- Email: [email protected]
Hepatectomy preserving drainage veins of the posterior section for liver malignancy invading the right hepatic vein: an alternative to right hepatectomy
The American Journal of Surgery (2012) 204, 717–723
Clinical Science
Hepatectomy preserving drainage veins of the posterior section for liver malignancy invading the right hepatic vein: an alternative to right hepatectomy Akira Shimizu, M.D., Ph.D., Akira Kobayashi, M.D., Ph.D.*, Takahide Yokoyama, M.D., Ph.D., Takenari Nakata, M.D., Ph.D., Hiroaki Motoyama, M.D., Ph.D., Koji Kubota, M.D., Ph.D., Norihiko Furusawa, M.D., Hiroe Kitahara, M.D., Ph.D., Noriyuki Kitagawa, M.D., Kentaro Fukushima, M.D., Tomoki Shirota, M.D., Shinichi Miyagawa, M.D., Ph.D. First Department of Surgery, Shinshu University School of Medicine, Asahi 3-1-1, Matsumoto, 390-8621, Japan KEYWORDS: Drainage veins of the posterior section; DVPS-preserving hepatectomy; Three-dimensional computed tomography; Color-Doppler intraoperative ultrasonography
Abstract BACKGROUND: Although a right hepatectomy (RH) traditionally has been performed for liver tumors infiltrating the main trunk of the right hepatic vein (RHV), the presence of drainage veins of the posterior section (DVPS) beside the RHV provides a chance to preserve their draining area even if the main trunk of the RHV is removed. METHODS: Since 2005, we systematically have performed DVPS-preserving hepatectomies whenever possible. In the present study, we describe our experience treating 12 consecutive patients who underwent this procedure. RESULTS: We performed the following types of liver resections concomitant with the main trunk of the RHV without packed red cell transfusion, liver failure, or 90-day mortality: extended right anterior sectionectomy in 2 patients, extended segmentectomy 7 in 3, extended segmentectomy 8 in 2, and partial resection of segment 7 in 2 and segment 8 in 3. Postoperative morbidity was observed in 4 (33%) cases, all of which had pleural effusion requiring a tap. A free resection margin was obtained in all patients. CONCLUSIONS: This procedure could be a useful alternative to RH, providing a chance for radical liver resection with minimal parenchymal sacrifice in selected patients with DVPS. © 2012 Elsevier Inc. All rights reserved.
For liver tumors infiltrating the main trunk of the right hepatic vein (RHV) adjacent to its caval confluence, a right hepatectomy (RH) traditionally has been performed in Western countries. Although surgical techniques and periThere was no financial support for this study. * Corresponding author. Tel.: ⫹81-263-37-2654; fax: ⫹81-263-35-1282 E-mail address: [email protected] Manuscript received October 11, 2011; revised manuscript February 6, 2012
0002-9610/$ - see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2012.02.011
operative care have improved dramatically, postoperative morbidity or mortality is not negligible after major liver resection even in patients with otherwise normal liver.1,2 Thus, care should be taken to preserve nontumorous liver parenchyma as much as possible, provided that a curative resection can be secured. In patients with an inferior right hepatic vein, one of the drainage veins of the posterior section (DVPS), the drainage area can be preserved even after the main trunk of the RHV
718
The American Journal of Surgery, Vol 204, No 5, November 2012
is transected.3– 6 In addition to the inferior RHV, several hepatic veins drain the posterior section, such as the middle right hepatic vein,7,8 right superior vein (referred to as V7 in this study),9 and the thick tributary of the middle hepatic vein draining segment 6 (V6).10 In theory, the presence of at least one of these veins could provide a chance to preserve their drainage territory, if cancer free, even if the main trunk of the RHV must be removed.5 Since 2005, we systematically have performed DVPSpreserving hepatectomies, whenever possible, for liver malignancy invading the main trunk of the RHV. We routinely performed a preoperative simulation of the hepatectomy using 3-dimensional (3D) computed tomography (CT), and color-Doppler intraoperative ultrasonography (IOUS) to evaluate venous congestion in the posterior section. Here, we describe our experience treating 12 consecutive patients who underwent this procedure.
Patients and Methods Between 2000 and 2010, a total of 301 patients with primary or secondary liver cancer underwent liver resection
at Shinshu University Hospital. Among these, 12 cases (4%) who underwent DVPS-preserving hepatectomies were included in the present analysis. The patients were 8 men and 4 women, with a mean age of 70 ⫾ 9 years. The anterior approach,11 in which liver mobilization is preceded by parenchymal transection, was not used in this series.
Eligibility criteria for parenchyma-preserving hepatectomy In patients with any of the following: (1) liver malignancies invading the main trunk of the RHV adjacent to its caval confluence, (2) cancer-free DVPS, and (3) a cancerfree Glissonian pedicle of the posterior section, we first planned a DVPS-preserving hepatectomy even in patients with a normal liver. If no DVPS was present and/or the posterior Glissonian pedicle was infiltrated by the tumor, an extended right posterior sectionectomy12 was planned instead, provided that the Glissonian pedicle of the anterior section was cancer-free and that the value of the indocyanine green retention rate at 15 minutes was less than 20%. When the Glissonian pedicle of the anterior and the poste-
Figure 1 Contrast-enhanced CT scan. (A) Cholangiocellular carcinoma in the anterior section of the liver (arrowhead), infiltrating the RHV (arrow). (B) A thick tributary of the RHV draining segment 7 (V7) (arrow). (C) A thick inferior RHV (arrow) were identified.
