Digestive Diseases and Sciences

, Volume 53, Issue 9, pp 2405–2414 | Cite as

Accuracy of Endoscopic Ultrasound in the Diagnosis of Distal and Celiac Axis Lymph Node Metastasis in Esophageal Cancer: A Meta-Analysis and Systematic Review

  • Srinivas R. Puli
  • Jyotsna B. K. Reddy
  • Matthew L. Bechtold
  • Mainor R. Antillon
  • Jamal A. Ibdah
Original Paper

Abstract

Background Published data on the accuracy of endoscopic ultrasound (EUS) for staging distant and celiac axis lymph node (CLN) metastasis in patients with esophageal cancer (ECA) has varied. Aim To evaluate the accuracy of EUS in diagnosing distal and CLN metastasis in ECA patients. Method Study selection: EUS studies confirmed by surgery were selected. Statistical method: Pooling was conducted by both fixed and random-effects models. Results Data were extracted from 25 studies (N = 2029) which met the inclusion criteria. In ECA patients, pooled sensitivity of EUS was 67.2% (95% CI: 62.6–71.6) in diagnosis of distal metastasis and 66.6% (95% CI: 61.9–71.1) in diagnosis of CLN metastasis. EUS had a pooled specificity of 97.9% (95% CI: 97.1–98.6) for distal metastasis and 98.1% (95% CI: 97.3–98.7) for CLN metastasis. Conclusions Although EUS has excellent specificity in accurately diagnosing distal and CLN metastasis in patients with ECA, the sensitivity is low.

Keywords

Meta-analysis Systematic review Esophageal cancer Distal metastasis Celiac axis lymphadenopathy 

