0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Original Article |

Hepatic Resection for Bilobar Hepatocellular Carcinoma:  Is It Justified? FREE

Chi-Leung Liu, MS, FRCS; Sheung-Tat Fan, MS, MD, FRCS; Chung-Mau Lo, MS, FRACS, FRCS; Irene Oi-Lin Ng, MD, FRCPath; Ronnie Tung-Ping Poon, MS, FRCS; John Wong, PhD, FRACS, FRCS
[+] Author Affiliations

From the Centre for the Study of Liver Disease and the Departments of Surgery (Drs Fan, Wong, Liu, Lo, and Poon) and Pathology (Dr Ng), University of Hong Kong Medical Centre, Queen Mary Hospital, Hong Kong, China.


Arch Surg. 2003;138(1):100-104. doi:10.1001/archsurg.138.1.100.
Text Size: A A A
Published online

Hypothesis  Patients with bilobar stage IVa hepatocellular carcinoma (HCC) are generally considered unsuitable for hepatic resection. Recent data suggest that palliative hepatic resection in selected patients with advanced HCC may result in a favorable survival outcome. The aim of the present study was to evaluate the operative outcome and survival benefits of hepatic resection for patients with bilobar HCC.

Design  Retrospective study.

Setting  Tertiary referral center.

Patients  The study comprised 78 patients who were diagnosed as having unilobar HCC and considered initially suitable candidates for curative hepatic resection on preoperative investigations from 1989 to 2000. Bilobar disease with discrete tumor nodules in the contralateral lobe was diagnosed in these patients on laparoscopy (44 patients) or laparotomy (34 patients) with the help of intraoperative ultrasonography. Fifteen patients (19%) underwent palliative hepatic resection (group A), and hepatic resection was not performed in the remaining 63 patients (81%) (group B).

Main Outcome Measures  The clinicopathologic data and operative and survival outcomes of both groups of patients were compared.

Results  The clinicopathologic parameters were comparable in both groups of patients. In group A, 12 patients (80%) underwent major hepatic resection, and the mean ± SEM size of the resected tumors was 8.3 ± 0.9 cm. The operative morbidity and mortality were 20% and 0%, respectively. Treatment for tumors in the contralateral lobe included wedge excision (5 patients), alcohol injection (5 patients), cryotherapy (2 patients), and transarterial oily chemoembolization (3 patients). In group B, treatment for HCC included transarterial oily chemoembolization (42 patients), systemic chemotherapy (3 patients), transarterial oily chemoembolization and systemic chemotherapy (5 patients), cryotherapy (2 patients), tamoxifen (3 patients), and no treatment (8 patients). The median survival of patients in group A was 19.5 months, with 4 patients surviving for more than 3 years. The survival in group A was significantly better than in group B (median = 7.1 months; P = .008). On multivariate analysis, hepatic resection and preoperative serum α-fetoprotein level were the 2 independent factors that significantly affected patient survival.

Conclusions  Hepatic resection for HCC in patients with stage IVa bilobar disease results in a better survival outcome than nonresectional therapies. It should be considered in selected patients with low operative risks and satisfactory liver function.

Figures in this Article

PATIENTS WITH bilobar hepatocellular carcinoma (HCC) (stage IVa disease by International Union Against Cancer classification) are generally considered unsuitable for hepatic resection. Multidisciplinary treatment has often been performed in these patients, such as transarterial oily chemoembolization (TOCE), radiofrequency ablation, percutaneous ethanol injection, and microwave ablation.1,2 However, no generally effective treatment for these patients has yet been reported. Despite recent advances in diagnostic modalities, advanced HCC in some patients is only diagnosed on laparoscopy or laparotomy with the help of intraoperative ultrasonography.3,4 When bilobar disease is diagnosed intraoperatively, surgeons face the dilemma of whether to proceed with palliative resection, since the survival benefits of this surgical approach are uncertain. Palliative cytoreduction surgery in patients with advanced HCC has been advocated recently. However, its survival benefits over a nonresectional therapeutic approach in this group of patients have not been documented. The aim of our study was to evaluate the operative outcome and survival benefits of hepatic resection in patients with bilobar HCC.

