Matthijs Swannie

Oudkerk, L. Tjiam,

Liver

MD, MD

PhD Paul

#{149}

Bart van Ooijen, MD, PhD #{149}Sybrand P. M. Mali, MD I. M. Schmitz, MD, PhD #{149} Theo Wiggers, MD, PhD

#{149}

Metastases

Detection

with

A diagnostic

from Continuous

approach to assess liver from colorectal carcinoma was prospectively evaluated in 30 patients with and without metastases on the basis of findings at conventional computed tomography (CT). With the technique, termed continuous CT angiography (CCTA), CT data were continuously sampled for 24 seconds at the same section level after initiation of a 3-second injection of 10-20 mL of contrast medium in the common hepatic artery. The procedure was repeated for each contiguous section level of the liver. Findings at preoperative ultrasound (US), conventional CT, and CCTA were compared with those at intraoperative US and surgical exploration as the standard of reference. Forty-four liver metastases were identified in 16 patients, and 14 patients had no metastases. CCTA had a sensitivity of 98% (43 lesions identified) and higher accuracy (81% 154 of 67 diagnoses]) than US and conventional CT. The data indicate that CCTA can supplement information obtained with conventional imaging techniques in patients who must undergo hepatic surgery because of metastases from colorectal carcinoma. metastases

Index

terms:

tomography (CT), tomography (CT), technology #{149} Liver neoplasms, angiography, 761.124 #{149} Liver neoplasms, CT, 761.1211, 761.332 #{149} Liver neoplasms, secondary, 761.332 comparative

Radiology

Computed

studies

1992;

#{149} Computed

185:157-161

I From the Departments of Diagnostic Radiology (MO., S.P.M.M., S.L.T.), Surgical Oncology (B.v.O., T.W.), and Statistics (P.I.M.S.), Dr. Daniel den Hoed Cancer Center, Groene Hilledijk 301, 3075 EA Rotterdam, The Netherlands. Received November 12, 1991; revision requested December 26; final revision received May 11, 1992; accepted May 14. Address reprint requests to MO. C RSNA, 1992

T

Colorectal

Carcinoma:

CT Angiography’

HE presence

or absence of liver metastases is a major determinant of prognosis in patients with colorectal carcinoma (1). Surgical resection of liver tumors has become a widely accepted and utilized therapy in selected patients (2-4). Five- and 10-year survival data have shown a plateau after resection, and long-term survivors seem to have the same risk of death as their age-matched populalion without cancer (2). Over the past decade, the standard modalities for preoperative evaluation of hepatic disease have been computed tomography (CT) and ultrasonography (US) (5,6). Sensitivity of only 38% (14 of 37) to 68% (65 of 95), however, has been reported for diagnosis of hepalic metastatic disease with these modalities

(7-10). Because of the low efficacy of US and CT in predicting liver disease and/or resectability, other preoperalive imaging techniques have been investigated, including angiography, CT angiography, and magnetic resonance (MR) imaging (10-12). CT angiography may be more sensitive for tumor detection than all other methods (10). Intraoperative US is advocated in many institutions as an adjunct to hepalic resection. In one study, intraoperative US resulted in the detection of 25% (40 of 167) and 35% (59 of 150) more lesions compared with preoperalive US and CT, respectively (13). In another study, intraoperative US a!lowed identification of 23% (six of 26) of metastases in cases in which palpalion, preoperative US, or CT did not show any lesions at all (14). Intraoperalive US in combination with surgical palpation is at present considered to be the best method for staging of liver disease (13-15). To our knowledge, CT angiography and intraoperalive US have not been compared in any type of study. In the present study, we prospectively assessed preoperalive US, conventional contrast-me-

dium-enhanced CT, and CT angiography performed with a continuously rotating CT scanner (CCTA) in palients with or without liver metastases from colorectal carcinoma on the basis of findings at conventional CT. Imaging modalities were used independently by different investigators, and all findings were compared with findings at surgical palpation and intraoperalive US as the standard of reference. Correlation with resected specimens was attempted whenever possible. PATIENTS

AND

METHODS

Thirty consecutive patients with a current or previous carcinoma of the colon or rectum (with or without liver involvement) and selected for laparotomy on the

basis of conventional subject of the study.

