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Differentiating malignant from benign thrombosis in hepatocellular carcinoma: contrast-enhanced ultrasound

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Abstract

Background

To determine the accuracy of contrast-enhanced ultrasonography (CEUS) in differentiating malignant and benign venous thrombosis complicating hepatocellular carcinoma (HCC).

Methods

Fifty patients (M:F = 41:9; age range 46–83 years) with HCC and venous thrombosis [portal vein (PV) in 45 and hepatic vein (HV) in 5] detected on CT or MR scan were evaluated with CEUS. Reference standard of malignant and benign thrombosis was based on serial clinicoradiologic follow-up (n = 43) or pathology (n = 7). Two independent, blinded readers retrospectively recorded the enhancement features of the venous thrombosis and diagnosed as benign or malignant thrombosis with a five-point confidence scale. Receiver operating characteristic (ROC) curves were calculated to determine the diagnostic performance of CEUS in differentiating malignant from benign thrombosis. Confidence level ratings were also used to calculate the sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) for the diagnosis of malignant thrombosis. Inter-reader agreement was calculated using κ statistics in each assessed finding. Gray scale and Doppler characteristics of primary tumor and thrombosis were also assessed.

Results

Of the 50 patients, 37 were malignant (33 with PV thrombosis and 4 with HV thrombosis) and 13 were benign (12 with PV thrombosis and 1 with HV thrombosis). In ROC curve analysis for differentiating malignant from benign thrombosis, Az was 0.947 (CI 0.841–0.991) for reader 1 and 0.958 (CI 0.861–0.995) for reader 2 with excellent inter-reader agreement (κ = 0.86). When the confidence level ratings of 1 or 2 were considered malignant thrombosis, the sensitivity, specificity, PPV, and NPV in differentiating malignant from benign thrombosis were 100%, 83%, 95%, and 100% for reader 1 and 100%, 92%, 97%, and 100% for reader 2.

Conclusion

CEUS is useful to differentiate malignant and benign venous thrombosis associated with HCC with high diagnostic accuracy.

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References

  1. Pirisi M, Avellini C, Fabris C, et al. (1998) Portal vein thrombosis in hepatocellular carcinoma: age and sex distribution in an autopsy study. J Cancer Res Clin Oncol 124(7):397–400. doi:10.1007/s004320050189

    Article  CAS  PubMed  Google Scholar 

  2. Pawarode A, Voravud N, Sriuranpong V, Kullavanijaya P, Patt YZ (1998) Natural history of untreated primary hepatocellular carcinoma: a retrospective study of 157 patients. Am J Clin Oncol 21(4):386–391

    Article  CAS  PubMed  Google Scholar 

  3. Takizawa D, Kakizaki S, Sohara N, et al. (2007) Hepatocellular carcinoma with portal vein tumor thrombosis: clinical characteristics, prognosis, and patient survival analysis. Dig Dis Sci 52(11):3290–3295. doi:10.1007/s10620-007-9808-2

    Article  PubMed  Google Scholar 

  4. Sakata J, Shirai Y, Wakai T, et al. (2008) Preoperative predictors of vascular invasion in hepatocellular carcinoma. Eur J Surg Oncol (EJSO) 34(8):900–905. doi:10.1016/j.ejso.2008.01.031

    Article  CAS  Google Scholar 

  5. Ogren M, Bergqvist D, Bjorck M, et al. (2006) Portal vein thrombosis: prevalence, patient characteristics and lifetime risk: a population study based on 23,796 consecutive autopsies. World J Gastroenterol 12(13):2115–2119

    PubMed  Google Scholar 

  6. Francoz C, Valla D, Durand F (2012) Portal vein thrombosis, cirrhosis, and liver transplantation. J Hepatol 57(1):203–212. doi:10.1016/j.jhep.2011.12.034

    Article  PubMed  Google Scholar 

  7. Sotiropoulos G, Radtke A, Schmitz K, et al. (2008) Liver transplantation in the setting of hepatocellular carcinoma and portal vein thrombosis: a challenging dilemma? Dig Dis Sci 53(7):1994–1999. doi:10.1007/s10620-007-0099-4

    Article  PubMed  Google Scholar 

  8. Lim JH, Auh YH (1992) Hepatocellular carcinoma presenting only as portal venous tumor thrombosis: CT demonstration. J Comput Assist Tomogr 16(1):103–106

    Article  CAS  PubMed  Google Scholar 

  9. Tanaka K, Numata K, Okazaki H, et al. (1993) Diagnosis of portal vein thrombosis in patients with hepatocellular carcinoma: efficacy of color Doppler sonography compared with angiography. AJR Am J Roentgenol 160(6):1279–1283

