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by the American Institute of Ultrasound in Medicine J Ultrasound Med 23:1549-1555 • 0278-4297 Intraoperative Ultrasonography of the Liver in Patients With Abdominal TumorsA New ApproachUniversidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (C.M.G., J.F.C.); Ultrasonography School (UNISOM), Rio de Janeiro, Brazil (C.M.G., E.P.d.Q.A.); Instituto Nacional do Câncer, Rio de Janeiro, Brazil (M.M.C.); and School of Medicine, São Lucas Hospital, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil (M.B.). Address correspondence and reprint requests to Carlos Marques Guimarães, MD, Rua do Catete 228, Sala 314, Catete, Rio de Janeiro, Brazil. E-mail: cmguimara{at}universiabrasil.net.
Objectives. To compare liver intraoperative ultrasonography (IOU), computed tomography (CT), preoperative ultrasonography (USG), and intraoperative inspection and palpation in the detection of hepatic lesions in patients with abdominal tumors. Methods. This was a prospective study including 60 patients with abdominal tumors evaluated by USG, CT, inspection and palpation, and hepatic IOU during exploratory laparotomy. Sensitivity, specificity, and positive and negative predictive values for all methods were calculated. Agreement of methods with histopathologic results was calculated by  statistics and the Spearman coefficient. Results. Of the 60 patients, 49 (81.6%) had positive findings for hepatic lesions. Lesions could not be counted in 3 patients. The 46 remaining cases were diagnosed by histologic examination. Sensitivity, specificity, and positive and negative predictive values were 42.9%, 88.9%, 90%, and 40% for USG; 59.5%, 77.8%, 86.2%, and 45.2% for CT; 69.0%, 88.9%, 93.5%, and 55.2% for inspection and palpation; and 90.5%, 77.8%, 90.5%, and 77.8% for IOU, with histologic examination used as a criterion standard. Fair to moderate agreement was found for USG, CT, and inspection and palpation ( = 0.24, 0.31, and 0.49, respectively). Substantial agreement was found for IOU ( = 0.68). Changes in surgical strategy were made in 19 (41.3%) of the 46 cases with positive findings. Conclusions. High sensitivity associated with substantial agreement with histopathologic findings shows that IOU is an indispensable evaluation method for hepatic screening in patients with abdominal tumors who undergo laparotomy and should become a routine procedure wherever available.
Key Words: diagnosis • hepatic tumors • intraoperative periods • palpation • sensitivity • sonographically guided procedures • specificity • x-ray computed tomography Abbreviations: CT, computed tomography • IOU, intraoperative ultrasonography • USG, ultrasonography
Several studies have evaluated the accuracy of intraoperative ultrasonography (IOU) in comparison with other imaging methods to detect metastatic hepatic lesions in patients with colorectal tumors.1–6 More recent studies have reported excellent results for IOU as a diagnostic method, with sensitivity ranging from 92.3% to 98% and specificity around 95%.4 Also, IOU was used as the criterion standard in several studies that evaluated preoperative imaging techniques to detect hepatic lesions secondary to colorectal tumors.7,8
At the same time, we think that determination of agreement between different imaging methods in the detection of hepatic lesions, which can be assessed by
The purpose of this study was to evaluate preoperative imaging methods (ultrasonography [USG] and computed tomography [CT]) and intraoperative methods (inspection and palpation and IOU) in the detection of hepatic lesions in patients with abdominal tumors independent of their primary site.
