State of the Art of Intraoperative Ultrasound in Liver Surgery: Current Use for Staging and Resection Guidance

Abstract

The performance of hepatic surgery without a parenchyma-sparing strategy carries significant risks for patient survival because of the not negligible occurrence of postoperative liver failure. In modern liver surgery the use of intraoperative ultrasound (IOUS) includes staging of the liver disease and more importantly resection guidance. IOUS allows the performance of so-called “radical but conservative surgery”, which is pivotal in offering a chance of a cure to an increasing number of patients who until a few years ago were considered only for palliative care. The present article details the rationale of IOUS for staging and for resection guidance in liver surgery.

• Literatur/References

• 1 Torzilli G, Montorsi M, Donadon M et al. "Radical but conservative" is the main goal for ultrasonography-guided liver resection: prospective validation of this approach. J Am Coll Surg 2005; 201: 517-528
• 2 Arita J, Takahashi M, Hata S et al. Usefulness of contrast-enhanced intraoperative ultrasound using Sonazoid in patients with hepatocellular carcinoma. Ann Surg 2011; 254: 992-999
• 3 Takahashi M, Hasegawa K, Arita J et al. Contrast-enhanced intraoperative ultrasonography using perfluorobutane microbubbles for the enumeration of colorectal liver metastases. Br J Surg 2012; 99: 1271-1277
• 4 Hata S, Imamura H, Aoki T et al. Value of visual inspection, bimanual palpation, and intraoperative ultrasonography during hepatic resection for liver metastases of colorectal carcinoma. World J Surg 2011; 35: 2779-2787
• 5 Ayuso C, Rimola J, Garcia-Criado A. Imaging of HCC. Abdom Imaging 2012; 37: 215-230
• 6 Sahani DV, Bajwa MA, Andrabi Y et al. Current status of imaging and emerging techniques to evaluate liver metastases from colorectal carcinoma. Ann Surg 2014; 259: 861-872
• 7 Kim YK, Kwak HS, Kim CS et al. Hepatocellular carcinoma in patients with chronic liver disease: comparison of SPIO-enhanced MR imaging and 16-detector row CT. Radiology 2006; 238: 531-541
• 8 Sun HY, Lee JM, Shin CI et al. Gadoxetic acid-enhanced magnetic resonance imaging for differentiating small hepatocellular carcinomas (< or =2 cm in diameter) from arterial enhancing pseudolesions: special emphasis on hepatobiliary phase imaging. Invest Radiol 2010; 45: 96-103
• 9 Vauthey JN, Dixon E, Abdalla EK et al. Pretreatment assessment of hepatocellular carcinoma: expert consensus statement. HPB (Oxford) 2010; 12: 289-299
• 10 Hammerstingl R, Huppertz A, Breuer J et al. Diagnostic efficacy of gadoxetic acid (Primovist)-enhanced MRI and spiral CT for a therapeutic strategy: comparison with intraoperative and histopathologic findings in focal liver lesions. Eur Radiol 2008; 18: 457-467
• 11 Takigawa Y, Sugawara Y, Yamamoto J et al. New lesions detected by intraoperative ultrasound during liver resection for hepatocellular carcinoma. Ultrasound Med Biol 2001; 27: 151-156
• 12 Caturelli E, Costarelli L, Giordano M et al. Hypoechoic lesions in fatty liver. Quantitative study by histomorphometry. Gastroenterology 1991; 100: 1678-1682
• 13 Kokudo N, Bandai Y, Imanishi H et al. Management of new hepatic nodules detected by intraoperative ultrasonography during hepatic resection for hepatocellular carcinoma. Surgery 1996; 119: 634-640
• 14 Blomley MJ, Albrecht T, Cosgrove DO et al. Improved imaging of liver metastases with stimulated acoustic emission in the late phase of enhancement with the US contrast agent SH U 508A: early experience. Radiology 1999; 210: 409-416
• 15 Heckemann RA, Cosgrove DO, Blomley MJ et al. Liver lesions: intermittent second-harmonic gray-scale US can increase conspicuity with microbubble contrast material-early experience. Radiology 2000; 216: 592-596
