Branching patterns of the left portal vein and consequent implications in liver surgery: The left anterior sector

Mtti Grncini MuroAlessndro Scotti Luc Ginotti Antonio Rovere Fio Uggeri Mrco Brg Frizio Romno

a Unit of Hepatobiliary Pancreatic Surgery, Department of General Surgery 1, ASST-Monza, San Gerardo Hospital, Milano-Bicocca University, via Pergolesi 33,20900 Monza, MB, Italy

b Unit of Interventional Radiology, Department of Radiology, ASST-Monza, San Gerardo Hospital, Milano-Bicocca University, via Pergolesi 33, 20900 Monza,MB, Italy

TotheEditor:

There are still some open issues about the systematization of the knowledge of the branching of the left portal vein (LPV) and the division in anatomo-functional units within the left liver.

The first controversial topic concerns the division of S4 in subsegments.The Brisbane 20 0 0 system of Nomenclature of Hepatic Anatomy and Resections (B20 0 0) [1]does not mention such subdivision, but in literature this is still a matter of discussion.Some scholars described S4 ′ s vascularization as a “bouquet of vessels”from the right horn (the right distal branching at the tip of LPV) and found no rational in subdividing S4 [2].On the contrary, others reported that S4 may have several portal branches originating even from the umbilical portion (UPLPV), the angle,or the transverse portion of the LPV (TPLPV) and concluded that frequently S4a (the superior portion of S4) and S4b (the inferior portion of S4) are independently supplied and represent two separated subsegments [3].

The second open issue regards the division in sectors within the left liver.As reported in literature, hepatic sectors are defined as anatomical portions of parenchyma delimited by main hepatic veins and supplied by independent portal pedicles (PPs) [4].Following the B20 0 0, the left liver should be divided into a left lateral sector including S2 (whose sectorial PP, in truth, is the segmental PP for S2) and a left medial sector including S3 and S4 (whose sectorial PP should be represented by the distal portion of the LPV downstream of the origin of S2).The precise relationship between the origins of segmental PPs for S4 and for S2 may be crucial: in presence of portal branches for S4 originating upstream of portal branches for S2, the independence of the sectorial PP for the left medial sector may be questioned, and the surgical strategy to plan an anatomic left medial sectorectomy may be a matter of discussion.

The aim of this study was to analyze the branching patterns of the LPV, in order to assess if S4a and S4b have independent segmental PPs, if left medial sector and left lateral sector have independent sectorial PPs, and eventually to explore alternative modalities for the division of the left liver in anatomo-functional units consistent with the more frequent branching patterns of the LPV.

A retrospective review of 204 triphasic contrast enhanced computed tomography (CECT) of the abdomen was performed.All the CECTs were performed in ASST-Monza, San Gerardo Hospital, between January 1 and March 15, 2019, using a Philips ICT ELITE 256 layer.Exclusion criteria were: previous liver surgery and portal thrombosis.

For each CECT, the following data were collected and analyzed:age, sex, presence, site of origin and number of PPs for S2, S3, S4a and S4b, relationship between the origin of PPs supplying S2 and S4.

Terminology for liver anatomy and resection was based on the B20 0 0 [1].We referred to the anatomic course of the LPV as reported in literature [5].In order to systematize our analysis, we detailed the branching of the LPV not in general terms of branches or vessels, but in terms of PPs.A PP was considered in functional terms, considering only its origin and the portion of parenchyma supplied; moreover, when a portal branch was represented by a bouquet of vessels originating next to each other (within 5 mm), it was considered as one PP regardless of the number of vessels that made it up ( Fig.1 A).

Among 204 patients enrolled in this study, 96 (47.1%) were female, and 108 (52.9%) were male; mean age was 65.8 years.Three patients with sectorial PP for the right anterior sector originating from the LPV and 1 patient with agenesis of the left lobe were excluded.Among the 200 remaining cases, all the types of branching of the LPV were registered and those with similar characteristics were grouped, obtaining 4 main patterns.Normal anatomy with at least one independent PP for each of S2, S3, S4a, S4b (pattern I)was seen in 149 patients (74.5%).Anomalies with only one common PP for S2/S3 (pattern II), 1 common PP for S4a/S4b (pattern III) or common PPs for both S2/S3 and S4a/S4b (pattern IV) were found in 10 (5.0%), 37 (18.5%) and 4 (2.0%) patients, respectively( Fig.1 B).

Fig.1.The terminology and 4 main patterns of branching of the LPV.A: The terminology used in the present survey regarding the anatomy of the PV and the definition of PP (the curve of the LPV directed anteriorly and separating the TPLPV from the UPLPV is named the “angle of the LPV”); B: the 4 main patterns of branching of the LPV and their incidence were reported.Each pattern was represented by a picture; these pictures must be considered conceptual stigmatizations of the LPV’s branching.To simplify pictures, when a segment/subsegment was supplied by more than one PP, only the more frequent or representative PP was illustrated; independent PPs for S4a,when present, were always represented originating from the angle of LPV.PP: portal pedicle; PV: portal vein; LPV: left portal vein; RPV: right portal vein; TPLPV: transverse portion of the left portal vein; UPLPV: umbilical portion of the left portal vein.

