Key words : Dimensional reconstruction, Liver anatomy, Living donor liver transplantation, Liver mapping, Liver volumetry

Introduction

Knowledge of segmental portal vein (PV) and territorial hepatic vein (HV) anatomy and their overlapping pathways is seminal for the planning of complex liver resections and adult living donor liver transplant.^1-4 Portal vein segments are extremely inconsistent in size, shape, and topographic location,⁵ with highly variable PV inflow and HV outflow patterns.⁶ Although previous publications have proposed PV and HV branching nomenclatures based on areas of distribution, the territorial anatomy remains poorly defined and classified.^7-9

We performed a comprehensive systematic analysis of both individual and overlapping PV and HV maps to preoperatively identify surgically relevant volume dominance patterns by means of individualized 3-dimensional (3D) inflow and outflow crossmatch volumes. High-risk virtual congestion volumes were particularly addressed and outlined from scientific anatomic and practical surgical points of view to assist in the planning of extensive and complex liver resections.

We considered 3 essential queries for high-risk hepatectomies: (1) estimated remnant liver volumes involving right/left lateral sectors for right versus left trisectionectomies, (2) the drainage advantage of the inferior (accessory) hepatic vein (IHV) in remnant livers after extended left hepatectomies, and (3) the risky middle hepatic vein (MHV) drainage patterns in the right lateral sector in extended left hepatec-tomies.

Materials and Methods

Study population
Between January 2003 and December 2020, 3D-computed tomography (CT) reconstructions and segmental/territorial liver maps of 140 potential living liver donors (72 women and 68 men; mean age of 37 ± 10 years) were prospectively analyzed at the University Hospitals of Essen and Tuebingen, Germany. All donors were related to recipients. Relationships included siblings, cousins, husband/wife, and children.

Computed tomography protocol
Computed tomography imaging, as originally published by Schroeder and colleagues,10 was performed using a 16-row multidetector CT scanner (Sensation16, Siemens) and 2 × 64-row multidetector CT scanner (Somatom Force, Siemens).

Image analysis and reconstruction
Computed tomography images were analyzed with HepaVision software (Frauenhofer MeVis Research GmbH). Segmental and territorial maps of PV and HV branches (Figure 1) inclusive of the corres-ponding volumes were calculated.^11-13

Portal vein and hepatic vein map definitions
The Pringle maneuver demarcation line arising from the simulated right/left-sided main portal branch occlusion (virtual Pringle clamp test) was used to define the boundary between right hemiliver (RHH) and left hemiliver (LHH).^12,14

The RHH (segments 5-8) consisted of right lateral (RL) and right medial (RM) sectors, and the LHH (segments 2-4) consisted of left lateral (LL) and left medial (LM) sectors. Each sector was bi-segmental, with RL consisting of segments 6/7, RM consisting of segments 5/8, LL consisting of segments 2/3, and LM consisting of segments 4A/B.

Per the Couinaud classification8 modified by Kumon,15 the caudate lobe consisted of a left (segment I or Spiegel lobe) and a right (segment IX or caudal process) portion and the paracaval section (or pars intermedia).

Statistical analyses
We calculated volume as mean ± SD and percentages. The chi-square test was used for dichotomous variables. The Wilcoxon matched pairs test was used to compare 2 variables lacking normal distribution. The Mann-Whitney U was used to test the significance of differences between 2 independent samples and differences in 2 groups.P< .05 was considered significant. We used Statistica 7.0 (Statsoft Inc) for statistical analysis.

This study was approved by the institutional review board and the ethics committee of the Department of General, Visceral and Transplantation Surgery, University Hospital Essen (Essen,Germany).

Results

Portal vein
Portal vein dominance in total liver volume.
We evaluated hemiliver, sectorial, and segmental volumes of the whole liver (total liver volume; TLV) with respect to dominance based on PV branching hierarchy.

The RHH was dominant in all 140 instances (P< .001, Wilcoxon matched pairs test) with up to 77% TLV. Volume variability for the RHH was slightly greater than that of the LHH (Figure 2). The distribution of sectorial and segmental mean volumes were as follows: RM > RL > LL > LM and segment 8 > segment 5 > segment 7 > segment 6 > segment 3 > segment 2 > segment 4B > segment 4A > caudate lobe (Figure 3,a and b). Both the RM sector and segment 5 had the greatest volume variability, whereas the LM, caudate lobe, and segment 4A had the least volume variability.

