Safety and efficacy of right portal vein embolization in patients with prior left lateral liver resection

Abstract

Background

In patients with bilobar metastatic liver disease, surgical clearance of both liver lobes may be achieved through multiple-stage liver resections. For patients with extensive disease, a major two-staged hepatectomy consisting of resection of liver segments II and III before right-sided portal vein embolization (PVE) and resection of segments V–VIII may be performed, leaving only segments IV ± I as the liver remnant.

Purpose

To describe the outcome following right-sided PVE after prior complete resection of liver segments II and III.

Material and Methods

In this retrospective study, 15 patients (mean age = 60.4 ± 9.3 years) with liver metastases from colorectal cancer (n = 14) and uveal melanoma (n = 1) who were scheduled to undergo a major two-stage hepatectomy, were included. Total liver volume (TLV) and volume of the future liver remnant (FLR) were measured on pre- and postinterventional computed tomography (CT) scans, and standardized FLR volumes (ratio FLR/TLV) were calculated. Patient data were retrospectively analyzed regarding peri- and postinterventional complications, with special emphasis on liver function tests.

Results

The mean standardized post-PVE FLR volume was 26.9% ± 6.4% and no patient developed hepatic insufficiency after the PVE. Based on FLR hypertrophy and liver function tests, all but one patient were considered eligible for the subsequent right-sided hepatectomy. However, due to local tumor progression, only 9/15 patients eventually proceeded to the second stage of surgery.  

Conclusion

Right-sided PVE was safe and efficacious in this cohort of patients who had previously undergone a complete resection of liver segments II and III as part of a major staged hepatectomy pathway leaving only segments IV(±I) as the FLR. 

Keywords

Portal vein embolization staged hepatectomy segment IV safety efficacy

Introduction

Surgery represents the gold standard treatment for resectable liver metastases from colorectal cancer or uveal melanoma today, since the surgical resection has been shown to prolong survival compared to palliative treatment (systemic chemotherapy) and may even be potentially curative (1 –3). Advances in surgical technique and multidisciplinary care have therefore led to the development of multistage resection strategies for patients with extensive metastatic liver disease. In patients with bilobar liver metastases, for example, a two-stage hepatectomy with surgical clearance of both liver lobes may be performed. This strategy was first described by Adam et al. (4) in 2000 and usually involves atypical or segmental resections of tumors in the left liver lobe (first stage of surgery) followed by a right hepatic portal vein embolization (PVE). Once the future liver remnant (FLR) has reached a sufficient size, a right hemihepatectomy completes the treatment pathway (second stage of surgery).

The most aggressive version of a two-stage hepatectomy consists of a complete left lateral hepatectomy, i.e. resection of segments II and III, during the first stage of surgery, which leaves only the hypertrophied segments IV ± I as the liver remnant after completion of the surgical treatment pathway.

The current existing literature covering safety and efficacy of a right hepatic PVE after a complete left lateral hepatic resection is, however, scarce, with most previous studies being small and heterogenous regarding the types of embolic agents and the extent of the left hepatic surgery during the first stage of the pathway (5 –8).

Therefore, the aim of the present study was to describe the safety and efficacy of percutaneous PVE with n-buthylcyanoacrylat via an ipsilateral approach in the setting of a two-stage hepatectomy pathway with preservation of segments IV ± I as the future liver remnant.

Material and Methods

Patients

The present study was approved by the institutional review board and the need to obtain informed consent was waived due to the retrospective nature of the study.

Electronic medical records of 15 consecutive patients (8 men, 7 women) with bilobar liver metastases from colorectal cancer (n = 14) or uveal melanoma (n = 1), who underwent PVE as part of a planned major two-stage hepatectomy at our institution between March 2012 and October 2019 were reviewed. All patients had liver-only disease, i.e. they were considered to be suitable candidates for a curative treatment approach by means of extensive liver resection. Only patients who were treated according to the following two-stage hepatectomy pathway were included: all patients initially underwent left-lateral liver resection, i.e. complete resection of liver segments II and III (first stage of surgery), before undergoing PVE of the portal vein branches of liver segments V–VIII about 1–2 weeks later. After a 3–6-week time interval to allow for hypertrophy of the FLR, the patients underwent right hemihepatectomy, i.e. resection of segments V–VIII (second stage of surgery). The hypertrophied liver segments IV ± I were supposed to remain as the liver remnant in all patients. All patients who received merely simple atypical or incomplete resections of liver segments II and III as first part of a two-stage hepatectomy were excluded.

