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Meta-Analysis
. 2015 Feb 6;2015(2):CD009944.
doi: 10.1002/14651858.CD009944.pub2.

Diagnostic accuracy of endoscopic ultrasonography (EUS) for the preoperative locoregional staging of primary gastric cancer

Simone Mocellin  1 , Sandro Pasquali
Affiliations
Meta-Analysis

Diagnostic accuracy of endoscopic ultrasonography (EUS) for the preoperative locoregional staging of primary gastric cancer

Simone Mocellin et al. Cochrane Database Syst Rev. .

Abstract

Background: Endoscopic ultrasound (EUS) is proposed as an accurate diagnostic device for the locoregional staging of gastric cancer, which is crucial to developing a correct therapeutic strategy and ultimately to providing patients with the best chance of cure. However, despite a number of studies addressing this issue, there is no consensus on the role of EUS in routine clinical practice.

Objectives: To provide both a comprehensive overview and a quantitative analysis of the published data regarding the ability of EUS to preoperatively define the locoregional disease spread (i.e., primary tumor depth (T-stage) and regional lymph node status (N-stage)) in people with primary gastric carcinoma.

Search methods: We performed a systematic search to identify articles that examined the diagnostic accuracy of EUS (the index test) in the evaluation of primary gastric cancer depth of invasion (T-stage, according to the AJCC/UICC TNM staging system categories T1, T2, T3 and T4) and regional lymph node status (N-stage, disease-free (N0) versus metastatic (N+)) using histopathology as the reference standard. To this end, we searched the following databases: the Cochrane Library (the Cochrane Central Register of Controlled Trials (CENTRAL)), MEDLINE, EMBASE, NIHR Prospero Register, MEDION, Aggressive Research Intelligence Facility (ARIF), ClinicalTrials.gov, Current Controlled Trials MetaRegister, and World Health Organization International Clinical Trials Registry Platform (WHO ICTRP), from 1988 to January 2015.

Selection criteria: We included studies that met the following main inclusion criteria: 1) a minimum sample size of 10 patients with histologically-proven primary carcinoma of the stomach (target condition); 2) comparison of EUS (index test) with pathology evaluation (reference standard) in terms of primary tumor (T-stage) and regional lymph nodes (N-stage). We excluded reports with possible overlap with the selected studies.

Data collection and analysis: For each study, two review authors extracted a standard set of data, using a dedicated data extraction form. We assessed data quality using a standard procedure according to the Quality Assessment of Diagnostic Accuracy Studies (QUADAS-2) criteria. We performed diagnostic accuracy meta-analysis using the hierarchical bivariate method.

Main results: We identified 66 articles (published between 1988 and 2012) that were eligible according to the inclusion criteria. We collected the data on 7747 patients with gastric cancer who were staged with EUS. Overall the quality of the included studies was good: in particular, only five studies presented a high risk of index test interpretation bias and two studies presented a high risk of selection bias.For primary tumor (T) stage, results were stratified according to the depth of invasion of the gastric wall. The meta-analysis of 50 studies (n = 4397) showed that the summary sensitivity and specificity of EUS in discriminating T1 to T2 (superficial) versus T3 to T4 (advanced) gastric carcinomas were 0.86 (95% confidence interval (CI) 0.81 to 0.90) and 0.90 (95% CI 0.87 to 0.93) respectively. For the diagnostic capacity of EUS to distinguish T1 (early gastric cancer, EGC) versus T2 (muscle-infiltrating) tumors, the meta-analysis of 46 studies (n = 2742) showed that the summary sensitivity and specificity were 0.85 (95% CI 0.78 to 0.91) and 0.90 (95% CI 0.85 to 0.93) respectively. When we addressed the capacity of EUS to distinguish between T1a (mucosal) versus T1b (submucosal) cancers the meta-analysis of 20 studies (n = 3321) showed that the summary sensitivity and specificity were 0.87 (95% CI 0.81 to 0.92) and 0.75 (95% CI 0.62 to 0.84) respectively. Finally, for the metastatic involvement of lymph nodes (N-stage), the meta-analysis of 44 studies (n = 3573) showed that the summary sensitivity and specificity were 0.83 (95% CI 0.79 to 0.87) and 0.67 (95% CI 0.61 to 0.72), respectively.Overall, as demonstrated also by the Bayesian nomograms, which enable readers to calculate post-test probabilities for any target condition prevalence, the EUS accuracy can be considered clinically useful to guide physicians in the locoregional staging of people with gastric cancer. However, it should be noted that between-study heterogeneity was not negligible: unfortunately, we could not identify any consistent source of the observed heterogeneity. Therefore, all accuracy measures reported in the present work and summarizing the available evidence should be interpreted cautiously. Moreover, we must emphasize that the analysis of positive and negative likelihood values revealed that EUS diagnostic performance cannot be considered optimal either for disease confirmation or for exclusion, especially for the ability of EUS to distinguish T1a (mucosal) versus T1b (submucosal) cancers and positive versus negative lymph node status.

