Abstract
Introduction
Colorectal liver metastases (CRLM) infiltrating the hilar bifurcation is rarely described. We investigated the outcome of partial hepatectomy combined with resection of the hilar bifurcation.
Methods
Data collection for patients who underwent resection for CRLM at our institution was performed prospectively from January 2008 to August 2021. Follow-up ended in August 2023. Patients with and without bile duct infiltration of CRLM were analyzed retrospectively. The primary endpoints were overall (OS) and recurrence-free survival (RFS).
Results
A total of 1,156 liver resections were screened. Out of those, 18 were combined resections of the liver and the hilar bifurcation. Bile duct infiltration of CRLM was histologically proven in 5 of 18 cases. Preoperative mild obstructive jaundice occurred in 6 of 18 patients and was treated by drainage. Out of those, only 2 had a confirmed infiltration of the hilar bifurcation by CRLM. The median recurrence-free survival (RFS) was 10 months in those patients with bile duct infiltration compared to 9 months in those with no infiltration (p = 0.503).
Conclusion
While CRLM is common, infiltration into the central biliary tract is rare. Tumor invasion of the biliary tree can cause jaundice, but jaundice does not necessarily mean tumor invasion. We have shown that combined resection of the liver and hilar bifurcation for CRLM is safe and infiltration of the bile duct by CRLM did not seem to have a significant effect on RFS or OS.
Keywords: Colorectal liver metastases, Liver resection, Hilar bifurcation, Biliodigestive anastomoses
Introduction
Colorectal cancer is one of the most common types of cancer in the world [1–3]. About 25–30% of patients with colorectal cancer develop liver metastases (CRLM), either synchronous or metachronous [4, 5]. Surgical removal of these metastases is the standard of care, but at the time of diagnosis, only about 20–30% of CRLM are deemed resectable, mainly because of advanced disease with massive intra- and extrahepatic tumor spread or, less frequently, involvement of major vascular structures. Due to recent advances in chemotherapy for downsizing metastases as well as surgical techniques, such as portal and hepatic vein embolization and two-stage procedures, the number of patients with CRLM being eligible for liver resection has dramatically increased. In addition, progress in vascular resection techniques and the acceptance of an R1-vascular status have improved the resectability of CRLM with supposed vascular infiltration [6, 7]. Biliary infiltration on the other hand is an uncommon manifestation, and in particular, there are little data on CRLM with supposed invasion of the hilar bifurcation. To achieve a complete removal of the tumor, combined resection of the liver and hilar bifurcation and reconstruction of the biliary tract is necessary. This surgical procedure is also used to treat patients with perihilar cholangiocarcinoma where it is associated with raised morbidity and mortality rates. Literature about the surgical and oncological outcomes for patients with CRLM undergoing this procedure is scarce. We therefore investigated the outcome of partial hepatectomy combined with resection of the hilar bifurcation at our institution. Additionally, we conducted a literature review to compare our data to what has already been published.
Methods
Case-Cohort
Patients who underwent liver resection for CRLM at our institution were collected in a prospective liver resection database. Data collection was completed by August 2021 with a minimum follow-up of 24 months until August 2023. Data included preoperative clinical findings, operative details, perioperative complications and pathology reports. Patients with and without bile duct infiltration of CRLM were analyzed retrospectively with respect to patient characteristics as well as overall and recurrence-free survival. Morbidity was defined as a complication requiring intervention, according to the Dindo-Clavien classification grade III or higher [8]. Postoperative liver failure was diagnosed according to the Vauthey criterion as a peak serum bilirubin level ≥7 mg/dL [9]. Patients were also screened for posthepatectomy liver failure grade C as defined by the International Study Group of Liver Surgery (ISGLS) [10].
Pathology
All resected hilar bifurcations and the samples of areas with suspected bile duct infiltration were immunohistochemically stained with antibodies against cytokeratin 7 (CK 7), cytokeratin 20 (CK 20), and caudal type homeobox 2 (CDX2). Bile duct origin was defined by a CK7+, CK20−, and CDX2− phenotype while colorectal adenocarcinoma showed a CK7−, CK20+, and CDX2+ phenotype. Immunohistochemistry was performed on paraffin-embedded specimens fixed in 4% buffered formalin, using 4 μm thick histological sections. Biliary infiltration of CRLM was defined by bile duct wall invasion. Slides were digitalized using a digital whole slide scanner (NanoZoomer, Hamamatsu Photonics, Hamamatsu, Japan).
