Endoscopy 2005; 37(7): 635-645
DOI: 10.1055/s-2005-861422
Update on Upper GI Submucosal Tumors
© Georg Thieme Verlag KG Stuttgart · New York

Endoscopic Ultrasound and Endoscopic Ultrasound-Guided Fine-Needle Biopsy for the Diagnosis of Malignant Submucosal Tumors

M.  Polkowski1
  • 1Department of Gastroenterology, Medical Center for Postgraduate Education, Institute of Oncology, Warsaw, Poland
Further Information

Publication History

Publication Date:
11 July 2005 (online)

Introduction

Epidemiological data are scant and imprecise, but approximately one in every 300 routine endoscopies reveals a bulging of the gastrointestinal wall covered by smooth mucosa of normal appearance [1] (Figure [1]). Such a finding, though usually incidental, raises questions of clinical significance: Does the bulging represent a pathology that is real or only a figment of the endoscopist’s imagination? Does it result from pressure on the wall from the outside, and if so, what is the compressing structure? Or is there a tumor deep in the wall, under the smooth surface of the overlying mucosa, a so-called submucosal tumor (SMT)? Finally, and most importantly, what is the risk that the lesion in question is malignant and requires treatment?

Figure 1 a Endoscopic appearance of a small gastric submucosal tumor (SMT) and extraluminal compression (EC) caused by an adjacent bowel loop or the gallbladder. b There was little doubt in this case that the larger bulge was caused by an extraluminal structure because after a while it started moving and finally disappeared; however, endoscopic differentiation between SMTs and extraluminal compression is usually not that easy. False-positive diagnosis of a tumor in a patient with extraluminal compression is the most common error.

Endoscopic ultrasound (EUS) has been used for more than two decades to answer these questions in everyday clinical practice; over the same period many studies have provided numerous data on the capabilities and limitations of this method. This review focuses on the endosonographic diagnosis of malignant SMTs and the role that EUS-guided needle biopsy plays in this setting.

