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10.1245/s10434-006-9087-8
Annals of Surgical Oncology 13:1560-1568 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Disruption of the Middle Hepatic Vein is not Crucial for Liver Regeneration of the Remnant Liver After Right Hemihepatectomy for Hepatic Tumors

Daisuke Morioka, MD, PhD, Kuniya Tanaka, MD, PhD, Hitoshi Sekido, MD, PhD, Ken-ichi Matsuo, MD, PhD, Mitsutaka Sugita, MD, PhD, Michio Ueda, MD, Itaru Endo, MD, PhD, Shinji Togo, MD, PhD and Hiroshi Shimada, MD, PhD

Department of Gastroenterological Surgery, Yokohama City University Graduate School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama, 236-0004, Japan

Correspondence: Address correspondence and reprint requests to: Daisuke Morioka, MD, PhD; E-mail: dmorioka{at}hotmail.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: To clarify the role of the middle hepatic vein (MHV) in liver regeneration of the remnant liver after right hemihepatectomy for hepatic tumors, we reviewed 29 patients to evaluate liver regeneration for up to 12 postoperative months.

Methods: Volume regeneration of the remnant liver was investigated by computed tomography at 3, 6, and 12 postoperative months. The remnant liver was divided into the following three areas: the medial section (segment IV), the lateral section (segments II and III), and segment I. The patients were divided into two groups: group A (n = 17), in which the MHV was preserved in the remnant liver, and group B (n = 12), in which the MHV was removed.

Results: Volume regeneration of each area continued until 6 postoperative months but did not increase thereafter. On univariate analysis, differences in the volume regeneration of each area between the groups were not significant at any measured time point. Furthermore, disruption of the MHV was determined to not be crucial to the volume regeneration of any liver area on multivariate analysis. Only the resection volume (percentage) significantly affected liver regeneration of the remnant liver.

Conclusions: Disruption of the MHV does not decisively affect liver regeneration of remnant liver after right hemihepatectomy for hepatic tumors.

Key Words: Right hemihepatectomy • Liver regeneration • Middle hepatic vein • Venous disruption


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Venous disruption had been considered to have no negative effect on liver regeneration after hepatectomy, on the basis of studies assuming that venous collaterals rapidly develop.1,2 However, to date, venous disruption has been shown to disadvantageously affect liver regeneration of the remnant or graft liver, primarily according to advances in living donor liver transplantation. Specifically, the middle hepatic vein (MHV) has been reported to play a significant role in liver regeneration of the medial section (MS; segment IV) in right-liver donors and in that of the anterior section (segments V and VIII) in left-liver donors or right-liver recipients, because the MHV is a main drainage vein for these liver areas.3–5 Although the authors of these previous studies based their conclusions regarding liver regeneration on results obtained at 3 months after hepatectomy, Pomfret et al.6 have reported that liver regeneration continues throughout the first postoperative year, according to their study of living right-liver donors. Therefore, an accurate evaluation of liver regeneration of the remnant liver in right-hepatectomized patients seems to require a serial observation for up to 12 postoperative months.

However, in the field of liver surgery for hepatic tumors, the resection of the MHV in right hemihepatectomy is often performed according to the location of tumors. In this study, we investigated how disruption of the MHV affects liver regeneration of the remnant liver in patients undergoing right hemihepatectomy for up to 12 postoperative months. The aim of this study was to determine whether disruption of the MHV is crucial when performing right hemihepatectomy for hepatic tumors.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Selection
From May 1994 to April 2003, of 487 patients undergoing hepatectomy at our institution, right hemihepatectomy with or without the preservation of the MHV was performed in 53 patients. Neither resection and reconstruction of the bile duct nor total resection of segment I (SI) was performed in these patients. Of these 53 patients, no patient died of posthepatectomy liver failure. Twenty-four of these 53 patients were excluded from the study; the reasons for the exclusion were living right-liver donors in 11 cases, portal embolization that preceded right hemihepatectomy in 9, and partial resection of the left liver or ablation therapy for the tumors located in the left liver in addition to the right hemihepatectomy in 4. Consequently, 29 patients who underwent right hemihepatectomy alone for hepatic tumors were enrolled in this study.