    Article  CAS  PubMed  Google Scholar 

  10. Van Gansbeke D, Avni EF, Delcour C, Engelholm L, Struyven J (1985) Sonographic features of portal vein thrombosis. AJR Am J Roentgenol 144(4):749–752

    Article  PubMed  Google Scholar 

  11. Dodd GD 3rd, Memel DS, Baron RL, Eichner L, Santiguida LA (1995) Portal vein thrombosis in patients with cirrhosis: does sonographic detection of intrathrombus flow allow differentiation of benign and malignant thrombus? AJR Am J Roentgenol 165(3):573–577

    Article  PubMed  Google Scholar 

  12. Ricci P, Cantisani V, Biancari F, et al. (2000) Contrast-enhanced color Doppler US in malignant portal vein thrombosis. Acta Radiol 41(5):470–473

    CAS  PubMed  Google Scholar 

  13. Tublin ME, Dodd GD, Baron RL (1997) Benign and malignant portal vein thrombosis: differentiation by CT characteristics. ARJ Am J Roentgenol 168(3):719–723

    Article  CAS  Google Scholar 

  14. Levy HM, Newhouse JH (1988) MR imaging of portal vein thrombosis. AJR Am J Roentgenol 151(2):283–286

    Article  CAS  PubMed  Google Scholar 

  15. Zirinsky K, Markisz JA, Rubenstein WA, et al. (1988) MR imaging of portal venous thrombosis: correlation with CT and sonography. AJR Am J Roentgenol 150(2):283–288

    Article  CAS  PubMed  Google Scholar 

  16. Okumura A, Watanabe Y, Dohke M, et al. (1999) Contrast-enhanced three-dimensional MR portography. Radiographics 19(4):973–987

    Article  CAS  PubMed  Google Scholar 

  17. Rossi S, Rosa L, Ravetta V, et al. (2006) Contrast-enhanced versus conventional and color Doppler sonography for the detection of thrombosis of the portal and hepatic venous systems. AJR Am J Roentgenol 186(3):763–773. doi:10.2214/AJR.04.1218

    Article  PubMed  Google Scholar 

  18. Rossi S, Ghittoni G, Ravetta V, et al. (2008) Contrast-enhanced ultrasonography and spiral computed tomography in the detection and characterization of portal vein thrombosis complicating hepatocellular carcinoma. Eur Radiol 18(8):1749–1756. doi:10.1007/s00330-008-0931-z

    Article  PubMed  Google Scholar 

  19. Sorrentino P, D’Angelo S, Tarantino L, et al. (2009) Contrast-enhanced sonography versus biopsy for the differential diagnosis of thrombosis in hepatocellular carcinoma patients. World J Gastroenterol 15(18):2245–2251

    Article  PubMed  Google Scholar 

  20. Song ZZ, Huang M, Jiang TA, et al. (2010) Diagnosis of portal vein thrombosis discontinued with liver tumors in patients with liver cirrhosis and tumors by contrast-enhanced US: a pilot study. Eur J Radiol 75(2):185–188. doi:10.1016/j.ejrad.2009.04.021

    Article  PubMed  Google Scholar 

  21. Piscaglia F, Gianstefani A, Ravaioli M, et al. (2010) Criteria for diagnosing benign portal vein thrombosis in the assessment of patients with cirrhosis and hepatocellular carcinoma for liver transplantation. Liver Transpl 16(5):658–667. doi:10.1002/lt.22044

    PubMed  Google Scholar 

  22. Obuchowski NA (2005) ROC analysis. AJR Am J Roentgenol 184(2):364–372

    Article  PubMed  Google Scholar 

  23. Cicchetti DV, Sparrow SA (1981) Developing criteria for establishing interrater reliability of specific items: applications to assessment of adaptive behavior. Am J Ment Defic 86(2):127–137

    CAS  PubMed  Google Scholar 

  24. Minagawa M, Makuuchi M (2006) Treatment of hepatocellular carcinoma accompanied by portal vein tumor thrombus. World J Gastroenterol 12(47):7561–7567

    CAS  PubMed  Google Scholar 

  25. Minagawa M, Makuuchi M, Takayama T, Ohtomo K (2001) Selection criteria for hepatectomy in patients with hepatocellular carcinoma and portal vein tumor thrombus. Ann Surg 233(3):379–384

