Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

Dynamic Contrast-Enhanced Ultrasound of Gastric Cancer: Correlation with Perfusion CT and Histopathology

  • Ijin Joo (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Se Hyung Kim (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Dong Ho Lee (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Joon Koo Han (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine)
  • Received : 2018.04.27
  • Accepted : 2018.12.10
  • Published : 2019.05.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: To assess the relationship between contrast-enhanced ultrasound (CEUS) parameters and perfusion CT (PCT) parameters of gastric cancers and their correlation with histologic features. Materials and Methods: This prospective study was approved by our Institutional Review Board. We included 43 patients with pathologically-proven gastric cancers undergoing CEUS using SonoVue® (Bracco) and PCT on the same day. Correlation between the CEUS parameters (peak intensity [PI], area under the curve [AUC], rise time [RT] from 10% to 90% of PI, time to peak [TTPUS], and mean transit time [MTTUS]) and PCT parameters (blood flow, blood volume, TTPCT, MTTCT, and permeability surface product) of gastric cancers were analyzed using Spearman's rank correlation test. In cases of surgical resection, the CEUS and PCT parameters were compared according to histologic features using Mann-Whitney test. Results: CEUS studies were of diagnostic quality in 88.4% (38/43) of patients. Among the CEUS parameters of gastric cancers, RT and TTPUS showed significant positive correlations with TTPCT (rho = 0.327 and 0.374, p = 0.045 and 0.021, respectively); PI and AUC were significantly higher in well-differentiated or moderately-differentiated tumors (n = 4) than poorly-differentiated tumors (n = 18) (p = 0.026 and 0.033, respectively), whereas MTTCT showed significant differences according to histologic types (poorly cohesive carcinoma [PCC] vs. non-PCC), T-staging (≤ T2 vs. ≥ T3), N-staging (N0 vs. N-positive), and epidermal growth factor receptor expression (≤ faint vs. ≥ moderate staining) (p values < 0.05). Conclusion: In patients with gastric cancers, CEUS is technically feasible for the quantification of tumor perfusion and may provide correlative and complementary information to that of PCT, which may allow prediction of histologic features.

Keywords

Acknowledgement

We thank Chris Woo, BA, for his assistance in editing the manuscript.

