Preoperative color Doppler ultrasonography predicts early recurrence in AFP‑positive hepatocellular carcinoma

Chen,Miao; Wang,Duo; Zhao,Yuan; Lu,Dan‑Mei; Li,Hong‑Xue; Liu,Jun‑Jie; Li,Hang

doi:10.3892/ol.2019.10825

Preoperative color Doppler ultrasonography predicts early recurrence in AFP‑positive hepatocellular carcinoma

Authors:
- Miao Chen
- Duo Wang
- Yuan Zhao
- Dan‑Mei Lu
- Hong‑Xue Li
- Jun‑Jie Liu
- Hang Li
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Affiliations: Department of Ultrasound, Affiliated Tumor Hospital of Guangxi Medical University, Nanning, Guangxi Zhuang Autonomous Region 530021, P.R. China, Department of Hepatobiliary Surgery, Affiliated Tumor Hospital of Guangxi Medical University, Nanning, Guangxi Zhuang Autonomous Region 530021, P.R. China, Department of Ultrasound, The First People's Hospital of Nanning, Nanning, Guangxi Zhuang Autonomous Region 530021, P.R. China, Department of Ultrasound, Affiliated Tumor Hospital of Guangxi Medical University, Nanning Guangxi Zhuang Autonomous Region 530021, P.R. China
Published online on: September 9, 2019 https://doi.org/10.3892/ol.2019.10825
Pages: 4703-4711
Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The present study aimed to evaluate the hepatic hemodynamics of patients with α‑fetoprotein (AFP)‑positive hepatocellular carcinoma (HCC) and early recurrence (ER), as determined by color Doppler ultrasound. Screening with color Doppler ultrasound was performed in 150 patients with AFP‑positive HCC, yielding 43 cases with postoperative ER. In addition, 35 healthy controls were enrolled in the study for comparison of the blood flow parameters between the healthy control and the HCC groups. Receiver operating characteristic curve analysis was performed to evaluate the predicted effect of Doppler for the ER of HCC. The average mean flow velocity of portal vein in patients with HCC (14.686±5.873 cm/s) was significantly lower in the HCC group compared with the healthy control group (17.631±3.569 cm/s; P=0.005). Additionally, the preoperative portal vein diameter in the HCC group was significantly higher compared with that in the healthy control group (P=0.001). Regarding the effect of surgery, the portal vein diameter was significantly increased in the patients postoperatively compared with preoperatively (P=0.003), while the pulsation and resistance indexes exhibited a decreasing trend in the postoperative group (P=0.001 and P=0.003, respectively). Notably, patients with HCC and ER presented with a higher resistance index (1.163±0.342) compared with the ER‑free group (1.023±0.176; P=0.004). Furthermore, a significant difference in hepatic artery pulsation index was also observed between the ER group (0.673±0.075) and the ER‑free group (0.624±0.056; P=0.018), indicating that an increased hepatic artery pulsation index may significantly predict the ER of HCC. In addition, areas under the curve of 0.683 and 0.700, respectively, suggested that the hepatic artery resistance and pulsation indexes may be used to diagnose ER in HCC (P=0.009 and P=0.004, respectively). Taken together, Doppler ultrasound provides a reliable and accurate quantification of hepatic hemodynamics for detecting ER in HCC with a good diagnostic accuracy.