Preoperative Assessment of the Right-Hepatectomized Patients
Preoperative computed tomography (CT) was performed with a Hitachi model CTW-1000 (Hitachi Medico Co., Hitachi, Japan). Serial transverse scans were performed at 7-mm intervals from the dome to the most inferior part of the liver with contrast enhancement. The volume of the resected and overall liver, excluding tumors, was estimated by the methods described by Heyms field et al.,7 with minor modifications using digitizing software (Scion Image Beta 4.02; http://www.scioncorp.com, Maryland, USA). Volume estimation by using CT has been known to predict the actual liver volume with acceptable accuracy.8–10 The MHV and right hepatic vein, gallbladder, right portal vein trunk, umbilical portion of the left portal vein, left portal vein trunk, and inferior vena cava were used as landmarks to determine liver areas according to the International Hepato-Pancreato-Biliary Association Brisbane Classification for liver anatomy11 as follows: the posterior section (segments VI and VII), the anterior section (segments V and VIII), the MS (segment IV), the lateral section (LS; segments II and III), and SI. The estimated liver resection volume (percentage) was calculated from the estimated volume of the resected liver and overall liver:


Formula

The planned transecting line of the hepatectomy was determined on the basis of the patient’s diagnosis. In patients with malignant hepatic tumors, the planned transecting line was drawn along the right border of the MHV if all tumors were >1 cm from the MHV. If the most median tumor was located within 1 cm of the MHV, the MHV was considered to be involved in the resected liver, and the transecting line was drawn at least 1 cm from the tumor to ensure a safe surgical margin. In patients with benign tumors, the MHV was involved in the resected liver only if the tumor was in broad contact with the MHV. If not, the planned transection line was drawn along the right margin of the MHV. Two abdominal radiologists and two surgeons independently evaluated the borderlines between liver areas and came to a final consensus.

An indocyanine green test was performed within 1 week before surgery according to a method described elsewhere.12,13 We used the prediction score (PS) as introduced by Yamanaka et al.14 to determine whether a right hemihepatectomy was acceptable for an accordant patient. PS was calculated with the following formula:


Formula

where x1 is the resection volume (percentage) calculated from CT volumetry, x2 is the indocyanine green retention rate at 15 minutes, and x3 is the age of the patient. In patients with healthy liver or chronic hepatitic liver determined from their clinical findings, a PS ≤45 was acceptable for performing a right hemihepatectomy. In patients with cirrhotic livers, a PS ≤40 was acceptable. In patients who did not fulfill these criteria, other limited hepatic resection or other therapeutic modalities such as chemotherapy or ablation therapy were used for the treatment.

Operative Procedure
An inverted L–shaped incision was made, and the abdominal cavity was entered. First, the right hemiliver was mobilized to enable exposure of the right side of the inferior vena cava and isolation of the right hepatic vein outside the liver. After the mobilization of the right hemiliver, dissection at the right side of the liver hilum after cholecystectomy exposed the right hepatic artery and the right portal trunk. The right portal vein was freed, and individual branches to SI were divided between ties. Intraoperative ultrasonography was then performed to identify the major vascular structures and the orientation of hepatic tumors. Special attention was paid to the anatomy of the junction of the MHV and the left hepatic vein (LHV) and the presence of the fissure vein. In this study, we defined the fissure vein as the thickest vein distributing to the MS and joining within 2 cm to the right or left of the junction of the MHV and LHV.

The demarcation line produced by a temporary clamping of the right hepatic artery and right portal trunk was marked on the liver surface. Parenchymal transection was performed by using a Cavitron Ultrasonic Surgical Aspirator (CUSA System 200; Valleylab Inc., Boulder, CO). All sizable vascular and biliary structures were divided between ligatures. In patients with malignant hepatic tumors whose most median tumor was located >1 cm from the MHV or patients with benign hepatic tumors that were not in broad contact with the MHV, the transection plane was mostly in accordance with the demarcation line and designed to pass through the right margin of the MHV. In patients with malignant hepatic tumors whose most median tumor was located within 1 cm of the MHV or patients with benign hepatic tumors that were in broad contact with the MHV, the transection plane was designed to involve the MHV in the resected liver and to ensure a surgical margin of 1 cm if the diagnosis was malignant. When the MHV must be involved in the resected liver, careful attention must be paid to the division of the MHV to preserve the fissure vein, if present. In patients with extremely large hepatic tumors >10 cm in diameter, mobilization of the right hemiliver was preceded by parenchymal transection according to the methods introduced as "the anterior approach" by Liu et al.15

Measurement of Remnant Liver Volume on CT
Postoperative CT with contrast enhancement by using the same system and method as the preoperative CT evaluation was routinely conducted at 3, 6, and 12 postoperative months to evaluate postoperative liver volume regeneration. If some clinical problems arose, an additional CT examination was performed as the occasion demanded. The liver volume of the remnant liver was calculated by the same methods as were used in the preoperative assessment.

