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Ultraschall Med 2012; 33(7): E218-E224
DOI: 10.1055/s-0032-1312958
Original Article
© Georg Thieme Verlag KG Stuttgart · New York

Preoperative T Staging of Advanced Gastric Cancer using Double Contrast-Enhanced Ultrasound

Präoperatives T-Staging bei fortgeschrittenem Magenkarzinom mittels doppelt-kontrastverstärkter Sonografie
S. Li
1   Department of Diagnostic Ultrasound and Echocardiography, Sir Run Run Shaw Hospital, Zhejiang University College of Medicine
,
P. Huang
2   Department of Ultrasonography, the 2nd Affiliated Hospital Zhejiang University College of Medicine
,
Z. Wang
3   Department of Pathology, the 2nd Affiliated Hospital of Wenzhou Medical College
,
J. Chen
4   Department of General Surgery, the 2nd Affiliated Hospital Zhejiang University College of Medicine
,
H. Xu
1   Department of Diagnostic Ultrasound and Echocardiography, Sir Run Run Shaw Hospital, Zhejiang University College of Medicine
,
L. Wang
5   Department of Ultrasonography, the 2nd Affiliated Hospital of Wenzhou Medical College
,
Y. Zhang
2   Department of Ultrasonography, the 2nd Affiliated Hospital Zhejiang University College of Medicine
,
G. Mo
2   Department of Ultrasonography, the 2nd Affiliated Hospital Zhejiang University College of Medicine
,
J. Zhu
2   Department of Ultrasonography, the 2nd Affiliated Hospital Zhejiang University College of Medicine
,
D. Cosgrove
6   Imaging Sciences Department, Imperial College, Hammersmith Hospital
› Author Affiliations
Further Information

Publication History

07 January 2012

17 May 2012

Publication Date:
28 June 2012 (online)

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Abstract

Purpose: To determine the accuracy of double contrast-enhanced ultrasound (DCEUS), in which intravenous microbubbles are used together with an oral contrast agent, in the preoperative T staging of advanced gastric cancer.

Materials and Methods: This prospective, ethics committee-approved study recruited 350 patients who gave informed consent. All had gastric cancer proved by endoscopic biopsy and underwent preoperative ultrasound staging using the TNM classification (UICC 2002). The results of DCEUS were compared with postoperative pathologic findings. The staging accuracy of oral contrast-enhanced ultrasound (OCEUS) and DCEUS were compared to each other. Sensitivity and specificity for assessing serosal involvement by DCEUS were evaluated, and the concordance of this method was analyzed using Kappa statistics.

Results: The accuracies of OCEUS and DCEUS in determining the T stage of advanced gastric cancer were 75.1 % (70.4 % for T2, 79.5 % for T3, 68.1 % for T4) and 87.4 % (83.3 % for T2, 89.7 % for T3, 87.2 % for T4), respectively, and the difference between the two methods was statistically significant (χ2 = 17.364, p< 0.001). The performance of DCEUS for staging lesions in the cardia (69.81 %), fundus (85.71 %) and body (85.56 %) had lower accuracy than that of other parts (93.94 % for antrum; 92.11 % for pylorus). Sensitivity and specificity for assessing serosal involvement by DCEUS were 98.76 % and 83.33 % respectively. The reliability was almost perfect with Kappa values of 0.89 (p< 0.001) for intra-observer and 0.82 (p< 0.001) for inter-observer agreement.

Conclusion: DCEUS could be considered as an accurate, non-invasive, and reliable diagnostic method for preoperative staging of advanced gastric cancer.

Zusammenfassung

Ziel: Bestimmung der Genauigkeit des doppelt-kontrastverstärkten Ultraschalls (DCEUS) unter Verwendung von intravenös verabreichten Mikrobläschen zusammen mit einem oralen Kontrastmittel beim präoperativen T-Staging des fortgeschrittenen Magenkarzinoms.

Material und Methoden: In diese prospektive, von der Ethikkommission anerkannte Studie wurden 350 Patienten nach Abgabe der Einverständniserklärung aufgenommen. Alle hatten ein durch eine endoskopische Biopsie bestätigtes Magenkarzinom und unterzogen sich der präoperativen Stadieneinteilung unter Verwendung der TNM-Klassifikation (UICC 2002). Die DCEUS-Befunde wurden mit den postoperativen pathologischen Befunden verglichen. Die Genauigkeit des Stagings mittels oralen kontrastverstärkten Ultraschalls (OCEUS) und DCEUS wurden miteinander verglichen. Die Sensitivität und Spezifität des DCEUS im Hinblick auf die Beurteilung der Beteiligung der Serosa wurde ermittelt und die Übereinstimmung dieser Methode mittels Kappa-Statistik analysiert.

