**2. General aspects**

Currently, there is a wide range of equipment for IOUS, probes of different types and shapes, adapted according to the type and localization of the lesion. Standard transductors for transabdominal ultrasound can also be used, but there may be some limitations on image resolution and on the large size of the transducer that do not offer optimal maneuverability [1]. Conventional transducers can be used at the beginning of the liver examination to obtain an overview of the organ anatomy [1, 11]. The transducers used in IOUS usually operate at high frequency: 7.5–10 MHz [12]. There are different shapes: linear T-shaped probes, interdigital probes, microconvex probes and more recently, T-shaped probes with trapezoidal scanning window [13]. In case of liver surgery, the ideal transducer should be a small one that can be easily manipulated in narrow spaces, with a special design to allow the probe to be held in the palm between two fingers, thus allowing the operator to have permanent contact with the surface of the liver, without omitting to scan some areas [11, 14] (**Figure 1**).

The possibility of performing intra-operative contrast ultrasound (CE-IOUS) is an important factor in choosing the ultrasound equipment. Nowadays, the most commonly used contrast agents are SonoVue (Gaseous sulfur hexafluoride, Bracco, Milan Italy) and Sonazoid (Gaseous

**Figure 2.** Intraoperative laparoscopic ultrasound of the liver. HCC on cirrhotic liver. L44LA intraoperative probe, 13–2 MHz, 36 mm, Hitachi Aloka Medical, Ltd., Japan (intraoperative aspect, from the personal archive of the authors).

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In order to ensure a good examination, the ultrasound machine should be positioned in front of the main operator, the patient (the organ to be examined) being located between the surgeon and the monitor (a collinearity between operator, organ and monitor) in order to view simultaneously the ultrasound monitor and the surgical field. The ultrasound monitor should have size and resolution large enough to allow optimal remote viewing. Examination must always begin with the inspection and palpation of the liver and of the entire peritoneal cavity. These steps should not be avoided in favor of IOUS [20]. Mobilization of the liver begins with the sectioning of suspensory ligaments, thus creating enough space to manipulate the ultrasound transducer. Worth mentioning some of the artifacts that may appear on the examination of the VIIIth and IVa liver segments after the sectioning of the cavo-hepatic adhesions. Therefore, in the case of suspected lesions located in these areas (adjacent to the cavo-hepatic region), dis-

Benign tumors can develop on a normal or steatotic liver, may be solitary or multiple, with increased echogenity (hemangiomas, focal nodular hyperplasia) or anechogenic, with posterior acoustic strengthening (serous cysts) and distinct contours (hydatid cysts), with no vascularization or characteristic circulatory pattern; may have a mass effect on liver structures or even adjacent organs. A characteristic for benign tumors is the fact that they have elastic

*Hemangiomas* are benign tumors, mostly asymptomatic, incidentally discovered. These tumors can present themselves under various echographic aspects; most commonly, are well-defined, round, hyperecogenic, homogeneous, usually small (<3 cm), and may present the posterior acoustic strengthening effect [22]. As hemangiomas grow in size, they can change their echogenicity,

perflutane, GE Healthcare, Norway/DaiichiSankyo, Japan) [11, 16–19].

section at this level should be performed only after ultrasound exploration.

**3. IOUS of the liver: benign tumors**

consistency and do not invade vascular elements [20, 21].

When necessary, IOUS can also be used in laparoscopic surgery, with special transducers suitable for this type of approach. Transducers used during laparoscopic surgery are either linear or curved, mounted at the end of a long, thin articulated arm, with a design that allows insertion and manipulation inside the trocar (**Figure 2**) [15].

**Figure 1.** Scanning the liver surface with a intraoperative mini-convex probe, 1–13 MHz, 65°, Hitachi Aloka Medical, Ltd., Japan (intraoperative aspect, from the personal archive of the authors).

**Figure 2.** Intraoperative laparoscopic ultrasound of the liver. HCC on cirrhotic liver. L44LA intraoperative probe, 13–2 MHz, 36 mm, Hitachi Aloka Medical, Ltd., Japan (intraoperative aspect, from the personal archive of the authors).

The possibility of performing intra-operative contrast ultrasound (CE-IOUS) is an important factor in choosing the ultrasound equipment. Nowadays, the most commonly used contrast agents are SonoVue (Gaseous sulfur hexafluoride, Bracco, Milan Italy) and Sonazoid (Gaseous perflutane, GE Healthcare, Norway/DaiichiSankyo, Japan) [11, 16–19].