Authors' conclusions: By analyzing the data from the largest series ever considered, we found that the diagnostic accuracy of EUS might be considered clinically useful to guide physicians in the locoregional staging of people with gastric carcinoma. However, the heterogeneity of the results warrants special caution, as well as further investigation for the identification of factors influencing the outcome of this diagnostic tool. Moreover, physicians should be warned that EUS performance is lower in diagnosing superficial tumors (T1a versus T1b) and lymph node status (positive versus negative). Overall, we observed large heterogeneity and its source needs to be understood before any definitive conclusion can be drawn about the use of EUS can be proposed in routine clinical settings.

PubMed Disclaimer

Conflict of interest statement

The review authors declare no conflict of interest.

Figures

1
1
Study flow diagram.
2
2
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study
3
3
Risk of bias and applicability concerns graph: review authors' judgements about each domain presented as percentages across included studies
4
4
Summary ROC Plot of studies assessing the accuracy of EUS in discriminating T1 ‐ T2 versus T3 ‐ T4 gastric carcinomas. Each study sensitivity/specificity value is represented by an empty circle. The summary point for sensitivity/specificity is represented by a black filled circle. Dotted closed line: 95% confidence region of the summary point. Dashed closed line: 95% prediction region.
5
5
Fagan plot estimating how much the result of EUS changes the probability that a patient has a T1 ‐ T2 (rather than T3 ‐ T4) gastric cancer, considering a given pre‐test probability (here the mean pre‐test probability found in eligible studies is shown as an example).
6
6
EUS ability to discriminate between T1‐T2 and T3‐T4 gastric carcinomas. Likelihood ratio (LR) scattergram defining quadrants of informativeness based on desirable thresholds (positive LR>10, negative LR<0.1): left upper quadrant (test suitable both for diagnosis exclusion and confirmation), right upper (confirmation only), left lower (exclusion only), right lower (neither confirmation nor exclusion).
7
7
Summary ROC Plot of 46 studies investigating the EUS ability to discriminate between T1 versus T2 gastric carcinomas.
8
8
Fagan plot estimating how much the result of EUS changes the probability that a patient has a T1 (rather than T2) gastric cancer, considering a given pre‐test probability (here the mean pre‐test probability found in eligible studies is shown as an example).
9
9
EUS ability to discriminate between T1 and T2 gastric carcinomas. Likelihood ratio (LR) scattergram defining quadrants of informativeness based on desirable thresholds (positive LR>10, negative LR<0.1): left upper quadrant (test suitable both for diagnosis exclusion and confirmation), right upper (confirmation only), left lower (exclusion only), right lower (neither confirmation nor exclusion).
10
10
Summary ROC Plot of 20 studies investigating the diagnostic ability of EUS to discriminate between T1a versus T1b tumors.
11
11
Fagan plot estimating how much the result of EUS changes the probability that a patient has a T1a (rather than T1b) gastric cancer, considering a given pre‐test probability (here the mean pre‐test probability found in eligible studies is shown as an example).
12
12
EUS ability to discriminate between T1a and T1b gastric carcinomas. Likelihood ratio (LR) scattergram defining quadrants of informativeness based on desirable thresholds (positive LR>10, negative LR<0.1): left upper quadrant (test suitable both for diagnosis exclusion and confirmation), right upper (confirmation only), left lower (exclusion only), right lower (neither confirmation nor exclusion).
13
13
Summary ROC Plot of 44 studies addressing the issue of EUS ability to discriminate between lymph node negative (N0) and positive (N+) cases.
14
14
Fagan plot estimating how much the result of EUS changes the probability that a patient has a N+ (metastatic lymph nodes) (rather than a N0, disease free lymph nodes) gastric cancer, considering a given pre‐test probability (here the mean pre‐test probability found in eligible studies is shown as an example).
15
15
EUS ability to discriminate between N+ (metastatic lymph nodes) and N0 (disease free lymph nodes) gastric carcinomas. Likelihood ratio (LR) scattergram defining quadrants of informativeness based on desirable thresholds (positive LR>10, negative LR<0.1): left upper quadrant (test suitable both for diagnosis exclusion and confirmation), right upper (confirmation only), left lower (exclusion only), right lower (neither confirmation nor exclusion).
1
1. Test
T12 vs T34.
2
2. Test
T1 vs T2.
3
3. Test
T1a vs T1b.
4
4. Test
N0 vs N+.
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References