Of the 2269 patients who were diagnosed as having HCC from January 1989 to December 2000, 673 were considered as having unilobar disease and were deemed suitable for curative hepatic resection after preoperative evaluation according to a standard protocol. Preoperative investigation of the patients included blood biochemistry, α-fetoprotein (AFP) assay, chest x-ray, percutaneous ultrasonography, computed tomography of the abdomen, and hepatic angiography in selected cases.5 Preoperative liver function was assessed with an indocyanine green clearance test and Child-Pugh grading.6 Bilobar HCC with discrete tumor nodules in the contralateral lobe was diagnosed in 78 patients intraoperatively during either laparoscopy (44 patients) or laparotomy (34 patients), with the help of intraoperative ultrasonography. Patients who had satellite lesions around the main tumor or direct extension of the tumor to the contralateral lobe and in whom curative resection could be performed with an extended hepatectomy were excluded from our study. Patients with other contraindications, including peritoneal metastasis and portal vein tumor thrombosis, that precluded curative hepatic resection were also excluded. Fifteen (19%) of the 78 patients underwent palliative hepatic resection (group A). Hepatic resection was abandoned in the remaining 63 patients (81%, group B) and various nonresectional therapies, including TOCE, systemic chemotherapy, cryotherapy, and oral tamoxifen, were provided. The clinicopathologic data and operative and survival outcomes of both groups of patients were compared.

Hepatic resection was performed following the standard technique described previously,7,8 and an ultrasonic dissector was used for parenchymal transection.9,10 All patients received the same perioperative care by the same team of surgeons and were nursed in the intensive care unit during the early postoperative period after hepatic resection. All intraoperative complications and postoperative morbidities were recorded prospectively. Hospital mortality was defined as death during the same period of hospitalization for the hepatic resection. All patients were followed up with serial AFP assay, and ultrasonography or computed tomography scan of the abdomen was performed every 3 months.

The clinical data on all patients were recorded prospectively in a computerized database by a single research assistant. Statistical analysis was performed by the χ2 test or the Fisher exact test to compare discrete variables. The Mann-Whitney test was used to compare continuous variables. Survival analysis was estimated by the Kaplan-Meier survival method. Statistical comparison of survival distributions was analyzed by log-rank tests. Multivariate analysis by the Cox proportional hazard regression model was used to identify independent clinical factors that significantly affected patient survival. Statistical analyses were performed by SPSS for Windows software (SPSS Inc, Chicago, Ill). A P value of less than .05 was considered to indicate statistical significance. Numeric values are expressed as mean ± SEM unless otherwise stated.

The study comprised 78 patients who had an intraoperative diagnosis of bilobar HCC with discrete tumor nodules in the contralateral lobe. There were 70 men (90%) and 8 women (10%), with a mean age of 51 ± 2.1 years (range, 13-79 years). Fifteen patients underwent palliative hepatic resection (group A), and hepatic resection was not performed in the remaining 63 patients (group B). The clinicopathologic parameters were comparable in both groups of patients (Table 1).

Table Graphic Jump LocationTable 1. Clinical and Laboratory Data of Patients Who Had Stage IVa Bilobar Hepatocellular Carcinoma and Underwent Hepatic Resection (Group A) and Those Who Did Not Undergo Hepatic Resection (Group B)*
GROUP A

The extent of hepatic resection in group A is presented in Table 2. Twelve patients (80%) underwent major hepatic resection involving 3 or more Couinaud segments.8 The mean size of resected tumors was 8.3 ± 0.9 cm, and 87% of the patients had underlying chronic liver diseases (Table 3). Treatment for tumor nodules in the contralateral lobe included wedge excision, ethanol injection, cryotherapy, and postoperative TOCE (Table 4). The mean operative blood loss was 1.5 ± 0.3 L, and 8 patients (53%) did not receive blood transfusion (Table 5). Postoperative complications occurred in 3 patients, resulting in an operative morbidity rate of 20%. The complications included chest infection (1 patient), pleural effusion that required chest tapping (1 patient), and wound infection (1 patient). There was no hospital death. The mean postoperative hospital stay was 12.2 ± 1.4 days.

