Abstract
Hepatectomy had a high mortality rate in the previous decade because of inadequate techniques, intraoperative blood loss, liver function reserve misdiagnoses, and accompanying postoperative complications. However, the development of several modalities, including intraoperative ultrasonography (IOUS), has made hepatectomy safer. IOUS can provide real-time information regarding the tumor position and vascular anatomy of the portal and hepatic veins. Systematic subsegmentectomy, which leads to improved patient outcomes, can be performed by IOUS in open and laparoscopic hepatectomy. Although three-dimensional (3D) computed tomography and gadoxetic acid-enhanced magnetic resonance imaging have been widely used, IOUS and contrast-enhanced IOUS are important modalities for risk analyses and making decisions regarding resectability and operative procedures because of the vital anatomical information provided and high sensitivity for liver tumors, including “disappearing” liver metastases. Intraoperative color Doppler ultrasonography can be used to delineate the vascular anatomy and evaluate the blood flow volume and velocity in hepatectomy patients and recipients of deceased- and living-donor liver transplantation after vessel reconstruction and liver positioning. For liver surgeons, IOUS is an essential technique to perform highly curative hepatectomy safely, although recent advances have also been made in virtual modalities, such as real-time virtual sonography with 3D visualization.
Similar content being viewed by others
Abbreviations
- IOUS:
-
Intraoperative ultrasonography
- 3D-CT:
-
Three-dimensional computed tomography
- EOB-MRI:
-
Gadoxetic acid-enhanced magnetic resonance imaging
- HCC:
-
Hepatocellular carcinoma
- ICG:
-
Indocyanine green
- PTCD:
-
Percutaneous transhepatic cholangial drainage
- RVS:
-
Real-time virtual sonography
- MIPS:
-
Medical imaging projection system
- CTAP:
-
CT during arterial portography
- CE-IOUS:
-
Contrast-enhanced IOUS
- DLM:
-
“Disappearing” liver metastasis
References
Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Tahara M, Yamashita K, et al. Perioperative management of hepatic resection toward zero mortality and morbidity: analysis of 793 consecutive cases in a single institution. J Am Coll Surg. 2010;211(4):443–9.
Kamiyama T, Nakagawa T, Nakanishi K, Kamachi H, Onodera Y, Matsushita M, et al. Preoperative evaluation of hepatic vasculature by three-dimensional computed tomography in patients undergoing hepatectomy. World J Surg. 2006;30(3):400–9.
Uchida K, Taniguchi M, Shimamura T, Suzuki T, Yamashita K, Ota M, et al. Three-dimensional computed tomography scan analysis of hepatic vasculatures in the donor liver for living donor liver transplantation. Liver Transpl. 2010;16(9):1062–8.
Asiyanbola B, Chang D, Gleisner AL, Nathan H, Choti MA, Schulick RD, et al. Operative mortality after hepatic resection: are literature-based rates broadly applicable? J Gastrointest Surg. 2008;12(5):842–51.
Ezaki T, Stansby GP, Hobbs KE. Intraoperative ultrasonographic imaging in liver surgery: a review. HPB Surg. 1990;3(1):1–4.
Kokudo N, Takemura N, Ito K, Mihara F. The history of liver surgery: achievements over the past 50 years. Ann Gastroenterol Surg. 2020;4(2):109–17.
Takayama T, Makuuchi M. Intraoperative ultrasonography and other techniques for segmental resections. Surg Oncol Clin N Am. 1996;5(2):261–9.
Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet. 1985;161(4):346–50.
Shindoh J, Makuuchi M, Matsuyama Y, Mise Y, Arita J, Sakamoto Y, et al. Complete removal of the tumor-bearing portal territory decreases local tumor recurrence and improves disease-specific survival of patients with hepatocellular carcinoma. J Hepatol. 2016;64(3):594–600.
Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Matsushita M, Todo S. The impact of anatomical resection for hepatocellular carcinoma that meets the Milan criteria. J Surg Oncol. 2010;101(1):54–60.
