World J. Surg. 24, 43–48, 2000DOI: 10.1007/s002689910009 WORLD

Journal ofSURGERY© 2000 by the Societe

Internationale de Chirurgie

Intraoperative Ultrasonography versus Helical Computed Tomography andComputed Tomography with Arterioportography in Diagnosing Colorectal LiverMetastases: Lesion-by-lesion Analysis

Johannes Schmidt, M.D.,1 Markus Strotzer, M.D.,2 Stefan Fraunhofer, M.D.,1 Herman Boedeker, M.D.,3

Hubert Zirngibl, M.D.1

1Department of Surgery, University of Witten-Herdecke, Heusner-Strasse 40, D-42883 Wuppertal, Germany2Department of Radiology, University of Regensburg, Franz-Josef-Strauss-Allee 11, D-93042 Regensburg, Germany3Department of Surgery, University of Regensburg, Franz-Josef-Strauss-Allee 11, D-93042 Regensburg, Geramny

Abstract. Helical computed tomography with arterioportography (CTAP)and intraoperative sonography (IOUS) are both recognized to be ex-tremely sensitive in the detection of liver metastases measuring <2 cm indiameter. As sensitivity and specificity values for both techniques differsignificantly in the literature and in default of sufficient published dataregarding this subject, a lesion-by-lesion analysis was considered neces-sary. Accuracy of IOUS was compared with helical computed tomography(CT) and portal-phase contrast enhancement (CTAP) in the preoperativedetection of liver metastases from colorectal carcinoma projected as aprospective blinded study. Cost efficiency should be determined. LiverCTAP and IOUS were evaluated in 33 patients with colorectal carcinoma.Metastases were resected in 10 cases, and the remaining 23 patients wereobserved for follow-up with CT investigations every 3 months for a periodof 1 year. CTAP and IOUS detected all 13 lesions measuring 5–10 mm(13/13). One metastasis measuring >10 mm was missed by IOUS. CTAPpresented an ideal sensitivity of 100%, but specificity was as low as 68%.IOUS sensitivity was 98% and specificity was 95%. IOUS and CTAP are ofcomparable value regarding the detection of liver metastases <10 mm.Both techniques may be used if resections of synchronous or metachro-nous metastases are planned in order not to miss limiting small lesionsand to prevent superfluous liver surgery. Helical CT scan with dynamicintravenous contrast enhancement is considered the most cost-effectivepreoperative staging method, although local staging may not be achievedbecause of insufficient intraabdominal survey.

The prevalence of colorectal cancer reaches approximately260,000 new cases in western Europe every year [1, 2]. From 15 to25% of these patients present with synchronous liver metastasesand at least another 20% are believed to harbor occult hepaticmetastases which have remained undetected by conventional im-aging techniques such as ultrasonography and standard computedtomographic (CT) scan [3].

Only 6% of patients with untreated solitary liver metastasesmay reach a 5-year survival. With the surgical improvements ofthe past 10 years, leading to better segmental conducted resec-tions due to better understanding of liver anatomy, the outcomeof resected patients has improved remarkably. Therefore, resec-tion of hepatic metastases has gained an important role in the

management of colorectal carcinoma [1]. Even multiple lesionsmay be treated in both lobes when segmental resection is possibleand sufficient liver tissue is left behind [4].

Computed tomography with arterioportography (CTAP) andintraoperative ultrasonography (IOUS) are both recognized asthe most sensitive staging modalities, but CTAP has not beenaccepted as a routine procedure yet because of its invasiveness[4–9]. Helical CT with portal-phase contrast enhancement is verysensitive in detecting hepatic lesions .10 mm, but it is insensitivebelow this diameter [5]. Although there are numerous publica-tions related to these techniques, sufficient data are not availableregarding a lesion-by-lesion and patient-by-patient analysis in cor-relation with the size of the corresponding intrahepatic tumor[10].

In these times of diminishing and indebted health care systems,we have been encouraged to select the most cost-effective stagingprocedure while taking into consideration the different qualitiesof all the above-mentioned techniques. Therefore, we conductedthis prospective blinded study to compare the accuracy of helicalCT, helical CTAP, and IOUS in the detection of hepatic metas-tases from colorectal carcinoma.