Table Graphic Jump LocationTable 2. Hepatic Resection in 15 Patients Who Had Bilobar Stage IVa Hepatocellular Carcinoma (Group A)
Table Graphic Jump LocationTable 3. Pathologic Data of Patients Who Had Bilobar Stage IVa Hepatocellular Carcinoma and Underwent Hepatic Resection (Group A)
Table Graphic Jump LocationTable 4. Treatment for Tumors in the Contralateral Lobe in 15 Patients Who Underwent Hepatic Resection for Bilobar Hepatocellular Carcinoma (Group A)
Table Graphic Jump LocationTable 5. Intraoperative and Postoperative Data of 15 Patients Who Had Bilobar Hepatocellular Carcinoma and Underwent Hepatic Resection (Group A)
GROUP B

Patients in group B were diagnosed as having bilobar HCC on laparoscopy (37 patients) or laparotomy (26 patients). Among them, 14 (22%) were found to have normal, noncirrhotic livers. Postoperative complications occurred in 5 patients, resulting in an operative morbidity rate of 8%. These complications included chest infection (1 patient), pleural effusion that required chest tapping (2 patients), bleeding duodenal ulcer (1 patient), and wound infection (1 patient). There were 2 hospital deaths from chest infection and bleeding duodenal ulcer, respectively. The mean postoperative hospital stay was 8.7 ± 1.0 days. Various nonresectional therapies were provided for patients in group B (Table 6). Forty-two patients (67%) received TOCE, while 5 other patients received both TOCE and systemic chemotherapy. The median number of sessions of TOCE received by each patient was 3 (range, 1-24). Eight patients (13%) refused any form of nonsurgical treatment.

Table Graphic Jump LocationTable 6. Treatment for Hepatocellular Carcinoma in 63 Patients Who Had Bilobar Disease and Did Not Receive Hepatic Resection (Group B)
SURVIVAL RESULTS

The median survival of patients in group A was 19.5 months. Four patients, including 2 patients with normal noncirrhotic liver, survived for more than 3 years. The survival result was significantly better than that of group B (P = .008). At the time of preparation of the manuscript, 12 patients in group A had died of HCC. Three patients, with a median follow-up of 38 months, were alive with residual disease in the liver and pulmonary metastases. The median survival of patients in group B was 7.1 months (Figure 1).

Place holder to copy figure label and caption

Cumulative survival of 389 patients who had stage IVa bilobar hepatocellular carcinoma from 1989 to 2000. Group A: 15 patients who underwent hepatic resection; group B: 63 patients who underwent laparoscopy or laparotomy but did not receive hepatic resection; group C: 311 patients who were found to have bilobar disease on preoperative evaluation and did not undergo surgery (P = .008, group A vs group B; P = .008, group A vs group C; P = .72, group B vs group C).

Graphic Jump Location

During the same study period, there were 311 patients with HCC who were found to be unsuitable for curative hepatic resection and did not undergo surgery because of bilobar disease detected on preoperative evaluation (group C). Among them, 175 patients (56%) received transarterial chemoembolization. The median survival of these 311 patients was 6.4 months, and was not different from that of 7.1 months of the patients in group B (P = .72). The survival results were significantly worse than those of the patients in group A (P = .008, Figure 1).

Statistical analysis was performed on all 78 patients to identify clinical factors that significantly affected the survival. Eleven potential prognostic discriminants were examined, which included patient factors (age, sex, hepatitis status, preoperative indocyanine green clearance test, serum total bilirubin level, and prothrombin time), tumor factors (preoperative serum AFP level, location and size of the main tumor, and number of tumor nodules), and the treatment factor (hepatic resection or not). On multivariate analysis, hepatic resection and preoperative serum AFP level were the 2 independent factors that significantly affected patient survival (Table 7).

Table Graphic Jump LocationTable 7. Multivariate Analysis Using Cox Proportional Hazard Regression Model on Factors Affecting Overall Cumulative Survival of the 78 Patients With Bilobar Hepatocellular Carcinoma

Hepatic resection remains the treatment of choice for HCC and offers the best chance of long-term survival. However, most patients are considered unsuitable for surgical resection at the time of diagnosis because of advanced disease and the presence of concomitant liver cirrhosis.1,11 In patients with bilobar multicentric HCC, hepatic resection is usually not recommended because of the high operative risks and the difficulty of total tumor eradication. Multidisciplinary treatment has often been performed for these patients. However, no effective treatment that results in satisfactory survival has been reported.12,13 Total hepatectomy with liver transplantation to remove all tumors has been recommended for multiple bilobar HCC,14 but the results of liver transplantation for large and bilobar multifocal HCC have been poor.15,16 In addition, its application to malignant liver disease remains limited by the scarce availability of cadaveric grafts, especially in Eastern countries.