CT scans Thirty-one

were the patients

had given informed consent over a 1-year period in the Dr. Daniel den Hoed Cancer Center, but one patient was withdrawn because peritoneal carcinomatosis made it impossible to perform intraoperative US of the liver. There were 16 women and 14 men, with a mean age of 58 years (range, 40-73 years). Seventeen patients were treated for primary colon cancer or local recurrence of a previously treated colorectal carcinoma, and 13 patients underwent surgery for isolated liver metastases, 12 for elective resection and one for selective hepatic artery infusion. All patients underwent preoperative evaluation with several imaging modalities. The

routine

included

performance

of

3.5- and 5-MHz US (128 XP; Acuson, Mountain View, Calif) and conventional and contrast-medium-enhanced CT (Somatom Plus; Siemens, Erlangen, Germany) with 5-mm contiguous sections, 1-second scanning time, and interscanning delay of 5 seconds. Contrast-enhanced CT, with administration of nomonic jopromide (Ultravist 300 [300 mg of iodine per miffi-

Abbreviation: raphy.

CCTA

=

continuous

CT angiog-

157

Table

1 Distribution Segment

of Meta

by Liver

stases,

No.

Segment* I

Figure 1. (a) Conventional contrast-enhanced old woman. (a) No liver lesions are evident scan at the same level shows a hypovascular rectly interpreted as a metastasis.

CT and (b) CCTA scans obtained in a 64-year on the conventional enhanced CT scan. (b) CCTA lesion (arrow) in segment VI, which was cor-

0

II

1

HI IV

3 8

II-Iv

2

V VI VII VIII

3 5 7 6

v_vmt

9t

Total

segment

onds; aging

phase with

2-50 mL all modalities

independently,

with

knowledge

than

in

100 was

a history

of colorectal

either

solid

all solid

lesions

Im-

anamnestic

cinoma, and findings with were described independently. anechoic

in

seconds. performed

no other

and

car-

range,

4-10

same

moment

mL/sec)

data

were

sampled

level

over

24 seconds

hold. The total did not exceed with

echo-

mL

both

started

data

at the

same

of jopromide

CT breath

dose

medium

and

(range,

ing to the segmentation of the liver as described by Couinaud (16). All lesions were coded and classified as certainly be-

to the liver

total contrast

CCTA

dose was

190-300

245

mL).

Time between the onset of each set of seclions was less than 3 minutes. An average of 13 sections (range, 10-18 sections) was

ating

obtained.

lesions,

and

lesions

tastases

at CT.

fatty

livers

der,

compatible

enhancing

were

and

classified

nonen-

as me-

Hyperattenuating

and

lesions

adjacent with

in

to the gallbladfocal

Section

nonsteatosis,

were not included. On the following day, angiography was performed and a selective catheter (5-F celiac, Simmons 1-3, or special 5-F; Cordis Europa, Roden, The Netherlands) was placed in the common hepatic artery. In two patients with separate left and right hepatic arteries (insertion from the superior mesenteric artery), the right hepatic artery was chosen. For the comparison with the standard of reference, those parts

of the

sessed

with

liver

that

had

not

all diagnostic

been

as-

techniques

were

excluded. patients

were rotating

before

angiography,

examined

with

CT

system

the

tiguous sections. was chosen for nods (corresponding lion

ond),

fact

represent

solid

lesions

artery These

raphy.

flow rate were amination neous)

injector

nati)

suspended

into

the

were established at angiogsame values for dose and

adjusted

to obtain filling of the

system

backflow

for the CCTA

optimal hepatic

(Liebel-Flarsheim,

from

ex-

(ie, homogevessels. A CT

Cincin-

the ceiling

and filled

with 70 mL of jopromide (300 mg of iodine per milliliter) diluted with 180 mL of norma! saline solution to a solution of 84 mg of iodine per milliliter was connected with the selective catheter after the patient was positioned in the gantry. For each CT sec-

tion, contrast seconds

158

(volume

#{149} Radiology

medium range,

injection 10-20

during mL;

flow

2-3

in

16 images

phases.

images

in

angiography

involves images

as opposed

vessels,

was

(hyper-

per

at

circular

the

capillary

over

peripheral

was

of other

classified reported

All

arterial

data

other

rectal carcinoma. laparotomy was

knowl-

results

than

a history

On the following performed without

of CCTA findings. means of a 5-MHz

by

or a sharp

without

areas (610; Aloka, by a radiologist

or anof cob-

day,

was who

no knowledge of previous imaging The liver surface was inspected

sonographically

by

means

of a water-filled

balloon. The intraoperative US findings were correlated with findings at surgical palpalion and visual inspection of surface besions.