Materials and Methods

Thirty-three patients with colorectal carcinoma were prospec-tively studied over a 16-month period from 1995 to 1996. Therewere 12 female and 21 male patients; mean age was 63 years(range 32–83). If there was evidence of irresectable liver metas-tases by means of intravenous (IV) contrast-enhanced helical CTthe patient was excluded. The group of patients investigated in thepresent study represents a selected population. These patientswere all referred specially to our institution because of sono-graphic evidence of hepatic tumor in coincidence with colorectalcarcinoma. Six patients presented with metachronous liver metas-tases after curative removal of the primary tumor. The remaining27 patients were referred for primary resection of colorectalcancer.Correspondence to: J. Schmidt, M.D.

CT studies were performed on Somatom Plus S scanners (Sie-mens Corp., Erlangen, Germany). For IV contrast-enhanced he-lical CT and helical CTAP, slice thickness was set at 5 mm (210mA, 120 kVp, 32 rotations) and table feed was 7 mm/s withreconstruction intervals of 4 mm. During IV contrast-enhancedhelical CT, 200–240 ml of iopamidol 300 (Solutrast 300, Byk-Gulden Corp., Konstanz, Germany) was injected at a flow rate of2.5–3.0 ml/s. Scan delay was set at 66–72 s, resulting in arterial andportal-venous enhancement. For helical CTAP, a 7F catheter wasplaced into either the superior mesenteric or the splenic artery.Injection of 90 ml of iopamidol 300 at a flow rate of 1.5 ml/sfollowed. Scan delay was set at 46 s. Helical CT studies wereperformed within 1 phase of breath hold of 32 s.

Examination of all CT images was performed by 2 independentgroups of investigators from the Department of Radiology andincluded number, size (divided into 5-mm steps), and character-ization of lesions. The readers were blinded. Segmental anatomywas used to define lesions at CTAP.

In all cases, patients underwent median laparotomy. The liverwas inspected and palpated bilaterally after mobilization if adhe-sions were present. IOUS was performed with a CS 9200 scanner(Hitachi-Picker Corp., Munich, Germany) using 6.5 and 7.5 MHzarrays in 2 steps. In the first step, the intraoperative investigatorwas blinded to the findings of preoperative imaging. Due toethical considerations, each examination was repeated withknowledge of the preoperative helical CT and CTAP results.

IOUS was performed by 2 investigators from the Departmentof Surgery (J.S./H.B.) with similar training in segmental sonogra-phy of the liver. The examining surgeon was not present at thetime of laparotomy and did not palpate the liver surface prior toIOUS. Examination included number of lesions, size, localizationwithin the liver (segment), abnormal vessel anatomy, distancefrom the anterior and posterior liver surface, and sonomorpho-logic characterization. The scanners were placed directly on theliver surface. IOUS sequences were documented on S-VHS videoand evaluated directly after the operation. If no hepatic resectionwas performed every lesion had to undergo a biopsy procedure torule out malignancy.

Three hemihepatectomies and 7 atypical liver resections wereperformed. The remaining 3 patients with metastases were ob-served for follow-up with helical CT scans every 3 months for aperiod of 1 year. All patients had to present to a standard fol-low-up every 3 months for examination of chest, liver, and labo-ratory and clinical status.

For statistical analysis, the chi-square test was used to comparesensitivities and specificities of helical CTAP with IV contrast-

enhanced helical CT and IOUS. For sensitivities and specificities,95% confidence intervals (CI) were calculated to correct forsample size.

All procedures were approved by the ethical committee onhuman experimentation of the University of Regensburg, Ger-many.

Results

Forty-nine lesions suspicious for metastases were found in 13 ofthe entire group of 33 patients; 24 lesions presented a diameter#10 mm (49%). Mean examination time for IOUS was 8 6 2 min.In 17 patients (52%), adhesions in the upper quadrant werepresent and had to be divided for liver palpation and IOUS.

Both radiologic imaging modalities were negative for 1 patientin whom a single metastasis measuring 4 mm was found bypalpation and IOUS. Helical CTAP was negative for 1 lesion ,5mm in diameter. This lesion was not biopsied because of technicalfailure. The largest metastasis missed by IV contrast-enhancedhelical CT was 16–20 mm. IOUS missed 1 lesion measuring 10–20mm located in the liver dome. In this particular case, division ofpresent adhesions was incomplete due to technical reasons. Bothlesions were confirmed as malignant by tru-cut needle biopsy.

