Laparoscopic and intraoperative ultrasound

European Journal of Radiology 27 (1998) S207 – S214

Laparoscopic and intraoperative ultrasound Mario Bezzi a,*, Gianfranco Silecchia b, Antonio De Leo b, Iacopo Carbone a, Daniela Pepino a, Plinio Rossi a b

a Department of Radiology, III Cattedra, Uni6ersity ‘La Sapienza’, Policlinico Umberto I, I-00161 Rome, Italy Department of Surgery, VIII Patologia Chirurgica, Uni6ersity ‘La Sapienza’, Policlinico Umberto I, 00161 Rome, Italy

Abstract Objecti6e. Intraoperative ultrasound has gradually expanded in the last two decades to a variety of surgical specialties and has gained an established role in many surgical procedures. Laparoscopic and thoracoscopic ultrasound are the latest modes of intraoperative sonography. They have been introduced mainly to overcome the two major drawbacks of laparoscopy, i.e. the capability of showing only the surface of the organs and the lack of manual palpation of the anatomical structures. We review and discuss the established and the most recent applications of intraoperative and laparoscopic ultrasound. Material and methods. The technology, new indications and results of intraoperative and laparoscopic ultrasound are reviewed. This review is based on the experience gained in our Institution during more than 500 surgical procedures and the analysis of the literature on the subject. Results. The yield of intraoperative and laparoscopic ultrasound consists in confirming preoperative studies and acquiring new data which would not be available otherwise. An important role of these techniques is determining the anatomy of the involved organs, thus providing a guidance for surgery. Both techniques have an important role in surgical decision-making, particularly with respect to hepatic, biliary and pancreatic malignancies. In some series the rate of major changes in the surgical strategy can be as high as 38%. A relatively new application of intraoperative ultrasound is the possibility to perform interstitial therapy of tumors at the time of the initial surgery. This can be useful, for example, in patients undergoing liver resection, when other unresectable lesions are found in a different segment or in the contralateral lobe. Finally, laparoscopic sonography has an important role in staging abdominal neoplasm, providing more information than preoperative imaging and laparoscopic exploration. This feature can be used to effectively stage gastrointestinal malignancies, pancreatic carcinoma, and abdominal lymphomas. Conclusion. The application of intraoperative ultrasound will increase in the era of minimally access surgery and this will be dependent not only on technical improvements in ultrasound technology. Indeed, it may be expected that a variety of open procedures will be performed with videolaparoscopic monitoring and will need the guidance of laparoscopic sonography. In the future, the staging of abdominal neoplasm may be markedly improved by laparoscopy combined with laparoscopic ultrasound; however a cost-benefit analysis of these techniques and a comparison with preoperative tests should be carried out. © 1998 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Laparoscopy; Laparoscopic surgery; Intraoperative ultrasound; Laparoscopic ultrasound

1. Introduction The use of ultrasound during surgery — intraoperative ultrasonography (US) — has expanded to a variety of surgical fields, since its introduction almost 20 years ago [1]. The recent rapid development of video-assisted surgical techniques has prompted a new interest in intraoperative US. High-frequency sonographic probes * Corresponding author. Tel.: + 39 6 4455602; fax: +39 6 490243.

have been designed to be passed through laparoscopic and thoracoscopic ports to help the surgeon during the procedures. The surgical technique and decison-making can therefore be altered according to the information provided by intraoperative imaging. With laparoscopic US, high resolution images can be obtained of the biliary ducts, the gallbladder and the abdominal parenchymas without the image degradation caused by overlying bowel gas or a thick abdominal wall. These features can be used to increase the value of

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diagnostic laparoscopy, for example in the staging of intra-abdominal malignancies. As a matter of fact, laparoscopy is accurate in detecting peritoneal deposits and small superficial liver metastases [2] but its efficacy is limited by the inability to reliably assess lesions deeply located in the liver parenchyma or in the retroperitoneum. These limitations can be overcome by the use of laparoscopic US. This imaging technique is increasingly used in staging malignancies involving the hepatobiliary system and other abdominal organs. During thoracoscopic surgery, intraoperative US may help to locate pulmonary nodules, determine their size and proximity to pleural surfaces. Based on the personal experience and a literature review, the new advances and specific applications of intraoperative US in general surgery will be summarized.

