Cardiovasc Intervent Radiol DOI 10.1007/s00270-014-0870-9
CLINICAL INVESTIGATION
Percutaneous Bone Biopsies: Comparison between Flat-Panel Cone-Beam CT and CT-Scan Guidance Lambros Tselikas • Julien Joskin • Florian Roquet • Geoffroy Farouil • Serge Dreuil • Antoine Hakime´ • Christophe Teriitehau • Anne Auperin Thierry de Baere • Frederic Deschamps
•
Received: 19 December 2013 / Accepted: 27 January 2014 Ó Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2014
Abstract Purpose This study was designed to compare the accuracy of targeting and the radiation dose of bone biopsies performed either under fluoroscopic guidance using a conebeam CT with real-time 3D image fusion software (FPCBCT-guidance) or under conventional computed tomography guidance (CT-guidance). Methods Sixty-eight consecutive patients with a bone lesion were prospectively included. The bone biopsies were scheduled under FP-CBCT-guidance or under CT-guidance according to operating room availability. Thirty-four patients underwent a bone biopsy under FPCBCT and 34 under CT-guidance. We prospectively compared the two guidance modalities for their technical success, accuracy, puncture time, and pathological success rate. Patient and physician radiation doses also were compared. Results All biopsies were technically successful, with both guidance modalities. Accuracy was significantly better using FP-CBCT-guidance (3 and 5 mm respectively: p = 0.003).
There was no significant difference in puncture time (32 and 31 min respectively, p = 0.51) nor in pathological results (88 and 88 % of pathological success respectively, p = 1). Patient radiation doses were significantly lower with FPCBCT (45 vs. 136 mSv, p \ 0.0001). The percentage of operators who received a dose higher than 0.001 mSv (dosimeter detection dose threshold) was lower with FPCBCT than CT-guidance (27 vs. 59 %, p = 0.01). Conclusions FP-CBCT-guidance for bone biopsy is accurate and reduces patient and operator radiation doses compared with CT-guidance.
L. Tselikas (&) J. Joskin G. Farouil A. Hakime´ C. Teriitehau T. de Baere F. Deschamps Interventional Radiology Department, Gustave Roussy, 114 rue Edouard Vaillant, 94805 Villejuif, France e-mail: [email protected]
F. Deschamps e-mail: [email protected]
Keywords Bone biopsy Guidance modality Cone beam CT CT scan Radiation dose
Introduction Bone tumors are frequent, especially in metastatic disease [1]. Despite the tremendous development of diagnostic
J. Joskin e-mail: [email protected]
F. Roquet A. Auperin Biostatistics Department, Gustave Roussy, 114 rue Edouard Vaillant, 94805 Villejuif, France e-mail: [email protected]
G. Farouil e-mail: [email protected]
A. Auperin e-mail: [email protected]
A. Hakime´ e-mail: [email protected]
S. Dreuil Medical Physics Department, Gustave Roussy, 114 rue Edouard Vaillant, 94805 Villejuif, France e-mail: [email protected]
C. Teriitehau e-mail: [email protected] T. de Baere e-mail: [email protected]
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
imaging [from conventional radiography [2] to computed tomography (CT) scan, magnetic resonance imaging (MRI) and functional and molecular imaging, such as positron emission tomography (PET)–CT [3], or MR spectroscopy [4]], characterization remains nonspecific. Because various treatment options are possible: chemotherapy or local treatment such as cementoplasty, radiofrequency ablation [5], cryoablation [6], external beam or stereotaxic radiotherapy, or focused ultrasound [7], pathological confirmation often is needed. Open bone biopsy was historically considered to be the reference, but since the early 1980s, image-guided biopsies have tended to replace surgery [8, 9]. Although ultrasound can be used for superficial lesions with cortical lysis and fluoroscopy for large tumors of peripheral bones, conventional computed tomography guidance (CT-guidance) has several advantages. As described by Solomon and Silverman [10], imaging in interventional oncology must provide sufficient information to plan the procedure, for intraprocedural targeting, monitoring and control, and for postprocedure assessment. CT-guidance satisfies all of these conditions, but its drawbacks include irradiation to both patient and radiologist [11], restricted workspace, difficulties for double obliquity puncture, and the lack of availability of dedicated CT scans. CT-guidance however is reliable and safe [12], and it has become the ‘‘gold standard,’’ replacing open surgical biopsy. Flat panel cone-beam CT (FP-CBCT) detectors are available in lots of interventional suites and tend to replace conventional CT-scan-guided procedures in many fields of interventional radiology. Initially used in neurovascular procedures [13], threedimensional (3D) real-time fluoroscopy, using image fusion software, can be used to guide most image-guided interventions. Recently, vascular [14] and percutaneous [15] procedures have been described in the literature. Previous studies have reported good results for bone biopsies and musculoskeletal procedures under fluoroscopic guidance using a FP-CBCT with real-time 3D image fusion software (FP-CBCT-guidance) [15–18]. Our study compared prospectively the technical success, puncture time, accuracy, pathological success, and radiation exposure during bone biopsies performed either under CTguidance or FP-CBCT-guidance.
