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Liver Metastases from Melanoma: Detection with Multiphasic Contrast-enhanced CT¹

¹ From the Departments of Radiology (S.P.B., K.W., V.R.) and Medicine (M.B.A.) and the Cutaneous Oncology Program (S.P.B., M.B.A.), Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Ave, Boston, MA 02215. From the 1998 RSNA scientific assembly. Received September 11, 1998; revision requested October 15; revision received December 18; accepted April 30, 1999. Address reprint requests to V.R. (e-mail: vraptopo @caregroup.harvard.edu).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To assess the clinical utility of multiphasic computed tomography (CT) of the liver in patients with metastatic melanoma.

MATERIALS AND METHODS: Nonenhanced and biphasic hepatic CT examinations were performed in 28 patients with metastatic melanoma, and liver lesion conspicuity was graded. CT studies in 20 patients met the eligibility criteria, and 13 patients had liver lesions.

RESULTS: A total of 57 liver lesions were seen on CT studies: 48 on hepatic arterial phase images, 49 on portal venous phase phase images, and 30 on delayed phase images. Of eight lesions overlooked on portal venous phase images, six were seen on nonenhanced images, and six were seen on arterial phase images. Twenty-eight lesions were graded as more conspicuous on portal venous phase images; 10 were graded as more conspicuous on arterial phase images.

CONCLUSION: CT images obtained only during the portal venous phase would have resulted in eight (14%) overlooked lesions, which implies that more than one phase is needed for hepatic CT in patients with malignant melanoma. The combination of nonenhanced and portal venous phase CT was as effective as the combination of arterial and portal venous phase CT in these patients. Delayed phase CT did not improve lesion detection either alone or in combination with CT at other phases.

Index terms: Computed tomography, technology, 761.1211 • Liver neoplasms, CT, 761.12111, 761.12112, 761.12114, 761.12115 • Liver neoplasms, secondary, 761.332 • Melanoma

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Malignant melanoma is an aggressive cancer in which systemic metastases frequently occur. The liver is a common site of metastases, and liver involvement has been associated with a particularly poor prognosis. Recent expansion of therapeutic options for metastatic melanoma has led to increased interest in accurate detection and quantification of disease burden for prognosis, clinical trial stratification, and monitoring of therapy (1).

Because metastases from melanoma are considered to be hypervascular, many institutions empirically perform multiphasic computed tomography (CT) through the liver, including CT during the hepatic arterial phase, when obtaining studies with intravenously administered contrast material enhancement (2–4). This results in added cost, time, radiation dose, and risks to the patient. Frederick et al (5) and Oliver et al (6) concluded that not enough added information was obtained to justify the routine use of hepatic arterial phase CT in cases of metastatic breast carcinoma and other hypervascular metastases to the liver; however, to our knowledge, the added value of the technique in cases of metastatic melanoma has not been specifically addressed, to date.

The purpose of this study was to evaluate whether more lesions can be detected by performing multiphasic liver CT in cases of melanoma and, if so, whether enough additional information would be obtained to justify routine use of a multiphasic technique. A secondary aim was to determine an appropriate phase or combination of phases that would be the most effective for CT examination for hepatic involvement by malignant melanoma.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
During 3 months, all patients with histologically proved metastatic melanoma who were referred for body or abdominal CT underwent nonenhanced CT followed by triphasic contrast-enhanced CT of the liver. Patients with melanoma were excluded from this study if they were unable to receive contrast material due to hypersensitivity. Other exclusion criteria were technical failures that resulted in acquisition of an inadequate biphasic image and limitations with regard to venous access that prevented injection of contrast material at the standard rate for biphasic imaging. Of the original 28 patients, eight were excluded for these reasons. The 20 patients (14 men, six women) included in the study were aged 25–77 years (median age, 55 years).

All patients underwent helical scanning with one of two identical helical CT scanners (CT HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis). All patients received oral contrast material (2% barium sulfate suspension, READI-CAT; E-Z-Em, Westbury, NY) before the examination. Nonenhanced imaging was then performed through the liver at 120 kVp, with a section thickness of 7 mm and a pitch of 1. The field of view and the milliampere-second level were set according to each patient's body habitus and were kept at that setting for each phase of scanning. A 512 x 512 matrix was used for all studies.

