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Ann Surg. Jul 2005; 242(1): 36–42.
PMCID: PMC1357702

Percutaneous Ethanol Injection Versus Surgical Resection for the Treatment of Small Hepatocellular Carcinoma

A Prospective Study
Guan-Tarn Huang, MD, PhD,* Po-Huang Lee, MD, PhD, Yuk-Ming Tsang, MD, Ming-Yang Lai, MD, PhD,* Pei-Ming Yang, MD, PhD,* Rey-Heng Hu, MD, PhD, Pei-Jer Chen, MD, PhD,* Jia-Horng Kao, MD, PhD,* Jin-Chuan Sheu, MD, PhD,* Cha-Ze Lee, MD, PhD,* and Ding-Shinn Chen, MD*



To compare disease recurrence and survival among patients with small hepatocellular carcinoma after surgical resection or percutaneous ethanol injection therapy, 2 treatments that have not been evaluated with a prospective study.


A total of 76 patients were randomly assigned to 2 groups based on treatment; all had one or 2 tumors with diameter ≤3 cm, with hepatitis without cirrhosis or Child class A or B cirrhosis without evident ascites or bleeding tendency.


Follow-up ranged from 12 to 59 months. Among percutaneous injection patients, 18 had recurrence 1 to 37 months after treatment (true recurrence, 11; original safety margin inadequate, 3; limitation of imaging technology to detect tiny tumors, 4). Three injection therapy patients died of cancer 25, 37, and 57 months after treatment. For the surgical resection group, 15 had recurrence 2 to 54 months after treatment (true recurrence, 12; limitation of imaging, 2; neck metastasis, 1). Five resection patients died of cancer at 11, 20, 23, 26, and 52 months, respectively. By Cox regression model and Kaplan-Meier survival analysis, there is no statistical significance for recurrence and survival between treatment groups. However, tumor size larger than 2 cm and alpha-fetoprotein over 200 ng/mL correlated with higher recurrence rate, and Child class B liver cirrhosis correlated with shorter survival.


Percutaneous ethanol injection therapy appears to be as safe and effective as resection, and both treatments can be considered first-line options for small hepatocellular carcinoma.

Hepatocellular carcinoma (HCC) is prevalent in Southeast Asia and sub-Saharan Africa.1 With the widespread use of alpha fetoprotein (AFP), ultrasound, and other diagnostic modalities as screening tools, many small HCC tumors are detected before symptoms develop and are treated effectively.2,3 Surgical resection is considered the standard treatment of small HCCs, and results have been promising.4 Initially, percutaneous ethanol injection therapy (PEIT) was considered an alternative treatment of patients with small HCC and poor liver reserve for whom resection posed the risk of liver failure. However, several studies have shown similar or even better results with PEIT than with surgical resection.5–7 In Taiwan, HCC is the leading cause of cancer mortality. Many small HCCs are detected by surveillance, and routine surveillance of at-risk groups has been common in daily practice for at least a decade.2,3 Resection and PEIT are both widely used for the treatment of small HCCs,4,8 and the Taiwan National Health Insurance covers both treatments. Because the existing literature does not contain objective comparisons of these 2 treatment modalities9 and a prospective randomized comparative trial has been suggested repeatedly,9–11 we performed a randomized study comparing surgicalresection with PEIT for the treatment of small HCC.


From August 1998 to December 2002, among a total of 1550 patients with HCC ≤3 cm diagnosed at the National Taiwan University Hospital, only 76 fit the inclusion criteria and agreed to participate in this clinical trial. The study was approved by the Human Research Committee of National Taiwan University Hospital (NTUH-47M2). A statistical consultant suggested a design including at least 60 patients for possible analysis of significance based on expected recurrence rate (estimated at 10% every year) and duration of enrollment and follow-up (estimated as a 5-year study with follow-up of at least 1 year). The selection of either resection or PEIT was determined by use of a random table; before enrollment closed, the 2 groups were adjusted to equalize patient numbers. All patients were informed about the study design prior to enrollment by their attending physicians. Informed consents for resection or PEIT were obtained from all patients before treatment. The PEIT patients received further explanation about the current status of treatments for small HCC. The 5 criteria for inclusion in the study were as follows: 1) the presence of one or 2 tumors with diameter ≤3 cm at locations allowing either resection or PEIT to be performed, 2) hepatitis without cirrhosis or Child class A or B liver function in the presence of cirrhosis, 3) platelet count >50,000/mm3 or correctable by platelet transfusion, 4) a prothrombin time prolongation of less than 5 seconds, and 5) absence of evident ascites or frank bleeding tendency. Any patient who would not accept the selected treatment was excluded from the study. Any patient with recurrence after prior therapy was also excluded. All enrolled patients had been followed for at least 1 year at the time of this writing. All patients were diagnosed by typical imaging studies, AFP, and/or tissue analysis.2,12

Before treatment, all patients received a workup as reported previously.2 Computed tomography arterial portography was used to determine the number of tumors when suspicious lesions were present. If computed tomography arterial portography confirmed the presence of 3 or more tumors, the patient was excluded from the study.

