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HPB : The Official Journal of the International Hepato Pancreato Biliary Association logoLink to HPB : The Official Journal of the International Hepato Pancreato Biliary Association
. 2015 Feb 28;17(6):529–535. doi: 10.1111/hpb.12397

Tumour growth after portal vein embolization with pre-procedural chemotherapy for colorectal liver metastases

Lidewij Spelt 1, Ernesto Sparrelid 2, Bengt Isaksson 2, Roland G Andersson 1, Christian Sturesson 1,✉
PMCID: PMC4430784  PMID: 25726854

Abstract

Background

For resection of colorectal cancer (CRC) liver metastases, pre-operative portal vein embolization (PVE) is used to increase the size of the future liver remnant (FLR) prior to advanced liver resection when indicated. PVE is speculated to cause tumour progression, but only a limited number of studies have analysed tumour growth after PVE in the context of pre-procedural chemotherapy, which was the aim of this retrospective study.

Methods

Patients treated with stabilizing chemotherapy and PVE before liver resection for CRC metastases were included. Tumour progression according to RECIST guidelines and a change in tumour volume was analysed on computed tomography (CT) scans prior to chemotherapy, before PVE and after PVE, respectively.

Results

Thirty-four patients were included, of whom 23 had bilobar disease. Of tumours in the embolized lobe, 3/34 showed progression after PVE as compared with 3/23 in the non-embolized lobe (P = 0.677). A decrease in tumour volume of 16% and 11% was noted in the embolized and non-embolized lobe, respectively (P = 0.368). Patients were off chemotherapy in a median of 16 days before PVE. There was a linear correlation between the growth of tumours and time between the end of chemotherapy and PVE (r = 0.25, P = 0.0005).

Conclusion

The rate of progression of CRC liver metastases after PVE and pre-procedural chemotherapy was lower in the present study as compared with previous reports. This applies to tumours in both the embolized and non-embolized lobes and is associated with keeping the time between the end of chemotherapy and PVE short.

Introduction

Within 3 years after the diagnosis of colorectal cancer (CRC), 29% of patients will have developed liver metastases.1 One of the criteria for resectability of CRC liver metastases is that a sufficient future liver remnant (FLR) remains after resection.2 Pre-operative portal vein embolization (PVE) can generally increase the FLR to 30% or more of the total functional liver volume (tFLV),3,4 by causing atrophy of the embolized lobe and hypertrophy of the contralateral lobe.5,6 In addition, chemotherapy is often used before PVE, either for neoadjuvant or downstaging purposes.

The risk for tumour progression in the neoadjuvant setting with modern chemotherapeutic agents is low, around 5–7%.7,8 Tumour progression during chemotherapy is considered at least a relative contraindication to advanced liver resection.9,10 For CRC liver metastases, there have been concerns about a tumour growth-promoting effect by PVE.11,12 However, only a few studies have considered tumour growth in the FLR with special reference to chemotherapy.13,14

Objective

The aim of this study was to investigate the growth of liver metastases after stabilization of the disease by chemotherapy before PVE. In addition, this study aims to investigate if tumour growth is different between tumours located in the embolized lobe and those in the non-embolized liver lobe. If pre-procedural chemotherapy can arrest tumour growth in the FLR between PVE and resection, this could have an impact on the indications for a two-stage hepatectomy (TSH).

Patients and methods

Patients

Between 2005 and 2013, all patients treated with PVE at Skåne University Hospital, Lund, Sweden, and between 2004 and 2010 at Karolinska University Hospital, Stockholm, Sweden, were identified. Of those, patients undergoing a PVE prior to a planned resection of CRC liver metastases were selected, including only patients who were treated with chemotherapy within 2 months prior to PVE and achieving at least tumour stabilization according to RECIST 1.1 guidelines.15 Exclusion criteria were a previous liver resection or ablation (including TSH), the absence of a follow-up abdominal computed tomography (CT) scan within 2 months after PVE or absence of a CT scan within 3 months prior to PVE.