Castaing D, Garden OJ, Bismuth H. Segmental liver resection using ultrasound-guided selective portal venous occlusion. Ann Surg. 1989;210(1):20–3.
Bismuth H, Castaing D, Garden OJ. The use of operative ultrasound in surgery of primary liver tumors. World J Surg. 1987;11(5):610–4.
Izumi K, Stein PD, Goldstein S. Sustained slow sinus rhythm entrained by retrograde atrial impulses. J Biomed Eng. 1993;15(4):349–52.
Parker GA, Lawrence W, Horsley JS, Neifeld JP, Cook D, Walsh J, et al. Intraoperative ultrasound of the liver affects operative decision making. Ann Surg. 1989;209(5):569–76.
Bloed W, van Leeuwen MS, Borel Rinkes IH. Role of intraoperative ultrasound of the liver with improved preoperative hepatic imaging. Eur J Surg. 2000;166(9):691–5.
Watanapa P, Hargrove NS, Sirivatanauksorn Y. The potential role of intraoperative ultrasonography in the surgical treatment of hilar cholangiocarcinoma. HPB Surg. 1996;9(2):93–6.
Papadimitriou JD, Fotopoulos AC, Prahalias AA, Vassiliou JG, Papadimitriou LJ. The impact of new technology on hepatic resection for malignancy. Arch Surg. 2001;136(11):1307–13.
Torzilli G, Montorsi M, Donadon M, Palmisano A, Del Fabbro D, Gambetti A, 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(4):517–28.
Torzilli G, Montorsi M, Gambetti A, Del Fabbro D, Donadon M, Bianchi P, et al. Utility of the hooking technique for cases of major hepatectomy. Surg Endosc. 2005;19(8):1156–7.
Gugenheim J, Mazza D, Katkhouda N, Goubaux B, Mouiel J. Laparoscopic resection of solid liver tumours. Br J Surg. 1996;83(3):334–5.
Berends FJ, Meijer S, Prevoo W, Bonjer HJ, Cuesta MA. Technical considerations in laparoscopic liver surgery. Surg Endosc. 2001;15(8):794–8.
Kaneko H, Takagi S, Shiba T. Laparoscopic partial hepatectomy and left lateral segmentectomy: technique and results of a clinical series. Surgery. 1996;120(3):468–75.
Buell JF, Koffron AJ, Thomas MJ, Rudich S, Abecassis M, Woodle ES. Laparoscopic liver resection. J Am Coll Surg. 2005;200(3):472–80.
Koffron AJ, Auffenberg G, Kung R, Abecassis M. Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg. 2007;246(3):385–92.
Santambrogio R, Opocher E, Ceretti AP, Barabino M, Costa M, Leone S, et al. Impact of intraoperative ultrasonography in laparoscopic liver surgery. Surg Endosc. 2007;21(2):181–8.
Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261(4):619–29.
Santambrogio R, Aldrighetti L, Barabino M, Pulitano C, Costa M, Montorsi M, et al. Laparoscopic liver resections for hepatocellular carcinoma. Is it a feasible option for patients with liver cirrhosis? Langenbecks Arch Surg. 2009;394(2):255–64.
Araki K, Conrad C, Ogiso S, Kuwano H, Gayet B. Intraoperative ultrasonography of laparoscopic hepatectomy: key technique for safe liver transection. J Am Coll Surg. 2014;218(2):e37-41.
Kawaguchi Y, Velayutham V, Fuks D, Mal F, Kokudo N, Gayet B. Operative techniques to avoid near misses during laparoscopic hepatectomy. Surgery. 2017;161(2):341–6.
Belli G, D’Agostino A, Fantini C, Belli A, Cioffi L, Limongelli P, et al. Laparoscopic hand-assisted right hemihepatectomy by ultrasound-directed intrahepatic approach. J Hepatobiliary Pancreat Surg. 2009;16(6):781–5.