Final enrollment was 46 men and 30 women ranging in age from 36 to 81 years. An additional 6 patients were excluded: 3 died of complications unrelated to liver disease after surgery, 1 was lost to follow-up after surgery, and 2 shifted from PEIT to resection (1 due to change of mind just before PEIT, and 1 to severe pain induced by PEIT). The next enrolled patient who fulfilled inclusion criteria was assigned to the group from which a patient had just been excluded.

Surgical resection was performed (lobectomy 10, segmentectomy 6, wedge resection 4, and nonanatomic hepatectomy 18) and patients followed up as previously reported.4 PEIT was performed under ultrasound guidance as reported previously.8 When the necrotic areas produced by this procedure were expected to be satisfactory by ultrasound, results were confirmed by measuring AFP levels and use of computed tomography (CT). Further PEIT was applied if the necrotic area indicated by CT was inadequate to cover the tumor. A complementary study with contrast ultrasound was also used to evaluate PEIT effects. If the AFP level did not decrease satisfactorily, magnetic resonance imaging and/or computed tomography arterial portography were performed to detect possible viable tumors, and additional PEIT was applied if viable tumors were demonstrated. Liver function tests were also serially performed before and after treatment to monitor possible liver injury induced by alcohol or resection.

For statistical analysis, Cox's regression model and the Kaplan-Meier method were used for both recurrence and survival analysis. The software used for analysis was Statview 5.0 (SAS Institute Inc. Cary, NC). The factors included for regression analysis were hepatitis B surface antigen, hepatitis C virus antibody, gender, age, tumor size, tumor number, liver function status, and AFP level. A P value of <0.05 was considered statistically significant.


Of the 76 patients included in the analysis, 38 were treated by PEIT and 38 by surgical resection. A total of 64 patients had single tumors and 12 had 2 tumors. Of the 12 patients with 2 tumors, 8 were treated with PEIT and 4 with resection. Basic patient data are summarized in Table 1. Except for gender ratio, presence of hepatitis viral markers, and number of tumors, no other parameters were statistically different.

Table thumbnail
TABLE 1. Basic Data Describing the 76 Patients With Small Hepatocellular Carcinoma

Of the 38 patients who received PEIT, 18 developed recurrence, including 5 patients with 2 baseline tumors (Fig. 1). By close follow-up, we further analyzed possible causes of recurrence. Of the 18 patients, 11 had single or double recurrent hepatic tumors in different segments from the treated tumor 10 to 37 months after completing treatment; we considered true recurrence (no undetectable tiny tumor before treatment and treated tumors considered to be completely eradicated) to be the cause. An additional 3 patients with recurrence had an inadequate safety margin created by PEIT due to viable tumor around the treated region per ultrasound, CT, or angiography 8 to 12 months later. The tumors of the remaining 4 patients were considered to be small growths below the limits of detection at baseline or located such that it was difficult to detect them with available imaging technology: 1 patient had a recurrent tumor 1 month after treatment, 1 had a tumor near the dome of the liver 7 months after treatment, and 2 had multiple tumors 5 and 9 months afterward, respectively (Table 2). All patients who had recurrent disease received further treatments (6 PEIT again, 8 transcatheter hepatic arterial embolization, 1 each for resection, radiofrequency ablation, and microwave coagulation, and 1 conservative treatment) and follow-up. There were 3 deaths among the 18 patients with recurrent disease, with cancer mortality occurring 25, 37, and 57 months after PEIT. Of the 38 patients treated with PEIT, 3 had some side effects. The blood pressure of 1 patient, who had underlying aortic stenosis, decreased temporarily after PEIT but returned to its original level 1 hour after conservative treatment with oxygen and intravenous normal saline. Also, 2 patients had wound pain, requiring analgesics for pain relief.

figure 6FF1
FIGURE 1. Survival and recurrence after randomization to surgical resection (SR) or percutaneous ethanol injection therapy (PEIT). Gray bars represent tumor-free intervals in months, and black bars indicate the point at which recurrence was detected (in ...
Table thumbnail
TABLE 2. Clinical Analysis of Recurrence in Study Patients

Of the 38 patients treated by surgical resection, 15 developed recurrence, including 1 patient who had 2 tumors before treatment (Fig. 1). Of the 15 patients with recurrent disease, 13 were considered to have true recurrence 9 to 54 months after surgery (including 1 patient with neck metastasis) and 2 were considered to be due to limitations of modern imaging because of very early recurrence only 2 months after resection (Table 2). Of the 15 patients with recurrent HCCs, 4 received resection again, 7 transcatheter hepatic arterial embolization, 1 transcatheter hepatic arterial embolization combined with microwave coagulation, 1 radiofrequency ablation, and 2 conservative treatment only. A total of 5 patients died 11, 20, 23, 26, and 52 months, respectively, after resection due to progressive cancer. There were no significant complications among the patients treated with surgical resection.