Baseline characteristics on patient, disease and treatment specifics were collected, such as age, body mass index (BMI), occurrence of synchronous or metachronous metastases, the number of liver metastases, size of the largest metastasis and chemotherapy regimens. Synchronous metastatic disease was defined as metastases occurring within 6 months after diagnosis of the colorectal cancer.

Abdominal CT scans were collected and studied on all patients, using the images from before the start of chemotherapy (CTpre-chemo), the most recent images before PVE, but not longer than 3 months prior to PVE (CTpre-PVE), and follow-up CT after PVE, at the latest 2 months after PVE (CTpost-PVE).

Liver metastases were deemed bilobar or unilobar according to their locations. Tumours stretching across the Cantlie's line were defined as situated in either the left or right lobe according to where its geometrical centre was located. tFLV was calculated by subtracting the total tumour volume from the total liver volume. In all patients, FLR was calculated for a potential extended right-sided hemihepatectomy, therefore calculating the volume of segments I–III according to the segments as described by Couinaud.16

Information on eventual liver resection was collected, including type of resection and whether a resection was radical based on pathology. Resections were classified either as a right-sided hemihepatectomy, i.e. segments V–VIII or an extended right-sided hemihepatectomy, i.e. segments IV-VIII. Both resection types were with or without additional atypical resections in remaining segments.

Outcome measures

Using RECIST 1.1 guidelines15 two target lesions were selected in the right and two in the left lobe, or fewer lesions in case of singular metastases or unilobar disease. By measuring the maximum diameter of the target lesions, tumour growth over time was noted between CTpre-chemo and CTpre-PVE, representing the effect of chemotherapy, as well as between CTpre-PVE and CTpost-PVE, representing tumour growth after PVE. For the right and the left lobe separately, the development between two CT scans was classified as complete remission (CR), partial regress (PR), stable disease (SD) or progressive disease (PD).

Also, the total volume of all metastases in the right and left lobe, respectively, was calculated in all three CT scans, by outlining the tumours in each transversal image to calculate the area, adding up all calculated areas from the different slides and then multiplying by slide thickness, which was 5 mm or less. Again, larger tumours occupying both the left and the right liver lobe were determined to have their centre in one lobe and were thus counted in one lobe only. Successively, the change in tumour volume between CTpre-chemo and CTpre-PVE was calculated by dividing the tumour volume pre-PVE by the tumour volume pre-chemo and multiplying by 100%. Hence, values between 0 and 100 represent tumour shrinkage whereas values over 100 represent tumour growth. The same was done to analyse the change in tumour volume between CTpre-PVE and CTpost-PVE.

Data collection and statistical evaluation

Baseline patient characteristics were collected retrospectively by reviewing patients' charts. Liver and tumour volumes were calculated from CT transversal plane images.17,18 Analyses were carried out to compare tumour progress between the right and the left lobe, thereby comparing tumour progress between the embolized and non-embolized liver lobe. Data on the right-sided tumors were compared with data on the left-sided tumours within the entire population of both patients with bilobar disease, as well as those with unilobar metastases.

Statistical analysis was performed using SPSS software (IBM SPSS Statistics for Windows, Version 21.0, IBM Corp., Armonk, NY, USA).

Median values (range) describe continuous variables whereas frequencies were calculated for categorical variables. RECIST classification was compared between groups and specifically the percentage of cases that showed progressive disease. Fisher's Exact Test was used to test for statistical significance. The tumour volume change, as described above, was compared between groups using the Mann–Whitney U-test. Correlation between the tumour growth rate and time between the end of chemotherapy and the time of PVE was calculated using linear regression analysis and computing a Pearson's correlation coefficient, r. P-values of <0.05 were considered to represent statistical significance.

The study was approved by the local human ethical committee at Lund University, Lund and Karolinska University Hospital, Stockholm.

Results

Patients

A total of 34 CRC patients, subjected to PVE prior to planned resection of liver metastases, were included for analysis. Patient characteristics are shown in Table1.

Table 1.