    Article  CAS  PubMed  Google Scholar 

  26. Shah ZK, McKernan MG, Hahn PF, Sahani DV (2007) Enhancing and expansile portal vein thrombosis: value in the diagnosis of hepatocellular carcinoma in patients with multiple hepatic lesions. AJR Am J Roentgenol 188(5):1320–1323. doi:10.2214/AJR.06.0134

    Article  PubMed  Google Scholar 

  27. Vilgrain V, Lebrec D, Menu Y, Scherrer A, Nahum H (1990) Comparison between ultrasonographic signs and the degree of portal hypertension in patients with cirrhosis. Gastrointest Radiol 15(3):218–222

    Article  CAS  PubMed  Google Scholar 

  28. Barrett BJ, Parfrey PS (2006) Clinical practice. Preventing nephropathy induced by contrast medium. N Engl J Med 354(4):379–386. doi:10.1056/NEJMcp050801

    Article  CAS  PubMed  Google Scholar 

  29. Peak AS, Sheller A (2007) Risk factors for developing gadolinium-induced nephrogenic systemic fibrosis. Ann Pharmacother 41(9):1481–1485. doi:10.1345/aph.1K295

    Article  PubMed  Google Scholar 

  30. Burns PN, Wilson SR, Simpson DH (2000) Pulse inversion imaging of liver blood flow: improved method for characterizing focal masses with microbubble contrast. Investig Radiol 35(1):58–71

    Article  CAS  Google Scholar 

  31. Choi BI, Kim TK, Han JK, et al. (1996) Power versus conventional color Doppler sonography: comparison in the depiction of vasculature in liver tumors. Radiology 200(1):55–58

    CAS  PubMed  Google Scholar 

  32. Marshall MM, Beese RC, Muiesan P, et al. (2002) Assessment of portal venous system patency in the liver transplant candidate: a prospective study comparing ultrasound, microbubble-enhanced colour Doppler ultrasound, with arteriography and surgery. Clin Radiol 57(5):377–383. doi:10.1053/crad.2001.0839

    Article  CAS  PubMed  Google Scholar 

  33. Tarantino L, Francica G, Sordelli I, et al. (2006) Diagnosis of benign and malignant portal vein thrombosis in cirrhotic patients with hepatocellular carcinoma: color Doppler US, contrast-enhanced US, and fine-needle biopsy. Abdom Imaging 31(5):537–544. doi:10.1007/s00261-005-0150-x

    Article  CAS  PubMed  Google Scholar 

  34. Danila M, Sporea I, Popescu A, Sirli R, Sendroiu M (2011) The value of contrast enhanced ultrasound in the evaluation of the nature of portal vein thrombosis. Med Ultrasonogr 13(2):102–107

    Google Scholar 

  35. Dusenbery D, Dodd GD, Carr BI (1995) Percutaneous fine-needle aspiration of portal vein thrombi as a staging technique for hepatocellular carcinoma. Cytologic findings of 46 patients. Cancer 75(8):2057–2062. doi:10.1002/1097-0142(19950415)75:8<2057::aid-cncr2820750805>3.0.co;2-k

    Article  CAS  PubMed  Google Scholar 

  36. Kubo S, Takemura S, Yamamoto S, et al. (2007) Risk factors for massive blood loss during liver resection for hepatocellular carcinoma in patients with cirrhosis. Hepatogastroenterology 54(75):830–833

    PubMed  Google Scholar 

  37. Bravo AA, Sheth SG, Chopra S (2001) Liver biopsy. N Engl J Med 344(7):495–500. doi:10.1056/NEJM200102153440706

    Article  CAS  PubMed  Google Scholar 

  38. Vilana R, Bru C, Bruix J, et al. (1993) Fine-needle aspiration biopsy of portal vein thrombus: value in detecting malignant thrombosis. AJR Am J Roentgenol 160(6):1285–1287

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Joint Department of Medical Imaging, Toronto General Hospital, University of Toronto, 585 University Avenue, Toronto, ON, M5G 2N2, Canada

    S. Arsalan Raza, Hyun-Jung Jang & Tae Kyoung Kim

  2. Department of Diagnostic Imaging, Cape Breton Regional Hospital, Sydney, NS, Canada

    S. Arsalan Raza

Authors
  1. S. Arsalan Raza
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  2. Hyun-Jung Jang
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  3. Tae Kyoung Kim
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Correspondence to Tae Kyoung Kim.

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Raza, S.A., Jang, HJ. & Kim, T.K. Differentiating malignant from benign thrombosis in hepatocellular carcinoma: contrast-enhanced ultrasound. Abdom Imaging 39, 153–161 (2014). https://doi.org/10.1007/s00261-013-0034-4

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