Ergebnisse: Für die Bestimmung der T-Stadien bei fortgeschrittenem Magenkarzinom betrug die Genauigkeit von OCEUS 75,1 % (70,4 % für T2, 79,5 % für T3, 68,1 % für T4), die von DCEUS 87,4 % (83,3 % für T2, 89,7 % für T3, 87,2 % für T4) und der Unterschied zwischen beiden Methoden war statistisch signifikant (χ2 = 17,364, p< 0,001). Die Durchführung von DCEUS beim Staging zeigte bei Läsionen im Bereich des Mageneingangs (69,81 %), des Fundus (85,71 %) und des Corpus (85,56 %) im Vergleich zu anderen Bereichen des Magens (93,94 % für das Antrum; 92,11 % für den Pylorus) eine geringere Genauigkeit. In Bezug auf die Abschätzung der Beteiligung der Serosa betrug die Sensitivität von DCEUS 98,76 % und dessen Spezifität 83,33 %. Die Reliabilität war bei einem Kappa-Wert von 0,89 (p< 0,001) für die Intraobserver- und von 0,82 (p< 0,001) für Interobserver-Übereinstimmung beinahe perfekt.

Schlussfolgerung: DCEUS kann als treffsichere, nicht invasive und verlässliche Diagnostik bei der präoperativen Stadieneinteilung bei fortgeschrittenem Magenkarzinom in Betracht gezogen werden.