Volume Regeneration Rate
The term volume regeneration rate (VrR) was defined as the percentage of increase at each postoperative month in this study. The VrR of each area of the remnant liver, i.e., the MS, the LS, and SI, was calculated by using the following formula:


Formula

The VrR of each area was defined as follows: VrRMS, VrR of theMS; VrR-LS, VrR of the LS; VrR-SI, VrR of the SI; and VrR-WL, VrR of the overall remnant liver.

Statistical Analysis
Relationships between volume regeneration of each area of the remnant liver and some variables that seem to affect liver regeneration, including the body-surface area,13 which were calculated with the equation of Du Bois and Du Bois,16 liver-function variables, pathologic findings of background liver, and the like, were statistically analyzed with univariate analysis and multivariate analysis. Pathologic findings of background liver were determined according to the grading and staging of the diagnostic criteria of chronic hepatitis in Japan.17

Values are shown as mean ± SD. Wilcoxon’s rank-sum test for paired comparisons and Mann- Whitney’s U-test or the Kruskal-Wallis test for unpaired comparisons were used for the two groups. Correlations in categorical data and numerical data were evaluated by the {chi}2 test and Spearman test, respectively. Multivariate analysis was performed by stepwise multiple regression analysis with analysis of variance, if indicated. We used SPSS commercial statistics software (SPSS 10.0 for Windows; SPSS Inc., Chicago, IL), and P values < .05 were regarded as significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Characteristics
Of the 29 patients enrolled in this study with the above-mentioned criteria, the MHV was preserved in the remnant liver in 17 patients (group A), and the MHV was removed in 12 patients (group B). Age, sex, liver-resection volume (percentage), estimated future remnant liver volume (milliliters), indocyanine green retention rate at 15 minutes, original diseases, possession of hepatitis viruses, and pathologic findings of background liver were similar between the two groups (Table 1Go).


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  		TABLE 1. Patient characteristics
 
Perioperative Findings and Complications
No deleterious intraoperative event occurred in any patient. The fissure vein was detectable with intraoperative ultrasonography in all cases and was entirely preserved in all group B patients. In group B patients, the fissure vein drained into the MHV in seven, the LHV in three, and the junction of the MHV and LHV in two. There was no difference between groups in operating time, intraoperative blood loss, intraoperative blood transfusion, postoperative maximum levels of serum ALT, total bilirubin, postoperative morbidity rate, or postoperative hospital stay (Table 2Go).


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  		TABLE 2. Univariate analysis of perioperative variables in a comparison between groups A and B
 
No serious complication was observed in any patient. Hyperbilirubinemia >3.0 mg/dL of serum total bilirubin was observed in seven patients, but all of these patients recovered promptly and returned to normal within 2 weeks. All patients were uneventfully discharged from the hospital within 30 days and returned to preoperative daily normal life within 2 months (Table 2Go).

In two patients of group A, recurrence of hepatocellular carcinoma was detected in the remaining liver at eight and nine postoperative months. In one patient of group A, the postoperative follow-up period had reached only 10 months when we reached the end of our study period. Furthermore, one group B patient died of brain metastasis of hepatocellular carcinoma at 11 postoperative months. Therefore, postoperative CT volumetric study could be performed only until 6 postoperative months in these four patients. The other 25 patients underwent postoperative CT volumetric study for at least up to 12 postoperative months.

Postoperative CT Findings: Presence or Absence of the MHV Trunk
The presence of the MHV trunk in all group A patients and the absence of the MHV trunk in all group B patients were confirmed by postoperative CT with contrast enhancement at any time when postoperative CT was performed. Furthermore, the fissure vein, which had been confirmed and entirely preserved during surgery, was also detectable in all group B patients.

Liver Regeneration Evaluated by CT
Chronological Changes in the Volume Regeneration of Each Area of the Remnant Liver
Chronological changes in the total residual liver volume and each liver area are shown in Fig. 1Go. The volumes of the total residual liver, MS, LS, and SI were not statistically different between group A and group B at each measured time point. Furthermore, the ratio of the volume of the MS, LS, or SI to the total residual liver volume was similar between the two groups.


Figure 1
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  		FIG. 1. Chronological changes in the volume regeneration of each area of the remnant liver. The volume of the total residual liver, medial section, lateral section, and segment I were not statistically different between group A and group B at each measured time point. Furthermore, the ratio of the volume of the medial section, lateral section, or segment I to the total residual liver volume was similar at each measured time point between the two groups. *P < .01 compared with the prior measurement;
{dagger}P < .05 compared with the prior measurement. Hx the day of hepatectomy.

