Abstract
Anatomical variations of the right hepatic vein, especially large variant right hepatic veins (≥5 mm), have important clinical implications in liver transplantation and resection. This study aimed to evaluate anatomical variations of the right hepatic vein using quantitative three‐dimensional visualization analysis. Computed tomography images of 650 patients were retrospectively analyzed, and three‐dimensional visualization was applied using the derived data to analyze large variant right hepatic veins. The proportion of the large variant right hepatic vein was 16.92% (110/650). According to the location and number of the variant right hepatic veins, the configuration of the right hepatic venous system was divided into seven subtypes. The length of the retrohepatic inferior vena cava had a positive correlation with the diameter of the right hepatic vein (rs = 0.266, p = 0.001) and the variant right hepatic veins (rs = 0.211, p = 0.027). The diameter of the right hepatic vein was positively correlated with that of the middle hepatic vein (rs = 0.361, p < 0.001), while it was inversely correlated with that of the variant right hepatic veins (rs = −0.267, p = 0.005). The right hepatic vein diameter was positively correlated with the drainage volume (rs = 0.489, p < 0.001), while the correlation with the variant right hepatic veins drainage volume was negative (rs = −0.460, p < 0.001). The number of the variant right hepatic veins and their relative diameters were positively correlated (p < 0.001). The volume and percentage of the drainage area of the right hepatic vein decreased significantly as the number of the variant right hepatic vein increased (p < 0.001). The findings of this study concerning the variations of the hepatic venous system may be useful for the surgical planning of liver resection or transplantation.
Keywords: 3D visualization, anatomical variation, large variant hepatic vein, quantitative anatomy, right hepatic vein
In this study, we used three‐dimensional visualization to classify the right hepatic venous system into seven subtypes according to the location and number of the variant right hepatic veins. The length of the retrohepatic inferior vena cava was positively correlated with the diameters of the right hepatic vein and variant right hepatic vein, while there was a negative correlation between the diameters of right hepatic vein and variant right hepatic vein. Variant right hepatic vein numbers were inversely proportional to the contribution of right hepatic vein to liver drainage.

1. INTRODUCTION
The correct understanding of complex vascular anatomy, including variations in the right hepatic vein (RHV), is important for successful liver surgery outcomes (Cawich et al., 2021; Majno et al., 2014; Sato et al., 2014; Watanabe et al., 2020). In liver transplantation, large right variant hepatic veins (VRHV) with a diameter of 5 mm must be reconstructed to form clear venous outflow pathways and prevent the graft from becoming congested, which can lead to functional impairment (Ito et al., 2016; Uchida et al., 2010). During liver resection, the presence of large VRHVs requires more diversified hepatectomy methods to achieve a satisfactory prognosis (Felli, Meniconi, Colasanti, Vennarecci, & Ettorre, 2018; Jiang, Wang, Xu, Wu, & Ding, 2014; Kubo et al., 2020).
The anatomy of the hepatic venous system has been studied in the past using cadaveric specimens and corrosion casts (Hribernik & Trotovšek, 2014; Liu, Chen, Chen, Guo, & Li, 2013). However, due to the loss of blood pressure and changes in the physiological state of the cadaver liver, the shape of the blood vessels is different from the living organ. Two‐dimensional (2D) images such as ultrasound and computed tomography (CT) have also been used to assess the hepatic vascular anatomy (Radtke et al., 2010; Sharma, Sood, Singh Chauhan, Verma, & Kapila, 2019), but measurement in 2D images is a single dimension and it is challenging to select the best measurement plane. However, assessment of the vasculature is not always accurate, as it is difficult to accurately measure anatomical features and conduct a quantitative analysis. As a consequence, there is still controversy surrounding the types of VRHV across different studies.
In recent years, three‐dimensional (3D) visualization has been widely used in liver surgery and has achieved satisfactory results (Fang, Zhang, & Qi, 2019; Mise et al., 2018). The 3D visualizations created from high‐quality CT data allow not only a stereoscopic view of the structural features of the liver and the vascular anatomy, but also enable the accurate and direct measurement of the diameter of the vessels as well as the volumes of their drainage areas (Ohshima, 2014). To our best knowledge, this is the first study to report the detailed evaluation and quantitative analysis of the right hepatic venous system with large VRHVs based on 3D visualization.
