World J Gastroenterol

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ISSN = 1007-9327 CN=20 14-1219/R World=20 J Gastroenterol = 2009=20 November 21; 15(43):=20 5481-5488
BRIEF=20 ARTICLE
Efficacy of = surgical=20 resection in management of isolated extrahepatic metastases = of=20 hepatocellular carcinoma

Kun-Ming Chan, Ming-Chin Yu, = Ting-Jung Wu,=20 Chen-Fang Lee, Tse-Ching Chen, Wei-Chen Lee, Miin-Fu=20 Chen

Kun-Ming Chan,=20 Ming-Chin Yu, Ting-Jung Wu, Chen-Fang Lee, Wei-Chen Lee, Miin-Fu = Chen,=20 Department=20 of General Surgery, Chang Gung Memorial Hospital-Linkou Medical = Center,=20 Chang Gung University College of Medicine, 33305 Taoyuan, Taiwan,=20 China

Tse-Ching Chen,=20 Department=20 of Pathology, Chang Gung Memorial Hospital-Linkou Medical Center, = Chang=20 Gung University College of Medicine, 33305 Taoyuan, Taiwan,=20 China

Author contributions: Chan = KM performed=20 the research, analyzed the data, and wrote the paper; Yu MC, Wu = TJ, Lee CF=20 and Chen TC collected the data; Lee WC and Chen MF designed the = research.=20

Correspondence to:=20 Wei-Chen Lee, MD, Department of General Surgery, Chang = Gung Memorial=20 Hospital-Linkou Medical Center, Chang Gung University College of = Medicine,=20 5, Fu-Hsing Street, Kwei-Shan Township, Taoyuan County, 33305, = Taiwan,=20 China. weichen@cgmh.org.tw

Telephone: +886-3-3281200 Fax:=20 +886-3-3285818

Received:=20 July 25, 2009 = Revised:=20 October 12, 2009

Accepted: = October 19,=20 2009

Published=20 online: November 21, 2009=20

Abstract

AIM: To clarify the benefit of surgical excision for patients = with=20 extrahepatic metastases of hepatocellular carcinoma=20 (HCC).

METHODS:=20 We=20 retrospectively reviewed the medical records of 140 patients with=20 pathologically proven extrahepatic metastases of HCC and evaluated = the=20 outcomes of those who had undergone surgical resection (SR) for=20 extrahepatic metastatic lesions. Prognoses made on the basis of=20 extrahepatic metastatic sites were also examined.=20

RESULTS:=20 The=20 survival rates of patients who underwent SR of extrahepatic = metastases=20 were significantly better than those of patients who did not = receive SR.=20 For the SR group, 1- and 3-year survival rates were 24% and 7%,=20 respectively, while for the non-resection group, the survival = rates were=20 8% and 0%, respectively (P < 0.0001). Survival rates related = to metastatic=20 sites were also significantly superior after SR of extrahepatic=20 metastases: median survivals were 32 mo with lung metastasis, 10 = mo with=20 bone metastasis, 6.1 mo with brain = metastasis.

CONCLUSION:=20 SR can=20 provide survival benefits for patients with 1 or 2 isolated = extrahepatic=20 metastases and who concurrently exhibit good hepatic functional = reserve=20 and general performance status as well as successful treatment of=20 intrahepatic HCC.

Key words: Hepatocellular=20 carcinoma; Hepatic resection; Extrahepatic metastases; Surgical = resection;=20 Outcome

Peer=20 reviewer: Osman C Ozdogan, Associate Professor, Department of=20 Gastroenterology, Liver Unit, Marmara University School of = Medicine,=20 Istanbul 34662, Turkey

Chan = KM, Yu MC, Wu=20 TJ, Lee CF, Chen TC, Lee WC, Chen MF. Efficacy of surgical = resection in=20 management of isolated extrahepatic metastases of hepatocellular=20 carcinoma. World J Gastroenterol 2009; 15(43): = 5481-5488 =20 Available from: URL: = http://www.wjgnet.com/1007-9327/15/5481.asp =20 DOI: http://dx.doi.org/10.3748/wjg.15.5481