Clinical Procedures We conducted a prospective study from January 2000 to March 2003 including 60 patients with abdominal tumors. Patients underwent preoperative USG and contrast-enhanced CT and IOU and inspection and palpation during exploratory laparotomy to investigate hepatic lesions, malignant or benign. All patients underwent surgical treatment of their primary neoplastic sites, resection of their preoperatively diagnosed metastatic hepatic lesions, or both. Of the 60 cases included in the study, 37 (60.7%) were primary colorectal tumors; 6 (9.8%) were bile duct tumors; 4 (6.5%) were liver tumors; 4 (6.5%) were pancreas tumors; 3 (4.9%) were stomach tumors; 2 (3.3%) were soft tissue tumors; 1 (1.6%) was a lung tumor; 1 (1.6%) was a breast tumor; 1 (1.6) was a retroperitoneal tumor; and 1 (1.6%) was a kidney tumor. Twenty-eight patients were male, and the mean age was 60 years (range, 38–80 years). This study was approved by the Ethics Committee of the institution where it was conducted. An informed consent form was signed by all patients included in the study or their family members. An experienced radiologist, with qualifications equivalent to certification by the American Board of Radiology, performed all CT studies. Three spiral CT scanners were used: Elscint Twin (Elscint, Hifa, Israel), Shimadzu SCT 700-TS (Shimadzu, Kyoto, Japan), and Picker PQ 2000 (Picker Medical Imaging, Cleveland, OH). One hundred to 120 mL of a contrast agent (Omnipaque [iohexol]; Amersham Health, Princeton, NJ) was administered via an infusion pump at a rate of 3 mL/s; the arterial phase was initiated 20 to 30 seconds after infusion, and the portal venous phase was initiated 50 to 70 seconds after infusion. After contrast agent injection was completed, a delayed scan phase after approximately 90 seconds was run to detect possible delayed contrast tumors. The reconstruction interval was 5 mm with a slice thickness of 5 mm, table speed of 15 mm per gantry rotation, and pitch of 5. Preoperative sonographic studies were performed with an HDI 3000 color Doppler scanner (Philips Medical Systems, Bothell, WA) with 3.5- to 5.0-MHz wideband convex transducers. Patients fasted for about 10 hours before the examination. Subcostal and intercostal views of the right upper quadrant of the abdomen were obtained to examine the full extension of the hepatic parenchyma and to identify all anatomic segments as described by Couinaud.9 During surgery, inspection and palpation of the liver, a routine examination procedure to detect hepatic lesions, was performed. All visible hepatic areas were inspected after the liver was mobilized by dissection of the falciform ligament. All of the hepatic surface was then palpated to identify superficial lesions according to the anatomic parameters described by Couinaud.9 The IOU study was conducted with the Philips HDI 3000 color Doppler scanner with 2 connected intraoperative convex and linear array 4- to 8- and 5- to 9-MHz transducers. The systematic sonographic examination was complemented with color Doppler imaging whenever a tumor was identified. Transverse and longitudinal views of all hepatic anatomic segments, intrahepatic portal branching, suprahepatic veins, the gallbladder, and the portal hilum were obtained, and the liver was mobilized whenever clinically necessary. The hepatic segments where the lesions were found and their relationships to vessels were observed. Both USG and IOU were performed by a physician with qualifications equivalent to certification by the American Board of Radiology. All lesions underwent biopsy by means of either core or surgical biopsy, and the material collected was sent for histologic examination. The patients in whom no lesions were identified were prospectively followed by outpatient consultations every 3 months during the first year after the procedure. During follow-up, patients underwent USG. If lesions were detected or if tumoral markers were elevated, the USG study was complemented with a CT study. This study also evaluated whether IOU determined changes in the preestablished surgical strategy defined according to preoperative USG and CT.
Statistical Analysis
At least 1 method showed a lesion in 49 (81.6%) of the 60 patients. There were 11 patients who underwent screening of hepatic lesions during surgical treatment of their primary sites; all had negative findings. Preoperative USG showed lesions in 40 patients; CT showed them in 45; inspection and palpation showed them in 42; and IOU showed them in 47. The numbers of lesions shown by each method were as follows: USG, 57 lesions in 37 patients; CT, 63 lesions in 42 patients; inspection and palpation, 82 lesions in 39 patients; and IOU, 121 lesions in 44 patients. Hepatic lesions could not be counted by any of the imaging or palpation methods in 3 patients with numerable and extensive unresectable metastases. All 46 cases (100%) that underwent biopsy were diagnosed by histologic study. In 1, the histologic diagnosis was inconclusive by IOU-guided core biopsy but was confirmed as a metastatic adenocarcinoma after excisional biopsy. The following diagnoses were made: 34 (73.9%) metastatic adenocarcinomas, 2 (4.3%) sarcomatous metastases, 1 (2.2%) carcinoid tumor, 1 (2.2%) epithelioid hemangioendothelioma, 1 (2.2%) hepatocarcinoma, 1 (2.2%) metastasis of ductal carcinoma of the breast, 1 (2.2%) leiomyosarcoma, 1 (2.2%) cholangiocarcinoma, and 4 benign lesions, including 1 (2.2%) focal nodular hyperplasia, 1 (2.2%) normal tissue within pathologic tissue (Wilson disease), 1 (2.2%) cystic lesion, and 1 (2.2%) hemangioma. The mean time from preoperative imaging studies to surgery was 42.5 days (range, 15–90 days).