References

  1. 1.
    Cossentino MJ, Wong RKH (2003) Barrett’s esophagus and risk of esophageal adenocarcinoma. Semin Gastrointest Dis 14(3):128–135PubMedGoogle Scholar
  2. 2.
    Bollschweiler E, Wolfgarten E, Gutschow C, Holscher AH (2001) Demographic variations in the rising incidence of esophageal adenocarcinoma in white males. Cancer 92(3):549–555PubMedCrossRefGoogle Scholar
  3. 3.
    Blot WJ, McLaughlin JK (1999) The changing epidemiology of esophageal cancer. Semin Oncol 26(5 Suppl 15):2–8PubMedGoogle Scholar
  4. 4.
    El-Serag HB, Mason AC, Petersen N, Key CR (2002) Epidemiological differences between adenocarcinoma of the oesophagus and adenocarcinoma of the gastric cardia in the USA. Gut 50(3):368–372PubMedCrossRefGoogle Scholar
  5. 5.
    Holmes RS, Vaughan TL (2007) Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol 17(1):2–9PubMedCrossRefGoogle Scholar
  6. 6.
    Fitzgerald RC (2004) Barrett’s oesophagus and associated adenocarcinoma—a UK prospective. Aliment Pharmacol Ther 20(Suppl 8):45–49PubMedCrossRefGoogle Scholar
  7. 7.
    Christie NA, Rice TW, DeCamp MM et al (1999) M1A/M1B esophageal carcinoma clinical relevance. J Thorac Cardiovasc Surg 118:900–907PubMedCrossRefGoogle Scholar
  8. 8.
    Malaisrie SC, Hofstetter WL, Correa AM, Ajani JA, Komaki RR, Liao Z, Phan A, Rice DC, Vaporciyan AA, Walsh GL, Lahoti S, Lee JH, Bresalier R, Roth JA, Swisher SG (2006) Endoscopic ultrasonography-identified celiac adenopathy remains a poor prognostic factor despite preoperative chemoradiotherapy in esophageal adenocarcinoma. J Thorac Cardiovasc Surg 131(1):65–72, Epub 5 Dec 2005PubMedCrossRefGoogle Scholar
  9. 9.
    Eloubeidi MA, Wallace MB, Hoffman BJ et al (2001) Predictors of survival for esophageal cancer patients with and without celiac axis lymphadenopathy impact of staging endosonography. Ann Thorac Surg 72:212–220PubMedCrossRefGoogle Scholar
  10. 10.
    Akiyama H, Tsurumaru M, Udagawa H et al (1994) Radical lymph node dissection for cancer of the thoracic esophagus. Ann Surg 220:364–373PubMedCrossRefGoogle Scholar
  11. 11.
    Bada M, Aikou T, Yoshinaka H et al (1994) Long-term results of subtotal esophagectomy with three-field lymphadenectomy for cancer of the thoracic esophagus. Ann Surg 219:310–316CrossRefGoogle Scholar
  12. 12.
    Daly JM, Karnell LH, Menck HR (1996) National cancer data base report on esophageal carcinoma. Cancer 78(8):1820–1828PubMedCrossRefGoogle Scholar
  13. 13.
    Reed CE, Mishra G, Sahai AV, Hoffman BJ, Hawes RH (1999) Esophageal cancer staging: improved accuracy by endoscopic ultrasound of celiac lymph nodes. Ann Thorac Surg 67(2):319–321PubMedCrossRefGoogle Scholar
  14. 14.
    Romagnuolo J, Scott J, Hawes RH, Hoffman BJ, Reed CE, Aithal GP, Breslin NP, Chen RY, Gumustop B, Hennessey W, Van Velse A, Wallace MB (2002) Helical CT versus EUS with fine needle aspiration for celiac nodal assessment in patients with esophageal cancer. Gastrointest Endosc 55(6):648–654PubMedCrossRefGoogle Scholar
  15. 15.
    Takashima S, Takeuchi N, Shiozaki H, Kobayashi K, Morimoto S, Ikezoe J, Tomiyama N, Harada K, Shogen K, Kozuka T (1991) Carcinoma of the esophagus: CT vs MR imaging in determining resectability. Am J Roentgenol 156(2):297–302Google Scholar
  16. 16.
    Quint LE, Glazer GM, Orringer MB (1985) Esophageal imaging by MR and CT: study of normal anatomy and neoplasms. Radiology 156(3):727–731PubMedGoogle Scholar
  17. 17.
    Lehr L, Rupp N, Siewert JR (1988) Assessment of resectability of esophageal cancer by computed tomography and magnetic resonance imaging. Surgery 103(3):344–350PubMedGoogle Scholar
  18. 18.