Ferrero A, Lo Tesoriere R, Russolillo N. Ultrasound liver map technique for laparoscopic liver resections. World J Surg. 2019;43(10):2607–11.
Wang X, Gao Q, Zhu X, Duan M, Zhou J, Fan J. Laparoscopic anatomical S8 segmentectomy with ICG fluorescence staining by laparoscopic ultrasound guided portal branch puncture approach. HPB. 2019;21:S214.
Sakoda M, Ueno S, Iino S, Minami K, Ando K, Kawasaki Y, et al. Pure laparoscopic subsegmentectomy of the liver using a puncture method for the target portal branch under percutaneous ultrasound with artificial ascites. Surg Laparosc Endosc Percutan Tech. 2013;23(2):e45–8.
Aoki T, Koizumi T, Mansour DA, Fujimori A, Kusano T, Matsuda K, et al. Ultrasound-guided preoperative positive percutaneous indocyanine green fluorescence staining for laparoscopic anatomical liver resection. J Am Coll Surg. 2020;230(3):e7–12.
Rhu J, Choi GS, Kim JM, Kwon CHD, Joh JW. Intraoperative ultrasonography as a guidance for dividing bile duct during laparoscopic living donor hepatectomy. Ann Transplant. 2019;24:115–22.
Satou S, Aoki T, Kaneko J, Sakamoto Y, Hasegawa K, Sugawara Y, et al. Initial experience of intraoperative three-dimensional navigation for liver resection using real-time virtual sonography. Surgery. 2014;155(2):255–62.
Lv A, Li Y, Qian HG, Qiu H, Hao CY. Precise navigation of the surgical plane with intraoperative real-time virtual sonography and 3D Simulation In Liver Resection. J Gastrointest Surg. 2018;22(10):1814–8.
Beller S, Hunerbein M, Eulenstein S, Lange T, Schlag PM. Feasibility of navigated resection of liver tumors using multiplanar visualization of intraoperative 3-dimensional ultrasound data. Ann Surg. 2007;246(2):288–94.
Yasuda J, Okamoto T, Onda S, Fujioka S, Yanaga K, Suzuki N, et al. Application of image-guided navigation system for laparoscopic hepatobiliary surgery. Asian J Endosc Surg. 2020;13(1):39–45.
Teatini A, Pelanis E, Aghayan DL, Kumar RP, Palomar R, Fretland AA, et al. The effect of intraoperative imaging on surgical navigation for laparoscopic liver resection surgery. Sci Rep. 2019;9(1):18687.
Nishino H, Hatano E, Seo S, Nitta T, Saito T, Nakamura M, et al. Real-time navigation for liver surgery using projection mapping with indocyanine green fluorescence: development of the novel medical imaging projection system. Ann Surg. 2018;267(6):1134–40.
Aoki T, Murakami M, Koizumi T, Matsuda K, Fujimori A, Kusano T, et al. Determination of the surgical margin in laparoscopic liver resections using infrared indocyanine green fluorescence. Langenbecks Arch Surg. 2018;403(5):671–80.
Fortunato L, Clair M, Hoffman J, Sigurdson ER, Sauter ER, Barber LW, et al. Is CT portography (CTAP) really useful in patients with liver tumors who undergo intraoperative ultrasonography (IOUS)? Am Surg. 1995;61(7):560–5.
Arita J, Ono Y, Takahashi M, Inoue Y, Takahashi Y, Matsueda K, et al. Routine preoperative liver-specific magnetic resonance imaging does not exclude the necessity of contrast-enhanced intraoperative ultrasound in hepatic resection for colorectal liver metastasis. Ann Surg. 2015;262(6):1086–91.
Arita J, Ono Y, Takahashi M, Inoue Y, Takahashi Y, Saiura A. Usefulness of contrast-enhanced intraoperative ultrasound in identifying disappearing liver metastases from colorectal carcinoma after chemotherapy. Ann Surg Oncol. 2014;21(Suppl 3):S390–7.
