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(Radiology. 2000;214:769-774.)
© RSNA, 2000

Vascular and Interventional Radiology

Small Hepatocellular Carcinoma: Safety and Efficacy of Single High-Dose Percutaneous Acetic Acid Injection for Treatment1

Huei-Lung Liang, MD, Chien-Fang Yang, MD, Huay-Ban Pan, MD, Kwok-Hung Lai, MD, Jin-Shiung Cheng, MD, Gin-Ho Lo, MD, Clement K. H. Chen, MD and Ping-Hong Lai, MD

1 From the Departments of Radiology (H.L.L., C.F.Y., H.B.P., C.K.H.C., P.H.L.), and Medicine (K.H.L., J.S.C., G.H.L.), Kaohsiung Veterans General Hospital, 386 Ta-Chung 1st Rd, Kaohsiung, Taiwan 813, and the Departments of Radiology (H.L.L., C.F.Y., H.B.P., C.K.H.C., P.H.L.) and Medicine (K.H.L., J.S.C., G.H.L.), National Yang-Ming University, Taipei, Taiwan. Received March 22, 1999; revision requested May 10; revision received June 21; accepted July 20. Address reprint requests to C.F.Y. (e-mail: cfyang@isca.vghks.gov.tw).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the safety and efficacy of single high-dose percutaneous acetic acid injection (PAI) for treatment of small (<3-cm-diameter) hepatocellular carcinoma (HCC).

MATERIALS AND METHODS: Eighteen patients with HCC (22 nodules; diameter range, 1.5–3.0 cm) underwent single PAI. With ultrasonographic or computed tomographic (CT) guidance, 4–11 mL of 50% acetic acid was slowly injected into the center of the nodule through a skinny multiple-side-hole needle. Follow-up was performed with helical contrast material–enhanced CT. Complications of high-dose PAI were recorded.

RESULTS: Seventeen nodules showed no local recurrence (follow-up, 6–29 months) after single PAI. At a mean follow-up of 15.6 months, mean tumor diameter was 2.1 cm and mean injected volume was 6.4 mL. Four nodules showed residual tumor (mean tumor diameter, 2.6 cm; mean injected volume, 5.8 mL). The mean ratio of injected to estimated volume of acetic acid was 1.21 in cases of successful single PAI and 0.72 in cases of local recurrence (P < .001). One patient with preexistent right portal venous thrombosis died of hepatic failure 37 days after PAI. Other complications included severe pain (11%), high fever (4%), and segmental wedge infarction (4%).

CONCLUSION: Single high-dose PAI is safe and effective for treatment of small HCC.

Index terms: Acetic acid, 761.1264, 761.1269 • Alcohol ablation, 761.1264, 761.1269 • Liver, interventional procedures, 761.1264, 761.1269 • Liver neoplasms, 761.323 • Liver neoplasms, CT, 761.12113, 761.12115 • Liver neoplasms, US, 761.12981, 761.12986


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Percutaneous ethanol injection (PEI) therapy has become a widely applied modality for treatment of hepatocellular carcinoma (HCC) (1–3). The effect of PEI therapy is almost comparable with that of surgical resection (2–5); however, a large number of treatment sessions are necessary, and recurrence after treatment is common, with reported rates of 83%–96% (2,3). When the number of punctures is increased, the risk of complications such as creation of arterioportal shunts, bile duct injury (6), and needle-track seeding (7–9) may also increase.