INTRODUCTION

Hepatocellular carcinoma (HCC) is = an=20 aggressive malignant tumor that occurs throughout the world. It is = one of=20 the leading causes of cancer-related death among people in East = Asian=20 countries. Recent progress in diagnostic tools has led to an = improved=20 prognosis for HCC patients because of enhanced detection of early = and=20 small HCC and better identification of those patients who qualify = for=20 hepatic resection (HR)^[1-5]. Moreover, treatment trends = towards=20 aggressive multimodal therapy in patients with intra-hepatic HCC = have also=20 improved long-term outcomes^[6-9]. Nevertheless, = extrahepatic=20 metastasis of primary HCC is still considered terminal-stage = cancer, and=20 the prognosis for patients at this stage continues to be poor due = to=20 limited effective treatment. Despite recognition of this = situation, there=20 appears to be no consensus among the medical community regarding = treatment=20 strategies for HCC patients with extrahepatic metastasis. = Therefore, to=20 improve the overall long-term survival of patients with HCC, more = active=20 treatment of extrahepatic metastases is necessary. Several studies = have=20 recently demonstrated that surgical resection (SR) of extrahepatic = metastases is able to provide benefits for selected patients with=20 HCC^[10-13]. However, the role of SR in HCC patients = with=20 extrahepatic metastases required further clarification. In this = study, we=20 present our experience with patients with extrahepatic metastases = of=20 primary HCC and evaluate the benefits of surgical removal of = extrahepatic=20 lesions.

MATERIALS AND=20 METHODS

Patients

A total of 2245 patients = with primary=20 HCC were treated at the Department of Surgery, Chang Gung Memorial = Hospital-Linkou Medical Center in Taiwan, during the study period = between=20 June 1988 and June 2008. Among them, medical records of 151 = patients with=20 pathologically proven extrahepatic metastases from primary HCC = were=20 retrospectively reviewed. Metastasis of HCC was confirmed for all = patients=20 by histological examination of specimens derived from either = biopsy or=20 excision of extrahepatic tumor lesions. Of the 151 patients, 11 = were lost=20 to follow-up; thus, the remaining 140 patients, including 108 men = and 32=20 women, were enrolled in the present study.

Diagnosis and treatment = of=20 intra-hepatic HCC

Intrahepatic = primary or=20 recurrent HCC was diagnosed by dynamic liver computed tomography = (CT)=20 scans and hepatic angiography, which shows hyperattenuation in the = arterial phase and hypoattenuation in the late phase indicating=20 hypervascular tumor mass. Ultrasound-guided biopsy was performed = only when=20 considered necessary. a-fetoprotein was also routinely = checked as a=20 parameter of diagnosis.

Treatment of intrahepatic HCC = consisted of=20 multimodal therapeutic procedures including hepatic resection = (HR),=20 radiofrequency ablation, percutaneous chemical reagent injection,=20 transcatheter arterial chemoembolization (TACE), or a combination = of these=20 treatment modalities. Treatment methods were selected for = hospitalized HCC=20 patients based on the following principles. HR was considered a = priority=20 for patients with intrahepatic HCC whenever the tumor was = determined to be=20 resectable. An alternative approach, such as local ablation or = TACE, was=20 performed as indicated if patients had systemic multiple tumors, a = difficult tumor location, unsuitable conditions for HR, or refused = surgical treatment. Patients might also have received concurrent = or=20 sequential multimodal treatments if conditions warranted.=20

Diagnosis and treatment = of=20 extrahepatic HCC

Detection of = extrahepatic HCC and=20 determination of tumor location was accomplished through X-ray, = CT,=20 magnetic resonance imaging (MRI), or bone scintigraphy as = indicated and=20 under two conditions: namely, recurrent and concurrent. Recurrent=20 extrahepatic HCC was noted during post-operative follow-up after = treatment=20 for primary HCC. Concurrent extrahepatic HCC was observed at the = initial=20 diagnosis stage of intrahepatic HCC. In order to ensure the = significance=20 and validity of our research, only those patients with = pathologically=20 proven extrahepatic metastasis of HCC were included in our study.=20

Treatment of extrahepatic = metastasis varied=20 according to the individual clinical characteristics of each = patient. SR=20 was selected for patients whose extrahepatic HCC was solitary, = isolated,=20 and considered resectable, and for whom intrahepatic tumor = recurrence was=20 not observed after previous treatment or for whom the intrahepatic = tumor=20 was completely treated by either HR or other treatment modalities. = Systemic chemotherapy was reserved for those patients deemed = unsuitable=20 for SR. Radiotherapy was performed to relieve patients=92 symptoms = as=20 indicated.

