Jean-Marc Catheline *, Richard Turner, Gerard ChampaultDepartment of Surgery, Hopital 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
Despite recent advances in medical imaging, thepre-operative evaluation of liver tumors is often
still lacking in accuracy and precision (Tubiana etal., 1992; John et al., 1994; Lo et al., 1998). Theprincipal objective of the surgeon is to identifythose tumors that are amenable to curative resec-tion with low risk. It sometimes happens thatlesions which appear resectable on the basis ofpre-operative imaging, are not so at operation(Adson, 1987; Makuuchi et al., 1987; Babineau etal., 1994).
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In laparotomies for liver tumors, intra-opera-tive ultrasound has been shown to provide accu-rate information on tumor invasion and therelationship of the tumor with the intra-hepaticportal veins (Castaing et al., 1986), thus aidingeventual resection (Bismuth et al., 1987). The useof contact ultrasound for the detection of livermetastases of other digestive tract cancers is alsowell-documented (Cuesta et al., 1993; Goletti etal., 1998). The detection of occult metastases,unseen by pre-operative imaging, is crucial for theoptimal management of these patients, and can befacilitated by intra-operative ultrasound (Harbinet al., 1980; Finlay and Mc Ardle, 1983; Huner-bein et al., 1998).
The advent of laparoscopic surgery has enabledthe benefits of diagnostic laparoscopy and intra-operative ultrasound to be combined (John andGarden, 1994). The visual inspection afforded bydiagnostic laparoscopy detects small hepatic andperitoneal metastases (Cuschieri et al., 1978;Lightdale, 1982). The discovery of such unre-sectable disease at laparoscopy avoids needlessand potentially morbid laparotomy (Jeffers et al.,1988). Nevertheless, simple diagnostic la-paroscopy is limited to the surfaces of accessibleorgans. The recent development of high frequencyultrasound probes, adapted for laparoscopy andpermitting direct acoustic contact with Glisson’scapsule, has added a further dimension to theevaluation of tumor spread (Miles et al., 1992).
The aim of this paper is to report the techniqueof laparoscopic ultrasound of the liver and todefine its role in the assessment of extent andresectability of hepatic lesions.
2. Methods
2.1. Technical considerations
The technique of laparoscopic ultrasound of theliver is based on that of conventional intra-opera-tive ultrasound (Machi et al., 1987; Charnley etal., 1991; Lau et al., 1993). However, the imageobtained is oriented longitudinally rather thantransversely. The ultrasound probe is introducedinto the peritoneal cavity via a 10-mm port situ-
ated at the umbilicus or at that level in the rightmid-clavicular or anterior axillary lines. The cam-era and probe can be shifted between ports toallow optimal access to different parts of the liver.In order to avoid damage to the fragile probe, it ispreferable to use ports with magnetic trapdoorvalves rather than trumpet valves.
Commercially available probes are capable ofexploring the entire liver, including the dome andthe termination of the hepatic veins in the inferiorvena cava. They also provide high quality images(Mosnier, 1993; Foley et al., 1998). The probe hasa flexible tip with a convex surface which permitsexamination of a sufficiently wide surface (4 cm)for easy interpretation. Compression of the liverby the transducer must be avoided, as this mayalter the quality of the image. A number of fre-quencies can be employed depending on the tissuepenetration required. Better acoustic contact, dueto the angulation of the probe, tends to compen-sate for the difficulty sometimes encounteredwhen trying to move the port within the elasticresistance of the abdominal wall. The angling ofthe port being limited, the mobility of the trans-ducer is aided by clockwise and anti-clockwiserotatory movements. Placement of the probe isguided by visualization with the camera, butsometimes the view can be obscured by the roundand falciform ligaments. In fact, the surgeon‘sonographer’ with sufficient experience, comes tobe guided by the images on the ultrasound screenitself. The initial ultrasound is carried out inclassical B mode (gray). For better identificationof anatomical structures, color and pulsedDoppler are employed. This is indispensable fordifferentiating between bile ducts, arteries andveins, and also for determining the direction offlow. To avoid artefacts, movements must be ex-tremely slow when using the colour Doppler. Dy-namic or static images can be recorded on video,computer disk or paper. Apart from certain pro-totypes and a recently commercially availableprobe with an operating channel (Ultra SoundLaparoscopic Transducer 8566, B&K Medical,France), current commercially available probes donot have an operating channel enabling biopsies.These must be performed with the aid of needlespassed transparietally according to the technique
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described by Bonhof et al. (1994). The needle isintroduced into the liver carefully avoiding theportal and hepatic veins. The use of needles witha striated tip is recommended to provide bettersonographic visibility (Bonhof et al., 1994). Theadvancement of the ‘shining’ signal representingthe tip of the needle, is followed on the ultrasoundscreen. Our recent experience suggests that it ismuch easier to perform biopsies using a probewith an operating channel.
