Eur Radio1 (2003) 13:M31-M41DOl 1O.1007/s00330-003-2129-8

© Springer-Verlag 2003

Pierre-Jean ValetteFrank PilleulArielle Crombe-Ternamian

MDCT of benign liver tumors and metastases

P.-J. Va1ette(~) . F. Pilleu1· A. Crombe-TernamianDepartment of Digestive Radiology,Pavillon H, Hopital Edouard Herriot,Place d' Arsonval, 69003 Lyon, Francee-mail: pierre-jean.va1ette@chu-1yon.frTel.: +33-47-2117540Fax: +33-47-2117541

Introduction

Multi-detector computed tomography (MDCT) theoreti­cally presents several advantages for liver imaging in­cluding optimal timing of tumor contrast enhancementand increased spatial resolution. Such advantages havebeen advocated to improve diagnosis of benign tumorsand detection of metastases. The results, however,should be carefully analyzed with reference to the vari­ous objectives of a liver CT. When performed to diag­nose a benign tumor, the role of CT is to demonstrate thenature of the liver mass. Highly specific and confidentdiagnosis with regard to the type of tumor is then expect­ed. In the case of extra-hepatic malignancy, the aim ofCT is to evidence, or even more importantly, to rule outliver metastases. High sensitivity and negative predictivevalue are needed. The MDCT also brings with it newchallenges concerning the acquisition and contrast-injec­tion protocols that should be adapted to the clinical situa­tion and type of lesion expected. A clear understandingof all these clinical data and technical parameters is nec­essary to state what might be the real advances of MDCTfor liver tumors exploration and how this technologymay modify the diagnostic strategies.

Technique

Detection of lesions in the liver is determined by cons­picuity which relates to the degree of liver-to-tumor con-

trast. This contrast is typically positive in cases of hyper­vascular lesion or negative in cases of hypovascularlesion. Some degree of characterization may also beobtained by analyzing the type of tumor enhancement incases of hypervascular tumor. Since the tumoral hypervas­cularity is related mainly to the arterial supply, a very sharptiming of acquisition is needed after contrast injection, tooptimize both, tumor conspicuity and characterization.

This timing of acquisition is described in severalphases [1, 2]. At 20 s, there is relatively little enhance­ment of the liver parenchyma and all types of tumors.!his very early phase, namely the "early arterial phase,"IS used only to determine the hepatic arterial anatomybefore hepatic surgery and has little interest in terms oftumor detection or characterization. At 30-35 s, suffi­cient time has elapsed for the tumoral vasculature to en­hance the hypervascular lesions. Liver enhancement,which mainly results from later portal supply, is still lim­ited at this point, and hypervascular tumors are moreconspicuous and typically appear hyperdense. This peri­od is named the "late arterial phase." After 1 min, thedegree of enhancement of the liver and hypervascular le­sions becomes similar and the lesions conspicuity de­c~e~ses, whereas hypovascular lesions become clearlyvisible as hypodense masses inside the liver. This periodis termed the "portal venous phase." Late phases, afterseveral minutes, may also be of interest to demonstratelate tumoral enhancement as observed in hemangiomasand fibrotic lesions.

One of the advantages of MDCT is to provide fasteracquisitions compared with single-slice helical CT. Withrespect to the multiphase liver-to-tumor-contrast uptakedescription, MDCT, which allows a true late-arterial­phase imaging of the entire liver, should improve hyper­vascular lesion exploration (Fig. 1). Imaging of hypovas­cular lesions (Fig. 2) should take less advantage of thistechnology except for the fact that thinner slices may beobtained with an increased spatial resolution and theoret­ically, produce better results in detection of small nod-

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Table 1 Scan protocols for liver imaging