2. Equipment and examination technique The two basic types of probes for intraoperative US are linear and sector probes; in general surgery, linear 7.5 Mhz probes are the most commonly used. The depth of sound penetration with 7.5 MHz transducers is approximately 7– 8 cm, which is usually adequate in most situations; in several units the frequency can be switched from 5 to 7.5 MHz according to the area of interest. The probes are designed, as for size and shape, so that they can be easily manipulated in operative fields, which at times are limited in space. Intraoperative probes of different design are marketed by several manufacturers; when selecting them, one should choose at least two probes of different shapes, so that he or she can adequately face the different operative conditions. The probes used in laparoscopic US are essentially made of a transducer placed on the tip of a long shaft. The shaft is usually 10 mm or less in diameter and 35 – 45 cm in length, to permit a wide examination field from any single port. Transducers are available in the 5 – 10 MHz frequency range. They are mounted in front-view or side-view fashion on a rigid or deflectable tip. Probes with a flexible tip are more versatile in scanning less accessible regions, such as the dome of the liver. Access for the US probe to the peritoneal or thoracic cavity is achieved through 10 or 11 mm ports which are usually the same ports that give access to the video camera. The examination is usually performed by contact scanning using the liquid film of the serosal surfaces as a coupling agent. In the abdomen, the stomach is emptied to avoid air-related artifacts. Surgical dissection, if necessary, is kept to a minimum, as the presence of gas in the tissues, caused by electrocoagulation, may interfere with subsequent imaging.

The examination technique is somewhat different for the different operative situations [3]. In the hepatobiliary system, transverse and oblique scans of the gallbladder and liver hilum are obtained by using the hepatic parenchyma of segment four as an acoustic window. This allows good visualization of the intrahepatic bile duct, ductal confluence and proximal common bile duct (CBD). The surgeon subsequently raises the gallbladder anteriorly; the probe is placed directly onto the hepatoduodenal ligament and gently slid toward the duodenum and the pancreatic head. These steps allow for the investigation of the CBD in its entire length, down to the region of the papilla [4]. The approach through the umbilical port is used to study the gallbladder and the bile ducts by sagittal planes, which permit also the identification of the cystic duct confluence. During the exam, one realizes that the pressure exerted to achieve probe contact may flatten the veins and the bile ducts but not the arteries. This flattening should be taken into account, particularly when investigating the CBD. The liver parenchyma should be imaged scanning from the superior and from the posterior surface. The dome can be depicted adequately with a flexible probe [4]. When using a rigid probe, the dome is more difficult to study because of lack of adequate contact between the straight probe and the curving liver surface. This can be overcome by instilling 1–3 l of isotone saline and scanning the highest part of the organ through the fluid. In thoracoscopic surgery, the probe is placed on the pleura at the site of the suspected abnormality. When the nodule to be resected is identified, the location is marked on the pleural surface with the electrocoagulator. The examination and image interpretation are done by surgeons in some centers; in our Institution they are performed by a radiologist trained in intraoperative US.

3. Clinical applications

3.1. Li6er For both primary and metastatic liver tumors, intraoperative US is indicated to determine resectability and to choose the type of surgery. The technique is also used to screen for metastatic tumors, particularly from colorectal carcinoma. During liver tumor surgery, intraoperative US provides information that is not obtained by preoperative tests and by surgical inspection. Unpalpable satellite tumors can be discovered and vascular involvement by neoplasm can be assessed. On the basis of the US findings, surgical procedures initially proposed on the