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    1. Ziegler K, Sanft C, Zimmer T, Zeitz M, Felsenberg D, Stein H, et al. Comparison of computed tomography, endosonography, and intraoperative assessment in TN staging of gastric carcinoma. Gut 1993;34(5):604‐10. [PUBMED: 8504959] - PMC - PubMed

References to studies excluded from this review

Abe 1993 {published data only}
    1. Abe S, Lightdale CJ, Brennan MF. The Japanese experience with endoscopic ultrasonography in the staging of gastric cancer. Gastrointestinal Endoscopy 1993;39(4):586‐91. [PUBMED: 8365619] - PubMed
Aibe 1986 {published data only}
    1. Aibe T, Takemoto T. [Diagnosis of the infiltrating depth of gastric cancer by endoscopic ultrasonography]. Gan No Rinsho 1986;32(10):1173‐5. [PUBMED: 3537361] - PubMed
Aibe 1992 {published data only}
    1. Aibe T, Fujimura H, Yanai H, Okita K, Takemoto T. Endosonographic diagnosis of metastatic lymph nodes in gastric carcinoma. Endoscopy 1992;24(Suppl 1):315‐9. [PUBMED: 1633772] - PubMed
Ajani 2004 {published data only}
    1. Ajani JA, Mansfield PF, Janjan N, Morris J, Pisters PW, Lynch PM, et al. Multi‐institutional trial of preoperative chemoradiotherapy in patients with potentially resectable gastric carcinoma. Journal of Clinical Oncology 2004;22(14):2774‐80. [PUBMED: 15254045] - PubMed
Akahoshi 1992 {published data only}
    1. Akahoshi K, Misawa T, Fujishima H, Chijiiwa Y, Nawata H. Regional lymph node metastasis in gastric cancer: evaluation with endoscopic US. Radiology 1992;182(2):559‐64. [PUBMED: 1732981] - PubMed
Akahoshi 1997 {published data only}
    1. Akahoshi K, Chijiiwa Y, Sasaki I, Hamada S, Iwakiri Y, Nawata H, et al. Pre‐operative TN staging of gastric cancer using a 15 MHz ultrasound miniprobe. British Journal of Radiology 1997;70(835):703‐7. [PUBMED: 9245882] - PubMed
Asaki 1989 {published data only}
    1. Asaki S, Nakayama Y, Ohara M, Hirasawa Y, Kanazawa N, Ota K. Comparison of the efficacy of endoscopic ultrasonography and submucosography in diagnosing the depth of gastric cancer invasion. Tohoku Journal of Experimental Medicine 1989;159(3):227‐35. [PUBMED: 2696138] - PubMed
Bösing 2003 {published data only}
    1. Bösing N, Schumacher B, Frieling T, Ohmann C, Jungblut R, Lübke H, et al. Endoscopic ultrasound in routine clinical practice for staging adenocarcinomas of the stomach and distal esophagus. Chirurg 2003;74(3):214‐21. [PUBMED: 12647078] - PubMed
Chen 2004 {published data only}
    1. Chen VK, Eloubeidi MA. Endoscopic ultrasound‐guided fine needle aspiration is superior to lymph node echofeatures: a prospective evaluation of mediastinal and peri‐intestinal lymphadenopathy. American Journal of Gastroenterology 2004;99(4):628‐33. [PUBMED: 15089893] - PubMed
Chen 2010 {published data only}
    1. Chen RJ, Huang PT, Li YP, Zheng ZQ, Zhao YP, Huang FG, et al. Comparison of preoperative T staging by oral contrast enhanced ultrasonography and double contrast enhanced ultrasonography in advanced gastric carcinoma. Zhonghua Zhong Liu Za Zhi 2010;32(7):551‐4. [PUBMED: 21029703] - PubMed
Davies 2006 {published data only}
    1. Davies AR, Deans DA, Penman I, Plevris JN, Fletcher J, Wall L, et al. The multidisciplinary team meeting improves staging accuracy and treatment selection for gastro‐esophageal cancer. Diseases of the Esophagus 2006;19(6):496‐503. [PUBMED: 17069595] - PubMed
Dewitt 2005 {published data only}
    1. DeWitt J, Kesler K, Brooks JA, LeBlanc J, McHenry L, McGreevy K, et al. Endoscopic ultrasound for esophageal and gastroesophageal junction cancer: Impact of increased use of primary neoadjuvant therapy on preoperative locoregional staging accuracy. Diseases of the Esophagus 2005;18(1):21‐7. [PUBMED: 15773837] - PubMed
Fiore 2006 {published data only}
    1. Fiore D, Baggio V, Ruol A, Bocus P, Casara D, Corti L, et al. Multimodal imaging of esophagus and cardia cancer before and after treatment. Radiologia Medica 2006;111(6):804‐17. [PUBMED: 16896560] - PubMed
