DOI: 10.1148/radiol.2473070949
(Radiology 2008;247:896-902.)
© RSNA, 2008
Vascular and Interventional Radiology |
Imaging Findings after Liver Resection by Using Radiofrequency Parenchymal Coagulation Devices: Initial Experiences1
John P. McGahan, MD and
Vijay P. Khatri, MBChB
1 From the Departments of Radiology (J.P.M.) and Surgery (V.P.K.), University of California Davis Medical Center, 4501 X St, Suite 3010, Sacramento, CA 95817. Received March 3, 2007; revision requested August 2; revision received August 29; accepted September 27; final version accepted October 29.
Address correspondence to V.P.K. (e-mail: vijay.khatri{at}ucdmc.ucdavis.edu).
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ABSTRACT
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Purpose: To retrospectively evaluate the imaging features and potential pitfalls in interpreting the findings at the site of surgery in patients undergoing hepatic resection by using the InLine and TissueLink radiofrequency devices for parenchymal coagulation prior to transection.
Materials and Methods: This HIPAA–compliant study was approved by the Institutional Review Board with waiver of informed consent. Twenty-six patients (14 men, 12 women; mean age, 56 years), in whom intraoperative Inline and TissueLink devices were used for resection of hepatocellular carcinoma or metastatic liver disease or other liver tumors, were identified. Information such as tumor characteristics, diagnostic studies, surgical therapy, and surveillance methods were reviewed. All computed tomographic (CT) and positron emission tomographic (PET) scans and the single magnetic resonance and ultrasonographic images of the abdomen were retrospectively reviewed by a radiologist and compared with the initial interpreting physician's report.
Results: Of 35 CT scans, 33 revealed a hypodense line of demarcation (mean thickness, 13.2 mm) between the surgical resection clips and the normal liver parenchyma. This demarcation was interpreted as "could not exclude site recurrence" in three cases and "recurrence or probable recurrence" in five cases. In two CT scans, the hypodense demarcation was not present. In all seven PET scans, the uniform hypermetabolic activity associated with the demarcation was labeled as a recurrence. At follow-up CT (median, 12.5 months), marginal recurrence was not detected in 25 patients, though in one case there was a recurrence in close proximity to the surgical site.
Conclusion: The use of InLine and TissueLink devices during hepatectomy is associated with a linear hypodense demarcation at the surgical margin that also demonstrates a symmetrical rimlike hypermetabolic activity seen on PET scans.
© RSNA, 2008
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INTRODUCTION
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Intraoperative blood loss during liver resection is a major factor associated with both morbidity and mortality (1–4). To reduce blood loss during parenchymal transection there has been recent development of radiofrequency (RF) devices such as the InLine Multichannel (four to six electrodes on a linear array) Radiofrequency Device (Resect Medical, Fremont, Calif) (ILMRD) that produces coagulative necrosis along the transection plane, thus minimizing blood loss (5). Additional hemostasis is achieved with the TissueLink dissecting sealer (TissueLink Medical, Dover, NH), which also uses RF energy to precoagulate liver parenchyma (6). We term this intraoperative procedure RF parenchymal coagulation (RPC) to indicate that it is distinct from therapeutic RF ablation of the hepatic tumor itself. To date, and to our knowledge, there has been no description of the imaging features in patients undergoing InLine and TissueLink coagulation with hepatic resection by using these devices or outlining of the potential pitfalls in interpretation of the findings seen at the site of surgical resection as observed on surveillance imaging. Thus, the purpose of our study was to retrospectively evaluate the imaging features and potential pitfalls in interpretation of the findings at the site of surgical resection in patients undergoing hepatic resection by using the InLine and TissueLink RF devices for parenchymal coagulation prior to transection.
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MATERIALS AND METHODS
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Patients and Imaging
All patients in whom both Inline and TissueLink devices were used for resection of hepatocellular carcinoma (HCC) or metastatic liver disease or other liver tumors (May 2004 to December 2006) were identified. Medical records were reviewed to obtain demographic information, tumor characteristics, diagnostic studies performed, surgical therapy used, and clinical follow-up of the patients (J.P.M., V.P.K.). Approval from the Institutional Review Board was obtained to conduct this study and research conduct was Health Insurance Portability and Accountability Act–compliant. Informed consent was waived by the Institutional Review Board.
