Capron JP, Quenum C. Leiomyoblastoma of the stomach: endoscopic treatment. Endoscopy 1984;16:157-9. 8. Kaneko E, Kumagai J, Honda N, et al. Evaluation of the new giant biopsy forceps in the diagnosis of mucosal and submucosal gastric lesions. Endoscopy 1983;15:322-6. 9. Gertsch Ph, Mossimann R. A rare tumor of the esophagus: the granular cell myoblastoma. Report of a case and review of the literature. Endoscopy 1980;12:245-9. 10. Balfe DM, Koehler RE, Karstaedt N, et al. Computed tomog-
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GASTROINTESTINAL ENDOSCOPY
GASTROINTESTINAL ENDOSCOPY Copyright © 1990 by the American Society for Gastrointestinal Endoscopy
Endoscopic ultrasonography for the evaluation of smooth muscle tumors in the upper gastrointestinal tract: an experience with 42 cases T. L. Tio, MD, PhD G. N. J. Tytgat, MD, PhD F. C. A. den Hartog Jager, MD Amsterdam, The Netherlands
Before surgery, 12 patients with suspected leiomyoma and 12 patients with suspected leiomyosarcoma were studied by endoscopic ultrasonography (EUS), computed tomography (CT), endoscopy, and barium swallow. The results were correlated with surgery and histology. Ten leiomyomas, one benign gastric ulcer, one carcinoid metastasis, eight leiomyosarcomas, two leiomyoblastomas, one mucus secreting adenocarcinoma, and one bronchial carcinoma were diagnosed. Eighteen additional patients suspected to have benign submucosal lesions by endoscopy and barium meal were treated non-surgically, and studied by EUS and CT. EUS was superior to other imaging techniques in the detection, staging, and follow-up of submucosal smooth muscle tumors because of clear imaging of the intramural abnormality and adjacent lymph nodes. (Gastrointest Endosc
1990;36:342-350)
Submucosal gastrointestinal tumors are usually detected by single or double-contrast barium swallow demonstrating a smoothly marginated filling defect in the barium column or a double contour. Distinction between a benign and malignant lesion may be difficult or impossible.l-5 Endoscopy can visualize a submucosal neoplasm as a bulge covered with normal mucosa or occasionally associated with a central ulcer. 6 ,7 Endoscopic biopsy is not always helpful in ascertaining the diagnosis because the lesion cannot always be reached with a standard biopsy forceps except when special techniques are used. B, 9 Computed tomography (CT) may identify a submucosal tumor as a hypodense lesion immediately adjacent to the lumen or as a thickening of the gastrointestinal wall after filling the lumen with contrast. 1O- l5 Endoscopic ultrasonography (EUS) is accurate in the detection and staging of gastrointestinal Received July 20, 1989. For revision September 26, 1989. Accepted November 27, 1989. From the Academic Medical Center, Department of Gastro-EnteroHepatology, Amsterdam, The Netherlands. Reprint requests: T. L. Tio, MD, Department of Gastro-Entero-Hepatology, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands.
342
neoplasms by directly approaching the target lesion with a high frequency real-time ultrasonic beam via the gastrointestinal lumen. 16- 26 Endoscopic ultrasonography (EUS) has been reported to be more accurate than endoscopy, barium meal, and CT in the detection and staging of smooth muscle tumors in the upper gastrointestinal tract. 27 A more extended series than our previously published data was performed to assess the accuracy and limitations of EUS in the detection, staging, and followup of smooth muscle tumors in the upper gastrointestinal tract by comparing EUS findings to those of CT, endoscopy, barium swallow, and histology of resected tissue. Moreover, application of EUS-guided aspiration cytology is described. MATERIALS AND METHODS
Between December 1983 and April 1988, EUS was performed in 42 patients in whom a smooth muscle tumor was suspected after endoscopic and radiographic examination. CT scan was performed before or after EUS examination. Interpretation of EUS images was made prospectively without knowledge of the results of other investigations. The patients were divided into three groups. The first group GASTROINTESTINAL ENDOSCOPY
(group 1) consisted of 12 patients undergoing surgery for a large lesion or a bleeding tumor thought to be benign because initial endoscopic biopsies were negative for malignancy. The second group (group 2) consisted of 12 patients who underwent surgery because of suspected malignancy. The timing of surgery was approximately 4 weeks after EUS and CT examination. The third group (group 3) consisted of 18 patients with smaller, sharply delineated lesions, thought to
Figure 1. A prototype Olympus video echoendoscope (VUM2) with a small echoprobe (e) attached to the tip of a sideviewing videoendoscope.
