Robot-assisted microwave thermoablation

of liver tumors: a single-center experience

L. P. Beyer, B. Pregler, C. Niessen,

M. Dollinger, B. M. Graf, M. Müller,
H. J. Schlitt, C. Stroszczynski &
P. Wiggermann
International Journal of Computer
Assisted Radiology and Surgery
A journal for interdisciplinary research,
development and applications of image
guided diagnosis and therapy

ISSN 1861-6410

Int J CARS
DOI 10.1007/s11548-015-1286-y

1 23
Your article is protected by copyright and all
rights are held exclusively by CARS. This e-
offprint is for personal use only and shall not
be self-archived in electronic repositories. If
you wish to self-archive your article, please
use the accepted manuscript version for
posting on your own website. You may
further deposit the accepted manuscript
version in any repository, provided it is only
made publicly available 12 months after
official publication or later and provided
acknowledgement is given to the original
source of publication and a link is inserted
to the published article on Springer's
website. The link must be accompanied by
the following text: "The final publication is
available at link.springer.com”.

1 23
 Author's personal copy
Int J CARS
DOI 10.1007/s11548-015-1286-y

ORIGINAL ARTICLE

Robot-assisted microwave thermoablation of liver tumors:

a single-center experience
L. P. Beyer1 · B. Pregler1 · C. Niessen1 · M. Dollinger1 · B. M. Graf2 ·
M. Müller3 · H. J. Schlitt4 · C. Stroszczynski1 · P. Wiggermann1

Received: 10 May 2015 / Accepted: 17 August 2015

© CARS 2015

Abstract microwave applicator with high accuracy. The complica-

Purpose To evaluate and compare the needle placement tion rate and ablation success of percutaneous microwave
accuracy, patient dose, procedural time, complication rate thermoablation of malignant liver tumors using either CT flu-
and ablation success of microwave thermoablation using a oroscopy or robotic guidance for needle positioning showed
novel robotic guidance approach and a manual approach. no significant differences in the 6-week follow-up.
Methods We performed a retrospective single-center eval-
uation of 64 microwave thermoablations of liver tumors
in 46 patients (10 female, 36 male, mean age 66 years) Keywords Interventional radiology · Robotic assistance ·
between June 2014 and February 2015. Thirty ablations Microwave ablation · Liver tumor · CT-guided
were carried out with manual guidance, while 34 ablations
were performed using robotic guidance. A 6-week follow-up
(ultrasound, computed tomography and MRI) was performed Introduction
on all patients.
Results The total procedure time and dose-length product Microwave ablation is a special form of thermal ablation.
were significantly reduced under robotic guidance (18.3 vs. It uses alternating electromagnetic waves to induce tissue-
21.7 min, p < 0.001; 2216 vs. 2881 mGy×cm, p = 0.04). heating effects leading to thermal denaturation of solid
The position of the percutaneous needle was more accurate tumors and the surrounding tissue [1]. It is a therapeutic
using robotic guidance (needle deviation 1.6 vs. 3.3 mm, method for curative or palliative treatment in nonsurgical
p < 0.001). There was no significant difference between candidates. Hepatocellular carcinoma and liver metastasis
both groups regarding the complication rate and the ablation constitute a classic field of application for thermal ablation.
success. Many studies have proven that there are similar survival rates
Conclusion Robotic assistance for liver tumor ablation compared to surgery [2,3].
reduces patient dose and allows for fast positioning of the The microwave applicator can be positioned using ultra-
sound, computed tomography or magnetic resonance imag-
B L. P. Beyer ing [4]. Needle positioning is challenging in the case of
[email protected] barely visible tumors or difficult approaches, and reposi-
1 tioning of the microwave applicator is often unavoidable.
Department of Radiology, University Medical Center
Regensburg, Franz-Josef Strauss Allee 11, 93053 Every needle replacement leads to a higher complication rate
Regensburg, Germany [5,6]. Using computed tomography-guided applicator posi-
2 Department of Anesthesia, University Medical Center tioning, the dose to the patient and interventionalist leaps
Regensburg, Regensburg, Germany with increasing complexity [7]. As a result, a relatively high
3 Department of Internal Medicine I, University Medical Center radiation dose can occur in difficult ablation scenarios [8,9].
Regensburg, Regensburg, Germany Modern, robot-assisted CT-based navigation systems allow
4 Department of Surgery, University Medical Center for precise planning of the applicator approach and the
Regensburg, Regensburg, Germany expectable ablation area in a 3D image data record. High