References

  • 1 Hedenbro J L, Ekelund M, Wetterberg P. Endoscopic diagnosis of submucosal gastric lesions. The results after routine endoscopy.  Surg Endosc. 1991;  5 20-23
  • 2 Hwang J H, Kimmey M B. The incidental upper gastrointestinal subepithelial mass.  Gastroenterology. 2004;  126 301-307
  • 3 Nesje L B, Laerum O D, Svanes K. et al . Subepithelial masses of the gastrointestinal tract evaluated by endoscopic ultrasonography.  Eur J Ultrasound. 2002;  15 45-54
  • 4 Rosch T, Lorenz R, Dancygier H. et al . Endosonographic diagnosis of submucosal upper gastrointestinal tract tumors.  Scand J Gastroenterol. 1992;  27 1-8
  • 5 Kawamoto K, Yamada Y, Utsunomiya T. et al . Gastrointestinal submucosal tumors: evaluation with endoscopic US.  Radiology. 1997;  205 733-740
  • 6 Chak A, Canto M, Stevens P D. et al . Clinical applications of a new through-the-scope ultrasound probe: prospective comparison with an ultrasound endoscope.  Gastrointest Endosc. 1997;  45 291-295
  • 7 Buscarini E, Stasi M D, Rossi S. et al . Endosonographic diagnosis of submucosal upper gastrointestinal tract lesions and large fold gastropathies by catheter ultrasound probe.  Gastrointest Endosc. 1999;  49 184-191
  • 8 Kojima T, Takahashi H, Parra-Blanco A. et al . Diagnosis of submucosal tumor of the upper GI tract by endoscopic resection.  Gastrointest Endosc. 1999;  50 516-522
  • 9 Waxman I, Saitoh Y, Raju G S. et al . High-frequency probe EUS-assisted endoscopic mucosal resection: a therapeutic strategy for submucosal tumors of the GI tract.  Gastrointest Endosc. 2002;  55 44-49
  • 10 Kajiyama T, Hajiro K, Sakai M. et al . Endoscopic resection of gastrointestinal submucosal lesions: a comparison between strip biopsy and aspiration lumpectomy.  Gastrointest Endosc. 1996;  44 404-410
  • 11 Boyce G A, Sivak M V, Rosch T. et al . Evaluation of submucosal upper gastrointestinal tract lesions by endoscopic ultrasound.  Gastrointest Endosc. 1991;  37 449-454
  • 12 Palazzo L, Landi B, Cellier C. et al . Endosonographic features predictive of benign and malignant gastrointestinal stromal cell tumours.  Gut. 2000;  46 88-92
  • 13 Nesje L B, Odegaard S, Kimmey M B. Transendoscopic ultrasonography during conventional upper gastrointestinal endoscopy. Clinical evaluation of a linear 20-MHz probe system.  Scand J Gastroenterol. 1997;  32 500-508
  • 14 Sun S, Wang M, Sun S. Use of endoscopic ultrasound-guided injection in endoscopic resection of solid submucosal tumors.  Endoscopy. 2002;  34 82-85
  • 15 Koch J, Halvorsen R A, Levenson S D. et al . Prospective comparison of catheter-based endoscopic sonography versus standard endoscopic sonography: evaluation of gastrointestinal-wall abnormalities and staging of gastrointestinal malignancies.  J Clin Ultrasound. 2001;  29 117-124
  • 16 Yasuda K, Nakajima M, Yoshida S. et al . The diagnosis of submucosal tumors of the stomach by endoscopic ultrasonography.  Gastrointest Endosc. 1989;  35 10-15
  • 17 Caletti G, Zani L, Bolondi L. et al . Endoscopic ultrasonography in the diagnosis of gastric submucosal tumor.  Gastrointest Endosc. 1989;  35 413-418
  • 18 Hyun J H, Jeen Y T, Chun H J. et al . Endoscopic resection of submucosal tumor of the esophagus: results in 62 patients.  Endoscopy. 1997;  29 165-170
  • 19 Hashimoto H, Mitsunaga A, Suzuki S. et al . Evaluation of endoscopic ultrasonography for gastric tumors and presentation of three-dimensional display of endoscopic ultrasonography.  Surg Endosc. 1989;  3 173-181
  • 20 Tsai T L, Changchien C S, Hu T H. et al . Demonstration of gastric submucosal lesions by high-resolution transabdominal sonography.  J Clin Ultrasound. 2000;  28 125-132
  • 21 Fletcher C D, Berman J J, Corless C. et al . Diagnosis of gastrointestinal stromal tumors: A consensus approach.  Hum Pathol. 2002;  33 459-465
