British Journal of Radiology (2006) 79, 473-478
© 2006 British Institute of Radiology
doi: 10.1259/bjr/29855825
Portal vein embolisation prior to hepatic resection for colorectal liver metastases and the effects of periprocedure chemotherapy
I K Beal, MBBS, MRCP, FRCR
S Anthony, MBBS, MRCP, FRCR
A Papadopoulou, MBBS, FRCR
R Hutchins, MBBS, MS, FRCS
G Fusai, FRCS
R Begent, MBBS, MRCS, LRCP
N Davies, MBBS, FRCS, FRCR
J Tibballs, MRCP, FRCR, FRANZCR
and
B Davidson, MBChB, MD, FRCS
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Abstract
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Portal vein embolisation (PVE) is an effective method of increasing future liver remnant (FLR) but may stimulate tumour growth. The effect of periprocedure chemotherapy has not been established. 15 consecutive patients underwent PVE prior to hepatic resection for colorectal liver metastases with a FLR <30% of tumour-free liver (TFL). Liver and tumour volumes pre-PVE and 6 weeks post-PVE were calculated by CT or MRI volumetry and correlated with the periprocedure chemotherapy regimen. PVE increased the FLR from 18±5% of TFL to 27±8% post-PVE (p<0.01). Post-PVE chemotherapy did not prevent hypertrophy of the FLR but the volume increase with chemotherapy (median 89 ml, range 7–149 ml) was significantly reduced (median 135 ml, range 110–254 ml without chemotherapy) (p = 0.016). Tumour volume (TV) decreased in those receiving post-PVE chemotherapy (median TV decrease 8 ml, range –77 ml to +450 ml) and increased without chemotherapy (median TV increase 39 ml, range –58 ml to +239 ml). Of the 15 patients, eight underwent resection; four were not resected due to disease progression and three due to insufficient hypertrophy of the FLR. PVE increased the FLR by an average of 9% allowing resection in 50% of patients. Periprocedure chemotherapy did not prevent but did reduce hypertrophy. A trend towards tumour regression was observed.
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Introduction
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Liver resection surgery provides the main possibility of cure in patients with colorectal liver metastases. 5-year survival ranges from 25% to 40% [1–4]. One of the contraindications to hepatic resection is a small future liver remnant (FLR), which usually arises in patients with congenitally small left lateral segments (II and III) who require an extended right hepatectomy. The small residual liver volume increases the risk of post-operative liver failure. A FLR of 25–30% of non-tumour liver volume has been recommended in patients with normal liver function who are to undergo hepatic resection [3, 5–8], although resections have been carried out successfully with a FLR of <20% [9]. Selective portal vein embolisation (PVE) can produce atrophy of the segments affected by the cancer and compensatory hypertrophy of the contralateral segments [6–8]. The technique was first developed in patients with hilar cholangiocarcinoma where extended right hepatectomy is often required [10]. Although residual liver volumes can be increased, there remains some controversy as to whether this results in improved post-operative outcome [11]. There are now several reports in the literature of PVE applied to patients with colorectal metastases [6–8, 12–14].
One of the potential difficulties with using PVE in metastatic colorectal cancer is that tumour growth may be promoted by PVE. Kokudo and colleagues [15] studied patients undergoing PVE prior to hepatic resection for colorectal liver metastases and found that PVE increased tumour growth in the embolised segments, possibly increasing the incidence of recurrence following liver resection. This also risks tumours becoming unresectable during the interval between PVE and surgery. The growth of liver metastases in the non-embolised segments following PVE has also been shown to be greater than the hypertrophy rate of the normal liver parenchyma [16]. However, in a study of the long term survival following PVE, which included 41 patients with colorectal cancer (CRC) liver metastases, there was no evidence to suggest that patients whose surgery had been made possible by PVE were associated with a poorer long term survival [7].
PVE has also been applied to patients with hepatocellular carcinoma and has been associated with improved operative outcomes as well as long term survival [17, 18].
Chemotherapy has been shown to increase the survival of patients with unresectable liver metastases [1]. Downstaging chemotherapy using Oxaloplatinum and 5-Fluorouracil (5FU) allows some initially unresectable CRC liver metastases to be successfully resected [19–21].
The effect of chemotherapy administered after PVE on the FLR hypertrophy and on the tumour growth in embolised segments, in patients with colorectal liver metastases, has not been investigated. The aim of this study was to assess, first, whether chemotherapy prevents tumour progression between PVE and surgery and, second, whether chemotherapy has a detrimental effect on FLR hypertrophy.