Statistics
Continuous variables were expressed as median values and range. The Fisher exact test was performed when normal distribution was given, Mann-Whitney U test was used when no normal distribution was given. To analyze categorical data, the χ2 test was used. Survival was calculated using the Kaplan-Meier method, to compare the median survival log-rank test was performed. p values below 0.05 were considered significant.
Literature Review
We performed a systematic literature review by searching in MEDLINE via PubMed for combinations of the following Mesh terms: colorectal liver metastasis, liver metastases, metastatic liver disease, liver resection, hepatectomy, bile duct, infiltration, invasion, extrahepatic, biliodigestive anastomosis, Roux-en-Y. Title and abstract of the articles were scanned for their relevance. Literature regarding different tumor entities such as hepatocellular carcinoma or cholangiocellular carcinoma as well as articles describing different surgical approaches such as partial pancreatectomies were excluded. All other prospective and retrospective case reports and cohort studies covering surgical removal of CRLM infiltrating central biliary ducts were included. Articles were then scanned for number of patients, number of patients with biliodigestive anastomoses and number of patients with histologically proven infiltration of CRLM into the biliary tract. If available, RFS and OS were tracked as well.
Results
Between January 2008 and August 2021, a total of 841 patients underwent 1,156 liver resections of colorectal liver metastases at our institution. Out of those, 18 underwent extensive liver surgery including resection of the hilar bifurcation and reconstruction of the biliary tract. There was no lost follow-up.
Patient Characteristics
We included 18 patients, 13 female and 5 male with a median age of 62.5 years (range 47–78 years) at the time of surgery. The primary tumor had been located in the colon in 7 cases (39%) and in the rectum in 10 cases (56%), 1 patient had suffered from a double carcinoma (5%). TNM-stages of the initial tumor were not on record for 3 patients (17%). In the remaining 15 patients, T stages according to TNM classification were either T2 (n = 3; 17%), T3 (n = 9; 50%), or T4 (n = 3; 17%). N stage was positive in 8 cases (44%) and negative in 7 cases (39%). Timing of liver metastasis was synchronous in 6 patients (33%) and metachronous in 12 patients (67%), out of which 8 patients had already undergone surgery for CRLM before. Neoadjuvant chemotherapy was administered in 9 out of 18 cases (50%). Preoperative mild jaundice caused by biliary obstruction occurred in 6 patients (33%) and was either treated by internal stent drainage (n = 5) or by percutaneous transhepatic cholangiodrainage (PTCD; n = 1). In 1 patient, preoperative processing suggested a perihilar cholangiocarcinoma. Because of the patient’s recurrence-free survival of more than 10 years after resection of colon cancer and the clinical presentation with obstructive jaundice, CRLM seemed unlikely. The histological workup after resection though determined the tumor to be a metastasis of the abovementioned colorectal cancer. In Figure 1, a preoperative CT scan of a similar case with suspected biliary infiltration of CRLM is shown. Overall, a bile duct infiltration of CRLM could be histologically proven in 5 of 18 cases. In the following analysis, patients were divided into two groups based on whether CRLM infiltrated the bile duct (group A) or not (group B). Patient characteristics are presented in Table 1 and did not differ significantly between both groups.
Fig. 1.
Colorectal liver metastasis infiltrating the biliary tract. Preoperative CT-scan shows a large tumor manifestation in liver segment 4b (red circle). The suspected infiltration of the biliary tract (yellow arrow) with consecutively dilated bile ducts (*) is shown.
Table 1.
