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Utility of Sonography for Small Hepatic Lesions Found on Computed Tomography in Patients With Cancer

Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, New York USA.

Address correspondence and reprint requests to Steven Eberhardt, MD, Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021 USA.

	Abstract

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Objective. To assess the performance of sonography in evaluating small indeterminate liver lesions detected on computed tomography in patients with cancer. Methods. Radiology database review from January 1, 1998, to August 4, 2000, identified 76 patients with 124 indeterminate hepatic lesions smaller than 1.5 cm on computed tomography who had abdominal sonography within 3 months. Sonographic reports and images were reviewed to assess whether lesions were referenced or specifically sought and to verify lesion correspondence, detection, and characterization. The validity of sonographic characterization was determined by histopathologic examination or follow-up imaging (mean time to follow up, 17 months; range, 6.5–38.8 months). Results. Sixty (48%) of 124 indeterminate lesions were evident on sonography. Detection improved when lesions were specifically sought and lesion size was greater than 0.5 cm. Forty (66%) of 61 lesions were detected when the radiologist referenced the preceding computed tomography versus 20 (32%) of 63 lesions when the computed tomographic findings were not referenced (P = .0004). Fifty-one (67%) of 76 lesions measuring 0.6 to 1.5 cm were detected on sonography versus 9 (19%) of 48 lesions measuring 0.1 to 0.5 cm. Lesion size (P < .0001) and body habitus (P = .02) were significant factors influencing lesion detection. Sonography characterized 56 (93%) of 60 detected lesions (33 cysts, 18 solid lesions/metastases, and 5 hemangiomas). Sonographic diagnoses were supported in 42 (93%) of 45 lesions by follow-up imaging (37 of 40) or histopathologic examination (5 of 5). Conclusions. Sonography may be useful in cancer patients with average body habitus to characterize small (0.6- to 1.5-cm) indeterminate liver lesions detected on computed tomography.

Key Words: cancer • liver lesions • metastases

Abbreviations: CT, computed tomography • MRI, magnetic resonance imaging

	Introduction

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Small liver lesions (<1.5 cm) detected during routine computed tomography (CT) of the abdomen are frequent, estimated as present on abdominal CT in up to 17% of outpatients.¹ Schwartz et al² evaluated indeterminate and small hepatic lesions (<1.0 cm) found in CT examinations of 378 patients with cancer and found that, despite a nonspecific imaging appearance, 12% of such lesions represented metastases on the basis of interval growth on follow-up. Computed tomography has become the principal examination for initial staging and follow-up of malignancies; however, difficulty in characterizing small hepatic lesions by CT has long been understood.³ Some authors have advocated sonography to characterize such small hepatic lesions.⁴ More recently, the American College of Radiology recommendations judged state-of-the-art CT or hepatic sonography as requisite for initial liver lesion characterization and made recommendations for use of magnetic resonance imaging (MRI) for indeterminate lesions.⁵ We noted increased referrals for sonographic evaluation of small indeterminate liver lesions found on CT, but to our knowledge, the role of sonography for targeted characterization of such lesions in patients with cancer has not been specifically explored.

As technical capabilities of imaging equipment advance, periodic reinvestigation is warranted, with the aim of maintaining clinical efficacy in medical imaging, as outlined by Thornbury.⁶ Determination of the nature of small liver lesions is important, because patients with cancer are now more frequently undergoing hepatic resections for metastatic disease.^7,8 Also, accurate pretreatment staging for nonoperable malignancies influences the choices of treatment regimens. In this study, we sought to retrospectively assess the performance of sonography in detection and characterization of small indeterminate hepatic lesions found on CT examinations in patients with cancer.

	Materials and Methods

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A radiology report database (QuadRIS; Cerner Corporation, Kansas City, MO) at a tertiary care cancer center from January 1, 1998, to August 4, 2000, was searched to identify patients who had CT of the abdomen followed by abdominal sonography within 3 months. These reports were surveyed for descriptions of small indeterminate liver lesions that were typically described as having low density relative to hepatic parenchyma and a size of 1.5 cm or smaller and often deemed "too small to characterize." This phrase generally implied that meaningful Hounsfield density measurements were not valid at the examination slice thickness because of the small lesion size and volume-averaging effects. Cases were excluded if the lesion of interest was characterized in the CT report or if there were reported multiple lesions diagnosed as (or "consistent with") hepatic metastases, even if some of the smaller lesions could be considered indeterminate. Specialized examinations such as CT portography and limited abdominal sonographic examinations also were excluded.