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basis of preoperative studies and surgical exploration, can be altered. In some series the percentage of significant changes in the surgical strategy can be as high as 38% [5]. When surgery is undertaken for liver metastasis, the use of intraoperative US is mandatory. In a study of 250 patients with colorectal carcinomas, intraoperative US detected unknown liver metastases in 25 patients (10%) [6]. Thus intraoperative US can help to reduce the number of unnecessary liver resections. A relatively new application of intraoperative US is the possibility to perform interstitial therapy of liver tumors at the time of the initial surgery. This can be useful, for example, in patients undergoing liver resection, when another deep or unresectable lesion is found in another segment or in the contralateral lobe. While the resectable tumor is removed, the other lesion can be treated by thermal ablation with radiofrequency or laser probes placed directly under US guidance. Laparoscopic US of the liver, which is the most easily accessible organ for this technique, has possibilities similar to intraoperative ultrasound. One recent study by John et al. [7] using laparoscopic exploration of 50 hepatic tumors revealed that laparoscopic US detected tumors missed at laparosopy in 33% of cases and provided staging information additional to those of laparoscopy alone in 42% (Fig. 1). Laparoscopic US can have an impact on intraoperative surgical decision-making in the evaluation of liver metastases as well. Before laparotomy, the abdominal cavity can be explored by laparoscopy and the liver scanned by laparoscopic US, thus giving the possibility to detect peritoneal implants and liver deposits. The lesion detected can also be biopsied under laparoscopic US guidance. It would therefore be possible to exclude unresectable cases from being subjected to the morbidity of open surgery [8]. Screening for secondary liver lesions can also be done any time laparoscopy is performed to diagnose, stage or treat an abdominopelvic neoplasm. Finally, laparoscopic US can be used to guide thermal ablation of liver tumors, either by radiofrequency or laser, in all the cases in which percutaneous ablation is not feasible or not indicated.

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leiomyioma, granular cell tumor, and lipoma. Pseudotumors include cholesterol polyps, inflammatory polyps and adenomatous hyperplasia. It is generally accepted that colesterol polyps never degenerate whereas adenoma and adenocarcinoma are pre-malignant and malignant lesions, respectively. In a patient with a polypoid lesion of the gallbladder, surgery is usually indicated because of symptoms, because the lesion is larger than 10 mm, or because a progressive increase in size has been detected at US. A preoperative and intraoperative differential diagnosis of the various lesions is useful since it may address the surgical strategy. Cholesterol polyps, by far the most common, can be safely removed by laparoscopic cholecystectomy, while pre-malignant and malignant lesion are best treated by open surgery. Unsuspected gallbladder cancer removed by laparoscopic cholecystectomy may result in spread onto the peritoneum or within the abdominal wall [10]. Preoperative differential diagnosis of such lesions is difficult. Transabdominal US is the only imaging test

3.2. Gallbladder and bile ducts Laparoscopic US can be valuable in the assessment of the gallbladder wall in patients who are undergoing laparoscopic surgery for gallbladder polyps or in whom a gallbladder wall condition is suspected or discovered incidentally. Polypoid lesions of the gallbladder are commonly classified into tumors and pseudotumors [9]. Tumors include malignant lesions such as as adenocarcinoma and metastases, and benign lesions such as adenoma,

Fig. 1. Laparoscopic US in staging of liver tumors. (a) Inhomogeneous, 3.5 cm hepatocellular carcinoma of right lobe of the liver, with the nodule-within-nodule appearance. (b) Small 10 mm nodule in the left lobe, not detected at other imaging studies.