Materials and Methods Patients The institutional review board approved this single-center study, and informed consent was obtained from all patients. Sixty-eight consecutive patients, referred for a bone
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biopsy, were included prospectively between December 2011 and July 2012 (Table 1). The bone lesion had to be visible on pre-procedure CT or MRI exam. All patients had a pre-existing history of malignancy. The patient had to be able to lie reasonably still. There were no restrictions in terms of tumor location or size. Patients with a contraindication for percutaneous interventions were excluded, e.g., platelets \50,000/mm3, international normalized ratio superior to 1.5, or an activated partial thromboplastin time exceeding twofold the normal value or impossible interruption of anticoagulant therapy. Procedure, Material, and Technique The pre-procedure imaging files were examinated by an interventional radiologist (GF, FD, or TDB with 7, 11, and 25 years of experience in interventional radiology respectively), and the procedure was scheduled by the medical secretary according to availability of the two operating rooms in the interventional radiology department without any other specific instructions. Bone biopsies were performed under local anesthesia by an interventional radiologist either under CT-guidance in an operating room equipped with a 16-slice multidetector CT scanner (LightSpeed 16, GE Medical Systems, Milwaukee, WI) or under FP-CBCT-guidance in another operating room equipped with a flat panel detector (InnovaTM 4100IQ, GE Healthcare, Chalfont St Giles, UK). All operators worked without distinction in both operative rooms. Biopsies were performed using a core needle bone biopsy set with an 11-gauge coaxial system (BedfordTM, Laurane medical, Le Pradet, France). FP-CBCT-Guidance Protocol Rotational imaging over 200° from lateral to lateral (Right Anterior Oblique 100° to Left Anterior Oblique 100°) was performed in all patients with breath holding, after lifting their arms above the head (Fig. 1). The protocol used had a frame rate of 40° per second during a 5-s rotation, generating 148 projections each. The images were acquired with a field of view (FOV) of 40 cm, without collimation during the C-arm rotation. Three-dimensional reconstructions were done with a matrix of 512 9 512 voxels, covering a cylinder of 23.2 cm in diameter and 23.2 cm in height. Various renderings of the 3D images were performed such as Volume Rendering, Maximum Intensity Projection, and Multi-Planar Reformations, and the bony structures were segmented and saved. On the first CBCT image, needle trajectory was planned using a dedicated guidance-software (TrackVision software and Advantage Workstation Volume Share 4, Chalfont St Giles, UK), where target and skin entry point are manually chosen to create an ideal needle trajectory. Based on this
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance Table 1 Study population flowchart
68 patients included Feasibility analysis n = 68 34 biopsies under FP-CBCT guidance
34 biopsies under CT guidance
- 1 procedure interrupted (Pain, and unable to remain still, before the 1st 3D acquisition)
- 1 control 3D acquisition missing
- 2 software-guidance incorrectly handled (Impossible to compare 3D acquisitions) Biopsy sample were obtained n = 31
Technical success
n = 33
n = 31
Puncture time
n = 33
n = 31
Accuracy
n = 33
n = 33
Pathological success
n = 34
n = 23
Patient irradiation dose
n = 23
n = 33
Operator’s irradiation dose
n = 34
n Number of patients available for analysis
trajectory, the guidance-software automatically computes two optimal projections, for viewing and controlling needle advancement. In the so-called ‘‘Bull-eye’s view,’’ the trajectory is seen en face, appearing thus as a single point on the image, whereas in the ‘‘progress’’ view, the gantry is automatically positioned to place the trajectory perpendicular to the image obtained. This trajectory and the 3D segmented bone volume are then superimposed upon the fluoroscopy on a dedicated monitor and adjusted in real time for all changes in C-arm angulations, FOV or table position, thus invariably providing needle localization when required. Thanks to a specific radiological-like rendering of the bone anatomy available on the fusion software, we were able to assess constantly the registration quality in real time and adjust it when necessary (e.g., after patient movement). Alternating between the ‘‘bull-eye’’ and the ‘‘progress’’ views, we were able to guide the needle up to the target along the needle trajectory. A second FP-CBCT acquisition was then performed to check the needle position in relation to the target. If the needle tip was correctly positioned, the biopsy was performed and the needle was withdrawn. Otherwise, the needle was repositioned and another FP-CBCT acquisition was performed. At least two 3D CBCT acquisitions were
performed during each procedure: one to plan the needle trajectory, and the second to assess the needle position within the lesion before performing the biopsy. CT-Guidance Protocol All procedures were performed with a 16-slice helical multidetector CT scan (Fig. 2). Protocol parameters were: voltage 120 kV, rotation time 0.8 s, spiral pitch 1.375, collimation 20 mm, and tube current modulation (noise index 15, 100–400 mA), a large field of view (FOV), 1.25mm slice width reconstructed every 1.25 mm for helical 3D acquisition; and 120 kV, 1 s, 60 mA, 3 slices of 2.5mm thickness reconstructed every 1.25 mm per tube rotation for biopsy mode acquisition. At least two helical acquisitions were performed during each procedure allowing 3D reformations. The first was used to plan the biopsy path using a dedicated workstation (Advantage Workstation 4.5, GE-Healthcare, Chalfont St Giles, UK). The needle trajectory was exported to the interventional suite monitor to be visualized by the operator during the entire procedure without superimposing it onto pre or per-procedural images. Needle insertion and progression were done under sequential scan guidance (SmartStep, GE Medical Systems). This system provides a
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Fig. 1 FP-CBCT-guided biopsy of a lumbar vertebra, with a lytic, ovarian adenocarcinoma, metastasis. A, B Needle trajectory on the first 3D acquisition in axial oblique and sagittal views. C, D Trajectory and bone structure images overlaid (red) with fluoroscopy, showing
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needle placement; on the Bull’s eye (C) and progression views (D). E, F Needle position control using the second 3D acquisition, after registration with the needle planned trajectory
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
Fig. 2 CT scan-guided biopsy of an osteolytic, breast cancer metastasis, of the proximal femur in a 55-year-old woman. A Planned trajectory on the first helical acquisition (axial plan). B In-room monitor: three sequential images (with 50 % overlap) on
the top and image of reference (with the planned trajectory) on the bottom of the screen. C Needle position inside the tumor (control helical acquisition). D Control and planning helical acquisitions after registration showing the planned trajectory and needle position
set of three images for each rotation displayed on an inroom monitor, from superior to inferior with a 50 % overlap among the z-axis. The reference image, with the predefined trajectory is displayed just above these three images. There is an in-room handheld controller to control
scanning and image review parameters and a foot pedal to launch sequential acquisitions. The objective was to reproduce the predefined trajectory. The second helical acquisition was performed after needle placement to assess the position of the needle tip. If
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance Table 2 Patient and lesion characteristics FP-CBCT n = 34
CT-scan n = 34
p value
63 (47–90)
57 (27–89)
0.026a
Male
16 (52 %)
15 (48 %)
0.81b
Female
18 (49 %)
19 (51 %)
7 (58 %)
5 (42 %)
Patient Age (years) Median (range) Sex
Tumor Location Cervical/thoracic Lumbar
0.5b
12 (50 %)
12 (50 %)
Pelvic
7 (37 %)
12 (63 %)
Peripheral
