DOI:10.2214/AJR.07.2887
AJR 2008; 190:1314-1317
© American Roentgen Ray Society
CT Laparoscopy for Detecting Small Superficial Metastatic Lesions of the Liver Surface: Initial Experience
Yoji S. Maetani1,
Hiroyoshi Isoda1,
Akinori Nomura2,
Shigeki Arizono1,
Yuusuke Hirokawa1,
Toshiya Shibata1 and
Togashi Kaori1
1 Department of Radiology, Kyoto University Graduate School of Medicine, 54
Shogoin-Kawaharacho, Sakyoku, Kyoto 606-8507, Japan.
2 Division of Gastrointestinal Surgery, Department of Surgery, Kyoto University
Graduate School of Medicine, Kyoto, Japan.
Received July 18, 2007;
accepted after revision November 6, 2007.
Address correspondence to Y. S. Maetani
(mbo{at}kuhp.kyoto-u.ac.jp).
Abstract
OBJECTIVE. The purpose of this study was to determine the efficacy
of CT laparoscopy in the detection of superficial metastasis of the liver
surface.
SUBJECTS AND METHODS. From April 1, 2007, to July 1, 2007, a total
of 34 consecutively registered patients (19 men, 15 women; median age, 55
years) with various intraabdominal malignant tumors underwent preoperative CT
and composed the study population. All patients underwent superparamagnetic
iron oxide–enhanced MRI and portal phase contrast-enhanced 64-MDCT,
including CT laparoscopy. CT laparoscopy is a form of volume-rendering 3D
imaging of the liver that depicts the liver surface in detail.
RESULTS. Among 23 patients who underwent surgery for management of a
primary tumor, four patients had seven superficial metastatic lesions of the
liver surface. None of these lesions had been detected with preoperative axial
CT or superparamagnetic iron oxide–enhanced MRI. In contrast, CT
laparoscopy revealed four of seven lesions in four patients. On a
lesion-by-lesion basis, the sensitivity was 57%, the positive predictive value
was 100%, and the accuracy was 57%.
CONCLUSION. Our initial experience proves that CT laparoscopy is a
promising method for detecting small superficial metastatic lesions of the
liver surface. The findings can influence decisions regarding tumor
resectability.
Keywords: 64-MDCT • CT laparoscopy • liver surface • superficial liver metastasis • volume rendering
Introduction
With advances in various imaging techniques, the detectability of hepatic
metastasis has been increasing
[1,
2]. It is still difficult,
however, to detect small superficial metastatic lesions of the liver surface
[3–6]
that are encountered during laparotomy. The presence of even a small
metastatic lesion of the liver changes therapeutic strategy. For example, the
presence of a single hepatic metastatic lesion from pancreatic cancer
indicates an inoperable state. Preoperative detection of small superficial
metastatic lesions of the liver surface therefore is important. With the
development of MDCT, various 3D images can be obtained, including liver
surface images with CT laparoscopy. To the best of our knowledge, there has
been no report on CT laparoscopy. The purpose of our study was to investigate
the utility of CT laparoscopy in the detection of small superficial metastatic
lesions of the liver surface.
Subjects and Methods
Patients
This prospective study was approved by the institutional review board at
our institution. The study population was 34 consecutively registered patients
(19 men, 15 women; median age, 55 years) with various intraabdominal malignant
tumors who underwent preoperative CT from May 1 to June 7, 2007. Thirteen
other patients who had CT or MRI findings of intrahepatic or lung or bone
metastasis during the study period were not included in the study because
surgical confirmation of the presence of superficial metastasis of the liver
surface was not obtained.
The primary malignant diseases were gastric cancer (n = 5),
colorectal cancer (n = 17), pancreatic cancer (n = 10), and
bile duct cancer (n = 2). Twenty-three patients found to have no
metastasis of the primary tumor on preoperative CT and MRI underwent surgery
for management of the primary disease. Eleven patients underwent exploratory
surgery because findings on preoperative imaging studies suggested the
presence of peritoneal dissemination or small superficial metastasis of the
liver surface, which were detected only with CT laparoscopy. During surgery,
careful inspection and palpation were performed, especially on the liver
surface. The surgeons recorded the location, size, and number of lesions. The
bare area of the liver, however, was not examined. Informed consent was not
obtained from patients because CT laparoscopy was performed with raw MDCT
data.
Imaging
All patients underwent superparamagnetic iron oxide–enhanced MRI and
64-MDCT that included CT laparoscopy. MRI was performed with a superconducting
magnet operating at 1.5 T (Symphony, Siemens Medical Solutions) with a
six-channel phased-array body coil. All images were acquired in the transverse
plane; the field of view was 32 x 24 cm, the slice thickness was 6 mm
with a 1-mm gap, and the reduction factor of integrated parallel acquisition
technique was 2. Dual-echo T1-weighted gradient-echo imaging (FLASH) was
performed with the following parameters: TR/TE, 200/4.76 in-phase;
opposed-phase TE, 2.38 milliseconds; flip angle, 80°; matrix size, 256
x 134; number of signals averaged, 1. Respiration-triggered T2-weighted
fast spin-echo MRI was performed with the following parameters:
5,100–7,500/109; fat saturation with the Cornell high-energy synchrotron
source method; flip angle, 150°; matrix size, 256 x 115; number of
signals averaged, 4. Diffusion-weighted imaging was performed with the
following parameters: 2,100/78; b values, 0 and 1,000 s/mm2; fat
saturation; matrix size, 128 x 106; number of signals averaged, 4. After
these images were acquired, ferucarbotran (Resovist, Nihon Schering) was
injected. Iron in a dose of 0.56 mg/kg (injection volume, 0.8–1.2 mL)
was administered through an antecubital vein. Approximately 15 minutes after
injection of the contrast material, contrast-enhanced images were obtained.