Ohnishi et al (10) reported that acetic acid has a stronger cytotoxic effect than does ethanol in the treatment of small HCC. In a randomized study, Ohnishi et al (11) concluded that percutaneous acetic acid injection (PAI) is superior to PEI in terms of both local recurrence rate (8% vs 37%) and 2-year survival rate (92% vs 63%). In their clinical practice, however, they injected a small volume (1–3 mL) of 50% acetic acid at each session, with a total of 2.0-3.5 sessions for treatment of small HCC lesions (11,12). The aim of the present study was to evaluate the safety and efficacy of single PAI therapy by injecting a higher dose (4.0–10.5 mL per session) of 50% acetic acid to treat small (<3-cm-diameter) HCC.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Since June 1995, 18 patients with a total of 22 small HCC nodules had undergone single PAI therapy at Kaohsiung Veterans General Hospital (Taiwan). There were 15 men and three women aged 43–80 years (mean, 66 years). The cause of liver cirrhosis was hepatitis B infection in 10 patients and hepatitis C infection in eight. The liver function grade was Child class A in 11 patients, class B in six, and class C in one. Three patients did not undergo any previous treatment for HCC, and 15 had newly redeveloped HCC after surgical resection (n = 5) or transcatheter arterial embolization (n = 10). Thirteen patients were considered not to be candidates for transcatheter arterial embolization because of the presence of (a) occlusion of the hepatic artery secondary to previous transcatheter arterial embolization (n = 6), (b) small tumor vessels (n = 2), (c) faint tumoral opacification on selective hepatic angiograms (n = 3), (d) poor liver function (n = 1), and (e) technical failure of superselective embolization (n = 1).

Histopathologic proof of HCC was available at the time of initial diagnosis in 17 patients. The newly redeveloped HCC was diagnosed on the basis of hypervascular characteristics on dynamic helical computed tomographic (CT) or magnetic resonance (MR) images and/or elevated level of serum {alpha}-fetoprotein. Tumor size was assessed with ultrasonographic (US) images, CT images, or both. Nine HCC nodules were smaller than 2 cm in diameter, and 13 were 2.1–3.0 cm in diameter. PAI usually was performed with US guidance, although CT guidance was used in one patient with lesions that were difficult to localize on US images and in two patients with superficial lesions.

The procedure for PAI was as follows: The patient was instructed to fast for 6–8 hours, and a coagulation profile was checked. Meperidine hydrochloride (40 mg) was injected intramuscularly 30 minutes before PAI. After local anesthesia (1% lidocaine) was applied at the site of puncture, a 20-cm-long, skinny (21–22-gauge), multiple-side-hole needle (Cliny, Yokohama, Japan) was inserted percutaneously into the center of the tumor with the aid of real-time US (Tosbee; Toshiba, Tokyo, Japan ) or CT (Somatom Plus; Siemens Medical Systems, Erlangen, Germany) guidance.

For nodules smaller than 2 cm in diameter, needles with six side holes (7–10-mm span) were used; for nodules 2–3 cm in diameter, needles with 14 side holes (15–20-mm span) were used. Because there is no end hole in the needle, the needle tip is placed close to a portion of the lesion that is opposite the needle-entry site. In most cases, two or three passes were needed to ensure that the needle was positioned in the center of the tumor. Adjustment of position was performed only in normal hepatic parenchyma, before the needle was inserted in the tumor. After insertion, the needle was connected by means of an extension tube to a 1- or 3-mL syringe filled with 50% acetic acid. Acetic acid (4–11 mL) was injected slowly into small (<=3-cm-diameter) HCC lesions at each session. Because of the spiral distribution of the side holes along the needle, there was no need to withdraw or rotate the needle during injection.

The capability of 50% acetic acid to cause hepatocyte necrosis is assumed to be about three times that of absolute alcohol (10). The initially estimated volume of acetic acid for injection in our study was calculated with V = [4/3 · {pi}(R + 0.5)3] · 1/3, where V is the volume of acetic acid, and R is the radius of the lesion in centimeters. Because the optimal single-injection dose of 50% acetic acid was uncertain, an additional 1–2 mL of acetic acid was injected if the patient did not report discomfort after injection of the estimated volume. Injection was discontinued, however, if the patient reported severe pain or if intravasation of acetic acid into the portal vein was seen at US monitoring, even if the volume of the injection was less than that initially calculated.

After injection of acetic acid, the needle was left in place for 2–3 minutes and then slowly withdrawn to reduce acetic acid reflux along the needle track (13). US images of lesions before and after PAI are shown in Figure 1.