8 (62 %)
5 (38 %)
25 (10–80)
23(10–98)
0.48a
89 (25–150)
87 (35–130)
0.9a
Osteolytic
23 (62 %)
14 (38 %)
0.028b
Sclerotic
11 (35 %)
20 (65 %)
Size (mm) Median (range) Depth (mm) Median (range) Appearance
a
Wilcoxon test
b
v2 test
the position of the needle tip was inside the bone tumor, the biopsy was performed and the needle was withdrawn. If the needle tip was not inside the bone tumor, the needle was repositioned and another 3D acquisition was performed. Data Collection and Analysis We prospectively collected patient characteristics (age/ gender), bone tumor characteristics: size, depth, location (cervical/thoracic, lumbar, pelvic or peripheral), and the predominantly lytic or sclerotic appearance (Table 2). We have evaluated the technical success, puncture time, accuracy, pathological success, and the radiation dose to the patient and to the operator during bone tumor biopsies. Technical success was achieved when the needle tip was successfully placed inside the bone tumor targeted for biopsy, on the final 3D control acquisition. The puncture time was defined as the time between the first and the last 3D acquisition. Accuracy was defined as the maximal distance between the tip of the needle on the last 3D acquisition and the target point defined on the first 3D or helical acquisition, after semiautomatic rigid registration (ADW 4.5, GE-Healthcare). For this purpose, two radiologists (LT and JJ with 5 and 6 years of experience in interventional radiology respectively) measured and consensually agreed upon the distance between the needle tip
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Fig. 3 Accuracy measures: the maximal distance (red line) between the needle tip (black dot) and the target point (orange dot) was evaluated on the oblique view. Planned (PT) and needle (NT) trajectory and (a, green), (b, blue) and (c, purple) for maximal error measured on a sagittal, axial, and coronal plan
and the target point, in all three plans (coronal, sagittal, and axial distances) and in a 3D volume (oblique measurement) in order to measure the maximal distance (Fig. 3). Puncture angulation also was reported. We documented the number of punctures performed ‘‘in an axial plane’’ or ‘‘out of plane’’ using both CT and FP-CBCT-guidance. Pathological success was defined as a contributive biopsy for pathological diagnosis compared with inconclusive (nondiagnostic) biopsies. Contributive (diagnostic) biopsies were classified into two groups: malignant (metastasis or malignant primary bone tumor), and nonmalignant (lesions without malignant characteristics; such as pseudotumors, post-radiochemotherapy changes, osteoporosis, or benign primary tumors). Pathological success was evaluated for all procedures when at least one specimen was sampled. Radiation Dose The dose area product (Gy cm2) for FP-CBCT-guidance and the dose length product (mGy cm) for CT-guidance were documented as well as 3D and helical acquisition doses for both modalities. Because no comparison has yet been widely adopted to compare effective doses from FP-
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
Fig. 4 Patient radiation dosimeters placement: 3 thermo-luminescent calibrated dosimeters (TLDs) placed on the same z-axis. Transverse (A) and lateral (B) views
CBCT imaging and conventional CT-scan, dedicated dosimeters were used. Patient radiation dose was evaluated for the last 46 patients (dosimeters were not available for 22 procedures) using 3 thermoluminescent dosimeters TLD (IRSN, Fontenay-aux-Roses, France) per procedure, placed next to the skin entry point and on both right and left side of the patient, along the same z-axis (Fig. 4). The TLDs were calibrated in the French Institute for Radiological protection and Nuclear Safety (IRSN) cobalt-60 reference beam. A correction factor was applied to the dosimeters reading assuming a W80 X-ray beam quality (ISO 4037-3). The radiation dose was measured for each dosimeter. The peak skin dose was considered as the most representative and clinically relevant dose and was used for the statistic analysis. The lowest measurable dose was 50 lGy. The operator radiation dose was measured using operational electronic dosimeters (DMC 2000S, Mirion, MGP instruments, San Ramon, US) under a 0.25-mm lead equivalent apron. Dosimeters were calibrated to register personal dose equivalent Hp(d) at a 10-mm depth, Hp(10), and the lowest effective detectable dose was 1 lSv. The results were analyzed using two classes: an effective dose below or above 0.001 mSv (dosimeter detection limit). Dedicated TLDs ring dosimeters (Mirion, MGP instruments, San Ramon, US), were used to measure hand equivalent dose. The measured quantity was Hp(0.07) and lowest detectable dose was 20 lSv. Due to a ‘‘high detection limit,’’ the same dosimeter was used for each guidance modality for all the procedures. The final dose for the two ring-dosimeters was divided by the number of procedures to obtain a mean dose per procedure. Because the individual dose at each procedure was not recorded, the variability of the dose was unknown and statistical test to compare the dose between the two procedure types was not possible. Complications were reported according to society of interventional radiology (SIR) guidelines [19] for all procedures.
Table 3 Procedure characteristics and results FP-CBCT (n = 31)
CT scan (n = 33)
31/31(100 %)
33/33 (100 %)
32 (16–63)
31 (15–61)
0.51a
3 (1–8)
5 (2–16)
0.003a
(n = 33)
(n = 34)
Malignant Nonmalignant
15 (46 %) 14 (42 %)
19 (56 %) 11 (32 %)
Success
29/33 (82 %)
30/34 (88 %)
Inconclusive
4/33 (12 %)
4/34 (12 %)
Technical success
p univariate
Puncture time (min) Median (range) Accuracy (mm) Median (range) Pathological findings
a
Wilcoxon test
b
Fisher exact test
1.0b
Statistical Analysis Characteristics by patients and tumors were presented as number and percentage for qualitative variables and median and range for quantitative variables. Comparisons between groups were performed with v2 test or Fisher exact test for qualitative variables and with Student t test or Wilcoxon nonparametric test for quantitative variables. For all analyses, a two-sided p value \0.05 was considered statistically significant. Statistical analysis was performed with SAS statistical Software, version 9.2 (Cary, NC).
Results Both groups were similar except for age (patients were significantly older in the group of biopsies performed under FP-CBCT-guidance), and the sclerotic or lytic character of the tumor (biopsies of sclerotic lesions were more frequently performed under CT-scan guidance).
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance Table 4 Patient and operator’s radiation doses during bone biopsies
Patient irradiation
FP-CBCT
CT scan
(n = 23)
(n = 23)
p univariate
Peak skin dose (mGy) (TLD dosimeter)a Median (range) Operator irradiation
45 (17–193)
136 (51–764)
(n = 33)
(n = 34)
\0.0001a
Effective dose (mSv) (operational dosimeter)b \0.001
24/33 (73 %)
14/34 (41 %)
[0.001
9/33 (27 %)
20/34 (59 %)
0.01b
Hand (mSv/procedure) (ring dosimeter) Mean
0.33
0.32
mSv millisievert; mGy milligray a
Wilcoxon test
b
Chi square test
Technical Success, Puncture Time, and Accuracy Thirty-one patients were considered for technical success, puncture time, and accuracy analysis in the FP-CBCTguidance (2 incorrect handling of guidance-software, 1 interrupted procedure for a patient who was unable to stay still because of pain—patient with multiple metastases) and 33 patients for conventional CT-guidance (1 control scan not acquired). The results are summarized in Table 3. All procedures were technically successful. The median puncture time was 31 min using FP-CBCT-guidance and 32 min using CT-guidance (p = 0.51). Cervical and thoracic procedures were significantly longer compared with other bone tumor locations (p = 0.022) using both guiding modalities. Accuracy was significantly better using FP-CBCT compared with CT-guidance: median of 3 versus 5 mm; p = 0.003. No other factor, such as lesion size, location, depth, sclerotic, or lytic appearance, was associated significantly with accuracy. Under FP-CBCT-guidance, 32 % of the puncture were performed ‘‘in the axial plane’’ versus 100 % using CT-guidance (p \ 0.001).