Follow-up =

All patients were = closely followed up=20 at regular intervals until death or until the writing of this = article. The=20 duration of follow-up after first diagnosis of HCC ranged from 1 = to 138 mo=20 (median, 16 mo). Follow-up after diagnosis of extrahepatic = metastasis=20 ranged from 0.8 to 96 mo (median, 6.1 mo).

Statistical=20 analysis

All data were analyzed = using the=20 statistical software Prism 5.0 (GraphPad Software, San Diego, CA, = USA).=20 Survival rates were calculated by the Kaplan-Meier method, and the = log-rank test was used to compare survival rates. Patients who = died from=20 surgical complications were excluded from the survival curve. A = value of=20 P < 0.05 was considered statistically significant.=20

RESULTS

Clinical=20 features of patients with extrahepatic metastases from=20 HCC

The clinical = characteristics of=20 patients at initial diagnosis of extrahepatic metastases are = summarized in=20 Table = 1.=20 The average age of these patients was 55.8 years (range, 13 to 81 = years).=20 Predominant clinical elements were male gender (77%, 108/140) and = a=20 positive test for the hepatitis B virus (47%, 66/140). These = findings were=20 similar to those of our previous reports on primary = HCC^[14,15].=20 Further, 66 patients (47%) had previously undergone HR for primary = HCC.=20 Among these patients, 7 had received multiple HRs for intrahepatic = HCC and=20 2 had undergone liver transplantation. Extrahepatic metastases had = occurred mainly at bone, brain, lung, and soft tissue locations. = Patients=20 categorized into the soft tissue group had extrahepatic metastases = to=20 intra-abdominal soft tissue (6 patients), intra-abdominal organs = (4=20 patients), abdominal wall (16 patients), breast (1 patient), and = skin plus=20 subcutaneous tissue (8 patients).

SR of=20 extrahepatic metastases of HCC was performed on 86 patients (64 = male and=20 22 female: Table=20 2). Further, 59 out of 86 patients had intrahepatic tumors = at the=20 time of extrahepatic metastasis detection. Among these patients, = 54 were=20 also treated by TACE, local ablation, or a combination of both = therapies=20 for their intrahepatic lesion; thus, most patients received more = than one=20 course of treatment prior to resection of the extrahepatic lesion. = Five=20 patients underwent simultaneous HR for intrahepatic HCC and SR of=20 extrahepatic metastases.

Survival of patients=20

The median length of = patient survival=20 was 6.9 mo (range, 0.8 to 96 mo), and the overall 1-, 3-, and = 5-year=20 survival rates were 31%, 7%, and 4%, respectively, for all = patients with=20 extrahepatic metastases of HCC (Figure = 1A).=20 Long-term overall survival was significantly better in patients = who=20 underwent SR of extrahepatic metastases than in those who did not=20 [non-resection (NR) patients]. The 1-year/3-year survival rates = were=20 24%/7% for the SR group as compared with the 1-year/3-year = survival rates=20 of 8%/0% for the NR group (Figure = 1B, P=20 < 0.0001).

We further analyzed = survival rates=20 according to whether HR had been performed. Sixty-six patients had = previously undergone HR (Table = 1),=20 including 5 patients who underwent simultaneous resection of = intrahepatic=20 and extrahepatic tumors at initial diagnosis and 61 patients who = underwent=20 resection of intrahepatic tumors followed by subsequent resection = of=20 extrahepatic tumor recurrence. The outcome for patients who = underwent SR=20 was significantly better than that of the NR patients (Figure 2A and = B), and the survival rate of SR patients in the HR group=20 (1-year/3-year, 52.5%/32.1%) was considerably better than that of = the=20 non-HR group (1-year/3-year, 19.4%/3.9%, P =3D 0.0020; = Figure = 2C).=20