Futawatari 2008 {published data only}
    1. Futawatari N, Kikuchi S, Sakuramoto S, Kida M, Watanabe M. A new diagnostic method for early gastric cancer: volume measurement by 3‐dimensional endoscopic ultrasonography in early gastric cancer and its clinical significance. Anticancer Research 2008;28(5B):2907‐12. [PUBMED: 19031933] - PubMed
Ghiţă 2011 {published data only}
    1. Ghiţă D, Glavici A, Pleşea IE, Săftoiu A, Dumitrescu D, Ciurea T. Invasion assessment in gastric carcinoma ‐ imagistic and histopathologic combined study. Romanian Journal of Morphology and Embryology 2011;52(Suppl 1):349‐61. [PUBMED: 21424074] - PubMed
Giovannini 1993 {published data only}
    1. Giovannini M, Seitz JF, Thomas P, Houvenaeghel G, Delpero JR, Giudicelli R, et al. Electronic sectorial ultrasound endoscopy in benign and malignant tumoral pathology of the stomach. Results in 30 patients [Echoendoscopie sectorielle electronique en pathologie tumorale benigne et maligne de l'estomac. Resultats chez 30 patients]. Gastroenterologie Clinique et Biologique 1993;17(1):26‐32. [PUBMED: 8467967] - PubMed
Gorshkov 2001 {published data only}
    1. Gorshkov AN, Meshkov VM, Gracheva NI, Zaritskaia VA. Possibilities of radiologic methods (ultrasonography, computed tomography) in the preoperative evaluation of intramural invasion of gastric cancer [Vozmozhnosti luchevykh metodov issledovaniia (UZI, KT) v predoperatsionnoi otsenke vnutristenochnoi invazii raka zheludka]. Vestnik Rentgenologii i Radiologii 2001;2(Mar‐Apr):27‐34. [PUBMED: 11503175] - PubMed
Greenberg 1994 {published data only}
    1. Greenberg J, Durkin M, Drunen M, Aranha GV. Computed tomography or endoscopic ultrasonography in preoperative staging of gastric and esophageal tumors. Surgery 1994;116(4):696‐701. [PUBMED: 7940168] - PubMed
Grimm 1992 {published data only}
    1. Grimm H, Hamper K, Binmoeller KF, Soehendra N. Enlarged lymph nodes: malignant or not?. Endoscopy 1992;24(Suppl 1):320‐3. [PUBMED: 1633773] - PubMed
Grotenhuis 2013 {published data only}
    1. Grotenhuis BA, Wijnhoven BP, Poley JW, Hermans JJ, Biermann K, Spaander MC, et al. Preoperative assessment of tumor location and station‐specific lymph node status in patients with adenocarcinoma of the gastroesophageal junction. World Journal of Surgery 2013;37(1):147‐55. [PUBMED: 23015224] - PubMed
Heeren 2004 {published data only}
    1. Heeren PA, Westreenen HL, Geersing GJ, Dullemen HM, Plukker JT. Influence of tumor characteristics on the accuracy of endoscopic ultrasonography in staging cancer of the esophagus and esophagogastric junction. Endoscopy 2004;36(11):966‐71. [PUBMED: 15520913] - PubMed
Heintz 1991a {published data only}
    1. Heintz A, Junginger T. Endosonographic staging of cancers of the esophagus and stomach. Comparison with surgical and histopathologic staging [Endosonographisches staging von karzinomen in spreiserohre und magen. Vergleich mit der chirurgischen und histopathologischen stadieneinteilung]. Bildgebung 1991;58(1):4‐8. [PUBMED: 2070101] - PubMed
Heintz 1991b {published data only}
    1. Heintz A, Junginger T. Endosonography in preoperative staging of gastrointestinal tumors [Die endosonographie zur praoperativen stadienbeurteilung gastrointestinaler tumoren]. Langenbecks Archiv fur Chirurgie 1991;376(1):3‐8. [PUBMED: 2034002] - PubMed
Heyer 1998 {published data only}
    1. Heyer T, Frieling T, Häussinger D. How accurate is preoperative staging as a basis for treatment decisions in gastric carcinoma? [Wie sicher ist das praoperative staging als grundlage der therapieentscheidung beim magenkarzinom?]. Praxis (Bern 1994) 1998;87(13):443‐6. [PUBMED: 9584569] - PubMed
Hirata 1989 {published data only}
    1. Hirata K, Fukuda M. Progress in image diagnosis: endoscopic ultrasonography. Hokkaido Igaku Zasshi 1989;64(5):537‐41. [PUBMED: 2687144] - PubMed
Holden 1996 {published data only}