Radiation Dose Patient Irradiation Results of the patient radiation dose analysis were available for 23 patients in the FP-CBCT-guidance group and 23 for the conventional CT-guidance group (Table 4). The peak skin radiation doses, using TLD dosimeters, were significantly lower for FP-CBCT-guidance procedures (median dose: 45 vs. 136 mGy, p \ 0.0001). Lesion characteristics (location, size, depth, sclerotic, or lytic appearance) did not affect the radiation dose. Machine dose indices also were documented. Using FPCBCT-guidance, mean procedure Dose area product (DAP) was 48.6 ± 58.8 Gycm2, of which 26.8 ± 22.8 Gycm2 was attributed to 3D acquisitions. Under CT-guidance mean dose length product (DLP) was 1,289 ± 385 mGycm, and helical acquisitions were responsible for 977 ± 324 mGycm. Operator Irradiation Operator whole body irradiation analyzed for 33 procedures using FP-CBCT-guidance (1 intervention was interrupted due to patient’s pain before any irradiation of the operator), and for all procedures with CT-guidance, was significantly lower using FP-CBCT. The percentage of procedures that demonstrated an operator’s irradiation below the dosimeter detection limit was 73 % using FPCBCT-guidance and 41 % CT-guidance (p = 0.01). Lesions characteristics were not significantly associated with operator irradiation. Operator hand radiation dose reached a mean of 0.332 mSv/procedure with FP-CBCTguidance and 0.319 mSv/procedure using CT-guidance. Complications No major complication occurred for any patient. The procedure was interrupted once in the FP-CBCT group because of pain and the patient’s instability to remain still.
Pathological Results FP-CBCT-guided biopsies were diagnostic in 29 of 33 cases (88 %), when at least 1 sample was obtained (1 procedure was interrupted because of pain) and in 30 of 34 cases (88 %) for CT-guidance (p = 1). Contributive biopsies (when the pathologist was able to make a diagnosis) include 34 malignant lesions (58 %): metastasis or malignant primitive bone tumors, and 25 lesions without malignant characteristics (42 %), such as pseudotumors, post-radiochemotherapy alterations, or benign primitive tumors.
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Discussion Three-dimensional FP-CBCT imaging was initially developed for angiography. More recently such systems have been used for guidance of percutaneous needle interventions [20, 21]. Guiding and fusion software and novel detector technology have increased procedure accuracy, facilitate guidance, and visibility for lesion sampling and tend to reduce irradiation, which is one of medical imaging community’s major concern [22].
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
Due to greater availability, facility of use, real-time fluoroscopy and CT-scan–like imaging combination [18] and a more comfortable workspace, FP-CBCT-guidance is being used increasingly for percutaneous procedures instead of CT-guidance [16]. It has been evaluated for renal [23, 24] and lung [25] biopsies, for thoracic and lumbar vertebroplasty [17] and for percutaneous radiofrequency ablation of osteoid osteomas [26] and hepatocarcinomas [27] with excellent results. However, few studies have compared FP-CBCT-guidance and CT-guidance in terms of accuracy and radiation dose [15, 25, 28–30]. As reported in previous studies [15], feasibility and technical success of FP-CBCT-guidance is excellent. In this study, we demonstrate that FP-CBCT-guidance with real-time 3D image fusion software increases accuracy of bone biopsy compared to CT-guidance. Error distance was less than 1 cm for all procedures, which is consistent with results reported by Tam [17] for CBCTguided vertebroplasty and Leschka et al. series [29]. Thanks to the good visibility of bony structures under X-ray, registration between FP-CBCT images and fluoroscopy is easy to control [20] and to correct when there is a mismatch, due to patient’s movement, in order to increase accuracy. It is interesting to notice that 67 % of FP-CBCT guided puncture-paths were ‘‘out of plane’’ with angulations in z contrarily to CT-guidance where all procedures (100 %) were ‘‘in-plane.’’ Most biopsies are currently performed in an axial plane under CT-guidance for obvious practical reasons, but it does not always correspond to the best access. This is explained by the difficulty to realize puncture with double obliquity using conventional CT-scans, even if gantry angling and recently developed software could improve such approach under CT-guidance. Several studies have report benefits in terms of patient irradiation exposure [30], but results remain controversial [31], without any specific data for operator irradiation exposure. In our study, the radiation dose reduction was significant for both. We chose to compare ‘‘measured’’ as opposed to ‘‘calculated’’ radiation doses, even if calculation methods for the evaluation of the effective dose during needle procedures are widely accepted [21, 32]. A previous study reported an effective dose reduction of 13–42 % for patients having a thoracic needle puncture using CBCT compared with CT scan [28]. In order to be able to compare with other studies, using the ‘‘dose area product (DAP) to the effective dose conversion factor’’ of 0.29 mSv(Gy-1cm-2) described by Suzuki et al. [32], under FP-CBCT-guidance, a mean effective dose per procedure of 14.1 mSv was calculated, which is very close to the radiation doses reported (14.7 mSv for musculoskeletal procedures for Braak et al. [15] series and 19.2 mSv for Leschka et al. [29] study).
