European Journal of Cancer 38 (2002) 887–898

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Radiology of colorectal cancer

M.E.J. Pijla,*, A.S. Chaouib, R.L. Wahlc, J.A. van Oostayena
a
Department of Radiology, Leiden University Medical Centre, Albinusdreef 2, 2333 ZA Leiden, The Netherlands
b
Department of Radiology, Boston Medical Center, Boston University School of Medicine, Boston, MA, USA
c
Department of Nuclear Medicine, Johns Hopkins Medical Institute, Baltimore, MD, USA

Received 12 December 2001; accepted 6 February 2002

Abstract
In the past 20 years, the radiology of colorectal cancer has evolved from the barium enema to advanced imaging modalities like
phased array magnetic resonance imaging (MRI), virtual colonoscopy and positron emission tomography (PET). Nowadays, pri-
mary rectal cancers are preferably imaged with transrectal ultrasound or MRI, while barium enema is still the most often used
technique for imaging of colonic cancers. Virtual colonoscopy is rapidly evolving and might considerably change the imaging of
colorectal cancer in the near future. The use of virtual colonoscopy for screening purposes and imaging of the colon in occlusive
cancer or incomplete colonoscopies is currently under evaluation. The main role of PET is in detecting tumour recurrences, both
locally and distantly. Techniques to fuse cross-sectional anatomical (computer tomography (CT) and MRI) and functional (PET)
images are being developed. Apart from diagnostic imaging, the radiologists has added image-guided minimally invasive treatments
of colorectal liver metastases to their arsenal. The radio-frequency ablation technique is now widely available, and can be used
during laparotomy or percutaneously in selected cases. # 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Colorectal; Review; Radiology; Diagnostic imaging

1. Radiology of colorectal cancer
Radiology of colorectal cancer has dramatically
evolved over the past two decades. In the 1980s, colo-
rectal cancer could be diagnosed with a barium enema,
and its liver metastases with ultrasound (US) and incre-
mental computer tomography (CT). Nowadays, there is
a definite difference in the imaging approach of either
colonic or rectal cancer. The method of choice for ima-
ging of colonic cancer is still a double-contrast barium
enema (DCBE), while rectal cancer is preferably imaged
with transrectal ultrasound (TRUS) or magnetic reso-
nance imaging (MRI). Both the use and clinical impact
of DCBE and CT in the imaging of rectal cancer is
limited nowadays. New imaging techniques for both
colonic and rectal cancer are still evolving: virtual
colonoscopy (CT- or MRI-based), positron emission
tomography (PET), and the combination of PET and
a cross-sectional technique like CT (image fusion).
Colorectal liver metastases are imaged with US, MRI,
helical or multi-detector CT and PET. MRI, helical or
multi-detector CT and PET can also be used to image
the direct extension, lymphatic spread and peritoneal
seeding of colorectal cancer. Image-guided, minimally
invasive treatment of colorectal liver metastases is
another new component in the radiology of colorectal
cancer.
The radiology of colorectal cancer is addressed in this
review in four separate sections. In the first section, the
various widely available diagnostic methods for imaging
of primary colorectal cancer are reviewed. The second
and third sections are on virtual colonoscopy, and PET
and image fusion, respectively. The final part describes
the image-guided treatment of colorectal liver meta-
stases. The interaction of endoscopy and radiology in
primary colorectal cancer, and the imaging of colorectal
liver metastases are beyond the scope of this review.
2. Imaging of colorectal cancer
2.1. Introduction

* Corresponding author. Tel.: +31-71-526-4376; fax: +31-71-524-

Most, if not all, colorectal cancers develop via the
8256. adenoma–carcinoma sequence with an adenoma dwell
E-mail address: m.e.j.pijl@lumc.nl (M.E.J. Pijl). time, in the majority of patients, of two to three
0959-8049/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.
PII: S0959-8049(02)00052-7
888 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
decades. The adenoma dwell time for colorectal cancer
in patients with flawed mismatch repair genes is far less,
sometimes less than 2 years [1,2]. The malignant poten-
tial of an adenomatous polyp can be estimated by: size,
presence and length of a stalk, extent of villous change
and degree a cellular atypia and dysplasia [3,4]. Size is
probably the most practical predictor of malignancy.
The risk of cancer increases from virtually zero for
polyps smaller than 5–6 mm to 40–50% for polyps
larger than 2 cm. Sessile polyps carry a high risk
for colorectal cancer in over 50%, compared with 10%
for pedunculated polyps. An increase in the extent
of villous changes in the polyp carries a higher cancer
risk.
2.2. Barium enema
Both colorectal adenomas and colorectal cancers can
be depicted with a barium enema examination. Three
out of four determinants for the estimation of malignant
potential of a polyp can be assessed with a barium
enema: size, presence or absence of a stalk and archi-
tecture (extent of villous change). The villous tumours
often have a fine granular or reticular appearance on
double-contrast barium enemas (DCBE), because bar-
ium gets trapped in fissures at the surface of the tumour.