Torzilli G, Del Fabbro D, Palmisano A, Donadon M, Bianchi P, Roncalli M, et al. Contrast-enhanced intraoperative ultrasonography during hepatectomies for colorectal cancer liver metastases. J Gastrointest Surg. 2005;9(8):1148–53.
Leen E, Ceccotti P, Moug SJ, Glen P, MacQuarrie J, Angerson WJ, et al. Potential value of contrast-enhanced intraoperative ultrasonography during partial hepatectomy for metastases: an essential investigation before resection? Ann Surg. 2006;243(2):236–40.
Yanagisawa K, Moriyasu F, Miyahara T, Yuki M, Iijima H. Phagocytosis of ultrasound contrast agent microbubbles by Kupffer cells. Ultrasound Med Biol. 2007;33(2):318–25.
Forsberg F, Piccoli CW, Liu JB, Rawool NM, Merton DA, Mitchell DG, et al. Hepatic tumor detection: MR imaging and conventional US versus pulse-inversion harmonic US of NC100100 during its reticuloendothelial system-specific phase. Radiology. 2002;222(3):824–9.
Kindberg GM, Tolleshaug H, Roos N, Skotland T. Hepatic clearance of Sonazoid perfluorobutane microbubbles by Kupffer cells does not reduce the ability of liver to phagocytose or degrade albumin microspheres. Cell Tissue Res. 2003;312(1):49–54.
Watanabe R, Matsumura M, Munemasa T, Fujimaki M, Suematsu M. Mechanism of hepatic parenchyma-specific contrast of microbubble-based contrast agent for ultrasonography: microscopic studies in rat liver. Invest Radiol. 2007;42(9):643–51.
Cervone A, Sardi A, Conaway GL. Intraoperative ultrasound (IOUS) is essential in the management of metastatic colorectal liver lesions. Am Surg. 2000;66(7):611–5.
Jarnagin WR, Bach AM, Winston CB, Hann LE, Heffernan N, Loumeau T, et al. What is the yield of intraoperative ultrasonography during partial hepatectomy for malignant disease? J Am Coll Surg. 2001;192(5):577–83.
Conlon R, Jacobs M, Dasgupta D, Lodge JP. The value of intraoperative ultrasound during hepatic resection compared with improved preoperative magnetic resonance imaging. Eur J Ultrasound. 2003;16(3):211–6.
van Vledder MG, de Jong MC, Pawlik TM, Schulick RD, Diaz LA, Choti MA. Disappearing colorectal liver metastases after chemotherapy: should we be concerned? J Gastrointest Surg. 2010;14(11):1691–700.
Auer RC, White RR, Kemeny NE, Schwartz LH, Shia J, Blumgart LH, et al. Predictors of a true complete response among disappearing liver metastases from colorectal cancer after chemotherapy. Cancer. 2010;116(6):1502–9.
Ferrero A, Langella S, Russolillo N, Vigano L, Lo Tesoriere R, Capussotti L. Intraoperative detection of disappearing colorectal liver metastases as a predictor of residual disease. J Gastrointest Surg. 2012;16(4):806–14.
Tani K, Shindoh J, Akamatsu N, Arita J, Kaneko J, Sakamoto Y, et al. Management of disappearing lesions after chemotherapy for colorectal liver metastases: relation between detectability and residual tumors. J Surg Oncol. 2018;117(2):191–7.
Sturesson C, Nilsson J, Lindell G, Andersson RG, Keussen I. Disappearing liver metastases from colorectal cancer: impact of modern imaging modalities. HPB (Oxford). 2015;17(11):983–7.
Park MJ, Hong N, Han K, Kim MJ, Lee YJ, Park YS, et al. Use of imaging to predict complete response of colorectal liver metastases after chemotherapy: MR imaging versus CT imaging. Radiology. 2017;284(2):423–31.
