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Published online before print January 14, 2008, 10.1148/radiol.2463070390
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(Radiology 2008;246:947-955.)
© RSNA, 2008

Vascular and Interventional Radiology

Complications of Laser Ablation for Hepatocellular Carcinoma: A Multicenter Study1

Vincenzo Arienti, MD, Stefano Pretolani, MD, Claudio Maurizio Pacella, MD, Fabrizio Magnolfi, MD, Bruno Caspani, MD, Giampiero Francica, MD, Angelo Salomone Megna, MD, Renato Regine, MD, Massimo Sponza, MD, Ettore Antico, MD, and Francesca Marta Lilja Di Lascio, PhD

1 From the Department of Internal Medicine, Maggiore Hospital, Largo B. Nigrisoli 2, 40133 Bologna, Italy. From the 2005 RSNA Annual Meeting. Received February 28, 2007; revision requested May 9; revision received June 4; accepted June 27; final version accepted September 6. Supported in part by Gruppo Italiano Ultrasonografia in Medicina Interna for liver tumor database design and Image Aided Laser Therapy for costs of extraction of data from the database and part of statistical evaluation. Address correspondence to V.A. (e-mail: vincenzo.arienti{at}unibo.it).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Purpose: To retrospectively and prospectively determine the rate and type of complications and their association with clinical or technical factors after percutaneous laser ablation (LA) for hepatocellular carcinoma (HCC).

Materials and Methods: The institutional research board of each center approved the study and all patients provided informed consent. By using an Internet liver tumor database of nine Italian centers, 520 patients were included with HCC nodules of any size (small, 0–3 cm; intermediate, >3–5 cm; large, >5 cm). Postprocedural complications were related to clinical or percutaneous LA factors by using the Student t and {chi}2 tests. Follow-up was carried out with computed tomography (CT) at 1, 3, 6, 9, and 12 months, and primary effectiveness rate was defined as the percentage of HCCs completely ablated after percutaneous LA.

Results: A total of 353 men and 147 women (age range, 24–86 years; Child-Pugh score A = 63.4%, B = 30.8%, C = 5.9%) with 647 nodules (mean diameter, 3.2 cm ± 1.7) were treated by 1004 percutaneous LA sessions. There were four (0.8%) deaths in 520 patients; 15 (1.5%) of 1004 sessions presented major complications without any seeding. Major complications were associated with excess energy (10 520 J ± 7073 vs 7474 J ± 3803; P = .001) and high-risk location (P = .05). Sixty-two (6.2%) sessions resulted in minor complications associated with excess energy (P = .001), high bilirubin level (1.74 mg/dL ± 1.10), and low prothrombin time (P = .01). Primary effectiveness rates were 60% in all HCCs and 81% in HCCs smaller than 3 cm.

Conclusion: Percutaneous LA may be considered a safe treatment for small HCCs.

© RSNA, 2008


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Percutaneous ethanol injection (PEI) and radiofrequency (RF) are the recommended ablation treatments for small hepatocellular carcinoma (HCC) (1), given that the smaller the lesion ablated, the better the survival (2). Since laser photocoagulation for tumor destruction was introduced (3), an Nd:YAG laser has been successfully employed to treat a wide range of liver malignancies by using two procedures: laser-induced thermotherapy, which uses a single cannulation needle (7F or 9F, if internally cooled) (4), and laser ablation (LA), where laser light is delivered to the tumor with multiple bare-tip 300-nm fibers inserted into spinal needles (21 gauge) (5). Regarding the total number of patients treated, effectiveness, and outcome, LA may now be considered a competing procedure with PEI and RF for the single- (4) and multiple-needle (6) techniques.

To date, LA has been proved safe and effective for HCC treatment in small single-center series (7). However, to our knowledge, there are no clinical studies regarding curative treatment for HCC on the basis of standardized reporting criteria (8) or on minimal registration data sets (9) collected from liver tumor databases (10). Thus, the purpose of our study was to retrospectively and prospectively determine the rate and type of complications and their association with clinical or technical factors after LA for HCC.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Liver Tumor Ablation Database
In December 2003, we created an Internet database to enter patients with primary and secondary liver tumors treated with percutaneous ablation techniques. Image Aided Laser Therapy, Florence, Italy, is the company that contributed to the costs of data extraction from the database and part of the statistical evaluation. The authors had control of the data and information submitted for publication. The database was developed by a multidisciplinary board of epidemiologists, hepatologists, interventional radiologists, and pathologists and was proposed to nine Italian centers. All of these centers had considerable experience (range, 11–21 years) in percutaneous ablation of liver tumors and in 1996 adopted the LA procedure introduced by Pacella et al (5).