Computed tomographic reports and images were retrospectively reviewed by 1 of 5 radiologists to confirm lesion size, location, and lack of characterization on CT. Lesion size was measured on picture-archiving and communication workstations (GE Medical Systems, Milwaukee, WI) and recorded as a single value equivalent to the average maximal axial cross-sectional diameter to the nearest 0.1 cm. All lesions included in the analysis met the following CT criteria: size not greater than 1.5 cm, Hounsfield region of interest density measurement greater than 20, and conspicuity due to low density relative to surrounding normal hepatic parenchyma. Any lesions not meeting the study criteria were excluded during retrospective review.

Eighty-four (19%) of 453 patients had CT reports that described indeterminate small hepatic lesions. Seventy-six patients (33 male and 43 female; mean age, 62 years; range, 20–95 years) with 124 indeterminate hepatic lesions met inclusion criteria and constituted the study group. The mean time between CT and sonography was 22 days (range, 0–105 days). The mean number of analyzed lesions per patient was 1.6 (range, 1–5). The average cross-sectional diameter for the liver lesions on CT was 0.75 cm (range, 0.1–1.5 cm). Primary cancer diagnoses were 17 colorectal, 11 breast, 6 hepatocellular, 5 unknown primary, 4 lung, 4 pancreas, 3 bladder, 3 bile duct, 3 gallbladder, 3 leukemia, 3 lymphoma, 3 ovary, 3 thyroid, and 8 other.

Computed tomographic examinations were performed on LightSpeed, HiSpeed CT/i, and HiLite Advantage scanners (GE Medical Systems). The CT technique consisted of a helical examination in 66 patients and a conventional scan in 10 patients. Slice thickness ranged from 5 to 10 mm (mean, 7 mm; most scans were 7 mm helical; n = 46). Seventy-five examinations were performed with an intravenous contrast agent (150 mL of 300 mgI/mL iohexol [Omnipaque; Amersham Health, Princeton, NJ]), and 1 examination was performed without the intravenous contrast agent because of renal insufficiency. The delay times to scan through the liver were 70 seconds for helical examinations and 30 seconds for conventional examinations. Four helical scans were multiphasic studies in 5-mm sections, with an arterial phase series acquired at 30 seconds after injection.

Sonographic examinations were performed with 3- to 4-MHz vector transducers and Sequoia and 128XP machines (Acuson; Siemens Medical Solutions, Mountain View, CA) or 2- to 5-MHz curved array transducers and ATL HDI 5000 machines (Philips Medical Systems, Bothell, WA) machines. Eighty (65%) of 124 lesions were evaluated with harmonic imaging. Sonography was performed initially by a technologist, and, as standard practice, findings were confirmed by 1 of 3 radiologists.

Sonographic reports and images were retrospectively reviewed in conjunction with CT images to determine whether an indeterminate lesion shown on CT was detected sonographically and to confirm lesion correspondence. If the original sonographic report included reference to the preceding CT, then the lesion was categorized as referenced, examiner aware of lesion; all others were categorized as nonreferenced, examiner unaware of lesion. This assumption was based on an established departmental policy of including mention of all referenced prior studies within radiology reports. Detection rates for referenced and nonreferenced lesions on sonography were stratified according to lesion size.

Other variables such as lesion location, body habitus, and sonographic technical factors also were analyzed. Lesion location above or below the hepatic veins was recorded from review of the CT images. The depth of lesions from the anterior or lateral liver surface was measured on CT to estimate whether lesions were peripheral or deep. A peripheral location was defined as a distance of 3 cm or less from the liver surface, and deep lesions were located greater than 3 cm from the surface. Body habitus was estimated by measuring anterior abdominal wall thickness on CT in the midline at the level of the portal vein bifurcation. Technical factors such as the use of harmonic sonography and limitations such as fatty liver and pneumobilia were also recorded.

If a lesion was identified on the sonogram, it was characterized into one of the following categories: cyst, solid/metastasis, hemangioma, or indeterminate/other. Lesions were considered cystic if there was a thin, smooth wall, posterior enhancement, and no internal echoes. Hypoechoic solid masses, target lesions with peripheral haloes, and solid masses with heterogeneous echogenicity were categorized as solid/metastases. Uniformly hyperechoic masses with no surrounding haloes were considered hemangiomas provided that there was no history of hepatoma, cirrhosis, or carcinoid tumor. Lesions not defined by any of the above criteria were considered not characterized by sonography.

To assess the validity of sonographic lesion characterization, follow-up imaging results or histopathologic findings were sought for all lesions. Histopathologic diagnoses were accepted as definitive, and if histopathologic findings were not available, interval growth on follow-up CT or sonography was considered sufficient evidence of metastases. Stability in size and appearance for a minimum period of 6 months was considered evidence that the lesion characterization was validated for benign lesions such as cysts and hemangiomas. Although imperfect, such criteria have been used previously.¹

Statistical analyses comparing proportions of lesions detected between independent groups separated by lesion and examination characteristics were performed by a hypothesis test as applied to a 2 x 2 contingency table, assuming a normal distribution. Two-tailed P values were derived from sample data, P < .05 was considered statistically significant.