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Patients and methods
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Between September 1999 and December 2002, a single surgical firm in a specialist tertiary referral centre performed right or extended right hepatectomy for colorectal liver metastases in 57 patients. Over this time period, 15 patients who required a right or extended right hepatectomy to resect their metastases were found to have a calculated FLR of less than 30% in an otherwise normal liver (n = 14), or less than 40% (n = 1) in a diseased liver (imaging findings consistent with steatosis). These patients underwent right PVE. Nine patients had synchronous and six metachronous colorectal liver metastases. There were six females and nine males, mean age 65 years (range 52–74 years). The stage of the original tumour was Dukes' B in 4 and Dukes' C in 11. The mean number of metastases was 4 (range 1–11). Three of the 15 patients had undergone resection for metastases in the left lobe of liver prior to PVE. Three patients had minor extension of tumour into segment IV, but no patient had discrete metastases in non-embolised liver.
Chemotherapy
Following initial diagnosis and bowel cancer resection, adjuvant chemotherapy had been carried out in the referring hospital in 11 of the 15 patients (Dukes' C n = 9, Dukes' B n = 2). In all cases this comprised a standard 5FU and folinic acid based protocol. In five of these patients, this had been completed between 6 months and 18 months prior to PVE. In six patients (synchronous metastases n = 5, metachronous metastases n = 1) chemotherapy was continued until 1 month prior to PVE (5FU/FA (n = 2) or 5FU/Oxaliplatin (n = 4)). In the remaining four patients no chemotherapy was administered following bowel cancer resection. Following PVE, eight patients who had already received chemotherapy underwent a further course of 5FU/FA (n = 1), 5FU/FA+oxaliplatin (n = 5) or 5FU/FA+Irinotecan (n = 2).
Two patients who had not previously had chemotherapy were given post-PVE chemotherapy with 5FU/FA +oxaliplatinum (n = 1), 5FU/FA alone (n = 1). Chemotherapy post-PVE was started at 2 weeks post-embolisation and continued for 6 weeks. Three patients who had received chemotherapy post-bowel resection or prior to embolisation did not receive post-PVE chemotherapy.
Two patients remained chemo-naive.
For the purpose of analysis, the patients were grouped into post-PVE chemotherapy (n = 10) and no chemotherapy post-PVE (n = 5).
Volumetric analysis
Liver volume measurements of the whole liver (WL), segments I-III or I-IV (FLR) and tumour (TV) were performed by CT (n = 2) (GE Medical Systems High speed system, Milwaukee, WI) or MRI (n = 13) using Philips Intera 1 T system (Philips, Best, Netherlands). Total functioning liver (TFL) was measured by subtracting TV from WL (Philips Easyvision workstation [release 4.3]) and GE Medical Systems Advantage Windows 2.0 3D Analysis). The technique for measuring volumes by CT has been described elsewhere [5, 7]. Briefly, axial 10 mm sections through the liver were obtained in a single breath-hold. Using a workstation, the areas of TV, WL and FLR were calculated by multiplying the area of each liver image by the slice thickness. The percentage fraction of FLR was calculated: FLR/TFLx100. The measurements performed by MRI involved the same process using the scanner software and a similar technique as described by Caldwell et al [22]. An experienced Hepatobiliary Radiologist performed all measurements. The liver volume measurements were repeated approximately 6 weeks post-PVE.
Portal vein embolisation (PVE)
This was performed by a percutaneous transhepatic approach under general anaesthetic (n = 2) or local anaesthesia and intravenous sedoanalgesia (n = 13). An ultrasound-guided percutaneous portal vein puncture was performed using a Neff set (William Cook Europe A/S, Bjaeverskov, Denmark). A left-sided approach was preferred (n = 9) but when not possible due to the small size of the left lobe a right-sided approach was used (n = 6). 5 Fr or 6 Fr sheaths were introduced and the branches of the right portal vein were embolised sequentially using 4 Fr cobra or sidewinder shaped catheters. Embolisation was performed with alcohol (n = 3) and with/without 500 µm polyvinylalcohol (PVA) particles (William Cook Europe A/S, Bjaeverskov, Denmark) (n = 2/1, respectively) or enbucrilate tissue adhesive (Histoacryl; B Braun Medical AG, Emmenbrucke, Switzerland) and Lipiodol (Guerbet, Roissy, France) at an enbucrilate:Lipiodol ratio of 1:3–1:5 (n = 12). Prior to PVE and daily for 2 days post-PVE, full blood count, clotting profile and liver function tests were measured.