The intravenous contrast material used was ioversol (Optiray 320 [320 mg of iodine per milliliter]; Mallinckrodt, St Louis, Mo). By using a mechanical power injector, 150 mL of ioversol was injected at a rate of 4 mL/sec (iodine dose, 48 g). Contrast-enhanced CT of the liver was then performed with 7-mm collimation and a pitch of 1 during the hepatic arterial phase (25 seconds after the start of injection), the portal venous phase (60 seconds after the start of injection), and a delayed phase (3–5 minutes after injection).

All studies were recorded with 20 images per sheet of 35 x 43-cm film. Standard window level and center settings were used (width, 200 HU; center, 40 HU for nonenhanced and 70 HU for enhanced images). The hard copies were reviewed by a panel of three radiologists (S.P.B., K.W., V.R.), with decisions made by consensus. A standard questionnaire was completed for each patient. The number of lesions seen at each phase and the size, shape, presence of enhancement, and nature of the margin of the lesions were noted on the questionnaire. A five-point scoring system was used to grade conspicuity for each lesion on images obtained at each phase: score of 1, not visible; score of 2, probably not visible; score of 3, possibly visible; score of 4, probably visible; score of 5, definitely visible. The same approach was used to grade discrimination of lesions from vessels on images from each phase, with a score of 1 for no discrimination to a score of 5 for excellent discrimination, and to subjectively grade which phase was considered to be most useful, with a score of 1 for not useful to a score of 5 for most useful.

The maximum number of lesions evaluated in each patient was limited to 10; this was to reduce the possibility of bias due to a small number of patients with a large number of lesions. One patient had more than 10 lesions (approximately 40 lesions), all showing the same enhancement characteristics. The count was limited by choosing three representative imaging levels that yielded a total of 10 lesions.

Lesions with CT characteristics of cyst or hemangioma were excluded by the panel. If the CT appearance was not specific for cyst (low attenuation, no enhancement) or hemangioma (peripheral nodular enhancement with centripetal filling on delayed images) and if there were no other confirmatory test results (eg, ultrasonographic findings for cysts or magnetic resonance imaging findings for cysts or hemangioma), then the lesion in question was included in the final analysis. Although all patients had proved recurrent or metastatic melanoma, histologic proof of metastases to the liver was available in only one patient. In the remaining patients, the diagnosis of liver metastases was inferred because the lesions were new (ie, were not seen on previous studies [10 patients]) or were present on initial staging images but had undergone interval growth (two patients).

The data on the questionnaires were collected and tabulated by using a commercially available spreadsheet program (EXCEL; Microsoft, Redmond, Wash), and statistical analyses were performed by using software (MINITAB; Minitab, State College, Pa). Contingency tables with the ² test and the statistic were used to assess agreement between groups. The Wilcoxon signed rank test and the Student t test were used to test for significant differences, with a threshold P value of .05.

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
No liver lesions were detected on images obtained during any phase in seven of 20 patients, and images in these patients were excluded from further analysis. Of the 13 patients in whom liver lesions were detected, eight were men and five were women (age range, 24–70 years; median age, 47 years). Time since diagnosis of melanoma was 1–16 years (median, 3 years). All patients had already undergone treatment for metastatic melanoma prior to the start of the study, including immunotherapy (n = 1) and combined biologic therapy and chemotherapy (n = 12).

The results are summarized in the Table. After review of images obtained at all phases (nonenhanced and hepatic arterial, portal venous, and delayed phases) and with a maximum of 10 lesions considered in any one patient, a total of 57 liver lesions were detected in 13 patients. Of these, 41 (sensitivity, 72%) were seen on nonenhanced images; 48 (sensitivity, 84%), on arterial phase images; 49 (sensitivity, 86%), on portal venous phase images; and 30 (sensitivity, 53%), on delayed phase images. There was no significant difference between the number of lesions seen on arterial phase images and the number seen on portal venous phase images.

In eight patients, the same number of lesions was seen on arterial and portal venous phase images. In three patients, more lesions were seen on arterial phase images. In two patients, more lesions were seen on portal venous phase images. None of these differences were significant. In three patients, more lesions were seen on nonenhanced images than on portal venous phase images; two of these were patients in whom more lesions were seen on arterial phase images than on portal venous phase images, and one patient had a solitary lesion not seen on images from any other phase.

There were no patients in whom a lack of arterial phase images would have changed the assessment of liver involvement or the overall staging of the disease or that would have resulted in a change in treatment.

