Value of contrast-enhanced ultrasound for preoperative assessment of liver reserve function in patients with liver tumors

Autoři: Huiming Yi aff001;  Baohuan Cai aff002;  Xi Ai aff003;  Ruobing Liu aff001;  Kaiyan Li aff001;  Wei Zhang aff001
Působiště autorů: Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan City, Hubei Province, China aff001;  Department of Pediatrics, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan City, Hubei Province, China aff002;  Department of Hepatic Surgery, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan City, Hubei Province, China aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222514


This study aimed to investigate the value of contrast-enhanced ultrasound (CEUS) for preoperative assessment of liver reserve function in patients with liver tumors. The indocyanine green (ICG) clearance tests and CEUS examinations of 45 noncirrhotic patients with liver tumors were performed prior to liver resection. Parameters time to peak (TtoPk), arrival time (Atm) as well as perfusion parameters A, k and A x k were generated from time-intensity curve (TIC) of CEUS. The correlation analyses of the ICG clearance per unit time (ICGK) and the retention rate at 15 min (ICGR15) with TtoPk, Atm, A, k and A x k were performed, and the diagnostic ability as well as optimal cut-off values of TtoPk and Atm for differentiating patients with ICGR15>10% from ICGR15<10% were analyzed. There were significant correlations of ICGK with TtoPk and Atm, and the correlation coefficients were 0.363 (p = 0.014) and -0.482 (p = 0.001), respectively. Significant correlations of ICGR15 with TtoPk and Atm were revealed, and the correlation coefficients were -0.416 (p = 0.004) and 0.303 (p = 0.043), respectively. No correlation of ICGK or ICGR15 with A, k and A x k was found in this study. There were significant differences in TtoPk and Atm between patients with ICGR15>10% and ICGR15<10% (p = 0.028 and p = 0.026, respectively). TtoPk and Atm both had good diagnostic abilities in diagnosing patients with ICGR15>10% verusus ICGR15<10% (AUROC = 0.711 and 0.721, respectively). For ICGR15>10% vs ICGR15, the optimal cut-off values of TtoPk and Atm were 13.307 s and 11.007 s, respectively, while the sensitivity and specificity were 75.0% and 72.7%, 60.6% and 75.0%, respectively. This study revealed that CEUS has the potential to be a new method to evaluate the liver reserve function of patients. With the optimal cut-off values of TtoPk and Atm, qualitative assessment of patients with ICGR15>10% could be more easily achieved by CEUS with good diagnostic abilities.

Klíčová slova:

Medicine and health sciences – Surgical and invasive medical procedures – Digestive system procedures – Hepatic resection – Hepatectomy – Surgical resection – Diagnostic medicine – Diagnostic radiology – Radiology and imaging – Gastroenterology and hepatology – Liver function tests – Liver diseases – Hepatocytes – Oncology – Cancer treatment – Radiation therapy – Clinical oncology – Clinical medicine – Research and analysis methods – Imaging techniques – Ultrasound imaging – Biology and life sciences – Cell biology – Cellular types – Animal cells – Anatomy – Liver


1. Sheng QS, Lang R, He Q, Yang YJ, Zhao DF, Chen DZ. Indocyanine green clearance test and model for end-stage liver disease score of patients with liver cirrhosis. Hepatobiliary Pancreat Dis Int. 2009;8(1):46–9. 19208514

2. Gupta S, Chawla Y, Kaur J, Saxena R, Duseja A, Dhiman RK, et al. Indocyanine green clearance test (using spectrophotometry) and its correlation with model for end stage liver disease (MELD) score in Indian patients with cirrhosis of liver. Trop Gastroenterol. 2012;33(2):129–34. 23025060

3. Haegele S, Reiter S, Wanek D, Offensperger F, Pereyra D, Stremitzer S, et al. Perioperative non-invasive indocyanine green-clearance testing to predict postoperative outcome after liver resection. PloS one. 2016;11(11):e0165481. doi: 10.1371/journal.pone.0165481 27812143

4. Wang YY, Zhao XH, Ma L, Ye JZ, Wu FX, Tang J, et al. Comparison of the ability of Child-Pugh score, MELD score, and ICG-R15 to assess preoperative hepatic functional reserve in patients with hepatocellular carcinoma. Journal of surgical oncology. 2018;118(3):440–45. doi: 10.1002/jso.25184 30259515

5. Wang L, Xie L, Zhang N, Zhu W, Zhou J, Pan Q, et al. Predictive Value of Intraoperative Indocyanine Green Clearance Measurement on Postoperative Liver Function After Anatomic Major Liver Resection. Journal of Gastrointestinal Surgery. 2019;13:1–10.

6. Seyama Y, Kokudo N. Assessment of liver function for safe hepatic resection. Hepatol Res. 2009;39(2):107–16. doi: 10.1111/j.1872-034X.2008.00441.x 19208031

7. Wildner D, Schellhaas B, Strack D, Goertz RS, Pfeifer L, Fiessler C, et al. Differentiation of malignant liver tumors by software-based perfusion quantification with dynamic contrast-enhanced ultrasound (DCEUS). Clinical hemorheology and microcirculation. 2019;71(1):39–51. doi: 10.3233/CH-180378 29865043

8. Cosgrove D, Harvey C. Clinical uses of microbubbles in diagnosis and treatment. Med Biol Eng Comput. 2009;47(8):813–26. doi: 10.1007/s11517-009-0434-3 19205774

9. Quaia E. Assessment of tissue perfusion by contrast-enhanced ultrasound. Eur Radiol. 2011;21(3):604–15. doi: 10.1007/s00330-010-1965-6 20927527

10. Wang Z, Dabrosin C, Yin X, Fuster MM, Arreola A, Rathmell WK, et al. Broad targeting of angiogenesis for cancer prevention and therapy. Semin Cancer Biol. 2015;35 Suppl:S224–S43.