Patient characteristics
| Overall (n = 18) | Bile duct infiltration (group A; n = 5) | No bile duct infiltration (group B; n = 13) | p value | |
|---|---|---|---|---|
| Age | ||||
| Years, median (range) | 62.5 (47–78) | 65 (59–74) | 60 (47–78) | 0.712 |
| Sex | ||||
| Male | 12 | 2 | 10 | 0.176 |
| Female | 6 | 3 | 3 | |
| Site of primary tumor | ||||
| Colon | 7 | 3 | 4 | 0.477 |
| Rectum | 10 | 2 | 8 | |
| Double carcinoma | 1 | – | 1 | |
| Primary tumor | ||||
| T stage | ||||
| T0–T1 | – | – | – | 0.506 |
| T2 | 3 | 1 | 2 | |
| T3 | 9 | 3 | 6 | |
| T4 | 3 | – | 3 | |
| Unknown | 3 | 1 | 2 | |
| N stage | ||||
| N negative | 7 | 2 | 5 | 0.645 |
| N positive | 8 | 2 | 6 | |
| Unknown | 3 | 1 | 2 | |
| Timing of liver metastasis | ||||
| Synchronous | 6 | 1 | 5 | 0.439 |
| Metachronous | 12 | 4 | 8 | |
| Preoperative jaundice | 6 | 2 | 4 | 0.561 |
| Preoperative internal stent drainage | 5 | 2 | 3 | 0.669 |
| Preoperative percutaneous transhepatic drainage | 1 | 0 | 1 | |
| Preoperative chemotherapy | 9 | 1 | 8 | 0.107 |
| Postoperative chemotherapy | 2 | 1 | 1 | 0.521 |
Surgical Procedures
The majority of liver resections were extended right hepatectomies (n = 7; 39%). Out of those, a two-stage approach was performed in 3 cases to achieve resectability with two ALPPS procedures and one preoperative portal vein embolization 6 weeks prior to liver resection [11]. The remaining resections were extended left hepatectomies (n = 5; 28%), left hepatectomies (n = 3; 17%), a right hepatectomy (n = 1; 6%), a mesohepatectomy (n = 1; 6%) and a segmental resection (n = 1; 5%). For the biliodigestive anastomosis usually a hepaticojejunostomy with a Roux-en-Y anastomosis was performed. In one case, a hepaticoduodenostomy because of extensive intestinal adhesions was conducted. The majority of reconstructions were executed as one bile duct ostium into one anastomosis (n = 11; 61%) or as two ostiums into two anastomoses (n = 5; 28%). In one case two ostiums were sutured into one biliodigestive anastomosis, while in another case with 6 remaining biliary ostiums after resection a total of 4 anastomoses were needed. Hilar lymph node dissection was performed in 13 cases (72%). No dissection or little dissection was performed in those patients with repeated hepatectomy and prior lymphadenectomy in the hepatic hilum. Other extrahepatic procedures that were inevitable to achieve R0 resection were the reconstruction of the portal vein (n = 4; 22%) and the vena cava inferior (n = 1; 5%) as well as partial resection of the diaphragm (n = 3; 17%). Surgical procedures are presented in Table 2 and did not differ significantly between both groups.
Table 2.
Perioperative outcome
| Overall (n = 18) | Bile duct infiltration (group A; n = 5) | No bile duct infiltration (group B; n = 13) | p value | |
|---|---|---|---|---|
| Size of metastases >5 cm | 11 | 3 | 8 | 0.513 |
| Median number of resected metastases (range) | 2 (1–11) | 2 (1–5) | 2 (1–11) | 0.513 |
| Liver resection margin | ||||
| R0 | 14 | 4 | 10 | 0.440 |
| R1 | 4 | 1 | 3 | |
| R1 parenchyma | 1 | – | 1 | |
| R1 vascular | 3 | 1 | 2 | |
| Biliodigestive anastomoses | ||||
| Number of anastomoses | ||||
| 1 | 13 | 4 | 9 | 0.795 |
| 2 | 4 | 1 | 3 | |
| 3 | – | – | – | |
| 4 | 1 | – | 1 | |
| Number of ostiums | ||||
| 1 | 11 | 2 | 9 | 0.306 |
| 2 | 6 | 3 | 3 | |
| 6 | 1 | – | 1 | |
| Extend of liver resection | ||||
| Extended right hepatectomy | 7 | – | 7 | 0.191 |
| Extended left hepatectomy | 5 | 2 | 3 | |
| Right hepatectomy | 1 | 1 | – | |
| Left hepatectomy | 3 | 2 | 1 | |
| Mesohepatectomy | 1 | – | 1 | |
| Segment resection | 1 | – | 1 | |
| Two-stage procedure | ||||
| ALPPS | 2 | – | 2 | |
| Portal vein embolization | 1 | – | 1 | |
| Associated extrahepatic procedures | ||||
| Vascular resection | ||||
| Portal vein | 4 | 1 | 3 | 0.701 |
| Vena cava inferior | 1 | – | 1 | 0.722 |
| Hilar lymph node dissection | 13 | 4 | 9 | 0.567 |
| Partial diaphragm resection | 3 | 1 | 2 | 0.650 |
ALPPS, associated liver partition and portal vein ligation for staged hepatectomy.
