Abstract
Background
The current role of intra-operative ultrasound (IOUS) is questioned because of recent progress in medical imaging. The aim of the present study was to determine the accuracy of IOUS in the detection of a hepatic tumour (HT) compared with a pre-operative multi-detector computed tomography (MDCT) scan and magnetic resonance imaging (MRI).
Methods
This retrospective study included 418 patients evaluated using an 8-slice MDCT scan (SCAN8), 64-slice MDCT scan (SCAN64) and MRI alone or combined with a computed tomography (CT) scan. The pathological result was used as a gold standard.
Results
Correlation rates for the number of detected lesions compared with pathology results were 0.627 for SCAN8, 0.785 for SCAN64, 0.657 for MRI and 0.913 for IOUS. Compared with pathology, the rate of concordance was significantly higher with IOUS (0.871) than with SCAN8 (0.736; P = 0.011), SCAN64 (0.792; P < 0.001) and MRI (0.742; P < 0.001). IOUS was responsible for a change in operative strategy in 16.5% of patients. Surgery was extended in 12.4%, limited in 1.7% and abandoned in 2.4%.
Conclusions
Compared with cross-sectional pre-operative imaging, IOUS is still superior for the detection of HT and the planning of surgery. IOUS remains recommended as a routine procedure in patients having a hepatic resection in the era of modern pre-operative imaging.
Keywords: hepatic tumours, intra-operative ultrasound
Introduction
The role of liver resection is well established for the management of metastatic colorectal or neuroendocrine cancers, with 5-year survival rates after a hepatic resection approaching 50% for colorectal liver metastases and up to 76% for neuroendocrine metastases.1–3 Recently, a hepatic metastasectomy for other solid tumours such as breast cancer, sarcoma, melanoma, has also been reported.4,5 Furthermore, the most effective treatment for primary liver tumours is hepatic resection or liver transplantation.6 A thorough pre-operative evaluation for patients with metastatic disease confined to the liver or with primary liver tumours is required to determine which patients can benefit from surgery.
Almost 30 years ago, Makuuchi and Bismuth et al. published the first papers on the use of intra-operative ultrasonography (IOUS) for hepatic resections.7–9 However, over the past decades the quality and speed of pre-operative imaging using a multidetector computed tomography (MDCT) scan or magnetic resonance imaging (MRI) have improved dramatically. Helical and multidetector scanners have had a massive impact on CT scanning for the detection of lesions defined to the liver.10,11 With the use of enhanced protocols and contrast agents, MRI has also improved considerably.12,13 This progress in modern imaging techniques has raised questions about the diagnostic validity and accuracy of IOUS, a method that has also undergone technological refinement. The aim of the present study was to assess the accuracy of IOUS in the detection of hepatic tumours (HT) compared with pre-operative CT and MRI.
Materials and methods
This retrospective study, approved by the institutional review board, included 418 patients with hepatic malignancy operated consecutively between January 2005 and December 2009.
There were 252 (60.3%) men, the mean age was 61.5 (± 9.8) years. Two hundred and ninety-seven (71.1%) patients presented with hepatic metastases from colorectal cancer, 82 (19.6%) with a primary hepatic tumour (hepatocellular carcinoma or cholangiocarcinoma) and 39 (9.3%) with another hepatic malignancy.
Patients were evaluated using an 8-slice MDCT scan (SCAN8) from January 2005 to October 2007, a 64-slice MDCT scan (SCAN64) from November 2007 to December 2009 and a 1.5-Tesla MRI (GE Signa MRI system [General Electric Medical Systems, Milwaukee, WI, USA]) either alone or combined with a MDCT scan. Contrast-enhanced CT scanning was performed using Iohexol, 300 mg/ml (Omnipaque 300, GE Healthcare, Princeton, NJ) which was administered with the use of a power injector at a rate of 3 ml/s. For patients weighing between 60 and 80 kg, a total dose of 125 cc was given, for patients weighing between 80 and 105 kg 175 cc was given and for patients weighing more then 105 kg 200 cc was given. Forty-five seconds after the start of the infusion, entire liver imaging was performed during a breath-hold. Subsequently, the portal venous phase was obtained at 70 s. Each image was reconstructed with a contiguous 5-mm-slice thickness. For MRI, Gadobenate Dimeglumine (Multihance, Bracco Diagnostics, Inc., Princeton, NJ, USA)-enhanced imaging of the liver was performed. Intravenous contrast was power injected at rate of 3 ml/s, and the contrast dosage used was 0.025 mmol/kg (0.1 ml/kg). Post-contrast sequences were acquired at 30 s, 1-min, 3-min and 5-min delay. Slice thickness was 7 mm. Patients were instructed to hold their breath in during image acquisition.