11. Zhan Y, Zhou FB, Yu XL, Luo F, Liu FY, Liang P, et al. Quantitative dynamic contrast-enhanced ultrasound may help predict the outcome of hepatocellular carcinoma after microwave ablation. Int J Hyperther. 2019;35(1):105–11.

12. Wu HP, Patel RB, Zheng YY, Solorio L, Krupka TM, Ziats NP, et al. Differentiation of Benign Periablational Enhancement from Residual Tumor Following Radio-Frequency Ablation Using Contrast-Enhanced Ultrasonography in a Rat Subcutaneous Colon Cancer Model. Ultrasound in Medicine and Biology. 2012;38(3):443–53. doi: 10.1016/j.ultrasmedbio.2011.12.008 22266229

13. Youden WJ. Index for Rating Diagnostic Tests. Cancer. 1950;3(1):32–5. doi: 10.1002/1097-0142(1950)3:1<32::aid-cncr2820030106>;2-3 15405679

14. Swets JA. Measuring the Accuracy of Diagnostic Systems. Science. 1988;240(4857):1285–93. doi: 10.1126/science.3287615 3287615

15. Takano S, Oishi H, Kono S, Kawakami S, Nakamura M, Kubota N, et al. Retrospective analysis of type of hepatic resection for hepatocellular carcinoma. Brit J Surg. 2000;87(1):65–70. doi: 10.1046/j.1365-2168.2000.01308.x 10606913

16. Erdogan D, Heijnen BH, Bennink RJ, Kok M, Dinant S, Straatsburg IH, et al. Preoperative assessment of liver function: a comparison of 99mTc-Mebrofenin scintigraphy with indocyanine green clearance test. Liver Int. 2004;24(2):117–23. doi: 10.1111/j.1478-3231.2004.0901.x 15078475

17. Ibis C, Albayrak D, Sahiner T, Soytas Y, Gurtekin B, Sivrikoz N. Value of Preoperative Indocyanine Green Clearance Test for Predicting Post-Hepatectomy Liver Failure in Noncirrhotic Patients. Med Sci Monitor. 2017;23:4973–80.

18. El-Desoky A, Seifalian AM, Cope M, Delpy DT, Davidson BR. Experimental study of liver dysfunction evaluated by direct indocyanine green clearance using near infrared spectroscopy. Brit J Surg. 1999;86(8):1005–11. doi: 10.1046/j.1365-2168.1999.01186.x 10460634

19. Kim HJ, Kim CY, Park EK, Hur YH, Koh YS, Kim HJ, et al. Volumetric analysis and indocyanine green retention rate at 15 min as predictors of post-hepatectomy liver failure. Hpb. 2015;17(2):159–67. doi: 10.1111/hpb.12295 24964188

20. De Gasperi A, Mazza E, Prosperi M. Indocyanine green kinetics to assess liver function: Ready for a clinical dynamic assessment in major liver surgery? World J Hepatol. 2016;8(7):355–67. doi: 10.4254/wjh.v8.i7.355 26981173

21. Shinohara H, Tanaka A, Kitai T, Yanabu N, Inomoto T, Satoh S, et al. Direct measurement of hepatic indocyanine green clearance with near-infrared spectroscopy: Separate evaluation of uptake and removal. Hepatology. 1996;23(1):137–44. doi: 10.1053/jhep.1996.v23.pm0008550033 8550033

22. Chijiiwa K, Watanabe M, Nakano K, Noshiro H, Tanaka M. Biliary indocyanine green excretion as a predictor of hepatic adenosine triphosphate levels in patients with obstructive jaundice. Am J Surg. 2000;179(2):161–6. doi: 10.1016/s0002-9610(00)00274-9 10773154

23. Ohno N, Miyati T, Yamashita M, Narikawa M. Quantitative Assessment of Tissue Perfusion in Hepatocellular Carcinoma Using Perflubutane Dynamic Contrast-Enhanced Ultrasonography: A Preliminary Study. Diagnostics. 2015;5(2):210–8. doi: 10.3390/diagnostics5020210 26854150

Článek vyšel v časopise


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Zvyšte si kvalifikaci online z pohodlí domova

Ulcerative colitis_muž_břicho_střeva
Ulcerózní kolitida
nový kurz

Blokátory angiotenzinových receptorů (sartany)
Autoři: MUDr. Jiří Krupička, Ph.D.

Antiseptika a prevence ve stomatologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Citikolin v neuroprotekci a neuroregeneraci: od výzkumu do klinické praxe nejen očních lékařů
Autoři: MUDr. Petr Výborný, CSc., FEBO

Zánětlivá bolest zad a axiální spondylartritida – Diagnostika a referenční strategie
Autoři: MUDr. Monika Gregová, Ph.D., MUDr. Kristýna Bubová

Všechny kurzy