The impact of intraoperative ultrasonography on the surgical treatment of patients with colorectal liver metastases.

Abstract

Intraoperative ultrasonography (IOUS) has been the standard in surgical decision making in oncologic liver surgery. Preoperative imaging techniques have improved substantially in recent years; therefore, the importance of IOUS might change. The current results of IOUS were compared with preoperative high-resolution helical CT scanning and the impact of IOUS on surgical decision making was evaluated.
A total of 100 consecutive patients who underwent open surgery for colorectal liver metastases within 4 weeks after preoperative imaging, performed with high-speed helical CT scanners, were included for this study. During surgery, IOUS was performed by a liver specialized radiologist. The findings on preoperative and intraoperative imaging and surgical exploration were compared regarding number, site, and size of the hepatic lesions. The preoperative surgical plan was compared with the final surgical treatment.
One hundred patients with CRLM underwent 117 surgical treatments. In 38 patients IOUS differed from preoperative data. In 23 cases IOUS identified more metastatic lesions. In five patients, intraoperative findings identified smaller or less hepatic lesions. Additional information on the localization of the hepatic lesions was gathered by IOUS and changed the surgical treatment in ten cases. IOUS alone altered the surgical strategy 35 times during 117 procedures. In nearly all cases, discrepancy between the preoperative CT scan and IOUS resulted in a change of surgical treatment.
Despite improvement in preoperative imaging technology, the intraoperative use of ultrasonography remains of crucial importance. The detection of preoperatively unknown lesions remains high with great consequence on surgical therapy.

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The impact of intraoperative ultrasonography on the surgical
treatment of patients with colorectal liver metastases
C. Sietses•M. R. Meijerink•S. Meijer•
M. P. van den Tol
Received: 7 August 2009/Accepted: 19 December 2009/Published online: 29 January 2010
? The Author(s) 2010. This article is published with open access at Springerlink.com
Abstract
Introduction
been the standard in surgical decision making in oncologic
liver surgery. Preoperative imaging techniques have
improved substantially in resent years; therefore, the
importance of IOUS might change. The current results of
IOUS were compared with preoperative high-resolution
helical CT scanning and the impact of IOUS on surgical
decision making was evaluated.
Methods
A total of 100 consecutive patients who under-
went open surgery for colorectal liver metastases within
4 weeks after preoperative imaging, performed with high-
speed helical CT scanners, were included for this study.
During surgery, IOUS was performed by a liver specialized
radiologist. The findings on preoperative and intraoperative
imaging and surgical exploration were compared regarding
number, site, and size of the hepatic lesions. The preop-
erative surgical plan was compared with the final surgical
treatment.
Results
One hundred patients with CRLM underwent 117
surgical treatments. In 38 patients IOUS differed from
preoperative data. In 23 cases IOUS identified more met-
astatic lesions. In five patients, intraoperative findings
identified smaller or less hepatic lesions. Additional
information on the localization of the hepatic lesions was
gathered by IOUS and changed the surgical treatment in
ten cases. IOUS alone altered the surgical strategy 35 times
Intraoperative ultrasonography (IOUS) has
during 117 procedures. In nearly all cases, discrepancy
between the preoperative CT scan and IOUS resulted in a
change of surgical treatment.
Conclusions
Despite improvement in preoperative imag-
ing technology, the intraoperative use of ultrasonography
remains of crucial importance. The detection of preopera-
tively unknown lesions remains high with great conse-
quence on surgical therapy.
Keywords
Colorectal liver metastasis ? Liver surgery
Radiology ? Ultrasonography ?
Preoperative mapping of metastatic lesions in the liver is of
crucial importance when patientsare consideredfor surgical
treatment. Computer tomography (CT) and intraoperative
ultrasonography (IOUS) are most frequently used. Histori-
cally, CT missed approximately 20–40% of the malignant
lesions compared with IOUS. The influence of IOUS on
surgical decision making for hepatic malignancies has been
documented by numerous reports since the 1980 s. The
preoperativelyplannedsurgicalprocedureswerechangedas
a result of IOUS in 19–65% of cases [1–4].