The liver tumor Internet database was designed (V.A.) to offer a central repository of records with a high level of safety for data (individual passwords for each center and each operator, C.D.) and to ensure simple, easy, and controlled data entry at any time and place. It is noteworthy that most of the characteristics of the database were similar to those included in the minimal registration data set for clinical trials (9). Each record of the database has more than 90 items to complete, including demographic and clinical characteristics, associated diseases or risk factors, liver and kidney function test values, viral hepatitis and oncologic biomarkers, and histologic, topographic and morphologic features of liver nodules assessed by using ultrasonography (US) and computed tomography (CT).

Concerning ablation techniques, the items recorded were type of ablation (PEI, LA, RF), number of sessions, number and type of needles used, amount of energy delivered or ethanol injected, procedural time, type and time of ablation-related complications (with a predefined set of complications and a free text field for any complications [major, minor, or side effect] not included in the tables), technical success and technique effectiveness, tumor recurrence, other tumor therapies, follow-up, and death.

The level of experience in performing ablation techniques for any single center was categorized according to the total number of ablations performed: A = 500 or more, B = 150–499, C = 75–149, and D = 0–74. In February 2004, the database was available to all centers that had decided to take part in the HCC-LA study. From February 2004 to February 2005, the centers entered their data in the database including: (a) all patients treated from January 1996 to January 2004, who would thus constitute the retrospective part of the study, and (b) all new patients treated from February 2004 to February 2005, who would make up the prospective part of the study. The Ethics Committees of all participating centers approved the database and its use, as well as the retrospective portion of our study, provided we obtained informed consent from the formerly treated patients. Approval was also given for the prospective portion of our study by the Ethics Committees of all centers and informed consent was obtained.

HCC-LA Study
HCC nodules.—We performed a retrospective and prospective study on complications of LA in patients with HCC selected from the above cited liver tumor database. Inclusion criteria were as follows: (a) diagnosis of HCC by using standard histology or dynamic CT and {alpha}-fetoprotein according to the European Association for the Study of the Liver criteria (11); (b) tumor nodules of any size and not more than three in number, with no indication for surgery (12); and (c) at least one HCC nodule treated by using LA (not more than three sessions). Exclusion criteria were severe coagulation deficit (<43% for prothrombin time and/or a platelet count <38 x 109/L) and severe hepatic dysfunction (Child-Pugh grades >12 [C]) and/or severe ascites (grade 2, assessed after Child-Pugh classification).

HCCs nodules that were not imaged and characterized with at least biphasic CT were also excluded. In each center, all patients had been previously assigned to undergo LA by an interdisciplinary tumor board (surgeon, radiologist, hepatologist). Informed consent was obtained from all patients in the retrospective part of our study (see above), while for the patients in the prospective group informed consent for use of their data for research was obtained at the same time as consent to treat.

We included 520 patients in our study: 448 in the retrospective group and 72 in the prospective group. In each center, laboratory data were reviewed and clinical and US evaluations were performed by the author responsible for the center. When available, information on esophageal varices and portal hypertensive gastropathy was obtained with the local endoscopy unit which performed the upper gastrointestinal examinations.

HCC nodules were characterized by using US and CT as follows: diameter (in centimeters); site, defined as superficial (<5 cm) or deep (≥5 cm), according to the distance measured at imaging from the liver capsule of the patient to the center of the HCC nodule; localization, defined as subcapsular (<2 cm from the glissonian capsule, either diaphragmatic or not), paravascular or parabiliary (≤1 cm from the portal vein, inferior vena cava, hepatic hilum/main bile ducts, and/or gallbladder) or isolated. Nodules were classified, depending on their size, as small (≤3 cm), intermediate (>3 and ≤5 cm), or large (>5 cm).

LA procedure and complications.—LA was performed in all centers under local anesthesia with conscious sedation in hospitalized patients, following the method published by Pacella et al (5). This procedure was adopted in all centers since preliminary studies have shown that with the energy level used (7200 J, delivered by four laser fibers passed through four 21-gauge spinal needles in a single session of 6 minutes) it is possible to achieve a mean necrosis diameter of 3.1 cm with a mean necrosis volume of 15 mL in the treated HCC nodule (7). The following data were recorded for each session: (a) the number of fibers used and (b) total energy delivered into the HCC nodule during a single session. LA monitoring (8) was assessed by US, and postprocedural follow-up after LA was assessed by US, CT, and clinical examination at 30 days and then every 3 months. The end point of the ablation process was defined by achieving complete necrosis (defined as absence of any enhancement in the treated HCC nodule at dynamic CT) after not more than three LA sessions (Fig 1). The type and number of complications during the follow-up were recorded and classified as major or minor complications and side effects, according to Goldberg et al (8).