be benign, who did not have surgery but were followed with EUS, endoscopy, and CT when available. The results of EUS were correlated with the results of endoscopy, barium swallow, CT scan, and detailed histological examination of resected specimens and/or long-term follow-up. The interpretation of the gastrointestinal wall structure was based upon the results obtained by detailed examination of fresh autopsy materials and resected specimens. The normal gastrointestinal wall was visualized as a five-layer structure, which showed a close correlation with microanatomy.17-20,26 A diagnosis of benign tumor was made with EUS when a sharply demarcated hypoechoic (echo poor) homogeneous mural tumor, without evidence of penetration into surrounding tissue or lymph node involvement was recognized. Penetration was defined as extension of the mural hypoechoic pattern into the adjacent structures with total destruction of the normal gastrointestinal wall architecture. A diagnosis of malignancy was considered when an irregularly demarcated hypoechoic inhomogeneous mass lacking clear margins was found, or when a clearly demarcated hypoechoic and inhomogeneous tumor penetrated into adjacent structures was visualized. Associated central ulcerative defect within the hypoechoic mass or fistula, with or without evidence of lymph node involvement, may be found. 27 Analysis of accuracy of EUS interpretation was based on the histology of resected specimens, transmural biopsy at surgery or long-term follow-up.
Table 1. Results of endoscopy, barium swallow, CT, EUS, and histology of the resection specimens (group 1) Size No. of of patients tumor (cm)
Localization
Endoscopy
Barium swallow
CT
Hypodense tumor
3
3
Esophagus
Bulge with normal mucosa
Filling defect
1
3
Esophagus
Bulge with normal mucosa
Filling defect
1
4
Stomach
No abnormality
2
5
Stomach
Bulge with normal mucosa
No abnormality Filling defect
2
3
Stomach
Bulge with normal mucosa
Filling defect
2
4
Stomach
Bulge with an ulcer
Filling defect
1
3
Stomach
Bulge with an ulcer
Filling defect
VOLUME 36, NO.4, 1990
EUS
Sharply demarcated homogeneous hypoechoic lesion (N = 2) or local thickening of the muscularis propria (N = 1) Hypodense tumor Sharply delineated hypoechoic tumor in the submucosa Aortic aneurysm Sharply demarcated hypoechoic tumor Hypodense tumor Sharply demarcated hypoechoic tumor with anechoic ductular structures Thickening of Local thickening of the the wall (N = muscularis propria 1) Hypodense tumor Sharply demarcated hypoechoic mass with a central ulcer protruding into the gastric lumen No abnormality Sharply demarcated hypoechoic lesion in the submucosa adjacent to an ulcerative lesion
Histology
Leiomyoma
Carcinoid metastasis Leiomyoma Leiomyoma with blood vessels
Leiomyoma
Leiomyoma
Benign ulcer with extensive nodular margins
343
Studies were routinely performed with a prototype Olympus echoendoscope (EU-M1) or a commercially available model (EU-M2) in which a small mechanical sector echoprobe was attached to a side-viewing endoscope. The length of the rigid tip was 4.2 cm and the diameter of the echoprobe was 13 mm. 17- 26 The frequency of the transducer was 7.5 MHz with a penetration depth of approximately 10 cm and an axial resolution of 0.2 mm. Axial resolution was defined as the ability of the echoprobe to distinguish between two points within the direction of a transmitted wave. A prototype Olympus echoendoscope with a frequency of 10 MHz was also used. The penetration depth of ultrasound was 5 cm with an axial resolution of 0.15 mm. Recently, an Olympus echoendoscope with a switchable frequency of 7.5 MHz and 12 MHz and a biopsy channel for ultrasonic guided puncture or biopsy (EU-M3) became available. Currently, we use a videoechoendoscope for simultaneous recording of endoscopic and ultrasonic images (Fig. 1). The echoprobe was routinely covered with a water-filled balloon to improve ultrasonic images. This water-filled balloon method was particularly useful for the investigation of the esophagus, cardia, and the pyloric region. Filling the gastric lumen with water facilitated clear visualization of the gastric wall. Lesions which could not be adequately coated with water were investigated using both methods. 21 • 22 Duration of EUS examination was approximately 15 to 20 min. No complications occurred during EUS examination in this study. RESULTS