PVE technique

PVE of the right portal veins (segments V–VIII) was performed via an ipsilateral approach in all cases. All procedures were performed by one of four different interventional radiologists with at least six years of experience in oncologic interventions. A peripheral intrahepatic right portal vein branch was punctured via an intercostal approach under combined fluoroscopic and ultrasound guidance using a 22-G Chiba needle. A 6-Fr sheath was advanced into the main stem of the portal vein. Subsequent catheterization of the right portal vein branches was performed using a 5-Fr Sidewinder catheter (Merit Medical, South Jordan, UT, USA) and a 2.4-Fr Microcatheter (Renegade; Boston Scientific, Marlborough, MA, USA). Embolization of the right liver (segments V–VIII) was performed using the same embolic agent in all cases: a 1:3 mixture of N-buthylcyanoacrylat (NBCA) (Histoacryl, Braun, Germany) and iodized oil (Lipiodol, Guerbet, France). After successful embolization of all right portal vein branches, the puncture tract was sealed using the same glue mixture during removal of the sheath and catheters. Patients were usually discharged one day after PVE.

Assessment of safety

A retrospective review of electronic medical records and all angiographic images and postinterventional computed tomography (CT) examinations was performed to investigate the occurrence of adverse events during or after the PVE, and all complications were classified according to the CIRSE Classification System for Complications (9). To assess the impact of the PVE on the liver function, laboratory liver function markers (albumin, bilirubin, AST, ALT) before PVE, one day after PVE, and 3–4 weeks later were reviewed and noted.

Assessment of efficacy

All patients received a baseline contrast-enhanced CT scan within three weeks before PVE, i.e. this baseline examination was also before the first stage of hepatectomy. All CT examinations were acquired on a 192-slice scanner (Somatom Force, Siemens, Forchheim, Germany) using a standard dual-phasic protocol (arterial and venous phase). Three to six weeks after PVE, all patients underwent a follow-up CT for assessment of hypertrophy of the FLR. The total liver volume (TLV) and absolute volume of the FLR, i.e. liver segments IV and I, were measured on the baseline and follow-up CTs of each patient. Volume measurements were performed on venous phase images with a slice thickness of 5 mm using a dedicated software tool (IntelliSpace Portal CT Liver Analysis application, Philips, Eindhoven, The Netherlands). From these absolute measurements, the standardized functional liver remnant (sFLR) ratio and the degree of hypertrophy (DH, the relative increase of the percentage of the sFLR) were calculated using the following formulas:

{sFLR}_{baseline} = \frac{V_{{S I V + I}_{base l ine}}}{{TLV}_{baseline}}

{sFLR}_{postPVE} = \frac{V_{{S I V + I}_{postPVE}}}{{TLV}_{baseline}}

D H = {sFLR}_{postPVE} - {sFLR}_{prePVE}

Current consensus guidelines recommend that in patients with a history of neoadjuvant chemotherapy treatment, an sFLR ratio ≥30% is safe to avoid liver insufficiency after resection (10). However, since this value appears quite conservative and is derived from extrapolation of single-stage resections, it may not be applicable in the setting of a multistaged resection. Therefore, at our institution all patients with a history of chemotherapy with an sFLR ratio > 25% and normal liver function were considered to be suitable surgical candidates. For those patients without a history of chemotherapy, the threshold for sFLR size was >20%, as per above mentioned consensus guidelines. Whenever these thresholds were not reached 3–6 weeks after PVE, patients would receive systemic chemotherapy to allow more time for hypertrophy of the FLR and these patients would get reevaluated regarding their FLR size after three months.

Data analysis

Further data regarding the interventional procedure, postinterventional follow-up, surgical treatment, and postoperative follow-up (survival) were gathered from the hospital information system and the institutional radiological information system. Technical success of the PVE procedure was defined as complete cessation of portal blood flow in liver segments V–VIII on the final portal venography in combination with patency of the non-target portal venous branches of segment IV and I. International normalized ratio (INR) and serum bilirubin values on the fifth postoperative day were used to assess the occurrence of post-hepatectomy liver failure (PHLF) as defined by Rahbari et al. (11). Categorical data were expressed as numbers (percentages), while quantitative data were expressed as mean ± SD or median and range.

Results

Demographic and clinical data of all patients are shown in Table 1. A sample case illustrating the two-stage resection pathway is shown in Fig. 1.

Table 1.

Patient characteristics.