Of 49 malignant lesions, 44 were confirmed by either resectionor biopsy. Three lesions ,5 mm and 1 lesion 6–10 mm in size,which appeared to be metastases by IOUS or CTAP, could not bebiopsied at the operation. Follow-up revealed progression in allcases, so these lesions may be classified as malignant as well.

A total of 43 benign lesions were detected in 13 patients. Thesewere 34 cysts, 8 hemangiomas, and 1 focal fatty infiltration (con-firmed through biopsy). Helical CTAP combined with IV con-trast-enhanced helical CT yielded 9 false-positive lesions (3 cysts,3 hemangiomas, 1 focal fatty infiltration, and 2 unexplained le-sions). IOUS detected 1 false-positive lesion that turned out to bea fatty infiltration. Resectable lesions in 10 patients could becorrectly classified by all imaging modalities. In the other group(n 5 3) with irresectable metastases, helical CTAP missed 1 casewhereas IOUS predicted inoperability in all patients.

In the lesion-by-lesion analysis there was no statistically signif-icant difference between CTAP and IOUS for the whole range oflesion sizes. On the other hand, a statistically significant difference(p , 0.01) was noted between the detection rates of IOUS/CTAPand helical IV CT both for lesion sizes #10 mm. Finally, there wasno statistical difference between CTAP and helical IV CT forlesions measuring .10 mm in diameter. The smallest lesion de-tected was 3 mm (Table 1).

Table 1. Lesion-by-lesion analysis of intrahepatic metastasis in colorectal carcinoma by intraoperative sonography (IOUS), helical computedtomography (CT) with intravenous (IV) contrast enhancement, and helical CT with arterioportography (CTAP).

Lesion size (mm) No. of lesions

Lesions detectedHistology confirmed byresection or biopsyHelical IV CT Helical CTAP IOUS

#5 11 1* 10 11* 86–10 13 3** 13 13** 1211–20 12 10 12 11 1121–30 8 7 8 8 8.30 5 5 5 5 5Total 49 26 48 48 44

*,**p , 0.01 (statistically significant differences; IOUS detected all lesions #10 mm).

44 World J. Surg. Vol. 24, No. 1, January 2000

When sensitivity and specificity were calculated on a per-patientbasis (based on 13 patients with and 20 patients without metas-tases) including the 95% CI, there was no statistical differencenoted between helical CTAP combined with IV contrast-en-hanced helical CT and IOUS by chi-square test (Table 2).

There were no complications observed either in combinationwith the application of IV contrast or with arterial catheterization.While performing CT or CTAP, 1 radiologist and 1 radiologicassistant attended the patient. Helical CT with IV contrast en-hancement took about 20 min. If helical CTAP was planned, thepatient first had to be placed on an angiographic table for inser-tion of the arterial catheter in the superior mesenteric or splenicartery under radiologic guidance. After this procedure the patientwas unable to walk and had to be lifted over to the CT scanner.This required at least 3 persons. Finally, the arterial puncture sitehad to be kept under pressure for at least 15 min after extractionof the catheter in order not to provoke hematoma. This entiremaneuver required about 50 min and therefore must be consid-ered a time-consuming event. It is also worth mentioning that dueto the arterial puncture, consecutive bandages under pressure for6 hr together with absolute resting are necessary, so the patientwill not be available for orthograde colon lavage if the operationis set for the next day.

In the postoperative follow-up, 3 of 5 patients with irresectableliver metastases presented with progression and additional intra-hepatic lesions. The 10 resected patients did not present recurrentmetastases during the first 9 postoperative months. If unidentifiedmetastases were present at the time of operation they should havebecome detectable after this period. The remaining 20 patientswithout synchronous liver metastases at operation were checkedevery 3 months. Two patients developed solitary metastases 6 and7 months after resection of the primary tumor. Both had had nointraoperative evidence of small lesions either by palpation or byIOUS. CTAP and helical CT with contrast enhancement also hadpresented normal findings at primary staging. There was no con-trast-induced nephropathy noted in any patient.

