Anatomical study of the paracaval branch of the caudate lobe: implications of paracaval portion-preserving right hepatectomy for donors with marginal remnant liver volume

Introduction

Background

Living-donor liver transplantation (LDLT) is prevalent in East Asian countries, including the Republic of Korea, as an alternative treatment modality for end-stage liver disease when there is an organ shortage. In adult-to-adult liver transplantation, a right lobe graft is preferred because it donates sufficient liver volume to the recipient (1,2). Donors should have a sufficiently large remaining left lobe to meet the metabolic demand until the remnant regenerates adequately. Therefore, a sufficient remnant liver volume (RLV) is critical for donor safety during donor selection. Many institutions adopt a standard for RLV of 35% for healthy donors, as they have demonstrated comparable outcomes in liver function and morbidity (3). Due to donor shortages, in limited cases, donor hepatectomy is also performed on marginal donors, ranging from 30% to 35% of RLV (4).

In the case of a donor with marginal RLV, preserving as much liver volume to the donor as possible during donor right hepatectomy (DRH) is beneficial for donor safety in cases where only the graft-to-recipient weight ratio (GRWR) is sufficient. During DRH, the right portal vein (RPV) is ligated at the bifurcation of the main portal vein (MPV) and the liver parenchyma is transected along the middle hepatic vein (MHV). Right hepatectomy involves the resection of the paracaval portion of the caudate lobe and the dorsal area of the MHV.

Rationale and knowledge gap

Few anatomical studies have been conducted on the portal vein of the caudate lobe (5,6). In Japan, a case report described right hepatectomy with preservation of the entire caudate lobe in a patient with colorectal liver metastases and marginal liver function (7). We assumed that if the portal branch of the paracaval portion was not derived from the RPV, preserving the paracaval portion of the caudate lobe would be feasible during DRH. To date, there have been no studies on DRH with preservation of the caudate lobe.

Objective

This study aimed to analyze the portal branch anatomy of the paracaval portion of the caudate lobe and evaluate the efficacy of caudate-lobe-preserving DRH based on these findings. We present this article in accordance with the STROCSS reporting checklist (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-196/rc).

Methods

Donor evaluation and study population

Between August 2022 and July 2023, a total of 104 LDLTs were performed in our institution. Among these, right liver grafts were used in 87 cases, left liver grafts in nine cases, left lateral segment grafts in five cases, right posterior segment grafts in two cases, and a right anterior segment graft in one case. This study is a retrospective review of the medical records of 87 donors who underwent DRH. Of these donors, 35 (40.2%) received laparoscopic-assisted open DRH, 39 (44.8%) underwent pure laparoscopic DRH, and 13 (14.9%) underwent robotic DRH (Table 1). This study was approved by the Yonsei University Institutional Review Board, which waived the requirement for informed consent (No. 4-2024-0019). In addition, this study was registered at Research Registry (UIN: researchregistry10402, www.researchregistry.com) in accordance with the World Medical Association’s Declaration of Helsinki and its subsequent amendments.

The donor evaluation and selection criteria followed in this study have been previously reported (8). All healthy donor candidates underwent comprehensive preoperative evaluation, including 1-mm slice thickness computed tomography (CT) and gadoxetic acid-enhanced magnetic resonance imaging with magnetic resonance cholangiopancreatography (MRCP). Volumetric evaluation of the grafts was performed using CT. A candidate is selected if the anticipated RLV is greater than 30% and the estimated GRWR is 0.8% or higher. However, for donors with a small RLV ranging from 30–35%, selection is restricted to young age donors.

Surgical procedures of DRH

The right liver was mobilized and cholecystectomy was performed. During hilar dissection, the right hepatic artery (RHA) and RPV were isolated and encircled using vessel loops. Temporary clamping of the RHA and RPV was performed to identify the ischemic demarcation line between the right and left liver. In robot-assisted or pure laparoscopic approaches, indocyanine green (ICG) is intravenously injected to demarcate the border. After retracting both sides of the liver using a rubber band, the liver parenchyma was transected along the right side of the MHV. The MHV branches of Segments 5 and 8 were identified and ligated. The right bile duct (BD) was divided based on the structure of the BD and location of the caudate branch. The operator determined the transection plane of the right hepatic duct (RHD) by tactile sensation under direct vision using a probing method in the open approach (9) or visible ICG fluorescence imaging in the laparoscopic approach. Finally, the RHA, RPV, and right hepatic vein were sequentially isolated and ligated.