2. METHODOLOGY
2.1. Patient selection
From January 2015 to September 2021, 650 patients who underwent enhanced abdominal CT were evaluated and screened. CT images of patients with large VRHV (≥5 mm) were included in the study. Patients with large liver masses compressing veins were excluded. Patients with other conditions that influenced the return of blood from the liver to the inferior vena cava (IVC), such as severe cirrhosis, large hemangiomas, severe portal hypertension, significant dilation of the bile duct, and a history of liver surgery, were also excluded from the study. The research protocol was approved by the Institutional Ethics Review Committee.
2.2. Reconstruction of 3D models and quality control
CT data was uploaded to the 3D visualization software Medical Image 3D Visualization System (MI‐3DVS; software copyright no. 2008SR18798) developed by our team to reconstruct the 3D models of the liver and blood vessels of patients with large VRHVs (≥5 mm) (Fang et al., 2015; Fang et al., 2020). To extract the edge ramifications and complete the data segmentation, we used an additional semi‐automatic setting of the seeding point. Each hepatic vein was extracted from the confluence with the IVC using the same settings. Following total liver volume and vascular reconstruction, the hepatic vein branches were established as the central point for virtual liver segmentation to construct the drainage area of the hepatic vein based on its course.
During the CT data acquisition and 3D reconstruction process, the following conditions are required to achieve a high degree of homogeneity: (1) Patients were instructed to hold their breath during the CT scan to avoid segmentation and difficulties in registering images from different periods. (2) The thickness of each layer of the original CT examination image was 1 mm. (3) The main trunk of the portal vein or IVC was the standard for defining the first‐level branch, and the 3D reconstruction of the intrahepatic vascular branches reached levels 3–4. (4) The 3D models were jointly determined, manually verified, and appropriately modified by the same group of liver surgeons and radiologists.
2.3. Hepatic vein evaluation criteria
A RHV was defined as a main hepatic vein that directly enters the IVC from the upper right side of the liver. In the present study, a VRHV was defined as a draining vein of the right hepatic lobe connected to the IVC independently of the RHV. The retrohepatic inferior vena cava (RHIVC) was defined as the portion of the IVC from the upper margin of the RHV confluence to the lower margin of the lowest variant hepatic vein confluence. A VRHV that drains blood from the upper third, middle third, or lower third of RHIVCs was defined as a superior variant right hepatic vein (sVRHV), middle variant right hepatic vein (mVRHV), or inferior variant right hepatic vein (iVRHV), respectively (Figure 1a).
FIGURE 1.

Classification of the right hepatic venous system. (a) Hepatic vein evaluation criteria. The retrohepatic inferior vena cava was defined as the part of the IVC extending from the upper margin of the RHV confluence to the lower margin of the lowest VRHV. A VRHV that drains blood in the upper third, middle third, and lower third of RHIVC was defined as sVRHV, mVRHV and iVRHV, respectively. (b) Classification of the right hepatic venous system. Type I, the RHV and iVRHV together dominate the right liver. Type Ia, including RHV and 1 iVRHV; Type Ib, including RHV and 2 iVRHVs; Type Ic, including RHV and 3 iVRHVs. Type II, RHV, iVRHV, and mVRHV together dominate the right liver; which can be subdivided into Type IIa, including RHV, mVRHV and 1 iVRHV; Type IIb, including RHV, mVRHV and 2 iVRHVs. Type III, RHV, iVRHV, and sVRHV together dominate the right liver and can be subdivided into Type IIIa, including RHV, sVRHV and 1 iVRHV; and Type IIIb, including RHV, sVRHV and 2 iVRHVs. In the present study, there were cases of with two concurrent mVRHVs or sVRHVs when the iVRHV was present. Further, there were no cases with concurrent presence of iVRHV, mVRHV, and sVRHV. Therefore, patients with Type IIc and Type IIIc were absent from this study. (c) Classification of the right hepatic venous system on three‐dimensional visualization. IVC, inferior vena cava; RHV, right hepatic vein; sVRHV, superior variant right hepatic vein; mVRHV, middle variant right hepatic vein; iVRHV, inferior variant right hepatic vein; RHIVC, retrohepatic inferior vena cava.
