Gastric Cancer

, Volume 12, Issue 1, pp 6–22 | Cite as

Imaging in assessing lymph node status in gastric cancer

  • Robert Michael Kwee
  • Thomas Christian Kwee
Review Article

Abstract

Background

Accurate assessment of lymph node status is of crucial importance for appropriate treatment planning and determining prognosis in patients with gastric cancer. The aim of this study was to systematically review the current role of imaging in assessing lymph node (LN) status in gastric cancer.

Methods

A systematic literature search was performed in the PubMed/MEDLINE and Embase databases. The methodological quality and diagnostic performance of the included studies was assessed.

Results

Six abdominal ultrasonography (AUS) studies, 30 endoscopic ultrasonography (EUS) studies, 10 multidetectorrow computed tomography (MDCT) studies, 3 conventional magnetic resonance imaging (MRI) studies, 4 18F-fluoro-2-deoxyglucose positron emission tomography (FDG-PET) studies, and 1 FDG-PET/CT fusion study were included. In general, the included studies had moderate methodological quality. The sensitivity and specificity of AUS varied between 12.2% and 80.0% (median, 39.9%) and 56.3% and 100% (median, 81.8%). The sensitivity and specificity of EUS varied between 16.7% and 95.3% (median, 70.8%) and 48.4% and 100% (median, 84.6%). The sensitivity and specificity of MDCT varied between 62.5% and 91.9% (median, 80.0%) and 50.0% and 87.9% (median, 77.8%). The sensitivity and specificity of MRI varied between 54.6% and 85.3% (median, 68.8%) and 50.0% and 100% (median, 75.0%). The sensitivity and specificity of FDG-PET varied between 33.3% and 64.6% (median, 34.3%) and 85.7% and 97.0% (median, 93.2%). The sensitivity and specificity of the FDG-PET/CT fusion study were 54.7% and 92.2%. For all the imaging modalities, there were no significant differences between the mean sensitivities and specificities of high- and low-quality studies.

Conclusion

AUS, EUS, MDCT, conventional MRI, and FDG-PET cannot reliably be used to confirm or exclude the presence of LN metastasis. The performance of highresolution PET/CT fusion and functional MRI techniques still has to be determined.