Analysis and classification of the paracaval branch of the caudate lobe

The anatomical structure of the portal vein of donors was analyzed through 3-dimensional (3D) reconstruction of the portal vein using the SYNAPSE (FUJI FILM, Tokyo, Japan) program and image review based on a 1-mm slice thickness CT. The caudate lobe consists of three subsegments: the Spiegel lobe, the caudate process, and the paracaval portion (10). The paracaval portion is located in the right part of the caudate lobe, posterior and inferior to the middle and right hepatic veins, and envelops the anterior aspect of the inferior vena cava (IVC). The caudate portal branch supplies the liver parenchyma anterior to the IVC. The paracaval branch was defined as the portal pedicle that feeds the paracaval portion (10).

Based on Kumon’s anatomical study, we categorized the paracaval branch into the RPV, left portal vein (LPV), and bifurcation of the MPV based on its origin from the root of the paracaval branch (Figure 1A-1C). Additionally, in the reconstructed 3D image, paracaval branches were classified into three categories based on the extent of the supplied area: (I) large size, reaching the liver surface; (II) medium size, not reaching the liver surface but supplying the anterior aspect of the IVC and the dorsal aspect of the root of the major hepatic veins; or (III) small size, supplying a small region (Figure 1, D1-D4).

Figure 1 The classification of the type and size of paracaval branches. The paracaval branch was derived from (A) right portal vein (black arrow), (B) bifurcation of the main portal vein (red arrows), and (C) left portal vein (red arrows). (D1) Paracaval volume is supplied from the large size of the paracaval branch reaching the liver surface. (D2) Expected preserved paracaval volume after paracaval portion-preserving donor right hepatectomy compared to that after conventional donor right hepatectomy. (D3) Medium size of the paracaval branch, not reaching the liver surface but supplying the anterior aspect of the IVC and the dorsal aspect of the root of the major hepatic veins. (D4) The small size of the paracaval branch, supplying a small region. (D1-D4) The reconstructed paracaval area is shown in green. IVC, inferior vena cava.

Volumetry for paracaval portion-preserving DRH

The liver volume supplied by the portal pedicle was estimated using SYNAPSE software (Figure 1, D1). Two donors for whom reconstruction and volumetry were not possible because of poor CT image quality were excluded. As the RPV needs to be divided during DRH, we assumed that paracaval portion-preserving DRH could be implemented when the paracaval branch originates from the LPV or the bifurcation of the MPV. Paracaval volume represents the measured liver volume of the area supplied by the paracaval branch. In paracaval portion-preserving DRH, the RPV is divided on the right side of the paracaval branch, preserving the liver area corresponding to the paracaval portion on the right side of the MHV. The quantified area was expressed as the expected preserved paracaval volume (Figure 1, D2). For patients who underwent paracaval portion-preserving DRH, the regenerated liver volume was measured as the entire preserved paracaval volume using a CT scan performed on postoperative 5 days and 1 month.

Statistical analysis

Results are presented as mean ± standard deviation (range) or numbers and percentages. All statistical analyses were performed using SPSS for Windows (version 26.0; IBM Corp., Armonk, NY, USA).

Results

The mean age of the 87 donors who underwent DRH was 38.3±13.2 (range, 17.0–66.0) years. Of them, 46 (52.9%) were male and 41 (47.1%) were female. Table 1 presents the details of the preoperative clinical factors and the types of paracaval branches analyzed for all the included donors.

The graft-related liver volume parameters were as follows: total liver volume (TLV) 1,238.4 mL, graft liver volume (GLV) 788.1 mL, and RLV 36.5%. In terms of paracaval branch types, 41 (47.1%) originated from the RPV, 37 (42.5%) from the LPV, and 9 (10.3%) from the bifurcation of MPV.