Statistics
Paired and two sample equal variance t-tests were used for statistical analysis. Data are expressed as means (± 1 SD), median values with range and 95% confidence intervals (CIs). p<0.05 was considered significant.
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Results
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Procedure of portal vein embolisation (PVE)
Embolisation of the right portal vein was technically successful in all 15 patients with no immediate complications. The first three patients were embolised with alcohol, which produced severe right upper quadrant pain. Subsequent embolisations were performed using enbucrilate. Post-embolisation, most patients had mild discomfort and low-grade pyrexia, which settled within 24 h. In one patient the 6-week follow-up MRI demonstrated complete portal vein thrombosis. This had not been recognized at the time of the procedure and his clinical course post-PVE was unremarkable. A CT scan showed evidence of enbucrilate:Lipiodol within the proximal left portal vein branch. This patient was not excluded from analysis.
Effect of portal vein embolisation (PVE) on future liver remnant (FLR) volume
Following PVE, there was no significant change in whole liver (WL) volume (median volume pre-PVE 1739 ml (range 1222–3114 ml) to a median volume post-PVE 1631 ml (range 1160–3398 ml)).
Volumetric analysis was carried out prior to PVE and was repeated at a median of 6 weeks post-PVE (range 5–12 weeks). Prior to PVE, the future liver remnant (FLR) volume ranged from 110 ml to 558 ml (median 281 ml), which represented 18(±5)% of the tumour free liver (TFL). The volume was significantly increased following PVE to a FLR range of 245–653 ml (median 404 ml) which represented 27(±8)% of the TFL (p = 0.0089). The mean increase in parenchymal volume was 123 ml, which represented a mean increase in FLR/TFL ratio of 9% (Table 1
). The one patient who had no significant increase in FLR post-PVE was found to have complete portal vein thrombosis.
Effect of portal vein embolisation (PVE) on tumour volume (TV)
The patient group had a median TV of 123 ml (range 29–1147 ml) prior to PVE and 139 ml following PVE (range 10–1597 ml). This difference was not statistically significant (p = 0.71). Of the 15 patients 8 had TV increase and 7 had a TV reduction.
Effect of chemotherapy on liver hypertrophy (future liver remnant (FLR) volume)
The effect of chemotherapy on the hypertrophy of the FLR following PVE is shown in Table 2. There was a significant increase in FLR following PVE in both groups. Patients who received chemotherapy post-PVE (n = 10) had less hypertrophy (increase in FLR volume median = 89 ml, range 7–149 ml) than those who received no chemotherapy post-PVE (n = 5) (increase in FLR volume median = 135 ml, range = 110–254 ml) (p = 0.016). The difference between the means was 70 ml (CIs = 26–115 ml).
The effects of chemotherapy on FLR hypertrophy are illustrated by Figures 1 and 2.
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Figure 1. Change in FLR volume after embolisation in all patients. FLR, future liver remnant volume; Pre, volume prior to PVE; Post, volume after PVE.
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Figure 2. Change in FLR volume after embolisation, according to chemotherapy administered. FLR, future liver remnant volume; Pre, volume prior to PVE; Post, volume after PVE; Post-PVE Chemo, chemotherapy administered after PVE; No post-PVE Chemo, no chemotherapy administered after PVE.
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Effect of chemotherapy on tumour volume (TV)
The effect of chemotherapy on TV following PVE is shown in Table 3.
There was a median TV decrease of 8 ml (range –77 ml to +450 ml) in those receiving post-PVE chemotherapy (n = 10) and a median TV increase of 39 ml (range –58 ml to +239 ml) in those who did not receive post-PVE chemotherapy (p = 0.476). The difference between the means was 58 ml (CIs = –82–198 ml).
Of the three patients who had tumour extending into segment IV, two showed no significant change in TV post-PVE (no post-PVE chemotherapy n = 1, post-PVE chemotherapy n = 1) and one had an overall increase in TV but no significant change of the TV in segment IV (no post-PVE chemotherapy).
The effects of chemotherapy on TV are illustrated by Figure 3.