We found the RM to be dominant with up to 58% TLV in 105/140 livers (75%), whereas the RL sector was dominant with up to 48% TLV in 35 livers (25%). Segment 8 was dominant in 71 livers (51%), segment 5 in 41 livers (29%), segment 6 in 14 livers (10%), and segment 7 in 14 livers (10%). In individual cases, the respective volumes of segments 5, 7, and 8 reached a maximum of 30% to 38% TLV. The LM sector had the smallest volume in TLV in 120 livers (86%), whereas the LL had the smallest volume in 20 livers (14%).

When we excluded the caudate lobe (smallest volume in 113 livers [81%]), segment 4A had the smallest volume (mean 5.1 ± 1.4%) in 88 livers (63%), followed by segment 2 (n = 23, 16%) and segment 4B (n = 29, 21%).

Dominance of right hemiliver by Pringle demarcation
For RHH (Figure 3c), the following mean volume distribution was observed: RM > RL and segment 8 > segment 5 > segment 7 > segment 6. The RL sector and segment 5 had the greatest volume variability. The RM sector was dominant in 104 livers (74%), whereas RL had a dominant volume in 36 livers (26%). Segment 8 was dominant in 67 livers (48%), segment 5 in 39 livers (28%), segment 6 in 16 livers (11%), and segment 7 in 18 livers (13%).

Dominance of left hemiliver by Pringle demarcation
For LHH (Figure 3d), the following distribution was observed for mean volumes: LL > LM and segment 3 > segment 2 > segment 4B > segment 4A. The LL sector and segment 3 showed the greatest volume variability. The LL sector was dominant in 121 livers (86%), whereas LM had a dominant volume in 19 livers (14%). Segment 3 was dominant in 87 livers (62%), segment 2 in 34 livers (24%), segment 4B in 12 livers (9%), and segment 4A in 7 livers (5%).

Dominance of right lateral sector
Segments 7 and 6 showed nearly identical mean volumes. Segment 7 had the greatest volume variability with up to 94% in the RL. Segment 7 was dominant in 81 livers (58%) and segment 6 in 59 livers (42%).

Dominance of right medial sector
Segment 8 had a slightly larger mean volume than segment 5 but a smaller volume variability. Segment 5 was dominant in 1 liver in 89% of the RM sector. Segment 8 was dominant in 92 livers (66%) and segment 5 in 48 livers (34%).

Dominance of left medial sector
Segment 4B had a larger mean volume and greater volume variability than segment 4A. Segment 4B was dominant in 1 liver in 91% of the LM sector and was dominant in 110 livers (79%).

Dominance of left lateral sector
Segment 3 had a larger mean volume and greater volume variability than segment 2. Segment 3 was dominant in 101 livers (72%) and segment 2 in 39 livers (28%).

Hepatic vein
Hepatic vein dominance in total liver volume
Two possible anatomic configurations were considered for the accessory IHV: absent (n = 73, 52%) or present (n = 67, 48%) (Figure 4).

Inferior (accessory) hepatic vein absent in 73 livers
The following mean drainage volume distribution was encountered: right hepatic vein (RHV) > MHV > left hepatic vein (LHV) (P< .001 andP< .0001, Wilcoxon matched pairs test). We determined that RHV had both the largest volume (up to 65% TLV) and the greatest volume variability, and LHV had both the smallest volume and the least volume variability.

Among the 73 livers with IHV absent, RHV was dominant in 60 livers (82%), MHV in 12 livers (16.5%), and LHV in 1 liver (1.5%) (up to 38.2% TLV). We determined that LHV had the smallest volume in 63 livers (86%), MHV in 9 livers (12.5%), and RHV in 1 liver (1.5%) (28.3% TLV).

Inferior (accessory) hepatic vein present in 67 livers.
Mean drainage volumes showed the following distribution: RHV > MHV > LHV> IHV (P< .455,P< .001, and P< .001, Wilcoxon matched pairs test). A single RHV with IHV present showed a significantly smaller drainage volume than RHV with IHV absent (P< .001 Mann-Whitney U test; Figure 4). We determined that MHV had the largest volume (up to 57% TLV) and IHV the smallest volume; RHV showed the greatest and LHV the least volume variability.

We found MHV to be dominant in 33 livers (49%), RHV in 32 livers (48%), and LHV in 2 livers (3%). The IHV was never dominant and had the smallest volume in TLV in 53 livers (79%). In 8 livers (12%), LHV showed the smallest volume, followed by RHV in 6 livers (9%). In these specific 6 livers, an RHV-IHV complex with a dominant IHV drainage volume was present.