The fourth determinant, being cellular atypia and dys-
plasia, obviously cannot be assessed.
The barium enema studies can be performed with
either single-contrast or double-contrast techniques.
The sensitivity of properly performed and interpreted
single-contrast versus double-contrast enemas for clini-
cally important lesions, polyps over 1 cm and colorectal
cancers, are similar. The choice to perform either a sin-
gle-contrast or double-contrast enema is therefore
determined by the patient’s ability to cooperate and the
likelihood of colon disease [5,6]. DCBE, though, depicts
polyps less than 1 cm in size better and more reliably
[5,6]. The reported sensitivity of DCBE for polyps over
1 cm is 33–100% [7–9] and for colorectal cancer 62–
100% [2,5,7–9]. The articles by Ott [8] and de Zwart and
colleagues [9] address the wide range of reported sensi-
tivities of DCBE for polyps and colorectal cancers, and
its probable causes, various types of study biases.
In up to 95% of patients, the entire colon can be
examined with DCBE, an obviously important feature,
when it is used as a screening tool for colorectal cancer
and its precursors [7]. The diagnosis of colorectal cancer
also warrants a careful examination of the entire colon
since 5% of patients have a synchronous colon cancer,
and more than one-third have additional adenomatous
polyps [4].
DCBE is generally well tolerated by patients and
complications are uncommon [10]. If a patient is clini-
cally ill or has signs of toxic megacolon, one should
refrain from performing a barium enema [6].
2.3. Computer tomography
The value of CT in the initial work-up of colorectal
cancer is limited. Accuracy rates reported for pre-
operative staging of colorectal cancer ranges between 48
and 77% [11,12]. In selected groups with patients suf-
fering from rectal cancer, the accuracy might be up to
82% [13]. These disappointing numbers are mainly due
to the inability of CT to determine the depth of tumour
bowel wall invasion and to differentiate malignant from
reactive lymph nodes. The former is caused by the lim-
ited intrinsic soft-tissue contrast of CT that prohibits
the visualisation of the various layers of the bowel wall,
and the latter because the detection of malignant lymph
nodes is based on size. In addition, the CT appearance
of colorectal cancer, a discrete soft-tissue mass or focal
wall thickening, is non-specific [14]. Despite these lim-
itations, CT can be used for treatment planning, detec-
tion of distant metastases and assessment of adjacent
organ involvement.
2.4. Ultrasound
Transabdominal ultrasound is generally not used for
the detection of colonic cancer, although many experi-
enced sonographers have probably stumbled over the
‘pseudo-kidney’ sign occasionally. In the detection and
staging of rectal cancer, transrectal ultrasound (TRUS)
is an important tool, since TRUS enables the distinction
of the various layers of the rectal wall [15–17]. With
TRUS, rectal tumours can be staged according to the
T(NM) classification: T1 for tumours confined to the
mucosa or submucosa, T2 for tumours invading the
proper muscle layer, but confined to the rectal wall
(intact outermost serosal layer), and T3 for tumours
penetrating the perirectal fat. The reported tumour sta-
ging accuracy of TRUS ranges between 67 and 93%
[15,16,18]. The most important staging error is over-
staging of T2 tumours as T3 tumours, caused by spon-
taneous (desmoplastic) or iatrogenic inflammation [19].
Contrary to normal (hyperechoic) lymph nodes,
malignant perirectal lymph nodes tend to be hypoe-
choic, and therefore can be fairly easy depicted by
TRUS within the echogenic perirectal fat. The para-iliac
and para-aortal lymph node chains, though, remain
invisible with TRUS. The accuracy of lymph node sta-
ging ranges between 62 and 83% [15,18,20].
A drawback of TRUS is the sub-optimal examination
of patients with a stenotic tumour, since the probe can-
not be placed close enough to the (upper margin of the)
tumour.
2.5. Magnetic resonance imaging
MRI is most useful in colorectal cancer located in the
rectosigmoid, because image quality is only minimally
 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
degraded by respiratory motion and peristalsis, in this
relatively fixed part of the colon. Initially, a body coil or
external surface coils were used to acquire the MRI
images, but nowadays endoluminal or phased array
coils are used [21–24]. MRI images generated with an
endoluminal coil demonstrate very high spatial resolu-
tion, permitting detailed visualisation of both tumour
and rectal wall but, because of the limited field of view,
the mesorectum and surrounding pelvic structures are
difficult to evaluate. When phased array coils are used,
the spatial resolution is not as high as with endoluminal
coils, but it permits imaging with a large field of view
and, thus, the assessment of mesorectum and surround-
ing pelvic structures is possible (Fig. 1). The superior
demonstration of rectal wall layers achieved by endo-
luminal MRI does not improve staging accuracy
(approximately 80%) of rectal cancer compared with
phased array MRI [22]. Beets-Tan and colleagues [21]
published that the clinically more important circumfer-
ential resection margin in rectal cancer can be predicted
very accurately and consistently with phased array
MRI. As with TRUS, the insertion of an endoluminal
coil can be impaired when dealing with a stenotic rectal
tumour.