Indication for paracaval portion-preserving DRH

Table 2 shows the results of the analysis of size and liver volume for donors with the paracaval branch type derived from the LPV and the bifurcation of the MPV. Among 46 donors, 21 (45.7%) were large size, 13 (28.3%) were medium size, and 12 (26.1%) were small size. Excluding two donors with poor images, the mean TLV of 44 donors was 1,272.9±196.1 mL (range, 930.0–1,642.2 mL), and the RLV after DRH was 35.9%±3.3% (range, 31.1–44.7%).

The measured paracaval volume averaged 38.0±29.9 mL (range, 11–186 mL), with 2.9±2.2% (range, 0.7–13.9%) of the TLV. If caudate-lobe preserving DRH had been performed as intended, the expected preserved paracaval volume would have been 27.3±26.9 mL (range, 3–165 mL), with 2.1%±2.0% (range, 0.3–12.3%) of the TLV. Among them, 27 donors had a small RLV, ranging from 30% to 35%. For these donors, the paracaval volume averaged 33.8±19.2 mL (range, 11–89 mL), with 2.6±1.3% (range, 0.8–5.8%) of the TLV, and the mean expected preserved paracaval volume was 22.4±14.8 mL (range, 3–70 mL), with 1.8±1.1% (0.3–4.6%) of the TLV.

Case series for paracaval portion-preserving DRH

Based on this study, caudate lobe-preserving DRH was performed in four cases at our center, as outlined in Table 3. Two cases were treated using the open approach, and two cases were treated using the laparoscopic approach, with Video S1 provided for each method (one open case and one laparoscopic case). Figure 2 shows the intraoperative images for paracaval portion-preserving DRH. The liver parenchyma was transected while preserving the paracaval portion, and the right hepatic vein (RHV) was exposed on the right side of the transected line (Figure 2A,2B, open approach; Figure 2D,2E, laparoscopic approach). Before dividing the RHD, Figure 2C shows the probing method, and Figure 2F shows ICG fluorescence imaging to verify the bifurcation and caudate branch of the BD.

Figure 2 The intraoperative view of the paracaval portion-preserving donor right hepatectomy. (A-C, open; D-F, laparoscopic). (A) Parenchymal transection in the open approach. (B) Exposure of RHV after finishing the parenchymal dissection. (C) Verification of the BD structure and caudate BD branch using the probing method. (D) Demarcation line on the liver surface beneath the diaphragm using ICG fluorescence image. (E) Parenchymal dissection in the laparoscopic approach. (F) Verification of the BD structure and caudate BD branch using ICG. The caudate BD branch originated from the right side of the bifurcation. (G) Schematic image of paracaval portal pedicle structure stacked on a Glissonean sheath. MHV, middle hepatic vein; RHV, right hepatic vein; BD, bile duct; ICG, indocyanine green.

All donors had an initial RLV ranging from 30% to 35%. Details of the four cases are summarized as follows: (I) bifurcation of MPV, medium size, TLV 1,301 mL, preserved area 35.6 mL (2.7%), initial RLV 31.8%; (II) LPV, large size, TLV 1,339 mL, preserved area 164.7 mL (12.3%), initial RLV 34.9%; (III) LPV, large size, TLV 1,526 mL, preserved area 70.2 mL (4.6%), initial RLV 31.4%; (IV) LPV, large size, TLV 1,014 mL, preserved area 20.3 mL (2.0%), initial RLV 30.4%. Figure 3 illustrates the third case, showing preservation of the paracaval portion located on the right aspect of the MHV on CT performed on postoperative 5 days. Each donor was discharged 7 days postoperatively with no surgical complications or functional regeneration problems. Additionally, each donor achieved liver regeneration, with the liver volume reaching approximately 70% or more of the RLV on CT scans after postoperative 1 month. In the case series, the preserved portion of the liver volume was 41, 81, 66, and 44 mL, respectively, in the CT performed 5 days after surgery. One month after surgery, the volumes were 67, 102, 78, and 58 mL, respectively.

Figure 3 Reconstruction image using the SYNAPSE program and postoperative CT scan of a patient who underwent paracaval portion-preserving donor right hepatectomy. (A) Portal structure and paracaval branch (red arrows) originating in the left portal vein. (B) Expected preserved area and measured liver volume. (C) Preserved paracaval portion area (yellow arrow) on the CT scan at postoperative 5 days. IVC, inferior vena cava; CT, computed tomography; POD, postoperative day.