In all patients, an IOUS was performed during surgery. An IOUS was performed with the ALOKA Ultrasound system (Aloka Co. Ltd. Tokyo, Japan) with a multifrequency 5–10 MHz transducer. After a laparotomy, the liver surface was inspected and palpated by the hepatobiliary surgeon, followed by a thorough segment-by-segment examination with IOUS. The number, relationship to segmental portal and hepatic veins and size of all lesions were evaluated. A change in operative strategy was defined as a change in the type of resection on the basis of IOUS findings, compared with the pre-operative planned resection. The pre-operative strategy was documented at the multidisciplinary tumour board which takes place several weeks before the operation. Surgery was classified as similar, extended, limited or cancelled. The pathological result of resected specimens was used as a gold standard to evaluate the accuracy of the different imaging techniques. Version 19.0 of SPSS (SPSS, Inc., Chicago, IL, USA) was used to provide all statistical analyses. The χ2-test, Spearman's rank correlation test and the McNemar's test were used for statistical evaluation.
Results
One hundred and seventy-seven patients (42.3%) were evaluated using a SCAN8, 180 (43.1%) using a SCAN64 and 205 (49.0%) using 1.5-Tesla MRI. In 142 patients (34.0%) both a CT scan and MRI were available (80 patients with SCAN8 and MRI and 62 patients with SCAN64 and MRI). Mean time from pre-operative imaging to time of the operation was 44.6 (±32) days.
The operative procedures are summarized in Table 1.
Table 1.
Summary of operative procedures
| Surgical procedure | Number of patients (%) |
|---|---|
| Central hepatectomy | 33 (7.9) |
| Right hepatectomy | 124 (29.7) |
| Extended right hepatectomy | 22 (5.3) |
| Left hepatectomy | 73 (17.5) |
| Extended left hepatectomy | 15 (3.6) |
| Segmentectomy/metastasectomy | 137 (32.8) |
| Hepatectomy cancelled | 14 (3.3) |
Number of hepatic tumours
In 24 patients(5.7%), pathology results could not be used as a gold standard for the number of lesions because a hepatectomy was combined with radiofrequency ablation or the intervention was cancelled because of intra-operative findings. Therefore, the accuracy of the different imaging techniques for the number of detected lesions compared with pathology could only be evaluated in 394 (94.3%) patients. When evaluating the number of tumours found in these patients, the number of hepatic tumours found on pathology per patient was 0, 1, 2, 3 and more than 3 for 10, 242, 69, 28 and 45 patients, respectively (Table 2).
Table 2.
Number of hepatic tumours found per patient
| No. of lesions | SCAN8 (%) | SCAN64 (%) | MRI (%) | IOUS (%) | Pathology (%) |
|---|---|---|---|---|---|
| 0 | 2 (1.3) | 2 (1.1) | 2 (1.1) | 10 (2.5) | 10 (2.5) |
| 1 | 104 (65.4) | 107 (60.1) | 124 (66.7) | 242 (61.4) | 242 (61.4) |
| 2 | 30 (18.9) | 37 (20.8) | 31 (16.7) | 69 (17.5) | 69 (17.5) |
| 3 | 15 (9.4) | 20 (11.2) | 14 (7.5) | 29 (7.4) | 28 (7.1) |
| 4 | 6 (3.8) | 6 (3.4) | 6 (3.2) | 30 (7.6) | 27 (6.9) |
| 5 | 1 (0.6) | 3 (1.7) | 3 (1.6) | 7 (1.8) | 11 (2.8) |
| 6 | 0 (0.0) | 2 (1.1) | 2 (1.1) | 5 (1.3) | 4 (1.0) |
| 7 | 1 (0.6) | 0 (0.0) | 2 (1.1) | 1 (0.3) | 1 (0.3) |
| 8 | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) |
| 9 | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) |
| 10 | 0 (0.0) | 1 (0.6) | 2 (1.1) | 1 (0.3) | 2 (0.5) |
| Total | 159100 | 178100 | 186100 | 394100 | 394100 |
MRI, magnetic resonance imaging; IOUS, intra-operative ultrasound.