Hand irradiation per procedure appears to be similar using both guidance modalities (0.033 mSv per procedure using FP-CBCT and 0.032 using CT guidance), even though it was not possible to compare them statistically. The duration of the guidance procedure is the same as reported by Braak et al. [15] for musculoskeletal procedures (34 min) and shorter than reported by Leschka et al. [29] (58 min). The difference might be explained by the anesthesia procedure (general anesthesia) and the use of a needle biopsy guidance device. The main limitation for the comparison of accuracy was that we could not overlay the predefined biopsy trajectory image with sequential-CT images in the conventional CTguidance group. This image was displayed on the same screen close to the imaging of needle progression. Consequently, the operator had to mentally apply it to the nearly real-time imaging instead of just follow it, as it was with FP-CBCT guidance. Two other potential limitations for the measurement of accuracy were: (1) the artifact caused by the needle-tip could be a source of systematic errors (we systematically measured distances from the center of the artifact to the predefined target); and (2) we used a rigid registration protocol that assumes linear deformation of the whole volume, which is not always the case. We focused our registration on the bone tumor location to minimize this error. Further limitations of our study were: the relatively small number of patient analyzed for ‘‘patient irradiation’’ and the positioning of the TLD dosimeters that measured patient dose. Patient irradiation exposure might be underestimated if the dosimeters were not centered on the correct z-axis in the CT-guidance group, and not in the beam of the FP-CBCT during some parts of the procedure; this was the reason why we decided to compare peak skin doses, using the TLD with the highest value for each procedure. This study confirms previous studies that demonstrated encouraging results for FP-CBCT imaging in interventional oncology. It is now legitimate to perform bone biopsies under FP-CBCT-guidance. Recent detection and postprocessing developments seem promising for the reduction of irradiation exposure using cone-beam-CT or multidetector-CT. Even more revolutionary technics, such as multimodality imaging registration and fusion or novel tracking techniques (electromagnetic, ultra-red, optical), may heighten precision, facilitate the procedure, and reduce patient and physician irradiation exposure [33].
Conclusions FP-CBCT is accurate for bone biopsies and reduces patient and operator radiation doses compared with conventional
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CT-guidance. FP-CBCT should be considered for percutaneous intervention, especially for ‘‘bone procedures.’’ Acknowledgments for editing.
Authors would like to thank Lorna Saint Ange
Conflict of interest L. Tselikas, J. Joskin, G. Farouil, S. Dreuil, A. Hakime´, C. Teriitehau, A. Auperin, T. de Baere, and F. Deschamps have no financial disclosures relative to this study.
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17. Tam AL, Mohamed A, Pfister M et al (2010) C-arm cone beam computed tomography needle path overlay for fluoroscopic guided vertebroplasty. Spine (Phila Pa 1976) 35:1095–1099 18. Pedicelli A, Verdolotti T, Pompucci A et al (2011) Interventional spinal procedures guided and controlled by a 3D rotational angiographic unit. Skelet Radiol 40:1595–1601 19. Cardella JF, Bakal CW, Bertino RE et al (2003) Quality improvement guidelines for image-guided percutaneous biopsy in adults. J Vasc Interv Radiol 14:S227–S230 20. Racadio JM, Babic D, Homan R et al (2007) Live 3D guidance in the interventional radiology suite. AJR Am J Roentgenol 189:W357– W364 21. Tsalafoutas IA, Tsapaki V, Triantopoulou C, Gorantonaki A, Papailiou J (2007) CT-guided interventional procedures without CT fluoroscopy assistance: patient effective dose and absorbed dose considerations. AJR Am J Roentgenol 188:1479–1484 22. Fazel R, Krumholz HM, Wang Y et al (2009) Exposure to lowdose ionizing radiation from medical imaging procedures. N Engl J Med 361:849–857 23. Kroeze SG, Huisman M, Verkooijen HM, van Diest PJ, Ruud Bosch JL, van den Bosch MA (2012) Real-time 3D fluoroscopyguided large core needle biopsy of renal masses: a critical early evaluation according to the IDEAL recommendations. Cardiovasc Intervent Radiol 35:680–685 24. Braak SJ, van Melick HH, Onaca MG, van Heesewijk JP, van Strijen MJ (2012) 3D cone-beam CT guidance, a novel technique in renal biopsy-results in 41 patients with suspected renal masses. Eur Radiol 22:2547–2552 25. Braak SJ, Herder GJ, van Heesewijk JP, van Strijen MJ (2012) Pulmonary masses: initial results of cone-beam CT guidance with needle planning software for percutaneous lung biopsy. Cardiovasc Intervent Radiol 35:1414–1421 26. Busser WM, Hoogeveen YL, Veth RP et al (2011) Percutaneous radiofrequency ablation of osteoid osteomas with use of real-time needle guidance for accurate needle placement: a pilot study. Cardiovasc Intervent Radiol 34:180–183 27. Morimoto M, Numata K, Kondo M et al (2010) C-arm cone beam CT for hepatic tumor ablation under real-time 3D imaging. AJR Am J Roentgenol 194:W452–W454 28. Braak SJ, van Strijen MJ, van Es HW, Nievelstein RA, van Heesewijk JP (2011) Effective dose during needle interventions: cone-beam CT guidance compared with conventional CT guidance. J Vasc Interv Radiol 22:455–461 29. Leschka SC, Babic D, El Shikh S, Wossmann C, Schumacher M, Taschner CA (2011) C-arm cone beam computed tomography needle path overlay for image-guided procedures of the spine and pelvis. Neuroradiology. doi:10.1007/s00234-011-0866-y 30. Strocchi S, Colli V, Conte L (2012) Multidetector CT fluoroscopy and cone-beam CT-guided percutaneous transthoracic biopsy: comparison based on patient doses. Radiat Prot Dosim 151: 162–165 31. Kwok YM, Irani FG, Tay KH, Yang CC, Padre CG, Tan BS (2013) Effective dose estimates for cone beam computed tomography in interventional radiology. Eur Radiol 23:3197–3204 32. Suzuki S, Furui S, Yamaguchi I et al (2009) Effective dose during abdominal three-dimensional imaging with a flat-panel detector angiography system. Radiology 250:545–550 33. Abi Jaoudeh N, Kruecker J, Kadoury S et al (2012) Multimodality image fusion-guided procedures: technique, accuracy, and applications. Cardiovasc Intervent Radiol 35:12
CLINICAL INVESTIGATION
Percutaneous Bone Biopsies: Comparison between Flat-Panel Cone-Beam CT and CT-Scan Guidance Lambros Tselikas • Julien Joskin • Florian Roquet • Geoffroy Farouil • Serge Dreuil • Antoine Hakime´ • Christophe Teriitehau • Anne Auperin Thierry de Baere • Frederic Deschamps
•
Received: 19 December 2013 / Accepted: 27 January 2014 Ó Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2014
Abstract Purpose This study was designed to compare the accuracy of targeting and the radiation dose of bone biopsies performed either under fluoroscopic guidance using a conebeam CT with real-time 3D image fusion software (FPCBCT-guidance) or under conventional computed tomography guidance (CT-guidance). Methods Sixty-eight consecutive patients with a bone lesion were prospectively included. The bone biopsies were scheduled under FP-CBCT-guidance or under CT-guidance according to operating room availability. Thirty-four patients underwent a bone biopsy under FPCBCT and 34 under CT-guidance. We prospectively compared the two guidance modalities for their technical success, accuracy, puncture time, and pathological success rate. Patient and physician radiation doses also were compared. Results All biopsies were technically successful, with both guidance modalities. Accuracy was significantly better using FP-CBCT-guidance (3 and 5 mm respectively: p = 0.003).