CT scanning techniques (as well as ultrasonographic
technology) have changed dramatically since then. The
accuracy of modern imaging with high-resolution helical
CT scanners has increased. However, the exact role of
these techniques for the analysis of liver metastasis and for
surgical decision making remains unclear.
The goal of this study was to determine the accuracy of
preoperative CT scanning compared with IOUS in patients
who were treated surgically for colorectal liver metastasis.
The preoperative surgical plan was compared with the final
surgical treatment to see whether intraoperative findings
C. Sietses ? S. Meijer ? M. P. van den Tol (&)
Department of Surgery, Vrije Universiteit Medical Centre,
P.O. Box 7057, 1007 MB Amsterdam, The Netherlands
e-mail: mp.vandenTol@vumc.nl
M. R. Meijerink
Department of Radiology, Vrije Universiteit Medical Centre,
Amsterdam, The Netherlands
123
Surg Endosc (2010) 24:1917–1922
DOI 10.1007/s00464-009-0874-8

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(IOUS and surgical exploration) affected the treatment
strategy in our patient population.
Methods
One hundred consecutive patients who underwent surgery
for colorectal liver metastases were included. All patients
underwent preoperative helical CT imaging. Patients who
are described in this series were for a large part also
included in a Dutch national study in which patients were
randomized between workup and follow-up with or without
FDG-PET. Therefore, not all patients were analyzed with
FDG-PET scanning.
In almost all patients referred to our institution, meta-
static lesions were identified or suspicion was raised based
on (periodic screening) transabdominal ultrasonography of
the liver and/or an increase of serum CEA levels.
Routine preoperative 4-phase helical CT scans of the
upper abdomen were obtained on a 4-slice multi-detector
CT scanner (Somatom Volume Zoom, Siemens, Erlangen,
Germany) or a 64-slice multi-detector CT scanner (Som-
atom Sensation, Siemens). The series were acquired at
maximum inspiration before (unenhanced phase) and 30
seconds (hepatic arterial phase), 70 seconds (portal venous
phase), and 300 seconds (equilibrium) after intravenous
injection (3–4 ml/s) of 100 ml of a low-osmolar, nonionic
contrast agent with an iodine concentration of 300 mg/ml
(Ultravist-300 Iopromide; Bayer Pharma AG, Berlin,
Germany), using an injection pump through an 18-g can-
nula in the left or right antecubital vein. Scanning param-
eters were 120 kV and 180 mAs with dose modulation at a
slice collimation of 4 x 2.5, rotation time of 0.5 seconds,
and pitch of 1.25 for the 4-slice multi-detector CT scanner,
and collimation of 32 x 0.6 mm, rotation time of 0.33
seconds, and pitch of 0.75 for the 64-slice multi-detector
CT. All series were reconstructed in 5-mm contiguous axial
and coronal slices.
In our hospital, 4-phase CT of the upper abdomen was
routinely performed for all patients who had no recent CT
scan (acquired maximum 4 weeks before surgery) and for
all atypical liver lesions on recent portal-venous-phase-
only scans from other hospitals (such as hypervascular or
cystic-appearing liver metastases). If necessary, gadolin-
ium-enhanced liver magnetic resonance imaging (MRI)
was used as a problem solver. Several patients already
underwent a preoperative CT scan at an outside institution.
All of these images were reviewed by our radiologists and
if needed additional scans were made.
All patients underwent IOUS (Prosound Alpha10; 10.0-
MHz linear intraoperative probe and 5.0/1.25-MHz convex
probe, Aloka, Tokyo, Japan) performed by an experienced
interventional radiologist, who carefully noted the exact
size (maximum diameter), number, and location of all
CRLM.
The intraoperative findings were saved. Data recorded
included the number and size of hepatic malignant lesions
and evidence of local extension of disease. The findings on
preoperative and intraoperative imaging and surgical
exploration were compared regarding number and exten-
sion of the hepatic lesions. To assess whether treatment
was altered, all surgeons’ reports were reviewed and
evaluated. Ultimately, the surgical treatment strategy
resection—radiofrequency ablation (RFA) alone or com-
bined with resection—was based on the intraoperative
findings.
