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European Radiology
ISSN 0938-7994
Eur Radiol
DOI 10.1007/s00330-014-3508-z
Preliminary clinical experience with a
dedicated interventional robotic system
for CT-guided biopsies of lung lesions: a
comparison with the conventional manual
technique
Michele Anzidei, Renato Argirò, Andrea
Porfiri, Fabrizio Boni, Marco Anile,
Fulvio Zaccagna, Domenico Vitolo, Luca
Saba, et al.
1 23
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INTERVENTIONAL
Preliminary clinical experience with a dedicated
interventional robotic system for CT-guided biopsies of lung
lesions: a comparison with the conventional manual technique
Michele Anzidei &Renato Argirò &Andrea Porfiri &Fabrizio Boni &Marco Anile &
Fulvio Zaccagna &Domenico Vitolo &Luca Saba &Alessandro Napoli &Andrea Leonardi &
Flavia Longo &Federico Venuta &Mario Bezzi &Carlo Catalano
Received: 22 May 2014 /Revised: 24 September 2014 /Accepted: 14 November 2014
#European Society of Radiology 2014
Abstract
Objective Evaluate the performance of a robotic system for
CT-guided lung biopsy in comparison to the conventional
manual technique.
Materials and methods One hundred patients referred for CT-
guided lung biopsy were randomly assigned to group A
(robot-assisted procedure) or group B (conventional proce-
dure). Size, distance from entry point and position in lung of
target lesions were evaluated to assess homogeneity differ-
ences between the two groups. Procedure duration, dose
length product (DLP), precision of needle positioning, diag-
nostic performance of the biopsy and rate of complications
were evaluated to assess the clinical performance of the ro-
botic system as compared to the conventional technique.
Results All biopsies were successfully performed. The size
(p=0.41), distance from entry point (p= 0.86) and position in
lung (p=0.32) of target lesions were similar in both groups
(p=0.05). Procedure duration and radiation dose were signif-
icantly reduced in group A as compared to group B (p=
0.001). Precision of needle positioning, diagnostic perfor-
mance of the biopsy and rate of complications were similar
in both groups (p=0.05).
Conclusion Robot-assisted CT-guided lung biopsy can be
performed safely and with high diagnostic accuracy, reducing
procedure duration and radiation dose in comparison to the
conventional manual technique.
Key Points
•CT-guided biopsy is the main procedure to obtain diagnosis
in lung tumours.
•The robotic device facilitates percutaneous needle place-
ment under CT guidance.
•Robot-assisted CT-guided lung biopsy reduces procedure
duration and radiation dose.
Keywords Robot .Lung biopsy .Lung cancer .
CT-guidance .Interventional radiology
Introduction
CT-guided lung biopsy is the procedure of choice to obtain
diagnoses in patients with pulmonary lesions suggestive of
malignancy at imaging [1–3]. Following the recent advances
in targeted therapies, biopsy of unresectable lung lesions has
also become necessary in order to assess genetic mutations in
unresectable non-small cell cancers (NSCLC), with core bi-
opsy usually being preferred to aspiration cytology owing to
the larger specimens made available for molecular analysis
[4]. CT-guided lung biopsy can be performed either with the
step-and-shoot or the fluoroscopic technique: the step-and-
M. Anzidei (*):R. Argirò :A. Porfiri :F. Boni :F. Zaccagna :
A. Napoli :A. Leonardi :M. Bezzi :C. Catalano
Department of Radiological, Oncological and Anatomopathological
Sciences - Radiology –Sapienza, University of Rome, Viale Regina
Elena 324, 00161 Rome, Italy
e-mail: michele.anzidei@gmail.com
M. Anile :F. Venu t a
Department of Thoracic Surgery –Sapienza, University of Rome,
Rome, Italy
D. Vitolo
Department of Radiological, Oncological and Anatomopathological
Sciences - Pathology –Sapienza, University of Rome, Rome, Italy
L. Saba
Department of Radiology, Azienda Ospedaliero Universitaria
(A.O.U.), di Cagliari-Polo di Monserrato, Monserrato, Italy
F. Lo n g o
Department of Radiological, Oncological and Anatomopathological
Sciences - Oncology –Sapienza, University of Rome, Rome, Italy
Eur Radiol
DOI 10.1007/s00330-014-3508-z
Author's personal copy
shoot approach is preferred in larger, non-moving lesions,
while CT-fluoroscopy is more advantageous when targeting
smaller lesions or nodules in the lower lobes that are suscep-
tible to respiratory motion [5]. Both procedures have technical
limitations that should be taken into consideration; in partic-
ular the step-and-shoot technique is based on the operator’s
subjective assessment of needle path and positioning and may
result in increased procedure duration and complication rate,
whereas CT-fluoroscopy is significantly faster and more pre-
cise but significantly raises radiation dose to both operator and
patient [6,7]. Various assisting technologies have been pro-
posed in order to increase the diagnostic accuracy and reduce
the duration of CT-guided biopsies, including external laser
targeting [8] and augmented reality (i.e. with a live indirect
view of anatomy by computer-generated video input) [9].