A. Shimizu et al.
DVPS-preserving hepatectomy
rior sections were infiltrated by the tumor, we planned a RH with or without portal vein embolization if the indocyanine green retention rate at 15 minutes was normal.13
719 based on the hepatic attenuation difference, as proposed by Kim et al.15
Surgical technique Perioperative work-up The maximum diameter of each DVPS was measured in the most suitable axial view on CT. The volume of the future remnant liver, drainage area of the RHV, and drainage territory of the DVPS were estimated on the basis of Digital Imaging and Communications in Medicine data of CT using 3D volumetry software (Organs Volume Analysis; Hitachi Medical Corporation, Chiba, Japan). Color-Doppler IOUS is used to assess parenchymal congestion by the direction of portal venous flow in the posterior section under RHV clamping.14 When hepatofugal flow, a sign of liver congestion in the corresponding area, is observed and the estimated noncongestive remnant liver volume is too small to meet the patient’s metabolic demands, reconstruction of the RHV may be indicated instead. Postoperative CT was performed 1 month after hepatectomy to evaluate the presence or absence of the parenchymal congestion of the remnant posterior section
A laparotomy was performed through a J-shaped incision with or without a right thoracotomy through the ninth intercostal space. After mobilization of the right hemiliver, the roots of the DVPS were taped. IOUS then was performed to verify the location of the tumor and its relationship to the RHV as well as the Glissonian pedicle of the right posterior section. The drainage territory of the DVPS was determined by temporary clamping of the right hepatic artery and the corresponding hepatic veins simultaneously. We confirmed hepatopetal portal flow in segment 6 or the posterior section before or after the parenchymal transection using color-Doppler IOUS under RHV clamping because hepatofugal flow in the corresponding area was considered an indication for RHV reconstruction. When the caval confluence of the RHV was involved by the tumor, the portal flow was confirmed under the side-clamping of the inferior vena cava including its caval confluence. Liver resection then was performed using the clamp crushing method and/or an ultrasonic dissector with electrocautery (SONOP 5000;
Figure 2 Preoperative simulation of hepatectomy using 3D volumetric analysis. (A) Hepatic veins and inferior vena cava were constructed in 3D. The V7 and the inferior RHV (IRHV) are colored red. (B) Right lateral view of the liver. (C) The sum of the drainage area of the V7 (arrow) and IRHV (arrowhead) was estimated to be 249 mL, corresponding to 20% of the total liver volume. (D) Simulation of an extended right anterior sectionectomy concomitant with the RHV. The noncongested remnant liver volume, that is, the left hemiliver plus drainage area of the V7 (arrow) and IRHV (arrowhead), was 517 mL, corresponding to 42% of the total liver volume. IVC, inferior vena cava; MHV, middle hepatic vein.
720
The American Journal of Surgery, Vol 204, No 5, November 2012
Aloka, Inc, Tokyo, Japan) under Pringle’s maneuver or the hemihepatic vascular occlusion technique. Bleeding from the raw surface of the transected liver was controlled by the meticulous placement of suture ligatures.
Case presentation A 55-year-old man presented with a diagnosis of cholangiocellular carcinoma in the anterior section, infiltrating the main trunk of the RHV (Fig 1A), suggesting the need for a right hepatectomy (RH) for radical resection. However, a RH with or without portal vein embolization was not feasible because of the small left liver volume (22% of the total liver volume) and rapid tumor growth. Since a CT scan also showed a thick V7 and IRHV draining the tumor-free posterior section (Fig 1B, C), we planned to preserve this area. Preoperative simulation using 3D volumetric analysis revealed that the left hemiliver plus the drainage area of the V7 and IRHV corresponded to 42% of the total liver volume (Fig 2). During the operation, the tumor was removed by an extended anterior sectionectomy with the RHV, preserving the posterior section drained by the V7 and IRHV (Fig 3).
Terminology The terminology for liver anatomy and resection was based on the Brisbane classification.16 Liver failure was defined based on Belghiti’s 50 –50 criteria.17 Cut-end recurrence was defined as a new lesion arising within 2 cm from the resection stump.18
Results
Figure 3 (A) Photograph and (B) scheme showing the surgical field after an extended right anterior sectionectomy. The V7 and the inferior RHV (IRHV) were preserved. (C) Posterior view of the preserved right posterior section. *Stump of the RHV. IVC, inferior vena cava.
The background characteristics and perioperative outcomes are summarized in Tables 1 and 2. A preoperative volume analysis showed that the median drainage volume of the DVPS was 214 mL (range, 70 –287 mL), which corresponds to 21% (range, 6%–27%) of the total liver volume (Table 2). We performed the following types of liver resections concomitant with the main trunk of the RHV without packed red cell transfusion, liver failure, or 90-day mortality: extended right anterior sectionectomy in 2 patients, extended segmentectomy 7 in 3, extended segmentectomy 8 in 2, and partial resection of segment 7 in 2 and segment 8 in 3. During the surgeries, none of the patients showed regurgitation of the portal venous flow in the posterior section under RHV clamping; thus, we did not perform RHV reconstruction. Postoperative morbidity was observed in 4 (33%) cases, all of which had pleural effusion requiring a tap. The median surgical time, blood loss, and postoperative hospital stay were 434 minutes (range, 256 –918 min), 435 mL (range, 100 –1,400 mL), and 25 days (range, 20 –50 days), respectively. A free resection margin (R0 resection) was obtained in all the patients, with a median width of surgical margin (SM) of 4 mm (range, 1–10 mm). No parenchymal congestion was observed on the postoperative CT examinations. The median overall and disease-free survival from the time of the hepatectomy were 40
Œ
CCC ⫽ cholangiocellular carcinoma; CLM ⫽ colorectal liver metastasis; HCC ⫽ hepatocellular carcinoma; ICG-R15 ⫽ indocyanine green retention rate at 15 minutes; IRHV ⫽ inferior right hepatic vein; MRHV ⫽ middle right hepatic vein; V6 ⫽ venous branch of the middle hepatic vein draining segment 6; V7 ⫽ venous branch of the right hepatic vein draining segment 7. An open circle represents preserved drainage veins of the posterior section in each patient. *Couinaud’s segment.