In detail, regarding portal supply of each segment/subsegment:PP for S2 was single in 84.5% and originated mostly from the angle of the LPV (75.5%) or the UPLPV (21.0%); PP for S3 was single in 79.0% and originated from the left horn in 99.0%.S2 and S3 had a common PP in 7.0% of cases.S4 showed a peculiar and complex portal vascularization with multiple branches originating from different portion of the LPV.A PP originating from the right horn was present in 98.5% of cases, and supplied only S4b in 19.5% of cases and both S4a and S4b (common PP) in 79.0%.S4a in 79.5% of cases was additionally supplied by 1 to 4 further PPs (1 in 33.0% of cases, 2 in 36.0%, 3 in 25.0%, 4 in 6.0%) originating from the UPLPV(64.5%) and/or the angle of LPV (17.5%) and/or the TPLPV (37.5%)and/or from a common PPs for S2 (2.0%) or S1 (0.5%), and/or from the right portal vein (RPV, 0.5%).

In a functional and surgical perspective, in 79.5% of patients(corresponding to patterns I + II patients), S4a and S4b had independent segmental PPs and could be considered two independent subsegments: after the theoretical surgical removal of S4b with section of the PP of the right horn at its origin, S4a would maintain its independent PP; similarly, after the surgical removal of S4a with section of its PP(s), the PP (mostly common for both S4a/S4b) originating from the right horn would become proper for S4b.

Regarding the subdivision in sectors, our analysis focused on the relationship between the origins of PPs for S2 and S4.The origin of all PPs for S4 was downstream of the PP(s) supplying S2 only in 66 cases (33.0%, mostly pattern III patients).In the remnant 67.0%, one or more PPs for S4a (originating from UPLPV, angle, TPLPV, RPV, branches for S2 or S1) originated at the same level or upstream from the PP supplying S2.

As a result, in 2/3 of patients the sectorial PP for the left medial sector could not be considered independent from the sectorial PP for left lateral sector, and the subdivision in sectors of the left liver following the B20 0 0 didn’t appear to respect the principle of independence of sectorial PPs [4].

Alternative modalities for the division of the left liver in sectors basing on the more frequent branching pattern of the LPV were analyzed: the anterior/posterior criteria appeared to be more suitable.In all pattern I patients, the anterior portion of the left hemiliver including S3 and S4b could be considered as a“l(fā)eft anterior sector”, being delimited by hepatic veins and supplied by an independent sectorial PP represented by the distal portion of the LPV downstream the origin of PPs for posterior segments (S2 and S4a).The cranial boundary of the left anterior sector may vary depending on the vascular territories of S4a and S4b.

The left anterior sector could be identified even in pattern II(including S2, S3, S4b) and pattern III patients (including S3, S4a,S4b; in such cases the left anterior sector overlaps with the left medial sector), but not in pattern IV.Overall, the presence of left anterior sector could be confirmed in 98.0% of patients, corresponding to all cases in which the theoretical section of the UPLPV(downstream the origin of PPs for posterior segments) and the removal of the anterior portion of the left liver (S3 + S4b in pattern I, S2 + S3 + S4b in pattern II, S3 + S4 in pattern III), would be possible sparing the posterior segments (S2 and/or S4a) and their PPs.

It is illustrated that in different types of branching of the LPV,the comparison of the sectorial PPs of the traditional left medial sector and of the proposed left anterior sector ( Fig.2 ).

Fig.2.This picture illustrates, in presence of different branching of the LPV (pattern I and III), the comparison of sectorial PP of the traditional LMS (dark grey) and of the proposed LAS (light grey).A: The sectorial PP for LAS overlapped with the sectorial PP for LMS; both of them were consistent with the principle of independence of sectorial PPs (pattern III, 18.5% of cases); B: the sectorial PP for LAS differed from the sectorial PP for LMS; both of them were consistent with the principle of independence of sectorial PPs (pattern I with PPs for S4a originating downstream of PP for S2, 14.5% of cases); C: the sectorial PPs of LAS and LMS differed from each other; only for the LAS the principle of independence of sectorial PPs was respected (pattern I with PPs for S4a and S2 originating at the same level, 22.0% of cases); D: the sectorial PPs of LMS and LAS differed from each other; only for the LAS the principle of independence of sectorial PPs was respected [pattern I with at least one PP for S4a originating upstream of S2’s pedicle (38.0% of cases)].LPV: left portal vein; PP: portal pedicle; LMS: left medial sector; LAS: left anterior sector.