	Results

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Lesion Detection on Sonography
Results for lesion detection on sonography for all lesions studied are summarized in Table 1. Sixty (48%) of 124 lesions were detected on sonography overall. Lesion detection improved when CT findings were known and referenced at the time of the sonography. Forty (66%) of 61 lesions specifically referenced were detected sonographically versus only 20 (32%) of 63 lesions when no reference was made in the sonographic report to prior CT findings (P = .0004). Lesion size was also a significant factor in lesion detection: 51(67%) of 76 lesions measuring 0.6 to 1.5 cm by CT were detected on subsequent sonography versus only 9 (19%) of 48 lesions measuring 0.1 to 0.5 cm (P < .0001). When lesion size was greater than 0.5 cm and the sonographic examiner was aware of the CT findings, 33 (83%) of 40 lesions were detected sonographically.

View larger version (239K): [in this window] [in a new window]   Figure 1. Images from a 38-year-old woman with breast cancer. A, Axial contrast-enhanced CT image of the liver showing a faint 0.8-cm low-density lesion (arrow). B, Subsequent sonogram showing a uniformly echogenic lesion (arrow) with no surrounding halo. Features were consistent with hemangioma. The lesion was stable on follow-up CT at 24 months.

View larger version (229K): [in this window] [in a new window]   Figure 3. Images from a 68-year-old man with cirrhosis and a history of hepatocellular carcinoma. A, Axial contrast-enhanced CT image showing a 0.6-cm low-density lesion (arrow) in segment 2. B, Sonogram at a corresponding location showing a lesion compatible with a cyst (small arrow), just posterior to a branch of the left portal vein (large arrow). The cyst remained stable on follow-up CT at 22 months.

Follow-up imaging in sonographically detected lesions was by CT (n = 35), sonography (n = 3), or MRI (n = 2). We found that 21 of 22 cysts remained stable on follow-up. One cyst in a patient with breast cancer under observation showed growth on later CT, but no histopathologic diagnosis was obtained. Thirteen stable lesions called cysts were found in patients who had finished chemotherapy, and 3 were in patients who were receiving chemotherapy and had progression elsewhere. All 4 lesions considered hemangiomas on sonography remained stable. In the solid/metastasis category, 4 of 4 lesions that underwent biopsy or were resected were metastases pathologically, and 8 of the remaining 10 with follow-up imaging grew larger, consistent with metastases. Two solid/metastatic lesions remained stable on follow-up. It was noted that these were in patients receiving chemotherapy for their disease.

Follow-up in Lesions Not Detected Sonographically
Follow-up in 64 cases with lesions that were not detected sonographically was available in 37 cases (58%). For 32 lesions with follow-up CT, 25 remained stable, 4 were not visualized, and 3 grew larger. Five lesions with follow-up MRI were all characterized as cysts.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
This study sought to assess sonography as a method of follow-up in patients with cancer who have hepatic lesions 1.5 cm and smaller and considered indeterminate by CT. We found that sonography showed 48% of these small indeterminate liver lesions overall, regardless of the indication for the sonographic examination. The context that we are most interested in is the indeterminate small lesion detected on CT that is subsequently sought by the sonographer for improved characterization, because this is the setting in which sonography may prove useful clinically. When we looked at lesion detection in cases in which it was apparent by the reports that the physician interpreting the sonography was aware of the prior CT examination, we noted an improved detection rate of 66% for all sizes of lesions studied.

Lesion size on CT was a significant factor influencing detection on sonography, with 67% of lesions of 0.6 to 1.5 cm detected overall compared with only 19% detection of lesions smaller than 0.6 cm. When we considered lesion size and whether a lesion was known or referenced, detection on sonography improved to 83% (33 of 40) for lesions in the range of 0.6 to 1.5 cm when the sonographer referenced the prior CT. This probably reflects typical detection performance in the target population that may benefit from sonography.

Lesion detection rates were lower for patients with large body habitus, and this factor should be considered when referring patients for sonographic evaluation of small indeterminate lesions on CT. Interestingly, high lesions above the hepatic veins were revealed with a frequency similar to that of lower lesions, possibly because of our routine use of intercostal scanning. The conspicuity of superficial lesions may be limited by near-field body wall artifacts, and deep lesions may be less evident because of artifacts in the far field, but neither of these factors caused any significant difference in lesion detection. There were few cases with fatty liver or pneumobilia, but even in these technically difficult examinations, most small indeterminate lesions were revealed.