Table 1 summarizes the results of endoscopy, barium swallow, CT, EUS, and histology of resected specimens (group 1). Endoscopy and barium swallow identified a bulging lesion with normal mucosa or a smooth filling defect suspicious for a benign smooth muscle tumor in 11 of 12 patients. CT revealed a clearly delineated hypodense tumor adjacent to the contrast-filled lumen in 10 of 12 patients. EUS imaged a well-circumscribed homogeneously hypoechoic tumor (diameter, 3 to 5 em) protruding into the esophagogastric lumen (Fig. 2) or extending into the perigastric tissue in 9 of 12 patients. In the remaining three patients, local thickening of the muscularis propria was recognized. In addition, anechoic duct-like patterns, presumably vascular structures, were found in 2 of 12 patients. The histology of resected specimens confirmed the diagnosis of leiomyoma in 10 patients. A carcinoid tumor of the bronchus penetrating into the esophageal wall was found in one patient and a benign gastric ulcer with extensive nodular margins in one patient. The accuracy rate of EUS was 83%. The sensitivity was 90%. Table 2 summarizes the results of endoscopy, barium swallow, EUS, and CT in the evaluation of maligFigure 2. A, EUS photograph shows a polypoid well-deline-
ated tumor mass (t) without penetration into the surrounding tissues, adjacent to the aorta (ao). b, water-filled balloon covering the echoprobe. B, CT scan shows a hypodense, 344
clearly delineated tumor mass (t) adjacent to the esophageal lumen (I). ao, aorta. C, Barium swallow photograph shows five smoothly marginated filling defects with sharply demarcated margins. GASTROINTESTINAL ENDOSCOPY
Table 2. Results of endoscopy, barium swallow, CT, EUS, and histology of the specimens (group 2) No. of patients
Size of tumor (cm)
Localization
Endoscopy
Barium swallow
CT
EUS
Histology
Bizarrely (lack of marginations) demarcated inhomogenous mass with or without hyperechoic structures (air) Hypoechoic mass adjacent to the transducer with suspicious adjacent lymph nodes Unsharply delineated mass adjacent to the liver or spleen Clearly demarcated hypoechoic mass with a central ulcerative lesion Clearly demarcated hypoechoic mass with suspicious lymph nodes Clearly demarcated hypoechoic mass with a central ulcerative lesion Clearly demarcated hypoechoic mass with a central ulcerative lesion
Leiomyosarcoma with or without a fistula
2
4 9
Esophagus
Ulcerative tumor with or without a fistula
Tumor with or without a deep fistula
Hypodense mass
1
5
Esophagus
Bulge covered with normal mucosa
Filling defect
Hypodense mass adjacent to the lumen
2
8
Stomach
Bulge covered with normal mucosa
Double contrast
3
5
Stomach
Bulge with an ulcer
Double contour mass with a central ulcer
Hypodense mass directly adjacent to the liver or spleen Not performed
2
Stomach
Bulge with a central ulcer
Double contour with a central ulcer
Hypodense mass
1
6
Stomach
Bulge with a central ulcer
Double contour with a central ulcer
Hypodense mass
1
4
Stomach
Bulge with a central ulcer
Double contour with a central ulcer
Hypodense mass
5/12
5/10
Correct diagnosis EUS/ histology
6/12
nant smooth muscle tumors (group 2). The tumors were proven to be non-resectable at surgery in three patients. In the remaining nine patients, resection was performed. In the non-resectable cases endoscopy and barium swallow recognized an extensive tumor in the esophagus and stomach in three patients suspicious for malignancy because of rigidity, displacement, and tortuosity of the involved organ. CT scan revealed a hypodense mass adjacent to the esophageal or gastric lumen without further clarification. EUS visualized a deeply penetrating hypoechoic, inhomogeneous tumor adjacent to the bronchus in one patient, infiltrating into the liver in a second patient and into the spleen in another. Adjacent lymph nodes were strongly suspicious of malignancy. The histology of the transmural biopsy of the tumor at the time of surgery confirmed the diagnosis of bronchogenic carcinoma in one patient and leiomyosarcoma in two patients. Endoscopy and barium swallow recognized a muVOLUME 36, NO.4, 1990
