Intraoperative and Laparoscopic Ultrasound During Liver Surgery



Fig. 15.1
T-style finger-grip intraoperative probe





IOUS of the Liver



Open Approach


The ultrasound scanner and monitor screen are placed to the right of the patient. The surgeon can begin with a small incision as it is easy to slide the hand between the liver and the diaphragm. If there are no contraindications to the planned operation, the incision can be extended and the liver mobilized to perform a complete IOUS.

The probe is placed directly on the surface of the liver. Typically, no gel is required, as the natural surface moisture of the liver is adequate for acoustic coupling. In some cases, however, some moisture on the liver surface is required. Only light pressure should be applied to the liver surface to avoid vascular compression. It is important to note that there is decreased resolution for about the first 5 mm between the probe and liver surface. In order to explore this area, probe standoff can be used with saline immersion (Fig. 15.2a, b) (refer to “Probe standoff scanning” for further information). The probe is moved in different directions by making small rotational movements around its axis. A standardized approach and technique is essential in order to ensure complete exploration of the organ. The liver is scanned completely from the upper to the caudal edge, moving from the left to the right through the entire organ in a systematic manner in order not to leave any area unexplored.

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Fig. 15.2
(a) Probe standoff technique: a saline-filled glove is placed between the probe and the liver in order to examine the superficial aspect of the liver. (b) Probe standoff (white arrow indicates saline interface) allows better visualization of superficial lesions (yellow arrows indicate lesions)

Aims of the liver ultrasound exploration are:



  • To identify tumors


  • To discover tumor thrombi and vascular invasion


  • To define the relation of these lesions with respect to the vascular anatomy

The initial step of IOUS of the liver is to identify each hepatic vein as it arises from the inferior vena cava. The probe is held in a transverse midline position on the anterior surface of the liver and angled toward the beating heart (Fig. 15.3). All three hepatic veins must be followed to their peripheral tributary branches by moving the probe along the hepatic veins’ axes.

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Fig. 15.3
The probe is angled toward the heart in order to identify hepatic veins

The next step is to identify and follow the portal pedicles in order to define segmental anatomy of the liver. This is best achieved by placing the transducer on the surface of the liver, at the level of the segment IV, and angling the transducer toward the porta hepatis. Beginning from the left of the round ligament, the left portal branches for segments 2, 3, and 4 are identified and followed. Thereafter, moving over to the right side of the round ligament, the anterior and the posterior branches of the right portal vein and the feeding vessels for segments 5, 6, 7, and 8 are identified and followed. By using the intraoperative Doppler and color flow setting, dilated bile ducts can be discriminated from adjacent vascular structures and define the flow direction. The examination is completed with ultrasound of gallbladder and the porta hepatis.


Laparoscopic Approach


As the use of laparoscopic procedures and minimally invasive surgery continues to increase, the role of IOUS during laparoscopy has become even more important. The laparoscopic approach has some limits as the surgeon is unable to palpate the liver and potential lesions. The technique of laparoscopic IOUS is similar to the open approach. The probe is introduced through a 12-mm epigastric or umbilical port for longitudinal imaging and a lateral abdominal port for transverse imaging. We use a 7.5-MHz linear-array transducer. A flexible probe is preferable as it allows better contact with the liver surface, which is limited by using a rigid probe (Fig. 15.4a, b). As in the open IOUS, the posterior segments of the liver are difficult to visualize. To explore this “blind area,” it is essential to obtain maximal medial displacement of the liver by placing the patient in the semi-lateral position with the right side elevated.

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Fig. 15.4
(a) The laparoscopic ultrasound probe with a flexible tip. (b). Angulation of the laparoscopic ultrasound probe allows for better exploration of the liver surface


Contrast-Enhanced Intraoperative Ultrasound (CE-IOUS)


There are limitations in liver ultrasound. In cirrhotic patients, IOUS is able to identify new lesions in 15–33 % of patient with hepatocellular carcinoma (HCC), which can change the surgical strategy [4, 6, 7]. On the other hand, tiny metastases from colorectal cancer may be not detected during IOUS [5].