Hepatic

lesions

were

located

of surgical

palpation

by and

vi-

sual inspection of the liver surface combined with intraoperative US. Without intraoperalive US, 38 lesions were identified. The additional six

accord-

detected

with

intraoper-

In 10 patients (14 !eintraoperative US data were

100% that the lesions were metastatic. Most of the other lesions were so superficially located that the macroscopic appearance and one or two positive

biopsy

garded as Of the six intraoperative proved as three, two same

proved

Intraoperatransducer

Tokyo) (S.L.T.)

as malig-

sions), correlated with resected specimens (5-mm slices), and concordance was

as a perfusion

examination

coded

in 16 patients

section phase,

pattern

means

found

were

circular

in the

lesions

were

US only.

time.

demarcated

nant

alive

or hypoattenuating)

with

abnormality. Results were

for small performed

ma-

lesions

were classified as metastases. Proirregular enhancement without a

knowledge live US

uncertainly

to the delinea-

seen

enhancement

demarcation

had data.

of differ-

These

level,

lesions

amnestic

benign,

Forty-four

1.5-second pe540#{176} reconstruc-

with

veins

con-

reconstruction

contiguous

section

hepatic

uncertainly

lignant, and certainly malignant. All diagnostic data were collected and supervised by a trial management office to guarantee independent reporting of each procedure.

exami37-54

with

CT angiography of only one or two

same

and

edge

without

Image

lion of arterial

mum

rate

10 mm

16-24 [maximum, 110] images obtained with CCTA). Detailed

clear

flow

CCTA (range,

transversal

(conventional obtainment the

was

resulting

angiographic

with the catheter in the hepatic artery. The maximum contrast medium dose that could be washed out from the liver parenchyma in 24 seconds and the maxi-

hepatic

data),

ent

phase longed

sec-

average total 50 minutes

nign,

RESULTS

peripheral

a continu-

(360#{176} per

was

thickness

and/or

Immediately ously

The

nation time minutes).

in

section

in a single

angiography

located

IV.

at the

collection.

radiation 280 mGy.

The average

modality At US, all

was

as CT

genic but not sharply demarcated lesions were classified as malignant. All solid lesions, hyperor hypoattenuhancing

44

* Couinaud classification. t Some lesions were also partially

liter]; Schering, Berlin) was performed two phases: phase 1-50 mL in 25 sec-

of

Lesions

tients

specimens

conclusive lesions

re-

detected

only

with

US, three were biopsy metastases; of the other in one patient were of the

appearance

as other

metastases. with

were

for metastalis.

no

There

metastases

biopsy-

were

14 pa-

detected,

nine patients with only one detectable mass, two with two metastases, two with three metastases, and three with four metastases. The mean diameter of solitary liver lesions

(in

In case

of multiple

nine

patients)

liver

was

6.2 cm.

metastases

(seven patients), the mean diameter was 2.3 cm. Overall, 19 lesions were less than 1 cm in diameter and 25

October

1992

S

4.r#{149}’

:

a.

b.

Figure 3. (a) Conventional contrast-enhanced CT and (b) CCTA scans obtained in a 55-yearold woman. A cyst (curved arrow) and a metastasis (open straight arrow) are evident on both scans. CCTA at the same section also revealed a hypovascubar solid lesion (solid arrow in b)

a.

with a hypervascular center. This was correctly interpreted flow of contrast medium in the splenic artery on the CCTA end of the series.

a 5’? b.

in diameter With

CCTA, with

were

detected,

F

20s e.

Figure

2.

(b-e) man.

(a) Contrast-enhanced

shows

no

lesions

at this

level.

CT

Lesions

were also not apparent at adjacent levels. No lesion is visible at (b) 16 seconds of CCTA, but after (c) 18 seconds, a small hypervascubar ring (arrow) of less than 1 cm in diameter became sharply visible. (d, e) The ring (arrow in d) gradually

The lesion

disappears

was correctly

after

2 seconds.

interpreted

as a me-

tastasis.

more

Thirty

than

lesions

1 cm in diameter. were

ated in the right V-VIII), whereas cated

in the

II-IV). caudate bution

left

is given

exclusively

liver lobe 14 lesions liver

lobe

situ-

(segments were !o(segments

in Table

enabled identification of 98% of all lesions and was the sensitive diagnostic modality

of 44)

most (P

the

< .001

two

vs CT

patients

right

artery

the

unperfused

was

or US)

(Figs

1-3).