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1	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2018. CA Cancer J Clin. 68:7–30. 2018. View Article : Google Scholar : PubMed/NCBI
2	Tang A, Hallouch O, Chernyak V, Kamaya A and Sirlin CB: Epidemiology of hepatocellular carcinoma: Target population for surveillance and diagnosis. Abdom Radiol (NY). 43:13–25. 2018. View Article : Google Scholar : PubMed/NCBI
3	Ayuso C, Rimola J, Vilana R, Burrel M, Darnell A, García-Criado Á, Bianchi L, Belmonte E, Caparroz C, Barrufet M, et al: Diagnosis and staging of hepatocellular carcinoma (HCC): Current guidelines. Eur J Radiol. 101:72–81. 2018. View Article : Google Scholar : PubMed/NCBI
4	Colombo F, Baldan F, Mazzucchelli S, Martin-Padura I, Marighetti P, Cattaneo A, Foglieni B, Spreafico M, Guerneri S, Baccarin M, et al: Evidence of distinct tumour-propagating cell populations with different properties in primary human hepatocellular carcinoma. PLoS One. 6:e213692011. View Article : Google Scholar : PubMed/NCBI
5	Jemal A, Ward EM, Johnson CJ, Cronin KA, Ma J, Ryerson B, Mariotto A, Lake AJ, Wilson R, Sherman RL, et al: Annual report to the nation on the status of cancer, 1975–2014, featuring survival. J Natl Cancer Inst. 109:2017. View Article : Google Scholar
6	He W, Peng B, Tang Y, Yang J, Zheng Y, Qiu J, Zou R, Shen J, Li B and Yuan Y: Nomogram to predict survival of patients with recurrence of hepatocellular carcinoma after surgery. Clin Gastroenterol Hepatol. 16:756–764.e10. 2018. View Article : Google Scholar : PubMed/NCBI
7	Shu T, Zhao D, Li B, Wang Y, Liu S, Li P, Zuo J, Bai P, Zhang R and Wu L: Prognostic evaluation of postoperative adjuvant therapy for operable cervical cancer: 10 years' experience of National Cancer Center in China. Chin J Cancer Res. 29:510–520. 2017. View Article : Google Scholar : PubMed/NCBI
8	Wang Y, Liao J, Qi W, Xie L and Li Y: Predictive value of conventional ultrasound and contrast-enhanced ultrasound in early recurrence of hepatocellular carcinoma after surgical resection. Ultrasound Med Biol. 42:1042–1048. 2016. View Article : Google Scholar : PubMed/NCBI
9	Poon RT, Fan ST, Ng IO, Lo CM, Liu CL and Wong J: Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer. 89:500–507. 2000. View Article : Google Scholar : PubMed/NCBI
10	Portolani N, Coniglio A, Ghidoni S, Giovanelli M, Benetti A, Tiberio GA and Giulini SM: Early and late recurrence after liver resection for hepatocellular carcinoma: Prognostic and therapeutic implications. Ann Surg. 243:229–235. 2006. View Article : Google Scholar : PubMed/NCBI
11	Gao Y, Zheng DY, Cui Z, Ma Y, Liu YZ and Zhang W: Predictive value of quantitative contrast-enhanced ultrasound in hepatocellular carcinoma recurrence after ablation. World J Gastroenterol. 21:10418. 2015. View Article : Google Scholar : PubMed/NCBI
12	Kamin PD, Bernardino ME and Green B: Ultrasound manifestations of hepatocellular Carcinoma. Radiology. 131:459–461. 1979. View Article : Google Scholar : PubMed/NCBI
13	Freitas TP, Gomes M, Fraga DB, Freitas LS, Rezin GT, Santos PM, Silveira PC, Paula MM, Pinho RA and Streck EL: Effect of therapeutic pulsed ultrasound on lipoperoxidation and fibrogenesis in an animal model of wound healing. J Surg Res. 161:168–171. 2010. View Article : Google Scholar : PubMed/NCBI