A total of 26 patients (14 men, 12 women; age range, 25–84 years; mean, 56 years) underwent hepatic resection by using both devices: 16 patients had liver metastasis, seven patients had primary HCC, and one patient each had a cavernous hemangioma, a focal nodular hyperplasia, and an inflammatory mass. Of 26 patients, four did not undergo follow-up imaging studies, leaving 22 patients (13 men, nine women; age range, 25–84 years; mean, 56 years). A total of 44 examinations (computed tomography [CT], positron emission tomography [PET], magnetic resonance [MR] imaging, or ultrasonography [US]) in these 22 patients were reviewed in this series. Patients underwent one to three imaging studies, depending on how long they had been followed-up postoperatively. Imaging studies included 34 contrast material–enhanced CT scans, one nonenhanced CT scan, seven PET scans, one MR image, and one US scan.
The seven PET scans were performed with a scanner (ST; GE Healthcare, Milwaukee, Wis) by using a dose of 17–25 mCi (269–925 MBq) of fluorine 18 fluorodeoxyglucose ([18F]-2-fluoro-2-deoxy-
-glucose), determined on the basis of body weight. Unenhanced CT imaging was performed with a scanner (Lightspeed-16; GE Healthcare) at 140 kV, 300 mA, and 3.75-mm collimation. Patients were scanned approximately 75 minutes after injection and instructed to void immediately prior to imaging. Standard imaging included PET, CT, and combined PET/CT imaging. Standard uptake values were obtained. In one patient, a contrast-enhanced MR was performed with a 1.5-T imager (12.1 L Signa; GE Healthcare) by using intravenous administration of contrast material (Omniscan; GE Healthcare). MR imagingincluded dual-echo T1-weighted sequence, coronal single-shot fast spin-echo sequence, and liver acquisition with volume acceleration sequences performed before and after contrast enhancement. Twenty patients underwent a total of 34 follow-up CT scans by using the same scanner mentioned previously (Lightspeed 16; GE Healthcare) and intravenous administration of 100–140 mL of contrast material (Omnipaque 350; GE Healthcare). The number of CT scans obtained in each patient varied with clinical parameters and length of follow-up. CT parameters included variable readings, usually 120 kV, 350 mA, and 5-mm collimation. CT protocols varied from two-phase (45–60 seconds and 3–5 minutes after injection) to a four-phase (base, arterial [automatically triggered], portal venous, and delayed [3–5 minutes after injection]) protocol. In one case, only an unenhanced CT was performed. In one patient, US was performed by using a 4-MHz scanner (Sequoia; Siemens-Acuson, Mountain View, Calif).
Surgical Techniques
All hepatic resections were performed in a standardized fashion by a surgical oncologist (V.P.K., with 12 years experience in liver surgery). Intraoperative US was performed to evaluate the extent of the disease, to assess proximity of the tumor to major vessels, and to facilitate optimal tumor-free margins during transection. All intraoperative US scans were obtained by an author (V.P.K.) and a certified US technician (a nonauthor, with 13 years experience). After blood supply to the resected liver segment was ligated, a demarcation line developed and the parenchymal transection was performed approximately 5–10 mm from this line. A US scanner (Sequoia; Siemens-Acuson) with a linear-array transducer (L7T, 8LT5, 6L3) was used. Intraoperative US was used to measure the width of the liver parenchyma at the transection plane (Fig 1a) to gauge how deep to insert the multiple linear electrodes of the device. Intraoperative RPC was performed with the bipolar ILMRD attached to a generator (Radiotherapeutics 1500; Radiotherapeutics, Mountain View, Calif). The ILMRD consists of six electrodes measuring either 4 or 6 cm in length evenly spaced along the device (Fig 1b) that can be inserted at variable lengths in the liver parenchyma. Insertion of these needles and tissue coagulation were monitored by using intraoperative US (Fig 1c). Once the liver plane was completely divided, the transection surface was slowly treated with a TissueLink coagulator.
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Figure 1a: (a) Transverse US scan of transection shows depth of liver tissue (4.5 cm) prior to insertion of ILMRD electrode (arrow indicates tumor). (b) Image of ILMRD with six electrodes inserted at variable lengths in liver. (c) Longitudinal US scan of transection plane (arrow) shows ablated hepatic parenchyma.