Overlap of portal vein and hepatic vein maps with inferior hepatic vein absent in 73 livers
Detailed delineations of the volume calculations are shown in Figure 5 and Figure 6.

Drainage of hemilivers by Pringle demarcation
We determined that RHV and LHV dominated RHH and LHH mean drainage volumes, respectively (P< .001 and P< .001, Mann-Whitney U test). In RHH, RHV was dominant in 70 livers (96%), showing the greatest volume variability in RHH, and MHV was dominant in 3 livers (4%). In LHH, LHV was dominant in 66 livers (90%) and MHV in 7 livers (10%), showing the greatest volume variability in LHH.

Drainage of liver sectors
When we looked at mean values, RHV significantly dominated in RL sector and was marginally dominant in RM sector drainage (P< .0001 andP= .231, Mann-Whitney U test). We found that RHV had the greatest volume variability in both sectors and drained in 16 livers (22%). In individual instances, MHV drained up to 42% of the RL sector.

We found that RHV dominated drainage of RL sector in 73 livers (100%) and of RM sector in 42 livers (58%); MHV had a dominant volume in RM in 31 livers (42%). When we looked at mean values, LHV and MHV dominated drainage of LL and LM sectors, respectively (P< .001 and P< .001, Mann-Whitney U test). We found that LHV dominated drainage of LL in 72 livers (99%), including 1 instance of 100% LL; MHV had a dominant volume in LM in 70 livers (96%), including 2 instances of 100% LM.

Drainage of liver segments 2 to 8
For segments 2 and 3, LHV dominated mean drainage (P< .001 and P< .001, Mann-Whitney U test); LHV and MHV had identical volume variability in both segments. For segments 2 and 3, LHV dominated drainage of 71 livers (97%), including 100% drainage of segment 2 in 6 livers (8%) and 100% drainage of segment 3 in 16 livers (22%).

For segments 4A and 4B, MHV dominated mean drainage (P< .001 and P< .001, Mann-Whitney U test), showing identical volume variability with LHV in both segments. We found that MHV dominated drainage of segment 4A in 55 livers (75%) and segment 4B in 72 livers (99%), including 100% drainage of segment 4A in 3 (4%) and of segment 4B in 5 livers (7%).

For segments 6, 7, and 8, RHV dominated mean drainage (P< .001,P< .001, and P< .001, Mann-Whitney U test), showing the greatest volume variability in those segments. In individual instances, MHV revealed up to 75% drainage of segment 6. We found that RHV dominated drainage of segment 6 in 70 livers (96%), segment 7 in 73 livers (100%), and segment 8 in 56 livers (77%), including 100% drainage of segment 6 in 26 (36%) and of segment 7 in 44 livers (60%); MHV dominated mean volume in segment 5 (P< .001, Mann-Whitney U test) in 48 livers (66%) (up to 87.5% of segment 5); and RHV drainage revealed the highest volume variability in segment 5, draining up to 79%.

Overlap of portal vein and hepatic vein maps with inferior hepatic vein present in 67 livers
When IHV was present, LHV significantly dominated mean drainage of LHH (P< .001, Mann-Whitney U test) (Figure 5b).

Drainage of right hemiliver by Pringle demarcation.
The RHV dominated mean drainage of RHH, showing RHV > MHV > IHV (P< .001 and P< .001, Wilcoxon matched pairs test). In RHH, we found that RHV had the greatest volume variability in RHH, and RHV drainage was dominant in 51 livers (76%), MHV in 10 livers (15%), and IHV in 6 livers (9%) (with up to 54%).

Drainage of right liver sectors
The RHV dominated mean drainage of the RL sector as follows: RHV > IHV > MHV (P< .001 andP< .001, Wilcoxon matched pairs test). We found that MHV had a dominant mean drainage of the RM sector as follows: MHV > RHV > IHV (P< .001 and P< .001; Mann-Whitney U test) (Figure 5d).

The RHV dominated drainage of the RL sector in 49 livers (73%), of IHV in 17 livers (25%), and of MHV in 1 liver (with 35%). The RHV and IHV shared the greatest volume variability in RL. The MHV had a dominant drainage volume of the RM sector in 42 livers (63%) cases and of RHV in 25 livers (37%). The RHV revealed the greatest volume variability in the RM sector. The IHV drainage territory in RM was detectable in 29 livers (43%) (up to 25% RM) with no evidence of dominance in any case.