Dedicated interventional robotic systems that operate under
imaging guidance also became available recently [10].
However, while these systems may theoretically represent an
important step toward the automation of interventional proce-
dures, clinical experience and comparative data with conven-
tional techniques are still lacking or insufficient. The
ROBIO™EX (Perfint Healthcare Pvt. Ltd, Florence, OR,
USA) is a CE approved robotic positioning system that facil-
itates percutaneous needle placement during CT-guided inter-
ventional procedures and that has been successfully tested for
CT-guided biopsy and ablation on phantoms [11] and for
clinical radiofrequency ablation of liver lesions [12]. The
objective of this study was to evaluate the clinical perfor-
mance of this system for CT-guided biopsy of lung lesions
in comparison with the conventional manual technique.
Materials and methods
Patient population and study details
This was a single-centre, double-arm, non-sponsored, pro-
spective study and received the approval of local institution
review board. Between June 2013 and February 2014, 115
patients with previously diagnosed lung lesions suggestive of
malignancy at chest CT, PET-CT or both were referred to the
thoracic surgery department of our tertiary care hospital for
histological characterization. Fifteen patients were excluded
from the study population (three patients refused further diag-
nosis/treatment, in five patients the lesions were characterized
as lung metastases following review of available imaging and
in seven patients diagnosis was obtained with bronchoscopy
and transbronchial biopsy). The remaining 100 patients (63
male, 37 female, age range 48–88 years, mean age 65 ±4 years)
were referred for CT-guided lung biopsy and randomly
assigned to group A (robot-assisted procedure) or group B
(conventional procedure). All enrolled patients gave their
written informed consent to participation after being
thoroughly informed of the benefits and potential risks of the
procedure.
Pre-procedure
All procedures were performed by the same radiologist (MA,
8 years of experience in CT-guided interventions, including
more than 300 lung biopsies) on a 128-MDCT dual-source
scanner (Somatom Definition, Siemens, Erlangen, Germany).
A standard inspiratory breath-hold scan of the chest (100 kV,
100 mAs, detector configuration 128×1 mm, slice thickness
1 mm, reconstruction interval 1 mm) was acquired in all cases
prior to biopsy, in order to confirm the presence and to assess
the position of the target lesion. Patients were laid on a
vacuum stabilization mattress and positioned in order to re-
duce at minimum the intrapleural path of the needle, as well as
to avoid critical lung structures (vessels, bronchi and fissures).
Local anaesthesia was performed with 10 mL of 1 % lidocaine
along the projected path of the biopsy needle into the soft
tissues, down to the epipleural space. In all cases an 18-G,
150/200-mm-long modified Menghini end-cutting needle
(SURECUT, TSK Laboratory, Tochigi-Shi, Japan) was used
for tissue sampling. Targeting CT scans were acquired with a
low-dose interventional protocol (100 kV, 50 mAs, detector
configuration 128×1 mm, slice thickness 1 mm, reconstruc-
tion interval 1 mm).
Conventional biopsy technique
All conventional biopsies were performed with the step-and-
shoot technique to assess needle positioning and angulation.
The z-axis extension of targeting scans was limited to include
only the needleand the target lesion. A minimum of two scans
(before the pleura and into the lesion) was required to target
lesions adjacent to the chest wall and a minimum of three
scans (before the pleura, midway to the lesion, into the lesion)
was required for deeper lesions. Additional scans and
multiplanar reconstructions were performed in real time when
necessary for needle adjustment. Once the needle tip was in
position, biopsy was performed with a combination of aspira-
tion and push/rotation movements.