 
Chronological Changes in the VrR of Each Area of the Remnant Liver
VrR-WL and VrR-LS significantly increased until six postoperative months but did not significantly increase thereafter in either group. Similarly, VrR-MS significantly increased until six postoperative months in group B. However, VrR-MS in group A significantly increased until three postoperative months but did not significantly increase thereafter. Furthermore, although VrR-SI increased until six postoperative months, it did not increase thereafter in either group, and differences between time points were not significant (Figs. 2Go and 3Go). When comparing the VrR of each liver area between group A and group B, we observed no statistical significance in any liver area.


Figure 2
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  		FIG. 2. Chronological changes in the volume regeneration rate of the overall remnant liver and the medial section. *P < .01 compared with the prior measurement; {dagger}P < .05 compared with the prior measurement.

 

Figure 3
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  		FIG. 3. Chronological changes in the volume regeneration rate of the lateral section and segment I. *P < .01 compared with the prior measurement; {dagger}P < .05 compared with the prior measurement.

 
Analysis of Clinical Factors Influencing the Final Liver Volume
Determination of the Most Appropriate Time Point for Analysis of Clinical Factors Influencing Liver Regeneration
Liver regeneration reached a plateau at approximately six postoperative months, according to the findings of chronological changes in the volume regeneration and VrR of each area. Accordingly, six postoperative months was considered to be the most appropriate time point for analysis of the clinical factors that influence liver regeneration.

Univariate Analysis
Fourteen variables were analyzed as possible determinants of the VrR for each area at six postoperative months (Tables 3Go and 4Go). With regard to univariate analysis, of these 14 variables regarding univariate analysis, only the resection volume (percentage) was found to be significantly correlated with VrR-WL (r = .699; P < .001), VrR-MS (r = .552; P = .003), and VrR-LS (r = .693; P < .001). However, VrR-SI was not affected by any of these 14 variables. When the correlation between the resection volume (percentage) and the VrR of each area was investigated separately in group A, in which the MHV was preserved in the remnant liver, or in group B, in which the MHV was removed, the resection volume (percentage) was significantly correlated with VrR-WL (group A: r = .706, P = .02; group B: r = .790, P = .007), VrR-MS (group A: r = .548, P = .028; group B: r = .575, P = .042), and VrRLS (group A: r = .709, P = .02; group B: r = .677, P = .022) in both groups, but not with VrR-SI in either group (group A: r = .506, P = .065; group B: r = -.232, P = .492). Preservation of the MHV did not advantageously affect VrR-WL, VrR-MS, VrRLS, or VrR-SI.


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  		TABLE 3. Univariate analysis of dichotomous clinical variables influencing volume regeneration at six postoperative months
 

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  		TABLE 4. Univariate analysis of continuous clinical variables influencing volume regeneration of each area at 6 postoperative months
 
Multivariate Analysis
Upon performing multivariate analysis, we evaluated the same 14 variables as we used in the univariate analyses by using stepwise multiple regression analyses. In these analyses, only the resection volume (percentage) significantly affected VrR-WL, VrR-MS, and VrR-LS. Analysis of variance results and the coefficient of determination (R2) were as follows: P < .001 and R2 = .572 for VrR-WL, P = .003 and R2 = .438 for VrR-MS, and P < .001 and R2 = .523 for VrR-LS. In other words, only the resection volume authentically explained 57.2% of VrR-WL, 43.8% of VrR-MS, and 52.3% of VrR-LS. Of these 14 variables, however, no variable was significantly correlated with VrR-SI (Table 5Go).


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  		TABLE 5. Results of multivariate analysis for clinical variables influencing volume regeneration of each area
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Since Maema et al.3 reported that disruption of the MHV impairs volume regeneration of the anterior section on the basis of their study of left-hemihepatectomized patients, growing evidence has suggested that venous disruption has a negative effect on liver regeneration of the remnant liver after hepatectomy. Furthermore, Kido et al.4 have shown that MHV disruption significantly impairs volume regeneration of the MS after right hemihepatectomy. These studies, however, were both conducted in the setting of living liver donor hepatectomy; as such, their results may not be applicable to cases involving hepatic tumors.