3. Virtual colonoscopy: a new tool for colorectal cancer
screening
3.1. Introduction
Virtual colonoscopy or CT colonography is a pro-
mising new method for assessing the colon. Helical CT
is used to generate high-resolution, two-dimensional
axial images of the abdomen and pelvis. Three-dimen-
sional images of the colon simulating those obtained
with conventional colonoscopy can be reconstructed
from the data obtained. Favourable attributes of virtual
colonoscopy include its safety, high patient acceptance,
and ability to provide a full structural evaluation of the
entire colon. Indications for virtual colonoscopy include
screening for polyps, incomplete or failed colonoscopy
and preoperative assessment of the colon proximal to an
occlusive cancer (defined as a tumour that cannot be
traversed endoscopically).
3.2. Technique
Although a variety of scanning techniques have been
described for virtual colonoscopy, the same basic imag-
ing principles apply: cleansing the patient’s colon using
a standard barium enema or colonoscopy bowel pre-
paration, colonic insufflation with room air and thin-
section helical CT of the abdomen and pelvis followed
by off-line computer manipulation of the CT dataset to
facilitate inspection of the colonic wall.
889
At this time, a full colon cleansing preparation is
required to achieve acceptable results. Orally adminis-
tered barium contrast products to mark or tag faecal
residue and suppress the need for bowel cleansing are
under investigation. Some investigators have recom-
mended the routine use of a muscle relaxant to prevent
unwanted colonic collapse and spasm, a problem
encountered most commonly in the sigmoid colon.
However, the benefit of spasmolytic agents is con-
troversial. Yee and colleagues [25] compared colonic
distension in 60 patients who were scanned in the supine
and prone positions, and reported no beneficial effect
from routine glucagon administration. In our experi-
ence, adequate distension of the colon and avoidance of
spasm can be obtained if the patients are allowed to
insufflate their colon themselves.
A single acquisition of the abdomen and pelvis is
obtained with the patient holding their breath for 20 s.
Following the supine scan, the helical CT is routinely
repeated with the patient prone. The use of both supine
and prone helical CT datasets helps differentiate mobile
stool from fixed pathology such as cancers and polyps,
allows more even distension of the colon and improves
visualisation of segments of colon obscured by intra-
luminal fluid [26,27]. Unlike fibre-optic colonoscopy,
sedation is not required and patients are immediately
discharged from the CT suite without the need for
observation or recovery. The patient’s ability to return
to work or other activities of daily living is important
when considering societal costs of colorectal cancer
screening programmes.
Fig. 1. 63-year-old male with T3 rectal cancer. MRI: axial T2-weigh-
ted turbo spin-echo image. Tumour almost completely fills the rectal
lumen and penetrates the muscular wall laterally (right side). The
shortest distance between tumour and the mesorectal fascia (white
arrows) is 12 mm (black double-headed arrow).
890 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
3.3. Radiation dose
Radiation dose is approximately 20% lower than the
typical dose for DCBE [28].
3.4. Image display
Following image acquisition, the CT data can be
viewed using a variety of techniques (Figs. 2 and 3).
These include simple evaluation of the axial CT images
at lung window settings (Fig. 2a), reformatted two-
dimensional, images at cross-sectional and orthogonal
planes to the long axis of the colon, and three-dimen-
sional, endoluminal (simulating conventional endoscopy
images (Fig. 2b)) and extraluminal images (simulating
barium enema images (Fig. 3b)). Many investigators
now agree, however, that review of 2D images at lung
window settings is sufficient for detection of potential
abnormalities, and 3D postprocessed views are only
necessary for characterisation of these potential lesions.
The main role of the postprocessed 3D views are to dif-
ferentiate polyps from complex normal colonic folds
Fig. 2. (a) 1 cm polyp (arrow) demonstrated on 2D axial computer
tomography (CT) image displayed at lung window settings. Rectal
tube (arrowhead). (b) Virtual colonoscopy image showing the 1 cm
polyp (crosshair).
which can have a similar appearance when viewed in
profile using the axial images alone.
3.5. CT colonography and polyp detection
Preliminary results indicated that the accuracy of CT
virtual colonoscopy for polyp detection exceeded bar-
ium enema and approached conventional colonoscopy.
Recent published studies from the Boston Medical
Center (BMC), the Mayo Clinic and the University of
California in San Francisco (UCSF) reported results on
relatively large patient populations (Table 1). Fenlon
and colleagues (BMC) [29] prospectively studied 100
patients at high risk for colorectal neoplasia. Virtual
colonoscopy was performed immediately before con-
ventional colonoscopy. The entire colon was visualised
Fig. 3. 50-year-old male with partial obstruction. (a) Axial computer
tomography (CT) image showing circumferential mass of the sigmoid
colon (arrows). (b) Volumetric rendering of the colonic mucosa from
CT data providing detail similar to double-contrast barium enema
(DCBE) showing a large apple core tumour (arrow) in the sigmoid
colon. Note that the colon proximal to this occlusive tumour is well
distended, and assessed by CT colonography. No synchronous tumour
detected.