There was no significant difference in puncture time (32 and 31 min respectively, p = 0.51) nor in pathological results (88 and 88 % of pathological success respectively, p = 1). Patient radiation doses were significantly lower with FPCBCT (45 vs. 136 mSv, p \ 0.0001). The percentage of operators who received a dose higher than 0.001 mSv (dosimeter detection dose threshold) was lower with FPCBCT than CT-guidance (27 vs. 59 %, p = 0.01). Conclusions FP-CBCT-guidance for bone biopsy is accurate and reduces patient and operator radiation doses compared with CT-guidance.
L. Tselikas (&) J. Joskin G. Farouil A. Hakime´ C. Teriitehau T. de Baere F. Deschamps Interventional Radiology Department, Gustave Roussy, 114 rue Edouard Vaillant, 94805 Villejuif, France e-mail: [email protected]
F. Deschamps e-mail: [email protected]
Keywords Bone biopsy Guidance modality Cone beam CT CT scan Radiation dose
Introduction Bone tumors are frequent, especially in metastatic disease [1]. Despite the tremendous development of diagnostic
J. Joskin e-mail: [email protected]
F. Roquet A. Auperin Biostatistics Department, Gustave Roussy, 114 rue Edouard Vaillant, 94805 Villejuif, France e-mail: [email protected]
G. Farouil e-mail: [email protected]
A. Auperin e-mail: [email protected]
A. Hakime´ e-mail: [email protected]
S. Dreuil Medical Physics Department, Gustave Roussy, 114 rue Edouard Vaillant, 94805 Villejuif, France e-mail: [email protected]
C. Teriitehau e-mail: [email protected] T. de Baere e-mail: [email protected]
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
imaging [from conventional radiography [2] to computed tomography (CT) scan, magnetic resonance imaging (MRI) and functional and molecular imaging, such as positron emission tomography (PET)–CT [3], or MR spectroscopy [4]], characterization remains nonspecific. Because various treatment options are possible: chemotherapy or local treatment such as cementoplasty, radiofrequency ablation [5], cryoablation [6], external beam or stereotaxic radiotherapy, or focused ultrasound [7], pathological confirmation often is needed. Open bone biopsy was historically considered to be the reference, but since the early 1980s, image-guided biopsies have tended to replace surgery [8, 9]. Although ultrasound can be used for superficial lesions with cortical lysis and fluoroscopy for large tumors of peripheral bones, conventional computed tomography guidance (CT-guidance) has several advantages. As described by Solomon and Silverman [10], imaging in interventional oncology must provide sufficient information to plan the procedure, for intraprocedural targeting, monitoring and control, and for postprocedure assessment. CT-guidance satisfies all of these conditions, but its drawbacks include irradiation to both patient and radiologist [11], restricted workspace, difficulties for double obliquity puncture, and the lack of availability of dedicated CT scans. CT-guidance however is reliable and safe [12], and it has become the ‘‘gold standard,’’ replacing open surgical biopsy. Flat panel cone-beam CT (FP-CBCT) detectors are available in lots of interventional suites and tend to replace conventional CT-scan-guided procedures in many fields of interventional radiology. Initially used in neurovascular procedures [13], threedimensional (3D) real-time fluoroscopy, using image fusion software, can be used to guide most image-guided interventions. Recently, vascular [14] and percutaneous [15] procedures have been described in the literature. Previous studies have reported good results for bone biopsies and musculoskeletal procedures under fluoroscopic guidance using a FP-CBCT with real-time 3D image fusion software (FP-CBCT-guidance) [15–18]. Our study compared prospectively the technical success, puncture time, accuracy, pathological success, and radiation exposure during bone biopsies performed either under CTguidance or FP-CBCT-guidance.
Materials and Methods Patients The institutional review board approved this single-center study, and informed consent was obtained from all patients. Sixty-eight consecutive patients, referred for a bone
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biopsy, were included prospectively between December 2011 and July 2012 (Table 1). The bone lesion had to be visible on pre-procedure CT or MRI exam. All patients had a pre-existing history of malignancy. The patient had to be able to lie reasonably still. There were no restrictions in terms of tumor location or size. Patients with a contraindication for percutaneous interventions were excluded, e.g., platelets \50,000/mm3, international normalized ratio superior to 1.5, or an activated partial thromboplastin time exceeding twofold the normal value or impossible interruption of anticoagulant therapy. Procedure, Material, and Technique The pre-procedure imaging files were examinated by an interventional radiologist (GF, FD, or TDB with 7, 11, and 25 years of experience in interventional radiology respectively), and the procedure was scheduled by the medical secretary according to availability of the two operating rooms in the interventional radiology department without any other specific instructions. Bone biopsies were performed under local anesthesia by an interventional radiologist either under CT-guidance in an operating room equipped with a 16-slice multidetector CT scanner (LightSpeed 16, GE Medical Systems, Milwaukee, WI) or under FP-CBCT-guidance in another operating room equipped with a flat panel detector (InnovaTM 4100IQ, GE Healthcare, Chalfont St Giles, UK). All operators worked without distinction in both operative rooms. Biopsies were performed using a core needle bone biopsy set with an 11-gauge coaxial system (BedfordTM, Laurane medical, Le Pradet, France). FP-CBCT-Guidance Protocol Rotational imaging over 200° from lateral to lateral (Right Anterior Oblique 100° to Left Anterior Oblique 100°) was performed in all patients with breath holding, after lifting their arms above the head (Fig. 1). The protocol used had a frame rate of 40° per second during a 5-s rotation, generating 148 projections each. The images were acquired with a field of view (FOV) of 40 cm, without collimation during the C-arm rotation. Three-dimensional reconstructions were done with a matrix of 512 9 512 voxels, covering a cylinder of 23.2 cm in diameter and 23.2 cm in height. Various renderings of the 3D images were performed such as Volume Rendering, Maximum Intensity Projection, and Multi-Planar Reformations, and the bony structures were segmented and saved. On the first CBCT image, needle trajectory was planned using a dedicated guidance-software (TrackVision software and Advantage Workstation Volume Share 4, Chalfont St Giles, UK), where target and skin entry point are manually chosen to create an ideal needle trajectory. Based on this
