Laparoscopic ultrasound of the liver

European Journal of Ultrasound 12 (2000) 169 – 177 www.elsevier.com/locate/ejultrasou Clinical Science: Review Paper Laparoscopic ultrasound of the liver Jean-Marc Catheline *, Richard Turner, Gérard Champault Department of Surgery, Hôpital Jean Verdier, ‘AP-HP’, A6enue du 14 juillet, F-93143 Bondy, France Received 10 March 2000; received in revised form 25 July 2000; accepted 7 August 2000 Abstract Objecti6e: despite recent advances in medical imaging, pre-operative evaluation of liver tumors, whether benign or malignant, is often lacking in accuracy and precision. With the development of surgical laparoscopy, the benefits of diagnostic laparoscopy have been combined with those of operative ultrasound. This article aims to describe the technique of laparoscopic ultrasound of the liver, and to define its applications and the role of its association with diagnostic laparoscopy in the localization and assessment for resectability of liver tumors. Methods: after an initial visual inspection with the laparoscope, laparoscopic ultrasound is utilized to further examine the liver. This relies largely on recognition of branches of the portal vein and tributaries of the hepatic veins. During this procedure, the hepatic parenchyma is also examined. Minimal displacement of the transducer, using clockwise and anti-clockwise rotatory movements, allows a full exploration of the liver. Results: the combination of visual with sonographic laparoscopy allows accurate localization of benign and malignant hepatic tumors, as well as ultrasound-guided biopsies of these. Laparoscopic ultrasound can detect small lesions previously unseen by pre-operative imaging techniques. The relationship of tumors to adjacent blood vessels can be defined. Portal vein thrombosis can be diagnosed. Conclusion: curability and liver tumor resectability can be determined and the appropriate surgical treatment thus planned. © 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Laparoscopy; Laparoscopic ultrasound; Liver tumor 1. Introduction Despite recent advances in medical imaging, the pre-operative evaluation of liver tumors is often * Corresponding author. Tel.: + 33-1-48026180; fax: + 331-48026161. E-mail address: [email protected] (J.M. Catheline). still lacking in accuracy and precision (Tubiana et al., 1992; John et al., 1994; Lo et al., 1998). The principal objective of the surgeon is to identify those tumors that are amenable to curative resection with low risk. It sometimes happens that lesions which appear resectable on the basis of pre-operative imaging, are not so at operation (Adson, 1987; Makuuchi et al., 1987; Babineau et al., 1994). 0929-8266/00/$ - see front matter © 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 9 2 9 - 8 2 6 6 ( 0 0 ) 0 0 1 1 2 - 9 170 J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 In laparotomies for liver tumors, intra-operative ultrasound has been shown to provide accurate information on tumor invasion and the relationship of the tumor with the intra-hepatic portal veins (Castaing et al., 1986), thus aiding eventual resection (Bismuth et al., 1987). The use of contact ultrasound for the detection of liver metastases of other digestive tract cancers is also well-documented (Cuesta et al., 1993; Goletti et al., 1998). The detection of occult metastases, unseen by pre-operative imaging, is crucial for the optimal management of these patients, and can be facilitated by intra-operative ultrasound (Harbin et al., 1980; Finlay and Mc Ardle, 1983; Hunerbein et al., 1998). The advent of laparoscopic surgery has enabled the benefits of diagnostic laparoscopy and intraoperative ultrasound to be combined (John and Garden, 1994). The visual inspection afforded by diagnostic laparoscopy detects small hepatic and peritoneal metastases (Cuschieri et al., 1978; Lightdale, 1982). The discovery of such unresectable disease at laparoscopy avoids needless and potentially morbid laparotomy (Jeffers et al., 1988). Nevertheless, simple diagnostic laparoscopy is limited to the surfaces of accessible organs. The recent development of high frequency ultrasound probes, adapted for laparoscopy and permitting direct acoustic contact with Glisson’s capsule, has added a further dimension to the evaluation of tumor spread (Miles et al., 1992). The aim of this paper is to report the technique of laparoscopic ultrasound of the liver and to define its role in the assessment of extent and resectability of hepatic lesions. 