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Figure 3. Change in tumour volume after embolisation, according to chemotherapy administered. Pre, volume prior to PVE; Post, volume after PVE; Post-PVE Chemo, chemotherapy administered after PVE; No post-PVE Chemo, no chemotherapy administered after PVE.
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Figures 4 and 5 demonstrate typical MRI findings pre-PVE and post-PVE in a patient receiving post-PVE chemotherapy with hypertrophy of the FLR and tumour volume regression.
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Figure 5. Post-embolisation: MRI demonstrates future liver remnant volume (FLR) hypertrophy and tumour volume regression.
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Haematology and biochemistry
Following PVE there were significant but transient increases in the levels of aspartate aminotransferase (AST) in all patients (p = 0.04) and bilirubin in 12 patients (p = 0.0007). An increase in international normalized ratio (INR) was seen in eight patients (p = 0.019) and a decrease in platelets noted in 13 patients (p = 0.002). A transient increase in white cell count (WCC) was noted in 10 patients (p = 0.009).
Surgery following portal vein embolisation (PVE)
Of the 15 patients who underwent PVE who would otherwise have been deemed unresectable due to their small-anticipated FLR, eight proceeded to a right or extended right hepatectomy (53%). Four patients had disease progression on their post-PVE imaging at 6 weeks, which precluded potentially curative resection (extrahepatic disease progression, n = 3 and intrahepatic and extrahepatic disease progression, n = 1). Of these four, two had received post-PVE chemotherapy and two had not received chemotherapy following embolisation. Three patients had insufficient hypertrophy of the FLR. Of the eight who had surgery, there were no operative or post-operative mortalities.
Follow up
Five of the eight patients undergoing surgery remain well and free of local or distant disease at a median of 18 months post-liver resection (range 14–26 months). Two patients developed distant metastatic disease and the third has undergone abdominoperineal resection for local recurrence of a rectal cancer. The three patients who had insufficient hypertrophy of the FLR, including the first patient with complete portal vein thrombosis, underwent palliative chemotherapy. The second of the three patients had an initial FLR of just 7.5% of the TFL. Despite a 123% increase in FLR this was still only 17% of TFL at 6 weeks post-PVE. The third patient had an extremely large tumour prior to embolisation, measuring 1147 ml. The percentage increase in FLR in this patient was just 16%. All three patients were included in the analysis.
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Discussion
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PVE is one of the major recent developments to facilitate resection in patients who would otherwise be contraindicated for liver surgery due to a small-anticipated residual liver volume. Patients in this study all had an anticipated FLR of 30% or less of tumour-free liver and were therefore deemed at risk of post-operative liver failure.
Alcohol was initially used for embolisation, but due to severe alcohol-induced pain requiring general anaesthetic, subsequent embolisations were performed using enbucrilate. This was well tolerated and produced results comparable with that in other series. A literature review has suggested no clear advantage to any specific embolic substance [5].
One patient in the series developed complete portal vein thrombosis. In retrospect, a number of factors may have contributed to this complication. Due to the small left lobe volume, the approach was right-sided and, on completion of embolisation, the catheter was withdrawn so no post-procedure venogram was obtained. This does not cause the complication, but prevented it being recognized at the time of the procedure. Embolisation of the left portal vein may occur if too large a volume of enbucrilate:Lipiodol is injected, i.e. due to operator error. This is not thought to have occurred in this case. Anatomical variants such as portal vein trifurcation, present in this case, may predispose to left portal vein embolisation.
The ability of PVE to increase the FLR was confirmed in the present study with a mean percentage increase in FLR/TFL ratio of 9%. This figure correlates well with the previous reports of 8–13% [5, 7, 8]. 50% of the patients undergoing PVE were able to proceed with potentially curative resection. In the series reported by Elias and colleagues, 88% of patients proceeded to resection [7]. This difference in resection rate may relate to the centre's selection of patients for PVE. In the present series the mean pre-PVE FLR/TFL ratio was 18%. This is lower than the 19–32% reported by other centres [5, 7]. Four of the patients in the present series had a FLR/TFL ratio of 15% or less prior to PVE and only one of these underwent resection. If a minimum FLR of 30% is to be achieved and the percentage increase with PVE is in the order of 10%, then patients with an FLR of less than 20% may not benefit from PVE. The minimal remnant volume required for safe resection, however, remains controversial and may be increased by any underlying parenchymal abnormality, such as steatosis. One series concluded that the hypertrophy of FLR induced by PVE had no beneficial effect on the post-operative outcome in patients with normal liver [11]. However, in this series, patients were undergoing a standard right hepatectomy with a satisfactory pre-embolisation FLR/TFL volume ratio of 33±10%. The same study concluded that in patients with chronic liver disease, pre-operative PVE significantly decreased post-operative complications. Another study has confirmed an association between a small FLR and an increase in post-operative complications [9]. Those patients with a standardized FLR of 20% or less had an increase in post-operative morbidity, but not mortality. A FLR of 40% has been recommended in patients who have previously undergone high dose chemotherapy [12].