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performed before surgery but it is not highly reliable. At our Institution preoperative ultrasound and laparoscopic ultrasound were performed in patients with polypoid lesions who underwent laparoscopic cholecystectomy and studied 105 polyps in 84 patients. For each lesion the size, morphology, echotexture and the presence of a pedicle were recorded. In addition, for each polyp the height, the width and the height/width ratio were calculated [11]. Laparoscopic US was more effective than preoperative US in visualizing the lesion and its pedicle, and in assessing the real diameters and orientation of the lesion in respect to the gallbladder wall. In the series all cholesterol polyps showed a prevalence of the height to the width with a height/ width ratio greater than 1.15, whereas the group of malignant and pre-malignant lesions showed a tendency to a ‘flat’ growth, parallel to the wall, with a height/ width ratio less than 0.70. In addition, cholesterol polyps were often attached to the underlying mucosa by a fragile pedicle (86% of cases), which was best visualized during laparoscopic US study. The analysis demonstrated also that multiple polyps were more frequently benign (p B 0.05). Differences in echotexture were not relevant for the differential diagnosis. If these observations are confirmed by other studies, laparoscopic US can safely be used to determine the nature of a suspected gallbladder wall lesion during laparoscopic cholecystectomy. The role of operative cholangiography (OCG) during laparoscopic cholecystectomy and whether it should be performed selectively or routinely, is a highly debated issue. Its routine use is advocated by some authors to exclude iatrogenic lesions of the bile duct, to evaluate possible anatomical variants of the biliary tree, and to verify the presence of CBD stones. Others support a more selective use of operative cholangiography, based on preoperative clinical, radiologic and biochemical considerations. Laparoscopic US has been proposed as an alternative to OCG in the study of the biliary tree, particulary as regards residual CBD stones (Fig. 2). Experiences on the use of laparoscopic US in detecting CBD stones have been published by several authors. Greig and coworkers [12] examined the CBD of 54 patients undergoing laparoscopic cholecystectomy. They found that laparoscopic US had a sensitivity of 71% and a specificity of 96% for CBD stones. In the same study OCG had a sensitivity of 83% and a specificity of 95%. Ro¨thlin et al. performed laparoscopic US and OCG (using conventional static film) on 100 consecutive patients during laparoscopic cholecystectomy. He reported a sensitivity of 100% and a specificity of 99% for CBD stones using laparoscopic US, both superior to OCG [13]. In another study conducted by Barteau and coworkers on 125 patients, OCG (using digital videofluoroscopy) was slightly superior to laparoscopic

Fig. 2. Common bile duct stones. Transverse scan of the suprancreatic portion shows that the CBD (c) is moderately dilated with thickened walls due to inflammation (left); at a more distal level (right), the lumen is obstructed by a 5 mm stone. From reference [4], with permission

US; it was more sensitive (92.8 versus 71.4%) but less specific (76.2 versus 100%) for choledocolithiasis than was US [14]. Similar results have been reported by other authors [15–17]. The general consensus among the surgeons who use both techniques, is that laparoscopic US is at least as accurate as OCG in diagnosing choledocholithiasis during laparoscopic cholecystectomy. The two techniques have a definite learning curve but once skills have been developed, laparoscopic US requires less time than OCG. The anatomical picture given by OCG is cited by some authors who advocate that the primary objective of biliary imaging during laparoscopic cholecystectomy is anatomical definition, so that the incidence of iatrogenic injuries to the bile ducts can be reduced. This unresolved issue will be probably answered by more experience on larger groups of patients.

3.3. Pancreas In patients with pancreatic tumor, the only chance for cure is surgical resection. However, only a small proportion of patients have a resectable tumor at laparotomy. Liver metastases and peritoneal implants are frequently present at the time of detection of the primary tumor and each of them precludes a curative resection. Local tumor extension outside the pancreatic head or into portal or superior mesenteric vessels, in many centres, contraindicates surgery. Laparoscopic US can be used, together with laparoscopy, in staging pancreatic tumors. Pancreatic adenocarcinomas are almost always hypoechoic compared to normal pancreatic parenchyma (Fig. 3). Since inflamed pancreatic tissue is also hypoe-

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choic, it can be difficult to differentiate focal pancreatitis or obstructive pancreatitis from a malignant neoplasm. Laparoscopic US is particularly useful in evaluating vascular infiltration. Signs of tumor invasion are thrombosis of a vessel, luminal narrowing and loss of the hyperechoic interface between vessel and tumor with or without the tumor actually protruding into the vascular lumen. Laparoscopic US allows also an easy study of the liver and peripancreatic nodes (Fig. 3). Suspected intrahepatic lesions and nodes can be biopsied percutaneously under combined laparoscopic and laparoscopic US guidance. The need for laparoscopic US comes from the observation that laparoscopy alone is not sufficient. In a series of 115 patients reported by Conlon et al. [18], laparoscopy failed to identify liver metastases in five patients and portal venous encasement in one patient. These findings can be detected by laparoscopic US.