These images were heavily T1-weighted 3D gradient-echo images (4.3/1.63; flip
angle, 15°; matrix size, 128 x 106; number of signals averaged, 1),
T2*-weighted images (169/9; flip angle, 60°; matrix size, 256 x 134;
number of signals averaged, 1), and respiration-triggered T2-weighted fast
spinecho images (2,100/85; flip angle, 150°; matrix size, 256 x 256;
number of signals averaged, 1).
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Fig. 1A —71-year-old woman with rectal cancer. Pathologic finding
after partial liver resection was metastatic adenocarcinoma from rectal
cancer. Intraoperative laparoscopic image shows white superficial hepatic
metastatic lesions (arrow) at right lower segment.
|
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Fig. 1B —71-year-old woman with rectal cancer. Pathologic finding
after partial liver resection was metastatic adenocarcinoma from rectal
cancer. CT laparoscopic image shows same finding (arrow) as
A.
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Fig. 1C —71-year-old woman with rectal cancer. Pathologic finding
after partial liver resection was metastatic adenocarcinoma from rectal
cancer. Frontal view CT laparoscopic image magnified three times nicely
delineates lesion (arrow).
|
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Fig. 1D —71-year-old woman with rectal cancer. Pathologic finding
after partial liver resection was metastatic adenocarcinoma from rectal
cancer. Axial contrast-enhanced portal phase CT scan does not depict lesion
(arrows).
|
|
CT was performed with a 64-MDCT scanner (Aquilion, Toshiba Medical) with a
tube voltage of 120 kV; tube current, 300 mA; rotation time, 0.4 second;
collimation, 64 x 0.5 mm; beam pitch, 53/64. Contrast-enhanced CT images
obtained in the portal phase were used for CT laparoscopy. Nonionic contrast
material (iomeprol, Iomeron 350, Bracco Eisai) was injected IV at a rate 3.3
mL/s with a power injector (Auto Enhance A-50, Nemoto Kyorindo). CT
laparoscopy was performed by the radiologist without knowledge of the
intraoperative findings. On a commercially available workstation (ZIO,
ZIOsoft), a volume-rendered 3D image of the upper abdomen was made at 0.5-mm
thickness with a 0.3-mm overlap of images. Various structures around the liver
on the 3D image were surrounded manually and then cut and removed
automatically. The liver then was extracted on the workstation (Figs.
1A,
1B,
1C,
1D and
2A,
2B,
2C,
2D). When this method is
performed with a 3D filter, which is a commercially available function for
making the liver surface smooth, it is possible to observe the surface of the
liver in detail. We also used the opacity transfer function. The window width
and level then were adjusted so that the hypovascular metastatic lesion would
be invisible against the surrounding liver tissue. As a result, small
superficial metastatic lesions of the liver surface were identified as small
depressions on 3D images. On 2D images, however, the lesions were visualized
as slight irregularities and were almost impossible to recognize as tumors.
The mean total operating time was 9 minutes (range, 7–12 minutes).
Preoperative image analysis was performed by consensus of three liver
radiologists with 9, 13, and 16 years of experience.
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Fig. 2A —72-year-old man with pancreatic cancer. Small white nodule
was present at anterior segment of liver. Intraoperative biopsy revealed
metastatic poorly differentiated adenocarcinoma from pancreatic cancer.
Photograph obtained at exploratory surgery shows tiny metastatic lesion
(arrow) of liver surface.
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Fig. 2B —72-year-old man with pancreatic cancer. Small white nodule
was present at anterior segment of liver. Intraoperative biopsy revealed
metastatic poorly differentiated adenocarcinoma from pancreatic cancer. CT
laparoscopic image at portal phase of dynamic CT shows lesion as small
depression. Lesion (arrow) is not enhanced in comparison with
liver.
|
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Fig. 2C —72-year-old man with pancreatic cancer. Small white nodule
was present at anterior segment of liver. Intraoperative biopsy revealed
metastatic poorly differentiated adenocarcinoma from pancreatic cancer.