In

in whom

only

perfused

at CCTA,

lateral

segments

the of

the left lobe were found to be free of metastases (Fig 4). The one false-negative lesion at CCTA was less than 1 cm

Volume

185

Number

#{149}

(18 of 19) of the of 1 cm

as were

100%

patients (n

with

or less

of the three

or

1

in one

(Fig

4), and

a focal

nod-

ties in very inhomogeneously attenuating liver parenchyma; this patient also had seven lesions that were correctly identified. The other three false-positive findings, in one patient,

probably

caused liver

(Fig

of these was interpreted as a satellite lesion but actually belonged the main process, and another with no correlation at surgery was retro-

to

spectively abnormality.

classified

Sensitivity, positive

values

are

as a perfusion

specificity, and negative given

CCTA had the methods (81%;

in Table

accuracy, predictive 4. Over

highest accuracy 54 of 67 diagnoses)

all,

12

HU) over the series of sections obtamed during repeated intraarterial injections. The mean enhancement of liver attenuation in the arterial phase immediately

after

contrast

medium

Therefore,

the

in liver

attenua-

Resection of hepatic lesions secondary to colorectal cancers has proved to be of value (2-4). So far, this is the only

treatment

reported

to be associ-

ated with cure. The most important prognostic factors determining surviva! among patients undergoing hepatic resection are the number of metastatic surgical

deposits margins

in the liver and of the resected

the speci-

men (3,4). Precise evaluation of the number and site of lesions (either unior bibobar) before surgery is therefore essential

to accurate

gery and operations.

avoidance of unnecessary US, CT, hepalic angiogra-

and

trast does

MR

imaging

planning

have

purpose (5-12,17), CT with a high

medium, not show

of sur-

been

used

but even dose of con-

as the best method, high sensitivity in de-

tection of liver metastases from cobrectal cancers, in comparison with that achieved with intraoperative US and surgical resection (13). The discussion on injection vebocity, scanning delay, and quantity contrast medium administered

of all

(Table 4). The overall liver attenuation increased (mean, 5 HU; maximum,

35 HU. increase

DISCUSSION

for this dynamic

by partially

parenchyma

was overall

lion did not influence the detection and conspicuity of the enhancing liver lesions from the beginning of the series to the end.

phy,

4); one

and

1.

CCTA (43

95%

nonperfused

No lesions were found in the lobe (segment I). The distriof lesions according to liver

segment

injection

ret-

ular hyperplasia in another (Fig 4). The other seven false-positive lesions, found in three patients, could not be verified with transection because the liver lobe was not resected. In one patient, four false-positive findings were probably perfusion abnormali-

were were

seen

slight

a diameter

in five

chyma

CT and

CCTA scans obtained in a 70-year-old (a) Conventional contrast-enhanced

scan

barely

5).

more metastases = 18). These percentages were far better than with US and CT (Table 2). CCTA, however, resulted in more false-positive findings (Table 3). Pathologic examination of liver resection specimens revealed a malignant protrusion belonging to the main process in three false-posilive cases, normal hepalic paren-

1

d.

was

(Fig

lesions lesions

,;..

and

rospecively

as a metastasis. Notice the backscan, which was obtained at the

of is not

yet closed (18-20), and differences between patient populations have been reported (7). In the average Dutch patient, in our experience, the injection of 30 g of iodine is adequate for enhancement of the liver parenchyma

and

vasculature.

In most studies, preoperative imaging findings are not correlated with findings at laparotomy or intraoperaRadiology

#{149} 159

Figure 4. False-positive CCTA findings. (a) Liver segments II and III are not perfused. misinterpreted as a metastasis. (b) Segments II and III are not perfused. A malignant sion abnormality (arrow) ventral from the main malignant process was misinterpreted fused. These enhanced after partial withdrawal of the selective catheter in the hepatic

The nonperfused portion in the right lobe (arrow) was lesion is in right dorsal segments VI and VII. The perfuas a satellite lesion. (c) Segments II and III are not perartery (an additional series of CCTA scans of the lateral

segments sion was

was misinterpreted

was obtained). a focal nodular

In segment hyperplasia.

IV, a hypovascular

solid

nodular

lesion

(arrow)

as a metastasis.

Table 2 Sensitivity Techniques

Histologically,

the be-

of Preoperative Diagnostic According to Size and of Lesions

Number

Lesions