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  		Figure 1. Intercostal US images demonstrate changes in a small HCC lesion after PAI. Left: Image obtained before PAI shows a hypoechoic HCC nodule (cursors) in the right lobe of the liver. Right: Image obtained after PAI shows that the nodule (arrow) has become highly hyperechoic.

 
Patients were followed up 2 months later with dynamic helical CT with contrast agent enhancement (Telebrix 35; Laboratoire Guerbet, Roissy, France). Tumor necrosis was considered to be complete when CT scans showed no areas of contrast enhancement within the lesion during the hepatic arterial phase and the lesion volume remained unchanged or was decreased. If viable tumor (local recurrence) was found in the treated area, another PAI was performed. Afterward, US and CT were performed every 2–3 months to evaluate changes in the treated lesion and to detect new nodules. New lesions were treated either with additional PAI or with transcatheter arterial embolization. The side effects of PAI were assessed by means of changes in symptoms and signs, as well as with biochemical and liver function (Child class) assays.

Written informed consent was obtained from each patient and from family member(s). This study was approved by the hospital research committee.

We calculated the ratio of the single-injection volume of 50% acetic acid to the estimated volume calculated with the equation reported earlier in this article. Comparison of this ratio between the group of patients in whom the single injection was successful and the group who had local recurrence was performed by means of a Mann-Whitney U test. A P value of less than .05 was considered to indicate a statistically significant difference between groups.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Efficacy
The effect of PAI therapy in 21 of 22 nodules could be evaluated on series of follow-up dynamic helical CT images. One patient died 37 days after the procedure (discussed subsequently). Seventeen of these 21 nodules (including two nodules treated with CT guidance) showed no residual tumor after single PAI therapy (Fig 2). The mean tumor diameter was 2.1 cm (range, 1.5–3.0 cm), and the mean injected volume of acetic acid was 6.4 mL (range, 4–11 mL). The mean follow-up was 15.6 months (range, 6–29 months).



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  		Figure 2. Left: Transverse T1-weighted dynamic gadolinium-enhanced gradient-echo MR image (repetition time, 120 msec; echo time, 2.3 msec) shows a 3-cm enhancing recurrent HCC lesion (arrow) in hepatic segment VII. Right: Follow-up transverse CT image obtained 12 months after single PAI shows complete cystic change (arrow).

 
Three patients (four nodules) had residual tumor on CT images obtained 2 months after single PAI. In these four patients, the mean tumor diameter was 2.6 cm (range, 2.5–2.7 cm), and the mean injected volume was 5.8 mL (range, 5–6 mL). In the four nodules (three patients) that showed signs of residual tumor, PAI was prematurely terminated due either to severe pain in three patients or to overt intravasation of acetic acid in one. In these patients, three nodules in two patients showed complete necrosis after a second PAI procedure (Fig 3). The mean ratio of injected volume to estimated volume in the group that underwent successful single PAI was 1.21 (range, 0.94–1.61), and the mean ratio in the group with local recurrence was 0.72 (range, 0.67–0.80) (P < .001). The clinical characteristics of the 18 patients are listed in the Table.



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  		Figure 3. Selective hepatic angiogram (top left) and CT image (top right) reveal a 2.5-cm nodule (arrow) in hepatic segment VI with blood supply from small feeding arteries. This nodule was considered to be unsuitable for transcatheter arterial embolization. A second PAI was performed owing to local recurrence after initial PAI. Middle right: Transverse CT image obtained 12 months after second PAI shows cystic change with a small, high-attenuating, nonenhancing area (arrowhead), which was considered to be an area of fibrosis. Transverse CT image (bottom right) and hepatic angiogram (bottom left) obtained 29 months after second PAI show no local recurrence, although mild liver atrophy (arrowhead, bottom right) is present.