• 16 Leen E, Angerson WJ, Yarmenitis S et al. Multi-centre clinical study evaluating the efficacy of SonoVue (BR1), a new ultrasound contrast agent in Doppler investigation of focal hepatic lesions. Eur J Radiol 2002; 41: 200-206
• 17 Quaia E, Calliada F, Bertolotto M et al. Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: diagnostic performance and confidence. Radiology 2004; 232: 420-430
• 18 Piscaglia F, Lencioni R, Sagrini E et al. Characterization of focal liver lesions with contrast-enhanced ultrasound. Ultrasound Med Biol 2010; 36: 531-550
• 19 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
• 20 Piscaglia F, Nolsoe C, Dietrich CF et al. The EFSUMB Guidelines and Recommendations on the Clinical Practice of Contrast Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall in Med 2012; 33: 33-59
• 21 Torzilli G, Del Fabbro D, Olivari N et al. Contrast-enhanced ultrasonography during liver surgery. Br J Surg 2004; 91: 1165-1167
• 22 Roncalli M, Roz E, Coggi G et al. The vascular profile of regenerative and dysplastic nodules of the cirrhotic liver: implications for diagnosis and classification. Hepatology 1999; 30: 1174-1178
• 23 Torzilli G, Palmisano A, Del Fabbro D et al. Contrast-enhanced intraoperative ultrasonography during surgery for hepatocellular carcinoma in liver cirrhosis: is it useful or useless? A prospective cohort study of our experience. Ann Surg Oncol 2007; 14: 1347-1355
• 24 Torzilli G. Ultrasound-Guided Liver Surgery: An Atlas. Milan: Springer-Verlag; 2014
• 25 Spolverato G, Ejaz A, Azad N et al. Surgery for colorectal liver metastases: The evolution of determining prognosis. World J Gastrointest Oncol 2013; 5: 207-221
• 26 Frankel TL, D'Angelica MI. Hepatic resection for colorectal metastases. J Surg Oncol 2014; 109: 2-7
• 27 Agrawal N, Fowler AL, Thomas MG. The routine use of intra-operative ultrasound in patients with colorectal cancer improves the detection of hepatic metastases. Colorectal Dis 2006; 8: 192-194
• 28 Machi J, Isomoto H, Kurohiji T et al. Accuracy of intraoperative ultrasonography in diagnosing liver metastasis from colorectal cancer: evaluation with postoperative follow-up results. World J Surg 1991; 15: 551-556 ; discussion 557
• 29 Conlon R, Jacobs M, Dasgupta D et al. The value of intraoperative ultrasound during hepatic resection compared with improved preoperative magnetic resonance imaging. Eur J Ultrasound 2003; 16: 211-216
• 30 Donadon M, Botea F, Del Fabbro D et al. The surgical policy predicts the impact of contrast enhanced intraoperative ultrasound for colorectal liver metastases. Eur J Radiol 2008; 67: 177-178
• 31 Rydzewski B, Dehdashti F, Gordon BA et al. Usefulness of intraoperative sonography for revealing hepatic metastases from colorectal cancer in patients selected for surgery after undergoing FDG PET. Am J Roentgenol Am J Roentgenol 2002; 178: 353-358
• 32 Sietses C, Meijerink MR, Meijer S et al. The impact of intraoperative ultrasonography on the surgical treatment of patients with colorectal liver metastases. Surg Endosc 2010; 24: 1917-1922
• 33 Tamandl D, Herberger B, Gruenberger B et al. Adequate preoperative staging rarely leads to a change of intraoperative strategy in patients undergoing surgery for colorectal cancer liver metastases. Surgery 2008; 143: 648-657
• 34 van Vledder MG, Pawlik TM, Munireddy S et al. Factors determining the sensitivity of intraoperative ultrasonography in detecting colorectal liver metastases in the modern era. Ann Surg Oncol 2010; 17: 2756-2763
• 35 Torzilli G, Procopio F, Botea F et al. One-stage ultrasonographically guided hepatectomy for multiple bilobar colorectal metastases: a feasible and effective alternative to the 2-stage approach. Surgery 2009; 146: 60-71