Discussion

Low specificity and nearly ideal values for sensitivity of helicalCTAP are well-known facts [7, 8, 11, 12]. On the other hand,IOUS is said to significantly improve detection of metastases fromcolorectal carcinoma to the liver [9, 13–15]. Rafaelsen et al. [9]conducted a study comparing preoperative transabdominal versusintraabdominal sonography and noted that most of the trials

presented for IOUS were projected as a lesion-by-lesion and nota patient-by-patient analysis. Regarding the various results of therecently published data on this subject (n 5 414; Table 3), wefound that overall sensitivity was 93% and specificity was 64% forCTAP in diagnosing liver metastasis from colorectal carcinoma [8,16–21]. Reviewing the literature on IOUS (n 5 546; Table 4), wefound an overall sensitivity of 97% and specificity of 98% fordetection of colorectal hepatic metastases [9, 19, 22–24]. The aimof this study was to determine the accuracy of IOUS as well asCTAP and to compare these results with helical CT and contrastenhancement as an approved technique for preoperative stagingof colorectal cancer [22, 25].

Thus contrast-enhanced helical CT in preoperative staging rep-resents the basic technique for determination of local tumorspread and involvement of lymph nodes. Some but not all inop-erable local instances of hepatic metastases can be ruled out byhelical CT so that these patients should not be eligible for CTAP.Furthermore, specificity values for contrast-enhanced helical CTare proved to be markedly higher than for CTAP [25]. In ourstudy, only 1 lesion that could be described histologically as focalfatty infiltration was mistaken as metastasis by this technique.Regarding our results, we strongly believe that contrast-enhancedhelical CT is necessary prior to CTAP to properly interpret thefindings with this rather unspecific but highly sensitive modality. It

Table 2. Detectability of metastases: sensitivity and specificity calculatedon a per-patient basis (based on 13 patients with and 20 patients withoutmetastases), including 95% confidence interval (CI).

Sensitivity(%) 95% CI

Specificity(%) 95% CI

Helical IV CT 94 0.68; 1.0 92 0.75; 1.0Helical CTAP 1

helical IV CT93* 0.68; 1.0 75* 0.51; 0.91

IOUS 98* 0.68; 1.0 95* 0.68; 0.99

*No statistical difference between helical computed tomography witharterioportography (CTAP) combined with intravenous (IV) contrast-enhanced helical computed tomography (CT) and intraoperative sonog-raphy (IOUS) by the chi-square test.

Table 3. Helical computed tomography with portal-phase contrastenhancement (CTAP) in diagnosing liver metastasis from colorectalcarcinoma.

Reference (year) nSensitivity(%)

Specificity(%)

Histologyconfirmed

Our results (1998) 33 100 68 YesRichter et al. [18]

(1996)18 100 65 Yes

van Ooijen et al. [16](1996)

37 94 35 Yes

Moran et al. [19](1995)

48 95 / Yes

Soyer et al. [8](1994)

23 94 73 Yes

Vogel et al. [20](1994)

58 88 73 Yes

Small et al. [21](1993)

197 91 68 Yes

Total 414 93 64

Table 4. Intraoperative ultrasonography (IOUS) in diagnosing livermetastasis from colorectal carcinoma.

Reference (year) nSensitivity(%)

Specificity(%)

Histologyconfirmed

Our results (1998) 33 98 95 YesTakeuchi et al. [24]

(1996)119 100 98 Yes

Moran et al. [19](1995)

48 98 96 Yes

Rafaelsen et al. [9](1995)

295 97 98 No

Knol et al. [22](1993)

51 88 97 No

Total 546 97 98

Schmidt et al.: Diagnosing Colorectal Liver Metastases 45

also allows early selection of patients who are not eligible forCTAP.

Preoperative sonography was not included as part of this studyas several authors have already pointed out the accuracy of thistechnique, presenting sensitivity ranges of 65% and specificityvalues near 90% [9, 26]. In our study, we found a high prevalenceof cysts and hemangiomas, which lead to better determination ofspecificity for the performed imaging modalities. The fact offinding 43 benign hepatic lesions is not very common if we look ata normal population of patients who undergo postoperative fol-low-up after colorectal carcinoma. As mentioned, all patientswere referred to our institution because of sonographic evidenceof hepatic tumor in coincidence with colorectal carcinoma. Thisshould be the reason for the higher incidence of benign hepaticlesions noted in our selected population.