Key words

Gastric cancer Lymph node metastasis Imaging Staging Systematic review 

References

  1. 1.
    Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74–108.PubMedCrossRefGoogle Scholar
  2. 2.
    Siewert JR, Böttcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: 10-year results of the German Gastric Cancer Study. Ann Surg 1998;228:449–461.PubMedCrossRefGoogle Scholar
  3. 3.
    Zhang XF, Huang CM, Lu HS, Wu XY, Wang C, Guang GX, et al. Surgical treatment and prognosis of gastric cancer in 2613 patients. World J Gastroenterol 2004;10:3405–3408.PubMedGoogle Scholar
  4. 4.
    Gotoda T, Yanagisawa A, Sasako M, Ono H, Nakanishi Y, Shimoda T, et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 2000;3:219–225.PubMedCrossRefGoogle Scholar
  5. 5.
    Hohenberger P, Gretschel S. Gastric cancer. Lancet 2003;362:305–315.PubMedCrossRefGoogle Scholar
  6. 6.
    Swan R, Miner TJ. Current role of surgical therapy in gastric cancer. World J Gastroenterol 2006;12:372–379.PubMedGoogle Scholar
  7. 7.
    Brennan MF. Current status of surgery for gastric cancer: a review. Gastric Cancer 2005;8:64–70.PubMedCrossRefGoogle Scholar
  8. 8.
    De Vita F, Giuliani F, Galizia G, Belli C, Aurilio G, Santabarbara G, et al. Neo-adjuvant and adjuvant chemotherapy of gastric cancer. Ann Oncol 2007;18(Suppl 6):20–23.Google Scholar
  9. 9.
    Barentsz J, Takahashi S, Oyen W, Mus R, De Mulder P, Reznek R, et al. Commonly used imaging techniques for diagnosis and staging. J Clin Oncol 2006;24:3234–3244.PubMedCrossRefGoogle Scholar
  10. 10.
    Rubin E, Palazzo JP. The gastrointestinal tract. In: Rubin E, Gorstein F, Rubin F, Schwarting R, Strayer D, editors. Rubin’s pathology. Clinicopathologic foundations of medicine. 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2005. p. 660–739.Google Scholar
  11. 11.
    Kelly S, Berry E, Roderick P, Harris KM, Cullingworth J, Gathercole L, et al. The identification of bias in studies of the diagnostic performance of imaging modalities. Br J Radiol 1997;70:1028–1035.PubMedGoogle Scholar
  12. 12.
    Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol 2003;3:25.PubMedCrossRefGoogle Scholar
  13. 13.
    Whiting PF, Weswood ME, Rutjes AW, Reitsma JB, Bossuyt PN, Kleijnen J. Evaluation of QUADAS, a tool for the quality assessment of diagnostic accuracy studies. BMC Med Res Methodol 2006;6:9.PubMedCrossRefGoogle Scholar
  14. 14.
    Kim YN, Choi D, Kim SH, Kim MJ, Lee SJ, Lee WJ, et al. Gastric cancer staging at isotropic MDCT including coronal and sagittal MPR images: endoscopically diagnosed early vs advanced gastric cancer. Abdom Imaging 2009;34:26–34.PubMedCrossRefGoogle Scholar
  15. 15.
    Chamadol N, Wongwiwatchai J, Bhudhisawasd V, Pairojkul C. Accuracy of spiral CT in preoperative staging of gastric carcinoma: correlation with surgical and pathological findings. J Med Assoc Thai 2008;91:356–363.PubMedGoogle Scholar
  16. 16.
    Yang Q-M, Kawamura T, Itoh H, Bando E, Nemoto M, Akamoto S, et al. Is PET-CT suitable for predicting lymph node status for gastric cancer? Hepatogastroenterology 2008;55:782–785.PubMedGoogle Scholar
  17. 17.
    Lok K-H, Lee C-K, Yiu H-L, Lai L, Szeto M-L, Leung S-K. Current utilization and performance status of endoscopic ultrasound in a community hospital. J Dig Dis 2008;9:41–47.PubMedCrossRefGoogle Scholar
  18. 18.
    Chen BB, Liang PC, Liu KL, Hsiao JK, Huang JC, Wong JM, et al. Preoperative diagnosis of gastric tumors by threedimensional multidetector row CT and double contrast barium meal study: correlation with surgical and histologic results. J Formos Med Assoc 2007;106:943–952.PubMedCrossRefGoogle Scholar