Due to lower blood pressure, the shape of the hepatic vein is elliptical rather than round like an artery. Thus, the diameter of the hepatic vein in this study was measured using the long diameter of the elliptical opening at the root of the vessel. The length of the RHIVC and the diameter of the hepatic vein were measured using the diameter measurement tool provided with the 3D visualization software. When there were multiple VRHVs, the sum of the diameters of all variant veins was calculated.
2.4. Classification of venous patterns
Based on the location of the entrance of the VRHV, the right hepatic venous system was classified into three major types: Type I (RHV and iVRHV); Type II (RHV, iVRHV, and mVRHV); and Type III (RHV, iVRHV, and sVRHV). According to the number of iVRHVs, each type can be subdivided into subtype a, one iVRHV; subtype b, two iVRHVs; subtype c, and three iVRHVs (Figure 1b).
2.5. Calculation of hepatic vein drainage area volume
Each hepatic vein was individually characterized and analyzed using MI‐3DVS with regard to the RHV, middle hepatic vein (MHV), left hepatic vein (LHV), and VRHVs. The liver was divided into several hepatic venous drainage regions based on the distribution of each hepatic venous tree. These regions of the liver dominated by independent hepatic veins were defined as hepatic venous drainage areas (Figure 2). The volume of these hepatic venous drainage areas was measured using a volumetric tool. In the presence of multiple hepatic venous drainage areas, the sum of their volumes was calculated.
FIGURE 2.

Division of the hepatic vein drainage area. (a) Three‐dimensional reconstruction of the hepatic veins. (b) The liver is divided into several hepatic venous drainage areas according to the hepatic vein distribution. RHV, right hepatic vein; iVRHV, inferior variant right hepatic vein; MHV, middle hepatic vein; and LHV, left hepatic vein.
2.6. Data analysis
Comparisons between veins and their relationships were evaluated using Student's t‐test, Shapiro–Wilk test, and Spearman's correlation analysis. The Shapiro–Wilk test and Spearman's correlation analysis were also used to analyze the relationship between veins and drainage volume. The Kruskal–Wallis test was used to analyze the correlation of the number of variant hepatic veins with the diameter of the vein and the volume of the drainage area. Differences between groups were evaluated using the Bonferroni method for multiple comparisons. Differences with p‐values <0.05 were considered statistically significant. All statistical analyses were performed in SPSS 26.0 for Windows (IBM Corp.).
3. RESULTS
3.1. Classification of the right hepatic venous system
Of the 650 initially selected patients, 110 had VRHV and were selected for 3D reconstruction; the occurrence rate of VRHV was 16.92% (110/650).
The configuration of the right hepatic venous system was divided into seven types: Type Ia (59/110, 53.64%), including the RHV and one inferior variant right hepatic vein (iVRHV); Type Ib (31/110, 28.18%), including the RHV and two iVRHVs; Type Ic (1/110, 0.91%), including the RHV and three iVRHVs; Type IIa (11/110, 10.00%), including the RHV, middle variant right hepatic vein (mVRHV) and one iVRHV; Type IIb (3/110, 2.73%), including the RHV, mVRHV and two iVRHVs; Type IIIa (4/110, 3.64%), including the RHV, superior variant right hepatic vein (sVRHV) and one iVRHV; as well as Type IIIb (1/110, 0.91%), including the RHV, sVRHV, and two iVRHVs. In the present study, when the iVRHV was present, there were no concurrent cases of two mVRHVs or two sVRHVs. There was also no simultaneous presence of iVRHV, mVRHV, and sVRHV (Table 1 and Figures 1b,c).
TABLE 1.