  • 22 Miettinen M, Majidi M, Lasota J. Pathology and diagnostic criteria of gastrointestinal stromal tumors (GISTs): a review.  Eur J Cancer. 2002;  38 S39-S51
  • 23 Miettinen M, El Rifai W, Sobin H L. et al . Evaluation of malignancy and prognosis of gastrointestinal stromal tumors: a review.  Hum Pathol. 2002;  33 478-483
  • 24 Miettinen M, Lasota J. Gastrointestinal stromal tumors - definition, clinical, histological, immunohistochemical, and molecular genetic features and differential diagnosis.  Virchows Arch. 2001;  438 1-12
  • 25 Joensuu H, Fletcher C, Dimitrijevic S. et al . Management of malignant gastrointestinal stromal tumours.  Lancet Oncol. 2002;  3 665-664
  • 26 DeMatteo R P, Lewis J J, Leung D. et al . Two hundred gastrointestinal stromal tumors: recurrence patterns and prognostic factors for survival.  Ann Surg. 2000;  231 51-58
  • 27 Rudolph P, Chiaravalli A M, Pauser U. et al . Gastrointestinal mesenchymal tumors - immunophenotypic classification and survival analysis.  Virchows Arch. 2002;  441 238-248
  • 28 Hasegawa T, Matsuno Y, Shimoda T. et al . Gastrointestinal stromal tumor: consistent CD117 immunostaining for diagnosis, and prognostic classification based on tumor size and MIB-1 grade.  Hum Pathol. 2002;  33 669-676
  • 29 Demetri G D, von Mehren M, Blanke C D. et al . Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors.  N Engl J Med. 2002;  347 472-480
  • 30 Gu M, Ghafari S, Nguyen P T. et al . Cytologic diagnosis of gastrointestinal stromal tumors of the stomach by endoscopic ultrasound-guided fine-needle aspiration biopsy: cytomorphologic and immunohistochemical study of 12 cases.  Diagn Cytopathol. 2001;  25 343-350
  • 31 Rader A E, Avery A, Wait C L. et al . Fine-needle aspiration biopsy diagnosis of gastrointestinal stromal tumors using morphology, immunocytochemistry, and mutational analysis of c-kit.  Cancer. 2001;  93 269-275
  • 32 Fu K, Eloubeidi M A, Jhala N C. et al . Diagnosis of gastrointestinal stromal tumor by endoscopic ultrasound-guided fine needle aspiration biopsy - a potential pitfall.  Ann Diagn Pathol. 2002;  6 294-301
  • 33 Hunt G C, Rader A E, Faigel D O. A comparison of EUS features between CD-117 positive GI stromal tumors and CD-117 negative GI spindle cell tumors.  Gastrointest Endosc. 2003;  57 469-474
  • 34 Ando N, Goto H, Niwa Y. et al . The diagnosis of GI stromal tumors with EUS-guided fine needle aspiration with immunohistochemical analysis.  Gastrointest Endosc. 2002;  55 37-43
  • 35 Okai T, Minamoto T, Ohtsubo K. et al . Endosonographic evaluation of c-kit-positive gastrointestinal stromal tumor.  Abdom Imaging. 2003;  28 301-307
  • 36 Vander Noot M R, Eloubeidi M A, Chen V K. et al . Diagnosis of gastrointestinal tract lesions by endoscopic ultrasound-guided fine-needle aspiration biopsy.  Cancer. 2004;  102 157-163
  • 37 Kinoshita K, Isozaki K, Tsutsui S. et al . Endoscopic ultrasonography-guided fine needle aspiration biopsy in follow-up patients with gastrointestinal stromal tumours.  Eur J Gastroeneterol Hepatol. 2003;  15 1189-1193
  • 38 Caletti G C, Brocchi E, Ferrari A. et al . Guillotine needle biopsy as a supplement to endosonography in the diagnosis of gastric submucosal tumors.  Endoscopy. 1991;  23 251-254
  • 39 Chak A, Canto M I, Rosch T. et al . Endosonographic differentiation of benign and malignant stromal cell tumors.  Gastrointest Endosc. 1997;  45 468-473
  • 40 Wallace M B, Hoffman B J, Sahai A S. et al . Imaging of esophageal tumors with a water-filled condom and a catheter US probe.  Gastrointest Endosc. 2000;  51 597-600
  • 41 Rosch T, Kapfer B, Will U. et al . Accuracy of endoscopic ultrasonography in upper gastrointestinal submucosal lesions: a prospective multicenter study.  Scand J Gastroenterol. 2002;  37 856-862