The hepatic Doppler perfusion index (DPI) is said to be moresensitive than IOUS in the early detection of occult colorectalliver metastases [26]. As a point of criticism, this technique wasnot used in our series. We assumed that along with no evidence ofliver metastases at the operation determined by IOUS as the mostsensitive technique and after ruling out small lesions in the outerlayers of the liver by palpation, we would have no tool in hand toprove malignancy if the DPI were abnormal.

As we did not include liver transplantation or autopsy as astandard of reference, the true number of all (including occult)metastases may not be determinable in this series. Therefore, thisstudy also has to face the criticism that liver resection was per-formed in only 10 of 33 patients and less than 10% of total livertissue was available for histology. We believe that the combinationof IOUS, intraoperative palpation, and inspection together withfollow-up studies can be used as a good standard of referencebecause the outer layer with 1 cm of thickness over the whole liverrepresents nearly 50% of the total hepatic mass [27, 28] and iseasily assessible for the surgeon. Furthermore, all deeper layersmay be visualized perfectly by IOUS [7] so that nearly all hepaticregions can be examined, excluding those localized in the liverdome when prior hepatic mobilization was not performed.

In the present series, a total of 24 metastases were #10 mm(49%). This may explain the low sensitivity value of contrast-enhanced helical CT. All lesions in this range were detected byIOUS and 1 was missed by CTAP (Table 1). There was nostatistical difference between IOUS and CTAP for all lesionsmeasuring ,10 mm. On the other hand, there also was no statis-tical difference among CTAP, IOUS, and contrast-enhanced he-lical CT for lesions .10 mm. Therefore, CTAP and IOUS areequal regarding accuracy in detecting liver metastasis from colo-rectal carcinoma.

Strotzer et al. [10] demonstrated that sensitivity of helicalCTAP did not differ from that of contrast-enhanced helical CTand superparamagnetic iron oxide (SPIO)-enhanced magneticresonance imaging (MRI), but was significantly higher regarding alesion-by-lesion analysis in their study. They concluded that heli-cal CTAP in combination with contrast-enhanced helical CTcould not be replaced by SPIO-enhanced MRI for detection ofhepatic metastasis from colorectal carcinoma [10]. SPIO-en-hanced MRI (AMI-25 5 Endorem, Laboratoire Guerbet, France)is said to improve detection of malignant hepatic lesions by ap-plication of a contrast agent based on SPIO particles [29, 30].

Total expenses for helical CTAP represent an increase of 50%compared with contrast-enhanced helical CT alone. As we believe

that helical CTAP of the liver cannot be interpreted properly inthe absence of a coexistent contrast-enhanced helical CT of theabdomen, costs for this investigation have to be added to theexpenses of helical CT alone so that total costs are doubled.Considering IOUS as a substitute for helical CTAP, however,presents some well-known insufficiencies. For all hepatic regionsto be visualized perfectly, it is necessary to remove adhesions andto mobilize the liver by cutting the triangular ligaments. Intraop-erative survey is not sufficient with IOUS, as only sequentialimaging of the liver is possible. Determination of tumor spreadand lymph node infiltration is also rarely possible. Finally, docu-mentation of IOUS is extremely dependent upon the intraopera-tive investigator. Therefore, reproduction of intrahepatic lesionsdoes not become feasible at a level of general consensus as ispossible with radiologic imaging modalities. In conclusion, IOUSmay not be used generally as the only staging modality in colo-rectal carcinoma (Table 2).

As soon as synchronous metastases are detected with contrast-enhanced helical CT, a helical CTAP should follow in order not tomiss limiting lesions ,10 mm and to avoid unnecessary hepaticresections. IOUS may be used alternatively in this special situa-tion. If metachronous liver metastases from colorectal carcinomaare present, preoperative helical CTAP is always advisable as liverresections can be planned or inoperable patients may be disclosedand provided with chemotherapy without prior (explorative) lap-arotomy. If cost efficiency is taken into consideration, contrast-enhanced helical CT scan of the entire abdomen together withintraoperative palpation and IOUS may represent the most favor-able staging combination in colorectal carcinoma.