Classification and diameter of the right hepatic vein system.
| Mean length/diameter (mm) | Type Ia 59/110 (53.64%) | Type Ib 31/110 (28.18%) | Type Ic 1/110 (0.91%) | Type IIa 11/110 (10%) | Type IIb 3/110 (2.73%) | Type IIIa 4/110 (3.64%) | Type IIIb 1/110 (0.91%) |
|---|---|---|---|---|---|---|---|
| RHIVC length | 56.54 | 57.27 | 63.90 | 61.71 | 64.83 | 61.08 | 52.90 |
| RHV diameter | 16.87 | 13.53 | 17.30 | 13.88 | 16.40 | 16.38 | 7.40 |
| MHV diameter | 12.07 | 11.69 | 7.60 | 11.47 | 17.23 | 11.43 | 11.90 |
| iVRHV diameter | 9.26 | 8.75 | 7.97 | 9.60 | 8.88 | 9.63 | 12.65 |
| mVRHV diameter | – | – | – | 7.03 | 8.23 | – | – |
| sVRHV diameter | – | – | – | – | – | 8.85 | 5.50 |
| VRHVs diameter | 9.26 | 17.50 | 23.90 | 16.63 | 26.00 | 18.48 | 30.80 |
Abbreviations. RHIVC, retrohepatic inferior vena cava; RHV, right hepatic vein; sVRHV, superior variant right hepatic vein; mVRHV, middle variant right hepatic vein; iVRHV, inferior variant right hepatic vein; VRHV, large variant hepatic vein.
3.2. Systematic analysis of the diameters of the hepatic veins
The diameters, lengths, and corresponding ratios of the hepatic veins are listed in Tables 1, S1. The results showed that the length of the RHIVC was positively correlated with the diameter of the RHV (rs = 0.266, p = 0.001) and the VRHVs (rs = 0.211, p = 0.027). The diameter of the RHV was positively correlated with that of the MHV (rs = 0.361, p < 0.001), while it was negatively correlated with the diameter of the VRHV (Figure 3).
FIGURE 3.

Relationship between the retrohepatic inferior vena cava and the right hepatic venous system in 110 patients. In the presence of multiple variant right hepatic veins (VRHVs), the sum of their diameters was calculated. (a). The correlation between the length of the retrohepatic inferior vena cava (RHIVC) and the diameter of the right hepatic vein (RHV) (rs = 0.266, p = 0.001). (b). The correlation between the length of RHIVC and the diameter of VRHV (rs = 0.211, p = 0.027). (c). The correlation between the diameter of the RHV and the diameter of the middle hepatic vein (MHV) (rs = 0.361, p < 0.001). (d). The correlation between the diameter of RHV and the diameter of VRHV (rs = −0.267, p = 0.005).
As shown in Figure 4, there was a positive correlation between the diameter and drainage volume of the RHV (rs = 0.489, p < 0.001), while there was an inverse correlation with the sum of the VRHV drainage volume (rs = −0.460, p < 0.001). Conversely, the sum of the diameter of VRHVs was positively correlated with their drainage volume (rs = 0.689, p < 0.001), while there was an inverse correlation with the RHV drainage volume (rs = −0.578, p < 0.001).
FIGURE 4.

Relationship between the diameter and drainage volume of the right hepatic venous system in 110 patients. In the presence of multiple variant right hepatic veins (VRHVs), the sum of their respective diameters and drainage volume was calculated. (a). The correlation between the diameter and drainage volume of the right hepatic vein (RHV) (rs = 0.489, p < 0.001). (b). The correlation between the diameter of the RHV and the drainage volume of VRHVs (rs = −0.460, p < 0.001). (c). The correlation between VRHV diameter and VRHV drainage volume (rs = 0.689, p < 0.001). (d). The correlation between diameter of VRHVs and drainage volume of RHV (rs = −0.578, p < 0.001).
3.3. Analysis of the number of VRHVs
According to the subtypes identified in this study, the one VRHV group included type Ia, the two VRHVs group included types Ib, IIa, and IIIa, while the three VRHVs group included types Ic, IIb, and IIIb. There were significant differences in the diameter of the RHV across the three groups (p = 0.002). When there was only one VRHV, the diameter of the RHV was greater than in the group with two VRHVs (p < 0.05). With increasing numbers of VRHVs, their diameters increased significantly (p < 0.001) (Table 2 and Figure 5).