Figure 1
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  		Figure 1: Transverse dynamic contrast-enhanced CT scan of right liver lobe 1 month after LA shows large hypoattenuated area (arrow) without enhancement in arterial phase, corresponding to complete necrosis of treated HCC nodule.

 
Effectiveness of LA.—Technique effectiveness was established by using dynamic CT scans 30–45 days after any session, according to the necrosis induced in the treated nodule, defined as complete or incomplete. All the evaluations of the CT scans were performed in each center by an independent radiologist with considerable experience (range, 6–20 years) in liver tumor imaging. LA primary effectiveness rate was calculated and related to the size of HCC nodules according to Goldberg et al (8).

Statistical Analysis
All statistical analyses were performed with commercially available software (Microsoft Excel, 2003, Microsoft, Seattle, Wash; STPLAN, 4.1, University of Texas, Houston, Tex; SPSS for Windows, version 14.0, SPSS, Chicago, Ill). Categoric variables were presented as percentages and continuous variables were presented as means ± standard deviations.

The post hoc power analysis was performed by having, as primary end point, the difference between the presence and absence of complication rates. By using a Fisher exact test, a sample size of 1004 LA sessions provided a significant difference between the rates cited above at a level of {alpha} = .05 (two-tailed).

The presence and type of major and minor complications were recorded and their association with demographic and clinical characteristics of patients, as well as with nodule and laser session characteristics, was analyzed by using a two-sample Student t test (two-tailed, {alpha} = .05) and a Fisher exact test (two-tailed, {alpha} = .05). We used a two-sample Student t test to compare the mean values of age, prothrombin time, energy, bilirubin level, and platelet count. These mean values were divided into two groups: a set of LA sessions with major complications and one without. We used the Fisher exact test to evaluate the presence of major complications with respect to the following variables: sex, Child-Pugh grade (A and B vs C), ascites (absent and controlled vs uncontrolled), esophageal varices (F1, F2, and F3 vs none), hypertensive gastropathy, and nodule site depth. Finally, we controlled the relationship between nodule site and type of complication (major or minor) by means of a Fisher exact test and the difference between the mean level of energy delivered to the nodule during a single LA session with respect to the type of complication (major, minor, and side effect) by means of a two-sample Student t test.

All random variables significant (P < .05) in the univariate analysis were introduced in a multivariate logistic regression model to test which nodule or patient characteristic has an influence on the probability of a major complication after LA. The binary outcome was the presence of major complications.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
The percutaneous ablation experience level of the nine participating centers was: level A = one, B = three, C = two, and D = three centers.

HCC-LA Study
Patients.—The 520 patients with 647 HCC nodules were treated with 1004 laser sessions. Hepatitis B or C-related cirrhosis was present in nearly all patients (92.5%) and liver function was reduced in 36.7% of patients, according to Child-Pugh B (30.8%) or C (5.9%) grade (Table 1). Portal hypertension was frequent, as demonstrated by the presence of esophageal varices and hypertensive gastropathy (13) in 42.2% and 29.9% of patients, respectively. Among associated diseases or risk factors, diabetes was present in nearly one-fifth of patients, but the frequency of any other condition did not exceed 1.5% (Table 1).


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  		Table 1. Demographic and Clinical Characteristics of 520 HCC Patients Treated with LA

 
Regarding size, the 647 HCC nodules (mean diameter, 3.2 cm ± 1.7) were distributed as 387 (60%) small, 180 (28%) intermediate, and 74 (11%) large nodules. In six (1%) patients the nodule diameter was not available.

Complications.—Fifteen patients (1.5% of 1004 LA sessions) had major complications (Table 2). There were four (0.8%) deaths out of 520 patients, all occurring during the initial LA period, from 1996 to 2000. All four of these had intermediate or large tumors, and two were in Child-Pugh C grade. The cause of death was due to liver failure in two patients (one associated with respiratory failure) 24–48 hours after LA, to colon perforation (owing to a large exophytic nodule that was in close contact with the bowel) 3 days after LA in the third patient, and to cardiovascular shock that occurred at home 8 days after LA in the fourth patient. Seeding was not reported.


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  		Table 2. Demographic, Clinical, Nodule, and LA Characteristics of 15 HCC Patients with Major Complications

 
Minor complications and side effects (Table 3, Fig 2) were also reported. Major and minor complications and side effects, according to nodule diameter and to LA sessions, showed that the frequency of major complications was lower in small HCC nodules (Table 4). However, the difference with intermediate HCC nodules was not significant (1.38% vs 1.86%) and the sample size of major complications in the group of large HCC nodules (one of 163 nodules treated) was too low for any statistical evaluation.