Contrast-enhanced intraoperative ultrasound (CE-IOUS) has improved the ultrasound capability in detection and characterization of hepatic nodules [8]. Second-generation microbubble contrast agents have further improved the sensitivity of CE-IOUS [9, 10]. The microbubble is an ideal ultrasound contrast agent as it is extremely echogenic, as well as biocompatible, multifunctional, and inexpensive. Microbubbles are gas spheres between 0.1 and 10 μm in diameter and are much smaller than the wavelength of diagnostic ultrasound, which is typically 100–1,000 μm [11]. The gas core has a low density and is highly compressible, allowing it to shrink and expand with the passage of an acoustic wave. The most widely used contrast agent is SonoVue (Bracco Imaging, Milan, Italy®) commercialized in Italy since the end of 2001. It is a pure intravascular contrast agent made of stabilized microbubbles containing sulfur hexafluoride, an echogenic and poorly soluble gas. Microbubbles have approximately the same size of red blood cells and are able to move into the vessels, but not through the vascular endothelium into the interstitial space. Recently, a new ultrasound contrast agent, Sonazoid (GE Healthcare, Oslo, Norway ®), has been developed, but it is not available in every country. It accumulates in hepatic Kupffer cells, providing a parenchyma-specific image in addition to demonstrating tumor vascularity [12, 13]. IOUS is initially performed in order to search for new nodules and to establish a surgical strategy. Following IOUS, CE-IOUS is performed in order to detect new nodules. CE-IOUS is also performed at the end of restorative face of liver transplantation (LT) in order to check the vascular anastomoses patency and the parenchyma perfusion. We use a dedicated probe for CE-IOUS and utilize SonoVue as contrast agent. The anesthesiologist injects 4.8 ml of SonoVue through a peripheral vein, which is followed by 10 ml of normal saline. The ultrasound is then performed using an US machine, which has contrast-specific software. Each phase of the ultrasound examination is recorded (arterial phase, portal phase, and late phase) (Fig. 15.5a, b). (Refer to section “Intraoperative contrast-enhanced ultrasound” in Chap.​ 23, for further information.)

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Fig. 15.5
Contrast-enhanced intraoperative ultrasound (CE-IOUS). (a) Arterial and portal features after injection of SonoVue. Portal bifurcation (PB) is showed by white arrow. (b) Hepatic veins in the late phase of CE-IOUS: right hepatic vein (RHV), middle hepatic vein (MHV), and left hepatic vein (LHV)



Normal Anatomy


Knowledge of the anatomy of the liver is very important in order to understand and analyze under ultrasound the different aspects of the hepatic parenchyma, segmental anatomy, and structures, such as the vessels and biliary tract.


Ultrasound Anatomy of the Liver


The normal liver parenchyma is of a medium echogenicity and is made of many thin spots creating a homogenous appearance. In comparison to the kidney, the liver is less echogenic. However, in the case of steatosis, there is an increase in liver echogenicity as compared to the kidney. The liver surface is normally very smooth. Irregular and nodular appearance with protrusions or indentations are typical features found in liver cirrhosis.


Segmental Anatomy of the Liver


The liver is a large organ without many landmarks. Its blood vessels are not identified or defined on the surface. These difficulties in defining liver anatomy and its vasculature can be resolved by performing IOUS. The importance of the intrahepatic vasculature as a guide for the recognition of the segmental anatomy of the liver is extremely important for liver resection and, in particular, for repeat liver resection. In cases of repeat liver resection, the liver surface is different and IOUS is paramount in defining the segmental anatomy and vasculature. IOUS is also very useful for marking vessels on the liver surface to guide the resection and to perform anatomic hepatectomies. To obtain the most useful information by performing IOUS, the surgeon must be familiar with the relevant intraoperative and vascular anatomy and the spectrum of normal and abnormal findings.

Segmental anatomy of the liver is based on the hepatic veins and the intrahepatic branches of portal system. As described by Healy and Schroy, hepatic territories are defined as Glissonian segments, which are based on Glissonian pedicles with an arterial branch, portal branch, and intrahepatic bile duct [14]. The pedicles are surrounded by the intrahepatic extension of the Glisson’s capsule that covers the liver surface. Alternatively, Couinaud described eight liver segments, whereby the left liver consists of segments 2, 3, and 4 and the right liver consists of segments 5, 6, 7, and 8 [15]. Note that in this terminology, the left lobe consists of segments 2 and 3 and the right lobe consists of the right liver (segments 5, 6, 7, and 8) and segment 4. The left hepatic vein travels between segments 2 and 3 in the left lobe. The middle hepatic vein divides the left and the right livers, whereby the right hepatic vein divides the right liver into the anterior sector (5 and 8) and the posterior sector (6 and 7) (Figs. 15.6 and 15.7).