    Dam HQ, Manzone TM, Sagar VV (2006) Evolving role of (18)F-fluorodeoxyglucose positron emission tomography in the management of esophageal carcinoma. Surg Oncol Clin N Am 15(4):733–749PubMedCrossRefGoogle Scholar
  19. 19.
    Wiersema MJ, Wiersema LM (1993) High-resolution 25-megahertz ultrasonography of the gastrointestinal wall: histologic correlates. Gastrointest Endosc 39(4):499–504PubMedGoogle Scholar
  20. 20.
    Pfau PR, Perlman SB, Stanko P, Frick TJ, Gopal DV, Said A, Zhang Z, Weigel T (2007) The role and clinical value of EUS in a multimodality esophageal carcinoma staging program with CT and positron emission tomography. Gastrointest Endosc 65(3):377–384PubMedCrossRefGoogle Scholar
  21. 21.
    Grimm H, Binmoeller KF, Hamper K, Koch J, Henne-Bruns D, Soehendra N (1993) Endosonography for preoperative locoregional staging of esophageal and gastric cancer. Endoscopy 25(3):224–230PubMedGoogle Scholar
  22. 22.
    Rosch T, Lorenz R, Zenker K, von Wichert A, Dancygier H, Hofler H, Siewert JR, Classen M (1992) Local staging and assessment of resectability in carcinoma of the esophagus, stomach, and duodenum by endoscopic ultrasonography. Gastrointest Endosc 38(4):460–467PubMedGoogle Scholar
  23. 23.
    Familiari P, Marchese M, Larghi A, Spada C, Costamagna G (2005) Staging of esophageal carcinoma: endoscopic ultrasonography. Rays 30(4):357–362PubMedGoogle Scholar
  24. 24.
    Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF, for the QUOROM Group (1999) Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Lancet 354:1896–1900PubMedCrossRefGoogle Scholar
  25. 25.
    Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, Lijmer JG, Moher D, Rennie D. de Vet HC (2003) Standards for reporting of diagnostic accuracy group. Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. The standards for reporting of diagnostic accuracy group. Croat Med J 44(5):635–638Google Scholar
  26. 26.
    Jadad AR et al (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12PubMedCrossRefGoogle Scholar
  27. 27.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012PubMedCrossRefGoogle Scholar
  28. 28.
    Puli SR, Singh S, Hagedorn CH, Reddy J, Olyaee M (2007) Diagnostic accuracy of EUS for vascular invasion in pancreatic and periampullary cancers: a meta-analysis and systematic review. Gastrointest Endosc 65(6):788–797PubMedCrossRefGoogle Scholar
  29. 29.
    Leemis LM, Trivedi KS (1996) A comparison of approximate interval estimators for the Bernoulli parameter. Am Stat 50:63–68CrossRefGoogle Scholar
  30. 30.
    Cox DR (1970) The analysis of binary data. Methuen, LondonGoogle Scholar
  31. 31.
    Agresti A (1984) Analysis of ordinal categorical data. John Wiley & Sons, New YorkGoogle Scholar
  32. 32.
    Deeks JJ (2001) Systematic reviews of evaluations of diagnostic and screening tests. In: Egger M, Smith GD, Altman DG (eds) Systematic reviews in health care. Meta-analysis in context. BMJ Books, LondonGoogle Scholar
  33. 33.
    Harbord RM, Egger M, Sterne JAC (2005) A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 25(20):3443–3457CrossRefGoogle Scholar
  34. 34.
    Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101PubMedCrossRefGoogle Scholar
  35. 35.
    Sterne JAC, Egger M, Davey-Smith G (2001) Investigating and dealing with publication and other biases in meta-analysis. Br Med J 323:101–105CrossRefGoogle Scholar
  36. 36.
    Sterne JAC, Egger M (2001) Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 54:1046–1055PubMedCrossRefGoogle Scholar
  37. 37.
    Catalano MF, Alcocer E, Chak A, Nguyen CC, Raijman I, Geenen JE, Lahoti S, Sivak MV Jr (1999) Evaluation of metastatic celiac axis lymph nodes in patients with esophageal carcinoma: accuracy of EUS. Gastrointest Endosc 50(3):352–356PubMedCrossRefGoogle Scholar