MDCT diagnosis of benign liver tumors

Benign tumors are often discovered in patients free ofsymptoms while undergoing imaging examinations forunrelated reasons. Hemangioma is the most frequent ofthese tumors with a prevalence ranging from 2 to 20% inthe general population. Focal nodular hyperplasia is thesecond most frequent benign tumor, far behind hemangi­oma. Liver adenoma is extremely rare compared with thepreviously mentioned tumors. The classical issue of im­aging is to characterize these liver lesions as benign andto rule out malignant tumors. A more practical approachis to demonstrate with full specificity the nature of thelesions, which deserve conservative management, in or­der to avoid unnecessary surgery. From this point ofview, the imaging strategy may be simplified by obtain­ing an unequivocal diagnosis of hemangioma or focal

4 slice

1201160/0.5s2.5mm

12.5 mm5mm3mm2 ml!kg4 mlls

Arterial phase 35 sPortal phase 55 s

KVlEffective mAslRotation time (s)Detector Collimation (mm)FeedIRotation (mm)Slice thickness (mm)IncrementIV Contrast Volume (400 mgUmg)/salineInjection RateScan Delay (s)

they are larger or equal to collimation. Finally, the userchoice may be resumed to the initial collimation thick­ness and to one or more sets of effective reconstructionwidths that suit the clinical situation. This choice is acompromise between spatial resolution, which is im­proved with thin sections, and image noise which growsdisproportionately when section width is forced to beidentical to collimation width. The last parameter to bechosen by the user, independently from the others, isslice overlapping which is needed when multiplanar re­construction is performed.

In clinical practice, a typical MDCT protocol for hy­pervascular tumors (including benign tumors and hyper­vascular metastases) is a dual-phase acquisition at 5-mmsection thickness, after contrast bolus injection at 4 mllsdelivery rate for total volume of 1.7-2 mllkg (Table 1).Synchronization with the late arterial phase is obtainedby setting a 35-s delay, or even better, with the use a bo­lus-triggering system. Portal phase is obtained, after 60-sdelay, with the same scanning parameters. An additionallate phase may be performed after 3 min, if needed(hemangiomas). For hypovascular metastases, similarparameters can be chosen, except that a single acquisi­tion, after 60-s delay, is often sufficient.

Fig. 1 Enhancement profile of liver hypervascular tumor, focalnodular hyperplasia (FNH)

Fig. 2 Enhancement profile of liver hypovascular tumor (livermetastases)

ules. A number of studies [3, 4, 5, 6] have now clearlydemonstrated how the injection parameters may influ­ence the liver and tumor enhancement in terms of quanti­ty, delivery rate, and type of contrast. The best visualiza­tion of hypervascular tumors is obtained at the arterialphase with the use of high-concentration contrast mediaand increased delivery rate. Enhancement during the por­tal phase is dependent mostly on the total dose of iodineadministered.

The other advantage of MDCT is the potential to re­duce the effective section width without excessive scanduration or limited length [7]. Section width is the finalreconstruction result of multiple acquisition parametersincluding, collimation, table feed per rotation, and pitch.The available choices of section thickness are dependenton the manufacturer and the type of multislice raw-datainterpolation and reconstruction. Multiple data sets, withvarying section width, may also be reconstructed fromthe same raw data, with the only precondition being that

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Fig. 3 Typical hemangioma at CT: globular enhancement similarto blood attenuation, at rapid CT with bolus administration of con­trast material, and late persistent opacification

nodular hyperplasia, when possible. Such strategy re­solves over 90% of cases of benign liver tumors. It ne­glects the difficult problem of adenomas, but this is oflittle consequence considering the rarity of these tumors.Moreover, adenomas must theoretically be surgically re­moved because of a potential risk of rupture and of thepossible confusion or association with a hepatocellularcarcinoma, which can only be ruled out after the system­atic screening of the entire lesion at pathology.