References

  1. Soerjomataram I, Lortet-Tieulent J, Parkin DM, Ferlay J, Mathers C, Forman D, et al. Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. Lancet 2012;380:1840-1850  https://doi.org/10.1016/S0140-6736(12)60919-2
  2. 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:vi120-vi123  https://doi.org/10.1093/annonc/mdm239
  3. Shah MA, Ajani JA. Gastric cancer--an enigmatic and heterogeneous disease. JAMA 2010;303:1753-1754  https://doi.org/10.1001/jama.2010.553
  4. Garcia-Figueiras R, Goh VJ, Padhani AR, Baleato-Gonzalez S, Garrido M, Leon L, et al. CT perfusion in oncologic imaging: a useful tool? AJR Am J Roentgenol 2013;200:8-19  https://doi.org/10.2214/AJR.11.8476
  5. Padhani AR. Dynamic contrast-enhanced MRI in clinical oncology: current status and future directions. J Magn Reson Imaging 2002;16:407-422  https://doi.org/10.1002/jmri.10176
  6. Kim SH, Kamaya A, Willmann JK. CT perfusion of the liver: principles and applications in oncology. Radiology 2014;272:322-344  https://doi.org/10.1148/radiol.14130091
  7. O'Connor JP, Jackson A, Parker GJ, Roberts C, Jayson GC. Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies. Nat Rev Clin Oncol 2012;9:167-177  https://doi.org/10.1038/nrclinonc.2012.2
  8. Frohlich E, Muller R, Cui XW, Schreiber-Dietrich D, Dietrich CF. Dynamic contrast-enhanced ultrasound for quantification of tissue perfusion. J Ultrasound Med 2015;34:179-196  https://doi.org/10.7863/ultra.34.2.179
  9. Jahng GH, Li KL, Ostergaard L, Calamante F. Perfusion magnetic resonance imaging: a comprehensive update on principles and techniques. Korean J Radiol 2014;15:554-577  https://doi.org/10.3348/kjr.2014.15.5.554
  10. Lu Q, Huang BJ, Wang WP, Li CX, Xue LY. Qualitative and quantitative analysis with contrast-enhanced ultrasonography: diagnosis value in hypoechoic renal angiomyolipoma. Korean J Radiol 2015;16:334-341  https://doi.org/10.3348/kjr.2015.16.2.334
  11. Lv WF, Han JK, Cheng DL, Zhou CZ, Ni M, Lu D. CT perfusion imaging can predict patients' survival and early response to transarterial chemo-lipiodol infusion for liver metastases from colorectal cancers. Korean J Radiol 2015;16:810-820  https://doi.org/10.3348/kjr.2015.16.4.810
  12. Zhang H, Pan Z, Du L, Yan C, Ding B, Song Q, et al. Advanced gastric cancer and perfusion imaging using a multidetector row computed tomography: correlation with prognostic determinants. Korean J Radiol 2008;9:119-127  https://doi.org/10.3348/kjr.2008.9.2.119
  13. Lee DH, Kim SH, Im SA, Oh DY, Kim TY, Han JK. Multiparametric fully-integrated 18-FDG PET/MRI of advanced gastric cancer for prediction of chemotherapy response: a preliminary study. Eur Radiol 2016;26:2771-2778  https://doi.org/10.1007/s00330-015-4105-5
  14. Joo I, Lee JM, Han JK, Yang HK, Lee HJ, Choi BI. Dynamic contrast-enhanced MRI of gastric cancer: correlation of the perfusion parameters with pathological prognostic factors. J Magn Reson Imaging 2015;41:1608-1614  https://doi.org/10.1002/jmri.24711
  15. Li T, Lu M, Song J, Wu P, Cheng X, Zhang Z. Improvement to ultrasonographical differential diagnosis of gastric lesions: the value of contrast enhanced sonography with gastric distention. PLoS One 2017;12:e0182332 
  16. Xue H, Ge HY, Miao LY, Wang SM, Zhao B, Wang JR, et al. Differential diagnosis of gastric cancer and gastritis: the role of contrast-enhanced ultrasound (CEUS). Abdom Radiol (NY) 2017;42:802-809  https://doi.org/10.1007/s00261-016-0952-z
  17. Yan C, Bao X, Shentu W, Chen J, Liu C, Ye Q, et al. Preoperative gross classification of gastric adenocarcinoma: comparison of double contrast-enhanced ultrasound and multi-detector row CT. Ultrasound Med Biol 2016;42:1431-1440  https://doi.org/10.1016/j.ultrasmedbio.2016.01.030
  18. 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 Med 2012;33:E218-E224  https://doi.org/10.1055/s-0032-1312958
  19. Tranquart F, Mercier L, Frinking P, Gaud E, Arditi M. Perfusion quantification in contrast-enhanced ultrasound (CEUS)--ready for research projects and routine clinical use. Ultraschall Med 2012;33 Suppl 1:S31-S38  https://doi.org/10.1055/s-0032-1312894