Preoperative superparamagnetic iron oxide–enhanced T2-weighted fast
spin-echo MR image (TR/TE, 5,000/109) does not depict small superficial
metastatic lesion (arrow).
|
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Fig. 2D —72-year-old man with pancreatic cancer. Small white nodule
was present at anterior segment of liver. Intraoperative biopsy revealed
metastatic poorly differentiated adenocarcinoma from pancreatic cancer. Axial
contrast-enhanced portal phase CT scan does not depict lesion
(arrow).
|
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Results
Among the 23 patients who underwent surgical management of the primary
tumor, metastasis was found in only one, who also had peritoneal
dissemination. Among the 11 patients who underwent exploratory surgery, small
metastatic lesions of the liver surface were suspected in four patients after
CT laparoscopy, and this suspicion was confirmed at surgery in all four. The
other seven patients were found to have peritoneal dissemination. The size and
the location of the superficial metastatic lesions of the liver surface were
identical to those found with CT laparoscopy. No lesion was detected
preoperatively with either axial CT or superparamagnetic iron
oxide–enhanced MRI. The primary lesions were pancreatic cancer in three
cases and colon cancer in one case. CT laparoscopy depicted four of seven
lesions. The sizes of these four lesions were 4, 5, 5, and 7 mm; those not
depicted were 2, 3, and 3 mm in diameter
(Table 1).
We did not perform statistical analysis because of the small sample size.
In one case, a subtle focal liver surface irregularity with slight depression
was seen at the right posterior inferior segment at exploratory laparoscopy
and laparoscopy with liver surface imaging (Fig.
1A,
1B,
1C,
1D). At subsequent partial
liver resection, a 7-mm-diameter metastatic adenocarcinoma from rectal cancer
was confirmed pathologically. At exploratory surgery, surgeons found a tiny
(4-mm diameter) metastatic lesion of the liver surface at the right anterior
inferior segment (S5) (Fig.
1A). Intraoperative biopsy proved the lesion was metastatic
adenocarcinoma from pancreatic cancer. In another case, a small depression on
the liver surface at S5 was detected with CT laparoscopy
(Fig. 2B). In a retrospective
study, the lesion was detected with superparamagnetic iron
oxide–enhanced T2-weighted imaging
(Fig. 2C), but it was not
detected prospectively. Three patients were found to have peritoneal
implantation. On a lesion-by-lesion basis, the sensitivity was 57%, the
positive predictive value was 100%, and the accuracy was 57%. On a
patient-by-patient basis, the sensitivity, specificity, positive predictive
value, and negative predictive value all were 100%.
Discussion
The liver is a common site of metastatic lesions from malignant tumors.
Advances in various imaging techniques have improved the detectability of
metastatic liver tumors [1,
2]. Small superficial
metastatic lesions of the liver surface, however, are not easy to detect
preoperatively
[3–7].
Warshaw et al. [4] reported
that CT did not depict small liver and peritoneal metastatic lesions in 86 of
88 cases of cancer of the pancreas and the ampulla. In patients with tumors of
the pancreatic head, the preoperative stage changed in 40%
[8]. Consequently, surgeons
sometimes find extrapancreatic metastasis only after laparotomy.
To our knowledge, this report is the first of CT laparoscopy. With this
method, we can visualize the surface of the liver in detail and detect subtle
changes derived from superficial metastasis, such as focal irregularity of the
liver surface. Hypovascular lesions appear as small depressions on the liver
surface because the liver is greatly enhanced in the portal phase but the
metastatic tumor is weakly enhanced. We can also visualize the lesion from any
direction, which cannot be done with intraoperative laparoscopy.
CT laparoscopy has potential clinical significance. It facilitates
detection of small superficial metastatic lesions of the liver surface and
avoids unnecessary surgery. As for pancreatic cancer, pancreatic resection
with curative intent is possible in a small percentage of patients who have
localized carcinoma without distant metastasis. The presence of single small
superficial metastatic lesions of the liver surface indicates an inoperative
state. Therefore, with CT laparoscopy, appropriate patient and therapy
selection can be performed, and unnecessary laparotomy for unresectable
disease can be avoided.
Our study had limitations. First, in this initial experience, the sample
size was small. A study with a larger number of patients should be undertaken.
Second, CT laparoscopy is not effective for patients with liver cirrhosis who
have an irregular liver surface. In addition, scarring on the liver surface
can be mistaken for superficial metastasis of the liver surface, and
hypervascular lesions such as hepatocellular carcinoma can be difficult to
discern. Third, it is difficult to detect superficial metastatic lesions of
the liver surface that are smaller than 4 mm in diameter. The liver surface is
usually somewhat irregular at CT laparoscopy performed with 64-MDCT. We
surmise, however, that with ongoing development of CT with higher spatial
resolution, we will be able to find smaller lesions. Fourth, CT laparoscopy
depicted small superficial metastatic lesions of the liver surface but did not
depict peritoneal dissemination, unlike diagnostic laparoscopy, because there
were no significant differences in density between peritoneal dissemination
and the surrounding structures. In patients with pancreatic cancer, however,
detection of a single hepatic metastatic lesion implies an inoperable state
and assists in determining therapeutic strategy. In addition, CT laparoscopy
is totally noninvasive, unlike diagnostic laparoscopy. CT laparoscopy also can
depict the lesion from any direction, unlike intraoperative laparoscopy.
Our initial experience showed decisively that CT laparoscopy is a promising
method for detecting small superficial metastatic lesions of the liver
surface. The observations can influence decisions regarding tumor
resectability.
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Abstract
Introduction