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  		Table 3. Minor Complications and Side Effects of 1004 LA Sessions in 520 HCC Patients

 

Figure 2A
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  		Figure 2a: Intrahepatic portal arteriovenous fistula in 69-year-old man 1 month after LA of 4-cm paravascular HCC. (a) Transverse color Doppler US scan shows intrahepatic oval area (arrow) with arterial spectral waveform. (b) Transverse dynamic contrast-enhanced CT scan shows hypoattenuating oval area in segment VII with internal eccentric enhancement (arrow) in arterial phase, which increases in portal phase, suggesting arteroportal fistula.

 

Figure 2B
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  		Figure 2b: Intrahepatic portal arteriovenous fistula in 69-year-old man 1 month after LA of 4-cm paravascular HCC. (a) Transverse color Doppler US scan shows intrahepatic oval area (arrow) with arterial spectral waveform. (b) Transverse dynamic contrast-enhanced CT scan shows hypoattenuating oval area in segment VII with internal eccentric enhancement (arrow) in arterial phase, which increases in portal phase, suggesting arteroportal fistula.

 

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  		Table 4. Complications by Nodule Diameter and LA Session in 520 HCC Patients

 
The presence of major complications was associated with a deep site of the nodule in the liver, in relationship with the number of LA sessions performed at either site (Fisher exact test, P < .05), and the proportion of major complications in deep nodules was significantly different (2.44% vs 0.8%, P < .05) compared with superficial nodules (Table 5). Higher mean levels of energy delivered in a single session were significantly more frequent in patients with major and minor complications with respect to those with side effects only (P < .05). The proportion of major complications in patients with absent or controlled ascites was significantly different (2.45% vs 9.52%, P < .05) compared with those with uncontrolled ascites (Table 6).


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  		Table 5. Complications by Nodule and LA-related Characteristics in 520 HCC Patients

 

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  		Table 6. Association of Major and Minor Complications with Patient and LA-related Characteristics in 520 HCC Patients

 
No association with levels of energy was found in the comparison between major and minor complications, and the difference was not significant.

Energy delivered in LA sessions followed by major complications was greater (Table 6) than that delivered in those without (10 520 J ± 7073 vs 7474 J ± 3803, P < .05).

Patients who reported minor complications had a lower prothrombin time (70.66 seconds ± 16.29 vs 77.10 seconds ± 16.01, P < .05), higher bilirubin values (1.74 mg/dL ± 1.1 vs 1.34 mg/dL ± 0.76 [29.75 µmol/L ± 18.81 vs 22.91 µmol/L ± 12.97], P < .05), and received higher energy (9871 J ± 4090 vs 7364 J ± 3823, P < .05), with respect to those without complications.

The three significant variables from univariate analysis (ascites, level of energy delivered, and nodule site) were tested by means of multivariate logistic regression with the binary outcome of presence of major complications. The ascites variable was eliminated because of its nonsignificant relationship with the outcome (P = .48) and the model was estimated again with the two remaining variables. The chosen cutoff for the level of energy delivered was 7200 J. The odds of a major complication are estimated to be 22 times higher for a patient who undergoes an LA session to ablate a deep nodule as compared with a superficial nodule, irrespective of energy level (odds ratio = 22; 95% confidence interval: 9, 55; P < .001). The odds of a major complication are estimated to be 32 times higher for a patient who undergoes an LA session where the energy level exceeds 7200 J as compared with less than 7200 J, irrespective of nodule site (odds ratio = 32; 95% confidence interval: 16, 66; P < .001).

With regard to the distribution of major complications between centers, no difference was found according to the level of ablation experience.

Effectiveness of LA
Complete necrosis was achieved in 60% of the 647 nodules, regardless of size, and in 81.1% of small nodules (Table 7).


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  		Table 7. Primary Effectiveness Rate of LA by Diameter in 647 nodules of 520 HCC Patients

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
We believe our study represents the largest series published today on LA for HCC and may be compared by sample size with other studies on complications of PEI (14–16) and RF (17–20). Moreover, the homogeneity of the reporting criteria in the liver database provides more standardization regarding comparison of results.

The results of our study show that major complications after LA were associated with technical and/or anatomic factors, but not with HCC diameter or patient characteristics. In fact, at multivariate analysis the odds of a major complication are estimated to be 22 times higher for a patient with a deep nodule as compared with a superficial one, and 32 times higher for a patient who undergoes an LA session where the energy level exceeds 7200 J, as compared with less than 7200 J, irrespective of nodule site.