  • 42 Nickl N, Gress F, McClave S. et al . Hypoechoic intramural tumor study: final report [abstract].  Gastrointest Endosc. 2002;  55 AB98
  • 43 Nakazawa S, Yoshino J, Nakamura T. et al . Endoscopic ultrasonography of gastric myogenic tumor. A comparative study between histology and ultrasonography.  J Ultrasound Med. 1989;  8 353-359
  • 44 Tio T L, Tytgat G N, Hartog Jager F C. Endoscopic ultrasonography for the evaluation of smooth muscle tumors in the upper gastrointestinal tract: an experience with 42 cases.  Gastrointest Endosc. 1990;  36 342-350
  • 45 Giovannini M, Seitz J F, Monges G. et al . Fine-needle aspiration cytology guided by endoscopic ultrasonography: results in 141 patients.  Endoscopy. 1995;  27 171-177
  • 46 Levy M J, Jondal M L, Clain J. et al . Preliminary experience with an EUS-guided trucut biopsy needle compared with EUS-guided FNA.  Gastrointest Endosc. 2003;  57 101-106
  • 47 Brand B, Oesterhelweg L, Binmoeller K F. et al . Impact of endoscopic ultrasound for evaluation of submucosal lesions in gastrointestinal tract.  Dig Liver Dis. 2002;  34 290-297
  • 48 Hizawa K, Iwai K, Esaki M. et al . Endosonographic features of Brunner’s gland hamartomas which were subsequently resected endoscopically.  Endoscopy. 2002;  34 956-958
  • 49 Yoshikane H, Tsukamoto Y, Niwa Y. et al . Carcinoid tumors of the gastrointestinal tract: evaluation with endoscopic ultrasonography.  Gastrointest Endosc. 1993;  39 375-383
  • 50 Hizawa K, Matsumoto T, Kouzuki T. et al . Cystic submucosal tumors in the gastrointestinal tract: endosonographic findings and endoscopic removal.  Endoscopy. 2000;  32 712-714
  • 51 Geller A, Wang K K, DiMagno E P. Diagnosis of foregut duplication cysts by endoscopic ultrasonography.  Gastroenterology. 1995;  109 838-842
  • 52 Palazzo L, Landi B, Cellier C. et al . Endosonographic features of esophageal granular cell tumors.  Endoscopy. 1997;  29 850-853
  • 53 Matsushita M, Hajiro K, Okazaki K. et al . Gastric aberrant pancreas: EUS analysis in comparison with the histology.  Gastrointest Endosc. 1999;  49 493-497
  • 54 Changchien C S, Hsiaw C M, Hu T H. Endoscopic ultrasonographic classification of gastric aberrant pancreas.  Changgeng Yi Xue Za Zhi. 2000;  23 600-607
  • 55 Matsushita M, Hajiro K, Okazaki K. et al . Gastric inflammatory fibroid polyps: endoscopic ultrasonographic analysis in comparison with the histology.  Gastrointest Endosc. 1997;  46 53-57
  • 56 Hizawa K, Aoyagi K, Kurahara K. et al . Gastrointestinal lymphangioma: endosonographic demonstration and endoscopic removal.  Gastrointest Endosc. 1996;  43 620-624
  • 57 Oka R, Okai T, Kitakata H. et al . Heterotopic pancreas with calcification: a lesion mimicking leiomyosarcoma of the stomach.  Gastrointest Endosc. 2002;  56 939-942
  • 58 Ninomiya Y, Seki M, Ohta H. et al . Increase in size of c-kit positive GI stromal tumor from 35 mm to 250 mm in 2 years: case report.  Gastrointest Endosc. 2003;  57 616-618
  • 59 Ueyama T, Kawamoto K, Iwashita I. et al . Correlation between tumor volume doubling time and histologic findings in gastric smooth muscle tumors: clinical implications of tumor volume doubling time.  J Surg Oncol. 1995;  60 12-17
  • 60 Chonan A, Mochizuki F, Fujita N. et al . Diagnosis of gastric myogenic tumor by endoscopic ultrasonography [in Japanese].  Stomach Intestine. 1995;  30 1133-1139
  • 61 Hamada S, Ohara S, Sekine H. A differential diagnosis of myogenic tumor by endoscopic ultrasonography [in Japanese].  Stomach Intestine. 1995;  30 1141-1149
  • 62 Ichimaru T, Fuchigami T, Yao T. et al . Natural history of smooth muscle tumor of the stomach: developmental differences of benign and malignant tumor analyzed by retrospective radiographic study [in Japanese].  Stomach Intestine. 1995;  30 1151-1162