Results
Between January 2007 and January 2009, 100 consecutive
patients (55 men, 45 women) with CRLM underwent 117
surgical procedures, resection, RFA, or a combination of
both. The characteristics of the patients and their primary
tumors are summarized in Table 1. The surgical treatment
methods are summarized in Table 2.
Overall, intraoperative findings (IOUS plus surgical
exploration) yielded additional information on number,
size, localization, and/or local extension of metastases in
45 cases (Fig. 1).
In 38 of the patients, findings on IOUS differed from
those of the preoperative CT scan. In 23 of those cases,
IOUS identified more hepatic malignant lesions than the
preoperative CT scan: 20 true new lesions, and 3 satellite
lesions originating from known metastases. In four
patients, IOUS detected fewer lesions. In one patient, the
metastatic lesion was smaller on IOUS than anticipated on
the preoperative CT scan, changing the surgical treatment
to a less extensive resection.
Additional information on the localization of the
hepatic lesions was gathered by IOUS and changed the
surgical treatmentin ten cases.This additional
Table 1 Characteristics of patients and localization of primary
carcinomas
Characteristic Data
Total no. patients 100
Male/female ratio 55/45
Age (yr)
Median 65
Range 37–82
Primary tumor
Colon68
Rectosigmoid 11
Rectum 21
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information led to more extensive resection in two cases.
In seven patients, a RFA procedure was performed
instead or additionally. In one patient, the hepatic lesion
was found to be located more superficial than expected,
changing the preoperative plan to perform a RFA pro-
cedure into a wedge resection.
Cohen’s kappa measure of concordance between CT and
IOUS findings was 0.84 for the number of CRLM and 0.79
for number, exact size, and localization of CRLM.
Surgical exploration identified more extensive extrahe-
patic disease in seven patients. In four patients, exploration
detected diaphragmatic invasion, which altered the treat-
ment; partial diaphragmatic resection was performed en
bloc with the liver metastasis.
Inthreepatients,surgicalexplorationidentifiedperitoneal
metastatic deposits. In two of these patients, the metastatic
deposits were so extensive that resection was not possible.
However, the other patient had only limited extrahepatic
disease (solitary peritoneal deposits), amenable for resection.
Intraoperative findings (IOUS plus surgical exploration)
changed the preoperative surgical plan for 42 of 117 pro-
cedures. In 45 patients, the intraoperative findings differed
from the information gathered preoperatively on CT; in
only three patients, these discrepancies did not result in a
change of treatment strategy.
Table 2 Summary of 117 surgical treatments of hepatic metastases
in 100 patients
Surgical treatment Frequency (%)
Hemihepatectomy 23 (20%)
Left12 (10%)
Right 9 (8%)
Extended
Partial resectiona
2 (2%)
46 (39%)
RFA alone
Combined treatmentb
30 (26%)
13 (11%)
RFA and resection11 (9%)
RFA and right portal vein ligation
Nonec
2 (2%)
5 (4%)
Total117 (100%)
aPartial resection comprises metastasectomies and segmentectomies
bRFA and right portal ligation was combined in two patients with
bilobar liver metastases to achieve hypertrophy of the left liver seg-
ments, making a secondary hemihepatectomy possible. In one patient,
portal vein ligation alone was attempted to achieve the same, but this
patient developed extrahepatic metastatic disease
cNo surgical treatment was undertaken in five patients because of
diffuse intrahepatic metastases in three and peritoneal carcinomatosis
in two patients. However, one patient with diffuse metastases under-
went combined RFA and resection of his bilobar metastases 7 months
after his explorative laparotomy and chemotherapy treatment
Procedures
117 (100%)
Concordance between pre- and
intraoperative findings
72 (62%)
Disconcordance between pre-
and intraoperative findings
45 (38%)
Hepatic disconcordance
38 (32%)
Extrahepatic disconcordance
7 (6%)
Diapragm extension 4 (3%)
Peritoneal depositis 3 (3%)
More metastases 23 (20%)
Less metastases 4 (3%)
Localization difference 10 (9%)
Considerable size difference 1
(1%)
Fig. 1 Concordance between
pre- and intraoperative
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IOUS alone altered the surgical strategy 35 times during
117 treatments (30%). In nearly all (92%) cases, discrep-
ancy between the preoperative CT scan and IOUS resulted
in a change of surgical treatment. In general, IOUS iden-
tified more hepatic metastases, necessitating more exten-
sive hepatic resection, RFA instead of resection, or a
combination of those treatment modalities.