 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
Table 1
Polyp detection with CT colonography
Study Patients Polyps
>5 mm
BMC [29] 100 58
Mayo Clinic [26] 180 263
UCSF [30] 300 223
a
Subcentimetre range resembles 6–9 mm for the BMC study, and 5–9.9 mm for the Mayo Clinic and UCSF study.
by virtual colonoscopy in 87 patients and by conven-
tional colonoscopy in 89. In 49 patients, a total of 115
polyps and three colorectal cancers were identified. Vir-
tual colonoscopy identified all three cancers, 91% of
polyps that were 10 mm or more in diameter, 82% of
polyps 6–9 mm, and 55% of polyps 5 mm or smaller.
The authors concluded that in patients at high risk for
colorectal neoplasia, virtual and conventional colono-
scopy have a similar efficacy for the detection of polyps
that are 6 mm or more in diameter. Fletcher and col-
leagues (Mayo Clinic) [26] published a series of 180
patients with 420 colonoscopically-proven polyps.
These patients were known to have or were suspected to
have colorectal neoplasms, except for 20 patients
recruited from a surveillance population with a low
prevalence of large polyps. By using supine and prone
patient positioning, the sensitivity and specificity for the
identification of patients with polyps 10 mm or greater
were 85% (82 of 96 patients) and 93% (78 of 84
patients), respectively. The sensitivity and specificity for
the detection of polyps 5 mm or greater were 88% (114
of 130 patients) and 72% (36 of 50 patients), respec-
tively. Yee and colleagues (UCSF) [30] published their
findings in a series of 300 patients. The sensitivity was
90% (74 of 82) for the detection of polyps 10 mm or
larger, 80% (113 of 141) for polyps 5.0–9.9 mm, and
59% (178 of 301) for polyps smaller than 5 mm. The
sensitivity was 94% (64 of 68) for the detection of his-
tologically-proven adenomas 10 mm or larger and 82%
(72 of 88) for histologically-proven adenomas 5.0–9.9
mm. CT colonography accurately detected all eight
colorectal cancers present in this series.
Proper technique is essential for achieving good
results. Results significantly improve if patients are
scanned in the prone and supine position and adequate
colon distension is achieved. Retained fluid in the colon
can be minimised with improvements in bowel prepar-
ation [26,29,31]. As is true for conventional colono-
scopy, virtual colonoscopy has a substantial learning
curve process.
3.6. CT colonography as a screening tool
CT colonography has been shown to be a safe test;
none of the studies published so far has reported com-
891
Per polyp sensitivity (%) Per patient sensitivity (%)
Subcentimetrea 10 mm Subcentimetrea 10 mm
82 91 92 96
47 75 88 85
80 90 93 100
plications. It is also acceptable and well tolerated by
patients. Fenlon and colleagues [29] reported that none
of their patients requested that virtual colonoscopy be
stopped because of discomfort or pain. The actual ana-
lysis of the colon is performed on the CT data at the
physician’s workstation and does not require the patient’s
continued presence. Patients can leave immediately after
the procedure, since no sedation is required.
Adenomatous polyps are common, being present in
30–50% of persons over 50 years of age. Most measure
less than 10 mm in size and, within this subset, the
probability of malignancy is extremely low and the
likelihood of any lesion progressing to malignancy is
extremely small. Many non-neoplastic polyps also
measure less than 10 mm in size. Because many small
polyps have no malignant potential, it may be possible
to target only polyps above a certain size threshold (6
mm or even 10 mm) for colon cancer screening and
colonoscopic removal and by doing so, achieve com-
parable benefits to universal polypectomy with con-
siderable savings in cost and risk. There is a consensus
among researchers that virtual colonoscopy has the
ability to separate patients with colons containing only
subcentimetre insignificant polyps or no polyps from
patients with clinically significant polyps. Only the latter
group would require therapeutic colonoscopy for poly-
pectomy. As only 3–10% of average risk persons age 50
years or over have a polyp 10 mm or greater in size, a
test that could reliably and accurately identify this
group would result in a dramatic reduction in the num-
ber of purely diagnostic colonoscopies performed, free-
ing up endoscopy services for those patients requiring
therapeutic intervention.
3.7. CT colonography and occlusive cancer
Fenlon and colleagues [32] recently reported another
application of virtual colonoscopy, the preoperative
assessment of the colon proximal to an occlusive cancer
(defined as a tumour that cannot be traversed
endoscopically). In 29 patients with occlusive colorectal
cancers, virtual colonoscopy depicted all 29 occlusive
cancers and demonstrated two additional cancers and 24
polyps in the proximal colon. Both of the synchronous
cancers were confirmed intra-operatively and resected.