  38. 38.
    Binmoeller KF, Seifert H, Seitz U, Izbicki JR, Kida M, Soehendra N (1995) Ultrasonic esophagoprobe for TNM staging of highly stenosing esophageal carcinoma. Gastrointest Endosc 41(6):547–552PubMedCrossRefGoogle Scholar
  39. 39.
    Grimm H, Binmoeller KF, Hamper K, Koch J, Henne-Bruns D, Soehendra N (1993) Endosonography for preoperative locoregional staging of esophageal and gastric cancer. Endoscopy 25(3):224–230PubMedGoogle Scholar
  40. 40.
    Giovannini M, Monges G, Seitz JF, Moutardier V, Bernardini D, Thomas P, Houvenaeghel G, Delpero JR, Giudicelli R, Fuentes P (1999) Distant lymph node metastases in esophageal cancer: impact of endoscopic ultrasound-guided biopsy. Endoscopy 31(7):536–540PubMedCrossRefGoogle Scholar
  41. 41.
    Salminen JT, Farkkila MA, Ramo OJ, Toikkanen V, Simpanen J, Nuutinen H, Salo JA (1999) Endoscopic ultrasonography in the preoperative staging of adenocarcinoma of the distal oesophagus and oesophagogastric junction. Scand J Gastroenterol 34(12):1178–1182PubMedCrossRefGoogle Scholar
  42. 42.
    Williams DB, Sahai AV, Aabakken L, Penman ID, van Velse A, Webb J, Wilson M, Hoffman BJ, Hawes RH (1999) Endoscopic ultrasound guided fine needle aspiration biopsy: a large single centre experience. Gut 44(5):720–726PubMedCrossRefGoogle Scholar
  43. 43.
    Vickers J (1998) Role of endoscopic ultrasound in the preoperative assessment of patients with oesophageal cancer. Ann R Coll Surg Engl 80(4):233–239PubMedGoogle Scholar
  44. 44.
    Tio TL, Coene PP, den Hartog Jager FC, Tytgat GN (1990) Preoperative TNM classification of esophageal carcinoma by endosonography. Hepato-Gastroenterology 37(4):376–381PubMedGoogle Scholar
  45. 45.
    Tio TL, Coene PP, Schouwink MH, Tytgat GN (1989) Esophagogastric carcinoma: preoperative TNM classification with endosonography. Radiology 173(2):411–417PubMedGoogle Scholar
  46. 46.
    Tio TL, Cohen P, Coene PP, Udding J, den Hartog Jager FC, Tytgat GN (1989) Endosonography and computed tomography of esophageal carcinoma. Preoperative classification compared to the new (1987) TNM system. Gastroenterology 96(6):1478–1486PubMedGoogle Scholar
  47. 47.
    Tio TL, Schouwink MH, Cikot RJ, Tytgat GN (1989) Preoperative TNM classification of gastric carcinoma by endosonography in comparison with the pathological TNM system: a prospective study of 72 cases. Hepato-Gastroenterology 36(2):51–56PubMedGoogle Scholar
  48. 48.
    Eloubeidi MA, Wallace MB, Reed CE, Hadzijahic N, Lewin DN, Van Velse A, Leveen MB, Etemad B, Matsuda K, Patel RS, Hawes RH, Hoffman BJ (2001) The utility of EUS and EUS-guided fine needle aspiration in detecting celiac lymph node metastasis in patients with esophageal cancer: a single-center experience. Gastrointest Endosc 54(6):714–719PubMedCrossRefGoogle Scholar
  49. 49.
    Reed CE, Mishra G, Sahai AV, Hoffman BJ, Hawes RH (1999) Esophageal cancer staging: improved accuracy by endoscopic ultrasound of celiac lymph nodes. Ann Thorac Surg 67(2):319–321; discussion 322PubMedCrossRefGoogle Scholar
  50. 50.
    DeWitt J, Kesler K, Brooks JA, LeBlanc J, McHenry L, McGreevy K, Sherman S (2005) Endoscopic ultrasound for esophageal and gastroesophageal junction cancer: Impact of increased use of primary neoadjuvant therapy on preoperative locoregional staging accuracy. Dis Esophagus 18(1):21–27PubMedCrossRefGoogle Scholar
  51. 51.
    Wallace MB, Hawes RH, Sahai AV, Van Velse A, Hoffman BJ (2000) Dilation of malignant esophageal stenosis to allow EUS guided fine-needle aspiration: safety and effect on patient management. Gastrointest Endosc 51(3):309–313PubMedCrossRefGoogle Scholar
  52. 52.