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Figure 1b: (a) Transverse US scan of transection shows depth of liver tissue (4.5 cm) prior to insertion of ILMRD electrode (arrow indicates tumor). (b) Image of ILMRD with six electrodes inserted at variable lengths in liver. (c) Longitudinal US scan of transection plane (arrow) shows ablated hepatic parenchyma.
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Figure 1c: (a) Transverse US scan of transection shows depth of liver tissue (4.5 cm) prior to insertion of ILMRD electrode (arrow indicates tumor). (b) Image of ILMRD with six electrodes inserted at variable lengths in liver. (c) Longitudinal US scan of transection plane (arrow) shows ablated hepatic parenchyma.
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Surveillance Program and Image Interpretation
All patients underwent standard surveillance after hepatectomy, which included four monthly clinical evaluations consisting of patient history and physical examination, supplemented with CT scans of the abdomen and pelvis. When there was suspicion of disease recurrence, staging PET scans were obtained. All imaging studies were retrospectively reviewed by a radiologist (J.P.M., with 25 years experience in abdominal CT and US and 5 years experience in abdominal MR) who consulted with a PET specialist (a nonauthor, with 2 years experience in abdominal PET). The senior radiologist personally reviewed all reports and individual CT, PET, MR, and US images. The initial physician's report was reviewed as to his or her interpretation of the site of surgical resection. Eight board-certified (institution faculty members) radiologists (with 4–25 years [average, 12 years] experience with abdominal CT) interpreted these scans. The classifications were (a) no evidence of recurrence, (b) cannot exclude a recurrence, (c) probable recurrence, and (d) partial circumferential.
The CT scans were reviewed to determine the presence of a line of demarcation at the coagulated site. If this tissue coagulation margin was seen, it was classified as (a) linear, (b) linear and nodular, (c) nodular, or (d) partial and circumferential. Also, the width of the coagulation margin was independently measured if surgical clips were left at the site of resection. The relationship of the location of the clips to the RF ablation margin was noted. Other incidental findings, such as fluid collection, were noted.
The PET scans were reviewed to determine the presence of hypermetabolic activity at the ablation site. The time from surgery to PET scan was also noted to see if the hypermetabolic activity persisted or normalized within that time.
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RESULTS
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Surgery
Of these 26 patients, 11 had undergone formal hepatic lobectomy (removal of 
4 segments) and the remaining 14, a segmental (removal of 1–3 segments) hepatic resection, with a median blood loss of 150 mL. Patients in this study were reviewed from 1 month 15 days to 27 months after surgical resection (median, 12.5 months). Three patients developed intrahepatic recurrence: One patient who had undergone segment 2 resection of a well-differentiated hepatoma developed bilobar recurrent tumors, one patient who had undergone right hepatic resection for breast cancer metastasis developed new liver recurrences, and one patient who had undergone resection of a hepatoma in the right lobe of the liver experienced a recurrence in close proximity to the surgical site.
CT Findings
Of these 26 patients, 22 had undergone follow-up imaging. The 35 (34 contrast-enhanced and one unenhanced) CT scans were obtained from 3 days to 15 months after surgery with tissue coagulation devices. Retrospective review of the scans (J.P.M.) demonstrated no region of decreased attenuation at the area of resection in two of 35 scans. A margin of demarcation was seen in the other 33 scans and included (a) a linear region of demarcation in 25 patients (Figs 2, 3), (b) a linear nodular margin at the area of resection in three patients (Fig 4), (c) a nodular appearance in three patients, and (d) a partial circumferential demarcation in two patients (Fig 5; Table). In almost all patients, the line of demarcation consisted of a region of decreased attenuation between the surgical resection clips and the rest of the normal parenchyma. This margin of attenuation at the site of resection averaged 13.2 mm in thickness (range, 4–24 mm). This line of decreased attenuation was not visualized in two cases. In the other 33 cases where the margin was seen, it persisted with time and showed only minimal decrease in thickness at follow-up CT. The recurrence close to the surgical site had a typical appearance of an HCC with a rounded mass with contrast-enhancement on arterial phase images, with rapid washout on delayed phase images (Fig 6).