Immediately after treatment, follow-up liver function tests showed a decreased serum albumin level in a resection-treated patient with progressive liver cancer. Decreased albumin level was also seen in one PEIT-treated patient who had persistent hepatitis C activity. Another PEIT-treated patient had progressive HCC and showed decreased albumin and increased bilirubin levels. Long-term monitoring of liver function showed that the remaining 73 patients each had stable liver function before the development of advanced cancer. Table 3 shows the relations of hepatitis B surface antigen, hepatitis C virus antibody status, and tumor recurrence. The liver status at baseline of the 33 patients with eventual recurrent disease was hepatitis without cirrhosis in 4 and cirrhosis in 29.

Table thumbnail
TABLE 3. Relations Between Viral Markers (HBsAg, Anti-HCV) and Tumor Recurrence

By Kaplan-Meier analysis, the 1- to 5-year survival rates were 100%, 100%, 96.7%, 92.1%, and 46% for the PEIT group and 97.4%, 91.3%, 88.1%, 88.1%, and 81.8% for the resection group, respectively. The 1- to 5-year tumor-free survival rates were 76.1%, 64.5%, 49.1%, 44.6%, and 44.6% for the PEIT group and 89.5%, 71.3%, 60.9%, 56.2%, and 48.2% for the resection group, respectively. The differences between treatment groups for recurrence rate and survival were not statistically significant.

The Cox regression model showed that tumor size larger than 2 cm (P = 0.0252) and elevated AFP level over 200 ng/mL (P = 0.0425) correlated with higher recurrence, and poor liver status (Child class B) correlated with shorter survival (P = 0.0134). The remaining factors that were analyzed did not significantly influence outcome.


Although both PEIT and surgical resection are generally accepted as treatment of small HCC, a randomized study comparing these treatments had not previously been done.9 PEIT is a popular treatment, and good results have been reported both in the East and West.5,6 In contrast, there are also studies that have found patients treated with surgical resection have significantly better long-term prognosis or tumor-free survival than those treated with PEIT.10,13 On balance, the opinion prior to the current study was that resection was the treatment of choice, even for small, early HCCs.13 However, this conclusion was often criticized because it was not based on a direct comparison. To resolve this debate, a prospective, randomized study like the present one was indeed needed. A possible limitation of our study is that both doctors and patients understood the protocol prior to patient enrollment, and patient willingness to enter randomized enrollment can interfere with the accuracy of results. However, the prospective design minimized possible bias.

Our prospective study showed that PEIT and surgical resection had nearly the same effectiveness for the treatment of small HCCs after an average follow-up of 37.7 months. For solitary HCCs less than 4 cm, a cohort study has demonstrated that patients treated with resection and PEIT have a similar prognosis.14 A matched case-control study for HCC patients with a single nodule less than 5 cm also indicated that patients treated with hepatic resection or PEIT have similar survival rates.11 In a comparative study for HCCs smaller than 3 cm and 3 or fewer in number, resection had better tumor-free survival than PEIT, but PEIT still achieved a 5-year survival rate of around 60%.10 Our data indicate that PEIT-treated patients had a slightly higher tumor recurrence rate than resection-treated patients. However, considering possible complications from surgery, PEIT may have a very important advantage in the treatment of small HCCs less than 3 cm, especially when a patient has some contraindications for surgery.

Incomplete tumor necrosis after PEIT is a very important problem.15 We also encountered this problem in our series despite active management and detailed follow-up with CT and ultrasound. To prevent incompleteness of necrosis after PEIT, injection not only into the center of the lesion, but also into sites close to the edges has been suggested.8,15 Even with wider coverage, we still had 3 patients with incomplete tumor necrosis after PEIT. We speculate that a broader safety margin may be needed, and this adaptation has worked smoothly to date. Difficulty in identifying what constitutes adequate tumor necrosis is a current shortcoming of PEIT. Many methods such as enhanced CT or dynamic magnetic resonance imaging have been claimed to be effective for detection.16 However, sometimes even multiple biopsies from the treated HCC tumor cannot document complete eradication of tumor cells.8 Contrast ultrasound has also been considered helpful.17 Nevertheless, close follow-up using imaging and AFP levels to detect possible viable tumor is still very important despite the satisfied safety margin.