The sonographic exploration of the liver de-pends on the recognition of the portal veinbranches and the tributaries of the hepatic veins.During the vascular exploration, the nature of thecorresponding parenchyma is also noted. Knowl-edge of the normal orientation of blood vessels inthe liver is essential for the precise localization ofintra-hepatic lesions (Gozzetti et al., 1986; Stadleret al., 1991). Exploration begins in a sagittalplane, then continues following the vascular ele-ments while rotating the probe in a clockwise andanti-clockwise fashion.
2.2. Imaging according to li6er segmentation
The transducer is first placed on the anteriorsurface of segment IV (Fig. 1). The starting pointis the bifurcation of the portal vein. At this levelthe right and left hepatic ducts are clearly visible.The left portal branch is followed by rotating theprobe in an anti-clockwise direction. Clockwisemovement reveals the right branch of the portalvein, from which the anterior and posterior divi-sions can be followed (Fig. 2). Examination isthen continued along the anterior and posteriorsectorial divisions of the right portal veinthroughout the remainder of the right lobe of theliver. The associated bile ducts are only visible ifdilated. Hepatic artery branches are always situ-ated anterior to the portal vein branches. The leftbranch of the portal vein and its segmentalbranches are traced throughout the left lobe ofthe liver. To thus examine the left lobe, the trans-ducer must be placed on segment II (Fig. 3), thenon segment III (Fig. 4). With the probe placed onsegment II, segment I and the termination of theleft portal branch can be visualized. Followingthis, the probe is placed in the region of the gall
bladder (segment V) (Fig. 5) where the middlehepatic vein can be found and followed to itsjunction with the inferior vena cava. The probeplaced on segment VIII (Fig. 6) allows all threehepatic veins (right, middle and left) to be viewedsuccessively by axial rotation of the probe. Dis-placing and rotating the probe to the right (clock-wise rotation), shows the right hepatic vein (Fig.7). Visualization of segment VII is difficult andnecessitates angling the probe over the convexupper surface of the liver. The right hepatic vein isfollowed from segment VII through to segmentVI, which is easily recognized because it is incontact with the right kidney (Fig. 8). The exami-nation of the liver is completed by viewing thehepatic pedicle (Catheline et al., 1999). The probeplaced on the anterolateral surface of the pedicleenables visualization of the bile duct, portal vein,and hepatic artery. Porta hepatis lymphadenopa-thy and portal vein thrombosis can thus bedetected.
3. Clinical applications
3.1. Malignant li6er lesions
3.1.1. Hepatocellular carcinomaPrimary liver tumors may appear as hyper-
echoic lesions with peripheral enhancement. Theyare particularly difficult to recognize in cirrhoticpatients in which case they may be completelyisoechoic and without a hypoechoic rim. In ex-treme cases their presence may only be detectedby a distortion in the hepatic vasculature. Ultra-sound examination of the cirrhotic liver is facili-tated by instilling normal saline into theperitoneal cavity. This ensures better acousticcontact between the transducer and the nodularliver surface.
In patients who have already had a pre-opera-tive diagnosis of hepatocellular carcinoma, thecombination of laparoscopy and laparoscopicevaluation with ultrasound guided biopsies can beperformed just prior to opening the abdomen forthe purpose of hepatic resection. The objective isto look for some contra-indications to resection: abenign nature of the lesion, an incurability (peri-
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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), rightlateral 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 preoperativeimaging).Fig. 10. Liver metastases (M) less than 10 mm in diameter not detected by preoperative imaging.
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toneal metastases, bilobar disease, invasion of ad-jacent organs, lymph nodes metastases), or anirresectability (inadequat liver remnant, locationprecluding resection near a major vein, main por-tal vein tumor thrombus, inferior vena cava tu-mor thrombus) (Lo et al., 1998). The combinationof diagnostic laparoscopy with laparoscopic ultra-sound may lead to the discovery of undetectedtumor sites or local tumor invasion into an adja-cent portal vein branch. It also helps to preciselylocalize the tumor and to define its relations toadjacent blood vessels (John and Garden, 1994;Lo et al., 1998). Tumor resectability can be deter-mined on the basis of these findings, thus mini-mizing the risk of needless laparotomies forunresectable tumors (John and Garden, 1994; Loet al., 1998). Laparoscopic liver biopsy underultrasound guidance has now become a routinelyused technique. Many surgeons require that apatient undergo a tissue biopsy prior to openingthe abdomen for a hepatic resection (Lo et al.,1998).