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Figure 2a: Transverse CT of 84-year-old man with colorectal metastasis, treated with partial left hepatectomy. Patient underwent RF ablation of two lesions in right liver lobe. (a) Portal venous phase scan obtained 3 days after partial left heparectomy shows surgical clip and linear region of decreased attenuation (arrow) between clip and normal enhancing liver parenchyma; this defect corresponds with ILMRD needle placement site. (b) Portal venous phase scan obtained 2 months after hepatectomy shows surgical clips and linear region of decreased attenuation (solid arrow) adjacent to normal enhancing liver parenchyma, which corresponds to ILMRD site. Circular region of decreased attenuation (open arrow) in liver segments 6 and 7 corresponds to ablated tumor.
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Figure 2b: Transverse CT of 84-year-old man with colorectal metastasis, treated with partial left hepatectomy. Patient underwent RF ablation of two lesions in right liver lobe. (a) Portal venous phase scan obtained 3 days after partial left heparectomy shows surgical clip and linear region of decreased attenuation (arrow) between clip and normal enhancing liver parenchyma; this defect corresponds with ILMRD needle placement site. (b) Portal venous phase scan obtained 2 months after hepatectomy shows surgical clips and linear region of decreased attenuation (solid arrow) adjacent to normal enhancing liver parenchyma, which corresponds to ILMRD site. Circular region of decreased attenuation (open arrow) in liver segments 6 and 7 corresponds to ablated tumor.
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Figure 3a: Images of 48-year-old woman with hepatitis C and HCC resection from liver segments 2 and 3. (a) Transverse contrast-enhanced portal venous phase CT scan obtained 2 months after segment 2-3 HCC resection shows linear region of decreased attenuation (arrow) between surgical clips and liver, corresponding to plane of ILMRD needle placement. (b) Transverse contrast-enhanced portal venous phase T1-weighted MR image (repetition time msec/echo time msec/inversion time msec, 3.872/1.848/7) by using liver acquisition with volume acceleration protocol obtained 6 months after surgery shows region of low signal intensity along resection site (arrow), corresponding to ILMRD needle placement.
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Figure 3b: Images of 48-year-old woman with hepatitis C and HCC resection from liver segments 2 and 3. (a) Transverse contrast-enhanced portal venous phase CT scan obtained 2 months after segment 2-3 HCC resection shows linear region of decreased attenuation (arrow) between surgical clips and liver, corresponding to plane of ILMRD needle placement. (b) Transverse contrast-enhanced portal venous phase T1-weighted MR image (repetition time msec/echo time msec/inversion time msec, 3.872/1.848/7) by using liver acquisition with volume acceleration protocol obtained 6 months after surgery shows region of low signal intensity along resection site (arrow), corresponding to ILMRD needle placement.
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Figure 4: Portal venous phase contrast-enhanced transverse CT scan obtained 4 months after partial right hepatectomy for colorectal metastasis shows linear-nodular region of decreased attenuation (arrow) between clips and normal liver corresponding to ILMRD defect. Overlying clips is small fluid collection.
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Figure 5a: Images of 43-year-old woman who underwent resection of cavernous hemangioma of liver. (a) Transverse contrast-enhanced arterial phase CT scan obtained 2 weeks after ILMRD and TissueLink RF ablation shows semicircular region of decreased attenuation (solid arrow) corresponding to site of hepatic parenchymal ablation. Note small fluid collection in surgical bed (open arrow). (b) Transverse US scan obtained 3 months after surgical resection shows hypoechoic seroma (open arrow), which was aspirated with US guidance. Also note hypoechoic-hypoechoic rim (solid arrow) at ILMRD needle placement site.
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Figure 5b: Images of 43-year-old woman who underwent resection of cavernous hemangioma of liver. (a) Transverse contrast-enhanced arterial phase CT scan obtained 2 weeks after ILMRD and TissueLink RF ablation shows semicircular region of decreased attenuation (solid arrow) corresponding to site of hepatic parenchymal ablation. Note small fluid collection in surgical bed (open arrow). (b) Transverse US scan obtained 3 months after surgical resection shows hypoechoic seroma (open arrow), which was aspirated with US guidance. Also note hypoechoic-hypoechoic rim (solid arrow) at ILMRD needle placement site.
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Figure 6a: Transverse contrast-enhanced CT of 76-year-old man after HCC resection with ILMRD. (a) Surveillance arterial phase scan obtained 9 months after resection shows area of enhancement (arrow) in close proximity to resection site noted by surgical clips. (b) Portal venous phase scan shows central washout with rim of enhancement in this recurrent HCC (arrow).