Pathology Reports
Complete resection of the metastases as defined by a tumor-free resection margin (R0) was achieved in 14 cases. In group A, 4 out of 5 cases showed a tumor-free resection margin, in group B there were 10 out of 13 resections classified as R0. Vascular R1 resection occurred in three cases, parenchymal R1 resection was confirmed in one case. Tumor cells in the hilar lymph nodes were found in 2 out 13 cases (15%). Portal vein infiltration occurred in 1 out of 4 cases (25%), infiltration of the diaphragm was confirmed in 1 out of 3 cases (33%). In 11 patients, the largest resected metastases were more than 5 cm in diameter. The median number of resected metastases was 2 in group A, ranging from 1 to 5. In group B, the median number was 2 as well, ranging from 1 to 11. Pathology reports are presented in Table 2, liver resection margins as well as size and number of resected metastases did not differ significantly between both groups. In 2 of the 6 patients with preoperative jaundice an infiltration of the bile duct could be histologically proven. In 2 out of 5 patients with proven biliary infiltration an intrabiliary tumor growth was described, but a distinction between direct metastasis to the bile duct and infiltration of the bile duct by CRLM could not be made. A tumor thrombus in the bile ducts was not seen in any of the cases.
Postoperative Data, Morbidity, and Mortality
Median duration of hospital stay was 32.5 days (range 7–99 days), with no significant difference between group A (median 36 days; range 12–99 days) and group B (median 29 days; range 7–65 days; p = 0.416). A total of 10 patients suffered complications grade III or higher according to the Dindo-Clavien classification. In group A, 3 patients developed a biliary fistula, either because of an insufficiency of the biliodigestive anastomosis or because of bile leakage at the liver transection plane. One of those patients died on day 98 after surgery due to septic shock and multi-organ failure (in-house mortality 5.6%). Out of group B, 5 developed a biliary fistula and 2 patients developed a transient liver failure from which they recovered. One patient died 82 days after surgery of unknown cause (90-day mortality 5.6%). The median follow-up of all included patients was 26 months (range 2–177 months). The median overall survival (OS) for patients in group A was 23 months (range 3–130 months) compared to 29 months (range 2–177 months) in group B and did not differ significantly (p = 0.703). The median recurrence-free survival (RFS) in group A was 10 months (range 3–76 months) compared to 9 months (range 2–177 months) in group B and did not differ significantly (p = 0.503). Morbidity rates are shown in Table 3. Overall and recurrence-free survival of patients in group A is listed in Table 4. In patient number 3 the recurrent liver metastasis was distant from the biliodigestive anastomosis. In patient number 5, multiple liver metastases were described.
Table 3.
Morbidity according to the Dindo-Clavien Classification and liver failure according to Vauthey as well as ISGLS grade C
| Overall (n = 18) | Bile duct infiltration (group A; n = 5) | No bile duct infiltration (group B; n = 13) | p value | |
|---|---|---|---|---|
| Median hospital stay, days (range) | 32.5 (7–99) | 36 (12–99) | 29 (7–65) | 0.416 |
| Morbidity | ||||
| Number of patients with grade III–IV complications | 9 | 2 | 7 | 0.185 |
| Number of patients with grade V complications | 1 | 1 | – | |
| Complications | ||||
| Biliary fistula | 8 | 3 | 5 | 0.382 |
| Liver failure | 3 | 1 | 2 | 0.299 |
Table 4.