3.1.2. Li6er metastasesThe sonographic appearance of liver secon-
daries is variable. They may be hyper-, hypo-, orisoechoic, as well as being homogeneous or het-erogeneous (Fig. 9). Large metastases often dis-play a hyperechoic center with posteriorshadowing due to calcifications within the lesion.Isoechoic metastases can only be identified by thedistortion of intra-hepatic vessels they produce.
Intra-operative ultrasound enables the detectionof liver metastases at the same time as resection ofa gastro-intestinal tumor (Cuesta et al., 1993;Goletti et al. 1998).
In patients who have already had a pre-opera-tive diagnosis of liver metastases, the objective isto look for some contra-indications to liver resec-tion: a benign nature of the lesion, an incurability(peritoneal carcinomatosis, bilobar disease, morethan five liver metastases, invasion of adjacentorgans), or an irresectability (location precludingresection near a major vein) (John et al., 1994)
The essential advantage of laparoscopic ultra-sound is in the detection of lesions less than10mm 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 thesurrounding normal liver. Tumor resectability canbe determined on the basis of these findings, thusminimizing the risk of needless laparotomies forunresectable tumors. Contact ultrasound also fa-cilitates interstitial therapies. For example, alco-hol injection (Incarbone et al., 1998) andcryotherapy (Cuschieri et al., 1995) of metastatictumors can both be achieved by employing ultra-sound guidance. The resulting tumor necrosiscan similarly be monitored by laparoscopicultrasound.
3.2. Benign li6er lesions
3.2.1. CystsSimple hepatic cysts are easy to recognise with
laparoscopic ultrasound (Marvik et al., 1993).Solitary or multiple, they are spherical andsmooth with a weakly echogenic wall. The con-tents of the cyst are typically anechoic, but thereis posterior enhancement. Haemorrhage into sucha benign cyst may alter the sonographic appear-ance of its contents. By placing the transducer indirect contact with the liver capsule, the depth ofthe cyst within the parenchyma can be deter-mined, as well as its relationship to major bloodvessels. These data are useful when consideringlaparoscopic fenestration of a cyst (Fabiani et al.,1991).
Hydatid cysts are similarly sonolucent but areseen to contain obvious daughter cysts. The cystwall is hyperechoic if calcified. Vascular relationsare defined with the aid of color Doppler whichcan foresee any potential difficulties with cystenucleation or laparoscopic liver resection(Katkhouda et al., 1992).
3.2.2. Benign solid lesionsHaemangiomas, in an otherwise sonographi-
cally normal liver, are seen as strongly echogenicwith posterior enhancement. Laparoscopic ultra-sound can nevertheless have difficulty distinguish-ing large haemangiomas from malignant tumors.
Focal nodular hyperplasia cannot be distin-guished from malignant tumors on the findings ofultrasound alone. However, the former lesionsoften have a hyperechoic center due to central
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fibrosis. Ultrasound guided biopsies must be per-formed (Bonhof et al., 1994).
The diagnosis of an adenoma can not be madesolely on ultrasound appearances. These tumorsoften have a sonographic appearance approach-ing that of focal nodular hyperplasia. Evenso, laparoscopic ultrasound can accurately local-ize the lesion and facilitate a guided biopsy(Bonhof et al., 1994). Moreover, the principalbenefit of laparoscopic ultrasound for benign le-sions is in determining the most sparing andbest adapted resection (laparoscopic or conven-tional), when operation is indicated (Cuesta et al.,1995).
The use of laparoscopy for the resection oflarge benign lesion of the liver is not currentlyrecommended. Despite the current availability ofthe laparoscopic cautery, and high flow suctionand irrigation sysyems, the potential for uncon-trollable bleeding from large hepatic resectionsremains the largest inhibiting factor in this ap-proach. Laparoscopic hepatic resection have cur-rently been limited to segmenties and small wedgeresections of superficial or peripheral lesions un-der laparoscopic ultrasound guidance (Cuesta etal., 1995).