2. Methods 2.1. Technical considerations The technique of laparoscopic ultrasound of the liver is based on that of conventional intra-operative ultrasound (Machi et al., 1987; Charnley et al., 1991; Lau et al., 1993). However, the image obtained is oriented longitudinally rather than transversely. The ultrasound probe is introduced into the peritoneal cavity via a 10-mm port situ- ated at the umbilicus or at that level in the right mid-clavicular or anterior axillary lines. The camera and probe can be shifted between ports to allow optimal access to different parts of the liver. In order to avoid damage to the fragile probe, it is preferable to use ports with magnetic trapdoor valves rather than trumpet valves. Commercially available probes are capable of exploring the entire liver, including the dome and the termination of the hepatic veins in the inferior vena cava. They also provide high quality images (Mosnier, 1993; Foley et al., 1998). The probe has a flexible tip with a convex surface which permits examination of a sufficiently wide surface (4 cm) for easy interpretation. Compression of the liver by the transducer must be avoided, as this may alter the quality of the image. A number of frequencies can be employed depending on the tissue penetration required. Better acoustic contact, due to the angulation of the probe, tends to compensate for the difficulty sometimes encountered when trying to move the port within the elastic resistance of the abdominal wall. The angling of the port being limited, the mobility of the transducer is aided by clockwise and anti-clockwise rotatory movements. Placement of the probe is guided by visualization with the camera, but sometimes the view can be obscured by the round and falciform ligaments. In fact, the surgeon ‘sonographer’ with sufficient experience, comes to be guided by the images on the ultrasound screen itself. The initial ultrasound is carried out in classical B mode (gray). For better identification of anatomical structures, color and pulsed Doppler are employed. This is indispensable for differentiating between bile ducts, arteries and veins, and also for determining the direction of flow. To avoid artefacts, movements must be extremely slow when using the colour Doppler. Dynamic or static images can be recorded on video, computer disk or paper. Apart from certain prototypes and a recently commercially available probe with an operating channel (Ultra Sound Laparoscopic Transducer 8566, B&K Medical, France), current commercially available probes do not have an operating channel enabling biopsies. These must be performed with the aid of needles passed transparietally according to the technique J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 171 described by Bonhof et al. (1994). The needle is introduced into the liver carefully avoiding the portal and hepatic veins. The use of needles with a striated tip is recommended to provide better sonographic visibility (Bonhof et al., 1994). The advancement of the ‘shining’ signal representing the tip of the needle, is followed on the ultrasound screen. Our recent experience suggests that it is much easier to perform biopsies using a probe with an operating channel. The sonographic exploration of the liver depends on the recognition of the portal vein branches and the tributaries of the hepatic veins. During the vascular exploration, the nature of the corresponding parenchyma is also noted. Knowledge of the normal orientation of blood vessels in the liver is essential for the precise localization of intra-hepatic lesions (Gozzetti et al., 1986; Stadler et al., 1991). Exploration begins in a sagittal plane, then continues following the vascular elements while rotating the probe in a clockwise and anti-clockwise fashion. bladder (segment V) (Fig. 5) where the middle hepatic vein can be found and followed to its junction with the inferior vena cava. The probe placed on segment VIII (Fig. 6) allows all three hepatic veins (right, middle and left) to be viewed successively by axial rotation of the probe. Displacing and rotating the probe to the right (clockwise rotation), shows the right hepatic vein (Fig. 7). Visualization of segment VII is difficult and necessitates angling the probe over the convex upper surface of the liver. The right hepatic vein is followed from segment VII through to segment VI, which is easily recognized because it is in contact with the right kidney (Fig. 8). The examination of the liver is completed by viewing the hepatic pedicle (Catheline et al., 1999). The probe placed on the anterolateral surface of the pedicle enables visualization of the bile duct, portal vein, and hepatic artery. Porta hepatis lymphadenopathy and portal vein thrombosis can thus be detected. 