Noncurative hepatic resection (otherwise known as palliative or cytoreduction resection) is a new concept in the treatment of advanced HCC. There is some evidence that suggests that removal of as many tumors as possible from the liver may be an important prognostic factor.17,18 This interesting concept in the management of HCC goes against the widely held dogma that hepatic resection should be offered only when curative resection is possible. While most hepatic surgeons will challenge the role of noncurative resection in advanced HCC, such a concept is not without rationale. Yamamoto et al19 suggested that stage IVa HCC was more likely to have slow-growing intrahepatic tumor clusters, and that removal of rapidly growing tumors from such clusters by cytoreduction surgery might be associated with prolonged survival. In addition, even in patients undergoing hepatic resection with a curative intent, the outcome turned out to be palliative in most instances, as evidenced by a postoperative recurrence of 75% to 100%.20 Such a high incidence of recurrence, nevertheless, has not been considered a deterrent to hepatic resection for HCC because of the availability of effective treatment for recurrence to prolong survival. Therefore, it appears reasonable to propose that combined cytoreductive hepatic resection for a large tumor and ablation of smaller tumor nodules in the contralateral lobe may be an effective treatment for stage IVa bilobar HCC.

Tanaka et al21 reported hepatic resection in 55 patients with advanced HCC with tumor thrombi in the portal vein, direct invasion or compression of the inferior vena cava, extrahepatic bile duct involvement, or bilobar disease. The extension of surgical indication for these patients with advanced HCC was found to result in satisfactory survival. In 1998, Ikai et al22 also reported the results of hepatic resection in a selected group of patients with stage IVa HCC without lymph node metastasis, and proposed it as a standard therapy for such patients. Patients who had bilobar disease and underwent hepatic resection had a 5-year survival rate of 20%, which was significantly better than that of 8% in patients who had vascular invasion. Although the survival results of patients who had stage IVa bilobar disease appeared satisfactory, the authors did not directly compare survival of these patients with a comparable group who underwent nonresectional multimodality therapies2,23,24 to justify the operative mortality and morbidity rates of 8.4% and 51%, respectively, reported in their series.

To justify noncurative hepatic resection for stage IVa bilobar HCC, some prerequisites should be satisfied. First, hepatic resection should be associated with a minimal major operative morbidity and a near-zero operative mortality. Second, effective treatment should be available for the smaller lesions in the contralateral lobe. Third, hepatic resection should result in improved survival compared with nonresectional therapies. In our study, hepatic resection in patients with bilobar HCC was found to be associated with acceptable morbidity and zero operative mortality, which were comparable with those who underwent curative hepatic resection.25,26 Prolongation of survival in patients with advanced HCC should not be expected with cytoreduction surgery alone. Therefore, multidisciplinary treatment, which included wedge excision, local ablative therapy, and postoperative regional chemoemolization, was provided for all patients with tumors in the contralateral lobe. This aggressive surgical approach was also shown to result in satisfactory survival, which was superior to that of patients with comparable clinicopathologic parameters treated by nonresectional therapies (group B).

Major limitations of our study included the small number of patients recruited and the nonrandomized selection of patients with bilobar HCC for hepatic resection. The decision to perform noncurative hepatic resection in group A was made at the time of laparoscopy or laparotomy. This resulted in a potential bias toward selecting patients based on favorable clinical and pathologic parameters. It can be observed that several important clinical parameters, including preoperative indocyanine green and serum bilirubin levels, were worse in group B (Table 1), although the difference did not reach statistical significance. However, on multivariate analysis, hepatic resection was identified to be one of the independent significant factors affecting survival of patients with bilobar HCC. In the future, a prospective randomized study to validate the findings of our study will be performed. Another deficiency of the present retrospective study is that the studied population only included patients with stage IVa bilobar HCC with intraoperative diagnosis of small tumor nodules in the contralateral lobe. Further investigation is required to document whether the results of our study can be extrapolated to patients with a preoperative diagnosis of bilobar disease.