4. Results
4.1. Historical background
Initially, laparoscopic ultrasound of the liver,using real time B mode, was reported by Ohta etal. (1981), Oda (1982). Once the prototypes wereperfected, Frank et al. (1985) noted that laparo-scopic ultrasound was capable of detecting intra-hepatic lesions previously unseen by pre-operativetransparietal ultrasound. With the advent of la-paroscopic surgery, probes compatible with theusual ports were developed. Commercially avail-able probes with a flexible tip allowing adequateacoustic contact represented a significant break-through in the uptake of this technology. Laparo-scopic ultrasound was quickly seen as animportant contribution to the diagnostic imagingof the liver (Miles et al., 1992).
4.2. Impact of laparoscopy and laparoscopicultrasound on surgery of malignant li6er tumors
The combination become a critical part of theclinical decision-making process. In a study byJohn et al. (1994), where 50 patients had a poten-tially resectable tumor, whether benign or malig-nant, on the basis of pre-operative investigations,laparoscopy showed the lesion to be unresectablein 23 of these (46%). Laparoscopic ultrasoundwas performed in 43 patients. In 14 cases (33%),laparoscopic ultrasound discovered liver tumorsthat were not visible on pre-operative imaging orvisual laparoscopy. In 18 of the 43 patients(42%), additional staging information was alsonoted: involvement of both lobes of the liver (14cases), hilar lymphadenopathy (five cases), andportal or hepatic vein invasion (five cases). Onthe basis of visual and sonographic exploration,only 14 patients (28%) came to laparotomy. Thir-teen of these had a potentially curative resection.The authors concluded that a combination oflaparoscopy and laparoscopic ultrasound was themost sensitive method for the detection of bothlocal and regional dissemination of liver tumors.
A recent study by Rahusen et al. (1999) lookedat 50 patients with colorectal liver metastasesjudged to be resectable on the basis of pre-opera-tive imaging. Eighteen of these (36%) were subse-quently excluded from a potentially curativeoperation after undergoing combined visual la-paroscopy and laparoscopic ultrasound.
According to Cozzi et al. (1996), for the detec-tion of liver metastases, laparoscopic ultrasoundhas comparable sensitivity to open intra-operativeultrasound.
In a study of 91 patients with potentially re-sectable hepatocellular carcinomas, Lo et al.(1998) found that combined laparoscopy and la-paroscopic ultrasound avoided exploratory la-parotomy in 60% of patients, who were shown tohave irresectable tumors. Morbidity was thus re-duced, length of hospital stay shortened, andnon-surgical treatments able to be institutedsooner. In addition, the mean duration of theprocedure was only 20 min. The authors con-cluded that combined laparoscopy and laparo-scopic ultrasound could avoid the morbidityassociated with needless exploratory laparotomies
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in hepatocellular carcinoma patients. They furtherrecommended that this investigation be performedin all cases before proceeding to a potentiallycurative hepatic resection (Lo et al., 1998).
4.3. Impact of laparoscopy and laparoscopicultrasound on laparoscopic surgery of benign li6erdiseases
The principal benefit is in determining the mostsparing and best adapted resection (laparoscopicor conventional), when operation is indicated.Laparoscopic fenestration of n hepatic cyst isuseful (Fabiani et al., 1991). The use of la-paroscopy for the resection of large benign lesionof the liver is not currently recommended. La-paroscopic hepatic resection has currently beenlimited to segmental and small wedge resectionsof superficial or peripheral lesions under laparo-scopic ultrasound guidance (Cuesta et al., 1995).
5. Conclusion
To perform a liver resection, a surgeon requiresprecise information. Similarly, he/she must beable to accurately assess the liver for metastasesbefore undertaking the resection of a gastro-intes-tinal malignancy. Liver ultrasound performed in‘open’ surgery has demonstrated efficacy. Laparo-scopic ultrasound provides the surgeon with im-portant information which complements that ofpre-operative imaging. Moreover it guides thechoice of liver resection. High frequency transduc-ers enable the detection of lesions less than 1 cmin diameter, Doppler mode defines the vascularrelations of tumors, and probes with an operatingchannel facilitate ultrasound-guided biopsies. La-paroscopic ultrasound is indispensable for anylaparoscopic liver surgery for benign disease.Likewise the initial results from published studieson laparoscopic ultrasound for malignant diseaseof the liver are encouraging. The combination ofvisual laparoscopy and laparoscopic ultrasoundimproves the selection of patients likely to benefitfrom an hepatic resection for malignant tumorwith curative intent while avoiding needless la-parotomy in others.
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