Œ Œ
Œ Œ Œ Œ Œ Œ
Œ
Œ
Œ
Œ
Œ Œ Œ Œ Œ Œ Œ Œ Œ
Extended right anterior sectionectomy Extended right anterior sectionectomy Partial resection Partial resection Extended segmentectomy Extended segmentectomy Extended segmentectomy Extended segmentectomy Extended segmentectomy Partial resection Partial resection Partial resection 5 6 7 9 9 13 13 14 15 17 19 22 — — — — Chronic hepatitis — Cirrhosis Chronic hepatitis — — Chronic hepatitis Cirrhosis 1 2 3 4 5 6 7 8 9 10 11 12
71/M 55/M 79/M 66/F 64/M 55/F 74/M 75/M 66/M 71/F 85/M 77/M
HCC CCC CLM CLM HCC CCC HCC HCC CLM HCC HCC HCC
8–5 8–5 7/1 7 7 7 8 8 7 8/6 8–7 8
1 Multiple 1/1 1 1 1 2 1 1 1/1 1 1
6.5 4.0 6.2 3.0 3.5 2.7 5.5 5.5 2.7 9.0 4.5 5.0
ICG-R15, %
Procedure
IRHV
MRHV
V7
V6
DVPS-preserving hepatectomy
Underlying liver disease Maximum size, cm Number Localization* Diagnosis Age/sex Case, n
Table 1
Baseline characteristics and surgical procedures in patients who underwent DVPS-preserving hepatectomy
Preserved drainage vein of the posterior section
A. Shimizu et al.
721 months (range, 12–95 months) and 13 months (range, 12–95 months), respectively. No cut-end recurrences were observed. At the time of the last follow-up evaluation, 4 patients (33%) had died, 5 were alive with disease (42%), and 3 were alive without disease (25%).
Comments We systematically have performed DVPS-preserving hepatectomies, whenever possible, for patients with liver malignancies invading the main trunk of the RHV since 2005. We routinely have applied preoperative simulations for hepatectomy using 3D CT and IOUS: the former helps us to plan the type of liver resection, and the latter, the most essential part of this procedure, can provide useful information regarding the relationship between the tumor and intrahepatic vascular structures.19 In addition, color Doppler IOUS can evaluate parenchymal congestion from the direction of portal venous flow under hepatic vein clamping.14 A large advantage of this procedure is that it can offer the chance to preserve the drainage area of the DVPS, which corresponds to one fifth of the total liver volume. Both the inflow and the outflow were maintained in the preserved area after the completion of the liver resection, as confirmed using color Doppler IOUS and routine postoperative CT. Because of the spared parenchyma, the maximum postoperative serum total bilirubin value, which is known to be a reliable marker of liver insufficiency,17 has never increased beyond 3 mg/dL in this series. This technically demanding procedure may raise some concerns regarding a possible increase in surgical risks.
Table 2 Perioperative outcomes in patients who underwent DVPS-preserving hepatectomy Volumetric analysis Drainage volume of DVPS, mL Drainage volume of DVPS/total liver volume, % Intraoperative outcomes Surgical time, min Pedicle clamping time, min Blood loss, mL Patients with packed red blood cell transfusion Surgical margin, mm Postoperative outcomes Total bilirubin maximum, mg/dL Hospital stay, d 90-day mortality rate, % Morbidity Pleural effusion Last follow-up evaluation Dead Alive with recurrence Alive disease-free
214 (70–287) 21 (6–27)
434 (256–918) 67 (27–155) 435 (100–1,400) 0 4 (1–10) 1.3 (.8–2.8) 25 (20–50) 0 4 (33) 4 (33) 5 (42) 3 (25)
Data are median (range) or number of patients (%).
722
The American Journal of Surgery, Vol 204, No 5, November 2012
However, we have performed these surgeries with zero mortality, zero packed red blood cell transfusion, and acceptable morbidities. One possible explanation for these results is the use of our meticulous surgical techniques for reducing blood loss.13 Under the guidance of IOUS, complete tumor clearance can be achieved in all the patients with a median SM of 4 mm. This result may raise another concern regarding increases in the risk of tumor recurrence in the liver remnant; however, no cut-end recurrences were observed in the present study. Regarding the width of the SM, several previous studies have shown that a narrow SM is associated with higher intrahepatic recurrence rates after liver resection for primary and/or secondary liver cancer; thus, it is regarded as an independent risk factor for recurrence.20 –23 By contrast, other studies have shown that an SM of less than 1 cm has no significant impact on survival, as long as the margin is cancer-negative.24 –26 Taken together, these results indicate that the optimal SM for the management of primary and secondary liver cancers remains controversial. Kokudo et al24 performed a histologic and genetic assessment of surgically resected colorectal liver metastases and showed that cut-end recurrences were observed in only 6% of the patients with margins ranging from 2 to 9 mm. The investigators proposed that a surgical margin of 2 mm was an acceptable minimum requirement. The anterior approach initially was reported by Lai et al11 for patients with bulky liver tumors with or without infiltration to the retrohepatic regions to prevent excessive bleeding, tumor rupture, and spread of tumor cells during liver mobilization. Although the oncologic benefit of the anterior approach remains controversial,27 this procedure may be useful to patients with huge liver tumor, reducing blood loss during liver transection when used in combination with a liver hanging maneuver.28 By contrast, the conventional approach (CA), in which liver mobilization is performed before parenchymal transection, has the advantage of enabling back bleeding to be controlled by the surgeon’s left hand during liver resection. When performing DVPS-preserving hepatectomies, the CA has another advantage in the ability to confirm and secure the DVPS before liver resection. In the present study, we used the CA in all patients without any increase in blood loss. Some criticisms of the indications for this procedure in patients with normal liver parenchyma may exist. Based on previous studies showing that the normal liver can tolerate the removal of up to 70%29 to 75%30,31 of its volume, a RH traditionally has been performed for liver tumors infiltrating the main trunk of the RHV in patients with normal liver. However, major liver resection still carries a high risk of postoperative hepatic dysfunction and infectious complications even in patients without underlying liver disease.1 Indeed, the Hospital Beaujon group reported that although the mortality rate is low after an extensive hepatectomy, leaving a very small remnant in patients with normal liver, clear trends toward a slower recovery, a
greater need for critical care, and a prolonged hospital stay exist.2 Thus, our policy is to preserve the nontumorous liver parenchyma as much as possible even in patients with normal liver, provided that a curative resection is secured. In conclusion, although this procedure is technically demanding, and is not commonly performed, thereby preventing a large-scale study from being conducted, it could be a useful alternative to RH, providing a chance for radical liver resection with minimal parenchymal sacrifice in selected patients with DVPS.