123
 Author's personal copy
Int J CARS

accuracy and precision are achieved [10]. These systems Peri-interventional imaging
could potentially lead to a reduced radiation dose for the
patient and interventionalist as well as to a lower number of All patients underwent three-phase multi-slice CT (Somatom
needle replacements and as a consequence to a lower com- Sensation 16, Siemens Healthcare, Forchheim, Germany)
plication rate. in apnea immediately before tumor ablation. Contrast-
There is only very limited data regarding robot-assisted enhanced arterial phase images were generated during injec-
microwave ablation of malignant liver tumors [11,12]. There- tion of 120 mL of nonionic contrast material at a flow rate of
fore, we report on our results comparing a novel robotic 3–4 mL/s using bolus tracking with a threshold of 100 HU.
system to the CT-guided fluoroscopic manual approach for Portal venous phase images were obtained 50 s after the arter-
needle positioning in microwave thermoablation of malig- ial phase scan. At the end of the ablation session, every patient
nant liver tumors. underwent a non-contrast multi-slice CT scan of the liver to
detect or exclude any complications.
In three-phase CT, the density values of tumor and liver
tissues were measured with circular ROIs (regions of inter-
Materials and methods est) with a size of 1 cm2 . The density differences between
liver tissue and tumor were determined in both the non-
Study design and participant selection contrast technique and the contrast-enhanced phase with the
best tumor visibility. The density difference was referred to
A single-center retrospective observational study was con- as the tumor conspicuity (TC). The size of the tumor was
ducted to assess radiological findings and interventional measured in the contrast-enhanced phase with the best tumor
reports from 64 consecutive CT-guided microwave abla- visibility in the short and long axis. In addition, the shortest
tion sessions between June 2014 and January 2015. Before distance from the skin to the tumor in axial plane (skin-to-
treatment, all patients were reviewed by members of an inter- tumor depth) was determined.
disciplinary tumor board who decided on the indication for
microwave ablation. Patients were selected for microwave Thermoablation procedure
ablation if surgical resection was precluded. Exclusion cri-
teria were coagulopathy, tumor resectability, unsuitability All ablation procedures were performed in general anesthesia
of the patient to undergo general anesthesia, or multifocal by an experienced interventional radiologist. In each patient,
hepatic disease not amenable to complete ablation. microwave ablation was carried out percutaneously using the
Forty-six patients (mean age 66 years; age range 54– Acculis microwave tissue ablation system (AngioDynamics,
85 years) with primary liver tumors or secondary liver Latham, NY, USA), which operates at 2.45 GHz with a maxi-
metastases underwent microwave ablation. Thirty-four of the mum power output of 140 W and uses electromagnetic waves
interventional procedures were robot-assisted and 30 were to induce tissue-heating effects leading to necrosis [1]. The
fluoroscopy-guided (Table 1). In all cases, preinterventional standard Acculis microwave applicator with a 1.8-mm diam-
MRI with liver-specific contrast media (Primovist, Bayer eter and 16-mm active tip was used in all cases. The shaft
Schering Pharma, Berlin) had been performed as reference length (14 or 19 cm) was selected depending on the distance
imaging. from the skin to the center of the tumor where the active point
In our hospital, all patients who underwent percutaneous of the probe should be placed. After needle placement for
ablation of malignant liver tumors without any complications ablation procedure, the parameters (ablation duration, num-
are discharged two days after the CT-guided intervention. ber of watts) were adjusted depending on the tumor size with
the aim to gain a preferable safety distance of 1 cm.

Table 1 Data regarding ablated lesions Manual approach

Tumor type n Manual or guided
CT fluoroscopy is an acquisition mode that allows continu-
Manual Guided
ous image update using in-room table control. After the initial
Lung cancer 1 1 0 three-phase planning CT, the antenna is placed by an inter-
Breast cancer 2 2 0 ventional radiologist with repeated checking of the needle
Colorectal cancer 12 2 10 position using CT fluoroscopy and if necessary repositioning
Prostate cancer 1 1 0 of the needle until the tumor center is reached. In 13 cases,
Hepatocellular carcinoma 48 24 24 a verification multi-slice CT scan of the needle placement
All 64 30 34 was then performed to ensure the correct needle position.
In the remaining 17 cases, the fluoroscopy images already

123
 Author's personal copy
Int J CARS

Fig. 1 Planned position of the microwave applicator with the simulated ablation volume (purple). The tumor that is manually marked in the 3D
image dataset (orange) is completely included in the ablation volume

confirmed a correct needle position. All patients underwent

a final non-contrast multi-slice CT scan to detect any com-
plications.