Patient characteristics

Characteristics (n = 34) Value range or %
Median age (years) 66 49–83
Male gender 21 62%
Median BMI 25 20–36
Synchronous metastases 28 82%
Median number of liver metastases 4 1–17
Median size of largest metastasis (mm) 50 15–192
Chemotherapy before PVE
 Oxaliplatin based 23 68%
 Irinotecan based 9 27%
 Both successively 1 3%
 Missing value 1 3%
Median number of chemotherapy cycles 7 1–27
Targeted therapy 16 47%
Median time between chemotherapy and PVE (days) 16 2–54
Median time between CTpre-chemo and CTpre-PVE (days) 142 22–546
Median time between CTpre-PVE and PVE (days) 34 1–92
Median time between PVE and CTpost-PVE (days) 29 18–43
Median tFLV (ml) 1544 1130–2524
Median FLR before PVE (ml) 285 133–796
Median FLR% before PVE 19 10–32
Median FLR after PVE (ml) 448 197–1032
Median FLR% after PVE 29 13–52
Liver resection
 Right-sided hemih epatectomy 9 26%
 Extended right-sided hemihepatectomy 17 50%
 No resection 8 24%
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BMI, body mass index; PVE, portal vein embolisation; CTpre-chemo, CT before chemotherapy; CTpre-PVE, CT before PVE; CTpost-PVE, CT after PVE; tFLV, total functional liver volume; FLR, future liver remnant.

A total of 23 patients had bilobar liver metastases, according to the definition described above.

All patients received chemotherapy prior to PVE. In approximately two-thirds of the patients, oxaliplatin-based therapy was applied, whereas most others were treated with irinotecan-based therapy. The median number of administered cycles was seven and about half of all patients also received targeted therapy, such as bevacizumab, cetuximab, panitumumab and erlotinib.

PVE was carried out as described previously17 using the embolizing agents polyvinyl alcohol particles in 30 patients and with n-butyl-2-cyanoacrylate in the remaining four cases. All patients underwent ipsilateral embolization of Couinaud's segments 5–8. Segment 4 is not routinely embolized in our institutions, and no included patient had embolization of segment 4.

Seventeen patients were eventually operated with an extended right-sided hemihepatectomy, whereas a right-sided hemihepatectomy was performed in nine patients. Another eight patients were not resected owing to extrahepatic tumour progress (3 patients), insufficient growth of the lateral segment after PVE (3 patients), strong progress of metastases in both liver lobes (1 patient) and one new unresectable metastasis detected peri-operatively in the FLR (1 patient).

Of the total of 26 resections performed, 23 were deemed radical on microscopic pathological analysis. Figs1 and 2 show an example of a patient with multiple tumours in the FLR treated with chemotherapy and PVE.

Figure 1.

Figure 1

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(a) Example of a patient with multiple metachronous liver metastases from rectal cancer involving all liver segments except the caudate lobe. (b) After nine cycles of oxaliplatin-based chemotherapy, there was a significant tumour regression. (c) After portal vein embolization. Embolization material is shown in the right portal veins

Figure 2.

Figure 2

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The patient from Fig.1 was operated with an extended right-sided hepatectomy plus five local resections in the lateral segment 4 weeks after portal vein embolization. Microscopic examination could reveal in total 10 metastases all with clear resection margins

Tumour progress

Tumour progress in the right lobe was analysed for all patients (n = 34) and tumour progress in the left lobe was analysed in patients with bilobar disease (n = 23). Results on tumour progress, comparing metastases in the embolized lobe to those in the non-embolized lobe, are shown in Table2. There was no difference in tumour growth between the embolized and non-embolized liver lobe after embolization (Table2). There was a linear correlation between the volumetric tumour growth and time between the end of chemotherapy and PVE (r = 0.25, P = 0.0005).

Table 2.