Hemangiomas

Most cavernous hemangiomas are easily diagnosed dueto characteristic features, such as near isoattenuationwith blood on nonenhanced images, globular or nodularperipheral enhancement similar to blood attenuation atrapid CT with bolus administration of contrast material,and late persistent opacification (Fig. 3). This typicalpresentation has been described for many years with theuse of monodetector CT, and the multidetector technolo­gy does not appear to be able to provide further diagnos­tic information in such cases. The presence of atypicalfeatures may, however, lead to misdiagnosis and confu­sion with other lesions [8]. Large heterogeneous heman­giomas with incomplete late filling, hyalinized heman­giomas with lack of peripheral enhancement, cystic hem­angiomas, and hemangiomas with adjacent arterioportalshunts all result in atypical enhancement at CT. Sincemost of these atypical presentations are not related toany type of feature that could be more accurately ex­plored at the arterial phase, there is little chance thatMDCT may improve the diagnosis in these cases. More­over, MR imaging has been shown to have global sensi-

tivity and specificity of >90% due to a relatively strongT2 hyperintensity, and is able to diagnose most caseswithout the need for a CT study (Fig. 4).

The interest in the multiphase CT technique has, how­ever, been specifically studied for the diagnosis of smallhemangiomas, which are difficult to characterize due tohomogeneous rapid filling at the arterial phase (Figs. 5,6), instead of early globular enhancement with late opa­cification. Kim et al. [9] reviewed 37 small hemangio­mas and 49 malignant tumors in 86 patients in order toassess the accuracy of three-phase helical CT for differ­entiating small hemangiomas from small hypervascularmalignant tumors. Kim et al. [9] confirmed that smallhemangiomas frequently show atypical appearance atCT. They also showed that multiphase CT does not im­prove the sensivity but does improve the specificity ofthe diagnosis of hemangioma up to 95% when isoattenu­ation to the blood pool at the combined, nonenhanced,arterial and portal phases is observed.

Focal nodular hyperplasia

Although focal nodular hyperplasias (FNH) are rare tu­mors, improvements in modern cross-sectional imaginghave made diagnosis of these lesions more frequent. TheFNHs are probably caused by a hyperplastic response tolocalized vascular abnormality and are made of normalhepatocytes; therefore, needle biopsies are likely to benondiagnostic and specific diagnosis is based primarilyon imaging methods.

The CT characteristics of FNH have been describedin multiple publications [10, 11]. The FNH is usually ho­mogeneous and isoattenuating to normal liver beforecontrast injection. At late arterial phase, FNH typicallypresents with a bright homogeneous enhancement and ahypodense central scar (Fig. 7). Infrequent, but also quitecharacteristic, are the radiating hypodense fibrous bands,

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Fig. 5 Atypical rapid fillingsmall hemangioma at CT: dif­ferential diagnosis with hyper­vascular tumor cannot be as­sessed

Fig. 4a, b Typical hemangioma at MR (same patient as in Fig. 3):enhancement pattern after gadolinium injection is similar to CT,and typical marked T2 hyperintensity is observed

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Fig. 6 Atypical rapid filling small hemangioma at MR (same patient as in Fig. 5): diagnosis of hemangioma can be assessed because ofcharacteristic T2 hyperintensity

Fig. 7 Typical FNH at CT. At late arterial phase, typical brighthomogeneous enhancement and hypodense central scar containingfeeding arteries. At portal phase, isoattenuation to the normal liverand hypodense central scar. At delayed phase hyperdensity of thecentral scar. Draining peripheral veins are also visible

or septas, arising from the scar. At portal phase, FNH re­turns to isoattenuation to the normal liver and may bedifficult to detect. Delayed phase often shows hyperden­sity of the central scar and septas due to the late opacifi­cation of the fibrotic content of these structures. Dilatedfeeding arteries penetrating the central scar, and drainingveins running at the surface of the lesion, may be recog­nized in large FNH. Additional common features of FNHare homogeneous pattern except for the scar area, well­defined margins without capsule , and lobulated contours.