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Fig. 15.6
Liver anatomy according to Couinaud segmentation. The middle hepatic vein (MHV) divides the right and left livers. The left hepatic vein (LHV) runs between segments 2 and 3


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Fig. 15.7
The right liver is divided by the right hepatic vein (RHV): the anterior sector (AS) and the posterior sector (PS)

The hepatic veins are identified beginning at their junctions with the IVC and are followed along their main axes. The hepatic veins divide the liver into different sectors. The plane between the middle hepatic vein and the IVC (inferior vena cava) divides the right (supplied by the right portal vein) and the left hepatic parenchymas (supplied by the left portal vein) (Fig. 15.6). The junction between the IVC and hepatic veins is easy to identify (Fig. 15.8). Since they are not surrounded by Glisson’s capsule, the walls of the hepatic veins are recognized as a thin echogenic line. Typically, the left and the middle hepatic veins have a common trunk (Fig. 15.8). Several branches including one large posterior and some small anterior tributaries usually form the left hepatic vein. Two anterior veins from segments 4 and 5 form the middle hepatic vein. Less frequently, there are small veins draining the upper part of the segment 4 and segment 8 into the middle hepatic vein. As indicated above, the plane between the IVC and the middle hepatic vein splits the liver in two different parts, each with its own portal supply. The line passing through this plane is called main portal scissure and is very useful to discriminate the limit between the right and left hepatectomies.

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Fig. 15.8
The common trunk (CT) is formed by the left (LHV) and middle (MHV) hepatic veins to empty into the inferior vena cava (IVC)

The junction between the IVC and the right hepatic vein is located on the right side of the IVC and typically (70 %) consists of a single large trunk (Figs. 15.9 and 15.10). There are usually three or four hepatic veins which drain segment 1 and very difficult to recognize due to their small size. The surgeon should also recognize the location of accessory hepatic veins, as this can be clinically important. For example, a right accessory hepatic vein draining the inferior right liver allows the surgeon to preserve the inferior portion of the right liver (segments 5, 6), even in case of ligature of the right hepatic vein [16, 17]. This vein is present in 13 % and joins the IVC directly at the level of the hepatic hilum.

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Fig. 15.9
The right hepatic vein (RHV) divides the right liver in the anterior and posterior sectors


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Fig. 15.10
Here, depicted are the right hepatic vein (RHV, white arrow) and the middle hepatic vein (MHV, yellow arrow)

The portal vein is the most important element of the hepatic hilum, and the intrahepatic branches are used to determine the segmental anatomy. The portal bifurcation is easily detectable under ultrasound by placing the probe transversely over the lower portion of segment 4 targeted on the hilum and through a horizontal plane. The arterial branch and the biliary system are typically anterior and superior to the portal system and can be difficult to identify (Fig. 15.11).

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Fig. 15.11
Portal bifurcation at the hepatic hilum

Keeping the probe in the same plane and moving it toward the left side, the extrahepatic portion of the left branch of the portal vein (i.e., the horizontal portion of the left portal vein) is followed. At this level, in the posterior plane, the segment 1 portal branches are identified. The left portal vein then turns anteriorly (i.e., the umbilical portion of the left portal vein) and extends to the round ligament, where the round ligament appears as a well-defined hyperechoic zone. Here, the left portal vein terminates in a cul-de-sac named the recess of Rex (Fig. 15.12a–d). At the “elbow” of the left portal vein, the branch to segment 2 arises (Fig. 15.13). At the level of the recess of Rex, the left portal vein terminates into two branches to segment 3 (to the left) and to segment 4 (to the right) (Fig. 15.14).

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Fig. 15.12
(ad) This series of images shows the left portal vein (LPV) (a) where it extends to the round ligament and as it terminates in the recess of Rex (b) at the round ligament (RL). The round ligament appears as a well-defined hyperechoic zone (c, d)


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Fig. 15.13
The picture shows the origin of the portal branch to segment 2 (BS2)


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Fig. 15.14
Left portal vein (LPV). Portal branches to segments 3 (3) and 4 (4) can be recognized at the level of the recess of Rex (REX). Also seen here is the portal branch to segment 1 (1)

The right branch of the portal vein is short as it divides early into its anterior and posterior branches (Fig. 15.15). The anterior branch of the right portal vein is located between the right and middle hepatic veins and supplies the anterior sector of the right liver with separate branches to segments 5 and 8. The posterior trunk of the right portal vein supplies the posterior sector of the right liver but is more variable as it supplies multiple branches to segments 6 and 7. One of the most important anatomic variations of the portal system is the trifurcation of the portal vein, where the main portal vein divides into the left, right anterior, and right posterior branches. Also important is the “slipping” of the right anterior branch, where this branch arises from the left portal vein. An arterial variation that is frequently relevant is a replaced right hepatic artery, which arises from the superior mesenteric artery and travels posterior to the portal vein. A replaced or accessory left hepatic artery arising from the left gastric artery and running through the ligamentum venosum may also be encountered. Intrahepatic arteries are not usually visible but may be enlarged in the case of arterialization of the liver (pathological finding) or after a major hepatectomy. The right and left bile ducts, as well as their confluence, are normally identifiable and their typical diameter is approximately 5 mm. The peripheral bile channels are not evident unless they are dilated for pathological reasons, such as in biliary obstruction.