TABLE 2.
Relationship between the number of VRHV and the diameter and drainage volume of the hepatic veins.
| Number of VRHV | RHV diameter (mm) | VRHV diameter (mm) | RHV drainage volume (mL) | VRHV drainage volume (mL) | Percentage of RHV drainage volume (%) | Percentage of VRHV drainage volume (%) |
|---|---|---|---|---|---|---|
| 1 (n = 59) | 16.87 ± 4.66* | 9.26 ± 2.57*# | 342.74*# (286.25–423.91) | 109.93*# (68.94–170.71) | 34.39*# (26.14–40.98) | 10.59*# (7.29–14.91) |
| 2 (n = 46) | 13.86 ± 3.80 | 17.37 ± 3.99 | 191.01 (141.56–332.83) | 217.01 (142.89–267.53) | 20.49 (13.58–29.94) | 20.31 (14.63–25.58) |
| 3 (n = 5) | 14.78 ± 5.36 | 26.54 ± 3.34 | 180.63 (148.40–239.86) | 244.36 (236.70–267.44) | 19.28 (13.55–22.22) | 23.06 (21.42–27.00) |
| p ‐values | 0.003 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 |
Note: *p < 0.05 for 1 VRHV versus 2 VRHVs; # p < 0.05 for 1 VRHV versus 3 VRHVs. RHV, right hepatic vein; VRHV, variant hepatic vein.
FIGURE 5.

Relationship between the number of VRHV and the diameter of the hepatic vein. (a) Mean diameter of the RHV among the three groups with different numbers of VRHV (p = 0.003). (b) Mean diameter of VRHV among the three groups with different numbers of VRHV (p < 0.001). RHV, right hepatic vein; VRHV, variant hepatic vein.
The volume of the RHV drainage area and its relation to the total liver volume decreased significantly as the number of VRHVs increased (p < 0.001). By contrast, the drainage volume of the VRHV and its relation to the total liver volume increased with the increasing number of VRHVs (p < 0.001) (Table 2 and Figure 6).
FIGURE 6.

Relationship between the VRHV number and the volume of the drainage area. (a) The volume of the RHV drainage area among the three groups with different numbers of VRHV (p < 0.001). (b) The proportion of the volume of the RHV drainage area of the total liver volume among the three groups with different numbers of VRHV (p < 0.001). (c) The volume of the VRHV drainage area among the three groups with different numbers of VRHV (p < 0.001). (d) The percentage of volume of the VRHV drainage volume of the total liver volume among the three groups with different numbers of VRHV (p < 0.001).
4. DISCUSSION
In the present study, high‐quality homogenized CT data were translated into 3D visualizations to obtain a working model that can effectively reveal the actual structure of the human liver, allowing the quantitative analysis of the hepatic venous system. The right hepatic venous system was classified into seven subtypes based on the position and number of VRHVs. Previous studies have classified the right hepatic venous system according to the relative size and location of the hepatic veins without distinguishing their diameter (Masselot, 1978; Watanabe et al., 2020). However, large hepatic veins receive particular attention and careful management in the field of liver surgery, while small veins are often directly clipped or left untreated. Therefore, we excluded hepatic veins smaller than 5 mm in this study, which resulted in a 16.92% incidence of VRHVs, a rate that was lower than in other studies (Kamel et al., 2001; Koc, Ulusan, Oguzkurt, & Tokmak, 2007; Schroeder et al., 2006).
The length of the RHIVC was positively correlated with the diameters of the RHV and VRHV. The RHIVC, which is surrounded by the dorsal parenchyma of the liver, is the blood vessel at which all hepatic veins converge. The length of the RHIVC can be considered to demarcate the posterior height of the liver. Hepatic veins with a larger opening can support a larger liver volume to ensure smooth blood flow. The anatomical features of the RHIVC and its relationship with the hepatic veins have important clinical implications in the selection of surgical approaches and interventional treatment in Budd‐Chiari syndrome (Sharma et al., 2019).