  19. 19.
    Bentrem D, Gerdes H, Tang L, Brennan M, Coit D. Clinical correlation of endoscopic ultrasonography with pathologic stage and outcome in patients undergoing curative resection for gastric cancer. Ann Surg Oncol 2007;14:1853–1859.PubMedCrossRefGoogle Scholar
  20. 20.
    Tan SY, Wang JY, Shen L, Luo HS, Shen ZX. Relationship between preoperative staging by endoscopic ultrasonography and MMP-9 expression in gastric carcinoma. World J Gastroenterol 2007;13:2108–2112.PubMedGoogle Scholar
  21. 21.
    Chen CY, Hsu JS, Wu DC, Kang WY, Hsieh JS, Jaw TS, et al. Gastric cancer: preoperative local staging with 3D multi-detector row CT-correlation with surgical and histopathologic results. Radiology 2007;242:472–482.PubMedCrossRefGoogle Scholar
  22. 22.
    Yang DM, Kim HC, Jin W, Ryu CW, Kang JH, Park CH, et al. 64 Multidetector-row computed tomography for preoperative evaluation of gastric cancer: histological correlation. J Comput Assist Tomogr 2007;31:98–103.PubMedCrossRefGoogle Scholar
  23. 23.
    Ozmen MM, Zulfikaroglu B, Kucuk NO, Ozalp N, Aras G, Koseoglu T, et al. Lymphoscintigraphy in detection of the regional lymph node involvement in gastric cancer. Ann R Coll Surg Engl 2006;88:632–638.PubMedCrossRefGoogle Scholar
  24. 24.
    Arocena MG, Barturen A, Bujanda L, Casado O, Ramírez MM, Oleagoitia JM, et al. MRI and endoscopic ultrasonography in the staging of gastric cancer. Rev Esp Enferm Dig 2006;98:582–590.PubMedCrossRefGoogle Scholar
  25. 25.
    Ganpathi IS, So JB, Ho KY. Endoscopic ultrasonography for gastric cancer: does it influence treatment? Surg Endosc 2006;20:559–562.PubMedCrossRefGoogle Scholar
  26. 26.
    Tsendsuren T, Jun SM, Mian XH. Usefulness of endoscopic ultrasonography in preoperative TNM staging of gastric cancer. World J Gastroenterol 2006;12:43–47.PubMedGoogle Scholar
  27. 27.
    Ang TL, Ng TM, Fock KM, Teo EK. Accuracy of endoscopic ultrasound staging of gastric cancer in routine clinical practice in Singapore. Chin J Dig Dis 2006;7:191–196.PubMedCrossRefGoogle Scholar
  28. 28.
    Mukai K, Ishida Y, Okajima K, Isozaki H, Morimoto T, Nishiyama S. Usefulness of preoperative FDG-PET for detection of gastric cancer. Gastric Cancer 2006;9:192–196.PubMedCrossRefGoogle Scholar
  29. 29.
    Potrc S, Skalicky M, Ivanecz A. Does endoscopic ultrasound staging already allow individual treatment regimens in gastric cancer? Wien Klin Wochenschr 2006;118(Suppl 2):48–51.PubMedCrossRefGoogle Scholar
  30. 30.
    Yun M, Lim JS, Noh SH, Hyung WJ, Cheong JH, Bong JK, et al. Lymph node staging of gastric cancer using (18)F-FDG PET: a comparison study with CT. J Nucl Med 2005;46:1582–1588.PubMedGoogle Scholar
  31. 31.
    Kim HJ, Kim AY, Oh ST, Kim JS, Kim KW, Kim PN, et al. Gastric cancer staging at multi-detector row CT gastrography: comparison of transverse and volumetric CT scanning. Radiology 2005;236:879–885.PubMedCrossRefGoogle Scholar
  32. 32.
    Shinohara T, Ohyama S, Yamaguchi T, Muto T, Kohno A, Ogura T, et al. Preoperative TNM staging of advanced gastric cancer with multi-detector row computed tomography. Japan Med Assoc J 2005;48:175–182.Google Scholar
  33. 33.
    Liao SR, Dai Y, Huo L, Yan K, Zhang L, Zhang H, et al. Transabdominal ultrasonography in preoperative staging of gastric cancer. World J Gastroenterol 2004;10:3399–3404.PubMedGoogle Scholar
  34. 34.