Total patients	n = 15
Mean age (years)	60.4 ± 9.3 (45–77)
Male/Female	8/7
Type of primary tumor (ratio)
Colorectal cancer	14/15 (93.3)
Uveal melanoma	1/15 (6.7)
Neoadjuvant chemotherapy (ratio)	13/15 (86.7)
Days between left hepatectomy and PVE	11 (6–342)*

Values are given as n (%), mean ± SD (range), or median (range).

*PVE was performed within two weeks after left lateral resection in all but one patient. In this one patient, small metastases in segment IV were detected intraoperatively during left lateral resection. This patient therefore was considered unsuitable to complete the planned pathway and therefore underwent extensive systemic chemotherapy. After almost one year with excellent response to systemic treatment, this patient was re-evaluated and considered to be a suitable candidate again for completion of the staged hepatectomy pathway with curative intent.

PVE, portal vein embolization.

Fig. 1.

Sample case illustrating the typical therapeutic pathway. (a) Axial contrast-enhanced CT image at the level of the right portal vein showing bilobar liver metastases (white arrows) in segments III, V, and VI in a patient with rectal cancer. The white dotted line indicates the part of the liver that will be removed during the initial left lateral liver resection. The black dotted line indicates the FLR_baseline, consisting of segments I and IV. (b) Fluoroscopy image after complete embolization of the portal veins of segments V–VIII with a histoacryl/lipiodol mixture (white arrow) with portal vein branches of segments IV and I remaining patent. Black arrow demarks the stump of the main left portal vein branch after left lateral resection. Adjacent operation clips are visible. (c) Axial contrast-enhanced CT image at the level of the right portal vein four weeks after PVE. This patient had an FLR_baseline of 202.9 mL and a TLV of 1621.5 mL, resulting in a sFLR_baseline of 12.5%. On the follow-up CT, the patient had a FLR_post-PVE of 348.7 mL, resulting in a sFLR_post-PVE of 28.0%, yielding a DH of 15.0%. The white dotted line indicates the part of the liver that will be removed during the planned right hepatectomy, consisting of segments V–VIII. (d) Axial contrast-enhanced CT image at the level of the left portal vein, one year after the right hepatectomy, showing an even increased hypertrophy of the FLR_post-PVE. CT, computed tomography; DH, degree of hypertrophy; FLR, future liver remnant; PVE, portal vein embolization; TLV, total liver volume.

All but two patients—both with colorectal liver metastases—received neoadjuvant chemotherapy and all patients had non-cirrhotic liver parenchyma. The PVE procedure was technically successful without any evidence of non-target embolization in all 15 cases (100%).

Safety

One grade 3 complication occurred after PVE: one of the patients developed a partial, non-occlusive thrombosis of the main portal vein, which was incidentally detected on the follow-up CT after PVE and treated with anticoagulation (low-molecular-weight heparin). The patient was asymptomatic and had normal laboratory liver function values at all times. The thrombus resolved completely within the next two months and the patient successfully underwent right hemihepatectomy (Fig. 2). No other peri- or postinterventional complications occurred in any of the remaining patients.

Fig. 2.

Case of a partial thrombosis of the main portal vein after the PVE procedure. (a) Axial CT image in portal veinous contrast phase demonstrating a marginal thrombus on the posterior wall of the extrahepatic main stem of the portal vein four weeks after PVE (white arrow). This patient did not develop any signs of portal hypertension and achieved sufficient hypertrophy to successfully undergo a subsequent right hemihepatectomy. Note the operation clips in liver segment IVb, after a wedge resection that took place at the same time as the left hemihepatectomy. (b) Axial CT image in the portal phase, acquired two months after the first image, shortly after right hepatectomy. The main portal vein is patent, the thrombus is completely resolved. CT, computed tomography; PVE, portal vein embolization.

Bilirubin levels were normal in all patients before and after PVE as well as four weeks later. Albumin levels were within normal limits in all but one patient at all timepoints and none of the patients showed a drop-off in serum albumin levels after PVE. One patient had a serum albumin level of 3.3 g/dL before PVE, but nevertheless had no signs or symptoms of hepatic dysfunction before or after PVE and subsequent right hemihepatectomy. Nearly all patients developed a transient increase in AST and ALT levels one day after PVE (up to 2158 U/L), but these values returned to pre-interventional levels four weeks after PVE in all but one patient (Table 3). None of the patients developed signs or symptoms of postinterventional liver failure after the PVE.

Efficacy

The mean absolute volume of the FLR before PVE (FLR_baseline) was 260.9 mL, the mean absolute volume of the FLR after PVE (FLR_post-PVE) was 442.5 mL. Percentagewise, the mean sFLR ratio before PVE was 15.7% and the mean sFLR ratio after PVE was 26.9%. The mean DH was therefore 11.3%, which corresponded to an average increase of the FLR volume by 79.8%. (Table 2)

Table 2.