References 1. Schindl MJ, Redhead DN, Fearon KC, et al. The value of residual liver volume as a predictor of hepatic dysfunction and infection after major liver resection. Gut 2005;54:289 –96. 2. Yigitler C, Farges O, Kianmanesh R, et al. The small remnant liver after major liver resection: how common and how relevant? Liver Transplant 2003;9:S18 –25. 3. Baer HU, Dennison AR, Maddern GJ, et al. Subtotal hepatectomy: a new procedure based on the inferior right hepatic vein. Br J Surg 1991;78:1221–2. 4. Hirai I, Kimura W, Fuse A, et al. Evaluation of inferior right hepatic vein-preserving hepatectomy with resection of the superior right hepatic vein. Hepatogastroenterology 2006;53:516 –20. 5. Makuuchi M, Hasegawa H, Yamazaki S, et al. Four new hepatectomy procedures for resection of the right hepatic vein and preservation of the inferior right hepatic vein. Surg Gynecol Obstet 1987;164:68 –72. 6. Ozeki Y, Uchiyama T, Katayama M, et al. Extended left hepatic trisegmentectomy with resection of main right hepatic vein and preservation of middle and inferior right hepatic veins. Surgery 1995;117: 715–7. 7. Makuuchi M, Hasegawa H, Yamazaki S, et al. The inferior right hepatic vein: ultrasonic demonstration. Radiology 1983;148:213–7. 8. Couinaud C. Le Foie. Etudes Anatomiques et Chirurgicales. Paris: Masson; 1957. 9. Nakamura S, Tsuzuki T. Surgical anatomy of the hepatic veins and the inferior vena cava. Surg Gynecol Obstet 1981;152:43–50. 10. Kakazu T, Makuuchi M, Kawasaki S, et al. Reconstruction of the middle hepatic vein tributary during right anterior segmentectomy. Surgery 1995;117:238 – 40. 11. Lai EC, Fan ST, Lo CM, et al. Anterior approach for difficult major right hepatectomy. World J Surg 1996;20:314 –7; discussion, 318. 12. Kobayashi A, Imamura H, Miyagawa S, et al. Extended right posterior segmentectomy for metastatic liver tumors. Surgery 1997;121:698 – 703. 13. Miyagawa S, Makuuchi M, Kawasaki S, et al. Criteria for safe hepatic resection. Am J Surg 1995;169:589 –94. 14. Sano K, Makuuchi M, Miki K, et al. Evaluation of hepatic venous congestion: proposed indication criteria for hepatic vein reconstruction. Ann Surg 2002;236:241–7. 15. Kim BS, Kim TK, Kim JS, et al. Hepatic venous congestion after living donor liver transplantation with right lobe graft: two-phase CT findings. Radiology 2004;232:173– 80. 16. Terminology Committee of the IHPBA. Terminology of liver anatomy and resections. HPB Surg 2000;2:333–9. 17. Balzan S, Belghiti J, Farges O, et al. The “50 –50 criteria” on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 2005;242:824 –9. 18. Takayama T, Makuuchi M, Hirohashi S, et al. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology 1998;28:1241– 6.
A. Shimizu et al.
DVPS-preserving hepatectomy
19. Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 1985;161:346 –50. 20. Are C, Gonen M, Zazzali K, et al. The impact of margins on outcome after hepatic resection for colorectal metastasis. Ann Surg 2007;246: 295–300. 21. Cady B, Stone M, McDermott WJ, et al. Technical and biological factors in disease-free survival after hepatic resection for colorectal cancer metastases. Arch Surg 1992;127:561– 8; discussion, 568 –9. 22. Lee CS, Sung JL, Hwang LY, et al. Surgical treatment of 109 patients with symptomatic and asymptomatic hepatocellular carcinoma. Surgery 1986;99:481–90. 23. Shirabe K, Takenaka K, Gion T, et al. Analysis of prognostic risk factors in hepatic resection for metastatic colorectal carcinoma with special reference to the surgical margin. Br J Surg 1997;84:1077– 80. 24. Kokudo N, Miki Y, Sugai S, et al. Genetic and histological assessment of surgical margins in resected liver metastases from colorectal carcinoma: minimum surgical margins for successful resection. Arch Surg 2002;137:833– 40. 25. Pawlik T, Scoggins C, Zorzi D, et al. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 2005;241:715–22; discussion, 722– 4. 26. Yamamoto J, Shimada K, Kosuge T, et al. Factors influencing survival of patients undergoing hepatectomy for colorectal metastases. Br J Surg 1999;86:332–7.
723 27. Shindoh J, Hasegawa K, Aoki T, et al. Significance of liver hanging maneuvers for invasive liver lesions in no-routine anterior approach policy. J Gastrointest Surg 2011;15:988 –95. 28. Belghiti J, Guevara OA, Noun R, et al. Liver hanging maneuver: a safe approach to right hepatectomy without liver mobilization. J Am Coll Surg 2001;193:109 –11. 29. Stone HH, Long WD, Smith RB 3rd, et al. Physiologic considerations in major hepatic resections. Am J Surg 1969;117:78 – 84. 30. Shoup M, Gonen M, D’Angelica M, et al. Volumetric analysis predicts hepatic dysfunction in patients undergoing major liver resection. J Gastrointest Surg 2003;7:325–30. 31. Vauthey JN, Chaoui A, Do KA, et al. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery 2000;127:512–9.
Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.amjsurg.2012.02.011.
Clinical Science
Hepatectomy preserving drainage veins of the posterior section for liver malignancy invading the right hepatic vein: an alternative to right hepatectomy Akira Shimizu, M.D., Ph.D., Akira Kobayashi, M.D., Ph.D.*, Takahide Yokoyama, M.D., Ph.D., Takenari Nakata, M.D., Ph.D., Hiroaki Motoyama, M.D., Ph.D., Koji Kubota, M.D., Ph.D., Norihiko Furusawa, M.D., Hiroe Kitahara, M.D., Ph.D., Noriyuki Kitagawa, M.D., Kentaro Fukushima, M.D., Tomoki Shirota, M.D., Shinichi Miyagawa, M.D., Ph.D. First Department of Surgery, Shinshu University School of Medicine, Asahi 3-1-1, Matsumoto, 390-8621, Japan KEYWORDS: Drainage veins of the posterior section; DVPS-preserving hepatectomy; Three-dimensional computed tomography; Color-Doppler intraoperative ultrasonography
Abstract BACKGROUND: Although a right hepatectomy (RH) traditionally has been performed for liver tumors infiltrating the main trunk of the right hepatic vein (RHV), the presence of drainage veins of the posterior section (DVPS) beside the RHV provides a chance to preserve their draining area even if the main trunk of the RHV is removed. METHODS: Since 2005, we systematically have performed DVPS-preserving hepatectomies whenever possible. In the present study, we describe our experience treating 12 consecutive patients who underwent this procedure. RESULTS: We performed the following types of liver resections concomitant with the main trunk of the RHV without packed red cell transfusion, liver failure, or 90-day mortality: extended right anterior sectionectomy in 2 patients, extended segmentectomy 7 in 3, extended segmentectomy 8 in 2, and partial resection of segment 7 in 2 and segment 8 in 3. Postoperative morbidity was observed in 4 (33%) cases, all of which had pleural effusion requiring a tap. A free resection margin was obtained in all patients. CONCLUSIONS: This procedure could be a useful alternative to RH, providing a chance for radical liver resection with minimal parenchymal sacrifice in selected patients with DVPS. © 2012 Elsevier Inc. All rights reserved.
For liver tumors infiltrating the main trunk of the right hepatic vein (RHV) adjacent to its caval confluence, a right hepatectomy (RH) traditionally has been performed in Western countries. Although surgical techniques and periThere was no financial support for this study. * Corresponding author. Tel.: ⫹81-263-37-2654; fax: ⫹81-263-35-1282 E-mail address: [email protected] Manuscript received October 11, 2011; revised manuscript February 6, 2012
0002-9610/$ - see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2012.02.011
operative care have improved dramatically, postoperative morbidity or mortality is not negligible after major liver resection even in patients with otherwise normal liver.1,2 Thus, care should be taken to preserve nontumorous liver parenchyma as much as possible, provided that a curative resection can be secured. In patients with an inferior right hepatic vein, one of the drainage veins of the posterior section (DVPS), the drainage area can be preserved even after the main trunk of the RHV
718
The American Journal of Surgery, Vol 204, No 5, November 2012
is transected.3– 6 In addition to the inferior RHV, several hepatic veins drain the posterior section, such as the middle right hepatic vein,7,8 right superior vein (referred to as V7 in this study),9 and the thick tributary of the middle hepatic vein draining segment 6 (V6).10 In theory, the presence of at least one of these veins could provide a chance to preserve their drainage territory, if cancer free, even if the main trunk of the RHV must be removed.5 Since 2005, we systematically have performed DVPSpreserving hepatectomies, whenever possible, for liver malignancy invading the main trunk of the RHV. We routinely performed a preoperative simulation of the hepatectomy using 3-dimensional (3D) computed tomography (CT), and color-Doppler intraoperative ultrasonography (IOUS) to evaluate venous congestion in the posterior section. Here, we describe our experience treating 12 consecutive patients who underwent this procedure.
Patients and Methods Between 2000 and 2010, a total of 301 patients with primary or secondary liver cancer underwent liver resection
at Shinshu University Hospital. Among these, 12 cases (4%) who underwent DVPS-preserving hepatectomies were included in the present analysis. The patients were 8 men and 4 women, with a mean age of 70 ⫾ 9 years. The anterior approach,11 in which liver mobilization is preceded by parenchymal transection, was not used in this series.
Eligibility criteria for parenchyma-preserving hepatectomy In patients with any of the following: (1) liver malignancies invading the main trunk of the RHV adjacent to its caval confluence, (2) cancer-free DVPS, and (3) a cancerfree Glissonian pedicle of the posterior section, we first planned a DVPS-preserving hepatectomy even in patients with a normal liver. If no DVPS was present and/or the posterior Glissonian pedicle was infiltrated by the tumor, an extended right posterior sectionectomy12 was planned instead, provided that the Glissonian pedicle of the anterior section was cancer-free and that the value of the indocyanine green retention rate at 15 minutes was less than 20%. When the Glissonian pedicle of the anterior and the poste-
Figure 1 Contrast-enhanced CT scan. (A) Cholangiocellular carcinoma in the anterior section of the liver (arrowhead), infiltrating the RHV (arrow). (B) A thick tributary of the RHV draining segment 7 (V7) (arrow). (C) A thick inferior RHV (arrow) were identified.