Conspicuity of each lesion also was assessed for images from each phase by using the five-point scale described earlier. The median conspicuity of the lesions on arterial phase images was 3 (interquartile range, 2–5), and that on portal venous phase images was 4 (interquartile range, 2–5), with no significant difference. Ten lesions were more conspicuous on arterial phase images (Fig 1), and 28 were more conspicuous on portal venous phase images (Fig 2), with the majority of the differences being within one grade. Fifteen lesions showed a difference of more than one grade between phases; six were more conspicuous on arterial phase images, and nine were more conspicuous on portal venous phase images (not significant). The value of 0.16 (weighted , 0.4) showed moderate agreement between the two phases (P < .02).

View larger version (143K): [in this window] [in a new window]   Figure 1a. CT images (window center, 70 HU; width, 200 HU) in a 58-year-old man with metastatic melanoma. (a) CT image obtained through the liver during the phase of peak hepatic arterial enhancement shows three enhanced lesions (arrows). The lesions were not present on previous images and are therefore considered to be malignant. (b) CT image obtained at the same level as a during the phase of peak portal venous enhancement shows that the three lesions are less conspicuous but are still visible.

View larger version (159K): [in this window] [in a new window]   Figure 1b. CT images (window center, 70 HU; width, 200 HU) in a 58-year-old man with metastatic melanoma. (a) CT image obtained through the liver during the phase of peak hepatic arterial enhancement shows three enhanced lesions (arrows). The lesions were not present on previous images and are therefore considered to be malignant. (b) CT image obtained at the same level as a during the phase of peak portal venous enhancement shows that the three lesions are less conspicuous but are still visible.

View larger version (118K): [in this window] [in a new window]   Figure 2a. CT images (window center, 70 HU; width, 200 HU) in a 51-year-old man with widely metastatic malignant melanoma. (a, b) CT images were obtained through the level of the hepatic veins during the phases of (a) peak hepatic arterial and (b) peak portal venous enhancement. The true extent of disease is best appreciated in b, as indicated by the presence of multiple hypoattenuating nodules in the liver. (c, d) CT images were obtained just above the level of the porta hepatis during the phases of (c) peak hepatic arterial and (d) peak portal venous enhancement. Lesions are better demonstrated in d. Multiple splenic lesions (arrows) also are visible. This patient had multiple other sites of disease throughout the chest, abdomen, pelvis, and skeleton.

View larger version (120K): [in this window] [in a new window]   Figure 2b. CT images (window center, 70 HU; width, 200 HU) in a 51-year-old man with widely metastatic malignant melanoma. (a, b) CT images were obtained through the level of the hepatic veins during the phases of (a) peak hepatic arterial and (b) peak portal venous enhancement. The true extent of disease is best appreciated in b, as indicated by the presence of multiple hypoattenuating nodules in the liver. (c, d) CT images were obtained just above the level of the porta hepatis during the phases of (c) peak hepatic arterial and (d) peak portal venous enhancement. Lesions are better demonstrated in d. Multiple splenic lesions (arrows) also are visible. This patient had multiple other sites of disease throughout the chest, abdomen, pelvis, and skeleton.

View larger version (135K): [in this window] [in a new window]   Figure 2c. CT images (window center, 70 HU; width, 200 HU) in a 51-year-old man with widely metastatic malignant melanoma. (a, b) CT images were obtained through the level of the hepatic veins during the phases of (a) peak hepatic arterial and (b) peak portal venous enhancement. The true extent of disease is best appreciated in b, as indicated by the presence of multiple hypoattenuating nodules in the liver. (c, d) CT images were obtained just above the level of the porta hepatis during the phases of (c) peak hepatic arterial and (d) peak portal venous enhancement. Lesions are better demonstrated in d. Multiple splenic lesions (arrows) also are visible. This patient had multiple other sites of disease throughout the chest, abdomen, pelvis, and skeleton.

View larger version (135K): [in this window] [in a new window]   Figure 2d. CT images (window center, 70 HU; width, 200 HU) in a 51-year-old man with widely metastatic malignant melanoma. (a, b) CT images were obtained through the level of the hepatic veins during the phases of (a) peak hepatic arterial and (b) peak portal venous enhancement. The true extent of disease is best appreciated in b, as indicated by the presence of multiple hypoattenuating nodules in the liver. (c, d) CT images were obtained just above the level of the porta hepatis during the phases of (c) peak hepatic arterial and (d) peak portal venous enhancement. Lesions are better demonstrated in d. Multiple splenic lesions (arrows) also are visible. This patient had multiple other sites of disease throughout the chest, abdomen, pelvis, and skeleton.