Future liver remnant and standardized future liver remnant before and after right PVE.

FLR_baseline (mL)	260.9 ± 103.9 (80.9–444.6)
FLR_post-PVE (mL)	442.5 ± 142.4 (121.2–646.5)
FLR_change (mL)	181.6 ± 92.2 (40.3–381.7)
sFLR_baseline (%)	15.7 ± 4.3 (7.4–23.8)
sFLR_post-PVE (%)	26.9 ± 6.4 (11.0–36.8)
DH (%)	11.3 ± 5.8 (3.6–25.3)

Values are given as mean ± SD (range).

DH, degree of hypertrophy; FLR, future liver remnant; PVE, portal vein embolization; sFLR, standardized future liver remnant.

Table 3.

Laboratory liver function markers.

	1 day before PVE	1 day after PVE	Follow-up (3–4 weeks after PVE)	Reference range
Bilirubin (mg/dL)	0.4 ± 0.06 (0.1–1.1)	0.5 ± 0.07 (0.2–1.0)	0.4 ± 0.04 (0.2–0.9)	<1.2
Albumin (g/dL)	3.8 ± 0.12 (3.3–4.4)	3.8 ± 0.34 (3.2–4.4)	4.2 ± 0.56 (3.1–4.8)	3.5–5.2
AST (U/L)	32.3 ± 11.6 (17–64)	509.1 ± 588.9 (25–2158)	40.8 ± 19.9 (23–104)	<35
ALT (U/L)	53.6 ± 42.9 (9–184)	395.6 ± 348.2 (36–1030)	37.0 ± 26.1 (7–108)	<35

ALT, alanine transaminase; AST, aspartate transaminase; PVE, portal vein embolization.

In 11 of 15 patients (73.3%) the goal of a sFLR_post-PVE ≥ 25% was achieved within 3–6 weeks after PVE. Three of the remaining four patients had a sFLR_post-PVE in the range of 20%–25%, and these patients therefore received additional cycles of chemotherapy before receiving another CT scan to re-evaluate the size of their FLR 3–6 months later. In all three patients, the FLR eventually surpassed the required size threshold within six months.

One patient did not develop sufficient hypertrophy of the FLR, with a sFLR_post-PVE of only 11%. This patient’s sFLR_baseline was only 8% and was further reduced after a microwave ablation of a metastasis in the transition area between segments VIII and IVa. Therefore, this was the only patient who could not proceed to the second stage of surgery due to insufficient hypertrophy of the FLR.

Clinical outcome

Of the 15 patients, 9 (60.0%) eventually completed the planned therapeutic pathway and underwent right hemihepatectomy after a median of 40 days (range = 25–190 days) after PVE. A total of six patients did not have second-stage surgery: one due to insufficient hypertrophy as mentioned above, and five due to new metastases in the FLR after PVE.

On the fifth postoperative day or later, the INR was within normal limits in all nine patients who completed the second stage of surgery (mean = 1.11; range = 0.95–1.38). Of nine patients, 5 (55.6%) still had transient mild hyperbilirubinemia on the fifth postoperative day, which slowly returned to normal limits over the further course of the follow-up; the mean serum bilirubin was 1.44 (range = 0.49–2.7). Therefore, none of the nine patients developed PHLF as defined by Shabari et al. (11). All patients receiving second-stage surgery were able to leave the hospital in good health and the median overall survival of these nine patients was 26.9 months (range = 13–38 months) after the second stage of surgery.

Discussion

PVE of the right portal vein was safe in this cohort of patients who had previously undergone complete resection of liver segments II and III as part of a major two-stage hepatectomy. Almost all patients also developed sufficient hypertrophy of the FLR (liver segments IV ± I) after PVE, although around one-third of patients did not complete the intended treatment pathway due to the occurrence of new metastases in the FLR before the second-stage surgery.

Percutaneous PVE is generally recognized to be a safe and effective intervention in the setting of a single-stage hepatectomy (12), as well as in the setting of a staged hepatectomy with varying degrees of minor left hepatic resections (5 –7,13). However, we are aware of only one study that focused on the safety and efficacy of PVE in the specific setting of a major two-stage hepatectomy, i.e. PVE in preparation for a right hemihepatectomy after prior complete resection of the left-lateral liver segments with the aim of retaining only liver segments IV and I as the future liver remnant (8). In this study by Cassinotto et al. (8), however, PVE was performed with a wide variety of embolic agents and a significant number of adverse events were observed, most notably portal thrombotic events in the FLR or the main portal vein in 20% of patients.