Table 1
Changes in surgical strategy were made in 19 of all cases evaluated, which corresponded to 31.6% of all cases and 41.3% of the 46 cases with positive results.
The purpose of this study was to determine the diagnostic performance of IOU in the detection of hepatic lesions, malignant or benign, in patients with abdominal tumors independent of their primary site. We also compared the performance of IOU with other imaging methods: preoperative USG, CT, and intraoperative palpation. Intraoperative ultrasonography showed high sensitivity for detecting hepatic lesions and a substantial correlation when compared with histopathologic results. In our cases, 38.3% had tumors that were not of colorectal origin. Our findings are in agreement with results reported in recent studies that evaluated hepatic lesions of colorectal origin2–4,6,8 and show that IOU is a method of great sensitivity even when used to evaluate secondary hepatic lesions of an origin other than colorectal.
The correlation with histopathologic results, calculated by Two cases in our series illustrate the benefits of the use of IOU to detect hepatic lesions, as well as the special care that should be taken when performing this examination. In the first case, preoperative CT identified lesions suggestive of hepatic metastases of pancreatic origin. Intraoperative evaluation with IOU, however, revealed that the lesions were cysts, which was confirmed by histopathologic examination of the IOU-guided biopsy. In the other case, preoperative examination suggested that there were 3 tumors. In fact, this was a case of diffuse hepatic disease (Wilson disease), and histologic examination of the specimens revealed normal tissue within pathologic tissue. This was a false-positive case of the preoperative and intraoperative imaging studies because USG and CT, as well as IOU, showed 3 pathologic nodules. Inspection, palpation, and videolaparoscopy findings, however, were negative. Also, the IOU-guided biopsy performed intraoperatively yielded negative findings for nodules. The technique used for IOU is somewhat difficult to perform for the identification of small, very superficial lesions (<1 cm) and when the liver is not mobilized. Higher-frequency transducers (11–13 MHz) should be used to identify these tumors. Moreover, the pressure of the costal arch against the hand of the operator when examining nonmobilized livers prevents adequate positioning of the focal zone and complicates the study of the hepatic surface when lesions are small and superficial, as well as when lesions are located in "blind" areas of the liver, that is, under the triangular and coronary ligaments. This may explain why some lesions were more accurately diagnosed by inspection and palpation.
The rate of changes in surgical strategy due to information provided by IOU was high in this study (31.6%; Figure 2
In addition to its diagnostic efficacy, IOU is an indispensable tool for the surgeon. It provides information about the textural characteristics of the lesions, their vascular connections, and the mapping of anatomic variations; it guides incisions into the Glisson capsule, biopsies, and fine-needle procedures; and, finally, it ensures that adequate margins are removed in tumor resections.
Only a few studies had previously determined the capacity of IOU to show hepatic nodules independent of primary sites. In this study, we found that the performance of IOU in the detection of metastatic hepatic lesions was similar to that found in studies that evaluated metastases of colorectal cancer. High sensitivity and specificity associated with substantial agreement with histopathologic results, calculated by
Received April 14, 2004, from Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (C.M.G., J.F.C.); Ultrasonography School (UNISOM), Rio de Janeiro, Brazil (C.M.G., E.P.d.Q.A.); Instituto Nacional do Câncer, Rio de Janeiro, Brazil (M.M.C.); and School of Medicine, São Lucas Hospital, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil (M.B.). Revision requested May 3, 2004. Revised manuscript accepted for publication August 18, 2004. We thank the physicians and students from the Ultrasonography School (UNISOM) and Universidade Federal do Rio de Janeiro for contributions to this study.
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Abstract
Introduction