Drainage of right liver segments 5 to 8
The RHV dominated mean drainage of segment 6 with the following volume distribution: RHV > IHV > MHVP< .001 andP< .001, Mann-Whitney U test). For segment 7, the volume distribution was RHV > IHV > MHV (P< .001 and P< .001, Mann-Whitney U test). For segment 8, the volume distribution was RHV > MHV > IHV (P< .001 and P< .001, Mann-Whitney U test). The RHV showed the highest volume variability in those segments (Figure 6).

The RHV dominated drainage of segment 6 in 38 livers (57%), of segment 7 in 54 livers (81%), and of segment 8 in 48 livers (72%), with 100% volume of segment 6 drainage in 4 livers (6%) and 100% volume of segment 7 drainage in 1 liver (1%). A dominant IHV drainage of segments 6 and 7 was detected in 25 (37%) and 13 livers (19%), respectively, including 100% volume of segment 6 drainage in 2 livers (3%). We found that IHV drainage was detectable in segment 8 in 30 livers (45%) (up to 24% of segment 8) with no evidence of dominance in any case. The MHV drainage was dominant in segment 6 in 4 livers (6%) (up to 83% of segment 6) and in segment 8 in 19 livers (28%) but was never dominant in segment 7 (Figure 6).

Segment 5 showed the following mean drainage volume distribution: MHV > RHV > IHV (P< .001 andP< .001, Mann-Whitney U test); MHV had equal volume variability with RHV. We found that MHV was dominant in 57 livers (85%) (up to 99.2% with segment 5), RHV drainage was dominant in 10 livers (15%) (up to 76% with segment 5), and IHV drainage was detectable in 26 livers (39%) (up to 34% with segment 5) with no evidence of dominance in any case.

Overlap of portal vein and hepatic maps: relevance for surgery planning
We applied a virtual analysis to identify liver resections at highest risk of postoperative liver failure and intrahepatic inflow/outflow derangements.

For extended right/left hepatectomies with right trisectionectomy (segments 5-8 + 4 + 1), 129 livers (92%) had borderline small remnant volume (RV; LL/TLV index of <25%) that fulfilled the criteria for preoperative portal vein embolization or for staged hepatectomy to induce compensatory remnant hypertrophy.^16,17

For extended right/left hepatectomies with left trisectionectomy (segment 1-4 + 5/8), 29 livers (21%) had an RL/TLV index of <25%, thus within a limit for a safe RV. Eleven livers (8%) had a large MHV drainage volume in segment 6 (>30%) at risk of extensive remnant congestion. A favorable IHV/RL index (>50%) was seen in 18 livers (13%). In 2 livers, a large IHV/segment 5 index (>30%) allowed for a comfortable extended left hepatectomy.¹⁸

Discussion

Territorial liver anatomy is still poorly defined and classified. Three-dimensional imaging techniques have recently allowed for the estimation of individualized intrahepatic inflow/outflow PV and HV crossmatch volumes.^19-21 Fischer and colleagues showed a strong disparity of portal maps when comparing state-of-the-art 3D imaging to conventional 2-dimensional CT segmental volume estimations.¹¹ In their analysis, small hepatic segments revealed the greatest size-shape-topography discrepancy among the 2 imaging modalities. Our 3D CT study addressed both “individual variability” and “physiologic plasticity” among healthy human livers, providing actual size-shape-topography of each individual portal (sub)segment and venous (sub)territory derived from the anatomy and distribution of intrahepatic PV and HV branching.

Couinaud’s 1-2-8 scheme represents an “ideal” anatomic model.²² The 1-2-20 ramification scheme recently proposed by Fasel⁵ described up to 20 peripheral PV branches that could not be clearly assigned to either sectorial (second-order) or segmental (third-order) levels. Fasel and colleagues stated that inherent individual multiramification, rather than predetermined hierarchical binary branching pattern, might provide a reasonable explanation for the “non-sectoriality/nonsegmentality” of their alternative “multi-territorial PV model.”²³ Our previous studies described the virtual backward shifting of branching hierarchy with random bi-/trifurcation constellations and duplication of sectorial or segmental branches.^24,25

Our actual work provides the first complete systematic approach to functional liver anatomy and represents the continuation of Couinaud’s pioneering work on liver casts. Our special focus addressed the essential queries for planning high-risk hepatec-tomies.