    1. Holden A, Mendelson R, Edmunds S. Pre‐operative staging of gastro‐oesophageal junction carcinoma: comparison of endoscopic ultrasound and computed tomography. Australasian Radiology 1996;40(3):206‐12. [PUBMED: 8826718] - PubMed
Hünerbein 1995 {published data only}
    1. Hünerbein M, Rau B, Schlag PM. Laparoscopy and laparoscopic ultrasound for staging of upper gastrointestinal tumours. European Journal of Surgical Oncology 1995;21(1):50‐5. [PUBMED: 7851554] - PubMed
Hünerbein 1996 {published data only}
    1. Hünerbein M, Dohmoto M, Rau B, Schlag PM. Endosonography and endosonography‐guided biopsy of upper‐GI‐tract tumors using a curved‐array echoendoscope. Surgical Endoscopy 1996;10(12):1205‐9. [PUBMED: 8939844] - PubMed
Kang 2010 {published data only}
    1. Kang HY, Kim SG, Kim JS, Jung HC, Song IS. Clinical outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Surgical Endoscopy 2010;24(3):509‐16. [PUBMED: 19585066] - PubMed
Kida 1998 {published data only}
    1. Kida M, Tanabe S, Watanabe M, Kokutou M, Kondou I, Yamada Y, et al. Staging of gastric cancer with endoscopic ultrasonography and endoscopic mucosal resection. Endoscopy 1998;30(Suppl 1):A64‐8. [PUBMED: 9765088] - PubMed
Kienle 2002 {published data only}
    1. Kienle P, Buhl K, Kuntz C, Düx M, Hartmann C, Axel B, et al. Prospective comparison of endoscopy, endosonography and computed tomography for staging of tumours of the oesophagus and gastric cardia. Digestion 2002;66(4):230‐6. [PUBMED: 12592099] - PubMed
Kroep 2003 {published data only}
    1. Kroep JR, Groeningen CJ, Cuesta MA, Craanen ME, Hoekstra OS, Comans EF, et al. Positron emission tomography using 2‐deoxy‐2‐[18F]‐fluoro‐D‐glucose for response monitoring in locally advanced gastroesophageal cancer; a comparison of different analytical methods. Molecular Imaging and Biology 2003;5(5):337‐46. [PUBMED: 14630513] - PubMed
Lavonius 2002 {published data only}
    1. Lavonius MI, Gullichsen R, Salo S, Sonninen P, Ovaska J. Staging of gastric cancer: a study with spiral computed tomography, ultrasonography, laparoscopy, and laparoscopic ultrasonography. Surgical Laparoscopy, Endoscopy and Percutaneous Techniques 2002;12(2):77‐81. [PUBMED: 119428291] - PubMed
Li 2012 {published data only}
    1. Li S, Huang P, Wang Z, Chen J, Xu H, Wang L, et al. Preoperative T staging of advanced gastric cancer using double contrast‐enhanced ultrasound. Ultraschall in der Medizin 2012;33(7):E218‐24. [PUBMED: 22744445] - PubMed
Matthes 2006 {published data only}
    1. Matthes K, Bounds BC, Collier K, Gutierrez A, Brugge WR. EUS staging of upper GI malignancies: results of a prospective randomized trial. Gastrointestinal Endoscopy 2006;64(4):496‐502. [PUBMED: 16996338] - PubMed
Meining 2002 {published data only}
    1. Meining A, Dittler HJ, Wolf A, Lorenz R, Schusdziarra V, Siewert JR, et al. You get what you expect? A critical appraisal of imaging methodology in endosonographic cancer staging. Gut 2002;50(5):599‐603. [PUBMED: 11950802] - PMC - PubMed
Mortensen 2007 {published data only}
    1. Mortensen MB, Edwin B, Hünerbein M, Liedman B, Nielsen HO, Hovendal C. Impact of endoscopic ultrasonography (EUS) on surgical decision‐making in upper gastrointestinal tract cancer: an international multicenter study. Surgical Endoscopy 2007;21(3):431‐8. [PUBMED: 17180286] - PubMed
Nagler 2011 {published data only}
    1. Nagler AK, Aslanian HR, Siddiqui UD. Endoscopic ultrasound and gastric lesions. Journal of Clinical Gastroenterology 2011;45(3):215‐21. [PUBMED: 21278579] - PubMed
Nakamura 1999b {published data only}
    1. Nakamura K, Morisaki T, Sugitani A, Ogawa T, Uchiyama A, Kinukawa N, et al. An early gastric carcinoma treatment strategy based on analysis of lymph node metastasis. Cancer 1999;85(7):1500‐5. [PUBMED: 10193939] - PubMed
Nakamura 2000 {published data only}
    1. Nakamura K, Morisaki T, Noshiro H, Torata N, Kinukawa N, Tanaka M. Morphometric analysis of regional lymph nodes with and without metastasis from early gastric carcinoma. Cancer 2000;88(11):2438‐42. [PUBMED: 10861417] - PubMed