In conclusion, hepatic resection for HCC in patients with bilobar stage IVa disease results in a better survival outcome when compared with those treated by nonresectional therapies. This treatment strategy should be considered in selected patients with low operative risks and satisfactory liver function. Further prospective randomized studies are required to evaluate the survival benefits of this aggressive surgical approach.

Corresponding author: Chi-Leung Liu, MS, FRCS, Department of Surgery, University of Hong Kong Medical Centre, Queen Mary Hospital, 102 Pokfulam Rd, Hong Kong, China (e-mail: clliu@hkucc.hku.hk).

Accepted for publication September 8, 2002.

Venook  AP Treatment of hepatocellular carcinoma: too many options? J Clin Oncol. 1994;121323- 1334
Liu  CLFan  ST Nonresectional therapies for hepatocellular carcinoma. Am J Surg. 1997;173358- 365
Link to Article
Makuuchi  MKosuge  TTakayama  T  et al.  Surgery for small liver cancers. Semin Surg Oncol. 1993;9298- 304
Link to Article
Lo  CMLai  ECLiu  CLFan  STWong  J Laparoscopy and laparoscopic ultrasonography avoid exploratory laparotomy in patients with hepatocellular carcinoma. Ann Surg. 1998;227527- 532
Link to Article
Fan  STNg  IOPoon  RTLo  CMLiu  CLWong  J Hepatectomy for hepatocellular carcinoma: the surgeon's role in long-term survival. Arch Surg. 1999;1341124- 1130
Link to Article
Pugh  RNMurray-Lyon  IMDawson  JLPietroni  MCWilliams  R Transection of the oesophagus for bleeding oesophageal varices. Br J Surg. 1973;60646- 649
Link to Article
Blumgart  LHJarnagin  WRFong  Y Liver resection for benign diseases and for liver and biliary tumors. Blumgart  LHSurgery of the Liver and the Biliary Tract 3rd ed. London, England W. B. Saunders2000;1639- 1713
Strasberg  SMBelghiti  JClavien  PA  et al.  The Brisbane 2000 terminology of liver anatomy and resections. HPB Surg. 2000;2333- 339
Fan  STLai  ECLo  CMChu  KMLiu  CLWong  J Hepatectomy with an ultrasonic dissector for hepatocellular carcinoma. Br J Surg. 1996;83117- 120
Link to Article
Liu  CLFan  STLo  CMTung-Ping  PRWong  J Anterior approach for major right hepatic resection for large hepatocellular carcinoma. Ann Surg. 2000;23225- 31
Link to Article
Okuda  KOhtsuki  TObata  H  et al.  Natural history of hepatocellular carcinoma and prognosis in relation to treatment: study of 850 patients. Cancer. 1985;56918- 928
Link to Article
Tanikawa  KTanaka  M Treatment of advanced hepatocellular carcinoma. Intern Med. 1995;34300- 302
Link to Article
Kanematsu  TMatsumata  TFuruta  T  et al.  Lipiodol drug targeting in the treatment of primary hepatocellular carcinoma. Hepatogastroenterology. 1990;37442- 444
Bismuth  HChiche  LAdam  RCastaing  DDiamond  TDennison  A Liver resection versus transplantation for hepatocellular carcinoma in cirrhotic patients. Ann Surg. 1993;218145- 151
Link to Article
Mazzaferro  VRegalia  EDoci  R  et al.  Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334693- 699
Link to Article
Yao  FYFerrell  LBass  NM  et al.  Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology. 2001;331394- 1403
Link to Article
Shimada  MTakenaka  KKawahara  N  et al.  Surgical treatment strategy for patients with stage IV hepatocellular carcinoma. Surgery. 1996;119517- 522
Link to Article
Usatoff  VIsla  AMHabib  NA Liver resection in advanced hepatocellular carcinoma. Hepatogastroenterology. 2001;4846- 50
Yamamoto  MIizuka  HMatsuda  MNagahori  KMiura  KItakura  J The indications for tumor mass reduction surgery and subsequent multidisciplinary treatments in stage IV hepatocellular carcinoma. Surg Today. 1993;23675- 681
Link to Article
Poon  RTPFan  STWong  J Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg. 2000;23210- 24
Link to Article
Tanaka  AMorimoto  TOzaki  N  et al.  Extension of surgical indication for advanced hepatocellular carcinoma: is it possible to prolong life span or improve quality of life? Hepatogastroenterology. 1996;431172- 1181
Ikai  IYamaoka  YYamamoto  Y  et al.  Surgical intervention for patients with stage IV-A hepatocellular carcinoma without lymph node metastasis: proposal as a standard therapy. Ann Surg. 1998;227433- 439
Link to Article
Zhou  XDTang  ZYYu  YQ  et al.  Multimodality treatment in advanced primary liver cancer. Gan To Kagaku Ryoho. 1995;22 (suppl 3) 286- 289
Tang  ZYYu  YQZhou  XD  et al.  Treatment of unresectable primary liver cancer: with reference to cytoreduction and sequential resection. World J Surg. 1995;1947- 52
Link to Article
Fan  STLo  CMLiu  CL  et al.  Hepatectomy for hepatocellular carcinoma: toward zero hospital deaths. Ann Surg. 1999;229322- 330
Link to Article
Torzilli  GMakuuchi  MInoue  K  et al.  No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? a prospective analysis of our approach. Arch Surg. 1999;134984- 992
Link to Article