    Polkowski M, Palucki J, Wronska E, Szawlowski A, Nasierowska-Guttmejer A, Butruk E. Endosonography versus helical computed tomography for locoregional staging of gastric cancer. Endoscopy 2004;36:617–623.PubMedCrossRefGoogle Scholar
  35. 35.
    Bhandari S, Shim CS, Kim JH, Jung IS, Cho JY, Lee JS, et al. Usefulness of three-dimensional, multidetector row CT (virtual gastroscopy and multiplanar reconstruction) in the evaluation of gastric cancer: a comparison with conventional endoscopy, EUS, and histopathology. Gastrointest Endosc 2004;59:619–626.PubMedCrossRefGoogle Scholar
  36. 36.
    Javaid G, Shah OJ, Dar MA, Shah P, Wani NA, Zargar SA. Role of endoscopic ultrasonography in preoperative staging of gastric carcinoma. ANZ J Surg 2004;74:108–111.PubMedCrossRefGoogle Scholar
  37. 37.
    Habermann CR, Weiss F, Riecken R, Honarpisheh H, Bohnacker S, Staedtler C, et al. Preoperative staging of gastric adenocarcinoma: comparison of helical CT and endoscopic US. Radiology 2004;230:465–471.PubMedCrossRefGoogle Scholar
  38. 38.
    Tian J, Chen L, Wei B, Shao M, Ding Y, Yin D, et al. The value of vesicant 18F-fluorodeoxyglucose positron emission tomography (18F-FDG PET) in gastric malignancies. Nucl Med Commun 2004;25:825–831.PubMedCrossRefGoogle Scholar
  39. 39.
    Stabile Ianora AA, Pedote P, Scardapane A, Memeo M, Rotondo A, Angelelli G. Preoperative staging of gastric carcinoma with multidetector spiral CT. Radiol Med (Torino) 2003;106:467–480.Google Scholar
  40. 40.
    Xi WD, Zhao C, Ren GS. Endoscopic ultrasonography in preoperative staging of gastric cancer: determination of tumor invasion depth, nodal involvement and surgical resectability. World J Gastroenterol 2003;9:254–257.PubMedGoogle Scholar
  41. 41.
    Chen CH, Yang CC, Yeh YH. Preoperative staging of gastric cancer by endoscopic ultrasound: the prognostic usefulness of ascites detected by endoscopic ultrasound. J Clin Gastroenterol 2002;35:321–327.PubMedCrossRefGoogle Scholar
  42. 42.
    Lee DH, Ko YT, Park SJ, Lim JW. Comparison of hydro-US and spiral CT in the staging of gastric cancer. Clin Imaging 2001;25:181–186.PubMedCrossRefGoogle Scholar
  43. 43.
    Willis S, Truong S, Gribnitz S, Fass J, Schumpelick V. Endoscopic ultrasonography in the preoperative staging of gastric cancer: accuracy and impact on surgical therapy. Surg Endosc 2000;14:951–954.PubMedCrossRefGoogle Scholar
  44. 44.
    Tseng LJ, Mo LR, Tio TL, Fresner YT, Jao N, Lin RC, et al. Video-endoscopic ultrasonography in staging gastric carcinoma. Hepatogastroenterology 2000;47:897–900.PubMedGoogle Scholar
  45. 45.
    Kim AY, Han JK, Seong CK, Kim TK, Choi BI. MRI in staging advanced gastric cancer: is it useful compared with spiral CT? J Comput Assist Tomogr 2000;24:389–394.PubMedCrossRefGoogle Scholar
  46. 46.
    Mancino G, Bozzetti F, Schicchi A, Schiavo M, Spinelli P, Andreola S. Preoperative endoscopic ultrasonography in patients with gastric cancer. Tumori 2000;86:139–141.PubMedGoogle Scholar
  47. 47.
    Kang BC, Kim JH, Kim KW, Lee DY, Baek SY, Lee SW, et al. Value of the dynamic and delayed MR sequence with Gd-DTPA in the T-staging of stomach cancer: correlation with the histopathology. Abdom Imaging 2000;25:14–24.PubMedCrossRefGoogle Scholar
  48. 48.
    Akahoshi K, Chijiwa Y, Hamada S, Sasaki I, Nawata H, Kabemura T, et al. Pretreatment staging of endoscopically early gastric cancer with a 15 MHz ultrasound catheter probe. Gastrointest Endosc 1998;48:470–476.PubMedCrossRefGoogle Scholar
  49. 49.