Overall and recurrence-free survival of patients with bile duct infiltration of colorectal liver metastasis
| Patient | R0/R1 | OS | RFS | Site of recurrence | Treatment of recurrence | Current status |
|---|---|---|---|---|---|---|
| 1 | R0 | 98 days | – | – | – | d |
| 2 | R0 | 130 months | 76 months | Lung | Lung resection | n.e.d. |
| 3 | R0 | 17 months | 10 months | Liver, Lung | Chemotherapy | d.o.d. |
| 4 | R0 | 62 months | 62 months | – | – | n.e.d. |
| 5 | R1 | 22 months | 9 months | Liver | Chemotherapy | a |
a, alive; d, died; n.e.d., no evidence of disease; d.o.d., died of disease.
Literature Review
A total of 8 studies, consisting of 7 case reports and one case-cohort analysis were identified by our literature research (Table 5). The study by Wiggers et al. [12] described 76 patients which underwent liver surgery for CRLM, but only 10 patients had a biliary resection and biliodigestive reconstruction. Of those, biliary infiltration of CRLM was histologically proven in 7 patients. They described difficulty of R0 resection because of tumor localization and concerns about sufficient future liver remnant, resulting in a 50% R1 resection rate. Median RFS was described as 9.5 months with a median OS of 19 months [12]. For the other 7 case reports, data regarding RFS and even OS is not well documented. OS might be comparable to Wiggers et al. [12] with 1 patient surviving for a total of 69 months after surgery [13].
Table 5.
Literature review
| Author | Year | Number of patients with hepatic resection and BDA/patients with biliary infiltration | Recurrence-free survival (median), months | Overall survival (median), months |
|---|---|---|---|---|
| Wenzel et al. [14] | 2003 | 1/1 | N/A | Alive after 12 |
| Tomizawa et al. [15] | 2003 | 1/1 | N/A | Dead after 15 |
| Colagrande et al. [16] | 2004 | 1/1 | N/A | N/A |
| Takamatsu et al. [17] | 2004 | 1/1 | N/A | N/A |
| Minagawa et al. [13] | 2004 | 1/1 | N/A | Died after 69 |
| Chedid et al. [18] | 2005 | 1/1 | N/A | Alive after 14 |
| Wiggers et al. [12] | 2016 | 10/7 | 9.5 | 19 |
| Ofuchi et al. [19] | 2020 | 1/1 | N/A | N/A |
Discussion
Infiltration of colorectal liver metastases into the extrahepatic biliary tract is a rare phenomenon. Surgical removal of CRLM is the standard of care, but whether this should be the case for the aforementioned special entity is up for discussion. In our series we demonstrated that patients with CRLM can present with an obstructive jaundice. If so, we preoperatively initiated biliary drainage either internally or externally. This is equivalent to preoperative treatment for patients with perihilar cholangiocarcinoma, which was mimicked by CRLM in one of our patients. Only 2 of 5 patients with proven bile duct infiltration presented with obstructive jaundice. In the other 3 patients, tumor infiltration into the bile duct did not obstruct the biliary tract to cause jaundice yet. On the other hand, there were 3 patients with no tumor infiltration of the hilar bifurcation but with jaundice. In these patients jaundice most likely was caused just by compression of the bile ducts through CRLM. Our data show that tumor invasion of the biliary tree does not necessarily cause jaundice, and the other way round, jaundice does not necessarily mean tumor invasion. Another possible explanation, although very unlikely, are infiltrations of the bile duct that remained undiscovered because of a limited number of histologic sections and examinations. In the future, pathology reports should also focus on the distinction between direct metastasis to the bile duct and infiltration of the bile duct by CRLM. This, as well as the presence of intrabiliary tumor growth or a tumor thrombus, could probably correlate with the outcome with rising patient numbers. The goal of surgery was to achieve a complete removal of all hepatic metastases. This often made an extended hepatic resection necessary, in some cases even together with extrahepatic resections as shown in Table 2. Parenchymal sparing techniques, although commonly used by us to treat CRLM, were not routinely applied to achieve R0 resection in the herein presented series. In one case, we accepted R1 parenchymal resection to guarantee sufficient future liver remnant. Three R1 vascular resections were accepted to spare resection of major hepatic veins, as the oncological outcome after R1-vascular resection has been shown to be almost similar to R0 resections [7]. Surgery for perihilar cholangiocarcinoma usually requires extended liver and extrahepatic bile duct resection, which is similar to the surgical procedures in the herein presented series for CRLM. Morbidity requiring intervention in these patients occurs in 40–55%, comparable to our study (10/18; 55%) [20]. Most of these complications were bile leakage or, less often, insufficiencies of the biliodigestive anastomosis and were treated either by PTCD or percutaneous abscess drainage (PAD). In Western countries mortality rates after resection of PHC is around 10% and reached up to about 20% or even higher depending on the extent of liver resection [21, 22]. Mortality rates for combined liver resection and biliodigestive anastomoses have been described as high as 25% [23]. On contrast, we describe one 90-day mortality (1/18; 5.6%) [23]. This is despite our collective containing several entities which are susceptible to higher morbidity and mortality rates such as repeated liver resection as well as resection and reconstruction of the portal vein, vena cava and the diaphragm. Our findings clearly suggest that surgery for PHC is not at all the same as combined liver and hilar resection for CRLM. It is most likely that in PHC there is – though reversible – a more severe damage of liver parenchyma due to cholestasis compared to the cases with biliary compression caused by CRLM.