Robot-assisted biopsy technique
Positioning and docking of the robotic system were performed
as previously described [11], with the arm and planning con-
sole located to the side of the CT bed (left or right, depending
on the required access) and firmly coupled to ground metal
plates on the floor to ensure stability. A preliminary inspira-
tory breath-hold CT of the chest was performed using a Breath
Hold® respiratory belt coupled to a light sign (Medspira,
Minneapolis, USA) mounted on a flexible arm, in order to
monitor the extent of chest movement and instruct patients to
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maintain and reproduce proper apnoea (Fig. 1). Images were
then exported over a local area network to the ROBIO™EX
workstation for biopsy planning. The centre of the target
lesion and the entry point on the skin were determined by
the operator, while the angulations of the needle, the depth of
the target and the needle path were automatically calculated by
the workstation and displayed in real time (Fig. 2). Each
parameter was readily modifiable by the operator in order to
avoid critical structures, such as ribs, bronchi and vessels.
Once the plan was confirmed, the CT table was moved to
the coordinates displayed on the workstation and the robotic
arm was activated and positioned for biopsy execution. A
plastic holder with a disposable bush was placed at the end
effector of the robotic arm to guide needle insertion.
Subsequently, the needle was manually inserted through the
chest wall directly into the lesion in a single pass, while the
patient maintained breath-hold to the same extent as that of the
initial positioning CT scan, guided by the light sign coupled to
the respiratory belt. After decoupling the needle from the end
effector and retraction of the robotic arm, needle positioning
was confirmed with a further CT scan (Figs. 3and 4)and
adjustments were performed if required. Biopsy was then
performed similarly to the conventional approach.
Data analysis
The homogeneity assessment of the two groups included
evaluation of the size, distance from entry point and position
in lung of target lesions. The size and distance from entry
point were compared between the two groups with the un-
paired sample ttest. Differences in the location (according to
lobar anatomy) of target lesions between the two groups were
assessed with the Mann–Whitney Utest.
In order to demonstrate statistically significant differences
(p<0.01) of clinical and technical performance between the
conventional biopsy approach and the robot-assisted tech-
nique, the following parameters were evaluated in the two
groups:
–Procedure duration (including planning time) and dose
length product (DLP) were compared with the unpaired
sample ttest.
–Number of needle adjustments was compared with the
unpaired sample ttest.
–Planar and craniocaudal deviations of the needle tip from
the planned target were calculated in millimetres and
compared between the two groups with the unpaired
sample ttest. Multiplanar reformatted images were used
for the evaluation of z-axis deviation.
–Orbital and craniocaudal angular deviations at the target
from the projected needle path were calculated in degrees
(°) for robot-assisted biopsies only. Multiplanar
reformatted images were used for the evaluation of
craniocaudal angular deviation.
–Diagnostic performance of the biopsy procedure was
evaluated qualitatively (diagnostic/non-diagnostic sam-
pling) and compared with the Mann–Whitney test.
–The rate of complications in the two groups was evaluat-
ed following the clinical practice guidelines of the Society
of Interventional Radiology [13] (no complications/minor
complications/major complications) and compared with
the Mann–Whitney Utest.
Results
All biopsies were successfully performed under CT guidance
in both groups. Lesions size (p=0.41), distance from entry
point (p=0.86) and lesions location (p=0.32) were similar in
the two groups. Full results of the homogeneity assessment of
the two groups are given in Table 1.
In group A procedure duration was significantly shorter
(p=0.001), DLP was lower (p=0.001) and just occasional
needle adjustments were required as compared to group B
(p=0.000). Planar and craniocaudal deviations of the needle
Fig. 1 Patient preparation. Respiratory belt placed in patients sight (a,
arrow) and coupled to the light sign (b,arrow). The belt registers the
extent of chest movement at each respiratory act and displays this as
coloured dots. More dots light up with wider respiratory movements. The
patients were asked to control their breath during the procedure trying to
avoid lighting of the outer dots
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tip from the planned target were similar in both groups (p=
0.05), while the orbital (transversal on the x-axis) and
craniocaudal (longitudinal on the z-axis) angular deviations
from the projected needle path in robot-assisted biopsies were
2± 1° and 2.5 ±0.5° (Fig. 5). The diagnostic performance of
CT-guided biopsies was similar in the two groups (p=0.05),
with four patients in group A and three patients in group B
Fig. 2 Biopsy planning on the ROBIO™EX workstation. Target lesion
in the lower right lobe at contrast-enhanced CT (a,arrow), surrounded by
atelectasis (a,arrowhead). The entry point on the skin (b,arrow)and
centre of target lesion (c,arrow) are determined by the operator. The
angulations and insertion path of the needle are automatically calculated
by the workstation and displayed in real time
Fig. 3 Needle positioning. Needle in position before insertion (a,arrow).