    Bowrey DJ, Clark GW, Roberts SA, Maughan TS, Hawthorne AB, Williams GT, Carey PD (1999) Endosonographic staging of 100 consecutive patients with esophageal carcinoma: introduction of the 8-mm esophagoprobe. Dis Esophagus 12(4):258–263PubMedCrossRefGoogle Scholar
  53. 53.
    Eloubeidi MA, Wallace MB, Hoffman BJ, Leveen MB, Van Velse A, Hawes RH, Reed CE (2001) Predictors of survival for esophageal cancer patients with and without celiac axis lymphadenopathy: impact of staging endosonography. Ann Thorac Surg 72(1):212–219; discussion 219–220PubMedCrossRefGoogle Scholar
  54. 54.
    Vazquez-Sequeiros E, Norton ID, Clain JE, Wang KK, Affi A, Allen M, Deschamps C, Miller D, Salomao D, Wiersema MJ (2001) Impact of EUS-guided fine-needle aspiration on lymph node staging in patients with esophageal carcinoma. Gastrointest Endosc 53(7):751–757PubMedCrossRefGoogle Scholar
  55. 55.
    Krasna MJ, Mao YS, Sonett J, Gamliel Z (1999) The role of thoracoscopic staging of esophageal cancer patients. Eur J Cardio-Thorac Surg 16(Suppl 1):S31–S33CrossRefGoogle Scholar
  56. 56.
    Kallimanis GE, Gupta PK, al-Kawas FH, Tio LT, Benjamin SB, Bertagnolli ME, Nguyen CC, Gomes MN, Fleischer DE (1995) Endoscopic ultrasound for staging esophageal cancer, with or without dilation, is clinically important and safe. Gastrointest Endosc 41(6):540–546PubMedCrossRefGoogle Scholar
  57. 57.
    Shimizu Y, Tsukagoshi H, Asaka M et al (1997) Endoscopic ultrasonography for the detection of lymph node metastasis in superficial esophageal carcinoma. Dig Endosc 9:178–182CrossRefGoogle Scholar
  58. 58.
    Nishimaki T, Tanaka O, Ando N, Ide H, Watanabe H, Shinoda M, Takiyama W, Yamana H, Ishida K, Isono K, Endo M, Ikeuchi T, Mitomi T, Koizumi H, Imamura M, Iizuka T (1999) Evaluation of the accuracy of preoperative staging in thoracic esophageal cancer. Ann Thorac Surg 68(6):2059–2064PubMedCrossRefGoogle Scholar
  59. 59.
    Fok M, Cheng SW, Wong J (1992) Endosonography in patient selection for surgical treatment of esophageal carcinoma. World J Surg 16(6):1098–1103; discussion 103PubMedCrossRefGoogle Scholar
  60. 60.
    Natsugoe S, Yoshinaka H, Morinaga T, Shimada M, Baba M, Fukumoto T, Stein HJ, Aikou T (1996) Ultrasonographic detection of lymph-node metastases in superficial carcinoma of the esophagus. Endoscopy 28(8):674–679PubMedCrossRefGoogle Scholar
  61. 61.
    Tio TL, den Hartog Jager FC, Tytgat GN (1986) The role of endoscopic ultrasonography in assessing local resectability of oesophagogastric malignancies. Accuracy, pitfalls, and predictability. Scand J Gastroenterol—Suppl 123:78–86PubMedCrossRefGoogle Scholar
  62. 62.
    Vilmann P (1996) Endoscopic ultrasonography-guided fine-needle aspiration biopsy of lymph nodes. Gastrointest Endoscopy 43(2 pt 2):S24–S29CrossRefGoogle Scholar
  63. 63.
    Wiersema MJ, Vazquez-Sequeiros E, Wiersema LM (2001) Evaluation of mediastinal lymphadenopathy with endoscopic US-guided fine-needle aspiration biopsy. Radiology 219(1):252–257PubMedGoogle Scholar
  64. 64.
    Vilmann P (1996) Endoscopic ultrasonography-guided fine-needle aspiration biopsy of lymph nodes. Gastrointest Endoscopy 43(2 pt 2):S24–S29CrossRefGoogle Scholar
  65. 65.
    Silvestri GA, Hoffman BJ, Bhutani MS, Hawes RH, Coppage L, Sanders-Cliette A, Reed CE (1996) Endoscopic ultrasound with fine-needle aspiration in the diagnosis and staging of lung cancer. Ann Thorac Surg 61(5):1441–1445; discussion 1445–1446PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Srinivas R. Puli
    • 1
  • Jyotsna B. K. Reddy
    • 1
  • Matthew L. Bechtold
    • 1
  • Mainor R. Antillon
    • 1
  • Jamal A. Ibdah
    • 1
  1. 1.Division of Gastroenterology and HepatologyUniversity of Missouri-ColumbiaColumbiaUSA

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