In order to ensure a good examination, the ultrasound machine should be positioned in front of the main operator, the patient (the organ to be examined) being located between the surgeon and the monitor (a collinearity between operator, organ and monitor) in order to view simultaneously the ultrasound monitor and the surgical field. The ultrasound monitor should have size and resolution large enough to allow optimal remote viewing. Examination must always begin with the inspection and palpation of the liver and of the entire peritoneal cavity. These steps should not be avoided in favor of IOUS [20]. Mobilization of the liver begins with the sectioning of suspensory ligaments, thus creating enough space to manipulate the ultrasound transducer. Worth mentioning some of the artifacts that may appear on the examination of the VIIIth and IVa liver segments after the sectioning of the cavo-hepatic adhesions. Therefore, in the case of suspected lesions located in these areas (adjacent to the cavo-hepatic region), dissection at this level should be performed only after ultrasound exploration.

## **3. IOUS of the liver: benign tumors**

the first time in the literature in the mid-80s [3]; later, it became an exploratory technique routinely performed in specialized centers for staging liver disease and guiding surgical procedures on patients diagnosed with hepatocarcinoma on cirrhotic liver [4–7]. Studies in the 90s showed that the information provided by IOUS may modify the initial therapeutic plan

Although first reports related to laparoscopic transducers used in A-mode date back to early

Currently, there is a wide range of equipment for IOUS, probes of different types and shapes, adapted according to the type and localization of the lesion. Standard transductors for transabdominal ultrasound can also be used, but there may be some limitations on image resolution and on the large size of the transducer that do not offer optimal maneuverability [1]. Conventional transducers can be used at the beginning of the liver examination to obtain an overview of the organ anatomy [1, 11]. The transducers used in IOUS usually operate at high frequency: 7.5–10 MHz [12]. There are different shapes: linear T-shaped probes, interdigital probes, microconvex probes and more recently, T-shaped probes with trapezoidal scanning window [13]. In case of liver surgery, the ideal transducer should be a small one that can be easily manipulated in narrow spaces, with a special design to allow the probe to be held in the palm between two fingers, thus allowing the operator to have permanent contact with the

When necessary, IOUS can also be used in laparoscopic surgery, with special transducers suitable for this type of approach. Transducers used during laparoscopic surgery are either linear or curved, mounted at the end of a long, thin articulated arm, with a design that allows

**Figure 1.** Scanning the liver surface with a intraoperative mini-convex probe, 1–13 MHz, 65°, Hitachi Aloka Medical,

1964, the laparoscopic IOUS technique has been developed relatively recent [10].

surface of the liver, without omitting to scan some areas [11, 14] (**Figure 1**).

insertion and manipulation inside the trocar (**Figure 2**) [15].

Ltd., Japan (intraoperative aspect, from the personal archive of the authors).

in up to 53% of cases [8, 9].

74 Liver Research and Clinical Management

**2. General aspects**

Benign tumors can develop on a normal or steatotic liver, may be solitary or multiple, with increased echogenity (hemangiomas, focal nodular hyperplasia) or anechogenic, with posterior acoustic strengthening (serous cysts) and distinct contours (hydatid cysts), with no vascularization or characteristic circulatory pattern; may have a mass effect on liver structures or even adjacent organs. A characteristic for benign tumors is the fact that they have elastic consistency and do not invade vascular elements [20, 21].

*Hemangiomas* are benign tumors, mostly asymptomatic, incidentally discovered. These tumors can present themselves under various echographic aspects; most commonly, are well-defined, round, hyperecogenic, homogeneous, usually small (<3 cm), and may present the posterior acoustic strengthening effect [22]. As hemangiomas grow in size, they can change their echogenicity, from homogeneous to heterogeneous, with their edges becoming irregular. These features make them more difficult to differentiate from malignant tumor formations. When surgery is indicated, IOUS has the role to localize and visualize the relationships of the hemangioma with the intrahepatic structures. The surgeon can trace the hepatic resection line outside the hemangioma, minimizing hemorrhagic risk, and preserving the healthy hepatic parenchyma to its full potential. The CE-IOUS can be useful, capturing the contrast agent by the hemangioma being most of the time characteristic. Differentiation from malignant tumor formation becomes difficult for arterial hemangiomas or for those with arterio-venous shunts [21].

can compress the intrahepatic vessels with mass effect, signs of invasion, or embedding of these structures being absent [21]. IOUS has the same indications as in the case of simple cysts, being a real help for the surgeon, for establishing surgical tactics and for checking the radicality of the treatment (the content of the remaining cavity, residual content, multilocular abscesses, etc.) [25].