No surgical treatment was undertaken initially for an
additional three patients because of diffuse intrahepatic
metastases. However, one of the patients with diffuse
metastases underwent combined treatment of RFA and
resection 7 months after successful downstaging with
chemotherapy.
Discussion
Intraoperative ultrasonography has been considered the
‘‘gold standard’’ since it was shown that the additional
information found for many patients had a great impact on
the surgical plan. Various authors reported that IOUS
provided new information that influenced surgery in up to
50% of cases [1–4]. With the availability of modern
imaging techniques, some have questioned the need for
IOUS as diagnostic tool and only use it to plan their
resection [5, 6].
In our series, however, the importance of IOUS in
detecting preoperatively unknown lesions remains high. In
38% of patients, IOUS differed from the preoperative CT
scan; more importantly, if discrepancies were found
between IOUS and CT it nearly always changed the type of
resection that was performed. These results are confirmed
by others. Even though Ellsmere et al. questioned, ‘‘Why
are we still performing IOUS during planned liver resec-
tion,’’ they found that the frequency of unrecognized
tumors during surgery did not change during the past
10 years. They compared 50 consecutive cases with a
comparable historical group. They found that the rate of
undetected tumors ranged between 14–20%, changing their
surgical plan in one fifth of patients [5].
In resent years not only the CT scan has been used for
the preoperative workup. FDG-PET is of great importance
in staging colorectal liver metastases, but whether FDG-
PET changes the ‘‘gold standard’’ of IOUS remains to be
seen. Patients described in this series were for a large part
also included in a Dutch national study in which patients
were randomized between workup and follow-up with or
without FDG-PET. As a result, half of the patients were
analyzed and operated without preoperative PET scan.
Therefore, we could not use these data in this analysis. The
results of this study were presented recently and showed
that workup with FDG-PET reduced the number of futile
laparotomies; however, it did not influence disease-free
survival or the total costs. The complete results will be
published in the near future. Wiering et al. analyzed the
accuracy of CT and FDG-PET compared with IOUS. Both
PET and CT were sensitive for detecting lesions[2 cm.
However, sensitivity declined rapidly when lesions were
\2 cm. Only 16% of lesions\1 cm were detected preop-
eratively [7]. The results of this study are comparable with
our data that 30% more lesions were found during lapa-
rotomy. Strangely, this difference with preoperative
knowledge had hardly any influence on clinical manage-
ment. Previous studies from this group did show that FDG-
PET decreased the number of futile laparotomies by better
detection of extrahepatic disease [8, 9].
Wildi et al. studied preoperative PET/CT with or with-
out IOUS and correlated these results with histopatholo-
gical and clinical follow-up data. They found that
sensitivity of PET/CT alone was 63% versus 93% when
PET/CT was combined with IOUS. After preoperative
chemotherapy, these data were comparable: PET/CT 77%
and combined with IOUS 100%. In 35% of the cases, IOUS
changed the surgical plan [10].
Rohren et al. also studied the importance of FDG-PET
and compared this with IOUS. They found that FDG-PET
is highly accurate in determining the presence or absence
of hepatic metastases; however, FDG-PET is less accurate
in determining the precise number and distribution of
hepatic metastases. FDG-PET accurately defined the
number and location on lesions in 55% of patients. As in
other studies, lesion size was a significant factor in the
detection of hepatic metastases by FDG-PET. Whether the
preoperative plan based on PET changed due to intraop-
erative finding was not discussed [11].
In contrast with these data are the resent results of
Figueras et al., which report a low sensitivity of CT scan
alone; however, IOUS only changed their surgical proce-
dure in 11% [12]. Overall, the conclusion can be made that
IOUS remains the ‘‘gold standard’’ for the number and
location of liver metastases. PET/CT is simply not sensitive
enough to detect smaller lesions.