The diameter of the MHV was positively correlated with that of the RHV, which is inconsistent with the conventional understanding that the presence of VRHVs results in significant changes in the constitution of the right hepatic outflow tract. Furthermore, the venous drainage of the right anterior section (segments V and VIII) proceeds via the MHV as well as the RHV, which may influence this presentation. The diameter of the RHV was negatively correlated with that of the VRHV, which is consistent across most studies (Fang et al., 2012; Sharma et al., 2019; Watanabe et al., 2020). A larger number of vessels results in greater importance of VRHVs for the liver's drainage system, while the diameter of the right hepatic vein gradually becomes smaller, and its share in the drainage of the right hepatic vein decreases.
The location and number of VRHVs are important factors in the diagnosis and treatment of liver diseases. VRHVs can form a collateral pathway with other veins in the liver to compensate for RHV obstruction due to right liver lesions, thus changing the expected disease process (Makuuchi et al., 1984). The presence of a VRHV necessitates a more specific and individualized choice of liver resection strategy. A large VRHV can limit the extent of liver resection, preserving the segment of the liver containing the VRHV to ensure adequate circulation of the remaining liver parenchyma without congestion. Segments or subsegments with large VRHVs can be retained without postoperative congestion during liver resection involving the right liver, such as segments VI and VII. Furthermore, in liver transplantation, it is generally accepted that anastomosis of the large VRHV in the graft to the recipient's IVC can reduce the risk of liver congestion and graft dysfunction.
Finally, in spite of its robust findings, this study also has some limitations. Although a large number of samples were collected in the present study, only five patients with three VRHVs were identified. A sufficient sample size will allow us to more fully explain the types and correlations of the right hepatic venous system in the future. However, because other hepatic veins can provide a strong synergistic effect on liver blood flow, the subpopulation with three or more VRHVs can be regarded as a rare minority. In addition, based on this study, additional blood reflux studies related to liver disease should be performed to better elucidate the clinical value of VRHVs.
5. CONCLUSIONS
In this study, we used 3D visualization to classify the right hepatic venous system into seven subtypes according to the location and number of VRHVs. The length of the RHIVC was positively correlated with the diameters of the RHV and VRHV, while there was a negative correlation between the diameters of RHV and VRHV. VRHV numbers were inversely proportional to the contribution of RHV to liver drainage. Based on these findings, it is recommended to evaluate the right hepatic venous system according to the current classification when performing liver resection, liver transplantation, and other clinical interventions that require a detailed understanding of the anatomical characteristics of the hepatic veinous system.
AUTHOR CONTRIBUTIONS
The study design was finished by Jinyu Lin, Haisu Tao, and Jian Yang. The acquisition of data was finished by Jinyu Lin, Junfeng Wang, Xinci Li, and Zhuangxiong Wang. The data analysis was finished by Jinyu Lin Haisu Tao, and Junfeng Wang. The drafting of the manuscript was finished by Jinyu Lin. The critical revision of the manuscript was finished by Jinyu Lin, Haisu Tao, Chihua Fang, and Jian Yang. All authors finished approval of the article.
CONFLICT OF INTEREST STATEMENT
All authors have no conflicts of interest or financial ties to disclose.
Supporting information
Table S1.
ACKNOWLEDGMENTS
This project was supported by National Natural Science Foundation of China (Grant No. 82272132), Guangdong Basic and Applied Basic Research Foundation (Grant No. 2021A1515011869), the Science and Technology Plan Project of Guangdong Province (Grant No. 2021A1414020003), Regional Joint Fund of Guangdong (Guangdong‐Hong Kong‐Macao Research Team Project) (Grant No.2021B1515130003), China Postdoctoral Science Foundation (Grant No. 2022 M721514), President's Fund of Zhujiang Hospital (Grant No.yzjj2022qn31).
Lin, J. , Tao, H. , Wang, J. , Li, X. , Wang, Z. , Fang, C. et al. (2024) Quantitative anatomy of the large variant right hepatic vein: A systematic three‐dimensional analysis. Journal of Anatomy, 244, 133–141. Available from: 10.1111/joa.13949
Jinyu Lin, Haisu Tao and Junfeng Wang had contributed equally to this work.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author 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.
Supplementary Materials
Table S1.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
