European Radiology

, Volume 28, Issue 5, pp 1986–1993 | Cite as

Ultrasound-ultrasound image overlay fusion improves real-time control of radiofrequency ablation margin in the treatment of hepatocellular carcinoma

  • Yasunori Minami
  • Tomohiro Minami
  • Satoru Hagiwara
  • Hiroshi Ida
  • Kazuomi Ueshima
  • Naoshi Nishida
  • Takamichi Murakami
  • Masatoshi Kudo
Hepatobiliary-Pancreas
  • 205 Downloads

Abstract

Objectives

To assess the clinical feasibility of US-US image overlay fusion with evaluation of the ablative margin in radiofrequency ablation (RFA) for hepatocellular carcinoma (HCC).

Methods

Fifty-three patients with 68 HCCs measuring 0.9–4.0 cm who underwent RFA guided by US-US overlay image fusion were included in this retrospective study. By an overlay of pre-/postoperative US, the tumor image could be projected onto the ablative hyperechoic zone. Therefore, the ablative margin three-dimensionally could be shown during the RFA procedure. US-US image overlay was compared to dynamic CT a few days after RFA for assessment of early treatment response. Accuracy of graded response was calculated, and the performance of US-US image overlay fusion was compared with that of CT using a Kappa agreement test.

Results

Technically effective ablation was achieved in a single session, and 59 HCCs (86.8 %) succeeded in obtaining a 5-mm margin on CT. The response with US-US image overlay correctly predicted early CT evaluation with an accuracy of 92.6 % (63/68) (k = 0.67; 95 % CI: 0.39–0.95).

Conclusion

US-US image overlay fusion can be proposed as a feasible guidance in RFA with a safety margin and predicts early response of treatment assessment with high accuracy.

Key points

• US-US image overlay fusion visualizes the ablative margin during RFA procedure.

• Visualizing the margin during the procedure can prompt immediate complementary treatment.

• US image fusion correlates with the results of early evaluation CT.

Keywords

Ablation techniques Hepatocellular carcinoma Liver Neoplasms Ultrasonography 

Abbreviations

3D

Three-dimensional

BCLC

Barcelona clinic liver cancer

CEUS

Contrast-enhanced ultrasonography

HCC

Hepatocellular carcinoma

MDCT

Multidetector CT

MPR

Multiplanar reconstruction

RFA

Radiofrequency ablation

ROI

Region of interest

SD

Standard deviation

US

Ultrasound

Introduction

The local efficacy of radiofrequency ablation (RFA) for small hepatocellular carcinomas (HCCs; i.e., < 2 cm) has been shown to be comparable to that of surgical outcomes [1, 2, 3, 4]. However, many studies have reported a trend towards higher recurrence in patients treated by RFA [5, 6, 7, 8, 9]. It has been reported that the local recurrence rates after RFA for HCC ranged from 1.7 % to 41 % over the 2–3 years of follow-up [10]. The local recurrence rate differs markedly depending on whether or not a 5-mm ablative margin is secured to eradicate potential microscopic invasion [11]. For the RFA procedure to be considered technically successful, the tumour and a sufficient ablative margin (at least 5 mm) must be included in the ablation zone [12]. Unfortunately, a safety margin is not always obtained in RFA therapy [13, 14]. Sonography is often restricted by the formation of gas bubbles showing strong acoustic scatters within the ablation zone, and then an irregular hyperechoic zone visually obscures the targeted tumour [15]. Blind assessments of an ablative margin on ultrasound (US) could result in an insufficient ablative margin, representing a significant risk factor for residual or recurrent HCC tumours [15, 16].