A time interval between PVE and hepatic resection is necessary to allow parenchymal hypertrophy. Although the FLR growth is maximal within the first 2 weeks [5, 8] it continues for 4–5 weeks following PVE [5, 6, 8]. For this reason, in the anticipation of maximum hypertrophy, this study allowed 6 weeks between PVE and repeat volume measurement. The delay of 12 weeks before repeat volume measurement in one patient was due to external circumstances and subsequent surgical resection was successful.
This is the first study to examine the use of chemotherapy in patients with colorectal liver metastases undergoing pre-operative PVE. Chemotherapy has usually been discontinued prior to PVE [7, 12] to encourage hypertrophy of the remnant liver parenchyma. In our study, chemotherapy was discontinued at least 1 month prior to PVE and it has been assumed that effects of this chemotherapy on post-PVE liver regeneration and oncogenesis would be minimal or insignificant. Chemotherapy in these circumstances is unproven. The particular chemotherapy regimen was administered according to individual oncologist practice. There was no significant difference in disease stage between the two groups. Due to the small study size, only the effects of chemotherapy post-PVE have been analysed. In the present study FLR hypertrophy occurred whether or not chemotherapy was given post-PVE. The hypertrophy was, however, significantly less in those patients who received post-PVE chemotherapy suggesting that although chemotherapy is not contraindicated, it should be considered carefully in those patients who require a large compensatory hypertrophy following the procedure (FLR of <20%).
There is evidence to suggest PVE may stimulate tumour growth in both the embolised and non-embolised lobes of the liver. We have only assessed tumours in the embolised segments. Elias et al [16] reported increased growth of liver metastases compared with normal liver parenchyma following PVE in five patients with tumour in the non-embolised lobe. Kokudo et al [15] assessed tumour growth in the embolised lobe and found oncogenesis was promoted by PVE, with the tumour doubling time being reduced from 92 days to 76 days. In the present study, patients undergoing chemotherapy had no overall increase in tumour volume, which would suggest that chemotherapy did inhibit the tumour growth associated with PVE. Tumour volume regression was not demonstrated by the use of chemotherapy but this would seem unlikely over the short period between pre-PVE staging and re-assessment at 6 weeks post-PVE. The confidence interval for the data is wide, suggesting that further numbers would be helpful.
This is the first study on the effects of peri-PVE chemotherapy and the relationship with FLR hypertrophy and tumour volume. Further studies are required to define the optimal chemotherapy regimen for patients with colorectal liver metastases who are undergoing PVE.
Received for publication April 26, 2005.
Revision received October 2, 2005.
Accepted for publication November 14, 2005.