2.2. Imaging according to li6er segmentation 3. Clinical applications The transducer is first placed on the anterior surface of segment IV (Fig. 1). The starting point is the bifurcation of the portal vein. At this level the right and left hepatic ducts are clearly visible. The left portal branch is followed by rotating the probe in an anti-clockwise direction. Clockwise movement reveals the right branch of the portal vein, from which the anterior and posterior divisions can be followed (Fig. 2). Examination is then continued along the anterior and posterior sectorial divisions of the right portal vein throughout the remainder of the right lobe of the liver. The associated bile ducts are only visible if dilated. Hepatic artery branches are always situated anterior to the portal vein branches. The left branch of the portal vein and its segmental branches are traced throughout the left lobe of the liver. To thus examine the left lobe, the transducer must be placed on segment II (Fig. 3), then on segment III (Fig. 4). With the probe placed on segment II, segment I and the termination of the left portal branch can be visualized. Following this, the probe is placed in the region of the gall 3.1. Malignant li6er lesions 3.1.1. Hepatocellular carcinoma Primary liver tumors may appear as hyperechoic lesions with peripheral enhancement. They are particularly difficult to recognize in cirrhotic patients in which case they may be completely isoechoic and without a hypoechoic rim. In extreme cases their presence may only be detected by a distortion in the hepatic vasculature. Ultrasound examination of the cirrhotic liver is facilitated by instilling normal saline into the peritoneal cavity. This ensures better acoustic contact between the transducer and the nodular liver surface. In patients who have already had a pre-operative diagnosis of hepatocellular carcinoma, the combination of laparoscopy and laparoscopic evaluation with ultrasound guided biopsies can be performed just prior to opening the abdomen for the purpose of hepatic resection. The objective is to look for some contra-indications to resection: a benign nature of the lesion, an incurability (peri- 172 J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 173 Fig. 1. Probe placed on segment IV (IV): right hepatic duct (rhd), left hepatic duct (lhd), hepatic artery (ha), portal convergence(pc), segment I (I). Fig. 2. Probe placed on segment IV (IV) with associated clockwise rotatory movement: right paramedian portal branch (rpb), right lateral branch (rlb), left paramedian branch (lpb). Fig. 3. Probe placed on segment II (II): left portal vein (lpv), portal branch for segment II (pbsII), insertion of lesser omentum (lo), segment I (I), veina cava (vc). Fig. 4. Probe placed on free edge of segment III (III): aorta, lesser omentum (lo), cœliac trunk (ct). Fig. 5. Probe placed on segment V (V): gall bladder (gb), portal branch of segment V (pbsV). Fig. 6. Probe placed on segment VIII (VIII): right hepatic vein (rhv), middle hepatic vein (mhv), left hepatic vein (lhv), segment IV (IV). Fig. 7. Probe placed on segment VII (VII): right hepatic vein (rhv), portal branch of segment VI (pbsVI), portal branch of segment VII (pbsVII), segment V (V), segment VI (VI). Fig. 8. Probe placed on segment VI (VI): image of right kidney (rk). Fig. 9. Metastases (M) than had been estimated during the preoperative screening (hypo-echoic lesions unknown by preoperative imaging). Fig. 10. Liver metastases (M) less than 10 mm in diameter not detected by preoperative imaging. 174 J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 toneal metastases, bilobar disease, invasion of adjacent organs, lymph nodes metastases), or an irresectability (inadequat liver remnant, location precluding resection near a major vein, main portal vein tumor thrombus, inferior vena cava tumor thrombus) (Lo et al., 1998). The combination of diagnostic laparoscopy with laparoscopic ultrasound may lead to the discovery of undetected tumor sites or local tumor invasion into an adjacent portal vein branch. It also helps to precisely localize the tumor and to define its relations to adjacent blood vessels (John and Garden, 1994; Lo et al., 1998). Tumor resectability can be determined on the basis of these findings, thus minimizing the risk of needless laparotomies for unresectable tumors (John and Garden, 1994; Lo et al., 1998). Laparoscopic liver biopsy under ultrasound guidance has now become a routinely used technique. Many surgeons require that a patient undergo a tissue biopsy prior to opening the abdomen for a hepatic resection (Lo et al., 1998). 