Of the 12 patients with 2 tumors each, including 8 receiving PEIT and 4 receiving surgical resection, each group (5 patients and 1 patient, respectively) had patients with recurrent disease; this included 2 PEIT-treated patients with recurrence due to imaging limitations. Although our period of follow-up might not be long enough to draw definite conclusions, these results suggest that whether tumors are single or double might not be crucially important for prognosis. Regardless of specifics (single or double tumor), these patients can be treated aggressively by either resection or PEIT.

In our series, the PEIT group had more female patients and more patients with double tumors. Viral marker distribution showed more hepatitis B virus-infected patients in the resection group and more hepatitis C-infected patients in the PEIT group. Because of the limited number of patients and relatively short follow-up duration, we could not draw any conclusions about the importance of such patient characteristics. Nevertheless, PEIT proved to be promising because some PEIT patients had relatively poor tumor status (higher tumor number) and relatively poor liver reserve before treatment. In short, the significance of gender difference and viral marker differences clearly needs further study.

The Cox regression model did show positive results in our studies. AFP level is usually considered an important factor influencing survival.18 With our data, it was confirmed again. Tumor size might be important for recurrence, but tumor size might not correlate with the survival;10 our analysis also showed that tumor size was related to recurrence but did not influence survival. Poor liver reserve is an important factor contributing to lower survival,10 and we have shown the same tendency in our study. However, all deaths in our series were due to progressive cancer. The limited patient number might induce the bias; therefore, the link between liver reserve and survival needs further observation to clarify the phenomenon.

Needle tract implantation of HCC after PEIT has been documented.19 Although implantation after biopsy was observed in 2% of patients in our previous study,12 we have not encountered any implantation of HCC after PEIT in the present study. Because our follow-up duration was long enough for new tumor growth to be detected, we are confident in concluding that PEIT has a lower incidence of needle tract implantation than that of cutting biopsy.

Recent advanced ultrasound-guided invasive approaches, including microwave coagulation20 and radiofrequency ablation,21,22 have shown very promising results in the treatment of small HCC. These techniques may be better because the even distribution of heat leads to a more adequate necrosis of tumor. However, these techniques still have some shortcomings such as causing more injuries and greater difficulties for treating tumors situated near vessels or the liver surface.20,23 Tumor necrosis achieved by radiofrequency has been reported to be better, and this method has the advantage that fewer sessions are needed to achieve total tumor necrosis.22 However, a higher complication rate has also been reported.24 At locations difficult to approach and unsafe for radiofrequency, PEIT may still be the treatment of choice.25 Thus, PEIT cannot be completely replaced by these newly available techniques. PEIT still has some role in the treatment of small HCCs because of its convenience, safety, and low costs.23

Liver transplantation has been reported as the best treatment of small HCC;26 however, in those with Child's A cirrhosis, resection has yielded a similar outcome27 and shortage of donors is an issue difficult to overcome. Therefore, treatments that remove or ablate tumor still have important and practical roles.

Besides treatment, the nature of tumors might also be an important factor determining prognosis after treatment. Size and number of tumors do not seem to be the only such factors.28,29 With the most sensitive imaging modalities available, detection of all tumors and determination of prognosis is not foolproof. Therefore, further development of more refined diagnostic techniques would be very valuable.

Resection has remained one of the best treatments for patients with small HCC, especially those with noninvasive tumors and well-compensated liver function.27,30 However, results of many studies also suggest that PEIT also leads to a promising outcome.10,31 With further consideration about the recurrence, mortality, and morbidity, PEIT seems more suitable for small HCCs,32 particularly when patients have some contraindications for surgery. Our prospective randomized study shows that patients receiving resection or PEIT had nearly the same outcome, although the number of patients and follow-up duration are perhaps still inadequate. Ongoing follow-up for these patients will definitely yield further useful data, especially on long-term outcome. With the present results, we conclude that both PEIT and resection are effective treatments for small HCC. Besides resection, PEIT can also be considered a treatment of choice for small HCCs, especially in patients with poor liver reserve or comorbidity that make them potentially poor surgical candidates. Despite the wide use and convincing results of radiofrequency ablation, PEIT has the advantage of being cheap, convenient, and safe. With these advantages, PEIT will still remain a practical modality for treatment of small HCC, especially in developing countries.


Supported in part by a grant from the Department of Health (DOH90-HP-1010), Executive Yuan, Taiwan.

Reprints: Ding-Shinn Chen, MD, Department of Internal Medicine, National Taiwan University Hospital No. 7, Chung-Shan South Road, Taipei, Taiwan. E-mail: wt.ude.utn.cm.ah@nehcsd.


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