Overall RFS did not differ between the two groups with and without bile duct infiltration with a median of 9.5 months. This is probably best explained by the already advanced tumor disease in our cohort. OS did not differ between both groups as well, with a median OS of 26 months. This is on the lower end of the described OS after resection of CRLM in literature (28–46 months), but data are hardly comparable because in our series there were many major hepatectomies with additional even vascular resections/reconstructions thus certainly exceeding the usual extent of resection for CRLM [24, 25]. We are certain that for the patients included in our study, surgery was the best possible treatment option. This holds true in particular for our 2 described long-term survivors, which are alive after more than 130 and 177 months after surgery. In contrast, chemotherapy in palliative intent only yields a OS of 15–21 months [25, 26]. And, furthermore, local therapies such as ablation or transarterial chemoembolization are difficult to apply or even contraindicated because of the proximity of CRLM to central bile ducts and the vascular inflow [24]. The fact that in our series patients with bile duct invasion has a similar or even superior survival than without is likely due to the small number of patients as well as a disproportionate amount of advanced cases. The small patient collective, in addition to the retrospective nature of the paper, is a limitation of our study. However, to the best of our knowledge the presented data, although including only 18 patients is the largest series published so far. Future studies, especially multicentric collaborations are needed to further investigate the outcome of patients undergoing this rarely indicated procedure for CRLM.
Conclusions
While occurrence of CRLM is common, infiltration into the central biliary tract is rare. Tumor invasion of the biliary tree does not necessarily cause jaundice, and on the other hand, jaundice does not necessarily mean tumor invasion. In this study we have shown that combined resection of liver and hilar bifurcation for CRLM is comparatively safe. Although pathophysiology of CRLM afflicting the hilar bifurcation is different the perioperative approach should be closely related to treatment of perihilar cholangiocarcinoma. In our study infiltration of the bile duct by CRLM did not seem to have a significant effect on RFS or OS.
Statement of Ethics
All patients signed an informed consent that allowed the data and follow-up to be collected anonymously and potentially used for scientific analysis. Abiding by the regulations of the federal state law (state hospital law §36 & §37) and according to the Independent Ethics Committee of Rhineland-Palatinate, no ethical approval was necessary for this study.
Conflict of Interest Statement
The authors declare that they have no competing interests.
Funding Sources
T.G. is supported by the “Else Kröner-Forschungskolleg” (Else-Kröner-Fellowship). The funder had no role in the design, data collection, data analysis, and reporting of this study.
Author Contributions
Conceptualization and writing – original draft preparation: Sebastian Daniel Hiller and Hauke Lang; data curation: Sebastian Daniel Hiller and Janine Baumgart; formal analysis: Sebastian Daniel Hiller, Tiemo Gerber, and Beate Katharina Straub.
Funding Statement
T.G. is supported by the “Else Kröner-Forschungskolleg” (Else-Kröner-Fellowship). The funder had no role in the design, data collection, data analysis, and reporting of this study.
Data Availability Statement
The data that support the findings of this study are not publicly available due to the data containing information that could compromise the privacy of the research participants but are available from the corresponding author Sebastian Daniel Hiller upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are not publicly available due to the data containing information that could compromise the privacy of the research participants but are available from the corresponding author Sebastian Daniel Hiller upon reasonable request.