Bronchus carcinoma
Non-resectable leiomyosarcoma
Leiomyoblastoma (N = 4) leiomyosarcoma (N
=
1) Leiomyosarcoma with adjacent lymph node metastasis Mucous-secreting adenocarcinoma with a fistula Leiomyoblastoma
10/12
cosal bulge with a periesophageal fistula (N = 1) or a central ulcerative lesion in the resectable cases. CT scan revealed a hypodense tumor adjacent to the gastric lumen. EUS visualized a clearly demarcated hypoechoic mass (diameter, 4 to 6 em) beyond the mucosa with a fistula or with an ulcerating defect or with smooth mucosa. Suspicious adjacent lymph nodes were found in two of these patients. Histology of resected specimens confirmed the size, configuration, and site of tumors obtained with EUS. Leiomyosarcoma was found in four, leiomyoblastoma in two 27- 33 (Fig. 3), mucoid secreting adenocarcinoma in one, and metastatic lymph nodes in two. During the follow-up period after surgical resection (from 9 to 36 months) in five patients, only EUS detected mural and nodal abnormalities. In the patient with a previous fistula in the distal esophagus, EUS demonstrated a submucosal deeply penetrating hypoechoic mass adjacent to the hilum of the liver with suspicious 345
B
Figure 5. A, EUS photograph shows a sharply delineated Figure 3. A, EUS photograph shows the transverse section
of an extensive tumor (t) with central ulcer (u). lu, lumen; b, balloon. B, Corresponding histology of the resection specimen reveals a leiomyoblastoma (t) with ulceration (u). C, Endoscopy reveals a tumor mass with a central ulcer carrying necrotic materials.
hypoechoic lesion (t) directly adjacent to the balloon (b) compatible with leiomyoma. B, Corresponding CT scan photograph shows a hypodense polypoid lesion (t) protruding into the esophageal lumen (Iu) ao, aorta. C, Corresponding endoscopic photograph shows bulging of the wall covered with normal mucosa.
regional lymph nodes. Cytology of the percutaneous ultrasonic guided puncture compared with the previous histology of the resected specimen ascertained the diagnosis of recurrent leiomyosarcoma. 34 ,35 In the
patient with adenocarcinoma EUS-guided aspiration cytology with a gastric aspiration biopsy needle was obtained. Malignant cells compatible with adenocarcinoma were found. 34
346
GASTROINTESTINAL ENDOSCOPY
Table 3 summarizes the results of endoscopy, barium swallow, ES, and CT (group 3). Endoscopy and barium swallow revealed a bulge covered with smooth overlying mucosa in the esophagus in 6 patients, in the stomach in 13 patients, and in the duodenum in 2 patients suspected of having a leiomyoma (Fig. 4). CT scan revealed wall thickening in the esophagus in four patients, in the stomach in three of five patients, and no abnormalities in the duodenum. Initial EUS imaged a sharply demarcated hypoechoic lesion with similar echodensity to the muscle layer in eight patients (Fig. 5) or local thickening of the muscularis propria beyond the normal overlying mucosa and submucosa (Fig. 6) suggestive of leiomyoma in seven patients. In the remaining three patients, EUS visualized a serpiginous duct-like anechoic structure adjacent to the esophageal wall suspicious for paraesophageal varices in one patient. A fine granular hyperechoic pattern in the submucosa without continuity to the muscularis propria, which appeared more hyperechoic compared with the muscle layer, was suspicious for a lipoma in two patients. A central duct-like echopattern with a hypoechoic rim localized to the posterior wall of the antrum suspicious of an ectopic pancreas was found in two patients. During follow-up of these patients (range, 1 to 3 years) EUS revealed no change in size, boundaries, and echopattern of the lesions.