Needle insertion through the chest wall directly into the lesion in a single
pass (b,arrow). Needle in final position (c,arrow) after detachment from
end effector and retraction of the robotic arm
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requiring re-biopsy due to inadequate quality of the biopsy
sample. The rate of complications was comparable in the two
groups (p=0.05); there were three (6 %) cases of pneumotho-
rax in group A and two (4 %) cases of pneumothorax in group
B requiring chest tube drainage and prolonged hospitalization.
Minor complications (including small pneumothorax not re-
quiring therapy and self-limiting peri-lesional haemorrhages)
occurred in two (4 %) cases in group A and four (7 %) in
group B. Full results of the assessment of the clinical and
technical performance of the two groups are given in Table 2.
Discussion
Imaging-guided interventional techniques currently represent
a fundamental tool in diagnosis and treatment of oncologic
pathologies. Among the various guidance modalities, CT is
the method of choice in the chest region owing to its excellent
spatial and contrast resolution for the visualization of lung
parenchyma, airways and cardiovascular structures that safely
allows biopsy of lung and mediastinal lesions, percutaneous
tube placement and thermal ablation of lung tumours. The
conventional technique for CT-guided interventional proce-
dures requires a trial-and-error method with the step-and-
shoot approach, or the application of a real-time fluoroscopic
monitoring in order to visualize and modify the path of
needles and percutaneous probes. Even if the clinical perfor-
mance of conventional approaches is highly reliable in expert
hands [4–7], these methods present well-known technical
limitations and their successful application depends signifi-
cantly on operators’manual skill and experience. In order to
reduce such operator dependence, several assisting devices
have been developed and tested in clinical practice, including
external laser [8]oroptical[14] targeting systems that project
and/or guide the needle path onto the skin surface, electro-
magnetic tracking with image fusion [15] and augmented
reality system under infrared guidance that display a real-
time simulation of needle movements [9]. Preliminary reports
are encouraging, but it should be noted that the success of
these technologies is highly dependent on the integration
between the assisting software/hardware, the CT system and
the operator, with increased complexity and costs as compared
to conventional techniques. Moreover, with the approaches
mentioned above the dependence on operator experience is
reduced but not completely eliminated, not mentioning the
need for adequate training. On the other hand, the use of
medical robots for surgical or imaging-guided procedures
allows extremely accurate tool guidance with stable access,
leading to increased precision, accuracy and reproducibility in
a variety of applications, including percutaneous ablations,
biopsies, orthopaedic fixture placement, hollow viscera or
solid organ access [10]. While earlier robots required exten-
sive installation and were often cumbersome to operate, being
time consuming and economically disadvantageous [16,17],
more recent systems, such as the ROBIO™EX, require
minimal effort to be mounted and registered to the imaging
Fig. 4 Positioning confirmation after control scan, immediately before
biopsy. Adjacent slices demonstrate overlapping between the planned
needle path (green line) and the actual needle position at the end of
insertion. Robot-assisted biopsy allowed correct sampling of tumour
tissue avoiding atelectasis. Final histological diagnosis was
adenocarcinoma
Tabl e 1 Full results of the homogeneity assessment of the two groups
Parameter Group A Group B pvalue
Lesion size (mm) 40.7±23.9 (range 15–150) 35.5±25 (range 13.5–160) 0.41
Distance from Entry point (mm) 73.1±30.7 (range 20–135) 72.1±21.6 (range 18–117) 0.86
Lesion location (according to lobar anatomy) RUL (n 11) RUL (n 9) 0.32
LUL (n 6) LUL (n 8)
ML (n 3) ML (n 2)
RLL (18) RLL (16)
LLL (12) LLL (15)
Values are expressed as average± standard deviation
RUL right upper lobe, LUL left upper lobe, ML middle lobe, RLL right lower lobe, LLL left lower lobe
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device [11], reducing the complexity of the procedure. Also
the fully automated movement of the robotic arm represents a
relevant advantage that removes the need for manual or joy-
stick adjustments in the pretreatment phase that are necessary
with other devices [18,19] and may further complicate the
clinical workflow. From a clinical point of view, our study
demonstrated in a large patient population that the presented
robotic system facilitates CT-guided lung biopsies, with re-
sults that are substantially in line with previous reports on
biopsies in phantoms [11] and clinical radiofrequency ablation
of liver lesions [12]. It should be considered that, apart from
these two preliminary studies performed with the samerobotic
platform, there is no literature evidence of large clinical series
of robot-assisted CT-guided interventions, in particular for
what regards chest procedures; hence, an indirect comparison
with the performance of different robotic devices is currently
impossible. In our single-centre experience, the precision in
lesion targeting, the diagnostic performance of the biopsy
sampling and the rate of complications in the robot-assisted
procedures were comparable to those of conventional biop-
sies, with accurate needle positioning and very few adjustment
required even in lesions as small as 15 mm, but the use of the
robot significantly reduced procedure duration and radiation
dose in comparison to the unassisted technique. This observa-
tion is particularly relevant, since in our study all procedures
were performed by an operator with previous experience of
more than 300 conventional CT-guided lung biopsies and,
notwithstanding this expertise, significant reduction of proce-
dure duration and radiation dose were in any case obtained in
robot-assisted procedures as compared to the conventional
technique. In this regard, future work should aim to evaluate
when and how operators with different levels of experience
may benefit from robot assistance in daily clinical routine, and
assess potential differences in the clinical performance of
robot-assisted procedures between expert and non-expert
Fig. 5 Biopsy of a deep solitary lung nodule in the right upper lobe. The
maximum transverse diameter of the nodule was 10 mm and its
craniocaudal size was 15 mm. Planning CT demonstrates the desired
needle path and tip positioning (a,arrowhead). Control CT scan after
needle positioning shows a slight angular deviation of the needle tip
resulting in a 1.5-mm deviation from the planned path (b,arrowhead).