Advances in computer processing and image display have allowed cross-sectional images of CT or MRI volume data to be displayed in the same plane as US in real-time by multiplanar reconstruction (MPR). It has been reported that US-CT/MRI fusion imaging-guided RFA was useful in the treatment of hepatic malignancies that were inconspicuous on B-mode US [17, 18, 19, 20]. Recently, the development of image fusion has made it possible to visualize the ablative margin on US [21]. By an overlay of preoperative and postoperative US, the tumour image could be projected onto the white ablation zone in real-time. Therefore, US-US overlay image fusion could show the ablative margin during the RFA procedure. In a good response case, two concentric circles containing the centred tumour within the ablative hyperechoic zone should be shown by US-US image overlay fusion. We hypothesized that this US-US image overlay fusion guidance in RFA could improve safety margin achievement and reduce the risk of local tumour progression. The purpose of this retrospective study was to assess the usefulness of US-US image overlay fusion with evaluation of the ablative margin in RFA for HCC.

Materials and methods

Patient selection and eligibility

Institutional review board approval and informed patient consent regarding the retrospective analysis of the clinical data were obtained for this single-centre study. Diagnosis of HCC was based on the clinical guidelines of the American Association for the Study of Liver Disease following the observation of arterial hyperenhancement with washout on delayed-phase images [22]. The therapeutic decision regarding RFA was made by consensus of the multidisciplinary tumour board before each treatment.

A total of 53 patients with 68 HCCs were treated with RFA between May 2014 and July 2015. The eligibility criteria were: (1) age 18 years or more; (2) proven HCC; (3) eligible for RFA (≤ 3 nodules with a maximum diameter ≤ 3 cm, Barcelona Clinic liver cancer (BCLC) stage 0 to B1; (4) patient unwilling to undergo hepatectomy or liver transplantation; (5) well-preserved liver function (Child–Pugh score ≤ 8, serum total bilirubin level ≤ 3 mg/dl and prothrombin time-international normalized ratio ≤ 1.5) and (6) Eastern Cooperative Oncology Group (ECOG) performance status score ≤ 1. The exclusion criteria were as follows: (1) tumour invasion of major hepatic vessels or extrahepatic metastases; (2) present or past history of uncontrolled ascites, hepatic encephalopathy or variceal bleeding; (3) severe dysfunction of the heart, kidney or other organs; and (4) active infection (except viral hepatitis).

Equipment

An US machine (LOGIQ E9, GE Healthcare, Chalfont St. Giles, UK) coupled with a low magnetic field generator was used. Two electromagnetic position sensors connected with a position-sensing unit were attached on the probe (4.0 mHz curvilinear C1-6, GE Healthcare) through a bracket. Both the transmitter and the sensors were connected to a position-sensing unit embedded in the ultrasound machine. Volume navigation system (V nav, GE Healthcare) delivers real-time image fusion of US with other modalities such as MRI or CT. The standard of volume navigation can serve a function of US-US image overlay fusion.

Patients were treated by RFA (VIVA RF ablation system; STARMed Co., Goyang, Gyeonggi, South Korea). Twenty 1-cm long, 17-gauge, monopolar internally cooled electrodes (VIVA RF electrode; STARMed) were used to deliver radiofrequency energy, and the active metallic tip could be adjusted in 5-mm intervals up to 3 cm long. A 200-W, 480-kHz monopolar radiofrequency generator regulated by impedance (VIVA RF generator, STARMed) and with three styles of power distribution (General, Auto, Continuance modes) was used as the energy source.

US-US image overlay fusion and RFA procedure

Before inserting the radiofrequency needle, the 3D US volume was obtained by scanning the liver in a manual sweeping manner with the patient in a breath-holding position (Fig. 1). The scanning area had to include not only the tumour but also intrahepatic vessels around the tumour. This 3D volume data contained the spatial information in the generated magnetic field. A cross-section of the 3D US volume was selected based on the largest diameter dimension of the tumour, and two green squares on the screen were arranged to fix a perpendicular line through the centre of the tumour image. Six rotated sections passing through the tumour centre were then automatically displayed. A ROI was drawn along the tumour border in each of the rotated sections using the ellipse ROI method, with the result that the tumour border could be traced three-dimensionally. The interior was colorized, and this 3D US volume data was stored within the US machine.
Fig. 1