Six lesions (in three patients) were seen on arterial phase images but not on portal venous phase images. Four of these were hyperattenuating as compared with liver parenchyma and were described in the preceding paragraph. The other two lesions were in one patient and were hypoattenuating on arterial phase images. In this patient, seven lesions were seen on arterial phase images, and five were seen on portal venous phase images; of note, there was a total of eight lesions in this patient, all depicted on the nonenhanced images.

We assessed discrimination of lesions from vessels on images from each phase, again by using a five-point scale. The median grade for discrimination of lesions from vessels on arterial phase images was 3.0 (95% CI = 3.0, 3.8), which was significantly different from the median score of 5.0 (95% CI = 4.6, 5.0) for portal venous phase images. (P = .002; Wilcoxon signed rank test).

Various combinations of phases were assessed: The best single phase was the portal venous phase, but with images from this phase alone, eight (14%) of 57 lesions would have been overlooked. The combination of nonenhanced and portal venous phase images depicted 55 (96%) lesions; the combination of arterial and portal venous phase images also depicted 55 (96%) lesions.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
In recent decades, the incidence of dermatologic malignancies of all types has been increasing at a dramatic rate. This is especially true of malignant melanoma, the most aggressive of the common skin malignancies: In 1997, there were approximately 40,000 new diagnoses of melanoma, with over 7,000 deaths due to the disease (7). These numbers may be an underestimation, for several reasons. In terms of the rate of increase in incidence, melanoma is the fastest increasing malignancy in men and the second fastest in women, after lung cancer. Estimates of the lifetime risk of melanoma for an individual born in 2000 are as high as one in 85 (1).

Malignant melanoma is a cancer of melanocytes, usually in the skin. Melanoma may be curable if the manifestation is early. It can be highly aggressive, however, with as many as 20% of patients developing metastases (1); if metastases occur, the resultant prognosis usually is poor, with a median survival of 6–9 months reported in most studies (7–9). Prognosis has been closely linked to the number of sites of metastases and to the presence of visceral involvement. Liver metastases, in particular, have been shown (8) to portend a grave prognosis, with a median survival of approximately 4 months.

In recent years, several treatment strategies have been developed that have shown promise in the treatment of metastatic melanoma (1). The use of immunotherapy, particularly interleukin 2, either alone or in combination with chemotherapy, has produced tumor response in as many as 60% of patients, with up to a 10% chance of complete response (ie, elimination of metastases) (9). As a result of the increased incidence of the disease and the increased number of therapeutic options, imaging is being performed at many institutions and with increasing frequency, with particular emphasis on CT.

Malignant melanoma is considered to be a hypervascular tumor that, when metastatic, commonly involves the liver (1,2–4,6). Because of this and because of the dual blood supply to the liver, clinicians at many institutions attempt to obtain images through the liver during multiple phases after contrast material injection (3,4,6) when evaluating for possible liver metastases from melanoma, whereas clinicians at other institutions routinely obtain portal venous phase images alone. Multiphasic CT is possible because of the development of modern helical CT scanners that use slip-ring technology, which allows faster acquisition times and, therefore, repeated scanning of the liver at different times after the contrast material injection.

Particular emphasis has been placed on the acquisition of images during the phase of peak hepatic arterial enhancement (hepatic arterial phase). Hepatic arterial phase imaging is performed with the more generally useful phase of peak portal venous enhancement (portal venous phase). Imaging of the rest of the abdomen, thorax, or pelvis is then performed as needed. This technique has been well described (3,4) and has been referred to as a biphasic or triphasic technique. In general a relatively large contrast medium dose is delivered at a high injection rate, and helical CT of the liver is performed 20–25 seconds after the start of injection, depending on the exact protocol used (4).

Experience with hepatic lesions such as hepatoma, carcinoid metastases, neuroendocrine tumor, and vascular sarcoma (3,4,10–12) has shown an increase in lesion detection with multiphasic CT, as compared with that achieved with portal venous phase CT alone. The utility of this technique for other tumors that are commonly thought of as hypervascular (eg, breast carcinoma, renal cell carcinoma, and melanoma) is less clear (5,6). It should be noted that the portal venous phase, per se, is usually considered to be the optimum phase for liver imaging, and it is the addition of the arterial phase that could potentially result in superior lesion detection (4–6). For malignant melanoma, the utility of arterial phase imaging of the liver is under debate, and this study was designed to evaluate its application.