Discussion

The caudate lobe is supplied by both the right and LPVs. In the present study, using 3D analysis with SYNAPSE, we examined and categorized the paracaval branch based on its origin and the extent of the supplied area. Furthermore, based on the results of the anatomical studies, we conducted a quantitative analysis to estimate the preserved liver volume during DRH while virtually sparing the hepatectomy of the paracaval portion. To the best of our knowledge, this is the first report of DRH with preservation of the paracaval portion.

To date, research on the portal branch of the paracaval portion is limited. A representative study, Kumon’s classification, categorized the origin of the paracaval branch based on the liver casts, revealing that the branch originated from RPV in 5 out of 19 cases (26.3%) and from LPV in 14 out of 19 cases (73.7%) (5). Another anatomical study by Mao et al. reported that in 41 liver specimens, the portal branch of the paracaval portion derived from RPV in 14 cases (34.15%), from the LPV in 22 cases (53.66%), and equally from both sides in 5 cases (12.19%) (6). In our study, the classification was based on images obtained through 3D reconstruction from CT scans with 1-mm slice thickness.

In the DRH, the RPV is cut just to the right side of the bifurcation, where the MPV divides into first-order branches. In conventional DRH, the paracaval portion located on the right side of the MHV is resected, and the portal pedicle crossing from the left side of the cut surface to the right side should be sacrificed. Given this background, DRH with paracaval portion preservation is feasible if the paracaval branch originates on the left side of the RPV division line. Based on our hypothesis, the cut surface is shifted to the right compared with conventional DRH, allowing for preservation of the pedicle of the paracaval portion. Consequently, we classified the paracaval branches into three groups: originating from the RPV, bifurcation of the MPV, and LPV. In our study, the proportion of donors suitable for paracaval portion preserving DRH was 46 out of 87 (52.9%). On average, an estimated 2.1% of the liver volume can be preserved, with the potential to preserve up to 12.3%. Considering the real clinical situation, among donors with an RLV of 30–35%, 27 donors were identified as an indication for this procedure. The mean preserved liver volume in these donors was estimated to be 1.8% with a maximum preservation of 4.6%.

Our study aimed to enhance donor safety by increasing the remaining liver volume in donors with marginal RLV to better support the metabolic demands essential for liver regeneration in clinical situations. Our findings suggest a potential reconsideration of donor candidates initially excluded because of low RLV. Several studies have shown that donors with a small RLV face increased risks, including delayed liver function recovery, a greater relative risk for morbidity, and longer hospital stays (4,11). In our institution, the donors with a small RLV (<35%) showed higher total bilirubin levels and prolonged international normalized ratio (INR) at postoperative 3 days than donors with an RLV >35%, but no significant difference at postoperative 5 days. However, irrespective of whether the RLV was smaller or larger than 35%, there was no significant difference in postoperative complications. In the donor selection process, if the RLV is <30% or the GRWR is too large for a right liver graft, a left liver graft is used if the GRWR is more than 0.8 and the anatomy is compatible. Therefore, of 104 cases, the left liver graft was used in nine cases. Additionally, based on the findings of our study, if a donor has appropriate anatomy and an acceptable RLV after paracaval portion-preserving DRH, the donor can be selected, providing recipients with the opportunity to undergo LDLT. However, since the graft size also becomes smaller, this procedure will be able when GRWR is 0.8 or more.

In a case report, a patient with marginal liver function required right hepatectomy with preservation of the entire caudate lobe (7). This study did not include an anatomical investigation, but described a procedure that retained the entire caudate lobe while preserving its portal pedicle. However, performing a right hepatectomy while leaving the paracaval portion anatomically accurate is challenging. Although there have been several studies on the right side boundary of the caudate lobe from segments 7 or 8 (12-14), it is still ambiguous because of the absence of landmarks. A case report demonstrated paracaval portion-preserving right hepatectomy using a positive-staining method. Indigo carmine was injected with an ICG solution into the paracaval branch to visually confirm the paracaval area (15).