    Hunerbein M, Ghadimi BM, Haensch W, Schlag PM. Transendoscopic ultrasound of esophageal and gastric cancer using miniaturized ultrasound catheter probes. Gastrointest Endosc 1998;48:371–375.PubMedCrossRefGoogle Scholar
  50. 50.
    Wang JY, Hsieh JS, Huang YS, Huang CJ, Hou MF, Huang TJ. Endoscopic ultrasonography for preoperative locoregional staging and assessment of resectability in gastric cancer. Clin Imaging 1998;22:355–359.PubMedCrossRefGoogle Scholar
  51. 51.
    Yeung HW, Macapinlac H, Karpeh M, Finn RD, Larson SM. Accuracy of FDG-PET in gastric cancer. Preliminary experience. Clin Positron Imaging 1998;1:213–221.PubMedCrossRefGoogle Scholar
  52. 52.
    Hamada S, Akahoshi K, Chijiiwa Y, Nawata H, Sasaki I. Relationship between histological type and endosonographic detection of regional lymph node metastases in gastric cancer. Br J Radiol 1997;70:697–702.PubMedGoogle Scholar
  53. 53.
    Düx M, Roeren T, Kuntz C, Richter GM, Kauffmann GW. TNM staging of gastrointestinal tumors by hydrosonography: results of a histopathologically controlled study in 60 patients. Abdom Imaging 1997;22:24–34.PubMedCrossRefGoogle Scholar
  54. 54.
    Kim JJ, Jung HC, Song IS, Choi KW, Kim CY, Han JK, et al. Preoperative evaluation of the curative resectability of gastric cancer by abdominal computed tomography and ultrasonography: a prospective comparison study. Korean J Intern Med 1997;12:1–6.PubMedGoogle Scholar
  55. 55.
    Hunerbein M, Dohmoto M, Rau B, Schlag PM. Endosonography and endosonography-guided biopsy of upper-GI-tract tumors using a curved-array echoendoscope. Surg Endosc 1996;10:1205–1209.PubMedCrossRefGoogle Scholar
  56. 56.
    François E, Peroux J, Mouroux J, Chazalle M, Hastier P, Ferrero J, et al. Preoperative endosonographic staging of cancer of the cardia. Abdom Imaging 1996;21:483–487.PubMedCrossRefGoogle Scholar
  57. 57.
    Stell DA, Carter CR, Stewart I, Anderson JR. Prospective comparison of laparoscopy, ultrasonography and computed tomography in the staging of gastric cancer. Br J Surg 1996;83:1260–1262.PubMedCrossRefGoogle Scholar
  58. 58.
    Perng DS, Jan CM, Wang WM, Chen LT, Su YC, Liu GC, et al. Computed tomography, endoscopic ultrasonography and intraoperative assessment in TN staging of gastric carcinoma. J Formos Med Assoc 1996;95:378–385.PubMedGoogle Scholar
  59. 59.
    Greenberg J, Durkin M, Van Drunen M, Aranha GV. Computed tomography or endoscopic ultrasonography in preoperative staging of gastric and esophageal tumors. Surgery 1994;116:696–701.PubMedGoogle Scholar
  60. 60.
    Smith JW, Brennan MF, Botet JF, Gerdes H, Lightdale CJ. Preoperative endoscopic ultrasound can predict the risk of recurrence after operation for gastric carcinoma. J Clin Oncol 1993;11:2380–2385.PubMedGoogle Scholar
  61. 61.
    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;34:604–610.PubMedCrossRefGoogle Scholar
  62. 62.
    Grimm H, Binmoeller KF, Hamper K, Koch J, Henne-Bruns D, Soehendra N. Endosonography for preoperative locoregional staging of esophageal and gastric cancer. Endoscopy 1993;25:224–230.PubMedCrossRefGoogle Scholar
  63. 63.
    Dittler HJ, Siewert JR. Role of endoscopic ultrasonography in gastric carcinoma. Endoscopy 1993;25:162–166.PubMedCrossRefGoogle Scholar
  64. 64.
    Botet JF, Lightdale CJ, Zauber AG, Gerdes H, Winawer SJ, Urmacher C, et al. Preoperative staging of gastric cancer: comparison of endoscopic US and dynamic CT. Radiology 1991;181:426–432.PubMedGoogle Scholar
  65. 65.
    Tio TL, Coene PP, Luiken GJ, Tytgat GN. Endosonography in the clinical staging of esophagogastric carcinoma. Gastrointest Endosc 1990;36(Suppl 2):2–10.CrossRefGoogle Scholar