Robotic guidance

Before robot-assisted image-guided tumor ablation, all

patients were positioned on a vacuum mattress to minimize
the movability of the patients between the planning multi-
slice CT scan which affects the real-time planning on the
robotic system and the positioning of the applicator. Based
on the initially performed three-phase CT of the liver, semiau-
tomatic liver segmentation and manual marking of the tumor
in a 3D image dataset were performed.
The entry point of the needle in the skin and the target
point of the needle tip were determined to plan the access
path. A simulation of the ablation volume is used to check
whether the previously marked tumor is completely included
in the ablation with sufficient safety distance (Fig. 1). This Fig. 2 Automatic placement of the robotic arm and insertion of the
simulation supports the right selection of adequate ablation microwave applicator by the radiologist
parameters (ablation duration, number of watts). The robot
software performs bone detection and semi-automatic liver
segmentation including liver vessels. During planning, warn- ified by the robot on the basis of the previously determined
ings are issued automatically if the needle path or ablation plan.
volume intersects critical structures, especially liver ves- After needle positioning, a multi-slice verification CT was
sels or bones. After approval of the plan by the radiologist, performed in every case to ensure correct antenna placement.
the robotic arm is automatically positioned over the patient After ablation, all patients underwent a non-contrast multi-
(Fig. 2). In this way the puncture direction and depth are spec- slice CT scan of the liver to detect complications.

123
 Author's personal copy
Int J CARS

Radiation exposure dose Table 2 Baseline lesion aspects

Manual or guided Manual Guided p
The total dose-length product (total DLP), fluoroscopy DLP, (N = 30) (N = 34)
the number of verification scans to check the location of the
needle during the intervention and the number of fluoroscopic Skin-to-tumor depth 57.6 ± 19.2 64.8 ± 23.5 0.190
images were recorded for every microwave ablation session. Tumor long axis 22.8 ± 12.4 19.1 ± 9.0 0.172
A k factor of 0.015 mSv/(mGy×cm) was used to convert Tumor short axis 19.6 ± 10.6 16.9 ± 8.0 0.253
DLP to effective dose. Tumor conspicuity native 9.9 ± 8.4 9.3 ± 14.1 0.824
Tumor conspicuity enhanced 35.8 ± 19.9 23.6 ± 17.3 0.011

Procedural accuracy Lesion conspicuity denotes the difference in attenuation between tumor
and liver parenchyma
Immediately prior to the start of tumor ablation, the Cartesian
distance from the active center of the microwave applicator Table 3 Deviation of the active center from the tumor center
to the tumor center was measured (ACFD, active center final Manual or guided Manual Guided p
deviation). We used OsiriX (OsiriX 6.5, OsiriX Foundation, (N = 30) (N = 34)
Geneva) to create a fusion between the contrast-enhanced CT
ACUD 3.3 ± 1.6 3.1 ± 2.5 0.772
scan with the best tumor visibility and the needle verification
ACFD 3.3 ± 1.6 1.6 ± 1.3 0.000
scan. If fluoroscopy was used and no verification scan was
available, we used the fluoroscopy images for fusion instead. The deviation after manual puncture is compared to the deviation after
In some cases, manual position correction was required after robot-assisted puncture, once before (ACUD, active center uncorrected
deviation) and once after manual position correction (ACFD, active
robot-assisted needle placement. In these cases, the distance center final deviation). Manual position correction was performed after
of the active center from the tumor center prior to position robot-assisted placement in 14 of 34 cases (41.2 %)
correction was documented (ACUD, active center uncor-
rected deviation).
Results
Complications Tumor characteristics

Complications were documented and defined according to Baseline lesion aspects are summarized in Table 2.
the standardized grading system of the Society of Interven-
tional Radiology (SIR) [13].
Procedural accuracy