The=20 cumulative 1- and 3-year survival rates after extrahepatic = metastases were=20 22.1%/4.1% for bony metastases, 11.8%/0% for brain metastases, = 59.4%/20.8%=20 for lung metastases, and 31.2%/27.3% for soft tissue metastases,=20 respectively. The comparison of survival curves in relation to = metastatic=20 sites is depicted in Figure = 3 and=20 indicates that patients who received SR of extrahepatic HCC = had a=20 significantly better prognosis than patients in the NR group. The = 1- and=20 3-year survival rates of the SR group vs the NR group by = metastatic=20 site were, respectively, 35.9%/9.0% (median survival,
10 = mo) vs=20 10%/0% (median survival, 3.6 mo) for bony metastases (Figure = 3A, P=20 =3D 0.0022); 13.6%/0% (median survival, 6.1 mo) vs = 0%/0% (median=20 survival, 1.7 mo) for brain metastases (Figure = 3B, P=20 =3D 0.0055); 89%/40% (median survival, 32 mo) vs = 37.5%/9.4%=20 (median survival, 7.9 mo) for lung metastases (Figure = 3C, P=20 =3D 0.0063); and 40.2%/40.2% (median survival, 10.1 mo) vs=20 16.7%/0% (median survival, 3.5 mo) for soft tissue metastases = (Figure = 3D, P=20 =3D 0.0080). Among those patients who had undergone SR, = resection of=20 lung metastases demonstrated most favorable outcomes when compared = with=20 the other metastatic sites (Figure = 4, P=20 < 0.05).

Patients with long-term = survival=20

The=20 clinical features of patients with favorable outcomes who survived = more=20 than 3 years after extrahepatic metastases diagnosis are listed in = Table = 3. Four=20 patients had undergone HR and one had received TACE for their = primary HCC.=20 All patients had experienced intrahepatic recurrence and were = treated by=20 either TACE or local ablation after initial treatment. A solitary=20 metastatic lesion at the 12th thoracic spine was noted in patient = 2 (Table = 3) 16 mo=20 after hepatic resection, and another episode of isolated pulmonary = metastasis was encountered in the subsequent 32 mo. Both events = were=20 successfully treated by SR, but the patient died 89 mo after = initial=20 detection of extrahepatic metastasis due to systemic metastases. = Three=20 patients were still living at the end of this study; follow-up of = patient=20 4 has been ongoing for 96 mo after SR of his intra-abdominal = metastatic=20 lesion.

DISCUSSION

HCC is=20 an aggressive malignant neoplasm with dismal prognosis because of = the high=20 incidence of intrahepatic recurrence after initial treatment. = However,=20 recent trends towards aggressive treatment of intrahepatic = recurrence with=20 multimodal therapy have significantly improved the overall outcome = of=20 patients with HCC^[6,9,16]. This trend, along with = better=20 treatment of intrahepatic HCC, may not only prolong a patient=92s = survival=20 but may also retard anticipated extrahepatic metastases. Because = the=20 prognosis of patients with extrahepatic metastases is considered = very poor=20 and because there is limited information regarding treatment = strategies=20 for these patients, it is necessary to actively develop more = aggressive=20 treatment methods in order to further improve the long-term = survival of=20 HCC patients with extrahepatic metastases.

HCC is=20 a hypervascular tumor and is believed to spread mainly through a=20 hematogenous route, causing extrahepatic metastases. It has been = reported=20 that extrahepatic metastases occur in 13.5%-41.7% of HCC=20 patients^[17-20]; however, actual prevalence may be = higher than=20 that reported. Although all HCC patients are followed up at = regular=20 intervals for intrahepatic recurrence = using a=20 variety of diagnostic tools, not all patients receive complete = examination=20 for extrahepatic metastases. Moreover, the majority of patients = with=20 extrahepatic metastases experience no specific symptoms, and it is = possible to overlook extrahepatic metastases upon examination. = Therefore,=20 increased detection of extrahepatic metastases suitable for=20 aggressive treatment may provide great benefit to patients and = improve=20 overall survival of those with HCC.