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Figure 6b: Transverse contrast-enhanced CT of 76-year-old man after HCC resection with ILMRD. (a) Surveillance arterial phase scan obtained 9 months after resection shows area of enhancement (arrow) in close proximity to resection site noted by surgical clips. (b) Portal venous phase scan shows central washout with rim of enhancement in this recurrent HCC (arrow).
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Of 35 CT scans initially viewed by the radiologist, the resection margin was interpreted as follows: (a) no evidence of recurrence in 25 patients, (b) could not exclude site recurrence in three patients, (c) recurrence or probable recurrence in five patients, (d) a liver laceration in one patient, and (e) a liver laceration and/or infarction in one patient (Table).
PET Findings
In patients who underwent PET scans 1, 3, and 4 months after resection by using the ILMRD (Fig 7), the margin of resection was initially interpreted as rimlike hypermetabolic activity at the site, consistent with possible tumor recurrence, as noted by the initial report and by the retrospective review (J.P.M.) (Table). This hypermetabolic activity was symmetric rather than focal at the site of surgical resection. In two patients who underwent a PET scan 6 months after resection, one had no activity and one had decreased activity compared with the prior PET scan. In two patients who underwent PET at 8 and 9 months, there was no increased activity, as noted by the initial report and by the retrospective review (J.P.M.).
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Figure 7a: Transverse 18F fluorodeoxyglucose PET/CT of 55-year-old man with hepatitis C after HCC resection with ILMRD. (a) Scan obtained 6 weeks after HCC resection shows symmetrical increased activity uptake surrounding resection site. Note surgical clips surrounded by tissue with hypermetabolic activity at margin of surgical resection (arrow). (b) Scan obtained 9 months after resection shows no evidence of hypermetabolic activity at site. Clips noted on adjacent scan.
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Figure 7b: Transverse 18F fluorodeoxyglucose PET/CT of 55-year-old man with hepatitis C after HCC resection with ILMRD. (a) Scan obtained 6 weeks after HCC resection shows symmetrical increased activity uptake surrounding resection site. Note surgical clips surrounded by tissue with hypermetabolic activity at margin of surgical resection (arrow). (b) Scan obtained 9 months after resection shows no evidence of hypermetabolic activity at site. Clips noted on adjacent scan.
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MR and US Findings
Only one patient underwent MR imaging. MR was performed 6 months after RF ablation and depicted a circumferential region of decreased signal intensity approximately 18 mm in diameter on a contrast-enhanced scan (Fig 3). One patient also underwent US examination in conjunction with needle aspiration. In this patient, there was a hypoechoic region, which was adjacent to the liver, with a hyperechoic region identified between a fluid collection region (seroma) and the nonresected liver (Fig 5).
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DISCUSSION
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In reviewing the interpretation of findings in cases in which ILMRD was used during hepatectomy, it was not infrequent in our study that the radiologist misinterpreted the region of RPC as possible recurrence because the line of tissue coagulation did not enhance as compared with the other portions of the liver. In fact, eight of 35 CT scans were interpreted as a possible recurrence or cannot exclude a recurrence at the site of resection. In retrospective review of the CT scans in these patients, the finding at the site of resection was that of a linear region of decreased attenuation on the contrast-enhanced CT scan. This region was usually between the surgical clips and the rest of the normal liver. On occasion, depending on the placement of the different needles, part of the margin did appear more nodular than linear. In addition, a third pattern was seen during resection of a large tumor in which the rest of the liver collapsed around the previous site of resection and had a semicircular appearance. Overall, the thickness of the CT margin was approximately 13 mm. The thickness for this margin decreased slightly, depending on the time from surgical resection but never completely disappeared during the follow-up period. This may be similar to what is identified as focal RF ablation of focal masses in which the lesion may persist as an unenhanced area of low attenuation without peripheral nodular enhancement (7). This was different from the contrast-enhanced mass observed in the patient with hepatoma in whom there was a recurrence close to the surgical margin. In both of our single cases of MR and US imaging, a similar margin was observed.