Resume

Objectif: La tomodensitometrie (TDM) helicoıdale etl’echographie peroperatoire (EPO) sont extremement sensiblesdans la detection de metastases hepatiques dont le diametre nedepasse pas 2 cm. Comme la sensibilite et la specificite de cesdeux techniques varient dans la litterature et en raisond’insuffisamment d’information publiee sur le sujet, nous avonsestime qu’une analyse, lesion par lesion, etait necessaire. Laprecision et le cout-efficiacite de l’echographie peroperatoire ontete comparees a celles de la TDM helicoıdale avec rehaussementau temps portal (RTP) dans la detection preoperatoire demetastases hepatiques d’origine colorectale dans une etudeprospective «aveugle». Methodes: 33 patients ayant un cancercolorectal ont ete examines par TDM avec RTP et par EPO. Ona detecte des metastases dans 10 cas, les 23 patients restants ontete revus avec une TDM tous les trois mois pendant un an.Resultats: La TDM avec RTP et l’EPO ont pu detecter toutes leslesions (13 sur 13) mesurant entre 5 et 10 mm. L’EPO n’a echoueque dans la detection d’une seule metastase de plus de 10 mm. LaTDM avec RTP avait une sensibilite «ideale» de 100% mais saspecificite etait basse (68%). La sensibilite de l’EPO etait de 98%alors que la specificite etait de 95%. Discussion: Les valeursrespectives de la TDM avec RTP et de l’EPO sont similaires dansla detection de metastases de diametre inferieur a 10 mm. Lesdeux techniques peuvent etre utilisees si on envisage des resectionsynchrones ou metachrones afin de ne pas manquer de petiteslesions rendant la chirurgie superflue. La TDM avec RTPdynamique par voie intraveineuse est consideree comme la

46 World J. Surg. Vol. 24, No. 1, January 2000

methode la plus cout efficace dans le bilan preoperatoire mais lestaging preoperatoire local peut parfois etre insuffisant.

Resumen

Objetivo: Tanto la tomografıa axial computarizada helicoidal(CTAP) como la ultrasonografıa intraoperatoria (IOUS) sonextremadamente sensibles para la deteccion de metastasis hepaticasde diametro menor a 2 cm; sin embargo, como los valores desensibilidad y especificidad obtenidos con ambas tecnicas, difierenbastante en la escasa literatura al respecto, nos parecio necesarioefectuar un analisis considerando, una a una, cada lesion. Se efectuoun estudio prospectivo ciego para evaluar, preoperatoriamente, laexistencia de metastasis hepatica por carcinoma colo-rectal,mediante la ultrasonografıa intraoperatoria (IOUS) y la tomografıaaxial computarizada con contraste venoso portal (CTAP). Tambiense evaluo la relacion costo/eficacia. Metodos: En 33 pacientes concarcinoma colo-rectal se estudio el hıgado, tanto con la CTAP comocon la IOUS. En 10 casos se procedio a resecar las metastasis; en losrestantes 23 pacientes se efectuo un seguimiento con CT, cada 3meses, durante 1 ano. Resultados: La CTAP y la IOUS permitierondetectar las 13 lesiones metastasicas, cuyo tamano oscilo en 5 y 10mm (13/13). Una metastasis mayor de 10 mm no fue detectada porla IOUS. La CTAP presento una sensibilidad ideal del 100%, pero suespecificidad fue baja: 68%. La sensibilidad de la IOUS fue del 98%y su especificidad del 95%. Discusion: Tanto la IOUS como la CTAPtienen el mismo valor para el diagnostico de metastasis hepaticasmenores a 10 mm. Ambas tecnicas deben de utilizarse si se pretenderealizar una reseccion metastasica sincronica o metacronica, conobjeto, de que no solo ninguna pequena lesion pase desapercibidasino tambien, para evitar una cirugıa hepatica superflua. La CT scanhelicoidal con contraste dinamico intravenoso aumenta el valordiagnostico de la CT y ha de considerarse como el mejor metodo,tambien en relacion con el costo/eficacia, para la estadificacionpreoperatoria, aunque no pueda llevarse a cabo una estadificacionlocal por una insuficiente vigilancia intraabdominal.