Image processing of US-US overlay image fusion in a demonstration case. (A) The still image during the sweep scanning shows a small hyperechoic nodule (arrow) in the right liver on B-mode (left) and blue cross-sections that depict the trajectory of sweeping the US transducer (right). (B) The box image mean 3D volume data of US by sweep scanning. Two green squares are arranged on the perpendicular line through the centre of the hyperechoic nodule. (C) The borders of the hyperechoic nodule are traced in each of six rotated sections using the ellipse region of interest method. (D) This US fusion imaging shows the real-time image on B-mode US (left) and the cross-section of 3D US volume data (right). The hyperechoic nodule is shown as green. (E) US-US overlay image fusion shows an orange-coloured background image overlaying these two images (left)

Fig. 2

Hepatocellular carcinoma in a 57-year-old man in segment VI of the liver. (A) Transverse arterial phase CT scan shows a viable hepatocellular carcinoma (HCC) measuring 1.6 cm in diameter (arrow) before radiofrequency ablation (RFA). (B) B-mode sonographic image shows a well-circumscribed irregular hyperechoic nodule. (C) Right shows a cross-sectional image of 3D US volume before ablation, and the tumour is shown as green. The orange-coloured background indicates real-time overlaying imaging before ablation onto the cross-sectional image after ablation. The overlay image shows the green colorised tumour inside the ablative hyperechoic zone. The ablative margin is then revealed. (D) Transverse portal phase CT scan shows that HCC and the surrounding area are not enhanced, indicating complete necrosis of the lesion

Fig. 3

Hepatocellular carcinoma in an 81-year-old woman in segment VII of the liver. (A) Transverse arterial phase CT scan shows a viable hepatocellular carcinoma (HCC) measuring 2.8 cm in diameter (arrow) before radiofrequency ablation (RFA). (B) B-mode sonographic image shows a well-circumscribed irregular hypoechoic nodule (arrow). (C) US-US overlay image fusion demonstrates the green colorised tumour inside the ablative hyperechoic zone. (D) Transverse portal phase CT scan shows that HCC and the surrounding area are not enhanced, indicating complete necrosis of the lesion

During and immediately after ablation, the clinical role of US is markedly limited because of the initial hyperechoic ablated zone, the so-called echogenic cloud, and the resultant acoustic shadowing [23]. When the acoustic shadowing had gradually begun to disappear at the deeper side of the tumour (2–3 min), the 3D US volume data were carefully fused with the real-time 2D US image to the millimetre using a volume navigation system (V nav). The fusion imaging showed the real-time 2D US image (post-ablation) and MPR US image (pre-ablation) side-by-side. If needed, some landmark markers were marked successively on each image set using a caliper. Thereafter, US-US image overlay could display the ablative hyperechoic zone including the coloured tumour. The image overlay allowed easy visualization of the ablative margin on US. When the ablation zone created with a single ablation was not sufficient to cover the index tumour with an adequate ablative margin, a multiple overlapping ablation technique was applied by replacing the electrode to insufficient ablation sites. After the final ablation, the ablative margin was assessed by US-US image overlay fusion.

All RFA procedures were performed by three experienced hepatologists (M.T, Y.M and H.I, with 6, 20 and 21 years of experience, respectively). The tip length choice for the active RF electrode was 0.5–1.0 cm over the tumour size. Under Auto mode, power was usually begun at 40 W with a 2-cm exposed-tip RF electrode or at 50 W with a 3-cm exposed-RF tip. After a few times of power roll-off, the RFA procedure was terminated if the ablative hyperechoic zone had expanded over the tumour with the safety margin assessed using US-US image overlay fusion.

Imaging data evaluation

A few days after treatment, the technical effectiveness of ablation was assessed with dynamic MDCT using 5-mm slice scans. The patients were classified into four groups as follows: grade A (absolutely curative), a 5-mm or larger ablative margin around the entire tumour; grade B (relatively curative), an ablative margin around the tumour but less than 5 mm in diameter in some places; grade C (relatively non-curative), only an incomplete ablative margin around the tumour although no residual tumour was apparent; grade D (absolutely non-curative), the tumour was not completely ablated [13, 14].