14	Zekanovic D, Ljubicic N, Boban M, Nikolic M, Delic-Brkljacic D, Gacina P, Klarin I and Turcinov J: Doppler ultrasound of hepatic and system hemodynamics in patients with alcoholic liver cirrhosis. Dig Dis Sci. 55:458–466. 2010. View Article : Google Scholar : PubMed/NCBI
15	Suk KT, Kim EJ, Kim DJ, Kim HS, Bang CS, Park TY, Baik GH, Kim SE, Park JW, Park SH, et al: Prognostic significance of hemodynamic and clinical stages in the prediction of hepatocellular carcinoma. J Clin Gastroenterol. 51:285–293. 2017.PubMed/NCBI
16	Yang YL, Di L, Duan YY, Liu X, Liu J, Yang RJ, Chen S and Yuan LJ: A prospective experimental study of liver fibrosis with ultrasound and its correlation with hepatic reserve function and hemodynamics. BMC Gastroenterol. 12:1682012. View Article : Google Scholar : PubMed/NCBI
17	Yang JD, Dai J, Singal AG, Gopal P, Addissie BD, Nguyen MH, Befeler AS, Reddy KR, Schwartz M, Harnois DM, et al: Improved performance of serum alpha-fetoprotein for hepatocellular carcinoma diagnosis in HCV cirrhosis with normal alanine transaminase. Cancer Epidemiol Biomarkers Prev. 26:1085–1092. 2017. View Article : Google Scholar : PubMed/NCBI
18	Sangiovanni A and Colombo M: Treatment of hepatocellular carcinoma: Beyond international guidelines. Liver Int. 36 (Suppl 1):S124–S129. 2016. View Article : Google Scholar
19	Colecchia A, Schiumerini R, Cucchetti A, Cescon M, Taddia M, Marasco G and Festi D: Prognostic factors for hepatocellular carcinoma recurrence. World J Gastroenterol. 20:5935–5950. 2014. View Article : Google Scholar : PubMed/NCBI
20	Tong MJ, Rosinski AA, Huynh CT, Raman SS and Lu DSK: Long-term survival after surveillance and treatment in patients with chronic viral hepatitis and hepatocellular carcinoma. Hepatol Commun. 1:595–608. 2017. View Article : Google Scholar : PubMed/NCBI
21	Annet L, Materne R, Danse E, Jamart J, Horsmans Y and Van Beers BE: Hepatic flow parameters measured with MR imaging and Doppler US: Correlations with degree of cirrhosis and portal hypertension. Radiology. 229:409–414. 2003. View Article : Google Scholar : PubMed/NCBI
22	Kondo T, Maruyama H, Sekimoto T, Shimada T, Takahashi M, Okugawa H and Yokosuka O: Impact of portal hemodynamics on Doppler ultrasonography for predicting decompensation and long-term outcomes in patients with cirrhosis. Scand J Gastroenterol. 51:236–244. 2016. View Article : Google Scholar : PubMed/NCBI
23	Mäkikallio K, Erkinaro T, Niemi N, Kavasmaa T, Acharya G, Päkkilä M and Räsänen J: Fetal oxygenation and Doppler ultrasonography of cardiovascular hemodynamics in a chronic near-term sheep model. Am J Obstet Gynecol. 194:542–550. 2006. View Article : Google Scholar : PubMed/NCBI
24	Maruyama H and Yokosuka O: Ultrasonography for noninvasive assessment of portal hypertension. Gut Liver. 11:464–473. 2017. View Article : Google Scholar : PubMed/NCBI
25	Berzigotti A, Reverter E, García-Criado Á, Abraldes JG, Cerini F, García-Pagán JC and Bosch J: Reliability of the estimation of total hepatic blood flow by Doppler ultrasound in patients with cirrhotic portal hypertension. J Hepatol. 59:717–722. 2013. View Article : Google Scholar : PubMed/NCBI
26	Biselli M, Conti F, Gramenzi A, Frigerio M, Cucchetti A, Fatti G, D'Angelo M, Dall'Agata M, Giannini EG, Farinati F, et al: A new approach to the use of alpha-fetoprotein as surveillance test for hepatocellular carcinoma in patients with cirrhosis. Br J Cancer. 112:69–76. 2015. View Article : Google Scholar : PubMed/NCBI