Fig. 3. Pancreatic head carcinoma. a. In this axial scan of the pancreatic head the tumor (T) is hypoechoic. There is no infiltration of the gastroduodenal artery (arrow) and mesenteric vessels, which are not included in the field of view. b. Enlarged lymph node at the proper hepatic artery (A). This proved to be metastatic at pathology.

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Fig. 4. Pancreatic insulinoma. This 1.5 cm hypoechoic nodule is completely surrounded by normal pancreatic tissue. There is a plane between the nodule and the splenic artery (S).

Bemelman et al. [19] clearly showed that additional information may be provided by laparoscopic US in patients with pancreatic head cancer. Laparoscopy and laparoscopic US combined revealed metastatic disease in 16 of 72 patients, who had potentially resectable tumors after preoperative staging. Liver metastases were detected in 13 patients. In six of these, metastases were seen only by laparoscopic US and in three patients by both laparoscopy and laparoscopic US. Laparoscopic US showed a high specificity and positive predictive value in evaluating overall unresectability (96 and 97%, respectively) and unresectability due to vascular tumor ingrowth (96 and 93%, respectively). John et al. [20] also reported additional value of this technique added to diagnostic laparoscopy in a series of 40 patients. Laparoscopic US demonstrated factors confirming an unresectable tumor in 23 patients (59%), provided staging information in addition to that of laparoscopy alone in 20 patients (53%) and changed the decision regarding tumor resectability in ten patients (25%). Laparoscopy combined with laparoscopic US was more specific and accurate in predicting tumor resectability than laparoscopy alone (88 and 89 versus 50 and 65%, respectively). Comparable results have been published by other authors [21,22]. Another potential field of application of laparoscopic US is represented by endocrine pancreatic neoplasms. Although our experience is limited to only four cases of endocrine neoplasm, laparoscopic ultrasound was able to detect the tumors and to accurately depict their relationships to the Wirsung’s duct, the splenic artery and vein [4] (Fig. 4). The information provided is useful to the surgeon in case of laparoscopic enucleation of the endocrine tumor. The role of intraoperative US in endocrine pancreatic surgery is, on the contrary, well established. Small islet

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cell tumors may not be palpable at operation and can be identified in up to 85 – 100% of cases by intraoperative US [23,24].

3.4. Gastroesophageal neoplasms TNM staging of gastroeophageal cancer takes advantage of the use of laparoscopy for the detection of occult metastases and of endoscopic sonography for T and possibly N staging. Laparoscopic US may combine the strengths of both techniques. It can be hypothesized that inclusion of laparoscopic US in the staging protocol will lead to a better preoperative identification of patients who will not be curable by surgery. The final goal is to increase the resection rate of patients who undergo laparotomy. In an initial experience, Bemelman et al. [25] found that laparoscopic US was of little value in these regards. In further studies, Anderson et al. [26] and Finch et al. [27], found that the TNM staging provided by laparoscopy and laparoscopic US was superior to that provided by preoperative imaging tests, including abdominal US and CT [26] and CT and endoscopic sonography [27]. What is more important is that the resection rate, after laparoscopic US staging, was increased to 88 [27] and 97% [26].

3.5. Colon In patients undergoing laparoscopic segmental resection of the colon for malignant neoplasm, laparoscopic US can be performed to detect liver metastases and to localize the segment to be resected. The colon is partially mobilized by the surgeon and then imaged by surface scanning. The tumor appears as a hypoechoic focal thickening of the wall (Fig. 5). The

two edges of the lesion are identified and surgical clips placed on the normal wall approximately 2–3 cm above and below the neoplasm [4]. These clips are then used by the surgeon as safety landmarks for resection. This technique for tumor localization can be used in small tumors that are not readily visible at laparoscopy and as an alternative to endoscopic trans-illumination, which is more complicated and may not show the proximal extent of the tumor in patients with tight stenosis. The potential role for comprehensive TNM staging in patients with cancer of the colon is similar to that reported above for gastroesophageal neoplasms.