  20. Shiyan L, Pintong H, Zongmin W, Fuguang H, Zhiqiang Z, Yan Y, 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  https://doi.org/10.1016/j.ultrasmedbio.2009.03.010
  21. Ang J, Hu L, Huang PT, Wu JX, Huang LN, Cao CH, et al. Contrast-enhanced ultrasonography assessment of gastric cancer response to neoadjuvant chemotherapy. World J Gastroenterol 2012;18:7026-7032  https://doi.org/10.3748/wjg.v18.i47.7026
  22. Ranganath PG, Robbin ML, Back SJ, Grant EG, Fetzer DT. Practical advantages of contrast-enhanced ultrasound in abdominopelvic radiology. Abdom Radiol (NY) 2018;43:998-1012  https://doi.org/10.1007/s00261-017-1442-7
  23. Lee DH, Kim SH, Joo I, Han JK. CT Perfusion evaluation of gastric cancer: correlation with histologic type. Eur Radiol 2018;28:487-495  https://doi.org/10.1007/s00330-017-4979-5
  24. Jang JY, Kim MY, Jeong SW, Kim TY, Kim SU, Lee SH, et al. Current consensus and guidelines of contrast enhanced ultrasound for the characterization of focal liver lesions. Clin Mol Hepatol 2013;19:1-16  https://doi.org/10.3350/cmh.2013.19.1.1
  25. Zongqiong S, Xiaohong L, Wei C, Jiangfeng Z, Yuxi G, Zhihui X, et al. CT perfusion imaging of the stomach: a quantitative analysis according to different degrees of adenocarcinoma cell differentiation. Clin Imaging 2016;40:558-562  https://doi.org/10.1016/j.clinimag.2015.11.006
  26. Lang SA, Moser C, Gehmert S, Pfister K, Hackl C, Schnitzbauer AA, et al. Contrast-enhanced ultrasound (CEUS) detects effects of vascular disrupting therapy in an experimental model of gastric cancer. Clin Hemorheol Microcirc 2014;56:287-299  https://doi.org/10.3233/CH-121658
  27. Goetti R, Reiner CS, Knuth A, Klotz E, Stenner F, Samaras P, et al. Quantitative perfusion analysis of malignant liver tumors: dynamic computed tomography and contrast-enhanced ultrasound. Invest Radiol 2012;47:18-24  https://doi.org/10.1097/RLI.0b013e318229ff0d
  28. Meijerink MR, van Waesberghe JH, van Schaik C, Boven E, van der Veldt AA, van den Tol P, et al. Perfusion CT and US of colorectal cancer liver metastases: a correlative study of two dynamic imaging modalities. Ultrasound Med Biol 2010;36:1626-1636  https://doi.org/10.1016/j.ultrasmedbio.2010.06.015
  29. Zhou JH, Zheng W, Cao LH, Liu M, Luo RZ, Han F, et al. Quantitative evaluation of viable tissue perfusion changes with contrast-enhanced greyscale ultrasound in a mouse hepatoma model following treatment with different doses of thalidomide. Br J Radiol 2011;84:826-832  https://doi.org/10.1259/bjr/14335925
  30. Zhuang H, Yang ZG, Chen HJ, Peng YL, Li L. Time-intensity curve parameters in colorectal tumours measured using double contrast-enhanced ultrasound: correlations with tumour angiogenesis. Colorectal Dis 2012;14:181-187  https://doi.org/10.1111/j.1463-1318.2011.02546.x
  31. Wang J, Lv F, Fei X, Cui Q, Wang L, Gao X, et al. Study on the characteristics of contrast-enhanced ultrasound and its utility in assessing the microvessel density in ovarian tumors or tumor-like lesions. Int J Biol Sci 2011;7:600-606  https://doi.org/10.7150/ijbs.7.600
  32. Yang JC, Tang J, Li Y, Fei X, Shi H. Contrast-enhanced transrectal ultrasound for assessing vascularization of hypoechoic BPH nodules in the transition and peripheral zones: comparison with pathological examination. Ultrasound Med Biol 2008;34:1758-1764  https://doi.org/10.1016/j.ultrasmedbio.2008.04.009
  33. Kawamura M, Naganuma H, Shibuya R, Kikuchi T, Sakai Y, Nagasaki F, et al. Analysis of microvascular density in early gastric carcinoma using magnifying endoscopy with narrow-band imaging. Endosc Int Open 2016;4:E832-E837  https://doi.org/10.1055/s-0042-110095
  34. Satoh A, Shuto K, Okazumi S, Ohira G, Natsume T, Hayano K, et al. Role of perfusion CT in assessing tumor blood flow and malignancy level of gastric cancer. Dig Surg 2010;27:253-260  https://doi.org/10.1159/000288703
  35. Tenderenda M, Rutkowski P, Jesionek-Kupnicka D, Kubiak R. 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 https://doi.org/10.1007/BF03032579