DISCUSSION
Smooth muscle tumors of the upper gastrointestinal tract are rare. Historically, such diseases were often described by surgeons because the diagnosis was difficult to establish prior to surgery. Endoscopy and barium swallow can often detect a bulge, which is in all probability only the tip of the iceberg. EUS improves the detection and staging of smooth muscle tumors in the upper gastrointestinal tract as illustrated in the tables and figures of this study. Imaging of intestinal wall architecture and identification of local extension of lesions can be quite precise. Criteria allowing identification of a leiomyoma are local thickening of the muscularis propria or the presence of a hypoechoic mass with clearly marginated boundaries beyond normal overlying mucosa and/or submucosa. Occasionally, a central ulcer or blood vessel within the extensive mass can be found, particularly when the size of the tumor is more than 4 em. This may be caused by a reduction of blood supply. Such lesions may lead to inhomogeneity of the echopattern, which may suggest the presence of malignancy. Lipoma, ectopic pancreas, and para-esophageal varices can be distinguished from leiomyoma based upon the echopattern, the site of origin, and the configuration. A cystic lesion adjacent to the papilla of Vater can readily be distinguished from a duodenal
Table 3. Results of endoscopy, barium swallow, CT scan, EUS initial, and follow-up (group 3) Diagnosis
No. of patients
Leiomyoma
4
Paraesophageal varices
1
Leiomyoma
8
Lipoma
Ectopic pancreas
2
Leiomyoma
2
VOLUME 36, NO.4, 1990
Localization Esophagus
Endoscopy
Barium swallow
Bulge with normal Filling defect mucosa
CT
EUS initial
Local thickening Sharply demarcated of the wall (N hypoechoic pat= 2) No abtern (N = 2), 10normalities (N cal thickening of = 2) the muscularis propria (N = 2) Esophagus Bulge with normal Filling defect No abnormality Serpentine anemucosa choic duct-like structure in the adventitia Stomach Bulge with normal Double contour Wall thickening Sharply demarcated mucosa hypoechoic patin 3 out of 5 patients tern (N = 6), local thickening of the muscularis propria (N = 3) Stomach Bulge with normal Filling defect No abnormality Hyperechoic patmucosa tern in the submucosa Posterior wall Bulge with a small Filling defect Not performed Hypoechoic rim of antrum central excavawith a central tion ductular like structure Duodenum Bulge with normal Filling defect No abnormality Local thickening of (1) mucosa the muscularis No abnormalpropria (N = 2) ity (1)
Follow-up No changes in size and echopattern
No changes in size and echopattern
No changes in size and echopattern
No changes in size and echopattern No changes in size and echopattern
No changes in size and echopattern
347
findings such as invasion into surrounding tissue or the presence of suspicious lymph nodes are helpful in distinguishing the malignant nature of the lesion. Carcinoma of the bronchus invading the esophageal wall and mucoid secreting adenocarcinomas with central ulceration cannot be distinguished from a leiomyosarcoma or leiomyoblastoma based solely on echopattern. EUS-guided cytological puncture (aspiration cytology) may become helpful in further ascertaining the correct diagnosis. 35,3? This appears to be important
Figure 4. A, EUS shows a hypoechoic well-delineated tumor without penetration into the surrounding tissues. B, Barium swallow shows a smooth double contour (arrows) in the descending duodenum.
tumor because of its pathognomonic anechoic pattern beyond the normal overlying mucosa. 36 In our series, carcinoid did simulate leiomyoma due to a similar echopattern, particularly by its circumscribed localization in the submucosa. Leiomyosarcoma or leiomyoblastoma are visualized as an inhomogeneous hypoechoic large mass with sharply demarcated boundaries or irregular margins, occasionally associated with a central ulcer or fistulous tract. Although tumor size and the occurrence of gross necrosis or fistulization are suggestive of malignancy, only the biological behavior of the process (frank local infiltration or remote metastasis) defines true malignancy in those submucosal tumors. Supplementary 348
Figure 6. A, EUS photograph shows a local thickening (t) of the muscularis propria (mp) extending into the submucosa (sm) covered with normal mucosa (m) bulging into the lumen (arrows) compatible with leiomyoma. B, Barium swallow photograph shows smoothly marginated double contour (arrows).