Liver tumour growth

Embolized lobe Non-embolized lobe P-value
n = 34 range or % n = 23 range or %
RECIST comparing CTpre-PVE to CTpre-chemoa
 CR 0 0% 3 14%
 PR 17 52% 11 50%
 SD 16 49% 8 36%
 PD 0 0% 0 0%
RECIST comparing CTpost-PVE to CTpre-PVE
 CR 1 3% 5 22%
 PR 5 15% 1 4%
 SD 25 74% 14 61%
 PD 3 9% 3 13%
PD after PVE 3 9% 3 13% 0.677
RECIST comparing CTpost-PVE to CTpre-chemoa
 CR 1 3% 9 41%
 PR 19 58% 6 27%
 SD 10 30% 4 18%
 PD 3 9% 3 14%
PD after both chemotherapy and PVEa 3 9% 3 14% 0.674
Median tumour volume CTpre-chemo (ml) 67 3–2185 7 1–125
Median tumour volume CTpre-PVE (ml) 22 1–712 2 0–152
Median tumour volume CTpost-PVE (ml) 17 0–443 1 0–178
Median tumour volume change during chemotherapy (% of previous volume) 40 3–201 26 0–122 0.268
Median tumour volume change after PVE (% of previous volume) 84 0–250 89 0–160 0.368
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a

n = 33 in the embolized lobe and n = 22 in the non-embolized lobe because one patient had no CTpre-chemo as chemotherapy was started right before PVE.

PVE, portal vein embolization; CTpre-chemo, CT before chemotherapy; CTpre-PVE, CT before PVE; CTpost-PVE, CT after PVE; CR, complete remission; PR, partial regress; SD, stabile disease; PD, progressive disease.

In 9/23 of patients with left lobe disease, tumours disappeared on the CT images after PVE. Six of these patients did show remaining sub-centimeter tumour burden in the left liver lobe intra-operatively as imaged by contrast-enhanced ultrasonography. Of those, five were treated with resection and one was deemed unresectable because of liver tumour progress. Two patients showed no evidence of a left-sided tumour intra-operatively, and thus no resection was performed on the left lobe. The ninth patient was never operated on owing to extrahepatic tumour progress.

Three cases of progressive liver disease were noted after PVE of tumours in the embolized as well as non-embolized lobe, representing 3/34 and 3/23 of cases, respectively (P = 0.677).

Discussion

This study shows a lower probability of progressive liver disease after PVE as compared with previous reports. If there is at least tumour stabilization on pre-embolization chemotherapy, progressive liver disease using RECIST criteria was found in the right liver lobe in 3/34 of patients, and 3/23 of patients with pre-embolization tumour burden in the left lobe. This translated into 2/34 patients not resected because of liver tumour progress. A tumour response after PVE has previously been investigated to a limited extent, and only one previous study has evaluated tumour response after PVE according to RECIST criteria.13 In the study by Fischer et al.,13 a rate of tumour progression of 34% after PVE was reported. However, it is difficult to compare these results as, in the above study, no details are mentioned about chemotherapy before PVE.

Using the measurement of tumour volume, the results of the present study differ from previous studies in that we found a decrease in tumour volume after PVE of 16% in right-sided tumors and of 11% in left-sided tumors. Simoneau et al.19 reported a large cohort of patients undergoing PVE after chemotherapy and they found a significant tumour growth after PVE. There was, however, a difference in the time interval from the ending of chemotherapy to PVE of 4 weeks in the above study, as compared with 16 days in the present study. The study by Pamecha et al.12 also reported an increase in tumour diameter after PVE. Although all patients were reported to have received pre-PVE chemotherapy, the details were not reported including chemotherapy response or time between the ending of chemotherapy and PVE, making comparison with the present study difficult.

Tumour regression after chemotherapy and PVE has, however, been reported previously. In the study by Pommier et al.14 tumour shrinkage of 4% in the right lobe and 9% in the left lobe was observed in patients with a ‘fast response’ to chemotherapy before PVE. The time interval between chemotherapy and PVE was also longer in that study as compared with the present study, which could, again, explain the differences between studies. Not very surprisingly, although not previously analysed, the present study showed that the longer the time between the end of chemotherapy and PVE, the greater the tumour growth.