Data are expressed as mean ± SD. US-US image overlay was compared to dynamic CT a few days after RFA for assessment of early treatment response. The accuracy of graded response was calculated, and the performance of US-US image overlay fusion for the evaluation of early response was compared with that of CT as the gold standard using a Kappa agreement test [24, 25, 26]. Statistical analyses were performed by using statistical software (SPSS 12.0; SPSS, Chicago, IL, USA).

Results

Fifty-three patients (39 men, 14 women; age range, 44–91 years; mean age ± SD, 70.0 ± 12.0 years) with 68 HCCs were analysed (Table 1). The maximal diameter of the tumours ranged from 0.9 to 4.0 cm (mean ± SD, 1.8 ± 0.7 cm) on dynamic CT. Forty-three patients had liver cirrhosis of Child-Pugh class A and the remaining eight had Child-Pugh class B cirrhosis. Nineteen patients with 26 HCCs had not previously been treated for these hepatic lesions. The remaining 34 patients with 42 HCCs had previously been treated by RFA at other sites in the liver. No patient had shown local tumour progression after various therapies.
Table 1

Baseline clinical characteristics of the patients

Number of patients

53

Sex

 Male

39 (73.6)

 Female

14 (26.4)

Age (year)

 Mean ± SD

70.0 ± 12.0

 Range

44–91

Aetiological cause of HCC

 Hepatitis B

4 (7.5)

 Hepatitis C

34 (64.2)

 nonBnonC

15 (28.3)

Mean serum albumin level (g/dl)*

3.7 ± 0.6

Mean serum total bilirubin level (g/dl)*

1.0 ± 1.0

Child-Pugh class

 A

43 (81.1)

 B

10 (18.9)

 C

0

Serum AFP level

 < 20 ng/ml

33 (62.2)

 20–200 ng/ml

19 (35.8)

 > 200 ng/ml

1 (1.9)

Number of HCCs

68

Tumour location

 Left lateral

10 (14.7)

 Left medial

8 (11.8)

 Right medial

25 (36.8)

 Right lateral

22 (45.8)

 Segment 1

3 (4.4)

Tumour size (cm)

 Mean ± SD

1.8 ± 0.7

 Range

0.9-4.0

Unless otherwise stated, data are number of patients or HCCs and data in parentheses are percentages

HCC hepatocellular carcinoma, AFP alpha-fetoprotein

*Data are means ± standard deviation

Technically effective ablation was achieved in a single session in all patients, and the total number of RF needle insertions for ablation was 1.9 ± 1.2 (range, 1–8) per tumour. Tumour enhancement completely disappeared in early assessment of treatment response in all patients (Figs. 2 and 3). According to the grading system for early assessment with MDCT, we classified 59 HCCs (86.8 %) as grade A, seven (10.3 %) as grade B, two (2.9 %) as grade C, and none as grade D. The response category with US-US image overlay correctly predicted the early MDCT response category with an accuracy of 92.6 % (63/68) (Table 2). The kappa coefficient comparing the agreement of dynamic CT and US-US image overlay fusion results was substantial (k = 0.67; 95 % confidence interval: 0.39– 0.95).
Table 2

Comparison of ultrasound-ultrasound (US-US) overlay image fusion and dynamic CT for early assessment of tumour response after radiofrequency ablation (RFA) for hepatocellular carcinoma (HCC)

US-US overlay image fusion

Dynamic CT

Total

Grade A

Grade B

Grade C

Grade D

Grade A

58

2

0

0

60

Grade B

1

5

2

0

8

Grade C

0

0

0

0

0

Grade D

0

0

0

0

0

Total

59

7

2

0

68

The mean follow-up was 17.8 ± 7.6 months (median 19 months; range 1–29 months). All procedures were performed successfully without immediate or late complications. During the follow-up period, none of the patients showed local tumour progression. Indeed, we found no local recurrence in patients with nine HCCs presenting grade B or C during the follow-up periods of 17–19 months. However, two patients demonstrated distant single metastases in the liver.