References

1. Greenway, B.: Hepatic metastases from colorectal cancer: resection ornot? Br. J. Surg. 75:513, 1988

2. McArdle, C.S., Hole, D., Hansell, D.: A prospective study of colorec-tal cancer in the West of Scotland: a ten year follow-up. Br. J. Surg.77:206, 1990

3. Finlay, I.G., McArdle, C.S.: Occult hepatic metastasis in colorectalcarcinoma. Br. J. Surg. 73:732, 1986

4. Nelson, R.C., Chezmar, J.L., Sugarbaker, P.H., Bernardino, M.E.:Hepatic tumors: comparison CT during arterial portography, delayedCT and MR imaging for preoperative evaluation. Radiology 172:27,1989

5. Kuszyk, B.S., Bluemke, D.A., Urban, B.A.: Portal-phase contrast-enhanced helical CT for detection of malignant hepatic tumors: sen-sitivity based on comparison with intraoperative and pathologic find-ings. Am. J. Radiol. 166:91, 1996

6. Heiken, J.P., Weyman, P.J., Lee, J.K.: Detection of focal hepaticmasses: prospective evaluation with CT, delayed CT, CT during arte-rial portography and MRI imaging. Radiology 171:47, 1989

7. Soyer, P., Levesque, M., Elias, D., Zeitoun, G., Roche, A.: Detectionof liver metastases from colorectal cancer: comparison of intraoper-ative US and CT during arterial portography. Radiology 183:541, 1992

8. Soyer, P., Bluemke, D.A., Hruban, R.H., Sitzmann, J.V., Fishman,E.K.: Hepatic metastases from colorectal cancer: detection and false-

positive findings with helical CT during arterial portography. Radiol-ogy 193:71, 1994

9. Rafaelsen, S.R., Kronborg, O., Larsen, C., Fenger, C.: Intraoperativeultrasonography in detection of hepatic metastases from colorectalcancer. Dis. Colon Rectum 38:355, 1995

10. Strotzer, M., Gmeinwieser, J., Schmidt, J., Fellner, C., Seitz, J., Al-brich, H., Zirngibl, H., Feuerbach, S.: Diagnosis of liver metastasesfrom colorectal adenocarcinoma: comparison of intravenous contrast-enhanced helical CT, helical CTAP, plain MRI and SPIO-enhancedMRI. Acta Radiol. 38:986, 1997

11. Ward, B.A., Miller, D.L., Franck, J.A.: Imaging of surgically relevanthepatic vascular and segmental anatomy. II. Extent and resectabilityof hepatic neoplasms. Am. J. Radiol. 149:180, 1987

12. Miller, D.L., Simmons, J.T., Chang, R.: Hepatic metastasis detection:comparison of three contrast enhancement methods. Radiology 165:785, 1987

13. Olsen, A.K.: Intraoperative ultrasonography and the detection of livermetastasis in patients with colorectal cancer. Br. J. Surg. 70:998, 1990

14. Charnley, R.M., Morris, D.L., Dennison, A.R., Hardcastle, J.D.: De-tection of colorectal liver metastases using intraoperative ultrasonog-raphy. Br. J. Surg. 78:45, 1991

15. Machi, J., Isomoto, H., Kurohiji, T.: Accuracy of intraoperative ultra-sonography in diagnosing liver metastases from colorectal cancer.World J. Surg. 15:551, 1991

16. Van Ooijen, B., Oudkerk, M., Schmitz, P.I.M., Wiggers, T.: Detectionof liver metastases from colorectal carcinoma: is there a place forroutine computed tomography arteriography? Surgery 119:511, 1996

17. Oudkerk, M., van Ooijen, B., Mali, S.P., Tjiam, S.L., Schmitz, P.I.,Wiggers, T.: Liver metastases from colorectal carcinoma: detectionwith continuous CT angiography. Radiology 185:157, 1992

18. Richter, G.M., Theobald, I., Roeren, T., Wunsch, C., Lehnert, T.,Kauffmann, G.W.: Spiral CT portography in preoperative diagnosis ofliver metastasis. Chirurg 67:630, 1996

19. Moran, B.J., O’Rourke, N., Plant, G.R., Rees, M.: Computed tomo-graphic portography in preoperative imaging of hepatic neoplasms.Br. J. Surg. 82:669, 1995

20. Vogel, S.B., Drane, W.E., Ros, P.R., Kerns, S.R., Bland, K.I.: Predic-tion of surgical resectability in patients with hepatic colorectal metas-tases. Ann. Surg. 219:508, 1994

21. Small, W.C., Mehard, W.B., Langmo, L.S., Dagher, A.P., Fishman,E.K., Heiken, J.P., Bernardino, M.E.: Preoperative determination ofthe resectability of hepatic tumors: efficacy of CT during arterialportography. Am. J. Radiol. 161:319, 1993