Spearman's rank correlation rates for the number of detected lesions compared with pathology are shown in Table 3. All correlations were significantly different from 0 (P < 0.010).
Table 3.
Spearman's rank correlation rates compared with pathology
| Imaging | Number | Correlation rates |
|---|---|---|
| SCAN8 | 159 | 0.627 |
| SCAN64 | 178 | 0.785 |
| MRI | 186 | 0.657 |
| IOUS | 394 | 0.913 |
The rate of concordance compared with pathology was 0.736 [95% confidence interval (CI): 0.666–0.805] for SCAN8, 0.792 (95% CI: 0.732–0.852) for SCAN64, 0.742 (95% CI: 0.679–0.805) for MRI and 0.871 (95% CI: 0.837–0.904) for IOUS. Compared with pathology, the rate of concordance was significantly higher with IOUS than with SCAN8 (P = 0.011), SCAN64 (P < 0.001) and MRI (P < 0.001) (Table 4).
Table 4.
Comparison of the proportion of concordance (Yes/No) to pathology for SCAN8, SCAN64 and magnetic resonance imaging (MRI) vs. intra-opertaive ultrasound (IOUS)
| Imaging | IOUS | McNemar test | |
|---|---|---|---|
| No | Yes | P | |
| SCAN8 | |||
| No | 19 | 23 | 0.011 |
| Yes | 8 | 109 | |
| SCAN64 | |||
| No | 12 | 25 | <0.001 |
| Yes | 4 | 137 | |
| MRI | |||
| No | 20 | 28 | <0.001 |
| Yes | 6 | 132 | |
Impact on operative strategy
In 86 patients (20.5%), operative strategy was changed intra-operatively. Of these, 17 (4.0%) patients had a change in operative strategy as a result of non-IOUS-related intra-operative findings (i.e. carcinomatosis, cirrhosis, etc.). In 69 patients (16.5%), IOUS was only responsible for the change in operative strategy (Fig. 1). In 47 (11.2%) of those patients additional lesions found on IOUS were responsible for a change in operative strategy. IOUS also had an impact on the accurate assessment of the proximity to or invasion of the hepatic vasculature which influenced the operative strategy in 22 patients (5.3%).
Figure 1.
Impact on operative strategy
Hepatic resection was extended as a result of IOUS in 52 patients (12.4%). In 37 (8.9%) of those patients additional lesions were found on IOUS and in 15 (3.5%) patients a change in volume of the lesion or proximity to or invasion of the hepatic vasculature was noted on IOUS. In 13 (3.1%) patients the operation was extended because additional lesions were discovered and/or palpated requiring more extensive surgery. The operation was limited as a result of IOUS in 7 patients (1,7%) and cancelled in 10 patients (2,4%). In four (1.0%) patients the operation was cancelled as a result of inspection and/or palpation (carcinomatosis in three patients and cirrhosis in one patient).
IOUS was responsible for a change in operative strategy in 35 patients (19.8%) with a SCAN8, in 21 patients (11.7%) with a SCAN64 and in 35 patients (17.1%) with an MRI (Table 5). Intergroup difference was not significant (P = 0.770).
Table 5.
Change in operative strategy (OS) according to type of pre-operative imaging
| Number of patients | No change in OS (%) | Change in OS (%) | Limited (%) | Abandoned (%) | Extended (%) | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| Total | IOUS | Total | IOUS | Total | IOUS | Total | IOUS | |||
| SCAN8 | 177 | 133 (75.1) | 44 (24.9) | 35 (19.8) | 2 (1.1) | 2 (1.1) | 9 (5.1) | 6 (3.4) | 33 (18.6) | 27 (15.2) |
| SCAN64 | 180 | 154 (85.6) | 26 (14.4) | 21 (11.7) | 2 (1.1) | 2 (1.1) | 2 (1.1) | 1 (0.6) | 22 (12.2) | 18 (10.0) |
| MRI | 205 | 162 (79.0) | 43 (21.0) | 35 (17.1) | 5 (2.4) | 5 (2.4) | 9 (4.4) | 8 (3.9) | 29 (14.1) | 22 (10.7) |
MRI, magnetic resonance imaging; IOUS, intra-operative ultrasound.
In 25 patients (6.0%) IOUS differed from pre-operative imaging but these findings did not result in a change in operative strategy.
