Ultraschall Med 2016; 37(06): 609-618
DOI: 10.1055/s-0034-1399485
Original Article
© Georg Thieme Verlag KG Stuttgart · New York

Factors Affecting the Enhancement Patterns of Intrahepatic Cholangiocarcinoma (ICC) on Contrast-Enhanced Ultrasound (CEUS) and their Pathological Correlations in Patients with a Single Lesion

Einflussfaktoren auf die Kontrast-Enhancement-Muster beim intrahepatischen Cholangiokarzinom (ICC) in der kontrastverstärkten Sonografie (CEUS) und deren pathologische Zuordnungen bei Patienten mit Einzelläsion
M. X. Yuan
1   Department of Ultrasound, Southwest hospital Affiliated to Third Military Medical University, Shapingba, China
,
R. Li
1   Department of Ultrasound, Southwest hospital Affiliated to Third Military Medical University, Shapingba, China
,
X. H. Zhang
1   Department of Ultrasound, Southwest hospital Affiliated to Third Military Medical University, Shapingba, China
,
C. L. Tang
1   Department of Ultrasound, Southwest hospital Affiliated to Third Military Medical University, Shapingba, China
,
Y. L. Guo
1   Department of Ultrasound, Southwest hospital Affiliated to Third Military Medical University, Shapingba, China
,
D. Y. Guo
2   Department of Pathology, Southwest hospital Affiliated to Third Military Medical University, Shapingba, China
,
M. K. Luo
3   Department of Mathematics, School of basic medicine, The Third Military Medical University, Shapingba, China
› Author Affiliations
Further Information

Publication History

12 August 2014

12 March 2015

Publication Date:
28 April 2015 (online)

Abstract

Purpose: To investigate the factors that influence the enhancement patterns of intrahepatic cholangiocarcinomas (ICC) on contrast-enhanced ultrasound (CEUS) and analyze the correlations between the enhancement patterns on CEUS and pathological findings.

Materials and Methods: Ninety-six patients with 96 pathologically confirmed ICCs underwent CEUS. CEUS images were retrospectively evaluated for tumor enhancement patterns in the arterial, portal and late phases. The arterial enhancement patterns were correlated with clinicopathological factors. The possible influencing factors were correlated with pathologic findings.

Results: Thirty-six patients with ICC demonstrated rim-like enhancement, and 60 exhibited non-rim-like enhancement in the arterial phase on CEUS. The incidence of non-rim-like-enhancing ICCs was higher in patients with cirrhosis and chronic viral hepatitis than patients with no chronic liver disease (p = 0.001). The sizes of the ICCs with homogeneous hyper-enhancement were significantly smaller than those with inhomogeneous hyper-enhancement (p = 0.007). Arterial non-rim-like-enhancing ICCs showed higher microvessel density (MVD) and arterial density (AD) and less fibrous stroma and necrosis than rim-like-enhancing ICCs. Arterial inhomogeneous-enhancing ICCs had lower MVD and AD and much more fibrous stroma and necrosis than homogeneous-enhancing ICCs.

Conclusion: The enhancement pattern of ICCs in the arterial phase on CEUS was affected by a liver cirrhosis and chronic viral hepatitis and tumor size. The amount of MVD, AD, fibrous stroma and necrosis in ICC tumors may be responsible for the difference in the enhancement patterns.

Zusammenfassung

Ziel: Suche nach Faktoren, die das Enhancement-Muster des intrahepatischen Cholangiokarzinoms (ICC) im kontrastverstärkten Ultraschall (CEUS) beeinflussen und mit den pathologischen Befunden korrelieren.

Material und Methoden: Bei 96 Patienten mit verifizierten ICC wurden die CEUS retrospektiv hinsichtlich der Tumor-Enhancement-Muster in der arteriellen portalen und späten Phase ausgewertet. Die Muster der arteriellen Phase wurden mit klinisch-pathologischen Daten verglichen und auf Korrelation mit den Pathologiebefunden verglichen.

Ergebnisse: Das Randenhancement in der arteriellen Phase fehlte bei 60 Tumoren, 36 mal war es nachweisbar. Bei Zirrhose und chronischer Virushepatitis fehlte es häufiger als bei Patienten ohne chronische Lebererkrankung (p = 0,001). Bei homogenem Hyperenhancement war die Größe der ICCs signifikant geringer als bei inhomogenem Enhancement (p = 0,007). ICCs mit fehlenden Randenhancement in der arteriellen Phase zeigten eine höhere Dichte an Mikrogefäßen („microvessel density“ MVD), größere Arteriendichte (AD) und weniger fibröses Stroma und weniger Nekrosen als ICCs mit Randenhancement. ICCs mit arteriellem inhomogenem Enhancement hattenniedrigere MVD und AD, sowie mehr fibröses Stroma und Nekrosen als ICCs mit homogenem Enhancement.

Schlussfolgerung: Die Kontrast-Enhancement-Muster des ICCs in der arteriellen CEUS-Phase wurden durch Leberzirrhose, chronische Virushepatitiden und von der Tumorgröße beeinflusst. Das Ausmaß an MVD, AD, fibrösem Stroma und Nekrose bei den ICC-Tumoren kann für die Unterschiede bei den Kontrast- Enhancement-Mustern verantwortlich sein.