In our clinic, we hold the policy to spare as much liver
parenchyma as possible—of course never at the cost of
irradicality. There are two reasons for this policy. First, it
reduces the need for major hepatectomies, which are
associated with morbidity and mortality. Second, it makes
secondary surgery for recurrent disease easier. IOUS helps
us plan our resections. The varying results of whether
IOUS changes the surgical plan depend, of course, mainly
on the extent of the planned resection [13]. If you are
sparing liver volume, it will change your surgical plan.
Even though IOUS can currently be considered the best
there is, it is obviously not good enough. Almost half of the
patients will have recurrent disease in the liver; most of
these lesions develop out of small metastases present
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during the first exploration and therefore were missed by
IOUS.
Various imaging techniques are analyzed to see whether
preoperative accuracy can be improved.
Recently, we published the preliminary results of total-
liver-volume perfusion CT (CTP) technique for the detec-
tion and characterization of liver metastases [14]. Twenty
patients underwent helical CT of the total liver volume
before and 11 times after intravenous contrast-material
injection. To decrease distortion artefacts, all phases were
coregistered using 3-D image fusion before creating blood-
flow maps. Lesion-based sensitivity and specificity for liver
metastases of first the conventional 4 phases and later all 12
phases, including blood-flow maps, were determined
compared to intraoperative ultrasound and surgical explo-
ration. These preliminary results showed significantly
increased sensitivity of total-liver-volume CTP.
Currently, we also are using contrast-enhanced intra-
operative ultrasound (CE-IOUS) to improve the results;
however, it is too early to report our data.
Leen et al. recently showed that CE-IOUS was signifi-
cantly more sensitive than IOUS (96.1% versus 81.5%)
[15]. It altered their surgical management in almost 30% of
cases. However, in this study there was no difference
between preoperative imaging and conventional IOUS,
which is somewhat surprising considering the current lit-
erature. Furthermore, the median size of the additional
lesions found with CE-IOUS was 8 mm, which is well over
the detection limit of conventional IOUS. Even though the
improved sensitivity of contrast-enhanced ultrasound is
confirmed in some studies, others question its value [16,
17].
The current results of gadolinium-enhanced MRI for
colorectal liver metastases are still under debate; however,
sensitivity and specificity seems slightly higher compared
with portal-venous-phase contrast-enhanced helical CT
[18].
In conclusion, despite improvement of preoperative
imaging technology, the intraoperative use of ultrasonog-
raphy remains crucially important. The detection of pre-
operativelyunknown lesions
consequence on surgical therapy. New techniques, such as
total-liver-volume perfusion CT and contrast-enhanced
intraoperative ultrasound and MRI, are being studied to
improve diagnostic accuracy of preoperative imaging.
ishigh withgreat
Disclosures
and Dr. M. P. van den Tol have no conflicts of interest or financial ties
to disclose.
Dr. C. Sietses, Dr. M. R. Meijerink, Prof. Dr. S. Meijer,
Open Access
Creative Commons Attribution Noncommercial License which per-
mits any noncommercial use, distribution, and reproduction in any
medium, provided the original author(s) and source are credited.
This article is distributed under the terms of the
References
1. Meijer S, Paul MA, Cuesta MA, Blomjous J (1995) Intra-oper-
ative ultrasound in detection of liver metastases. Eur J Cancer
31A(7–8):1210–1211
2. Bismuth H, Castaing D, Garden OJ (1987) The use of operative
ultrasound in surgery of primary liver tumors. World J Surg
11(5):610–614
3. Zacherl J, Scheuba C, Imhof M, Zacherl M, La ¨ngle F, Pokieser P,
Wrba F, Wenzl E, Mu ¨hlbacher F, Jakesz R, Steininger R (2002)