Increasing evidence = shows that SR of=20 metastatic lesions with curative intent has become standard = practice for=20 the management of several malignancies. SR of isolated metastatic = lesions=20 from colorectal cancer, gastrointestinal stromal tumors, = neuroendocrine=20 cancers, renal-cell carcinoma and sarcoma is associated with = favorable=20 outcomes^[21-24]. Furthermore, improvements in patient = safety=20 during complex surgeries have also lowered the threshold for more=20 aggressive surgical intervention. Recently, several reports have = shown=20 that SR of HCC metastases prolonged survival in selected=20 patients^{[10,11,13,25]}. Our results appear to be = comparable with=20 those reports which indicated that patients who received SR of=20 extrahepatic metastases had better outcomes than patients who did = not=20 receive SR. In addition, in our study, patients undergoing SR of = lung=20 metastases had better survival rates than patients with bony and = brain=20 metastases, which is comparable with previous reports that = surgical=20 resection of pulmonary metastasis from HCC has favorable outcome. = Although=20 the small number of patients involved in this study might not = reflect a=20 real variation in outcomes due to metastatic location, we believe = that our=20 observations are valid. However, the difference in outcomes based = on=20 metastatic site may be related to the molecular biological pattern = of HCC;=20 therefore, further studies involving basic science and using a = larger=20 number of patients should be conducted to clarify the significance = of our=20 results.

Bony=20 metastasis is one of the most frequent extrahepatic = metastasis of HCC=20 and occurs as multiple metastases in most=20 patients^[19,26,27]. In this study, the outcome of HCC = patients=20 with bony metastases was poor. Patients with metastases to bone = had a=20 median survival of 6.7 mo, which is similar to previous=20 reports^[28,29]. Data also indicate that the spine is = the most=20 common site of bony metastasis of HCC, and further studies suggest = that=20 surgical treatment for spinal metastatic HCC lesions usually = improves=20 quality of life instead of prolonging patient = survival^[30].=20 Nevertheless, prolongation of survival may still be achievable in = selected=20 patients, as observed in the current study. The longest survival = of a=20 patient who had undergone resection of metastasis at the left = femoral=20 shaft was 30 mo after the detection of extrahepatic=20 metastasis.

Brain metastasis of HCC = is relatively=20 rare and is detected in less than 1% of HCC = patients^[20,31].=20 The overall prognosis of patients with brain metastases is = extremely poor,=20 and the most recent report showed that the median survival of = these=20 patients was only 6.8 wk after the detection of metastatic brain=20 lesions^[32]. Clinically, brain metastases are = frequently=20 associated with mass-producing hemorrhage, a condition requiring = further=20 surgical treatment. Although the surgical excision of brain = metastases is=20 considered a palliative treatment, several reports have also shown = that a=20 favorable outcome was achievable in patients with a single brain=20 metastasis and good liver function and performance=20 status^[32,33]. Our study showed that patients who had = undergone=20 SR of brain metastases fared significantly better than NR = patients, with a=20 median survival of 6.1 mo vs 1.7 mo. Thus, SR of metastatic = brain=20 lesions of HCC should be considered in specific patients not only = to=20 improve quality of life but also to prolong life=20 expectancy.

Nonetheless, one might argue that = patients=20 who are not suitable for surgical resection are naturally in = poorer=20 condition than patients who underwent SR for extrahepatic = metastasis.=20 Indeed, although HCC with extrahepatic metastasis is considered = the=20 terminal-stage of TNM staging, the outcome of patients with = systemic=20 multiple metastases theoretically might be poorer than those of = one or two=20 isolated extrahepatic metastases. However, the accumulated data = and this=20 study have shown that SR of extrahepatic metastases can = effectively=20 provide real benefits for patients with HCC. Although there is no = standard=20 treatment for extrahepatic metastases of HCC, aggressive treatment = in=20 patients with HCC should be considered, not only in cases of = intrahepatic=20 HCC, but also in the event of extrahepatic metastases. Taking into = consideration that there are no effective nonsurgical treatment = modalities=20 for extrahepatic metastases of HCC, surgical treatment may be the = only=20 modality available for curing selected patients. As our study has = shown,=20 patients who have undergone HR prior to SR for extrahepatic = metastases had=20 the best outcome, indicating that patients should be closely = followed up=20 at regular intervals after initial treatment of primary HCC to = ensure=20 early detection of extrahepatic metastases at a resectable stage.=20