Discussion

Usually, the ablative margin cannot be precisely evaluated on B-mode US and/or CEUS immediately after RFA because gas bubbles due to the ablation hide the tumor and the surroundings. Therefore, CT/MRI is commonly used for evaluating the treatment response to local ablation therapy for HCC [11, 22, 27]. However, this US-US image overlay allowed us to evaluate the ablative margin during the RFA procedure. Using a grading system to assess the early response of RFA, Nishikawa et al. reported rates of grades from A (absolutely curative) to D (absolutely non-curative) of 18.2–19.0 %, 42.0–44.0 %, 27.2–27.5 % and 9.8–12.3 %, respectively [13, 14]. In contrast, our data were classified as 86.8 %, 10.3 %, 2.9 % and 0 %, respectively. The achievement of US-US image overlay fusion guidance supported sufficient margins because we could provide additional ablation more efficiently. We considered the following three features of US-US image overlay fusion as the reasons for our good results: first, the real-time monitoring of the ablating area; second, the effective decision-making regarding additional ablation; third, the confirmation of sufficient ablative margins during the RFA procedure.

Larger HCC had a higher frequency of portal vein invasion and intrahepatic metastases in the surrounding tumour than smaller HCC. Larger tumours require sufficient ablative margins to prevent recurrences by multiple ablations. It is often technically difficult to obtain a sufficient ablative margin over the whole of a large HCC. Many have reported that local recurrence rates increased with larger sizes of tumour in RFA [28, 29, 30]. However, we could obtain sufficient ablative margins in HCCs larger than 2 cm, and our data also showed very low rates of local tumour progression.

Many reports indicate that dynamic CT is currently a common technique to assess the early response within one week after RFA [12, 14, 15]. Early detection of residual HCC after RFA is critical and can facilitate successful retreatment. Late diagnosis results in peripheral regrowth and might make retreatment difficult owing to limited access. However, such HCC patients could tend to accumulate radiation exposure.

In addition, MRI for its intrinsic contrast resolution is particularly suitable in ‘identification’ and ‘quantization’ of the necrosis induced by ablative therapies. A further advantage of the combined interpretation of dynamic and hepatobiliary phase MR images was the lower number of false-positive findings compared with those using dynamic MR or CT image sets [31, 32]. However, the use of MRI can be hindered because of the generally high costs, long examination duration and limited availability in this clinical setting.

Furthermore, the diagnostic accuracy of the response category with US-US image overlay fusion was very high, 92.6 %, in this study. If precise image registration adjustment with US-US image overlay fusion can be achieved, contrast-enhanced CT or hepatospecific contrast-enhanced MRI for early response assessment of RFA could potentially be omitted.

The principal limitation of this study was its retrospective design. The second was that this study could suffer from selection bias because the patients were enrolled according to tumour size, number and/or location for RFA indication. Moreover, patients with a poor quality of US image of the liver due to artifacts might have been avoided from enrolling in this study because it was often difficult to adjust the location of intrahepatic vessels between two US images before and after ablation using US-US image overlay. Another limitation was the preliminary nature of the study, with a relatively small number of patients and a short follow-up time. Further prospective studies of this technique with a larger number of patients are warranted.

In conclusion, US-US image overlay fusion could visualize the ablative margin of RFA on US. US-US image overlay fusion guidance can contribute to obtaining sufficient margins for RFA therapy. US-US image overlay fusion could have potential usefulness for predicting the early response of treatment assessment during the RFA procedure.

Notes

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Prof. Masatoshi Kudo.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• case-control study

• performed at one institution

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Copyright information

© European Society of Radiology 2017

Authors and Affiliations

  • Yasunori Minami
    • 1
  • Tomohiro Minami
    • 1
  • Satoru Hagiwara
    • 1
  • Hiroshi Ida
    • 1
  • Kazuomi Ueshima
    • 1
  • Naoshi Nishida
    • 1
  • Takamichi Murakami
    • 2
  • Masatoshi Kudo
    • 1
  1. 1.Department of Gastroenterology and HepatologyKindai University Faculty of MedicineOsakaJapan
  2. 2.Department of RadiologyKindai University Faculty of MedicineOsakaJapan

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