A. Shimizu et al.
DVPS-preserving hepatectomy
rior sections were infiltrated by the tumor, we planned a RH with or without portal vein embolization if the indocyanine green retention rate at 15 minutes was normal.13
719 based on the hepatic attenuation difference, as proposed by Kim et al.15
Surgical technique Perioperative work-up The maximum diameter of each DVPS was measured in the most suitable axial view on CT. The volume of the future remnant liver, drainage area of the RHV, and drainage territory of the DVPS were estimated on the basis of Digital Imaging and Communications in Medicine data of CT using 3D volumetry software (Organs Volume Analysis; Hitachi Medical Corporation, Chiba, Japan). Color-Doppler IOUS is used to assess parenchymal congestion by the direction of portal venous flow in the posterior section under RHV clamping.14 When hepatofugal flow, a sign of liver congestion in the corresponding area, is observed and the estimated noncongestive remnant liver volume is too small to meet the patient’s metabolic demands, reconstruction of the RHV may be indicated instead. Postoperative CT was performed 1 month after hepatectomy to evaluate the presence or absence of the parenchymal congestion of the remnant posterior section
A laparotomy was performed through a J-shaped incision with or without a right thoracotomy through the ninth intercostal space. After mobilization of the right hemiliver, the roots of the DVPS were taped. IOUS then was performed to verify the location of the tumor and its relationship to the RHV as well as the Glissonian pedicle of the right posterior section. The drainage territory of the DVPS was determined by temporary clamping of the right hepatic artery and the corresponding hepatic veins simultaneously. We confirmed hepatopetal portal flow in segment 6 or the posterior section before or after the parenchymal transection using color-Doppler IOUS under RHV clamping because hepatofugal flow in the corresponding area was considered an indication for RHV reconstruction. When the caval confluence of the RHV was involved by the tumor, the portal flow was confirmed under the side-clamping of the inferior vena cava including its caval confluence. Liver resection then was performed using the clamp crushing method and/or an ultrasonic dissector with electrocautery (SONOP 5000;
Figure 2 Preoperative simulation of hepatectomy using 3D volumetric analysis. (A) Hepatic veins and inferior vena cava were constructed in 3D. The V7 and the inferior RHV (IRHV) are colored red. (B) Right lateral view of the liver. (C) The sum of the drainage area of the V7 (arrow) and IRHV (arrowhead) was estimated to be 249 mL, corresponding to 20% of the total liver volume. (D) Simulation of an extended right anterior sectionectomy concomitant with the RHV. The noncongested remnant liver volume, that is, the left hemiliver plus drainage area of the V7 (arrow) and IRHV (arrowhead), was 517 mL, corresponding to 42% of the total liver volume. IVC, inferior vena cava; MHV, middle hepatic vein.
720
The American Journal of Surgery, Vol 204, No 5, November 2012
Aloka, Inc, Tokyo, Japan) under Pringle’s maneuver or the hemihepatic vascular occlusion technique. Bleeding from the raw surface of the transected liver was controlled by the meticulous placement of suture ligatures.
Case presentation A 55-year-old man presented with a diagnosis of cholangiocellular carcinoma in the anterior section, infiltrating the main trunk of the RHV (Fig 1A), suggesting the need for a right hepatectomy (RH) for radical resection. However, a RH with or without portal vein embolization was not feasible because of the small left liver volume (22% of the total liver volume) and rapid tumor growth. Since a CT scan also showed a thick V7 and IRHV draining the tumor-free posterior section (Fig 1B, C), we planned to preserve this area. Preoperative simulation using 3D volumetric analysis revealed that the left hemiliver plus the drainage area of the V7 and IRHV corresponded to 42% of the total liver volume (Fig 2). During the operation, the tumor was removed by an extended anterior sectionectomy with the RHV, preserving the posterior section drained by the V7 and IRHV (Fig 3).
Terminology The terminology for liver anatomy and resection was based on the Brisbane classification.16 Liver failure was defined based on Belghiti’s 50 –50 criteria.17 Cut-end recurrence was defined as a new lesion arising within 2 cm from the resection stump.18
Results
Figure 3 (A) Photograph and (B) scheme showing the surgical field after an extended right anterior sectionectomy. The V7 and the inferior RHV (IRHV) were preserved. (C) Posterior view of the preserved right posterior section. *Stump of the RHV. IVC, inferior vena cava.
The background characteristics and perioperative outcomes are summarized in Tables 1 and 2. A preoperative volume analysis showed that the median drainage volume of the DVPS was 214 mL (range, 70 –287 mL), which corresponds to 21% (range, 6%–27%) of the total liver volume (Table 2). We performed the following types of liver resections concomitant with the main trunk of the RHV without packed red cell transfusion, liver failure, or 90-day mortality: extended right anterior sectionectomy in 2 patients, extended segmentectomy 7 in 3, extended segmentectomy 8 in 2, and partial resection of segment 7 in 2 and segment 8 in 3. During the surgeries, none of the patients showed regurgitation of the portal venous flow in the posterior section under RHV clamping; thus, we did not perform RHV reconstruction. Postoperative morbidity was observed in 4 (33%) cases, all of which had pleural effusion requiring a tap. The median surgical time, blood loss, and postoperative hospital stay were 434 minutes (range, 256 –918 min), 435 mL (range, 100 –1,400 mL), and 25 days (range, 20 –50 days), respectively. A free resection margin (R0 resection) was obtained in all the patients, with a median width of surgical margin (SM) of 4 mm (range, 1–10 mm). No parenchymal congestion was observed on the postoperative CT examinations. The median overall and disease-free survival from the time of the hepatectomy were 40
Œ
CCC ⫽ cholangiocellular carcinoma; CLM ⫽ colorectal liver metastasis; HCC ⫽ hepatocellular carcinoma; ICG-R15 ⫽ indocyanine green retention rate at 15 minutes; IRHV ⫽ inferior right hepatic vein; MRHV ⫽ middle right hepatic vein; V6 ⫽ venous branch of the middle hepatic vein draining segment 6; V7 ⫽ venous branch of the right hepatic vein draining segment 7. An open circle represents preserved drainage veins of the posterior section in each patient. *Couinaud’s segment.