3.6. Lymphoproliferati6e disease of the abdomen Management of lymphoproliferative diseases involving the abdomen entails an accurate diagnosis with histologic typifying and immunophenotyping (subgroup classification). Once a diagnosis is made, accurate staging is required. In patients with lymphoma, without peripheral lymphadenopathy, lymph node and/or hepatic biopsies and, in selected cases, splenectomy, are the standard procedures to achieve complete histologic typify. Percutaneous imaging-guided biopsies, due to the small size of the specimen obtainable, may allow a diagnosis of lymphoma but do not always permit a complete immunohistochemical and cytogenetic study. In our Institution the role of the minimally invasive access to diagnose and stage lymphoproliferative diseases of the abdomen is currently being investigated [28]. In this regard, the surgeon uses laparoscopic US to localize lymph nodes which were seen at preoperative CT but are deeply sited and cannot be seen at laparoscopy. This localization reduces the time necessary for surgical dissection. When a splenic and/or hepatic biopsy is scheduled, US can guide the surgical biopsy of lesions located just beneath the surface of the organ but not showing through the serosa (Fig. 6). Laparoscopy with laparoscopic US can replace both surgery and percutaneous biopsy, since it is efficacious, cost-effective and is highly accepted by the patients.

3.7. Lung

Fig. 5. Localization of colon cancer during laparoscopic resection. The tumor is seen as a hypoechoic nodule within the posterior wall of the bowel.

One of the most frequent indications for thoracoscopic surgery is wedge resection of pulmonary nodules for diagnostic and therapeutic purposes. Localization of these nodules at thoracoscopy is often not easy due to the limited exposure of intrathoracic structures and to the lung collapse which alters the spatial relationships of the nodules as seen on preoperative imaging. At thoracoscopy, US scanning can be performed with the same probe used in laparoscopic US. Complete collapse of the lung is essential to avoid interposition of air between the pleural surface and the nodule. The

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4. Conclusion Ultrasound equipment is ever evolving and this will also improve laparoscopic US imaging. Probes with a controllable tip with four movements may prove useful in scanning difficult areas and color Doppler facilities may be useful to investigate vessel patency and possibly to characterize liver lesions. A very important step forward in laparoscopic US will be the development of specially designed puncture probes, which allow accurate biopsy of deep seated nodules. Laparoscopic US as a technique for staging tumors is probably here to stay. It has the same potentials as intraoperative US, which has become an established technique by proving its value in comparative studies with such techniques as dynamic contrast enhanced CT and CT arterioportography [5]. It is expected that in the coming years the potentials and benefits of laparoscopy combined with laparoscopic US will be more extensively studied and it will become clear whether the technique can play a key role in tumor management. This will be dependent not only on the technical capabilities of laparoscopic US, but also on developments in other noninvasive imaging modalities and new minimally invasive surgical techniques.

References

Fig. 6. Splenic lymphoma. a. Multiple hypodense nodules are seen within the spleen in a preoperative unenhanced CT. b. Laparoscopic US of the spleen detects one of the lesions as a mixed hyperechoic mass (M) and directed surgical biopsy. The lesion was not showing through the serosal surface.

nodule or nodules can be localized with certainty and a tissue-sparing wedge resection of the lung can be performed. In 1993, Mack et al. [29] reported on a promising preliminary experience with a transrectal probe. More recently, Greenfield et al. [30] evaluated the technique prospectively in a series of 13 patients undergoing thoracoscopic nodule resection. The use of a dedicated probe allowed correct localization of the nodules in 12/13 patients; in six of them the nodules were seen by US only. The authors therefore propose the technique as an alternative to preoperative needle localization and hookwire placement under CT guidance, which must be closely coordinated with the operating room schedule and may cause delays due to procedural complications such as pneumothorax.

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