892 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
Virtual colonoscopy successfully demonstrated the
proximal colon in 26 of 29 patients studied compared
with preoperative barium enema that failed to ade-
quately demonstrate the proximal colon in any patient
studied. In 3 patients, retained stools proximal to an
occlusive tumour prevented a complete virtual colono-
scopic evaluation. Morrin and colleagues [33] had similar
results, and found that CT colonography is superior to
barium enema to assess the colon proximal to an
occlusive tumour. A total of 97% (87 of 90) of all colonic
segments were adequately visualised at CT colonography
in patients with obstructing colorectal lesions (15 patients
were referred after incomplete colonoscopy) compared
with 62% (26 of 42) of segments at barium enema.
3.8. CT colonography and incomplete colonoscopy
Colonoscopy fails to visualise the caecum in a sig-
nificant number of patients, the completion rate may be
80–90% or less. Thiis-Evensen and colleagues [34] pub-
lished their findings in a total of 241 men and women
randomly selected from the population register who
were offered a colonoscopic screening examination to
detect and remove polyps. The caecum was reached in
only 193 (80%) patients. More than half of the adeno-
mas detected were localised proximal to the sigmoid
colon and, in nearly half of the adenoma-bearing sub-
jects examined, the adenoma was proximal to the de-
scending colon. Nicholson and colleagues [35] reported
a similar distribution of adenomas in 1131 asympto-
matic individuals who underwent full colonoscopy. In
25% of people found to have adenomas, the adenomas
were found only in the proximal colon. This emphasises
the importance of a screening method being able to view
the entire colon.
Virtual colonoscopy excels in the evaluation of the
ascending colon, particularly the caecum due to the
degree of distension achievable and the typical lack of
spasm or muscular hypertrophy which is seen in the
sigmoid colon. It is therefore a useful complement to an
incomplete colonoscopy [36,37]. Morrin and colleagues
[36] prospectively studied 40 patients in whom the cae-
cum could not be reached endoscopically, despite
adequate bowel preparation. CT colonography was
performed within 2 h of incomplete colonoscopy in
these 40 patients. In addition, 26 patients (65%) under-
went barium enema immediately after CT colono-
graphy. CT colonography was better tolerated than
barium enema. CT colonography adequately revealed
96% of all colonic segments; in comparison, barium
enema adequately revealed 91% of all segments.
3.9. Extracolonic findings
Since the entire abdomen and pelvis are scanned, the
adjacent abdominal organs can also be assessed. In 264
consecutive patients, Hara and colleagues [38] identified
30 (11%) patients with highly important extracolonic
findings, which resulted in further examinations in 18
(7%) patients, including US in 8, CT in 13, and
intravenous pyelography in 1. 6 patients underwent
surgery because of incidentally discovered findings
(incidental abdominal aortic aneurysms greater than 4
cm in 2, asymptomatic renal adenocarcinomas in 2,
pneumothorax and inguinal hernia containing bowel in
1 patient each). Almost half of all patients had abnor-
mal extracolonic findings detected at CT colonography.
No other colorectal screening examination has the
advantage of detecting potentially life-threatening con-
ditions in an age group where those conditions are
prevalent.
3.10. Conclusions
Results of virtual colonoscopy published in the recent
literature are extremely encouraging. Software techni-
ques designed to improve the speed, accuracy and
reproducibility of results are rapidly emerging. The
challenge remains to reproduce these favourable results
in clinical practice and to evaluate the use of virtual
colonoscopy in a purely screening population. If virtual
colonoscopy proves to be an accurate, reliable and cost-
effective method for detecting polyps and early cancers,
it may dramatically improve participation among the
population in screening programmes and play a major
role in minimising the impact of colorectal cancer.
4. The role of positron emission tomography in
colorectal cancer
4.1. Introduction
Detection, staging and assessing/predicting response
to therapy are long-term goals for imaging in colorectal
cancer. Anatomical methods have been key in this area
and are likely to remain very important, but have lim-
itations. Anatomical methods generally detect cancer by
detecting a mass lesion. Tumours must grow to a certain
volume to be detectable. Furthermore, small tumours
may not be detected, as they cannot be distinguished
from normal variants in tissue anatomy. This is true for
primary lesions and for the most common initial site of
metastases, regional lymph nodes. Metastases to regio-
nal lymph nodes are detected by size criteria in imaging,
with nodes larger than 1 cm in diameter viewed as being
most consistent with malignancy. Anatomical methods
have reported sensitivities for tumour detection of fewer
than 50%. Larger masses are more likely malignant, but
this is not a given fact, as many larger lesions are simply
reactive tissue or scars. Detection of masses is also
dependent on comparisons with normal anatomy.
 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
Normal anatomy is markedly distorted by surgery and
radiation. Such surgical/postoperative changes can
make the diagnosis of tumour recurrence impossible.
Anatomical methods do not predict response to treat-
ment. Thus, methods to complement anatomical imag-
ing are needed.