 

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  		Clinical Characteristics in 18 Patients with 22 Small HCC Nodules
 
Complications
Most patients complained of tolerable, transient pain and had a mild to moderate elevation in body temperature (>37°C to 39°C), which returned to normal within 3–5 days. Other complications included (a) severe pain that caused premature termination of injection and required administration of additional analgesics in three (12%) of 25 procedures; (b) high fever (>39°C) in one (4%) procedure; (c) segmental wedge infarction of the right lobe of the liver in one (4%) procedure in a patient with occlusion of the right hepatic artery before PAI due to previous transcatheter arterial embolization; the patient died of variceal bleeding 15 months later; and (d) liver failure in one (4%) procedure in a patient who had undergone CT-guided PAI for a small (1.9-cm) recurrent HCC in hepatic segment IV. This patient had poor reserved liver function (54% at indocyanine green test) and right portal venous thrombosis seen on the CT image obtained before PAI. He developed hepatic failure and died 37 days after PAI.

Follow-up
There were no significant changes in the biochemical data, including levels of albumin, aspartate aminotransferase, alanine aminotransferase, and total bilirubin, or Child liver function class during a follow-up of at least 2 months, except in the patient with liver failure. One patient was lost to follow-up after 10 months. A newly redeveloped HCC nodule located in a different segment was present in six patients within 6 months and in another seven patients within 12 months after PAI. Eight patients died 1–22 months (mean, 12 months) after PAI: The cause of death was HCC in one (12%) patient, hepatic failure in three (38%), variceal bleeding in two (25%), acute myocardial infarction in one (12%), and respiratory failure in one (12%).


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
HCC is one of the most common malignant neoplasms worldwide. Surgery remains the first choice for treatment of HCC, and the authors of recent reports (4) have shown the encouraging result that the 5-year survival rate after surgical resection of small, asymptomatic HCC nodules is 50%. However, surgical resection is possible only in the small proportion of patients with well-preserved liver function.

Transcatheter arterial embolization with iodized oil with or without an additional chemotherapeutic agent is an effective alternative treatment for hypervascular HCC nodules (14–16). For small (<4-cm) hypervascular HCC nodules treated with subsegmental transcatheter arterial embolization, the 4-year survival rate in patients with Child class A or B liver function was 67% (15). Transcatheter arterial embolization does not, however, kill cancer cells that infiltrate into or outside of the capsule (16). Transcatheter arterial embolization also has a limited effect in the treatment of hypovascular HCC nodules, which are often encountered in cases of small, early HCC (12).

PEI is indicated for treatment of both hypervascular and hypovascular small HCC when there are no more than three lesions. The 4-year survival rate after PEI can be as high as 70% (17). The results of these percutaneous treatments are better than those of surgery. The disadvantages of PEI are (a) the requirement of a large number of treatment sessions, which might increase complication rates, medical costs, and patient discomfort, and (b) a higher local recurrence rate, reportedly up to 37% (11), which may be attributed to uneven diffusion of ethanol throughout tumors, especially in septated HCC, leaving some areas unharmed (1,18). Because of the disadvantages of traditional PEI (small injected volume [2–10 mL per session] and multiple treatment sessions), Redvanly et al (19) proposed that hepatic malignancies be treated with high-dose (up to 40 mL per session) PEI. Single PEI with general anesthesia has been performed at some medical institutions with an injected ethanol volume of as much as 210 mL (20,21).

Ohnishi et al (10) reported that acetic acid has a strong ability to penetrate cells and can dissolve lipids and extract collagen. The hepatocyte necrosis capability of acetic acid is equal to that of absolute alcohol at an acetic acid concentration of 15%, and the killing effect reaches a plateau at 50% concentration. In another study, Ohnishi et al (12) injected 1.4 mL of 50% acetic acid per session for HCC nodules 1–2 cm in diameter and 2.4 mL for nodules 2–3 cm in diameter. They (11) stated that a small HCC nodule cannot be successfully treated at one treatment session because it takes several hours or a day for acetic acid to solubilize collagen. In the present study, all 1–2-cm nodules and 11 of 15 2–3-cm nodules were treated successfully with single PAI. This may be because we used multiple-side-hole needles, which allowed a more even distribution of acetic acid to cover the whole nodule during one injection.