GASTROINTESTINAL ENDOSCOPY
because leiomyosarcoma or leiomyoblastoma has a more favorable prognosis than gastric adenocarcinoma. 30 The EUS pattern of non-Hodgkin lymphomas 19 ,22,25,27 may be similar to that of leiomyosarcoma, leiomyoblastoma, or mucoid secreting adenocarcinoma. EUS appears to be superior to other presently available imaging methods not only in the detection and staging of smooth muscle tumors but also superior during the follow-up of benign lesions and post-surgically resected malignant diseases. 27 The CT scan is often inadequate for the detection of an intramural lesion because the individual layer of gastrointestinal wall cannot be imaged. Thus, the site of origin of tumor may be difficult to identify.14 Most difficult for CT is distinguishing between a necrotic gastric leiomyosarcoma and an abscess, pseudocyst, or necrotic neoplasm arising in a perigastric organ or space. 13 Blood vessels within or adjacent to the mass can be difficult to distinguish from the primary lesion with a CT scan because of the static character of the procedure, except when intravenous contrast is added. Conversely, the real-time properties of EUS provide accurate differentiation between solid lesions such as tumor mass or lymph nodes and blood vessels without the use of contrast. The capability of endoscopic maneuvering of the transducer allows accurate assessment of lesions by employing cross-sectional, longitudinal, and oblique sections. Therefore, the maximal extent of gastrointestinal tumor can more accurately be assessed with EUS than CT. This is caused by the uni-cross sectional images of CT. The superiority of EUS as compared with CT in the staging of esophageal carcinoma has been reported elsewhere. 38 Postsurgical changes do not hamper EUS investigation because of the ability to visualize the transition between normal and pathological structures. By contrast' CT images are often hindered by the presence of post-surgical changes. The disadvantages of EUS over conventional imaging modalities include difficulties in operator interpretations of ultrasonic images because of inadequate positioning of the echoprobe due to luminal stenosis or because of difficulty in positioning the echoendoscope near the target lesion. In addition, because of the small field of image area secondary to limited penetration depth of high frequency ultrasound, and difficult topographic anatomical orientation, interpretation of EUS images may become complicated. The operator must have extensive experience in endoscopy particularly with side-viewing instruments as well as abdominal ultrasonography.17 We believe an optimal investigation can be performed by one operator with experience in both techniques in order to reduce the time required and to avoid higher cost related to examination by two operators. Technical improvements such as reduction of the length of the rigid tip and enlargement of the biopsy channel for EUSVOLUME 36, NO.4, 1990
guided cytological puncture or biopsy are necessary. Recently, a 20-MHz ultrasonic probe, which can be passed through the biopsy channel of an endoscope, has been reported. 39 However, the circumscribed penetration depth of this instrument limits its clinical application to the evaluation of superficial mural lesions. Recently available prototype echovideoendoscopy may become useful for teaching and demonstrating both endoscopic and ultrasonic images. There is easier passage through the pylorus due to the small echoprobe. In our experience EUS is helpful in planning the strategy of treatment. Submucosal tumors with a diameter of less than 4 cm without evidence of bleeding, obstruction, or malignancy at endoscopy and on EUS can be followed at intervals of 3 months. Extensive tumors with evidence of malignancy on EUS, with or without suspicious adjacent lymph nodes, should undergo EUS-guided aspiration puncture for cytology or biopsy. Negative results, however, do not exclude the possibility of malignancy. Therefore, follow-up EUS at intervals of 4 weeks is recommended. During the follow-up period, if there is detection of changes in echopatterns, boundaries, and size of tumors, surgery is recommended. Tumors with evidence of involvement of the surrounding tissue and lymph nodes should be treated surgically, e.g., local excision, partial or total resection of the involved organ. In this manner, we believe that this technique will become an important new diagnostic procedure available to gastroenterologists and surgeons as an aid in the clinical management of smooth muscle tumors of the upper gastrointestinal tract. ACKNOWLEDGMENTS
The authors thank all of the physicians, gastroenterologists, and surgeons of the Academic Medical Center and regional hospitals for referring the patients. REFERENCES 1. Baker HL, Good CA. Smooth muscle tumors of the alimentary tract. Their roentgen manifestations. AJR 1955;74:246-54. 2. Phillips JC, Lindsay JW, Kendall JA. Gastric leiomyosarcoma: roentgenologic and clinical findings. Am J Dig Dis 1970;15:23946. 3. Fargenburg D, Farman J, Dallemand S, et al. Leiomyoblastoma of the stomach. Report of 9 cases. Radiology 1975; 117:297-300. 4. Welch JP. Smooth muscle tumors of the stomach. Am J Surg 1975;130:279-85. 5. Nauert TC, Zornoza J, Ordonez N. Gastric leiomyosarcomas. AJR 1982;139:291-7. 6. Faivre J, Bory R, Moulinier B. Benign tumors of eosophagus: value of endoscopy. Endoscopy 1978;10:264-8. 7. Papazian A, Gineston JL, Capron JP, Quenum C. Leiomyoblastoma of the stomach: endoscopic treatment. Endoscopy 1984;16:157-9. 8. Kaneko E, Kumagai J, Honda N, et al. Evaluation of the new giant biopsy forceps in the diagnosis of mucosal and submucosal gastric lesions. Endoscopy 1983;15:322-6. 9. Gertsch Ph, Mossimann R. A rare tumor of the esophagus: the granular cell myoblastoma. Report of a case and review of the literature. Endoscopy 1980;12:245-9. 10. Balfe DM, Koehler RE, Karstaedt N, et al. Computed tomog-
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