Notwithstanding the deviation, biopsy was successfully performed
without further needle adjustments, achieving final histological
diagnosis of adenocarcinoma
Tabl e 2 Full results of the assessment of the clinical and technical performance of the two groups
Parameter Group A Group B pvalue
Procedure duration (min) 20.1±11.3 (range 10–31) 31.4±10.2 (range 18–42) 0.001
DLP (mGy) 324± 114.5 (range 117–386) 541.2±446.8 (range 334–589) 0.001
Number of needle adjustments 2.7± 2.6 (range 1–4) 6± 4 (range 2–12) 0.000
Deviations on the xand yaxes (mm) 2.3± 1.1 (x)2.5±1.5(y) (range 1–8) 3.0± 1.3 (x)2.1±1.6(y)(range2–11) 0.05
Orbital (o) and craniocaudal (c)
deviations (°)
2± 1° (o) 1.5±0.5° (c) N/A N/A
Final diagnosis 18 ADCA, 9 SCC, 6 SCLC, 10 mets,
3benignant
15 ADCA, 10 SCC, 7 SCLC, 14 mets,
1benignant
0.05
4 rebiopsy (1 ADCA, 2 SCC, 1 SCLC) 3 rebiopsy (2 ADCA, 1 SCC)
Complications (%) 10.4 11 0.05
Values are expressed as average± standard deviation
ADCA adenocarcinoma, SCC squamous cell carcinoma, SCLC small cell carcinoma, mets metastases, N/A not acquired
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radiologists. Moreover, even if a dedicated cost-analysis is
currently unavailable, it could be speculated that the use of
interventional robotic systems will be probably even more
beneficial in clinical settings in which financial resources or
time for appropriate training of interventional radiologists is
lacking, pushing less expert, non-interventional operators to
perform simple imaging-guided procedures. Even if these
preliminary results are encouraging, this study has some lim-
itations. First, the sample size was not determined in advance
with a power analysis in order to increase the relevance of the
statistical evaluation. Moreover, a statistical subanalysis based
on the anatomic characteristics of the target lesions (size,
distance to pleura and position in lung) was not performed;
hence we cannot provide clustered data on system perfor-
mance for the biopsy of smaller and hardly accessible lesions,
which should be the ideal target for robot-assisted procedures.
Last, an independent evaluation of the status of the lung
parenchyma surrounding the target lesions was not available
in order to assess the influence of local pulmonary factors
(emphysema, fibrosis, bronchiectases) on the rate of compli-
cations in the two groups, even if this parameter was probably
not influential, since our complication rates do not differ from
those reported in the literature [4–7]. Notwithstanding these
limitations, the results of our study demonstrate that robot-
assisted CT-guided lung biopsy is a safe and accurate inter-
ventional technique that can reduce procedure duration and
radiation dose in comparison to the conventional manual
approach even in expert hands. Further studies are needed to
confirm these data and to evaluate the performance of robot-
assisted interventional procedures in other clinical scenarios.
Acknowledgments The scientific guarantor of this publication is Dr.
Michele Anzidei. 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. The authors state that this work has not
received any funding. Dr. Fulvio Zaccagna kindly provided statistical
advice for this manuscript. Institutional review board approval was ob-
tained. Written informed consent was obtained from all subjects (patients)
in this study. No study subjects or cohorts have been previously reported.
Methodology: prospective, randomised controlled trial, performed at one
institution.
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