In the present study, all patients were embolized with the same liquid embolic agent (n-buthylcyanoacrylat) and the rate of adverse events was very low as only one patient (6.7%) developed a partial thrombosis of the main portal vein. This partial thrombosis was successfully treated by anticoagulation for two months and had no effect on the clinical outcome of the patient. Since a complete thrombosis of the main portal vein is a serious complication that most likely will result in the patient becoming unsuitable for a right hemihepatectomy, it is important to note that this complication is rare, even when performing a PVE in the setting of a major staged hepatectomy pathway. Otherwise, most patients showed mild and transient elevations of laboratory liver function values, but the PVE did not seem to permanently impair the liver function in any of the patients.

In this study, 5 of 15 patients (33%) did not proceed with the second stage of surgery due to progressive disease in the FLR. One reason for this may be that due to the long inclusion period, not all patients received an MRI with hepatobiliary contrast agent (EOB-MRI) before PVE/surgery. Since EOB-MRI has superior sensitivity for detection of small metastases in the FLR compared to contrast-enhanced CT, it would likely have aided in better patient selection. Nevertheless, in the single-stage setting, i.e. patients treated with PVE in preparation for right hemihepatectomy without prior left-sided liver resection, approximately 30% of patients do not proceed to surgery, mostly due to disease progression (14). Considering that the patient cohort in this study had a high bilobar tumor burden, the eventual result of 60.0% of patients completing the second stage of surgery is far from dissatisfactory.

The one patient with insufficient hypertrophy already had a very small baseline FLR. It is known that the presence of portal hypertension negatively correlates with hypertrophy (15,16). A plausible explanation would therefore be that in this patient, the small residual portal vessel volume led to a high portal venous pressure. A possible approach for these patients with a very small sFLR_baseline could therefore be a multistage PVE, i.e. embolization of the anteromedial and posterolateral right portal vein branches in different sessions in order to create a slower, more gradual increase in portal pressure. Additionally, combined portal and hepatic vein embolization or “associating liver partition with portal vein ligation for staged hepatectomy” (ALPPS) are other options for patients who are at risk for insufficient hypertrophy (17). In fact, results of a recent study by Sparrelid et al. (18) suggest that a lower sFLR_baseline is associated with a significant higher need of rescue ALPPS after PVE.

Expert panels have consensually established recommendations regarding the size of the FLR: its volume should be >20% of the TLV in patients with an otherwise normal liver, >30% in patients who, prior to surgery, received neoadjuvant chemotherapy, and >40% in patients with hepatic cirrhosis/fibrosis (10,19,20). However, in the present study, only 6 of 15 patients (40.0%) (2/2 patients without neoadjuvant chemotherapy and 4/13 patients with prior chemotherapy treatment) met these criteria. At our institution, patients with an FLR > 25% and normal liver function tests were considered eligible to undergo right hepatectomy and none of the patients that eventually completed the second stage of surgery developed PHLF (11).

The present study has some limitations. First, this was a retrospective observational study with a small number of patients and therefore the statistical power is very limited. In addition, the inclusion period is considerably long and improvements in diagnostics such as the increasing use of EOB-MRI may have changed the patient selection during this period. Additionally, the heterogeneity of the patient cohort, e.g. regarding the type of neoadjuvant treatment, further limits the general applicability of the results of this study. However, given the paucity of data regarding the use of PVE in the specific setting of a major two-stage hepatectomy, the results of the present study—very low complication rates and good effectiveness—nevertheless provide valuable starting points for larger future studies.

In conclusion, PVE in the specific setting of a major two-stage hepatectomy with preservation of liver segments IV and I as the FLR is a safe and effective procedure. However, further studies are necessary to validate these results in a larger patient cohort, to determine safe threshold values for the size of the FLR after PVE, and to determine whether there is a minimum requirement for the size of the FLR before PVE in order to have a realistic chance to reach an adequate size of the FLR after PVE.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Vincent Van den Bosch

Markus Zimmermann

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Safety and efficacy of right portal vein embolization in patients with prior left lateral liver resection

Abstract

Background

Purpose

Material and Methods

Results

Conclusion

Keywords

Introduction

Material and Methods

Patients

PVE technique

Assessment of safety

Assessment of efficacy

Data analysis

Results

Safety

Efficacy

Clinical outcome

Discussion

Footnotes

Declaration of conflicting interests

Funding

ORCID iDs

References

Safety and efficacy of right portal vein embolization in patients with prior left lateral liver resection