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance Table 1 Study population flowchart
68 patients included Feasibility analysis n = 68 34 biopsies under FP-CBCT guidance
34 biopsies under CT guidance
- 1 procedure interrupted (Pain, and unable to remain still, before the 1st 3D acquisition)
- 1 control 3D acquisition missing
- 2 software-guidance incorrectly handled (Impossible to compare 3D acquisitions) Biopsy sample were obtained n = 31
Technical success
n = 33
n = 31
Puncture time
n = 33
n = 31
Accuracy
n = 33
n = 33
Pathological success
n = 34
n = 23
Patient irradiation dose
n = 23
n = 33
Operator’s irradiation dose
n = 34
n Number of patients available for analysis
trajectory, the guidance-software automatically computes two optimal projections, for viewing and controlling needle advancement. In the so-called ‘‘Bull-eye’s view,’’ the trajectory is seen en face, appearing thus as a single point on the image, whereas in the ‘‘progress’’ view, the gantry is automatically positioned to place the trajectory perpendicular to the image obtained. This trajectory and the 3D segmented bone volume are then superimposed upon the fluoroscopy on a dedicated monitor and adjusted in real time for all changes in C-arm angulations, FOV or table position, thus invariably providing needle localization when required. Thanks to a specific radiological-like rendering of the bone anatomy available on the fusion software, we were able to assess constantly the registration quality in real time and adjust it when necessary (e.g., after patient movement). Alternating between the ‘‘bull-eye’’ and the ‘‘progress’’ views, we were able to guide the needle up to the target along the needle trajectory. A second FP-CBCT acquisition was then performed to check the needle position in relation to the target. If the needle tip was correctly positioned, the biopsy was performed and the needle was withdrawn. Otherwise, the needle was repositioned and another FP-CBCT acquisition was performed. At least two 3D CBCT acquisitions were
performed during each procedure: one to plan the needle trajectory, and the second to assess the needle position within the lesion before performing the biopsy. CT-Guidance Protocol All procedures were performed with a 16-slice helical multidetector CT scan (Fig. 2). Protocol parameters were: voltage 120 kV, rotation time 0.8 s, spiral pitch 1.375, collimation 20 mm, and tube current modulation (noise index 15, 100–400 mA), a large field of view (FOV), 1.25mm slice width reconstructed every 1.25 mm for helical 3D acquisition; and 120 kV, 1 s, 60 mA, 3 slices of 2.5mm thickness reconstructed every 1.25 mm per tube rotation for biopsy mode acquisition. At least two helical acquisitions were performed during each procedure allowing 3D reformations. The first was used to plan the biopsy path using a dedicated workstation (Advantage Workstation 4.5, GE-Healthcare, Chalfont St Giles, UK). The needle trajectory was exported to the interventional suite monitor to be visualized by the operator during the entire procedure without superimposing it onto pre or per-procedural images. Needle insertion and progression were done under sequential scan guidance (SmartStep, GE Medical Systems). This system provides a
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Fig. 1 FP-CBCT-guided biopsy of a lumbar vertebra, with a lytic, ovarian adenocarcinoma, metastasis. A, B Needle trajectory on the first 3D acquisition in axial oblique and sagittal views. C, D Trajectory and bone structure images overlaid (red) with fluoroscopy, showing
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needle placement; on the Bull’s eye (C) and progression views (D). E, F Needle position control using the second 3D acquisition, after registration with the needle planned trajectory
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
Fig. 2 CT scan-guided biopsy of an osteolytic, breast cancer metastasis, of the proximal femur in a 55-year-old woman. A Planned trajectory on the first helical acquisition (axial plan). B In-room monitor: three sequential images (with 50 % overlap) on
the top and image of reference (with the planned trajectory) on the bottom of the screen. C Needle position inside the tumor (control helical acquisition). D Control and planning helical acquisitions after registration showing the planned trajectory and needle position
set of three images for each rotation displayed on an inroom monitor, from superior to inferior with a 50 % overlap among the z-axis. The reference image, with the predefined trajectory is displayed just above these three images. There is an in-room handheld controller to control
scanning and image review parameters and a foot pedal to launch sequential acquisitions. The objective was to reproduce the predefined trajectory. The second helical acquisition was performed after needle placement to assess the position of the needle tip. If
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance Table 2 Patient and lesion characteristics FP-CBCT n = 34
CT-scan n = 34
p value
63 (47–90)
57 (27–89)
0.026a
Male
16 (52 %)
15 (48 %)
0.81b
Female
18 (49 %)
19 (51 %)
7 (58 %)
5 (42 %)
Patient Age (years) Median (range) Sex
Tumor Location Cervical/thoracic Lumbar
0.5b
12 (50 %)
12 (50 %)
Pelvic
7 (37 %)
12 (63 %)
Peripheral
8 (62 %)
5 (38 %)
25 (10–80)
23(10–98)
0.48a
89 (25–150)
87 (35–130)
0.9a
Osteolytic
23 (62 %)
14 (38 %)
0.028b
Sclerotic
11 (35 %)
20 (65 %)
Size (mm) Median (range) Depth (mm) Median (range) Appearance
a
Wilcoxon test
b
v2 test
the position of the needle tip was inside the bone tumor, the biopsy was performed and the needle was withdrawn. If the needle tip was not inside the bone tumor, the needle was repositioned and another 3D acquisition was performed. Data Collection and Analysis We prospectively collected patient characteristics (age/ gender), bone tumor characteristics: size, depth, location (cervical/thoracic, lumbar, pelvic or peripheral), and the predominantly lytic or sclerotic appearance (Table 2). We have evaluated the technical success, puncture time, accuracy, pathological success, and the radiation dose to the patient and to the operator during bone tumor biopsies. Technical success was achieved when the needle tip was successfully placed inside the bone tumor targeted for biopsy, on the final 3D control acquisition. The puncture time was defined as the time between the first and the last 3D acquisition. Accuracy was defined as the maximal distance between the tip of the needle on the last 3D acquisition and the target point defined on the first 3D or helical acquisition, after semiautomatic rigid registration (ADW 4.5, GE-Healthcare). For this purpose, two radiologists (LT and JJ with 5 and 6 years of experience in interventional radiology respectively) measured and consensually agreed upon the distance between the needle tip