The positive association with a deep HCC is understandable, according to our definition, as this site may correspond to the liver hilum, an area at higher risk for major complications, such as bile duct and main hepatic vessel injury (21,22). The bile duct damage in our study is lower than that reported for RF (21) and PEI (16) (0.3% vs 2.0% and 3.3%, respectively). However, this comparison is limited by differences in reporting and possibly in patient population, since this was not a direct comparison. The mortality rate was 0.8% and may be comparable with the rates reported for other ablation techniques (17,18,23). It is important to note that all deaths occurred only in patients with advanced liver disease (cirrhosis and/or HCC) and only during the initial LA period (from 1996 to 2000) when patients with Child-Pugh grade C, coagulation deficit, or large HCC nodules were not always excluded from treatment. Finally, the LA major complication rate, excluding death, was lower than that reported in previous PEI (14–16) and RF studies (18,20,21), even though the mean age of our study population was older (14,16,20). In our study, we found fewer major complications which needed surgery or interventional radiology than in the LA study by Vogl et al (4), even if in the German study only 42 (4.6%) of 899 patients were cirrhotic. Therefore, a potential advantage of LA versus laser-induced thermotherapy may result from the use of thinner needles (21-gauge vs 7F or 9F), which is less traumatic for the liver of cirrhotic patients who have reduced coagulation function.

Needle track seeding and cancer spreading are relevant issues for any oncologic interventional procedure (24), although the classification of seeding as a major complication has been recently questioned (8,25). The risk of seeding after percutaneous ablation for HCC varies from 0.3% to 1.9% for PEI (14–16) and from 0.5% to 2.7% for RF (19,26,27), but it has not been described for LA to date (28). In our study, neither seeding nor unexpected tumor spreading were observed and this may be because continuous illumination of laser fibers was maintained during needle extraction from the liver at the end of LA. Minor complications were mainly represented by asymptomatic perihepatic fluid collection or minimal subcapsular hematoma and were associated with lower prothrombin time but higher mean bilirubin and energy values. This confirms that reduced liver function must be considered a limiting factor as for PEI (14) and RF (19).

With regard to the effectiveness rate, the best results were obtained in the small nodules, possibly owing to complete histologic necrosis in the entire nodule, in relationship with the specific laser-induced progressive microvascular injury and complete DNA destruction experimentally observed in rats (29,30).

Any study on the complications of percutaneous ablative minimally invasive techniques is limited by a reduced statistical power owing to a low number of index events. Also in our study, the association of major complications with clinically and technically related factors was limited owing to the small number of patients with major complications–15 of 1004 laser sessions and only 1 large HCC of 163 LA sessions. Another limitation of our study consisted of its mainly retrospective nature, which may have resulted in a lack of data in some fields in the database. The prospective portion of the LA study started in 2004 will hopefully address these issues.

In conclusion, our study shows that LA is a safe, minimally invasive treatment for nonsurgical HCC and that its complications are associated with clinical and technique-related factors. Our study indicates that, thanks to its low rate of complications and to a primary effectiveness rate of 81% in small nodules, LA may also be considered as an alternative to PEI and RF for HCC.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 


   IMPLICATION FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
References
 


   ACKNOWLEDGMENTS
 
The authors thank Chiara Dellacasa, Electronics Engineer, Sistemi Informativi e Servizi per la Sanitá, Consorzio Interuniversitario, Bologna, Italy, for data extraction and partial statistical analysis; Susan Jane West, BA, Bologna, Italy for language editing; and Esterita Accogli, MD, Lorenzo Baldini, MD, Andrea Domanico, MD, Milena Micati, MD, Stefano Ramilli, MD, and Filippa Vitale, MD, Ultrasound Research and Education Center, Ospedale Maggiore, Bologna, Italy, for data collection and review.


   FOOTNOTES
 

Abbreviations: HCC = hepatocellular carcinoma • LA = laser ablation • PEI = percutaneous ethanol injection • RF = radiofrequency

See Materials and Methods for pertinent disclosures.

Author contributions: Guarantor of integrity of entire study, V.A.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, all authors; clinical studies, all authors; statistical analysis, V.A., S.P., C.M.P., F.M., F.M.L.D.L.; and manuscript editing, V.A., S.P., C.M.P., F.M.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 

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C. M. Pacella, G. Francica, F. M. L. Di Lascio, V. Arienti, E. Antico, B. Caspani, F. Magnolfi, A. S. Megna, S. Pretolani, R. Regine, et al.
Long-Term Outcome of Cirrhotic Patients With Early Hepatocellular Carcinoma Treated With Ultrasound-Guided Percutaneous Laser Ablation: A Retrospective Analysis
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