Ohashi 1989 {published data only}
    1. Ohashi S, Nakazawa S, Yoshino J. Endoscopic ultrasonography in the assessment of invasive gastric cancer. Scandinavian Journal of Gastroenterology 1989;24(9):1039‐48. [PUBMED: 2688069] - PubMed
Okai 1991 {published data only}
    1. Okai T, Yamakawa O, Matsuda N, Kawakami H, Watanabe H, Satomura Y, et al. Analysis of gastric carcinoma growth by endoscopic ultrasonography. Endoscopy 1991;23(3):121‐5. [PUBMED: 1860438] - PubMed
Park 2011 {published data only}
    1. Park JM, Ahn CW, Yi X, Hur H, Lee KM, Cho YK, et al. Efficacy of endoscopic ultrasonography for prediction of tumor depth in gastric cancer. Journal of Gastric Cancer 2011;11(2):109‐15. [PUBMED: 22076211] - PMC - PubMed
Patel 2007 {published data only}
    1. Patel PR, Mansfield PF, Crane CH, Wu TT, Lee JH, Lynch PM, et al. Clinical stage after preoperative chemoradiation is a better predictor of patient outcome than the baseline stage for localized gastric cancer. Cancer 2007;110(5):989‐95. [PUBMED: 17636525] - PubMed
Pedrazzani 2007 {published data only}
    1. Pedrazzani C, Manzoni G, Marrelli D, Giacopuzzi S, Corso G, Minicozzi AM, et al. Lymph node involvement in advanced gastroesophageal junction adenocarcinoma. Journal of Thoracic and Cardiovascular Surgery 2007;134(2):378‐85. [PUBMED: 17662776] - PubMed
Power 2009 {published data only}
    1. Power DG, Schattner MA, Gerdes H, Brenner B, Markowitz AJ, Capanu M, et al. Endoscopic ultrasound can improve the selection for laparoscopy in patients with localized gastric cancer. Journal of the American College of Surgeons 2009;208(2):173‐8. [PUBMED: 19228527] - PubMed
Rau 1995 {published data only}
    1. Rau B, Hünerbein M, Schlag PM. Laparoscopy and laparoscopic endosonography as staging examination of tumors of the upper gastrointestinal tract. Zentralblatt fur Chirurgie 1995;120(5):346‐9. [PUBMED: 7541926] - PubMed
Richards 2000 {published data only}
    1. Richards DG, Brown TH, Manson JM. Endoscopic ultrasound in the staging of tumours of the oesophagus and gastro‐oesophageal junction. Annals of the Royal College of Surgeons of England 2000;82(5):311‐7. [PUBMED: 11041028] - PMC - PubMed
Rösch 1992 {published data only}
    1. Rösch T, Lorenz R, Zenker K, Wichert A, Dancygier H, Höfler H, et al. Local staging and assessment of resectability in carcinoma of the esophagus, stomach, and duodenum by endoscopic ultrasonography. Gastrointestinal Endoscopy 1992;38(4):460‐7. [PUBMED: 1511822] - PubMed
Songür 1996 {published data only}
    1. Songür Y, Okai T, Fujii T. Endosonographic staging of gastric carcinoma. Digestive Endoscopy 1996;8:5‐13.
Tsuzuki 2011 {published data only}
    1. Tsuzuki T, Okada H, Kawahara Y, Nasu J, Takenaka R, Inoue M, et al. Usefulness and problems of endoscopic ultrasonography in prediction of the depth of tumor invasion in early gastric cancer. Acta Medica Okayama 2011;65(2):105‐12. [PUBMED: 21519368] - PubMed
Venkataraman 2010 {published data only}
    1. Venkataraman I, Rao HK, Singh P, Elangovan S, Kate V. Efficacy of hydrogastric sonography and spiral computed tomography in staging of gastric carcinoma‐‐a comparative study. Journal of Clinical Ultrasound 2010;38(9):480‐5. [PUBMED: 20848570] - PubMed
Wakelin 2002 {published data only}
    1. Wakelin SJ, Deans C, Crofts TJ, Allan PL, Plevris JN, Paterson‐Brown S. A comparison of computerised tomography, laparoscopic ultrasound and endoscopic ultrasound in the preoperative staging of oesophago‐gastric carcinoma. European Journal of Radiology 2002;41(2):161‐7. [PUBMED: 11809546] - PubMed
Yoshinaga 2012 {published data only}
    1. Yoshinaga S, Oda I, Nonaka S, Kushima R, Saito Y. Endoscopic ultrasound using ultrasound probes for the diagnosis of early esophageal and gastric cancers. World Journal of Gastrointestinal Endoscopy 2012;4(6):218‐26. [PUBMED: 22720122] - PMC - PubMed