When all these features are present, the diagnosis ofFNH may be considered as specific. Since early hyper­density of the tumor is the most reliable sign, MDCT,which allows the rapid scanning of the entire liver at thelate arterial phase, should facilitate the characterization

of FNH, particularly when multiple lesions at differentlocation levels are present; however, MR is now consid­ered as the imaging technique of choice in the case ofFNH. Before contrast medium injection, MR shows typi­cal nearly isointensity of the tumor mass to normal liverand hyperintensity of the central scar on T2-weightedimages (Fig. 8). After gadolinium injection, MR demon­strates the same characteristics as CT, without the risk oflarge quantities of iodine contrast-agent injection and ir­radiation.

Atypical FNH represents almost 50% of cases. TheseFNH induce two types of situations: firstly, lesionswhich have all FNH characteri stics except for the centralscar. Such presentation is usual with small FNH. It mayalso be observed in large FNH, when the scar is verythin, located near the surface of the tumor, or missing.Confident differential diagnosis with any type of hyper­vascular tumor, including adenomas and hepatocellularcarcinomas, is then more difficult to assess, but the diag­nosis of FNH still can be considered. Final diagnosis re­lies on MR, which sometimes is able to display a thin

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Fig. 8 Typical FNH at MR.Homogeneous isoattenuatingliver mass on TI and T2 se­quences. Central scar is hypo­intense on TI sequence andhyperintense on T2 sequence.Bright homogeneous tumor hy­perintensity at arterial-phase T1sequence, whereas at late portalphase the tumor returns to iso­intensity and the central scarbecomes hyperintense

Fig. 9 Atypical FNH at CT. Hypervascular tumor at late arterialphase with pseudocapule and missing clear picture of central scar.In addition, a peritumoral abnormal arterial liver perfusion is visi­ble. Tumor is not any more visible at portal phase

scar that is not detectable on CT. The MR is also moreaccurate than CT in demonstrating the homogeneity andliver isointensity of the lesion on all sequences (Figs. 9,10). Ba-Ssalamah et al. [12] also advocated the use ofliver-specific MR contrast agents. These agents result inhomogeneous contrast uptake with better delineation ofcentral scar which may help to make confident diagno­sis. Finally, some additional arguments may be obtained,

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Fig. 10 Atypical FNH at MR (same patient as in Fig. 9). Tl with­out contrast and TI-weighted images show an almost isointensenormal liver tumor. Diagnosis likely corresponds to FNH, al­though the central still remains undetectable. Final proof will beobtained at percutaneous biopsy

if needed, from large-needle percutaneous biopsies of thelesion and the adjacent liver. The histopathology of thesesamplings remains quite challenging but has been dem­onstrated to be of some value when performed into le­sions with non-specific , but FNH-compatible, radiologi­cal features [13]. Such strategy results in a final and con­fident diagnosis in over 90% of cases in which surgerycan be avoided.

In the second type of presentation, FNH has atypicalfeatures that should preclude the diagnosis. It may be apseudocapsule or an inhomogeneous content due to focaltelangectasic areas, fat deposits, or necrosis. Differentialdiagnosis is, therefore, almost impossible to obtain onimaging techniques and resection surgery must be per­formed.

Liver adenomas

As FNH, adenomas typically present hyperdensity on en­hanced scans at the late arterial phase. Ruppert-Kohl­mayr et al. [14] have tried to evidence some differencesin the tumor attenuation, after contrast injection, on tri­ple-phase CT to differenciate adenomas from FNH. Rel­ative enhancement is significantly higher in 100% oflarge FNH and lower in 87% of large adenomas at the ar­terial phase. These results induce a promising, global ac­curacy of approximately 96%; however, they are of lim­ited interest in clinical practice since they are not appli­cable to small tumors. Moreover, most large adenomasalso show a fibrotic capsule, subcapsular feeding arte­ries, or necrotic or fatty areas, which are even better

signs against the diagnosis of FNH (Figs. 11, 12). Anoth­er question is the differential diagnosis between adeno­mas and hepatocellular carcinomas developed on healthyliver. Both tumors may be very similar on imaging tech­niques and the final diagnosis of adenoma should beconsidered as almost impossible. This is the reason that adiagnosis of adenoma always induces a resection sur­gery.