Oba A, Mise Y, Ito H, Hiratsuka M, Inoue Y, Ishizawa T, et al. Clinical implications of disappearing colorectal liver metastases have changed in the era of hepatocyte-specific MRI and contrast-enhanced intraoperative ultrasonography. HPB (Oxford). 2018;20(8):708–14.
Makuuchi M, Kawarazaki H, Iwanaka T, Kamada N, Takayama T, Kumon M. Living related liver transplantation. Surg Today. 1992;22(4):297–300.
Sano K, Makuuchi M, Miki K, Maema A, Sugawara Y, Imamura H, et al. Evaluation of hepatic venous congestion: proposed indication criteria for hepatic vein reconstruction. Ann Surg. 2002;236(2):241–7.
Makuuchi M. Living donor liver transplantation: looking back at my 30 years of experience. Surg Today. 2019;49(4):288–94.
Poon RT, Chan J, Fan ST. Left hepatic vein kinking after right trisegmentectomy: a potential cause of postoperative liver failure. Hepatogastroenterology. 1998;45(20):508–9.
Hirai I, Kubota K, Aoki T, Kato M, Seyama Y, Sakamoto Y, et al. Use of ultrasonographic demonstration of hepatic venous flow to aid decisions on venous reconstruction during hepatectomy in a patient with an inferior right hepatic vein. J Ultrasound Med. 2001;20(5):549–52.
Nagasue N, Kohno H, Chang YC, Galizia G, Hayashi T, Yukaya H, et al. Intraoperative ultrasonography in resection of small hepatocellular carcinoma associated with cirrhosis. Am J Surg. 1989;158(1):40–2.
Choi BI, Han JK, Song IS, Kim CW, Han MC, Kim ST, et al. Intraoperative sonography of hepatocellular carcinoma: detection of lesions and validity in surgical resection. Gastrointest Radiol. 1991;16(4):329–33.
Soyer P, Levesque M, Elias D, Zeitoun G, Roche A. Detection of liver metastases from colorectal cancer: comparison of intraoperative US and CT during arterial portography. Radiology. 1992;183(2):541–4.
Takeuchi N, Ramirez JM, Mortensen NJ, Cobb R, Whittlestone T. Intraoperative ultrasonography in the diagnosis of hepatic metastases during surgery for colorectal cancer. Int J Colorectal Dis. 1996;11(2):92–5.
Schmidt J, Strotzer M, Fraunhofer S, Boedeker H, Zirngibl H. Intraoperative ultrasonography versus helical computed tomography and computed tomography with arterioportography in diagnosing colorectal liver metastases: lesion-by-lesion analysis. World J Surg. 2000;24(1):43–7.
Zacherl J, Scheuba C, Imhof M, Zacherl M, Langle F, Pokieser P, et al. Current value of intraoperative sonography during surgery for hepatic neoplasms. World J Surg. 2002;26(5):550–4.
Wiering B, Ruers TJ, Krabbe PF, Dekker HM, Oyen WJ. Comparison of multiphase CT, FDG-PET and intra-operative ultrasound in patients with colorectal liver metastases selected for surgery. Ann Surg Oncol. 2007;14(2):818–26.
Nomura K, Kadoya M, Ueda K, Fujinaga Y, Miwa S, Miyagawa S. Detection of hepatic metastases from colorectal carcinoma: comparison of histopathologic features of anatomically resected liver with results of preoperative imaging. J Clin Gastroenterol. 2007;41(8):789–95.
Blyth S, Blakeborough A, Peterson M, Cameron IC, Majeed AW. Sensitivity of magnetic resonance imaging in the detection of colorectal liver metastases. Ann R Coll Surg Engl. 2008;90(1):25–8.
Wagnetz U, Atri M, Massey C, Wei AC, Metser U. Intraoperative ultrasound of the liver in primary and secondary hepatic malignancies: comparison with preoperative 1.5-T MRI and 64-MDCT. AJR Am J Roentgenol. 2011;196(3):562–8.