 
  • References

  • 1 Khan SA, Thomas HC, Davidson BR et al. Cholangiocarcinoma. Lancet 2005; 366: 1303-1314
  • 2 Shaib YH, El-Serag HB, Davila JA et al. Risk factors of intrahepatic cholangiocarcinoma in the United States: a case-control study. Gastroenterology 2005; 128: 620-626
  • 3 Patel T. Increasing incidence and mortality of primary intrahepatic cholangiocarcinoma in the United States. Hepatology 2001; 33: 1353-1357
  • 4 Shaib YH, El-Serag HB. The epidemiology of cholangiocarcinoma. Semin Liver Dis 2004; 24: 115-125
  • 5 Strobel D, Seitz K, Blank W et al. Contrast-enhanced ultrasound for the characterization of focal liver lesions--diagnostic accuracy in clinical practice (DEGUM multicenter trial). Ultraschall in Med 2008; 29: 499-505
  • 6 Chen MH, Dai Y, Yan K et al. The role of contrast-enhanced ultrasound on the diagnosis of small hepatocellular carcinoma (</=3cm) in patients with cirrhosis. Hepatol Res 2006; 35: 281-288
  • 7 Claudon M, Cosgrove D, Albrecht T et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) – update 2008. Ultraschall in Med 2008; 29: 28-44
  • 8 Vilana R, Forner A, Bianchi L et al. Intrahepatic peripheral cholangiocarcinoma in cirrhosis patients may display a vascular pattern similar to hepatocellular carcinoma on contrast-enhanced ultrasound. Hepatology 2010; 51: 2020-2029
  • 9 Galassi M, Iavarone M, Rossi S et al. Patterns of appearance and risk of misdiagnosis of intrahepatic cholangiocarcinoma in cirrhosis at contrast enhanced ultrasound. Liver Internat 2013; 33: 771-779
  • 10 Li R, Zhang X, Ma K et al. Dynamic enhancing vascular pattern of intrahepatic peripherialcholangiocarcinoma on contrast-enhanced ultrasound: the influence of chronic hepatitis and cirrhosis. Abdom Imaging 2013; 38: 112-119
  • 11 Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005; 42: 1208-1236
  • 12 Claudon M, Dietrich CF, Choi BI et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver--update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultraschall in Med 2013; 34: 11-29
  • 13 D'Onofrio M, Vecchiato F, Cantisani V et al. Intrahepatic peripheral cholangiocarcinoma (IPCC): comparison between perfusion ultrasound and CT imaging. Radiol Med 2008; 113: 76-86
  • 14 Chen LD, Xu HX, Xie XY et al. Enhancement patterns of intrahepatic cholangiocarcinoma: comparison between contrast-enhanced ultrasound and contrast-enhanced CT. Br J Radiol 2008; 81: 881-889
  • 15 Li R, Guo Y, Hua X et al. Characterization of focal liver lesions: comparison of pulse-inversion harmonic contrast-enhanced sonography with contrast-enhanced CT. J Clin Ultrasound 2007; 35: 109-117
  • 16 Celli N, Gaian S, Piscaglia F et al. Characterization of liver lesions by real-time contrast-enhanced ultrasonography. Eur J GastroenterolHepatol 2007; 19: 3-14
  • 17 Chen LD, Xu HX, Xie XY et al. Intrahepatic cholangiocarcinoma and hepatocellular carcinoma: differential diagnosis with contrast-enhanced ultrasound. Eur Radiol 2010; 20: 743-753
  • 18 Boozari B, Soudah B, Rifai K et al. Grading of hypervascular hepatocellular carcinoma using late phase of contrast enhanced sonography – a prospective study. Dig Liver Dis 2011; 43: 484-490
  • 19 Jang HJ, Kim TK, Burns PN et al. Enhancement patterns of hepatocellular carcinoma at contrast-enhanced US: comparison with histologic differentiation. Radiology 2007; 244: 898-906.20
  • 20 Schuppan D, Afdhal NH. Livercirrhosis. Lancet 2008; 371: 838-851
  • 21 Edge SB, Byrd DR, Compton CC et al. editors. AJCC cancer staging manual. (7th ed). New York, NY: Springer; 2010
  • 22 Rimola J, Forner A, Reig M et al. Cholangiocarcinoma in cirrhosis: Absence of contrast washout in delayed phases by magnetic resonance imaging avoids misdiagnosis of hepatocellular carcinoma. Hepatology 2009; 50: 791-798
  • 23 Iavarone M, Piscaglia F, Vavassori S et al. Contrast enhanced CT-scan to diagnose intrahepatic cholangiocarcinoma in patients with cirrhosis. J Hepatol 2013; 58: 1188-1193
  • 24 Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 1996; 24: 289-293
  • 25 Xu J, Igarashi S, Sasaki M et al. Intrahepatic cholangiocarcinomas in cirrhosis are hypervascular in comparison with those in normal livers. Liver Int 2012; 32: 1156-1164
  • 26 Kim SA, Lee JM, Lee KB et al. Intrahepatic mass-forming cholangiocarcinomas: enhancement patterns at multiphasic CT, with special emphasis on arterial enhancement pattern--correlation with clinicopathologic findings. Radiology 2011; 260: 148-157
  • 27 Tyson GL, El-Serag HB. Risk factors for cholangiocarcinoma. Hepatology 2011; 54: 173-184
  • 28 Xu HX, Lu MD, Liu GJ et al. Imaging of peripheral cholangiocarcinoma with low-mechanical index contrast-enhanced sonography and SonoVue: initial experience. J Ultrasound Med 2006; 25: 23-33
  • 29 Kobayashi S, Nakanuma Y, Matsui O. Intrahepatic peribiliary vascular plexus in various hepatobiliary diseases: a histological survey. Hum Pathol 1994; 25: 940-946
  • 30 Nanashima A, Sumida Y, Abo T et al. Relationship between pattern of tumor enhancement and clinicopathologic characteristics in intrahepatic cholangiocarcinoma. Journal of Surgical Oncology 2008; 98: 535-539