• 36 DeOliveira ML, Pawlik TM, Gleisner AL et al. Echogenic appearance of colorectal liver metastases on intraoperative ultrasonography is associated with survival after hepatic resection. J Gastrointest Surg 2007; 11: 970-976 ; discussion 976
• 37 Torzilli G, Botea F, Donadon M et al. Criteria for the selective use of contrast-enhanced intra-operative ultrasound during surgery for colorectal liver metastases. (Oxford): HPB; 2014. 16. 994-1001
• 38 Yoshidome H, Kimura F, Shimizu H et al. Interval period tumor progression: does delayed hepatectomy detect occult metastases in synchronous colorectal liver metastases?. J Gastrointest Surg 2008; 12: 1391-1398
• 39 Fioole B, de Haas RJ, Wicherts DA et al. Additional value of contrast enhanced intraoperative ultrasound for colorectal liver metastases. Eur J Radiol 2008; 67: 169-176
• 40 Leen E, Ceccotti P, Moug SJ et al. Potential value of contrast-enhanced intraoperative ultrasonography during partial hepatectomy for metastases: an essential investigation before resection?. Ann Surg 2006; 243: 236-240
• 41 Torzilli G, Del Fabbro D, Palmisano A et al. Contrast-enhanced intraoperative ultrasonography during hepatectomies for colorectal cancer liver metastases. J Gastrointest Surg 2005; 9: 1148-1153 ; discussion 1153-4
• 42 Ruzzenente A, Conci S, Iacono C et al. Usefulness of contrast-enhanced intraoperative ultrasonography (CE-IOUS) in patients with colorectal liver metastases after preoperative chemotherapy. J Gastrointest Surg 2013; 17: 281-287
• 43 Schulz A, Dormagen JB, Drolsum A et al. Impact of contrast-enhanced intraoperative ultrasound on operation strategy in case of colorectal liver metastasis. Acta Radiol 2012; 53: 1081-1087
• 44 Cerwenka H, Raith J, Bacher H et al. Is intraoperative ultrasonography during partial hepatectomy still necessary in the age of magnetic resonance imaging?. Hepatogastroenterology 2003; 50: 1539-1541
• 45 Jarnagin WR, Bach AM, Winston CB et al. What is the yield of intraoperative ultrasonography during partial hepatectomy for malignant disease?. J Am Coll Surg 2001; 192: 577-583
• 46 Torzilli G, Donadon M, Marconi M et al. Systematic extended right posterior sectionectomy: a safe and effective alternative to right hepatectomy. Ann Surg 2008; 247: 603-611
• 47 Torzilli G, Palmisano A, Procopio F et al. A new systematic small for size resection for liver tumors invading the middle hepatic vein at its caval confluence: mini-mesohepatectomy. Ann Surg 2010; 251: 33-39
• 48 Torzilli G, Montorsi M, Del Fabbro D et al. Ultrasonographically guided surgical approach to liver tumours involving the hepatic veins close to the caval confluence. Br J Surg 2006; 93: 1238-1246
• 49 Donadon M, Costa G, Gatti A et al. Thoracoabdominal approach in liver surgery: how, when, and why. Updates Surg 2014; 66: 121-125
• 50 Donadon M, Procopio F, Torzilli G. Tailoring the area of hepatic resection using inflow and outflow modulation. World J Gastroenterol 2013; 19: 1049-1055
• 51 Torzilli G, Makuuchi M. Ultrasound-guided finger compression in liver subsegmentectomy for hepatocellular carcinoma. Surg Endosc 2004; 18: 136-139
• 52 Torzilli G, Procopio F, Cimino M et al. Anatomical segmental and subsegmental resection of the liver for hepatocellular carcinoma: a new approach by means of ultrasound-guided vessel compression. Ann Surg 2010; 251: 229-235
• 53 Torzilli G, Procopio F, Palmisano A et al. New technique for defining the right anterior section intraoperatively using ultrasound-guided finger counter-compression. J Am Coll Surg 2009; 209: e8-e11
• 54 Torzilli G, Donadon M, Palmisano A et al. Back-flow bleeding control during resection of right-sided liver tumors by means of ultrasound-guided finger compression of the right hepatic vein at its caval confluence. Hepatogastroenterology 2007; 54: 1364-1367