Figures

Place holder to copy figure label and caption

Cumulative survival of 389 patients who had stage IVa bilobar hepatocellular carcinoma from 1989 to 2000. Group A: 15 patients who underwent hepatic resection; group B: 63 patients who underwent laparoscopy or laparotomy but did not receive hepatic resection; group C: 311 patients who were found to have bilobar disease on preoperative evaluation and did not undergo surgery (P = .008, group A vs group B; P = .008, group A vs group C; P = .72, group B vs group C).

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Clinical and Laboratory Data of Patients Who Had Stage IVa Bilobar Hepatocellular Carcinoma and Underwent Hepatic Resection (Group A) and Those Who Did Not Undergo Hepatic Resection (Group B)*
Table Graphic Jump LocationTable 2. Hepatic Resection in 15 Patients Who Had Bilobar Stage IVa Hepatocellular Carcinoma (Group A)
Table Graphic Jump LocationTable 3. Pathologic Data of Patients Who Had Bilobar Stage IVa Hepatocellular Carcinoma and Underwent Hepatic Resection (Group A)
Table Graphic Jump LocationTable 4. Treatment for Tumors in the Contralateral Lobe in 15 Patients Who Underwent Hepatic Resection for Bilobar Hepatocellular Carcinoma (Group A)
Table Graphic Jump LocationTable 5. Intraoperative and Postoperative Data of 15 Patients Who Had Bilobar Hepatocellular Carcinoma and Underwent Hepatic Resection (Group A)
Table Graphic Jump LocationTable 6. Treatment for Hepatocellular Carcinoma in 63 Patients Who Had Bilobar Disease and Did Not Receive Hepatic Resection (Group B)
Table Graphic Jump LocationTable 7. Multivariate Analysis Using Cox Proportional Hazard Regression Model on Factors Affecting Overall Cumulative Survival of the 78 Patients With Bilobar Hepatocellular Carcinoma