  • 63 Melzer E, Fidder H. The natural course of upper gastrointestinal submucosal tumors: an endoscopic ultrasound survey.  Isr Med Assoc J. 2000;  2 430-432
  • 64 Nickl N, Behling C, McClave S. et al . Specific EUS features can identify hypoechoic masses which are not benign stromal cell tumors [abstract].  Gastrointest Endosc. 1999;  49 AB211
  • 65 Nickl N, Wackerbarth S, Gress F. et al . Management of hypoechoic intramural tumors: a decision tree analysis of EUS-directed vs. surgical management [abstract].  Gastrointest Endosc. 2000;  51 AB176
  • 66 Matsui M, Goto H, Niwa Y. et al . Preliminary results of fine needle aspiration biopsy histology in upper gastrointestinal submucosal tumors.  Endoscopy. 1998;  30 750-755
  • 67 Wiersema M J, Vilmann P, Giovannini M. et al . Endosonography-guided fine-needle aspiration biopsy: diagnostic accuracy and complication assessment.  Gastroenterology. 1997;  112 1087-1095
  • 68 Williams D B, Sahai A V, Aabakken L. et al . Endoscopic ultrasound guided fine needle aspiration biopsy: a large single centre experience.  Gut. 1999;  44 720-726
  • 69 Gress F G, Hawes R H, Savides T J. et al . Endoscopic ultrasound-guided fine-needle aspiration biopsy using linear array and radial scanning endosonography.  Gastrointest Endosc. 1997;  45 243-250
  • 70 Wiersema M J, Wiersema L M, Khusro Q. et al . Combined endosonography and fine-needle aspiration cytology in the evaluation of gastrointestinal lesions.  Gastrointest Endosc. 1994;  40 199-206
  • 71 Polkowski M, Palucki J, Butruk E. Transabdominal ultrasound for visualizing gastric submucosal tumors diagnosed by endosonography: can surveillance be simplified?.  Endoscopy. 2002;  34 979-983
  • 72 Li S Q, O'Leary T J, Buchner S B. et al . Fine needle aspiration of gastrointestinal stromal tumors.  Acta Cytol. 2001;  45 9-17
  • 73 Kwon M S, Koh J S, Lee S S. et al . Fine needle aspiration cytology (FNAC) of gastrointestinal stromal tumor: an emphasis on diagnostic role of FNAC, cell block, and immunohistochemistry.  J Korean Med Sci. 2002;  17 353-359
  • 74 Wieczorek T J, Faquin W C, Rubin B P. et al . Cytologic diagnosis of gastrointestinal stromal tumor with emphasis on the differential diagnosis with leiomyosarcoma.  Cancer. 2001;  93 276-287
  • 75 Seidal T, Edvardsson H. Diagnosis of gastrointestinal stromal tumor by fine-needle aspiration biopsy: a cytological and immunocytochemical study.  Diagn Cytopathol. 2000;  23 397-401
  • 76 Fields S, Libson E. CT-guided aspiration core needle biopsy of gastrointestinal wall lesions.  J Comput Assist Tomogr. 2000;  24 224-228
  • 77 Varadarajulu S, Fraig M, Schmulewitz N. et al . Comparison of EUS-guided 19-gauge trucut needle biopsy with EUS-guided fine-needle aspiration.  Endoscopy. 2004;  36 397-401
  • 78 Koon N, Schneider-Stock R, Sarlomo-Rikala M. et al . Molecular targets for tumour progression in gastrointestinal stromal tumours.  Gut. 2004;  53 235-240
  • 79 Antonescu C R, Viale A, Sarran L. et al . Gene expression in gastrointestinal stromal tumors is distinguished by KIT genotype and anatomic site.  Clin Cancer Res. 2004;  10 3282-3290
  • 80 West R B, Corless C L, Chen X. et al . The novel marker, DOG1, is expressed ubiquitously in gastrointestinal stromal tumors irrespective of KIT or PDGFRA mutation status.  Am J Pathol. 2004;  165 107-113
  • 81 Li S Q, O’Leary T J, Sobin L H. et al . Analysis of KIT mutation and protein expression in fine needle aspirates of gastrointestinal stromal/smooth muscle tumors.  Acta Cytol. 2000;  44 981-986

M. Polkowski, M.D.

Department of Gastroenterology, Medical Center for Postgraduate Education, Institute of Oncology

Roentgena 5 · 02-781 Warsaw · Poland

Fax: + 48-22-6447601

Email: polek@coi.waw.pl