3.1.2. Li6er metastases The sonographic appearance of liver secondaries is variable. They may be hyper-, hypo-, or isoechoic, as well as being homogeneous or heterogeneous (Fig. 9). Large metastases often display a hyperechoic center with posterior shadowing due to calcifications within the lesion. Isoechoic metastases can only be identified by the distortion of intra-hepatic vessels they produce. Intra-operative ultrasound enables the detection of liver metastases at the same time as resection of a gastro-intestinal tumor (Cuesta et al., 1993; Goletti et al. 1998). In patients who have already had a pre-operative diagnosis of liver metastases, the objective is to look for some contra-indications to liver resection: a benign nature of the lesion, an incurability (peritoneal carcinomatosis, bilobar disease, more than five liver metastases, invasion of adjacent organs), or an irresectability (location precluding resection near a major vein) (John et al., 1994) The essential advantage of laparoscopic ultrasound is in the detection of lesions less than 10mm in diameter (Fig. 10) (Cuesta et al., 1993; John et al., 1994; Feld et al., 1996). Its effective- ness depends largely on the echogenicity of the surrounding normal liver. Tumor resectability can be determined on the basis of these findings, thus minimizing the risk of needless laparotomies for unresectable tumors. Contact ultrasound also facilitates interstitial therapies. For example, alcohol injection (Incarbone et al., 1998) and cryotherapy (Cuschieri et al., 1995) of metastatic tumors can both be achieved by employing ultrasound guidance. The resulting tumor necrosis can similarly be monitored by laparoscopic ultrasound. 3.2. Benign li6er lesions 3.2.1. Cysts Simple hepatic cysts are easy to recognise with laparoscopic ultrasound (Marvik et al., 1993). Solitary or multiple, they are spherical and smooth with a weakly echogenic wall. The contents of the cyst are typically anechoic, but there is posterior enhancement. Haemorrhage into such a benign cyst may alter the sonographic appearance of its contents. By placing the transducer in direct contact with the liver capsule, the depth of the cyst within the parenchyma can be determined, as well as its relationship to major blood vessels. These data are useful when considering laparoscopic fenestration of a cyst (Fabiani et al., 1991). Hydatid cysts are similarly sonolucent but are seen to contain obvious daughter cysts. The cyst wall is hyperechoic if calcified. Vascular relations are defined with the aid of color Doppler which can foresee any potential difficulties with cyst enucleation or laparoscopic liver resection (Katkhouda et al., 1992). 3.2.2. Benign solid lesions Haemangiomas, in an otherwise sonographically normal liver, are seen as strongly echogenic with posterior enhancement. Laparoscopic ultrasound can nevertheless have difficulty distinguishing large haemangiomas from malignant tumors. Focal nodular hyperplasia cannot be distinguished from malignant tumors on the findings of ultrasound alone. However, the former lesions often have a hyperechoic center due to central J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 fibrosis. Ultrasound guided biopsies must be performed (Bonhof et al., 1994). The diagnosis of an adenoma can not be made solely on ultrasound appearances. These tumors often have a sonographic appearance approaching that of focal nodular hyperplasia. Even so, laparoscopic ultrasound can accurately localize the lesion and facilitate a guided biopsy (Bonhof et al., 1994). Moreover, the principal benefit of laparoscopic ultrasound for benign lesions is in determining the most sparing and best adapted resection (laparoscopic or conventional), when operation is indicated (Cuesta et al., 1995). The use of laparoscopy for the resection of large benign lesion of the liver is not currently recommended. Despite the current availability of the laparoscopic cautery, and high flow suction and irrigation sysyems, the potential for uncontrollable bleeding from large hepatic resections remains the largest inhibiting factor in this approach. Laparoscopic hepatic resection have currently been limited to segmenties and small wedge resections of superficial or peripheral lesions under laparoscopic ultrasound guidance (Cuesta et al., 1995). 