There are several disadvantages to routine arterial phase CT, mostly due to issues related to increased time, radiation dose, the high rate of contrast material injection, and increased cost. Instead of acquisition of a single CT study of the liver, multiphasic CT involves acquisition of two or three helical series, with a proportional increase in radiation dose. This also results in x-ray tube heating effects that will increase tube wear, decrease tube life, and can limit image quality and detection of low-contrast lesions by reducing the available milliampere-second level. The extra scanning, as well as any delay to allow the tube to cool, results in increased time to obtain the entire study.

All patients in this study had metastatic or recurrent melanoma proved with biopsy results, although the sampled lesion was not always in the liver. In our study, the assumption was made that every lesion that was clearly not a cyst or hemangioma represented a metastasis, because histologic proof could not be obtained from every lesion. This assumption has been made in other studies (5,6). Of the 13 patients with liver lesions, 10 did not show these lesions on staging studies obtained earlier in the course of the disease; in two patients, the lesions were present on the initial staging images but showed interval growth; in one patient, liver metastases were confirmed with biopsy results.

As the results indicate, delayed phase images did not significantly contribute to lesion detection, although contributions to diagnostic confidence or lesion characterization were not evaluated in this study. Seven lesions (in five patients) were seen at one phase only; all were less than 2 cm in diameter, and all were in patients with multiple lesions, with the exception of one individual, described subsequently, who had a solitary lesion seen only on nonenhanced images.

In our study, eight (14%) lesions (in four patients) would have been overlooked if CT images had been obtained only during the portal venous phase and not during the arterial phase or without contrast enhancement. In three of these patients, other liver lesions were present. Therefore, there was no difference with regard to metastatic status, but modern therapeutic considerations may call for more accurate determination of lesion number and size than that which can be provided by portal venous phase CT alone.

In the comparison of the number of lesions detected with combined nonenhanced and portal venous phase CT with the number detected with combined arterial phase and portal venous phase CT, there was no significant difference, with 55 lesions (96%) identified in each case. The two lesions that would have been overlooked without the addition of arterial phase CT were in a patient with five liver lesions, and the failure to detect these two lesions would not have altered staging or management. Of the two lesions that would have been overlooked without the addition of nonenhanced images, one was the only liver lesion in that patient, and this could have affected treatment decisions.

The relatively high contrast material injection rate of 4 mL/sec that we used could be expected to result in potentially greater enhancement of lesions relative to liver parenchyma during the arterial phase, and the findings may not be applicable when slower rates of injection are used (13). In addition, the patients in our group who had liver lesions had undergone some form of treatment for melanoma that involved interleukin 2–based immunotherapy. It is possible that the treatments administered could modify the enhancement characteristics of the tumor; therefore, any conclusions from this study may not apply in untreated patients or those who have not undergone immunotherapy.

With respect to follow-up hepatic CT in patients with malignant melanoma, we found that most liver lesions do not become hyperattenuating during arterial phase CT of the liver. We suggest, however, that liver CT be performed at more than one phase, because portal venous phase CT alone resulted in the failure to detect 14% of lesions. The combination of nonenhanced and portal venous phase CT in the patients in our study demonstrated as many lesions as the combination of hepatic arterial phase and portal venous phase CT and would have prevented the problems associated with routine hepatic arterial phase CT.

	Acknowledgments

 
The authors are grateful to Hugh Wheeler, PhD, for his contribution to the statistical analysis of the data in this manuscript.

	Footnotes

 
Author contributions: Guarantor of integrity of entire study, V.R.; study concepts and design, S.P.B., K.W., V.R.; definition of intellectual content, S.P.B., V.R.; literature research, S.P.B., K.W.; clinical studies, S.P.B., K.W.; data acquisition, S.P.B., K.W.; data analysis, S.P.B., K.W., V.R.; statistical analysis, S.P.B., V.R.; manuscript preparation, S.P.B.; manuscript editing and review, all authors.

	References

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

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3. Bonaldi VM, Bret PM, Reinhold C, Atri M. Helical CT of the liver: value of an early hepatic arterial phase. Radiology 1995; 197:357-363.[Abstract/Free Full Text]
4. Oliver JH, III, Baron RL. Helical biphasic contrast-enhanced CT of the liver: technique, indications, interpretation, and pitfalls. Radiology 1996; 201:1-14.[Abstract/Free Full Text]
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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Blake, S. P. Articles by Raptopoulos, V. Search for Related Content PubMed PubMed Citation Articles by Blake, S. P. Articles by Raptopoulos, V.