Œ Œ
Œ Œ Œ Œ Œ Œ
Œ
Œ
Œ
Œ
Œ Œ Œ Œ Œ Œ Œ Œ Œ
Extended right anterior sectionectomy Extended right anterior sectionectomy Partial resection Partial resection Extended segmentectomy Extended segmentectomy Extended segmentectomy Extended segmentectomy Extended segmentectomy Partial resection Partial resection Partial resection 5 6 7 9 9 13 13 14 15 17 19 22 — — — — Chronic hepatitis — Cirrhosis Chronic hepatitis — — Chronic hepatitis Cirrhosis 1 2 3 4 5 6 7 8 9 10 11 12
71/M 55/M 79/M 66/F 64/M 55/F 74/M 75/M 66/M 71/F 85/M 77/M
HCC CCC CLM CLM HCC CCC HCC HCC CLM HCC HCC HCC
8–5 8–5 7/1 7 7 7 8 8 7 8/6 8–7 8
1 Multiple 1/1 1 1 1 2 1 1 1/1 1 1
6.5 4.0 6.2 3.0 3.5 2.7 5.5 5.5 2.7 9.0 4.5 5.0
ICG-R15, %
Procedure
IRHV
MRHV
V7
V6
DVPS-preserving hepatectomy
Underlying liver disease Maximum size, cm Number Localization* Diagnosis Age/sex Case, n
Table 1
Baseline characteristics and surgical procedures in patients who underwent DVPS-preserving hepatectomy
Preserved drainage vein of the posterior section
A. Shimizu et al.
721 months (range, 12–95 months) and 13 months (range, 12–95 months), respectively. No cut-end recurrences were observed. At the time of the last follow-up evaluation, 4 patients (33%) had died, 5 were alive with disease (42%), and 3 were alive without disease (25%).
Comments We systematically have performed DVPS-preserving hepatectomies, whenever possible, for patients with liver malignancies invading the main trunk of the RHV since 2005. We routinely have applied preoperative simulations for hepatectomy using 3D CT and IOUS: the former helps us to plan the type of liver resection, and the latter, the most essential part of this procedure, can provide useful information regarding the relationship between the tumor and intrahepatic vascular structures.19 In addition, color Doppler IOUS can evaluate parenchymal congestion from the direction of portal venous flow under hepatic vein clamping.14 A large advantage of this procedure is that it can offer the chance to preserve the drainage area of the DVPS, which corresponds to one fifth of the total liver volume. Both the inflow and the outflow were maintained in the preserved area after the completion of the liver resection, as confirmed using color Doppler IOUS and routine postoperative CT. Because of the spared parenchyma, the maximum postoperative serum total bilirubin value, which is known to be a reliable marker of liver insufficiency,17 has never increased beyond 3 mg/dL in this series. This technically demanding procedure may raise some concerns regarding a possible increase in surgical risks.
Table 2 Perioperative outcomes in patients who underwent DVPS-preserving hepatectomy Volumetric analysis Drainage volume of DVPS, mL Drainage volume of DVPS/total liver volume, % Intraoperative outcomes Surgical time, min Pedicle clamping time, min Blood loss, mL Patients with packed red blood cell transfusion Surgical margin, mm Postoperative outcomes Total bilirubin maximum, mg/dL Hospital stay, d 90-day mortality rate, % Morbidity Pleural effusion Last follow-up evaluation Dead Alive with recurrence Alive disease-free
214 (70–287) 21 (6–27)
434 (256–918) 67 (27–155) 435 (100–1,400) 0 4 (1–10) 1.3 (.8–2.8) 25 (20–50) 0 4 (33) 4 (33) 5 (42) 3 (25)
Data are median (range) or number of patients (%).
722
The American Journal of Surgery, Vol 204, No 5, November 2012
However, we have performed these surgeries with zero mortality, zero packed red blood cell transfusion, and acceptable morbidities. One possible explanation for these results is the use of our meticulous surgical techniques for reducing blood loss.13 Under the guidance of IOUS, complete tumor clearance can be achieved in all the patients with a median SM of 4 mm. This result may raise another concern regarding increases in the risk of tumor recurrence in the liver remnant; however, no cut-end recurrences were observed in the present study. Regarding the width of the SM, several previous studies have shown that a narrow SM is associated with higher intrahepatic recurrence rates after liver resection for primary and/or secondary liver cancer; thus, it is regarded as an independent risk factor for recurrence.20 –23 By contrast, other studies have shown that an SM of less than 1 cm has no significant impact on survival, as long as the margin is cancer-negative.24 –26 Taken together, these results indicate that the optimal SM for the management of primary and secondary liver cancers remains controversial. Kokudo et al24 performed a histologic and genetic assessment of surgically resected colorectal liver metastases and showed that cut-end recurrences were observed in only 6% of the patients with margins ranging from 2 to 9 mm. The investigators proposed that a surgical margin of 2 mm was an acceptable minimum requirement. The anterior approach initially was reported by Lai et al11 for patients with bulky liver tumors with or without infiltration to the retrohepatic regions to prevent excessive bleeding, tumor rupture, and spread of tumor cells during liver mobilization. Although the oncologic benefit of the anterior approach remains controversial,27 this procedure may be useful to patients with huge liver tumor, reducing blood loss during liver transection when used in combination with a liver hanging maneuver.28 By contrast, the conventional approach (CA), in which liver mobilization is performed before parenchymal transection, has the advantage of enabling back bleeding to be controlled by the surgeon’s left hand during liver resection. When performing DVPS-preserving hepatectomies, the CA has another advantage in the ability to confirm and secure the DVPS before liver resection. In the present study, we used the CA in all patients without any increase in blood loss. Some criticisms of the indications for this procedure in patients with normal liver parenchyma may exist. Based on previous studies showing that the normal liver can tolerate the removal of up to 70%29 to 75%30,31 of its volume, a RH traditionally has been performed for liver tumors infiltrating the main trunk of the RHV in patients with normal liver. However, major liver resection still carries a high risk of postoperative hepatic dysfunction and infectious complications even in patients without underlying liver disease.1 Indeed, the Hospital Beaujon group reported that although the mortality rate is low after an extensive hepatectomy, leaving a very small remnant in patients with normal liver, clear trends toward a slower recovery, a
greater need for critical care, and a prolonged hospital stay exist.2 Thus, our policy is to preserve the nontumorous liver parenchyma as much as possible even in patients with normal liver, provided that a curative resection is secured. In conclusion, although this procedure is technically demanding, and is not commonly performed, thereby preventing a large-scale study from being conducted, it could be a useful alternative to RH, providing a chance for radical liver resection with minimal parenchymal sacrifice in selected patients with DVPS.