4. Results 4.1. Historical background Initially, laparoscopic ultrasound of the liver, using real time B mode, was reported by Ohta et al. (1981), Oda (1982). Once the prototypes were perfected, Frank et al. (1985) noted that laparoscopic ultrasound was capable of detecting intrahepatic lesions previously unseen by pre-operative transparietal ultrasound. With the advent of laparoscopic surgery, probes compatible with the usual ports were developed. Commercially available probes with a flexible tip allowing adequate acoustic contact represented a significant breakthrough in the uptake of this technology. Laparoscopic ultrasound was quickly seen as an important contribution to the diagnostic imaging of the liver (Miles et al., 1992). 175 4.2. Impact of laparoscopy and laparoscopic ultrasound on surgery of malignant li6er tumors The combination become a critical part of the clinical decision-making process. In a study by John et al. (1994), where 50 patients had a potentially resectable tumor, whether benign or malignant, on the basis of pre-operative investigations, laparoscopy showed the lesion to be unresectable in 23 of these (46%). Laparoscopic ultrasound was performed in 43 patients. In 14 cases (33%), laparoscopic ultrasound discovered liver tumors that were not visible on pre-operative imaging or visual laparoscopy. In 18 of the 43 patients (42%), additional staging information was also noted: involvement of both lobes of the liver (14 cases), hilar lymphadenopathy (five cases), and portal or hepatic vein invasion (five cases). On the basis of visual and sonographic exploration, only 14 patients (28%) came to laparotomy. Thirteen of these had a potentially curative resection. The authors concluded that a combination of laparoscopy and laparoscopic ultrasound was the most sensitive method for the detection of both local and regional dissemination of liver tumors. A recent study by Rahusen et al. (1999) looked at 50 patients with colorectal liver metastases judged to be resectable on the basis of pre-operative imaging. Eighteen of these (36%) were subsequently excluded from a potentially curative operation after undergoing combined visual laparoscopy and laparoscopic ultrasound. According to Cozzi et al. (1996), for the detection of liver metastases, laparoscopic ultrasound has comparable sensitivity to open intra-operative ultrasound. In a study of 91 patients with potentially resectable hepatocellular carcinomas, Lo et al. (1998) found that combined laparoscopy and laparoscopic ultrasound avoided exploratory laparotomy in 60% of patients, who were shown to have irresectable tumors. Morbidity was thus reduced, length of hospital stay shortened, and non-surgical treatments able to be instituted sooner. In addition, the mean duration of the procedure was only 20 min. The authors concluded that combined laparoscopy and laparoscopic ultrasound could avoid the morbidity associated with needless exploratory laparotomies 176 J.-M. Catheline et al. / European Journal of Ultrasound 12 (2000) 169–177 in hepatocellular carcinoma patients. They further recommended that this investigation be performed in all cases before proceeding to a potentially curative hepatic resection (Lo et al., 1998). 4.3. Impact of laparoscopy and laparoscopic ultrasound on laparoscopic surgery of benign li6er diseases The principal benefit is in determining the most sparing and best adapted resection (laparoscopic or conventional), when operation is indicated. Laparoscopic fenestration of n hepatic cyst is useful (Fabiani et al., 1991). The use of laparoscopy for the resection of large benign lesion of the liver is not currently recommended. Laparoscopic hepatic resection has currently been limited to segmental and small wedge resections of superficial or peripheral lesions under laparoscopic ultrasound guidance (Cuesta et al., 1995). 5. Conclusion To perform a liver resection, a surgeon requires precise information. Similarly, he/she must be able to accurately assess the liver for metastases before undertaking the resection of a gastro-intestinal malignancy. Liver ultrasound performed in ‘open’ surgery has demonstrated efficacy. Laparoscopic ultrasound provides the surgeon with important information which complements that of pre-operative imaging. Moreover it guides the choice of liver resection. High frequency transducers enable the detection of lesions less than 1 cm in diameter, Doppler mode defines the vascular relations of tumors, and probes with an operating channel facilitate ultrasound-guided biopsies. Laparoscopic ultrasound is indispensable for any laparoscopic liver surgery for benign disease. 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