Clinically, the remaining liver parenchyma must maintain adequate inflow, outflow, and biliary drainage. For precise anatomical liver resection, ICG fluorescence with negative or positive staining techniques is commonly used to identify the exact portal territory (16,17). In donor hepatectomy, ICG-negative staining was used to confirm the boundary between the left and right liver. As shown in Figure 2D, the demarcation line formed beneath the diaphragm and shifted to the RHV during the laparoscopic approach. However, owing to the transient inflow control, visually confirming the intraparenchymal boundary is challenging. This poses difficulties in accurately visualizing the boundary between segments 7 and 8 and the paracaval portion, hindering paracaval portion-preserving DRH. This technique was applied to four donors with an RLV of 30–35% at our institution, achieving preservation of up to 12.3%. During paracaval portion-preserving DRH, the boundary between the paracaval portion and segments 7 or 8 was identified based on the pattern of portal pedicle branches terminating in the intersegmental plane (Figure 2A,2E). The RHV was exposed and the paracaval portion was preserved on the right side of the MHV using open and laparoscopic approaches, respectively (Figure 2B,2E). Regarding hepatic outflow, it is essential to preserve short hepatic veins from the paracaval portion. Controlling short hepatic veins is particularly beneficial after dividing the RHD and assessing the exact boundary of the paracaval portion.

To preserve biliary drainage, we decided on the transection line of the RHD after visualizing the BD structure. Kumon et al. showed that the bifurcation sites of the portal and biliary branches in the paracaval portion varied among cases (5). Notably, in 5 out of 19 cases (26.3%), it was observed that the portal branch originated from the LPV, while the BD of the paracaval portion originated from the right ductal system. Despite this discrepancy, the portal vein, hepatic artery, and BD were aligned on the Glissonean sheath to form the portal pedicle as shown in Figure 2G. In the hilar plate, the portal pedicle of the paracaval branch, including the portal vein and BD, stacks on the Glissonean sheath; therefore, they are located close to each other, even though their bifurcations are different. Consequently, maintenance of BD drainage in the paracaval portion can be achieved by visually confirming the BD structure and subsequently dividing it.

In all four cases, the paracaval portion was regenerated, and the median regeneration rate of the preserved paracaval portion from 5 days to 1 month after surgery was 28.9% (range, 18.2–63.4%), suggesting that inflow, outflow, and biliary drainage were well maintained.

This study has several limitations. First, this was a single-center retrospective study. Additionally, our study focused on anatomical analysis, but was conducted indirectly rather than analyzing liver specimens. However, all donors were examined using a 1-mm slice thickness CT scan, and even small portal veins were reconstructed and analyzed using these images. The biliary system was not evaluated in our study because it was difficult to accurately evaluate the thin paracaval BD branch in the reconstructed MRCP images. Although the structure of the biliary tree was not analyzed, a verification procedure for the BD structure, such as the ICG fluorescence system or the probing method, can preserve the paracaval BD branch. Therefore, the liver parenchyma of the paracaval portion can be clinically preserved, and we estimated the preserved paracaval area based on portal vein anatomy. However, future research examining the biliary system in combination with the portal anatomy is necessary. Finally, only four cases were included in our study, which is inadequate to draw definitive conclusions. We aimed to suggest a new surgical concept based on anatomic analysis. All four cases showed an increase in RLV and regeneration of additionally preserved liver. Future studies with a larger sample size are required to analyze the outcomes of this procedure.

Conclusions

In conclusion, the paracaval branch can originate from the RPV, LPV, or MPV bifurcation. The indications for paracaval portion-preserving DRH, such as LPV or bifurcation type, may be for more than half of the donors. When there is a large size reaching the liver surface, marginal donors with a small RLV will benefit in terms of donor safety.

Acknowledgments

Medical Illustration & Design (MID), a member of the Medical Research Support Services of Yonsei University College of Medicine, provided excellent support with medical illustrations.

Footnote

Reporting Checklist: The authors have completed the STROCSS reporting checklist. Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-196/rc

Data Sharing Statement: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-196/dss

Peer Review File: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-196/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-196/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Yonsei University Institutional Review Board, which waived the requirement for informed consent (No. 4-2024-0019).

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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