  66. 66.
    Mönig SP, Zirbes TK, Schröder W, Baldus SE, Lindemann DG, Dienes HP, et al. Staging of gastric cancer: correlation of lymph node size and metastatic infiltration. AJR Am J Roentgenol 1999;173:365–367.PubMedGoogle Scholar
  67. 67.
    Will O, Purkayastha S, Chan C, Athanasiou T, Darzi AW, Gedroyc W, et al. Diagnostic precision of nanoparticle-enhanced MRI for lymph-node metastases: a meta-analysis. Lancet Oncol 2006;7:52–60.PubMedCrossRefGoogle Scholar
  68. 68.
    Tatsumi Y, Tanigawa N, Nishimura H, Nomura E, Mabuchi H, Matsuki M, et al. Preoperative diagnosis of lymph node metastases in gastric cancer by magnetic resonance imaging with ferumoxtran-10. Gastric Cancer 2006;9:120–128.PubMedCrossRefGoogle Scholar
  69. 69.
    Herborn CU, Lauenstein TC, Vogt FM, Lauffer RB, Debatin JF, Ruehm SG. Interstitial MR lymphography with MS-325: characterization of normal and tumor-invaded lymph nodes in a rabbit model. AJR Am J Roentgenol 2002;179:1567–1572.PubMedGoogle Scholar
  70. 70.
    Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 2007;188:1622–1635.PubMedCrossRefGoogle Scholar
  71. 71.
    Rohren EM, Turkington TG, Coleman RE. Clinical applications of PET in oncology. Radiology 2004;231:305–332.PubMedCrossRefGoogle Scholar
  72. 72.
    Stahl A, Ott K, Weber WA, Becker K, Link T, Siewert JR, et al. FDG PET imaging of locally advanced gastric carcinomas: correlation with endoscopic and histopathological findings. Eur J Nucl Med Mol Imaging 2003;30:288–295.PubMedGoogle Scholar
  73. 73.
    Koga H, Sasaki M, Kuwabara Y, Hiraka K, Nakagawa M, Abe K, et al. An analysis of the physiological FDG uptake pattern in the stomach. Ann Nucl Med 2003;17:733–738.PubMedCrossRefGoogle Scholar
  74. 74.
    von Schulthess GK, Steinert HC, Hany TF. Integrated PET/CT: current applications and future directions. Radiology 2006;238:405–422.CrossRefGoogle Scholar
  75. 75.
    Mullani NA, Mawlawi O. Why is the resolution of the Discovery PET/CT camera so poor? J Nucl Med 2005;46:898; author reply 898.PubMedGoogle Scholar
  76. 76.
    Hiratsuka M, Miyashiro I, Ishikawa O, Furukawa H, Motomura K, Ohigashi H, et al. Application of sentinel node biopsy to gastric cancer surgery. Surgery 2001;129:335–340.PubMedCrossRefGoogle Scholar
  77. 77.
    Tonouchi H, Mohri Y, Tanaka K, Konishi N, Ohmori Y, Kobayashi M, et al. Lymphatic mapping and sentinel node biopsy during laparoscopic gastrectomy for early cancer. Dig Surg 2003;20:421–427.PubMedCrossRefGoogle Scholar
  78. 78.
    Song X, Wang L, Chen W, Pan T, Zhu H, Xu J, et al. Lymphatic mapping and sentinel node biopsy in gastric cancer. Am J Surg 2004;187:270–273.PubMedCrossRefGoogle Scholar
  79. 79.
    Mura G, Vagliasindi A, Framarini M, Mazza P, Solfrini G, Verdecchia GM. The sentinel node biopsy in early gastric cancer: a preliminary study. Langenbecks Arch Surg 2006;391:113–117.PubMedCrossRefGoogle Scholar
  80. 80.
    Kitagawa Y, Fujii H, Kumai K, Kubota T, Otani Y, Saikawa Y, et al. Recent advances in sentinel node navigation for gastric cancer: a paradigm shift of surgical management. J Surg Oncol 2005;90:147–151.PubMedCrossRefGoogle Scholar

Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2009

Authors and Affiliations

  • Robert Michael Kwee
    • 1
  • Thomas Christian Kwee
    • 2
  1. 1.Department of RadiologyMaastricht University Medical CenterMaastrichtThe Netherlands
  2. 2.Department of RadiologyUniversity Medical Center UtrechtUtrechtThe Netherlands

Personalised recommendations