Four (18%) of the 22 nodules in our study showed evidence of residual tumor after single PAI. This rate was higher than the 8% rate reported by Ohnishi et al (11). In all four cases, PAI was prematurely terminated, which resulted in a low (<=0.8) ratio of injected volume to estimated volume. In patients who cannot tolerate or are not suitable candidates for high-dose PAI, conventional PAI with a small volume and multiple injection sessions is still our recommendation.

Hypervascular tumors located on the surface of the liver were once thought to be a contraindication for direct puncture, because of the possibility of complications (22,23). Transient pain after injection into a surface lesion was much more intense than that after treatment for lesions inside the liver. The discomfort usually precludes the use of single high-dose injection for superficial hepatic foci. To complete single PAI of a superficial lesion, CT guidance by way of an oblique route (11) can be used in some patients so that the needle may traverse a longer distance inside the liver (Fig 4).



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  		Figure 4. Left: Transverse CT image reveals a superficial 2-cm recurrent HCC lesion (arrow) in the lateral margin of the lateral segment, near a surgical clip (arrowhead). Right: Follow-up transverse CT image obtained 19 months after CT-guided single PAI shows complete regression of the nodule. Arrowhead = surgical clip.

 
CT-guided PAI or PEI is also useful for treatment of subdiaphragmatic nodules and of lesions not clearly discerned on a US scan (13). The drawbacks of CT guidance are that it is relatively more time-consuming than US guidance, especially for small nodules, and it does not allow real-time monitoring of acetic acid diffusion. Acetic acid or ethanol should be injected carefully to avoid passage into vessels adjacent to the lesion. If acetic acid or ethanol is seen to escape into blood vessels or bile ducts, the injection must be stopped immediately (24,25). With CT guidance, however, we could not stop the injection immediately when acetic acid escaped into vessels or ducts. This may have been the cause of liver failure in one patient after CT-guided single PAI.

Most of the severe complications of PEI reported in the literature (24–26) occurred when low doses of ethanol were used. The dose-dependent adverse effect of high-dose PEI was pain (19,27). Likewise, in our study, three patients complained of severe pain, which resulted in premature termination of single PAI. Conscious sedation may be of benefit for pain control during injection.

Yoshikawa et al (28) reported the CT appearance of parenchymal changes after PEI. Segmental and lobar atrophy were found in 17% and 3% of cases, respectively. The risk of liver atrophy may be higher in patients who already have hepatic arterial occlusion due to any cause, as was seen in one patient in our study. Single PAI should be performed more cautiously in these patients.

Needle-track implantation after percutaneous fine-needle biopsy is considered to be rare. The incidence was reported (9) to be about one in 15,000, but this may be an underestimate. Ishii et al (7) reported four cases of needle-track implantation after PEI, for a 2.2% frequency of contrast-enhanced HCC nodules larger than 2 cm. They concluded that needle-track implantation is not unusual. The cause of needle track implantation was attributed to multiple needle punctures of the lesions. A reduced number of injection sessions, especially when the single-injection method is used, might decrease the risk of needle track implantation.

In conclusion, our results suggest that small HCC nodules can be safely and successfully treated with single high-dose PAI in most patients, but careful selection of patients still is warranted. In patients who already have a compromised vessel (either hepatic arterial occlusion or portal venous thrombosis), conventional PAI with a small injected volume is recommended.


   Footnotes
 
Abbreviations: HCC = hepatocellular carcinoma PAI = percutaneous acetic acid injection PEI = percutaneous ethanol injection

Author contributions: Guarantor of integrity of entire study, C.F.Y.; study concepts and design, H.L.L.; definition of intellectual content, H.L.L.; literature research, H.L.L., H.B.P., J.S.C.; clinical studies, C.F.Y., G.H.L., K.H.L.; data acquisition, H.L.L., C.K.H.C.; data analysis, H.L.L., P.H.L.; manuscript preparation, H.L.L.; manuscript editing, C.F.Y., H.L.L.; manuscript review, C.F.Y., H.L.L., H.B.P., K.H.L.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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