Current value of intraoperative sonography during surgery for
hepatic neoplasms. World J Surg 26(5):550–554
4. Parker GA, Lawrence W Jr, Horsley JS 3rd, Neifeld JP, Cook D,
Walsh J, Brewer W, Koretz MJ (1989) Intraoperative ultrasound
of the liver affects operative decision making. Ann Surg
209(5):569–577
5. Ellsmere J, Kane R, Grinbaum R, Edwards M, Schneider B, Jones
D (2007) Intraoperative ultrasonography during planned liver
resections: why are we still performing it? Surg Endosc
21(8):1280–1283
6. Rydzewski B, Dehdashti F, Gordon BA, Teefey SA, Strasberg
SM, Siegel BA (2002) Usefulness of intraoperative sonography
for revealing hepatic metastases from colorectal cancer in
patients selected for surgery after undergoing FDG PET. AJR Am
J Roentgenol 178(2):353–358
7. Wiering B, Ruers TJ, Krabbe PF, Dekker HM, Oyen WJ (2007)
Comparison of multiphase CT, FDG-PET and intra-operative
ultrasound in patients with colorectal liver metastases selected for
surgery. Ann Surg Oncol 14(2):818–826
8. Wiering B, Krabbe PF, Dekker HM, Oyen WJ, Ruers TJ (2007)
The role of FDG-PET in the selection of patients with colorectal
liver metastases. Ann Surg Oncol 14(2):771–779
9. Ruers TJ, Langenhoff BS, Neeleman N, Jager GJ, Strijk S,
Wobbes T, Corstens FH, Oyen WJ (2002) Value of positron
emission tomography with [F-18]fluorodeoxyglucose in patients
with colorectal liver metastases: a prospective study. J Clin Oncol
20(2):388–395
10. Wildi SM, Gubler C, Hany T, Petrowsky H, Clavien PA, Jochum
W, Gerlach T, Fried M, Mullhaupt B (2008) Intraoperative
sonography in patients with colorectal cancer and resectable liver
metastases on preoperative FDG-PET-CT. J Clin Ultrasound
36(1):20–26
11. Rohren EM, Paulson EK, Hagge R, Wong TZ, Killius J, Clavien
PA, Nelson RC (2002) The role of F-18 FDG positron emission
tomography in preoperative assessment of the liver in patients
being considered for curative resection of hepatic metastases
from colorectal cancer. Clin Nucl Med 27(8):550–555
12. Figueras J, Planellas P, Albiol M, Lo ´pez-Ben S, Soriano J, Co-
dina-Barreras A, Pardina B, Rodrı ´guez-Hermosa JI, Falgueras L,
Ortiz R, Maroto A, Codina-Cazador A (2008) Role of intra-
operative echography and computed tomography with multiple
detectors in the surgery of hepatic metastases: a prospective
study. Cir Esp 83(3):134–138
13. Torzilli G, Procopio F, Botea F, Marconi M, Del Fabbro D,
Donadon M, Palmisano A, Spinelli A, Montorsi M (2009) One-
stage ultrasonographically guided hepatectomy for multiple
bilobar colorectal metastases: a feasible and effective alternative
to the 2-stage approach. Surgery 146:60–71
14. Meijerink MR, van Waesberghe JH, van der Weide L, van den
Tol P, Meijer S, van Kuijk C (2008) Total-liver-volume perfusion
CT using 3-D image fusion to improve detection and character-
ization of liver metastases. Eur Radiol 18:2345–2354
15. Leen E, Ceccotti P, Moug SJ, Glen P, MacQuarrie J, Angerson
WJ, Albrecht T, Hohmann J, Oldenburg A, Ritz JP, Horgan PG
(2006) Potential value of contrast-enhanced intraoperative
Surg Endosc (2010) 24:1917–19221921
123

Page 6

ultrasonography during partial hepatectomy for metastases: an
essential investigation before resection? Ann Surg 243(2):236–
240
16. Fioole B, de Haas RJ, Wicherts DA, Elias SG, Scheffers JM, van
Hillegersberg R, van Leeuwen MS, Borel Rinkes IH (2007)
Additional value of contrast enhanced intraoperative ultrasound
for colorectal liver metastases. Eur J Radiol 27
17. Larsen LP, Rosenkilde M, Christensen H, Bang N, Bolvig L,
Christiansen T, Laurberg S (2007) The value of contrast
enhanced ultrasonography in detection of liver metastases from
colorectal cancer: a prospective double-blinded study. Eur J
Radiol 62(2):302–307
18. Bipat S, van Leeuwen MS, Comans EF, Pijl ME, Bossuyt PM,
Zwinderman AH, Stoker J (2005) Colorectal liver metastases:
CT, MR imaging, and PET for diagnosis-a meta-analysis. Radi-
ology 237(1):123–131
1922 Surg Endosc (2010) 24:1917–1922
123