References

Venook  AP Treatment of hepatocellular carcinoma: too many options? J Clin Oncol. 1994;121323- 1334
Liu  CLFan  ST Nonresectional therapies for hepatocellular carcinoma. Am J Surg. 1997;173358- 365
Link to Article
Makuuchi  MKosuge  TTakayama  T  et al.  Surgery for small liver cancers. Semin Surg Oncol. 1993;9298- 304
Link to Article
Lo  CMLai  ECLiu  CLFan  STWong  J Laparoscopy and laparoscopic ultrasonography avoid exploratory laparotomy in patients with hepatocellular carcinoma. Ann Surg. 1998;227527- 532
Link to Article
Fan  STNg  IOPoon  RTLo  CMLiu  CLWong  J Hepatectomy for hepatocellular carcinoma: the surgeon's role in long-term survival. Arch Surg. 1999;1341124- 1130
Link to Article
Pugh  RNMurray-Lyon  IMDawson  JLPietroni  MCWilliams  R Transection of the oesophagus for bleeding oesophageal varices. Br J Surg. 1973;60646- 649
Link to Article
Blumgart  LHJarnagin  WRFong  Y Liver resection for benign diseases and for liver and biliary tumors. Blumgart  LHSurgery of the Liver and the Biliary Tract 3rd ed. London, England W. B. Saunders2000;1639- 1713
Strasberg  SMBelghiti  JClavien  PA  et al.  The Brisbane 2000 terminology of liver anatomy and resections. HPB Surg. 2000;2333- 339
Fan  STLai  ECLo  CMChu  KMLiu  CLWong  J Hepatectomy with an ultrasonic dissector for hepatocellular carcinoma. Br J Surg. 1996;83117- 120
Link to Article
Liu  CLFan  STLo  CMTung-Ping  PRWong  J Anterior approach for major right hepatic resection for large hepatocellular carcinoma. Ann Surg. 2000;23225- 31
Link to Article
Okuda  KOhtsuki  TObata  H  et al.  Natural history of hepatocellular carcinoma and prognosis in relation to treatment: study of 850 patients. Cancer. 1985;56918- 928
Link to Article
Tanikawa  KTanaka  M Treatment of advanced hepatocellular carcinoma. Intern Med. 1995;34300- 302
Link to Article
Kanematsu  TMatsumata  TFuruta  T  et al.  Lipiodol drug targeting in the treatment of primary hepatocellular carcinoma. Hepatogastroenterology. 1990;37442- 444
Bismuth  HChiche  LAdam  RCastaing  DDiamond  TDennison  A Liver resection versus transplantation for hepatocellular carcinoma in cirrhotic patients. Ann Surg. 1993;218145- 151
Link to Article
Mazzaferro  VRegalia  EDoci  R  et al.  Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334693- 699
Link to Article
Yao  FYFerrell  LBass  NM  et al.  Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology. 2001;331394- 1403
Link to Article
Shimada  MTakenaka  KKawahara  N  et al.  Surgical treatment strategy for patients with stage IV hepatocellular carcinoma. Surgery. 1996;119517- 522
Link to Article
Usatoff  VIsla  AMHabib  NA Liver resection in advanced hepatocellular carcinoma. Hepatogastroenterology. 2001;4846- 50
Yamamoto  MIizuka  HMatsuda  MNagahori  KMiura  KItakura  J The indications for tumor mass reduction surgery and subsequent multidisciplinary treatments in stage IV hepatocellular carcinoma. Surg Today. 1993;23675- 681
Link to Article
Poon  RTPFan  STWong  J Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg. 2000;23210- 24
Link to Article
Tanaka  AMorimoto  TOzaki  N  et al.  Extension of surgical indication for advanced hepatocellular carcinoma: is it possible to prolong life span or improve quality of life? Hepatogastroenterology. 1996;431172- 1181
Ikai  IYamaoka  YYamamoto  Y  et al.  Surgical intervention for patients with stage IV-A hepatocellular carcinoma without lymph node metastasis: proposal as a standard therapy. Ann Surg. 1998;227433- 439
Link to Article
Zhou  XDTang  ZYYu  YQ  et al.  Multimodality treatment in advanced primary liver cancer. Gan To Kagaku Ryoho. 1995;22 (suppl 3) 286- 289
Tang  ZYYu  YQZhou  XD  et al.  Treatment of unresectable primary liver cancer: with reference to cytoreduction and sequential resection. World J Surg. 1995;1947- 52
Link to Article
Fan  STLo  CMLiu  CL  et al.  Hepatectomy for hepatocellular carcinoma: toward zero hospital deaths. Ann Surg. 1999;229322- 330
Link to Article
Torzilli  GMakuuchi  MInoue  K  et al.  No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? a prospective analysis of our approach. Arch Surg. 1999;134984- 992
Link to Article

Correspondence

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
PubMed Articles
JAMAevidence.com

Care at the Close of Life EDUCATION GUIDES
Integrating Palliative Care for Liver Transplant Candidates