In=20 conclusion, we herein propose the following algorithm for surgical = management of extrahepatic metastases from HCC (Figure = 5).=20 Surgical excision of extrahepatic metastases should be considered = in=20 patients with one or two isolated extrahepatic metastases if the = patient=20 has otherwise good performance status, good hepatic functional = reserve,=20 and well-controlled intrahepatic HCC. Although the retrospective = nature of=20 the current study and the small number of patients with resectable = extrahepatic metastases makes it hard to compare outcome of = patients=20 undergoing SR for isolated extrahepatic metastasis with those who = do not=20 receive SR, the marked differences we observed may prove helpful = in the=20 management of patients with HCC. Furthermore, to achieve better = long-term=20 outcomes of patients with HCC, as well as effective treatment of=20 extrahepatic metastases, new promising treatments such as a novel = systemic=20 chemotherapy or targeting therapy should be developed. =

COMMENTS

Background

Hepatocellular carcinoma = (HCC) is a=20 common malignant tumor, and ranked within the top five of = cancer-related=20 deaths worldwide. Patients with extrahepatic metastases of primary = HCC are=20 clinically considered at terminal-stage cancer, and there is still = no=20 effective treatment as well as no consensus on treatment = strategies for=20 these patients. Recently, several reports have shown benefit of = surgical=20 resection of extrahepatic metastases from HCC. However, the role = of=20 surgical resection in the treatment of extrahepatic metastasis of = primary=20 HCC remains uncertain.

Research=20 frontiers

The concept of treating = metastatic=20 cancer has been changing recently. Patients with several types of=20 metastatic cancers such as colon cancer, gastrointestinal stromal = tumor,=20 neuroendocrine cancer, sarcoma, renal cell carcinoma, = etc.=20 are considered to gain benefit from surgical resection of = metastatic=20 lesions. Therefore, it seems reasonable to attempt aggressive = surgical=20 resection for HCC patients with extrahepatic metastases.=20

Innovations and=20 breakthroughs

In the present study, = the authors=20 gathered their experience in the management of HCC, and further = clarified=20 the role of surgical resection in dealing with extrahepatic = metastases=20 from HCC. The results show that although the outcome of patients = with=20 extrahepatic metastases remains very poor, surgical resection = could=20 provide survival benefits for patients who had 1 or 2 isolated=20 extrahepatic metastases under a prerequisite that patients has = good=20 performance status and good hepatic functional reserve, as well as = successful treatment of intrahepatic HCC.

Applications

According to results = from the study,=20 the authors have proposed an algorithm for the management of = extrahepatic=20 metastases. Since there is no effective treatment for extrahepatic = metastases in this era, surgical resection might be an applicable = option=20 and provide better outcome for well selected patients. =

Peer = review

The authors reviewed = their experience=20 in dealing with primary HCC with extrahepatic metastasis, and = proposed a=20 treatment strategy suggesting that surgical resection might = provide=20 benefit to patients.

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31 = Seinfeld=20 J, Wagner AS, Kleinschmidt-DeMasters BK. Brain metastases from = hepatocellular carcinoma in US patients. J Neurooncol 2006; = 76: 93-98 PubMed = ; =20 DOI

32 = Choi HJ,=20 Cho BC, Sohn JH, Shin SJ, Kim SH, Kim JH, Yoo NC. Brain metastases = from=20 hepatocellular carcinoma: prognostic factors and outcome: brain = metastasis=20 from HCC. J Neurooncol 2009; = 91: 307-313 =20 PubMed = ; =20 DOI

33 = Chang L,=20 Chen YL, Kao MC. Intracranial metastasis of hepatocellular = carcinoma:=20 review of 45 cases. Surg Neurol 2004; 62:=20 172-177 PubMed = ; =20 DOI

S- Editor = Tian=20 L L- Editor Logan = S E-=20 Editor Ma WH

Reviews Add

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