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Fig. 15.15
Right portal vein (RPV) and its anterior (AB-RPV) and posterior branches (PB-RPV). Also seen here is the anterior branch of right hepatic artery (AB-RHA)

The exploration of some areas of the liver is particularly challenging in the intraoperative setting.

For example, upper and lateral aspects of the right liver, whose access typically requires dissection of the falciform and triangular ligaments, can be difficult to image. In that case, it might be necessary to place the probe on the inferior surface of the liver. Lesions very close to the liver surface can also be difficult to image. In this case, a probe standoff technique, as discussed earlier, can be used or placing the probe on the opposite surface of the liver can image the lesion.


Ultrasound Features of Hepatic Tumors


IOUS can identify certain hepatic tumors due to different sonographic characteristics as compared to the normal liver parenchyma. Tumors are characterized as being an-, hyper-, or hypoechoic when compared to normal hepatic parenchyma. Anechoic (appears black) lesions are typically cystic and may be, for example, biliary cysts or hydatid cysts. Hyperechoic (appears brighter than the background liver) lesions are more commonly benign tumors such as hemangiomas and adenomas (Fig. 15.16). Less frequently, malignant lesions are hyperechoic. Finally, hypoechoic (appears darker than the background liver) lesions are typically malignant tumors (Fig. 15.17a–c), such as colorectal liver metastasis (CRLM), neuroendocrine tumor, or HCC. Homogenous isoechoic tumors are the most difficult to recognize. They may be identified only by their mass effect on neighboring vascular structures or by the presence of a hypoechoic border. Tumors may be either homo- or heterogeneous (mixed), compared to normal parenchyma, and the ultrasound beam beyond the lesion may be attenuated, increased, or completely absent. The usefulness of IOUS is even more important for unknown lesions detected intraoperatively. In this section, the ultrasound features of CRLM, HCC, and benign tumors as well as the role of IOUS in the detection of the primary and metastatic tumors will be discussed.

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Fig. 15.16
Hepatic adenoma. It appears as a hyperechoic round lesion placed side to hepatic vein without any signs of compression


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Fig. 15.17
Liver metastases. (a, b) The ultrasound characteristics of a lesion may be influenced by the degree of necrosis in response to chemotherapy. (a) This post-chemotherapy-treated colorectal liver metastasis is a heterogeneous lesion, which is predominantly hypoechoic with a central hyperechoic zone. The hyperechoic zone may represent calcification. (b) The border of the lesion is irregular as showed by red arrows. White arrows indicate the hypo- and hyperechoic characteristics of this lesion. (c) This hypoechoic lesion corresponds to a liver metastasis from neuroendocrine tumor. Note the proximity to the middle hepatic vein (MHV). RHV right hepatic vein, MHV median hepatic vein, LHV left hepatic vein, IVC inferior vena cava