Berger-Kulemann V, Schima W, Baroud S, Koelblinger C, Kaczirek K, Gruenberger T, et al. Gadoxetic acid-enhanced 3.0 T MR imaging versus multidetector-row CT in the detection of colorectal metastases in fatty liver using intraoperative ultrasound and histopathology as a standard of reference. Eur J Surg Oncol. 2012;38(8):670–6.
Ruzzenente A, Conci S, Iacono C, Valdegamberi A, Campagnaro T, Bertuzzo F, et al. Usefulness of contrast-enhanced intraoperative ultrasonography (CE-IOUS) in patients with colorectal liver metastases after preoperative chemotherapy. J Gastrointest Surg. 2013;17(2):281–7.
Ferrero A, Langella S, Giuliante F, Vigano L, Vellone M, Zimmitti G, et al. Intraoperative liver ultrasound still affects surgical strategy for patients with colorectal metastases in the modern era. World J Surg. 2013;37(11):2655–63.
Donadon M, Costa G, Torzilli G. State of the art of intraoperative ultrasound in liver surgery: current use for staging and resection guidance. Ultraschall Med. 2014;35(6):500–11.
Zhang XY, Luo Y, Wen TF, Jiang L, Li C, Zhong XF, et al. Contrast-enhanced ultrasound: improving the preoperative staging of hepatocellular carcinoma and guiding individual treatment. World J Gastroenterol. 2014;20(35):12628–36.
Ellsmere J, Kane R, Grinbaum R, Edwards M, Schneider B, Jones D. Intraoperative ultrasonography during planned liver resections: why are we still performing it? Surg Endosc. 2007;21(8):1280–3.
Zhang K, Kokudo N, Hasegawa K, Arita J, Tang W, Aoki T, et al. Detection of new tumors by intraoperative ultrasonography during repeated hepatic resections for hepatocellular carcinoma. Arch Surg. 2007;142(12):1170–5.
Pazaiti A, Toutouzas KG, Papadimitriou DI, Papadopoulos BD, Papacostas LS, Strigaris KA, et al. Change in preoperative strategy based on intraoperative ultrasound findings. Int Surg. 2009;94(1):58–62.
D’Hondt M, Vandenbroucke-Menu F, Preville-Ratelle S, Turcotte S, Chagnon M, Plasse M, et al. Is intra-operative ultrasound still useful for the detection of a hepatic tumour in the era of modern pre-operative imaging? HPB (Oxford). 2011;13(9):665–9.
Mitsunori Y, Tanaka S, Nakamura N, Ban D, Irie T, Noguchi N, et al. Contrast-enhanced intraoperative ultrasound for hepatocellular carcinoma: high sensitivity of diagnosis and therapeutic impact. J Hepatobiliary Pancreat Sci. 2013;20(2):234–42.
Hoch G, Croise-Laurent V, Germain A, Brunaud L, Bresler L, Ayav A. Is intraoperative ultrasound still useful for the detection of colorectal cancer liver metastases? HPB (Oxford). 2015;17(6):514–9.
Jrearz R, Hart R, Jayaraman S. Intraoperative ultrasonography and surgical strategy in hepatic resection: what difference does it make? Can J Surg. 2015;58(5):318–22.
Acknowledgements
I would like to thank Ms. Ayumi Kondo for her assistance with this article.
Author information
Authors and Affiliations
Contributions
All authors contributed to the conception and design of the study, literature review and analysis, and drafting, critical revision, and approval of the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
We report no potential financial or other conflicts of interest and no financial support.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kamiyama, T., Kakisaka, T. & Orimo, T. Current role of intraoperative ultrasonography in hepatectomy. Surg Today 51, 1887–1896 (2021). https://doi.org/10.1007/s00595-020-02219-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00595-020-02219-9