22. Knol, J.A., Marn, C.S., Francis, I.R., Rubin, J.M., Bromberg, J.,Chang, A.E.: Comparisons of dynamic infusions and delayed com-puted tomography, intraoperative ultrasound and palpation in thediagnosis of liver metastasis. Am. J. Surg. 165:81, 1993

23. Vitola, J.V., Delbeke, D., Sandler, M.P., Campbell, M.G.: Positronemission tomography to stage suspected metastatic colorectal carci-noma to the liver. Am. J. Surg. 171:23, 1996

24. Takeuchi, N., Ramirez, J.M., Mortensen, N.J., Cobb, R., Whittle-stone, T.: Intraoperative ultrasonography in the diagnosis of hepaticmetastases during surgery for colorectal cancer. Int. J. Colorectal Dis.11:92, 1996

25. Vassiliades, V.G., Foley, W.D., Alarcon, J.: Hepatic metastases: CTversus MR imaging at 1.5 T. Gastrointest. Radiol. 16:159, 1991

26. Leen, E., Angerson, W.J., Wotherspoon, H.W., Moule, B., Cooke,T.G., McArdle, C.S.: Comparison of the Doppler perfusion index andintraoperative ultrasonography in diagnosing colorectal liver metasta-ses. Ann. Surg. 220:663, 1994

27. Schultz, W., Hort, W.: The distribution of metastasis in the liver. Aquantitative post-mortem study. Virchows Arch. 394:89, 1981

28. Berry, C.L.: Liver lesions in an autopsy population. Hum. Toxicol.6:209, 1987

29. Grangier, C., Tourniaire, J., Mentha, G.: Enhancement of liver hem-angiomas on T1-weighted MR SE images by superparamagnetic ironoxide particles. J. Comput. Assist. Tomogr. 18:888, 1994

30. Vogl, T.J., Hammerstingl, R., Schwarz, W.: Superparamagnetic ironoxide-enhanced versus gadolinium-enhanced MR imaging for differ-ential diagnosis of focal liver lesions. Radiology 198:881, 1996

Schmidt et al.: Diagnosing Colorectal Liver Metastases 47

Invited Commentary

Shin Takeda, M.D.

Department of Surgery II, Nagoya University School of Medicine,Nagoya, Japan

This study is a prospective comparison of intraoperative ultra-sonography (IOUS), intravenous (IV) contrast-enhanced helicalcomputed tomography (CT), and helical CT with arterioportog-raphy (CTAP) in the preoperative detection of liver metastasesfrom colorectal carcinoma. So far, there are few sufficient dataavailable regarding a “lesion-by-lesion analysis” in correlationwith the size of the liver metastases.

I have thought that the combination of IOUS and intraoperativepalpation could be a good diagnostic technique for detecting livermetastases from colorectal carcinoma, whereas helical CTAP is themost modern and promising method for detecting hepatic lesions.

The results of Schmidt and coworkers show that there was nostatistical difference among IOUS, helical CTAP, and helical CTfor lesions .10 mm. On the other hand, the sensitivity for detec-tion of liver metastases that were #10 mm was much lower for

helical CT than for IOUS or helical CTAP. The authors show thathelical CTAP and IOUS are indeed equal regarding high sensi-tivity for detecting liver metastases from colorectal carcinoma.However, helical CTAP is a complicated, time-consuming, andexpensive technique. Based on their results, the authors discussthe indication of helical CTAP for preoperative detection of livermetastases from colorectal carcinoma.

I agree with their discussion and results. If synchronous metas-tases are detected with helical CT or US, a helical CTAP isnecessary to check for other lesions ,10 mm, which might changethe type of procedure. In addition, if metachronous liver metas-tases from colorectal carcinoma are detected by examinationssuch as US, CT, and magnetic resonance imaging (MRI), a pre-operative helical CTAP should be recommended as the choice ofliver resection or chemotherapy without laparotomy. Of course,we should perform the intraoperative palpation and IOUS duringsurgery in order not to miss the smaller (,10 mm) liver metasta-ses from colorectal carcinoma.

As the pitfall of IOUS is well noted in this paper, the authorsshould explain why the specificity of helical CTAP is a little low intheir series, since we know the frequency of sensitivity and spec-ificity of helical CTAP in detection of liver lesions.

48 World J. Surg. Vol. 24, No. 1, January 2000