Liver Metastasis


Approximately half of patients with colorectal cancer develop liver metastases [18, 19]. The only potentially curative option for these patients is surgical resection in order to reach a 5-year survival rate of 25–58 % [20, 21]. Intraoperative ultrasound has been recognized for years to be beneficial in those undergoing liver resection for colorectal liver metastases (CRLM). In particular, IOUS allows the surgeon to detect additional small CRLM not seen on preoperative cross-sectional imaging, typically those less than 2 cm and those metastases which have “disappeared” following chemotherapy (i.e., “missing” metastases). Several reports identify the additional detection rate of IOUS to be as high as 10–20 % [22, 23]. Sensitivity of more than 90 % has been reported with positive and negative predictive values of 90 and 70 %, respectively [24, 25]. Recent studies have suggested that with the improvement of preoperative imaging, there is no additional benefit of IOUS. However, Van Vledder and colleagues have demonstrated that IOUS leads to the detection of additional lesions in 10 % of patients and subsequently changes the surgical strategy in 9 % of patients [26]. Furthermore, they found that the probability of finding additional metastases varied considerably based on specific clinical and ultrasound features. Those who had more than four metastases or those who had hypoechoic lesions were found to have a higher chance of identifying additional lesions in 26 and 18 %, respectively. The detection of additional lesions may change the surgical approach and may contribute to improved outcomes. Recently, D’Hondt et al. reported that IOUS could change the operative strategy in 16.5 % of patients [27]. Furthermore, IOUS is useful to detect metastases, which have “disappeared” after chemotherapy. To improve surgical outcomes, there is an increasing trend to administer preoperative chemotherapy to patients with resectable CRLM. This leads to more patients who have a major radiological response but also leads to liver metastases which “disappear” after chemotherapy. A recent paper reports that IOUS increases the intraoperative detection of these “disappearing” metastases in more than 50 % of cases [28]. The ability of IOUS to detect additional metastases is also improved by the use of contrast agents (Fig. 15.18a, b). CE-IOUS is more sensitive than conventional IOUS for detecting CRLM [32], with a sensitivity rate reported around of 97 % [29]. Recent papers have shown that CE-IOUS leads to a change in the surgical strategy in 14–30 % of CRLM cases [30, 31].

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Fig. 15.18
Contrast-enhanced ultrasound. (a) IOUS is unable to detect this isoechoic lesion. The lesion is marked by the white arrows. (b) Following injection of contrast medium, the liver metastasis appears (white arrows and yellow +). This particular lesion had disappeared on the preoperative imaging following chemotherapy. This demonstrates the utility of CE-IOUS during standard IOUS, especially in those “missing” metastases following chemotherapy


Hepatocellular Carcinoma


HCC is the fifth most common malignancy and represents the principal cause of death of cirrhotic patients [3335]. Among the local treatments available, surgical resection is the most radical approach [3639]. Intraoperative ultrasound enables identification of new occult lesions in 15–33 % of patients with HCC, and it is responsible for a change in operative strategy in more than 15 % of cases [27, 40] (Fig. 15.19).

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Fig. 15.19
Hepatocellular carcinoma. Note that it is isoechoic (white arrow) with a hypoechoic irregular rim (red arrows)

IOUS is very important in those with cirrhosis and HCC. The hard and irregular surface of the cirrhotic liver makes detection of liver lesions by palpation very difficult, especially in the case of deep and small HCC [49]. Furthermore, atrophy or hypertrophy of the cirrhotic liver can make the localization of liver lesions and the definition of the liver vascularization more difficult. The use of IOUS allows for parenchymal-sparing resection and limits the number of patients undergoing major hepatectomy [50, 51].

However, IOUS has some limitations. In cirrhotic patients, less than half of the new lesions detected by IOUS are HCC. These lesions may be benign, which include regenerative and dysplastic nodules. The diagnosis of HCC is a critical point in cirrhotic patients to avoid resection and sacrifice of functioning parenchyma. In those with cirrhosis, the possibility to assess the vascularity of nodules detected by IOUS may improve the ability in discriminating malignant from benign lesions. In fact, except for those nodules with a mosaic ultrasound pattern, which are malignant in 80 % of cases, only 24–30 % of hypoechoic and 0–1 % of hyperechoic nodules are malignant when evaluating for HCC [4, 6]. A needle biopsy of a new lesion can be performed, but the false-negative rate is as high as 30 % [4042]. Furthermore, a needle biopsy can lead to tumor seeding and ultimately may worsen the prognosis of a patient [4345]. The analysis of a nodule’s vascularity may provide the crucial information for differentiation.

Recently, CE-IOUS has been reported to evaluate tumor vascularization as is done with other contrast imaging modalities [46, 47]. CE-IOUS using SonoVue has been advocated as an alternative to differentiate HCC from benign lesions found during IOUS [7]. Using CE-IOUS, a change in the surgical strategy has been reported in 35–79 % of cases [7, 48]. Even using the newer contrast agent Sonazoid, CE-IOUS is able to detect new lesions in more than 20 % of cirrhotic patients. In a prospective study, Arita and colleagues showed that the sensitivity and specificity of CE-IOUS with Sonazoid for differentiating HCC were 65 and 94 %, respectively, and with an accuracy of 87 % [40]. (Refer to section “Intraoperative contrast-enhanced ultrasound” in Chap.​ 23, for further information.)
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Jan 3, 2017 | Posted by in ABDOMINAL MEDICINE | Comments Off on Intraoperative and Laparoscopic Ultrasound During Liver Surgery
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