Follow-up Under consideration of position correction, the deviation of

the active center from the tumor center (ACFD) was sig-
All patients underwent a 6-week follow-up including an MRI nificantly smaller in robot-assisted ablation than in manual
with liver-specific contrast agent as well as a three-phase ablation (Table 3). In contrast, there was no significant dif-
computed tomography scan of the liver. The ablation volume ference if manual position correction (ACUD) was not taken
measured in the axial plane and the radiographic adjudica- into consideration.
tion/visual assessment of the complete success of the ablation
were analyzed by two experienced radiologists. Long-term
Procedural duration
follow-up was performed by MRI only if possible (no con-
traindication and normal short-term follow-up).
For the robot-assisted method, mean duration from the prein-
terventional planning multi-slice CT to the beginning of the
Statistical analysis ablation was 18.3 min (SD 2.0 min). In the cases, which
required manual position correction of the needle under flu-
R 3.02 was used to perform all statistical calculations. A oroscopy, there was an extra time add-on of 2.8 min (SD
p value of p < 0.05 was considered the cut-off point of 1.2 min). In primarily manual ablation (under fluoroscopy),
statistical significance. Normality was verified according to mean duration from the preinterventional planning multi-
statistical parameters (mean, median, skewness and kurtosis). slice CT to the beginning of the ablation was 21.7 min
Paired abnormally distributed data were compared with the (SD 4.1 min). The intervention duration under robot assis-
Mann–Whitney U test. The chi-squared test was used to test tance was significantly shorter than for manual ablation
for independence of categorical variables. ( p < 0.001).

123
 Author's personal copy
Int J CARS

Table 4 Comparison of the radiation dose parameters Ablation success

Manual or guided Manual Guided p
(N = 30) (N = 34)
In the follow-up after 6 weeks, complete ablation without
residual tumor was seen in 94.1 % (32 of 34) of robot-assisted
Total mAs 22609.4 ± 8036.2 18196.8 ± 4802.0 0.012 ablation cases and in 96.7 % (29 of 30) of manual ablation
Total DLP 2880.6 ± 1402.5 2216.4 ± 1057.3 0.035 cases. The difference was not statistically significant ( p = 1).
Verification 14.7 ± 21.6 18.3 ± 4.5 0.387
scans CTDI Complications
Verification 272.8 ± 355.6 417.6 ± 107.1 0.039
scans DLP
There were no complications in robot-assisted ablation. An
Fluoroscopy DLP 488.6 ± 436.1 40.9 ± 63.4 0.000
infected bilioma that was treated via drainage was diagnosed
Fluoroscopy number 64.3 ± 31.5 10.8 ± 14.8 0.000 in a patient with biliodigestive anastomosis 8 days after man-
of slices
ual ablation.
Fluoroscopy DLP 908.0 ± 956.4 73.7 ± 114.3 0.000

Discussion

Radiation dose In the present study, we evaluate robot-assisted percutaneous

microwave ablation of malignant liver tumors as an alterna-
The total DLP and the fluoroscopy DLP were signifi- tive to CT-guided manual ablation using fluoroscopy.
cantly lower in robot-assisted ablation than manual ablation For successful and complete ablation, positioning of
(Table 4). The effective dose for the entire intervention was the microwave applicator that is as precise as possible is
on average 33.2 mSv (SD 15.9 mSv) for robot-assisted abla- extremely important. In manually guided ablations, it is often
tion compared to 43.2 mSv (SD 21 mSv) for manual ablation challenging to detect the exact tumor location in the fluo-
( p = 0.04). In the fluoroscopic guided group, there was a sig- roscopy images without contrast media. On the other side,
nificant difference in radiation dose between patients with the robot software which allows the fusion of the preinterven-
and without a multi-slice CT verification scan to control cor- tional contrast-enhanced planning scan with the final needle
rect needle placement (DLP 3877.2 vs. 2118.5 mGy×cm, verification scan (Fig. 3) points out the exact deviation of the
p = 0.002). needle to the originally planned needle position (tumor cen-

Fig. 3 Image fusion of planning scheme and actual needle position (white arrow). The fusion shows an optimum needle position with only minimal
caudomedial deviation