Also of interest was that PET scans showed hypermetabolic activity in the surgical bed in the region of the RPC, which persisted for 4 months and either disappeared completely or decreased considerably at 6 months. This may be interpreted as a recurrent tumor. PET scans have been advocated to help detect residual tumors after RF ablation of primary and secondary liver tumors (8,9). In these cases, a region of hypermetabolic activity at PET has been shown to increase sensitivity of detection of recurrent tumors compared with contrast-enhanced CT alone. However, Veit et al (9) noted that after RF ablation, PET shows a rimlike area of increased glucose metabolism at the ablative margin, which they interpreted as increased activity secondary to heat-induced hyperperfusion and tissue regeneration. They did not note this normal rim of hyperactivity on the first day after RF ablation, but did note it 2 days after RF ablation. They did not comment on how long this hyperactivity persisted. They felt this homogeneous rimlike area of glucose metabolism cannot be attributed to residual tumor. An area of tumor recurrence instead is represented as an area of focally increased glucose metabolism (9). This correlates well with the imaging characteristics in our patients in whom there were homogeneous rimlike areas of increased 18F fluorodeoxyglucose activity at the site of RPC by using the ILMRD. Thus, one should recognize that some metabolic activity at PET occurs at the site of RPC with patients in whom this device is used. This may also persist for a few months following RPC and/or partial hepatectomy. However, a more focal region of increased glucose metabolism may more correctly correspond to a site of residual or recurrent tumor, as noted by Veit et al (9).
Postoperative surveillance imaging is important for evaluating the effectiveness of treatment, as well as screening for recurrence. Early detection not only allows potentially curative resection of recurrent liver metastases, but there may be significant clinical benefit to the earlier commencement of systemic chemotherapy with biologic agents (10,11) or provision of alternate therapies such as RF ablation (12), cryotherapy (13), chemoembolization (14), and selective intraarterial radiation therapy (15). Evolution of these various effective treatment options underscores the importance of accurate interpretation of surveillance imaging studies.
The limitations of this study included the fact that there was no pathologic proof as to the absence of marginal recurrence at the site of parenchymal coagulation. Therefore, stability of the margin of decreased attenuation at CT, no new areas of enhancement at CT, and temporal decreased hypermetabolic activity were used as indirect evidence of no local recurrence at the surgical margin.
The use of the ILMRD for parenchymal coagulation during hepatectomy usually results in a linear region of decreased attenuation, in the range of 1 cm or greater, observed at CT at the site of RPC. Surgical clips are noted between this area of attenuation and the rest of the normal liver. On PET imaging obtained shortly after surgical resection, the region of tissue coagulation may appear as a symmetric rimlike region of hypermetabolic activity at the surgical margin. Recognition of these normal features is important to avoid misinterpreting these findings as residual tumor or tumor recurrence, when InLine and TissueLink RF devices have been used for parenchymal coagulation during partial hepatectomy.
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ADVANCES IN KNOWLEDGE
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- The use of InLine and TissueLink devices during hepatectomy is associated with a linear hypoattenuating demarcation at the surgical margin.
- Hypermetabolic activity on PET scans can occur at the site of radiofrequency (RF) parenchymal coagulation with patients in whom intraoperative InLine/TissueLink devices are used.
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IMPLICATION FOR PATIENT CARE
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- Misinterpretation of a possible recurrence in the region of RF parenchymal coagulation can occur if one is not aware of the expected imaging features after the procedure.
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ACKNOWLEDGMENTS
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Special thanks to Stephen Wilkendorf, RT, RDMS, for providing intraoperative technical assistance with US and RF devices and Tammy LaPolt for preparation of this manuscript.
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FOOTNOTES
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Abbreviations: ILMRD = InLine multichannel RF device • HCC = hepatocellular carcinoma • RF = radiofrequency • RPC = RF parenchymal coagulation
Author contributions: Guarantors of integrity of entire study, J.P.M., V.P.K.; study concepts/study design or data acquisition or data analysis/interpretation, J.P.M., V.P.K.; manuscript drafting or manuscript revision for important intellectual content, J.P.M., V.P.K.; approval of final version of submitted manuscript, J.P.M., V.P.K.; literature research, J.P.M., V.P.K.; clinical studies, J.P.M., V.P.K.; and manuscript editing, J.P.M., V.P.K.
Authors stated no financial relationship to disclose.
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ABSTRACT
INTRODUCTION