Diagnosis of benign liver tumors in clinical practice

In clinical practice, with the sole objective of identifyinglesions that should not be resected, the diagnostics of be­nign liver tumor may be resumed for confident charac­terization of hemangiomas and FNH. This can beachieved with MDCT, but also with MR which demon­strates similar semiology after gadolinium and has theadvantage of providing additional information on the tu­mor content with the use of T I and T2 non-enhanced se­quences; therefore, although MDCT certainly has im­proved the conditions of CT examination of liver benigntumors with the use of multiphase acquisitions, it re­mains less appropriate than MR when a benign liver le­sion is suspected.

MDCT diagnosis of liver metastases

The diagnosis of liver metastases is often crucial for theinitial therapeutic management and follow-up of patientswith a malignant tumor. The CT is often used as ascreening method when a malignant tumor is discoveredto rule out metastases that may modify the treatmentplanning. Once liver metastases have been evidenced,CT provides information on size, number, and localiza­tion of the lesions that determine the feasibility of resec­tion or percutaneous radio-frequency treatment. When

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Fig. 11 Liver adenoma at CT. Moderately hypervascular tumor with inhomogeneous content both at late arterial and portal phase. Afalse image of central scar is visible

Fig. 12 Liver adenoma at MR (same patient as in Fig. 11). T2­weighted image shows an inhomogeneous tumor with hyperdenseareas that preclude the diagnosis of FNH. Gadolinium injection re­veals slight opacification at arterial phase

liver metastases are treated by chemotherapy, the treat­ment protocol is adapted to the response as estimated onthe tumor size measurements on CT images. Accordingto these multiple clinical situations, an efficient imagingmodality would be one which provides a high negative

Fig. 13 Small colon metastasi snot visualized a at 8-mm scanwidth and clearly evidenced atb 5-mm scan width (arrow)

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predictive value to rule out metastatic disease in patientsapparently free of liver lesions, a high sensitivity to de­tect small metastases distant to ones that could be resect­ed, and a minimally invasiveness since imaging tech­niques will have to be repeated several times during thecourse of the disease [15].

Hypervascular metastases come from thyroid, pancre­atic islet-cell tumors, carcinoid tumors, renal cell carci­noma, and variable breast tumors and melanoma. As forbenign liver tumors and hepatocellular carcinoma, tumordetection should be better at the late arterial phase whenthe lesions are hyperdense compared with adjacent liver.The MDCT has not yet been evaluated in such indica­tions, but some studies [16] have shown that late arterialphase provides added value in evaluating carcinoid livermetastasis .

Most liver metastases are hypovascular. The primarytumors which lead to hypovascular metastases includethose of the colon and rectum (most frequent), pancreas,lung, urothelium, prostate, and gynecological malignan­cies, except choriocarcinoma. At CT, these metastasesare hypodense, both at arterial and portal phases. Theymay also present with a thin peripheral enhancement, ne­crotic areas, or calcifications depending on the type ofprimary tumor. The portal phase is the one most adaptedto lesion detection since it provides the best tumor-to-liv­er ratio once the liver has been enhanced by the portaliodine supply; therefore, the scan timing does not appearto be as crucial as it is for examinations of tumors requir­ing a specific arterial phase evaluation. Valls et al. [17]showed, with a series of 157 patients with 290 provencolorectal metastases, that single-detector helical CT hasan overall detection rate of 85% with 4% false positivesonly. In terms of enhancement management , the rapidscanning provided by MDCT does not appear to be ableto improve these results; however, it would seem logicalthat MDCT could improve small metastases detection bythe systematic use of thin slices and higher spatial reso­lution (Fig. 13). In the study by Valls et al. [17], all false­negative findings were for lesions <1 em in diameter.