4.2. Technique
Positron emission tomography (PET) imaging is a
very sensitive quantitative nuclear medicine technique
which detects altered function in tissues, as opposed to
detecting masses alone. In PET, a positron emitter
labelled substance is injected intravenously and allowed
to distribute through the body. After the injection, the
patient is imaged with a PET camera, which looks much
like a CT scanner. The positron is not directly detected
but, rather, photons released from positron decay are
detected. Such detection is very efficient due to the use
of specialised electronics to resolve the time of arrival of
the photons at the camera detectors. A variety of bio-
chemical alterations exist in tumours which can be
imaged by PET with the proper choice of tracer,
including increased glucose metabolism, increased pro-
tein and DNA synthesis, altered receptor phenotypes
among many others. PET tracer choices are limited by
the available positron emitting isotopes, which have
short half lifes, from 2 to 109 min (Table 2). The PET
isotopes are made in a cyclotron, which must be rela-
tively near the PET camera.
The most commonly used PET radiopharmaceutical
for colorectal cancer imaging, and for cancer imaging in
general is [18F]fluoro-2-deoxyglucose (FDG). This agent
is handled much like glucose in the early stages of
tumour glycolytic metabolism. Most notably, it is
transported like glucose into cancer cells and then
phosphorylated by hexokinase to FDG-6-phosphate, a
polar molecule retained in cancer cells. Overexpression
of facilitative glucose transporters and glycolytic
enzymes is typical of colorectal cancer. PET images of
cancers detect FDG-6-phosphate in the cancer cells.
PET imaging with modern scanners is often more sen-
sitive and specific than anatomical methods for cancer
detection. Modern PET cameras and FDG allow imag-
ing of most of the body in less than 1 h.
Table 2
Radioisotopes for PET
Radioisotope Half-life (min)
15
Oxygen 2 A substantial number of manuscripts have been pub-
13
Nitrogen 10
11
Carbon 20
18
Fluorine 110
PET, positron emission tomography.
893
4.3. PET and primary colorectal cancer
PET is being used quite commonly in colorectal can-
cer management in institutions in which it is available.
It is a reimbursed technique by Medicare in the USA,
and this has heightened awareness of its utility. PET has
not been explored extensively in the diagnosis of pri-
mary colorectal cancer. While PET can detect primary
colorectal cancers with a high sensitivity, there are lim-
itations which have decreased interest in this approach.
In brief, there is substantial normal FDG activity in the
gut due to intestinal flora and due to normal uptake of
FDG in muscle, etc. This background tracer uptake makes
the detection of small lesions challenging and this area
has not been explored for screening applications due to
concerns of false-positive interpretations. Thus, the
apparent low specificity in this setting in limited studies
makes evaluation of primary lesions challenging at pre-
sent, at least without anatomical correlates. Of interest,
is that uptake in hyperplastic polyps to date has been low.
PET has been used to some extent for primary staging
of colorectal cancer. However, PET is not capable of
determining the extent or depth of tumour involvement.
For detecting nodal metastases, PET also has size lim-
itations in detection. A prospective trial by Nabi and
colleagues [39] showed a sensitivity of PET of only 29%
for the detection of nodal metastases. This was com-
parable to CT. Thus, PET should not be recommended
for routine use in assessing lymph nodes.
4.4. PET and local tumour recurrence
PET has had much better results in detecting distant
metastases and tumour recurrence. This is the clinical
situation in which PET is commonly used. One of the
earliest reports on the use of PET for clinical imaging
was with FDG in 1982, showing the feasibility of
detecting distant metastases of colorectal cancer [40].
However, the first larger follow-up study compared
PET and CT for local recurrence following abdominal
perineal resection for rectal cancer. In these two studies,
increased FDG uptake was noted in the patients with
tumour versus those with scar. Indeed, approximately
5-fold more uptake was seen in recurrent tumour
patients than in those with scarring. The quantitative
ability of PET was useful in these small studies [41,42].
Anatomical methods were unable to make the differ-
entiation between benign disease and recurrence.
4.5. PET and distant colorectal metastases
lished in the past several years in which more extended
portions of the body were evaluated by PET, using
‘whole body methods’ (Fig. 4). These allow evaluation
of the chest and abdomen, rather than limited regions of
894 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898

Fig. 4. Whole body [18F] fluoro-2-deoxyglucose (FDG) positron emission tomography (PET) images (left to right: axial, coronal and sagittal view)
showing three metastases (black spots) of colorectal cancer to the liver. Black areas in the renal collecting system and bladder represent excreted
tracer in the GU system. Uptake at upper aspect of middle image is in the brain, which is normal.

the body. These studies have shown that PET is more
sensitive than CT for recurrence, PET is more specific
than CT and patient management is changed by the
availability of the PET data.