123
 Author's personal copy
Int J CARS

ter). Consecutively precise correction of the needle position vs. 21.7 min, p < 0.001). In contrast, Mbalisike et al. 2014
is possible. report an intervention duration that is 3 min longer under
Mbalisike et al. [11] performed a prospective study using robot guidance. However, the difference was not significant.
70 patients to evaluate the accuracy of robot-assisted per- There was 1 complication in all our cases (manual ablation
cutaneous microwave ablation of malignant liver tumors. group). This patient came with a preexisting biliodigestive
Measuring the distance of the applicator active point to the anastomosis and developed an infected bilioma at the site of
center of the target tumor after final readjustment they come ablation 8 days after the intervention. Although there were no
to a result of a mean deviation of 1.9 mm which is similar to difficulties during the ablation procedure, it is a well-known
our mean ACFD of 1.3 mm. fact that there is a high risk (close to 40–50 %) of develop-
It must also be taken into consideration that manual posi- ing a liver abscess/infected bilioma when thermoablation is
tion correction was not necessary in 20 of 34 cases (58.8 %). performed in patients with a bilioenteric anastomosis [15].
We believe that this is the ideal case for two reasons. On the This study has some limitations. The single-center setup
one hand, it must be assumed that the risk of complications and the low number of procedures limit generalization of
increases with every repositioning of the microwave appli- our results. Another limitation is the retrospective nature of
cator. On the other hand, the interventionalist is not exposed the study. However, we think that within the framework of
to radiation. this study, we could demonstrate the marked reduction in
The effective dose for the entire intervention was on aver- radiation exposure and procedure length.
age 33.2 mSv (SD 15.9 mSv) for robot-assisted ablation
compared to 43.2 mSv (SD 21 mSv) for manual ablation. The
difference was significant ( p = 0.04). A highly significant
difference is seen in the separate analysis of the fluoroscopy Conclusion
DLP (73.7 vs. 908 mGy×cm, p < 0.001). Therefore, patient
and interventionalist are subjected to a lower radiation dose In summary, it can be stated that in percutaneous ther-
in case of robot-assisted tumor ablation. moablation of malignant liver tumors robot assistance is a
Although one recent study showed that CTF-guided chest fast, reliable and effective alternative to manual CT guid-
biopsies showed a significantly higher mean CT dose index ance using fluoroscopy. Robot assistance has the potential to
than MS-CT biopsy mode [14], we believe that in oncological increase precision and reduce radiation dose for the physician
interventions and mostly difficult reachable lesions in the and the patient without increasing risk of complications. We
liver it is essential to use CTF for optimal needle placement would like to state that robot assistance should be thoroughly
and to avoid complications. For the same reason in some evaluated for other CT-guided interventions like biopsies or
cases, ultrasound may be a discussable alternative but is not other ablation techniques like RFA or IRE to make the best
used in clinical routine in our hospital. MRI-guided ablations of this technique and to minimalize radiation exposure to
may play a more important role in the future but are not patient and physician.
applied in most hospitals because of the high expenditure.
We think that a combination of MRI and CT is very Compliance with ethical standards
important for best evaluation of ablation outcome in short-
term follow-up (after 6 weeks) in tumor patients with often Conflict of interest None.
severe preexisting medical condition. In particular, in these
Ethical standard All procedures performed in studies involving
patients MRI images often show artifacts due to respira- human participants were in accordance with the ethical standards of
tory motion and/or ascites, which makes evaluation of tumor the institutional and/or national research committee and with the 1964
recurrence/incomplete ablation difficult. In our opinion fur- Helsinki declaration and its later amendments or comparable ethical
ther control scans can be performed by MRI only if short-term standards.
follow-up is normal. Informed consent This study was evaluated retrospectively. For this
In the case of robot-assisted ablation, the time-intensive type of study formal consent and institutional review board approval is
manual procedure involving the microwave applicator in the not required by our hospital.
tumor is eliminated. Instead the robotic arm is positioned
automatically and the applicator is placed in apnea in one
continuous movement. However, the preparation of the robot,
the loading of the images and the planning of the access path References
require time. Nevertheless we were able to show that the
1. Lubner MG, Brace CL, Hinshaw JL, Lee FT Jr (2010) Microwave
entire intervention duration—from the creation of the CT
tumor ablation: mechanism of action, clinical results, and devices.
images to the final needle placement—was faster with robot J Vasc Interv Radiol JVIR 21(8 Suppl):S192–S203. doi:10.1016/j.
guidance than in the case of manual puncture alone (18.3 jvir.2010.04.007