References to studies awaiting assessment

Feng 2013 {published data only}
    1. Feng XY, Wang W, Luo GY, Wu J, Zhou ZW, Li W, et al. Comparison of endoscopic ultrasonography and multislice spiral computed tomography for the preoperative staging of gastric cancer ‐ results of a single institution study of 610 Chinese patients. PLoSOne 2013;8(11):e78846. [PUBMED: 24223855] - PMC - PubMed
Lei 2013 {published data only}
    1. Lei C, Huang L, Wang Y, Huang Y, Huang Y. Comparison of MRI and endoscope ultrasound detection in preoperative T/N staging of gastric cancer. Molecular and Clinical Oncology 2013;1(4):699‐702. [DOI: 10.3892/mco.2013.103] - DOI - PMC - PubMed
Mehmedović 2014 {published data only}
    1. Mehmedović A, Mesihović R, Saray A, Vanis N. Gastric cancer staging: EUS and CT. Medical Archives 2014;68(1):34‐6. [DOI: 10.5455/medarh.2014.68.34-36; PUBMED: 24783909] - DOI - PMC - PubMed
Spolverato 2015 {published data only}
    1. Spolverato G, Ejaz A, Kim Y, Squires MH, Poultsides GA, Fields RC, et al. Use of endoscopic ultrasound in the preoperative staging of gastric cancer: a multi‐institutional study of the US gastric cancer collaborative. Journal of the American College of Surgeons 2015;220(1):48‐56. [DOI: 10.1016/j.jamcollsurg.2014.06.023; PUBMED: 25283742] - DOI - PubMed

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