A good knowledge of the anatomy is a prerequisite for modern surgery of the liver [6]; the classification of precise anatomical references may be an important tool to identify and isolate the Glissonian sheaths and to simplify and make safer the anatomical liver surgery, in particular within the left liver where the LPV runs superficially in its fissures [7].

Some studies have previously described the anatomy of the LPV and found, within the left liver, up to 16 second-order branches and relative vascular territories and up to 9 branches supplying only a single segment [ 5 , 8 ].These studies were very explicative about the complexity of the left liver’s vascular anatomy and about the difficulty in developing reliable criteria of investigation and systematization.

The presence of portal branches for S4 arising directly from a portion of the LPV more proximal than the right horn in near 75%-80% of patients had been already described in literature [ 5 , 9 , 10 ].Our anatomical study confirmed this finding, and investigating the independence of PPs for S4a and S4b substantiated the rational to subdivide S4 in subsegments.

In literature, the division into sectors within the left liver has been widely discussed [ 4 , 11 ].The B20 0 0 managed to systematize this difficult topic.On the other hand, our finding regarding the non-independence between sectorial PPs for left medial sector and left lateral sector raised a practical question: from a surgical point of view, in presence of a tumor invading the sectorial PP of the left medial sector represented by the distal portion of the UPLPV,could it be technically feasible to perform a left medial sectorectomy with section of the sectorial PP at its origin (upstream from the origin of all the PPs supplying the left medial sector)? In the light of our results, the answer is that in 2/3 of patients it would not be possible to section the left medial sectorial PP without removing the segmental PP for S2 and performing a left hepatectomy( Fig.2 C and D).

To consider S4a and S4b as separated subsegments opened the field to a different subdivision in sectors within the left liver.Taking into account here the proposed definition of left anterior sector, the same oncological situation (tumor invading the distal portion of the UPLPV) could be theoretically managed in 98% of cases with the removal of left anterior sector, sparing S2 and/or S4a.

The concept of left anterior sector was firstly introduced by Henry Bismuth.In 1982, he proposed a revision of Couinaud’s systematization of the liver anatomy and subdivided the left hemiliver in a “l(fā)eft anterior sector”, including S4 and S3, and a “l(fā)eft posterior segment”, including S2 [11].This nomenclature was not adopted by the B20 0 0 which kept to subdivide the left hemiliver in terms of medial/lateral and not in terms of anterior/posterior [1].

We now discuss the concept of left anterior sector again, agreeing with the categorization in terms of anterior/posterior as more anatomically faithful.On the other hand, our concept of left anterior sector has some differences com pared to the one introduced by Prof.Bismuth, and could be considered a revisiting in the light of the subdivision of S4.

It must be specified that our concept of left anterior sector does not allow to clearly define a “l(fā)eft posterior sector”, but just one or two separated segments/subsegments (S2 and/or S4a).We believe that this peculiarity is not related to the concept of left anterior sector itself or to the type of classification (similarly, in the B20 0 0, the left lateral sector is a segment), but it should be addressed to the particular anatomy of the LPV.While the RPV is a short, centrally located vein that rapidly branches into sectorial vessels which in turn give segmental vessels, the LPV (for reasons connected with embryological development and fetal life) is a long conduit that runs itself to the periphery, yielding its segmental and subsegmental branches directly from the main trunk.RPV and LPV are different from each other; as a consequence, the left and right hemilivers are different and probably cannot be subdivided with the same criteria.

The main limitation of this study is the relatively small population.Moreover, it may be argued that the proposed concept of left anterior sector does not consider the arterio-biliary second-order branching.In this sense, Couinaud reported that, in the perspective to classify liver anatomy and liver surgery, portal vein segmentation should be preferred to arterio-biliary segmentation for beingmore reliable and accurate for both embryological and anatomical reasons [12].On the other hand, the concept of left anterior sector has been verified from the point of view of the arterio-biliary branching.

In conclusion, the LPV’s branching can be classified in 4 main patterns; S4a and S4b should be considered two functionally independent subsegments; the proposed left anterior sector could be considered a newanatomic entity of the left liver consistent with the branching of the LPV.

Acknowledgments

None.

CRediT authorship contribution statement

Mattia Garancini:Conceptualization, Methodology, Data curation, Formal analysis, Writing –original draft.Mauro Alessandro Scotti:Methodology, Data curation, Formal analysis, Investigation.Luca Gianotti:Supervision, Writing –review & editing.Antonio Rovere:Data curation, Formal analysis.Fabio Uggeri:Data curation, Formal analysis.Marco Braga:Supervision, Writing –review& editing.Fabrizio Romano:Supervision, Writing –review & editing.

Funding

None.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964DeclarationofHelsinkiand its later amendments or comparable ethical standards.

Competing interest

No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.