In this study, we investigated how venous disruption of the MHV affects liver regeneration of the remnant liver after right hemihepatectomy for hepatic tumors. The essential points of our results are as follows. Disruption of the MHV might to some extent impair volume regeneration of the overall remnant liver as well as the MS after right hemihepatectomy, but this impairment is not crucial. The most decisive factor influencing liver regeneration after right hemihepatectomy for hepatic tumors is the resection volume. In the field of liver surgery for hepatic tumors, the mode of hepatectomy is often limited according to the location of tumors. Thus, the MHV is often taken into the resected liver. On the basis of univariate analyses in this study, the resection volume was significantly correlated with VrR-MS in both groups when investigated separately in group A or group B. Furthermore, the resection volume was significantly correlated with VrR-MS when overall enrolled cases were investigated by univariate and multivariate analysis. This finding may indicate that disruption of the MHV does not crucially affect liver regeneration of the MS after right hemihepatectomy for hepatic tumors. Our study also suggests that disruption of the MHV does not affect the safety of right hemihepatectomy for hepatic tumors if the resection volume is limited in cases in which the PS is ≤ 40 or 45, calculated as mentioned previously, because none of our patients developed serious complications.

Incidentally, as to the SI, VrR-SI was not affected by any variable that we chose in this study, including the resection volume. When right hemihepatectomy is performed for hepatic tumors, the transecting plane is shifted to the right or left according to the location of the tumors, regardless of whether the MHV is preserved. Because the SI is very small and its transecting plane is quite varied despite its smallness, the remnant volume of the SI varies according to specific cases. This variety with regard to the remnant SI volume is thought to explain why VrR-SI was not affected by any variable in this study.

Pomfret et al.6 have demonstrated that liver regeneration of the remnant liver in living right-liver donors continues throughout the first postoperative year. Our cases, however, show that the regeneration reaches a plateau at six postoperative months. Unlike with living liver donors, the tumor tissues replace a considerable amount of the functional hepatic parenchyma in cases with hepatic tumors. Our therapeutic strategy for hepatic tumors is as follows. We consider that as much of the hepatic parenchyma as possible should be preserved if the hepatic tumors are completely removed. As such, we routinely choose a minimum systematic anatomical resection18 for hepatic tumors. For example, when two hepatic tumors are located on segments V and VII, we will perform separate segmentectomies of V and VII. Thus, when we choose a right hepatectomy, the total size of the tumors is quite large.

Furthermore, according to our therapeutic policy, the total tumor volume tends to be larger in cases in which the MHV should be removed than in cases in which the MHV might be preserved. Consequently, although the difference was not significant, the resection volume was lower in group B than in group A in this study. In such cases, the functional demand of the replaced parenchyma is assumed to be considerably shifted to another portion of the liver—e.g., the left hemiliver seems to have already been extensively regenerated at the time of operation because of the replacement of tumor tissues in the right hemiliver. As a result, we observed that the regeneration period ended early in the postoperative period compared with the right-liver donors in Pomfret’s study.

Maema et al.3 and Kido et al.4 have reported that the liver area, where uniform venous drainage is maintained, compensates for the impairment of volume regeneration in the areas with venous disruption, thus resulting in a regeneration imbalance between venous-disrupted areas and other areas. Unlike these reports dealing with living liver donors, our results indicate that the imbalance of volume regeneration between liver areas was similar between group A and group B. In our cases, volume imbalances between the liver areas might have already occurred because of the liver regeneration preceding hepatectomy caused by the presence of hepatic tumors. As to the disruption of the MHV, subsequent congestion after hepatectomy did not crucially affect the regeneration of appropriative areas. Furthermore, venous collaterals might have already begun to form before the hepatectomy according to possible obstruction of the MHV tributaries disrupted and/or compressed by the tumors located near the MHV.19

The fissure vein was present and entirely preserved in all of our cases in which the MHV was taken into the resected liver. When the MHV must be taken into the resected liver in a right hemihepatectomy, preservation of the fissure vein might be essential to preventing crucial congestion of the MS. Some investigators have reported that when the major hepatic veins are disrupted, neighboring hepatic veins compensate for the congestion of the area where the hepatic vein has been disrupted.1,2,19–21 In our cases, the fissure vein might have compensated the disrupted MHV for the congestion of the MS.

In conclusion, disruption of the MHV does not significantly affect liver regeneration of the remnant liver after right hemihepatectomy conducted for hepatic tumors. Therefore, when a right hemihepatectomy is performed for hepatic tumors, the MHV is justifiably taken into the resected liver according to the location of tumors if the resection volume does not exceed the safety limit of the PS for these procedures. However, the fissure vein should be preserved if possible, because it may play a crucial role in compensating the MHV for venous drainage of the MS.

Received for publication April 27, 2006. Accepted for publication May 2, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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