We found that sonographic findings provided additional potentially useful information regarding the nature of the lesion in 93% of detected lesions. In most cases, a specific diagnosis of hemangioma, metastasis, or a cyst was suggested. It has been reported previously that harmonic sonography may improve lesion detection and characterization,⁹ but in this study, we found no significant difference in the rates of detection or characterization among cases imaged with conventional sonography compared with harmonic sonography.

Lesion size on sonography was on average only 0.2 cm greater than on CT. If we consider a measurement error in either modality on the order of 1 to 2 mm, the importance of this observation is questionable. Measurement differences between the 2 modalities may be due to volume averaging on CT or possibly an effect of intravenous CT contrast material.¹⁰ The interval between examinations could explain a size increase for rapidly growing metastases, but the average time between examinations in this study was approximately 3 weeks.

Limitations to any conclusions drawn from this study mainly are due to the retrospective design and lack of available follow-up in an appreciable fraction of patients. Overall, follow-up was available for 45 (75%) of 60 lesions detected on sonography. In most cases, validation of the sonographic results was based on follow-up imaging. It would be optimal to get histopathologic diagnoses as a standard of reference in all cases, but this was not usually clinically appropriate. Despite this, the consistency of the sonographic characterization of benign versus solid/ metastasis for lesions with available follow-up in 93% of cases suggests a fairly high level of diagnostic accuracy for those lesions detected and characterized. Because small solid lesions may be presumed to be more difficult to identify sonographically compared with benign lesions such as cysts and hemangiomas, it may be that the undetected lesions had a higher percentage of solid, presumably metastatic, lesions among them. Only 3 (0.8%) of 37 lesions with follow-up that were not detected sonographically grew larger on follow-up, however. Magnetic resonance imaging may be the next appropriate examination in patients with undetected or indeterminate lesions, provided that the nature of the lesion is clinically relevant.

Although this study was retrospective, the results may be more representative of the actual clinical utility of sonography, because the findings were based on examinations performed by various operators with differing levels of experience on patients in a normal clinical setting. Results are therefore from typical practice conditions, which may add validity. Finally, cases studied included CT examinations from various scanners with differing protocols, resulting in some lack of data uniformity among the various lesions of interest. However, this also suggests that such indeterminate lesions continue to be encountered despite later-generation scanners and tailored protocols used to screen for neoplasms in the liver.

If characterization of a small indeterminate hepatic lesion is relevant for clinical management, then further evaluation is indicated. Hepatic cysts are the most common benign hepatic lesions, and the smallest ones are not easily characterized in the setting of routine CT examination because of volume averaging.³ It is incorrect and potentially serious to assume such lesions are metastases.⁴ The choice of methods for additional work-up includes: (1) returning to the original CT data set from a helical multidetector system, if available, in an attempt to get thinner reconstructed sections, which might allow a diagnosis to be made by overcoming volume-averaging effects; (2) performing dedicated additional CT, in particular a helical thin-section multiphase examination,^11–13 if not previously done, while also optimizing section thickness and reconstruction to decrease volume-averaging effects; (3) performing hepatic MRI, which, although costly, has been shown to be useful in characterizing lesions, benign and malignant^14–18; and (4) performing hepatic sonography, which we propose and others have reported as useful in characterizing hepatic lesions.^19–22

Our results suggest that most indeterminate lesions larger than 5 mm on CT can be detected and characterized on hepatic sonography. In situations in which other previously mentioned noninvasive methods are considered, the inclusion of sonography in the list of available options seems appropriate. Also of note, in cases in which biopsy is deemed the most appropriate clinical approach, some authors have reported that sonographic guidance provides an effective method.^23,24 Clearly, the next step in assessing the role of sonography in this clinical setting would be a well-designed prospective study optimally including comparison of the diagnostic efficacy and cost-effectiveness between the previously mentioned options.

In conclusion, for cancer patients with average body habitus, sonography may be useful for evaluation of small indeterminate hepatic lesions when CT findings are specifically referenced and the lesions are greater than 0.5 cm in diameter.

View larger version (217K): [in this window] [in a new window]   Figure 2. Images from a 78-year-old man with colon cancer. A, Axial contrast-enhanced CT image of the liver showing a 1.1-cm low-density lesion (arrow) at the hepatic dome. B, Sonogram showing a solid lesion (arrow) with a hypoechoic halo, consistent with a metastasis. Diagnosis was confirmed by histopathologic examination at resection.

	Footnotes

We thank Cathleen Cooper for invaluable help with data-keeping methods, research, and manuscript assistance.

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