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References
|
|---|
- Scheithauer W, Rosen H, Kornek GV, Sebesta C, Depisch D. Randomised comparison of combination chemotherapy plus supportive care with supportive care alone in patients with metastatic colorectal cancer. BMJ 1993;306:752–5.[Abstract/Free Full Text]
- Fong Y, Salo J. Surgical therapy of hepatic colorectal metastasis. Semin Oncol 1999;26:514–23.[Medline]
- Fusai G, Davidson BR. Management of colorectal liver metastases. Colorectal Dis 2003;5:2–23.[CrossRef][Medline]
- Jaeck D, Bachellier P, Guiguet M, Boudjema K, Vaillant JC, Balladur P, et al. Long-term survival following resection of colorectal hepatic metastases. Association Francaise de Chirurgie. Br J Surg 1997;84:977–80.[CrossRef][Medline]
- Abdalla EK, Hicks ME, Vauthey JN. Portal vein embolization: rationale, technique and future prospects. Br J Surg 2001;88:165–75.[CrossRef][Medline]
- de Baere T, Roche A, Vavasseur D, Therasse E, Indushekar S, Elias D, et al. Portal vein embolization: utility for inducing left hepatic lobe hypertrophy before surgery. Radiology 1993;188:73–7.[Abstract/Free Full Text]
- Elias D, Ouellet JF, de Baere T, Lasser P, Roche A. Preoperative selective portal vein embolization before hepatectomy for liver metastases: long-term results and impact on survival. Surgery 2002;131:294–9.[CrossRef][Medline]
- Madoff DC, Hicks ME, Abdalla EK, Morris JS, Vauthey JN. Portal vein embolization with polyvinyl alcohol particles and coils in preparation for major liver resection for hepatobiliary malignancy: safety and effectiveness--study in 26 patients. Radiology 2003;227:251–60.[Abstract/Free Full Text]
- Abdalla EK, Barnett CC, Doherty D, Curley SA, Vauthey JN. Extended hepatectomy in patients with hepatobiliary malignancies with and without preoperative portal vein embolization. Arch Surg 2002;137:675–81.[Abstract/Free Full Text]
- Makuuchi M, Thai BL, Takayasu K, Takayama T, Kosuge T, Gunven P, et al. Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery 1990;107:521–7.[Medline]
- Farges O, Belghiti J, Kianmanesh R, Regimbeau JM, Santoro R, Vilgrain V, et al. Portal vein embolization before right hepatectomy: prospective clinical trial. Ann Surg 2003;237:208–17.[CrossRef][Medline]
- Azoulay D, Castaing D, Smail A, Adam R, Cailliez V, Laurent A, et al. Resection of nonresectable liver metastases from colorectal cancer after percutaneous portal vein embolization. Ann Surg 2000;231:480–6.[CrossRef][Medline]
- de Baere T, Roche A, Elias D, Lasser P, Lagrange C, Bousson V. Preoperative portal vein embolization for extension of hepatectomy indications. Hepatology 1996;24:1386–91.[Medline]
- Imamura H, Shimada R, Kubota M, Matsuyama Y, Nakayama A, Miyagawa S, et al. Preoperative portal vein embolization: an audit of 84 patients. Hepatology 1999;29:1099–105.[CrossRef][Medline]
- Kokudo N, Tada K, Seki M, Ohta H, Azekura K, Ueno M, et al. Proliferative activity of intrahepatic colorectal metastases after preoperative hemihepatic portal vein embolization. Hepatology 2001;34:267–72.[CrossRef][Medline]
- Elias D, de Baere T, Roche A, Leclere J, Leclere J, Lasser P. During liver regeneration following right portal embolization the growth rate of liver metastases is more rapid than that of the liver parenchyma. Br J Surg 1999;86:784–8.[CrossRef][Medline]
- Azoulay D, Castaing D, Krissat J, Smail A, Hargreaves GM, Lemoine A, et al. Percutaneous portal vein embolization increases the feasibility and safety of major liver resection for hepatocellular carcinoma in injured liver. Ann Surg 2000;232:665–72.[CrossRef][Medline]
- Tanaka H, Hirohashi K, Kubo S, Shuto T, Higaki I, Kinoshita H. Preoperative portal vein embolization improves prognosis after right hepatectomy for hepatocellular carcinoma in patients with impaired hepatic function. Br J Surg 2000;87:879–82.[CrossRef][Medline]
- Adam R, Avisar E, Ariche A, Giachetti S, Azoulay D, Castaing D, et al. Five-year survival following hepatic resection after neoadjuvant therapy for nonresectable colorectal [liver] metastases. Ann Surg Oncol 2001;8:347–53.[Medline]
- Bismuth H, Adam R, Levi F, Farabos C, Waechter F, Castaing D, et al. Resection of nonresectable liver metastases from colorectal cancer after neoadjuvant chemotherapy. Ann Surg 1996;224:509–20.[CrossRef][Medline]
- Elias D, Lasser P, Rougier P, Ducreux M, Bognel C, Roche A. Frequency, technical aspects, results, and indications of major hepatectomy after prolonged intra-arterial hepatic chemotherapy for initially unresectable hepatic tumors. J Am Coll Surg 1995;180:213–9.[Medline]
- Caldwell SH, de Lange EE, Gaffey MJ, Sue M, Boyd JC, Dickson RC, et al. Accuracy and significance of pretransplant liver volume measured by magnetic resonance imaging. Liver Transpl Surg 1996;2:438–42.[Medline]
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Abstract
Introduction