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IOUS finds its usefulness in liver surgery for both primary and secondary malignant lesions facilitating the detection, characterization of lesions and guiding the surgical procedure [26, 27]. Most studies have evaluated the role of IOUS for treatment of hepatocarcinomas and hepatic metastases due to colorectal cancer, these pathologies being considered the most common liver malignant lesions. Intraoperative detection and local treatment of these lesions may have

HCC is the most common primary malignancy in the liver, and is frequently associated with

Ecographically, this tumor has the appearance of a solid tumor with irregular contours, heterogeneous, uni-, or multilocular ("encephaloid form"). Typically, it invades the liver vessels, primarily the portal branches, but also the suprahepatic veins. Doppler screening usually highlights a high-speed arterial flow. Vessel distribution is irregular, disordered. CE-US shows hypercaptation in the arterial phase with a specific "washout" of contrast substance in the venous phase. In the late phase, the tumor appears as hypoechoic. This behavior is usually

In the case of HCC, IOUS is superior in detecting lesions measuring less than 1 cm, preoperative MRI having a lower sensitivity and specificity for these lesions [11, 32]. It has also been shown in several studies that CE-IOUS can modify in 19–29% of the cases the initial treatment plan [33, 34]. CE-IOUS finds its usefulness especially in cirrhotic patients when it comes to differential diagnosis between malignant lesions and regenerative nodules [29, 35]. It has been demonstrated that neoangiogenesis of tumor nodules is a specific criteria for distinguishing

CE-IOUS has a sensitivity of 100%, a specificity between 69 and 100% and can modify the surgical strategy in up to 79% of patients [36–38], most frequently by detecting new lesions. The literature emphasizes that the filling pattern of the contrast agent in nodules found by IOUS can guide surgical resection [36]. It has also been shown that the vascular pattern of HCC visualized by using CE-IOUS has been associated with the expression of some genetic profiles, suggesting that CE-IOUS images can be used as an indicator for predicting prognosis of patients [39]. During hepatic resection, which is the standard treatment for HCC, particular attention should be paid in preserving as much hepatic parenchyma as we can, the remaining hepatic volume being an important prognostic factor for the short outcome [37, 39, 40]. Thus, local resection of the tumor formation or its ablation under IOUS guidance may be chosen to minimize the

**4. IOUS of the liver: malignant tumor**

a major impact in choosing surgical strategy [28, 29].

described in tumor nodules larger than 2 cm [21].

hepatocarcinomas from dysplastic or regenerative nodules [35].

**4.1. Hepatocarcinoma (HCC)**

cirrhosis [30, 31].

For *focal nodular hyperplasia*, the central location of a fibrous scar is characteristic. This tumor appears as a well-defined lesions with variable size, usually unique, of solid consistency and inhomogeneous structure. Rarely, the central scar can be distinguished when using simple ultrasound, without contrast agent. When using CE-IOUS, in the arterial phase, there is a central filling followed by a complete capture in the venous phase. At this stage, the center of the tumor becomes hypoechoic. In the late phase, the tumor remains isogenic together with the hepatic parenchyma, which strengthens the diagnosis of benign lesion [21].

*Hepatic adenoma* appears ecographically as a well-defined solid tumor lesion; it may have an inhomogeneous structure in the presence of intratumoral hemorrhage. Doppler ultrasound does not detect a vascular signal. When using CE-IOUS, in the arterial phase, there is a centripetal and inconsistent capture; in the venous phase, a moderate washout may be noted. In the late phase, the appearance is isoechoic or hyperechoic [21].

Differentiation between focal nodular hyperplasia and hepatic adenoma is important for establishing the therapeutic indication, surgery being indicated for large adenomas, due to the risk of rupture and hemorrhage as well as due to its malignant potential.

Because sometimes it is difficult to make a benign-malignant US differentiation, intraoperatory, when the situation imposes, might by necessary to make a bioptic puncture for establishing a correct diagnosis [20]. IOUS has an important guiding role, especially in the case of lesions located in the depth of the liver parenchyma, hard to reach when palpating.

*Simple hepatic cysts (biliary cysts)* are benign tumors with no malignant potential, usually asymptomatic, that can be easily diagnosed with ultrasound imaging. They are described by ultrasound as well-defined lesions with very thin walls, no Doppler signal, anechoic, with transonic content due to the liquid composition. Simple hepatic cysts have therapeutic indications only when they become symptomatic, often due to symptoms related to the mass effect they have on neighboring structures.

Percutaneous ultrasound guided treatment with cyst evacuation is often possible, but is followed by an increased risk of relapse, with the rebound of collection. In this idea, the laparoscopic surgical resection of the cystic dome is indicated. This technique is easy if the lesions are located superficially, in segments II, III, IVB, V, VI (after Couinaud) [23]. The lesions localized intraparenchymatous can be approached safely only when using IOUS [24].

Depending on the evolutionary stage, *hydatid cysts* may appear as single or multiple lesions, anechoic, with membranes and sediment inside, with thin or calcified walls. They may be multilocular or may contain multiple fluid compartments (daughter vesicles). IOUS helps the surgeon in finding the cysts and in some situations it can detect bile duct communication. These lesions can compress the intrahepatic vessels with mass effect, signs of invasion, or embedding of these structures being absent [21]. IOUS has the same indications as in the case of simple cysts, being a real help for the surgeon, for establishing surgical tactics and for checking the radicality of the treatment (the content of the remaining cavity, residual content, multilocular abscesses, etc.) [25].