References 1. Schindl MJ, Redhead DN, Fearon KC, et al. The value of residual liver volume as a predictor of hepatic dysfunction and infection after major liver resection. Gut 2005;54:289 –96. 2. Yigitler C, Farges O, Kianmanesh R, et al. The small remnant liver after major liver resection: how common and how relevant? Liver Transplant 2003;9:S18 –25. 3. Baer HU, Dennison AR, Maddern GJ, et al. Subtotal hepatectomy: a new procedure based on the inferior right hepatic vein. Br J Surg 1991;78:1221–2. 4. Hirai I, Kimura W, Fuse A, et al. Evaluation of inferior right hepatic vein-preserving hepatectomy with resection of the superior right hepatic vein. Hepatogastroenterology 2006;53:516 –20. 5. Makuuchi M, Hasegawa H, Yamazaki S, et al. Four new hepatectomy procedures for resection of the right hepatic vein and preservation of the inferior right hepatic vein. Surg Gynecol Obstet 1987;164:68 –72. 6. Ozeki Y, Uchiyama T, Katayama M, et al. Extended left hepatic trisegmentectomy with resection of main right hepatic vein and preservation of middle and inferior right hepatic veins. Surgery 1995;117: 715–7. 7. Makuuchi M, Hasegawa H, Yamazaki S, et al. The inferior right hepatic vein: ultrasonic demonstration. Radiology 1983;148:213–7. 8. Couinaud C. Le Foie. Etudes Anatomiques et Chirurgicales. Paris: Masson; 1957. 9. Nakamura S, Tsuzuki T. Surgical anatomy of the hepatic veins and the inferior vena cava. Surg Gynecol Obstet 1981;152:43–50. 10. Kakazu T, Makuuchi M, Kawasaki S, et al. Reconstruction of the middle hepatic vein tributary during right anterior segmentectomy. Surgery 1995;117:238 – 40. 11. Lai EC, Fan ST, Lo CM, et al. Anterior approach for difficult major right hepatectomy. World J Surg 1996;20:314 –7; discussion, 318. 12. Kobayashi A, Imamura H, Miyagawa S, et al. Extended right posterior segmentectomy for metastatic liver tumors. Surgery 1997;121:698 – 703. 13. Miyagawa S, Makuuchi M, Kawasaki S, et al. Criteria for safe hepatic resection. Am J Surg 1995;169:589 –94. 14. Sano K, Makuuchi M, Miki K, et al. Evaluation of hepatic venous congestion: proposed indication criteria for hepatic vein reconstruction. Ann Surg 2002;236:241–7. 15. Kim BS, Kim TK, Kim JS, et al. Hepatic venous congestion after living donor liver transplantation with right lobe graft: two-phase CT findings. Radiology 2004;232:173– 80. 16. Terminology Committee of the IHPBA. Terminology of liver anatomy and resections. HPB Surg 2000;2:333–9. 17. Balzan S, Belghiti J, Farges O, et al. The “50 –50 criteria” on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 2005;242:824 –9. 18. Takayama T, Makuuchi M, Hirohashi S, et al. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology 1998;28:1241– 6.
A. Shimizu et al.
DVPS-preserving hepatectomy
19. Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 1985;161:346 –50. 20. Are C, Gonen M, Zazzali K, et al. The impact of margins on outcome after hepatic resection for colorectal metastasis. Ann Surg 2007;246: 295–300. 21. Cady B, Stone M, McDermott WJ, et al. Technical and biological factors in disease-free survival after hepatic resection for colorectal cancer metastases. Arch Surg 1992;127:561– 8; discussion, 568 –9. 22. Lee CS, Sung JL, Hwang LY, et al. Surgical treatment of 109 patients with symptomatic and asymptomatic hepatocellular carcinoma. Surgery 1986;99:481–90. 23. Shirabe K, Takenaka K, Gion T, et al. Analysis of prognostic risk factors in hepatic resection for metastatic colorectal carcinoma with special reference to the surgical margin. Br J Surg 1997;84:1077– 80. 24. Kokudo N, Miki Y, Sugai S, et al. Genetic and histological assessment of surgical margins in resected liver metastases from colorectal carcinoma: minimum surgical margins for successful resection. Arch Surg 2002;137:833– 40. 25. Pawlik T, Scoggins C, Zorzi D, et al. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 2005;241:715–22; discussion, 722– 4. 26. Yamamoto J, Shimada K, Kosuge T, et al. Factors influencing survival of patients undergoing hepatectomy for colorectal metastases. Br J Surg 1999;86:332–7.
723 27. Shindoh J, Hasegawa K, Aoki T, et al. Significance of liver hanging maneuvers for invasive liver lesions in no-routine anterior approach policy. J Gastrointest Surg 2011;15:988 –95. 28. Belghiti J, Guevara OA, Noun R, et al. Liver hanging maneuver: a safe approach to right hepatectomy without liver mobilization. J Am Coll Surg 2001;193:109 –11. 29. Stone HH, Long WD, Smith RB 3rd, et al. Physiologic considerations in major hepatic resections. Am J Surg 1969;117:78 – 84. 30. Shoup M, Gonen M, D’Angelica M, et al. Volumetric analysis predicts hepatic dysfunction in patients undergoing major liver resection. J Gastrointest Surg 2003;7:325–30. 31. Vauthey JN, Chaoui A, Do KA, et al. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery 2000;127:512–9.
Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.amjsurg.2012.02.011.