Discussion
Direct surgical exploration of the liver in combination with IOUS has long been regarded as a gold standard against which any other result should be tested. For almost 30 years, decision making during a hepatectomy for primary and secondary hepatic malignancy is influenced by IOUS. In the 1980s and 1990s, a change in operative strategy as a result of IOUS was noted in 19% to 67% of patients.14–16 Other historical small series were published proving IOUS significantly improved detection of hepatic tumours.17–20 However, imaging techniques in the pre-operative assessment of patients with a hepatic tumour have improved over the years. Recent sensitivity estimates on a per-patient basis for non-helical CT, helical CT, MRI and positron emission tomography (PET) were 60.2%, 64.7%, 75.8% and 94.6%, respectively, and on a per-lesion basis 52.3%, 63.8%, 64.4% and 75.9%.21 In a recent meta-analysis, Niekel et al. even found that the sensitivity of MRI increased significantly after 2004.22 Furthermore, the combination of PET and CT provides simultaneous functional and anatomic information.23 Because of this recent progress in medical imaging, the role of IOUS has been questioned.
Within the current series, IOUS changed the operative strategy in 16.5% of patients. These findings are supported by other recently published smaller series.24–27
IOUS not only detected lesions not found on pre-operative investigation in a significant number of patients (47 patients, 11.2%) but also had an impact on the accurate assessment of the proximity to or invasion of the hepatic vasculature which can also influence the operative strategy (22 patients, 5.3%). Therefore, IOUS helps the hepatobiliary surgeon to understand the three-dimensional relationship between the liver vasculature and tumour but also improves patient outcome by defining adequate margins of resection and by selecting the correct type of resection.
As a result of ethical considerations, the hepatobiliary surgeon performing IOUS in our series was not blinded to the results of the pre-operative imaging modalities. This could be considered as a limitation of the present study. Nevertheless, this study clearly demonstrated that the use of IOUS is still recommended not only to confirm the results found on pre-operative imaging, but also to provide additional information to the surgeon which could change the surgical strategy intra-operatively.
The present study did not show any intergroup difference between the pre-operative imaging modalities. This is in contrast to the results of a recent meta-analysis.22 In this meta-analysis the authors concluded that MRI was the preferred first-line modality for evaluating colorectal liver metastases in patients with small lesions who have not previously undergone therapy. Sensitivity of MRI was significantly higher compared with the CT scan (P: 0.006). The non-superiority of MRI within the present study may be explained by the fact that MRI results evaluated in this series were not achieved from the most recent MRI as it has only been available at our institution since 2010. In their previous meta-analysis (which included 0.5-T, 1-T and 1.5-T MRI), Niekel et al. also found that the sensitivity of MRI performed before 2004 was significantly lower than that for MRI performed after 2004 (P < 0.001). Studies included in this series were achieved from the 1.5-Tesla GE Signa MRI system (General Electric Medical Systems, Milwaukee, WI) (version 1998 and 2001) which could explain non-superiority of MRI.
Over the past decade, PET and PET/CT has been increasingly used for the evaluation of patients with hepatic malignancy. The introduction of PET/CT has challenged the value of IOUS again.28 As recently shown by Wildi et al., the diagnostic performance of PET/CT combined with IOUS is higher compared with PET/CT for patients with colorectal liver metastasis.28 In their series, IOUS changed the surgical strategy in 35% of patients. However, smaller lesions often remain undetected in a significant number of patients and the exact role of FDG PET/CT is not yet clear owing to the small number of studies.23 Furthermore, most patients described in the current series were not analysed with PET/CT and therefore the results of PET/CT were not included for further analysis.
Yang et al. recently reported that the utility of the pre-operative helical CT to evaluate colorectal liver metastasis was inversely proportional to the time interval between imaging and surgery.29 Their model predicted that in order to achieve a sensitivity of over 90%, CT had to be performed no more than 26 days before surgery. One of the limitations of the present study was that cross-sectional pre-operative imaging was performed on an average of 44.6 days from hepatic resection, thus some hepatic lesions might have become more apparent during this time. In contrast to the results of Yang et al., no negative impact on accuracy for SCAN8, SCAN64 or MRI was found when performed more than 30 days from the hepatectomy (data not shown).
In conclusion, in spite of the refinement in modern pre-operative cross-sectional imaging, IOUS remains an important tool in the operative management of hepatic malignancy. In this series, IOUS altered the surgical strategy in 16.5% of patients.
Conflicts of interest
None.
References
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