The presented findings could potentially, if corroborated in larger studies, have important consequences for the operative strategy of the individual patient. With a low probability for tumour progression in the FLR after PVE, some patients today scheduled for a TSH with the intention of clearing the FLR from the tumour during the first-stage operation, could instead be managed by percutaneous PVE and a subsequent one-stage operation. Even patients with multiple tumours in the FLR can be managed in this way (Fig.1). A key factor for this, to be successful, seems to be a short interval between the end of chemotherapy and PVE. TSH is used in the case of bilobar disease deemed not resectable through a single operation because of a too small liver remnant. In TSH, a common strategy is to clear the future liver remnant from the tumour at the first operation combined with PVE.20

In TSH, the percentage of patients eventually undergoing the two planned operations has been evaluated to be 77% in a recent review.21 After PVE a curative resection rate of 60–82% has been reported.22 In the present study, the curative resection rate was 76%. Three out of 34 patients were not resected because of insufficient hypertrophy of the FLR. Recent data suggest that by using the ALPPS procedure, this number can be decreased.23

In a high proportion of patients (41%) with an initial tumour in the left liver lobe, the tumour disappeared on CT images after chemotherapy and PVE. However, disappearing liver metastases on cross-sectional imaging does not mean a cure in the majority of cases.24 Intra-operative contrast-enhanced ultrasonography helps to identify many of these lesions.25 Accordingly, in most patients with disappearing left-sided lesions on CT imaging, tumours were still identified in the left lobe intra-operatively by contrast-enhanced ultrasound. In the two cases without intra-operatively detectable tumours in the FLR, no resection was undertaken. How to handle the issue of intra-operatively disappearing liver metastases is somewhat controversial.24 In the study by Arita et al. out of seven unresected disappearing liver metastases not identifiable by intra-operative contrast-enhanced ultrasound, three recurred during follow-up.25

It has been suggested that chemotherapy before PVE will limit liver regeneration. Prolonged pre-PVE chemotherapy has been associated with reduced volume gain in the non-embolized lobe,17,26 but other studies have failed to show any influence of chemotherapy on regeneration.27,28 In the present study of right-sided PVE, the median FLR increased from 19% to 29%, which is similar, although somewhat lower, to what has been reported in previous studies.26,27

There have been few studies on the effect of the type of embolization material on growth of the future liver remnant. In the present study polyvinyl alcohol particles were used in most cases, whilst both a study on pigs29 and later a retrospective analysis of portal vein embolization in humans30 have shown a superior effect of n-butyl-2-cyanoacrylate as compared to particles.

The patients in this study all received pre-procedural chemotherapy, and since in practice patients who progressed during chemotherapy often were not offered PVE, these results should be interpreted with caution and only generalized to patients responding to chemotherapy. In addition, the number of included patients was limited, warranting further investigations to support the presented results.

There have been concerns about the tumour growth-promoting effect of PVE.11 Previous studies have seldom analysed tumour growth in the non-embolized lobe specifically. As patients undergoing PVE most often are planned to be operated with a right-sided or extended right-sided liver resection, tumour growth in the right lobe would not pose as an important factor as growth in the left lobe when determining resectability. After PVE the arterial blood flow to the embolized lobe increases, described as the hepatic arterial buffer response,31 preserving hepatic viability, whereas the lack of portal venous flow reduces the total blood flow and causes atrophy in this lobe. The non-embolized lobe receives an increased portal venous flow and this together with an increased release of cytokines and growth factors is believed to induce hypertrophy.32 However, relatively the arterial flow to the non-embolized lobe is decreased.31 Although pronounced changes in intrahepatic blood perfusion occur after PVE in addition to the fact that liver metastases are regarded to depend mainly on arterial blood supply,33 this does not seem to affect the growth of tumours in the left and right lobe differently. In the present study, the outcomes suggest that tumour growth in the right and left liver lobe after PVE is comparable. This is in accordance with two previous studies investigating the subject.13,14

Conclusion

This study shows that the rate of liver tumour growth after PVE is lower as compared with previous reports of the condition of tumour stabilization on pre-embolization chemotherapy. It is one of the first studies showing comparable tumour progression in the non-embolized lobe to that in the embolized lobe. A short interval between the end of chemotherapy and PVE is proposed to be essential for the presented results.

Conflict of interest

There are no conflicts of interest to be declared. No financial support was requested or received in the production of this article.

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