27	Lee SY, Konstantinidis IT, Eaton AA, Gönen M, Kingham TP, D'Angelica MI, Allen PJ, Fong Y, DeMatteo RP and Jarnagin WR: Predicting recurrence patterns after resection of hepatocellular cancer. HPB (Oxford). 16:943–953. 2014. View Article : Google Scholar : PubMed/NCBI
28	Yang P, Qiu J, Li J, Wu D, Wan X, Lau WY, Yuan Y and Shen F: Nomograms for pre-and postoperative prediction of long-term survival for patients who underwent hepatectomy for multiple hepatocellular carcinomas. Ann Surg. 263:778–786. 2016. View Article : Google Scholar : PubMed/NCBI
29	Ogihara H, Iizuka N and Hamamoto Y: Prediction of early recurrence of liver cancer by a novel discrete bayes decision rule for personalized medicine. Biomed Res Int. 2016:85674792016. View Article : Google Scholar : PubMed/NCBI
30	Zhang W, Lai SL, Chen J, Xie D, Wu FX, Jin GQ and Su DK: Validated preoperative computed tomography risk estimation for postoperative hepatocellular carcinoma recurrence. World J Gastroenterol. 23:6467–6473. 2017. View Article : Google Scholar : PubMed/NCBI
31	Mehta A and Singal AG: Hepatocellular Carcinoma surveillance: Does alpha-fetoprotein have a role. Gastroenterology. 149:816–817. 2015. View Article : Google Scholar : PubMed/NCBI
32	Bonnin P, Villemain A, Vincent F, Debbabi H, Silvestre JS, Contreres JO, Levy BI, Tobelem G and Dupuy E: Ultrasonic assessment of hepatic blood flow as a marker of mouse hepatocarcinoma. Ultrasound Med Biol. 33:561–570. 2007. View Article : Google Scholar : PubMed/NCBI
33	Rappaport AM: Hepatic blood flow: Morphologic aspects and physiologic regulation. Int Rev Physiol. 21:1–63. 1980.PubMed/NCBI
34	Kamiyama T, Kakisaka T, Orimo T and Wakayama K: Hepatectomy for hepatocellular carcinoma with portal vein tumor thrombus. World J Hepatol. 9:1296–1304. 2017. View Article : Google Scholar : PubMed/NCBI
35	Dong YH and Lin G: Experimental studies of portal venous embolization with iodized oil in rats with experimentally induced liver cancer. J Vasc Int Radiol. 4:621–624. 1993. View Article : Google Scholar
36	Han K, Kim JH, Ko GY, Gwon DI and Sung KB: Treatment of hepatocellular carcinoma with portal venous tumor thrombosis: A comprehensive review. World J Gastroenterol. 22:407–416. 2016. View Article : Google Scholar : PubMed/NCBI
37	Giorgio A, Calisti G, Montesarchio L, Scognamiglio U, Matteucci P, Coppola C, Scarano F, Amendola F and Giorgio V: Hepatocellular carcinoma invading portal venous system in cirrhosis: Long-term results of percutaneous radiofrequency ablation of both the nodule and portal vein tumor thrombus. A case control study. Anticancer Res. 34:6785–6790. 2014.PubMed/NCBI
38	Shimada S, Kamiyama T, Yokoo H, Orimo T, Wakayama K, Einama T, Kakisaka T, Kamachi H and Taketomi A: Clinicopathological characteristics of hepatocellular carcinoma with microscopic portal venous invasion and the role of anatomical liver resection in these cases. World J Surg. 41:2087–2094. 2017. View Article : Google Scholar : PubMed/NCBI
39	Tanaka S, Kitamura T, Fujita M, Nakanishi K and Okuda S: Color Doppler flow imaging of liver tumors. AJR Am J Roentgenol. 154:509–514. 1990. View Article : Google Scholar : PubMed/NCBI
40	Kamalov IR, Sandrikov VA, Gautier SV, Tsirulnikova OM and Skipenko OG: The significance of colour velocity and spectral Doppler ultrasound in the differentiation of liver tumours. Eur J Ultrasound. 7:101–108. 1998. View Article : Google Scholar : PubMed/NCBI