123
 Author's personal copy
Int J CARS

2. Shibata T, Niinobu T, Ogata N, Takami M (2000) Microwave coag- 10. Solomon SB, Patriciu A, Bohlman ME, Kavoussi LR, Stoianovici
ulation therapy for multiple hepatic metastases from colorectal D (2002) Robotically driven interventions: a method of using CT
carcinoma. Cancer 89(2):276–284 fluoroscopy without radiation exposure to the physician. Radiology
3. Tanaka K, Shimada H, Nagano Y, Endo I, Sekido H, Togo S (2006) 225(1):277–282. doi:10.1148/radiol.2251011133
Outcome after hepatic resection versus combined resection and 11. Mbalisike EC, Vogl TJ, Zangos S, Eichler K, Balakrishnan P,
microwave ablation for multiple bilobar colorectal metastases to Paul J (2014) Image-guided microwave thermoablation of hepatic
the liver. Surgery 139(2):263–273. doi:10.1016/j.surg.2005.07.036 tumours using novel robotic guidance: an early experience. Eur
4. Kurumi Y, Tani T, Naka S, Shiomi H, Shimizu T, Abe H, Radiol. doi:10.1007/s00330-014-3398-0
Endo Y, Morikawa S (2007) MR-guided microwave ablation 12. Abdullah BJ, Yeong CH, Goh KL, Yoong BK, Ho GF,
for malignancies. Int J Clin Oncol 12(2):85–93. doi:10.1007/ Yim CC, Kulkarni A (2015) Robotic-assisted thermal abla-
s10147-006-0653-7 tion of liver tumours. Eur Radiol 25(1):246–257. doi:10.1007/
5. Kuang M, Lu MD, Xie XY, Xu HX, Mo LQ, Liu GJ, Xu ZF, Zheng s00330-014-3391-7
YL, Liang JY (2007) Liver cancer: increased microwave deliv- 13. Omary RA, Bettmann MA, Cardella JF, Bakal CW, Schwartzberg
ery to ablation zone with cooled-shaft antenna-experimental and MS, Sacks D, Rholl KS, Meranze SG, Lewis CA (2003) Quality
clinical studies. Radiology 242(3):914–924. doi:10.1148/radiol. improvement guidelines for the reporting and archiving of inter-
2423052028 ventional radiology procedures. J Vasc Interv Radiol JVIR 14(9 Pt
6. Shimada S, Hirota M, Beppu T, Matsuda T, Hayashi N, Tashima S, 2):S293–S295
Takai E, Yamaguchi K, Inoue K, Ogawa M (1998) Complications 14. Prosch H, Stadler A, Schilling M, Burklin S, Eisenhuber E, Schober
and management of microwave coagulation therapy for primary E, Mostbeck G (2012) CT fluoroscopy-guided vs. multislice CT
and metastatic liver tumors. Surg Today 28(11):1130–1137 biopsy mode-guided lung biopsies: accuracy, complications and
7. Kloeckner R, dos Santos DP, Schneider J, Kara L, Dueber C, Pitton radiation dose. Eur J Radiol 81(5):1029–1033. doi:10.1016/j.ejrad.
MB (2013) Radiation exposure in CT-guided interventions. Eur J 2011.01.064
Radiol 82(12):2253–2257. doi:10.1016/j.ejrad.2013.08.035 15. Elias D, Di Pietroantonio D, Gachot B, Menegon P, Hakime A,
8. Rathmann N, Haeusler U, Diezler P, Weiss C, Kostrzewa M, Sadick De Baere T (2006) Liver abscess after radiofrequency ablation of
M, Schoenberg SO, Diehl SJ (2014) Evaluation of radiation expo- tumors in patients with a biliary tract procedure. Gastroenterol Clin
sure of medical staff during CT-guided interventions. J Am Coll Biol 30(6–7):823–827
Radiol JACR. doi:10.1016/j.jacr.2014.04.012
9. Kato R, Katada K, Anno H, Suzuki S, Ida Y, Koga S (1996)
Radiation dosimetry at CT fluoroscopy: physician’s hand dose and
development of needle holders. Radiology 201(2):576–578. doi:10.
1148/radiology.201.2.8888264

123