Haider et al. [18] showed that thinner collimation signifi­cantly increases the number of small hypoattenuating le­sions detected in metastatic livers. For a total number of88 liver lesions 1.5 ern or smaller, the pooled sensitivityfor all lesions was statistically different at 5-mm collima­tion (66%) and 2.5-mm collimation (82%); however,Haider et al. [18] indicated that no significant differencewas noted between collimations when only the metastat­ic lesions were considered (sensitivity of 80% at all col­limations).

Such results induce two different comments; the firstone is that, with similar injection parameters and scantiming, thin collimation does not improve the small me­tastases detection rate. Several explanations may be ad­vocated, including increased image noise and absence ofimproved tumor conspicuity. The well-demonstratedhigh sensitivity of CT arterial portography [19] indicatesthat the contrast material dose is probably the most sig­nificant factor of small-tumor conspicuity. The secondcomment raises the problem of small hypodense lesionsthat are better evidenced, but not related to the metastaticdisease. Jang et al. [20] specifically studied these lesionson single-phase helical CT. Among 1133 consecutive pa­tients with proven gastric or colorectal cancer, 268 pre­sented with 881 hypodense lesions 1.5 ern or smaller. Fi­nal diagnosis showed that 693 lesions (78%) in 248 pa­tients (92%) were benign, and 188 (21%) in 30 patients(11%) were metastases. As mentioned in the same paper[20], helical CT shows a prevalence of small hypodenselesions (25%) higher than that previously reported onconventional CT, whereas the proportion of malignancyis lower. These results confirm that the increase in num­ber of hypoattenuating lesions observed with recent CTtechniques is attributable mainly to improved visibilityof small benign tumors rather than better detection of ti­ny metastases. From a practical point of view, detectingmore metastases, but also more benign lesions that maybe confused with small metastases, would not be of greatclinical value unless differential diagnosis can be ob­tained. Most of these small benign tumors correspond to

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Fig. 14 Small liver hypoatten­uating lesion revealed in courseof a preoperative study for aleft lobe colon metastasis (notvisible here). Hyperintensityon T2-weighted MR sequencereveals the cystic nature of thelesion (proven to be a biliaryhamartoma at surgery; arrows)

cystic lesions, including biliary hamartomas, and focalfatty sparing. For Jag et al. [20], differential diagnosiswith true metastases, based on water attenuation andsharp margins in case of liver cysts, angular margins, andtypical location in case of fatty infiltration, is possiblewith careful analysis of CT findings; however, the num­ber of misclassified lesions did not decrease at thinnercollimation in the series of Haider et al. [18].

All these limitations bring into question the benefit ofcollimation of <5 mm for diagnosis of small metastases.A possible outcome would be the association of thin-col­limation MDCT for lesion detection, and thereafter, MRfor characterization of small undetermined lesions, sincethis technique is probably of greater value in demonstrat­ing small cysts on T2 sequences (Fig. 14) and focal fattyinfiltration on in/out-of-phase Tl sequences.

References

Conclusion

Multi-detector computed tomography reduces acquisi­tion times allowing reasonable breath-hold lengths andbetter synchronization of scanning with liver opacifica­tion phases, and allows systematic use of 5-mm sectionthickness, inducing better spatial resolution. At least forthese reasons, MDCT has definitely improved CT imagequality and reproducibility in clinical practice. Publisheddata, however, have not yet demonstrated statistical im­provements in the diagnosis of benign liver tumors andmetastases. Therefore, no significant changes in the di­agnostic strategies can be advanced at the present time.The MR still remains the gold standard examinationwhen a benign tumor is suspected. There is little chancethat, whatever the future technical refinements are,MDCT will change this fact. The CT remains a majortechnique for detection of metastases. Further studies areneeded to determine if collimation <5 mm associatedwith high-concentration media, postcontrast saline bolus,or any other innovative form of contrast administrationmay be of any interest to improve liver metastases detec­tion.

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