The primary aim was to identify “dominance” patterns in PV and HV maps based on the PV and HV branching anatomy encountered in healthy human livers. We found an extensive variability in PV and HV territorial anatomy under physiologic conditions. These findings also confirmed our previous observations describing considerable differences in HV drainage patterns, especially in the RHH.⁶ Tumoral (micro)vascular invasion and fibrotic/cirrhotic “remodeling” may further modify locoregional perfusion, leading to compensatory collateralization and parenchymal hypo/hypertrophy.^4,26

Our segmental map showed a profile consistent with the Tokyo series,²⁷ with a clear dominance of RHH, RM, and segment 8 volumes in total liver and the greatest volume variability in the RM sector and segment 5. In contrast, the LM sector and segment 4a had the highest volume consistency. Our inflow/outflow simulation showed a dominant RHV drainage in RHH, RL and a dominant LHV drainage in LHH, LL irrespective of the presence of IHV. Consistent with the findings of the Heidelberg series, we identified a dominant LHV drainage of segments 2 and 3 and an MHV dominance in segments 4A/B.²⁸ The drainage dominance in the RM sector shifted between MHV and RHV depending on the presence or absence of an accessory IHV. For total liver, RHV had both the largest volume estimate and the greatest volume variability, whereas LHV had both the smallest volume estimate and the least volume variability.

The second aim of this systematic study addressed the practical surgical query for favorable outcomes in extensive liver resections. Our virtual risk analysis depicted adequate RV and also high-risk congestive volumes relevant to the unaffected remnant liver function.

Although successful liver resections have been reported in the setting of RV/TLV <25% and optimal liver quality, RV/TLV of at least 25% to 30% is usually required to avoid small-for-size syndrome.¹⁶ Our virtual right trisectionectomy involved 92% marginally small remnants formed by the LL sector with borderline RV/TLV index of <25%. In comparison, our simulated left trisectionectomy had only 21% small-for-size remnants formed by the RL sector, requiring portal vein embolization for compensatory parenchymal growth to avoid postoperative liver failure.^3,17

In the setting of extended MHV-inclusive left hepatectomies (segments 1-4 + part 5/8), favorable IHV drainage of segment 5 can prevent serious local parenchymal congestion associated with the loss of MHV outflow. In contrast to our findings (we observed IHV drainage of segment 5 in 39% of cases), Buhe and colleagues in an autopsy study of 60 livers detected IHV branches draining only segments 6 and 7.¹⁸ In our left trisectionectomy simulations with liver remnants formed by RL, IHV had a 25% dominance and a 31% mean drainage volume for RL. Moreover, in 37% of our IHV-containing remnant livers, a favorable dominant (up to 100% volume) IHV drainage of segment 6 was identified. In contrast, in 8% of cases, we estimated a risky large MHV/segment 6 index of >30%, including a maximal 84% drainage of segment 6. In the latter anatomy constellation, the reconstruction of MHV/segment 6 tributaries to provide an optimal outflow should be considered, particularly in cases with marginally small liver remnants.

Inclusion of the MHV with LHH grafts remains the preferred option for adult living donor liver transplant.²⁹ Congestive volumes in LHH are dependent on the highly variable MHV anatomy. In the livers analyzed in our study, 24% showed a risky MHV/LHH index of >40%, suggesting MHV inclusion regardless of graft size. In comparison, the Nakamura and Tsuzuki ⁹ favorable type I-dominant LHV drainage of segment 4A/B with an LHV/LM index of >50% (allowing to safely forgo MHV drainage in the marginal area of the left graft) was encountered in only 3 (2%) of our livers.

Conclusions

Virtual LHH graft hepatectomies allowed a safe MHV graft exclusion in only 2% of the livers analyzed in our study. Virtual right versus left trisectionectomies identified small-for-size remnants at high risk for small-for-size syndrome with borderline RV/TLV index of <25% in 92% of LL and only 21% of RL sectors. Three-dimensional inflow/outflow crossmatch volumes for left trisectionectomy showed the following. First, a predominantly favorable MHV drainage pattern was shown, including MHV low mean drainage of 7.5% RL versus 10% segment 6 versus 3% segment 7. Second, there was a seldom risky MHV drainage pattern for severe venous congestion, including dominant drainage of 35% to 42% RL in 1.5% and large MHV/segment 6 index of >30% in 8% of livers. Third, there was a predominantly beneficial IHV drainage pattern, including IHV large mean drainage of 31% RL (maximum 95% RL), IHV/RL index of >50% in 13% of livers, IHV dominant drainage in segment 6 (up to 100% volume) in 37% of livers, and IHV dominant drainage in segment 7 (up to 100% volume) in 19% of livers.

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