Key words

stomach - ultrasound - tumor staging - CEUS
 

  • References

  • 1 Boring CC, Squires TS, Tong T. Cancer statistics, 1991. CA Cancer J Clin 1991; 41: 19-36
    CrossrefPubMedSearch in Google Scholar
  • 2 Sun XD, Mu R, Zhou YS et al. Analysis of mortality rate of stomach cancer and its trend in twenty years in China. Zhonghua Zhong Liu Za Zhi 2004; 26: 4-9
    PubMedSearch in Google Scholar
  • 3 Tenderenda M, Rutkowski P, Jesionek-Kupnicka D et al. Expression of CD34 in gastric cancer and its correlation with histology, stage, proliferation activity, p53 expression and apoptotic index. Pathol Oncol Res 2001; 7: 129-134
    CrossrefPubMedSearch in Google Scholar
  • 4 Kumano S, Murakami T, Kim T et al. T staging of gastric cancer: role of multi-detector row CT. Radiology 2005; 237: 961-966
    CrossrefPubMedSearch in Google Scholar
  • 5 Lee MH, Choi D, Park MJ et al. Gastric cancer: Imaging and staging with MDCT based on the 7th AJCC guidelines. Abdom Imaging 2011;
    PubMedSearch in Google Scholar
  • 6 Brenner DJ, Doll R, Goodhead DT et al. Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci USA 2003; 100: 13761-13766
    CrossrefPubMedSearch in Google Scholar
  • 7 Mocellin S, Marchet A, Nitti D. EUS for the staging of gastric cancer: a meta-analysis. Gastrointest Endosc 2011; 73: 1122-1134
    CrossrefPubMedSearch in Google Scholar
  • 8 Bösing N, Schumacher B, Frieling T et al. Endoscopic ultrasound in routine clinical practice for staging adenocarcinomas of the stomach and distal esophagus. Chirurg 2003; 74: 214-221 ; discussion 222-223
    CrossrefPubMedSearch in Google Scholar
  • 9 Jenssen C, Dietrich CF, Burmester E. Malignant neoplasias of the gastrointestinal tract – endosonographic staging revisited. Z Gastroenterol 2011; 49: 357-368
    Thieme ConnectPubMedSearch in Google Scholar
  • 10 Nuernberg D, Ignee A, Dietrich CF. Current status of ultrasound in gastroenterology – bowel and upper gastrointestinal tract – part 1. Z Gastroenterol 2007; 45: 629-640
    Thieme ConnectPubMedSearch in Google Scholar
  • 11 Iordache S, Saftoiu A, Georgescu CV et al. Vascular endothelial growth factor expression and microvessel density – two useful tools for the assessment of prognosis and survival in gastric cancer patients. J Gastrointestin Liver Dis 2010; 19: 135-139
    PubMedSearch in Google Scholar
  • 12 Laitakari J, Näyhä V, Stenbäck F. Size, shape, structure, and direction of angiogenesis in laryngeal tumour development. J Clin Pathol 2004; 57: 394-401
    CrossrefPubMedSearch in Google Scholar
  • 13 Lassau N, Lamuraglia M, Leclère J et al. Functional and early evaluation of treatments in oncology: interest of ultrasonographic contrast agents. J Radiol 2004; 85: 704-712
    CrossrefPubMedSearch in Google Scholar
  • 14 Shiyan L, Pintong H, Zongmin W et al. The relationship between enhanced intensity and microvessel density of gastric carcinoma using double contrast-enhanced ultrasonography. Ultrasound Med Biol 2009; 35: 1086-1091
    CrossrefPubMedSearch in Google Scholar
  • 15 Phillips P, Gardner E. Contrast-agent detection and quantification. Eur Radiol 2004; 14: P4-P10
    CrossrefPubMedSearch in Google Scholar
  • 16 Lutz H, Bauer U, Stolte M. Ultrasound diagnosis of the stomach wall – experimental studies. Ultraschall in Med 1986; 7: 255-258
    Thieme ConnectPubMedSearch in Google Scholar
  • 17 Akahoshi K, Misawa T, Fujishima H et al. Preoperative evaluation of gastric cancer by endoscopic ultrasound. Gut 1991; 32: 479-482
    CrossrefPubMedSearch in Google Scholar
  • 18 Kim IY, Kim SW, Shin HC et al. MRI of gastric carcinoma: results of T and N-staging in an in vitro study. World J Gastroenterol 2009; 15: 3992-3998
    CrossrefPubMedSearch in Google Scholar
  • 19 Sobin LH, Wittekind C. TNM classification of malignant tumours (UICC International Union Against Cancer). 6th ed. New York: Wiley-Liss; 2002
    Search in Google Scholar
  • 20 Japanese Research Society for Gastric Cancer. The general rules for the gastric cancer study in surgery ad pathology. Part II. Histological classification of gastric cancer. Jpn J Surg 1981; 11: 140-145
    CrossrefPubMedSearch in Google Scholar
  • 21 Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 1977; 33: 363-374
    CrossrefPubMedSearch in Google Scholar
  • 22 Worlicek H. Sonographic diagnosis of the fluid-filled stomach. Ultraschall in Med 1986; 7: 259-263
    Thieme ConnectPubMedSearch in Google Scholar
  • 23 Piscaglia F, Nolsøe C, Dietrich CF et al. The EFSUMB Guidelines and Recommendations on the Clinical Practice of Contrast Enhanced Ultrasound (CEUS): Update 2011 on non-hepatic applications. Ultraschall in Med 2011; DOI
    PubMedSearch in Google Scholar
  • 24 Abbas SM, Booth MW. Correlation between the current TNM staging and long-term survival after curative D1 lymphadenectomy for stomach cancer. Langenbecks Arch Surg 2005; 390: 294-299
    CrossrefPubMedSearch in Google Scholar
  • 25 Botet JF, Lightdale CJ, Zauber AG et al. Preoperative staging of gastric cancer: comparison of endoscopic US and dynamic CT. Radiology 1991; 181: 426-432
    PubMedSearch in Google Scholar
  • 26 Segura JM, Olveira A, Conde P et al. Hydrogastric sonography in the preoperative staging of gastric cancer. J Clin Ultrasound 1999; 27: 499-504
    CrossrefPubMedSearch in Google Scholar
  • 27 Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-1186
    CrossrefPubMedSearch in Google Scholar
  • 28 Zheng Z, Yu Y, Lu M et al. Double contrast-enhanced ultrasonography for the preoperative evaluation of gastric cancer: a comparison to endoscopic ultrasonography with respect to histopathology. Am J Surg 2011; 202: 605-611
    CrossrefPubMedSearch in Google Scholar
  • 29 Hwang SW, Lee DH, Lee SH et al. Preoperative staging of gastric cancer by endoscopic ultrasonography and multidetector-row computed tomography. J Gastroenterol Hepatol 2010; 25: 512-518
    CrossrefPubMedSearch in Google Scholar
  • 30 Setälä LP, Kosma VM, Marin S et al. Prognostic factors in gastric cancer: the value of vascular invasion, mitotic rate and lymphoplasmacytic infiltration. Br J Cancer 1996; 74: 766-772
    CrossrefPubMedSearch in Google Scholar
  • 31 Ludeman L, Shepherd NA. Serosal involvement in gastrointestinal cancer: its assessment and significance. Histopathology 2005; 47: 123-131
    CrossrefPubMedSearch in Google Scholar
  • 32 Takiguchi N, Nunomura M, Koda K et al. Neoadjuvant chemotherapy with CDDP and 5-fluorouracil for gastric cancer with serosal invasion. Oncol Rep 2003; 10: 433-438
    PubMedSearch in Google Scholar
  • 33 Sobin L, Gospodarowicz M, Wittekind C. TNM classification of malignant tumours (UICC International Union Against Cancer). 7th ed. New York: Wiley-Blackwell; 2009
    Search in Google Scholar