A representative study of Delbeke and colleagues [43]
showed the accuracy of PET to be 92% for extrahepatic
metastasis detection versus 71% for CT, with manage-
ment changed in 28% of patients. One of the largest
direct comparative trials of PET and CT for accuracy in
colorectal cancer, in 105 patients, showed the overall
sensitivity of PET to be 87% versus 68% for CT, and the
sensitivity for liver metastases superior to that of CT (89%
versus 71%). Of note in this study was that mucinous
tumours were less well detected than other histologies
(sensitivity 58% versus 92%), possibly due to their lower
cellularity than other tumours. While CT-angio-porto-
graphy is a sensitive technique, it has false-positives. PET is
probably also superior to this method in the liver [43].
Results from eleven studies with a total of 281
patients were recently evaluated as part of a meta-ana-
lysis. These showed a sensitivity of 97% for PET and a
specificity of 76% [44]. PET is superior to CT in all
locations, with the possible exception of the lungs,
where metastasis detection is probably comparable [45].
cancer, PET can be very useful in locating the source of
recurrence, with over half of the patients having a
source of the rising tumour marker identified [45,46].
In assessing treatment response, early studies by
Strauss and colleagues [41] and Ito and colleagues [42]
showed good accuracy of PET in assessing areas after
treatment. However, Haberkorn and colleagues [47]
cautioned that early after radiation therapy, false-posi-
tive results could be observed with PET, due to
‘inflammation’. It is generally believed that a delay of
several months after radiation therapy is completed will
reduce the likelihood of false-positive PET scans.
Data available on chemotherapy monitoring indicate
that declines in tumour glucose metabolism are quite
rapid and assessment can be made in a matter of a few
weeks after treatment. The precise role of PET in asses-
sing chemotherapy treatment response is still in evolu-
tion but, clearly, rapid declines in tumour glucose
metabolism are a desirable effect of treatment and seem,
from the body of literature available across a variety of
types of tumours, to be predictive of a favourable
tumour response.
4.7. Cost-effectiveness of PET

4.6. PET and follow-up PET is a more expensive study at most centres than a
CT scan. Is it cost-effective? Two studies have shown
In the setting of rising carcinoembryogenic antigen that it is, obtaining cost saving predictions of US $220
(CEA) levels after ‘definitive’ treatment for colorectal to over US $3000 per case in which PET is performed
 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
by avoiding unneeded or inappropriate surgical pro-
cedures [45,48]. The precise cost savings depend on the
patient population. It should be cautioned that these are
model calculations and may not reflect what happens in
practice if the test is applied to patient populations with
a lower prevalence of disease.
4.8. Image fusion
PET is a relatively new imaging method and like other
methods, one in which there is ongoing growth and
development of the imaging technology. One of the
exciting opportunities in PET at present is the fusion of
anatomical imaging methods and PET into hybrid images
(Fig. 5). This can be done by software methods (anato-
metabolic fusion) or by dedicated hardware devices, in
which PET and CT are performed in the same instru-
ment, a ‘PET-CT’ scanner. These devices will allow us
to combine the best in anatomical and functional ima-
ging, although it is not yet proven that they improve
diagnostic accuracy. None the less, our initial experi-
ence with such a device has been very encouraging.
4.9. Conclusions
PET with FDG is an important tool for colorectal
cancer imaging. The role of PET for primary lesion
detection is not established nor is the data on lymph
node staging promising. PET is very accurate at detect-
ing liver metastases and it could be argued that PET
would be reasonable in patients with larger primary
Fig. 5. Coronal reformatted computer tomography (CT) (left), positron emission tomography (PET) (centre) and fusion hybrid images (right) of
multiple colorectal liver metastases. The metastases appear slightly hyperdense in a steatotic liver on the CT image, black on the PET image and
bright on the fused image.
895
lesions to examine possible liver metastases, which
might be surgically treated at the time of initial resection.
However, the main role of PET in colorectal cancer
has been in detection of recurrence. Similarly, following
a rising CEA level, PET is often the first test performed
after the CT examination is not informative and may
ultimately be performed before CT. Less data exist
regarding the use of PET for routine surveillance, but in
patients with clinical symptoms suggesting recurrence,
PET should probably be considered. The optimal use
and frequency of imaging tests for detecting recurrent
tumour is controversial. In colorectal cancer where iso-
lated metastasis resection can be useful, a stronger case
can be made for routine PET imaging follow-up at reg-
ular intervals than in other, less treatable, conditions.
However, the evidence base to support such conclusions
is not yet firm. In the meta-analysis by Huebner and
colleagues [44], PET changed management in 29% of
patients.
5. Local treatment of colorectal liver metastases
5.1. Introduction
Approximately one-half of all colorectal cancer patients
will develop liver metastases. In 25% of cases, liver
metastases are present at the time of colorectal cancer
diagnosis (synchronous metastases) and a further 25%
will develop liver metastases within 3 years (metachronous
metastases) [49–52]. Without treatment, most patients with
896 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
liver metastases will die between 6 and 11 months,
depending on the amount of liver parenchyma involve-
ment [49]. Some subgroups of patients survive for more
than 2 years; 5-year survival without treatment is rare
[49]. Unfortunately, chemotherapy and radiation ther-
apy are ineffective treatment methods with no or limited
improvement in median survival rates, surgical resection
being the only potential curative option [53].
Surgical resection of colorectal liver metastases in
patients with liver-only solid tumour metastases, how-
ever, is only possible in 10–15% of patients due to pre-
sence of bilobar disease, unfavourable biology with the
presence of more than four metastases, tumour location
preventing the achievement of at least a 1 cm tumour-
free margin [54]. So, in the majority of patients, other
means of controlling or potentially curing liver metas-
tases must be explored [54]. Furthermore, combined
approaches in which surgical resection of one or more
segments and ablation in other segments are simulta-
neously performed, will become increasingly important.
With continued improvements in technology and
increasing clinical experience, one or more of the
following minimally invasive techniques may soon
challenge surgical resection as the treatment of choice
for patients with limited hepatic tumour involvement
[53].
5.2. Percutaneous ethanol injection
Within neoplastic cells, ethanol causes dehydration
and subsequent coagulation. Within vessels ethanol
induces necrosis of endothelium and platelet aggrega-
tion, leading to thrombosis and ischaemia [53]. Unlike
hepatocellular carcinoma, for which ethanol injection is
very effective, colorectal metastases are firm and have
no surrounding capsule making adequate deposition of
ethanol in these metastases difficult and uncontrolled,
leading to spread into surrounding liver tissue and in
the needle tract [49]. The same holds true for the
deposition of boiling saline and acetic acid.
5.3. Hepatic artery embolisation
The hepatic artery carries out 90% of tumour blood
supply and, tumours being sensitive to ischaemia, it
stands to reason to expect embolisation of the hepatic
artery, with or without adding chemotherapeutical
agents, to be effective. In clinical trials, significant
improvement of survival has, however, not been shown
[55,56].
5.4. Thermal ablation
Several thermal ablation methods are in operation
today: laser, microwave, radio-frequency and cryo-
ablation. They all rely on the principle of inflicting
thermal damage to tissue by either heating to more than
50  C or freezing below 30  C: denaturation of cellular
proteins, leading to cell membrane rupture and dehy-
dration, but also coagulation and thrombosis of vessels.
The combined effect leads to tumour destruction.
Ablations using laser, microwave and radio-frequency
can be performed in a percutaneous approach as well as
open (via laparotomy). Cryo-ablation is virtually always
performed in an open procedure. Correct placement of
the thermal device in or at the tumour is the hallmark of
all methods and is nearly always image-guided (CT,
transabdominal US or intra-operative US).
5.4.1. Laser ablation
A reproducible thermal injury can be produced with
neodymium yttrium aluminium garnet (Nd YAG) lasers
[53]. From a single, bare 400-mm laser fibre, light at
optical or near-infrared wavelengths will scatter within
tissue and be converted into heat. Lesions up to 2 cm
can be made. Larger lesions need multiple fibres or the
use of cooled-tip diffuser fibres. In the Middlesex Hos-
pital, London, UK, Lees has reached survival figures for
inoperable colorectal cancer metastases comparable
with those for patients with operable metastases using
laser ablation [53]. A definite advantage of the method
is its MR compatibility and visualisation of temperature
change and coagulation [53].
5.4.2. Microwave ablation
In this type of ablation, the basic mechanism of heat
generation consists of the rotation of water molecules
[53]. The rotation follows the alternating electric field
component of the 2450 MHz microwaves. Ablation
sizes of a single electrode are comparable to laser coag-
ulation. Experience with this method comes mainly
from Japan concerning hepatocellular carcinoma abla-
tion.
5.4.3. Radio-frequency ablation
The principle of radio-frequency ablation depends on
ionic agitation of molecules leading to frictional heat-
ing. The tissue around the electrode acts as a heat
source. A 450–480 kHz electric current flows from a
single electrode with multiple tines or cluster electrode,
depending on the manufacturer, to ground pads placed
on the patient’s thighs. To prevent charring of tissue,
which is detrimental to energy deposition in the tissue,
several methods are used ranging from saline infusion to
cooled tip electrodes. In addition, feedback of the tem-
perature at the tips of the tines and, thus, modulating
output power can diminish the occurrence of charring.
The creation of coagulation areas up to 5 cm is possible
[53].
Complete ablation rates of 52–71% and 5-year survi-
val rates comparable to surgery have been described
[49,53,57].
 M.E.J. Pijl et al. / European Journal of Cancer 38 (2002) 887–898
5.4.4. Cryo-ablation
Freezing tissues to below 30  C will destroy cell
membranes by the formation of ice crystals and will
subsequently destruct cellular structures [49]. Treatment
complications are higher than above-mentioned mod-
alities [53], but very much larger lesions (6–8 cm) can be
treated and the ice ball formation can be monitored by
intra-operative US. Another drawback of this system is
the high price of the equipment. Cryo-ablation is the
oldest of local thermal ablation techniques.
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