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Fig. 3 Accuracy measures: the maximal distance (red line) between the needle tip (black dot) and the target point (orange dot) was evaluated on the oblique view. Planned (PT) and needle (NT) trajectory and (a, green), (b, blue) and (c, purple) for maximal error measured on a sagittal, axial, and coronal plan
and the target point, in all three plans (coronal, sagittal, and axial distances) and in a 3D volume (oblique measurement) in order to measure the maximal distance (Fig. 3). Puncture angulation also was reported. We documented the number of punctures performed ‘‘in an axial plane’’ or ‘‘out of plane’’ using both CT and FP-CBCT-guidance. Pathological success was defined as a contributive biopsy for pathological diagnosis compared with inconclusive (nondiagnostic) biopsies. Contributive (diagnostic) biopsies were classified into two groups: malignant (metastasis or malignant primary bone tumor), and nonmalignant (lesions without malignant characteristics; such as pseudotumors, post-radiochemotherapy changes, osteoporosis, or benign primary tumors). Pathological success was evaluated for all procedures when at least one specimen was sampled. Radiation Dose The dose area product (Gy cm2) for FP-CBCT-guidance and the dose length product (mGy cm) for CT-guidance were documented as well as 3D and helical acquisition doses for both modalities. Because no comparison has yet been widely adopted to compare effective doses from FP-
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
Fig. 4 Patient radiation dosimeters placement: 3 thermo-luminescent calibrated dosimeters (TLDs) placed on the same z-axis. Transverse (A) and lateral (B) views
CBCT imaging and conventional CT-scan, dedicated dosimeters were used. Patient radiation dose was evaluated for the last 46 patients (dosimeters were not available for 22 procedures) using 3 thermoluminescent dosimeters TLD (IRSN, Fontenay-aux-Roses, France) per procedure, placed next to the skin entry point and on both right and left side of the patient, along the same z-axis (Fig. 4). The TLDs were calibrated in the French Institute for Radiological protection and Nuclear Safety (IRSN) cobalt-60 reference beam. A correction factor was applied to the dosimeters reading assuming a W80 X-ray beam quality (ISO 4037-3). The radiation dose was measured for each dosimeter. The peak skin dose was considered as the most representative and clinically relevant dose and was used for the statistic analysis. The lowest measurable dose was 50 lGy. The operator radiation dose was measured using operational electronic dosimeters (DMC 2000S, Mirion, MGP instruments, San Ramon, US) under a 0.25-mm lead equivalent apron. Dosimeters were calibrated to register personal dose equivalent Hp(d) at a 10-mm depth, Hp(10), and the lowest effective detectable dose was 1 lSv. The results were analyzed using two classes: an effective dose below or above 0.001 mSv (dosimeter detection limit). Dedicated TLDs ring dosimeters (Mirion, MGP instruments, San Ramon, US), were used to measure hand equivalent dose. The measured quantity was Hp(0.07) and lowest detectable dose was 20 lSv. Due to a ‘‘high detection limit,’’ the same dosimeter was used for each guidance modality for all the procedures. The final dose for the two ring-dosimeters was divided by the number of procedures to obtain a mean dose per procedure. Because the individual dose at each procedure was not recorded, the variability of the dose was unknown and statistical test to compare the dose between the two procedure types was not possible. Complications were reported according to society of interventional radiology (SIR) guidelines [19] for all procedures.
Table 3 Procedure characteristics and results FP-CBCT (n = 31)
CT scan (n = 33)
31/31(100 %)
33/33 (100 %)
32 (16–63)
31 (15–61)
0.51a
3 (1–8)
5 (2–16)
0.003a
(n = 33)
(n = 34)
Malignant Nonmalignant
15 (46 %) 14 (42 %)
19 (56 %) 11 (32 %)
Success
29/33 (82 %)
30/34 (88 %)
Inconclusive
4/33 (12 %)
4/34 (12 %)
Technical success
p univariate
Puncture time (min) Median (range) Accuracy (mm) Median (range) Pathological findings
a
Wilcoxon test
b
Fisher exact test
1.0b
Statistical Analysis Characteristics by patients and tumors were presented as number and percentage for qualitative variables and median and range for quantitative variables. Comparisons between groups were performed with v2 test or Fisher exact test for qualitative variables and with Student t test or Wilcoxon nonparametric test for quantitative variables. For all analyses, a two-sided p value \0.05 was considered statistically significant. Statistical analysis was performed with SAS statistical Software, version 9.2 (Cary, NC).
Results Both groups were similar except for age (patients were significantly older in the group of biopsies performed under FP-CBCT-guidance), and the sclerotic or lytic character of the tumor (biopsies of sclerotic lesions were more frequently performed under CT-scan guidance).
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance Table 4 Patient and operator’s radiation doses during bone biopsies
Patient irradiation
FP-CBCT
CT scan
(n = 23)
(n = 23)
p univariate
Peak skin dose (mGy) (TLD dosimeter)a Median (range) Operator irradiation
45 (17–193)
136 (51–764)
(n = 33)
(n = 34)
\0.0001a
Effective dose (mSv) (operational dosimeter)b \0.001
24/33 (73 %)
14/34 (41 %)
[0.001
9/33 (27 %)
20/34 (59 %)
0.01b
Hand (mSv/procedure) (ring dosimeter) Mean
0.33
0.32
mSv millisievert; mGy milligray a
Wilcoxon test
b
Chi square test
Technical Success, Puncture Time, and Accuracy Thirty-one patients were considered for technical success, puncture time, and accuracy analysis in the FP-CBCTguidance (2 incorrect handling of guidance-software, 1 interrupted procedure for a patient who was unable to stay still because of pain—patient with multiple metastases) and 33 patients for conventional CT-guidance (1 control scan not acquired). The results are summarized in Table 3. All procedures were technically successful. The median puncture time was 31 min using FP-CBCT-guidance and 32 min using CT-guidance (p = 0.51). Cervical and thoracic procedures were significantly longer compared with other bone tumor locations (p = 0.022) using both guiding modalities. Accuracy was significantly better using FP-CBCT compared with CT-guidance: median of 3 versus 5 mm; p = 0.003. No other factor, such as lesion size, location, depth, sclerotic, or lytic appearance, was associated significantly with accuracy. Under FP-CBCT-guidance, 32 % of the puncture were performed ‘‘in the axial plane’’ versus 100 % using CT-guidance (p \ 0.001).
Radiation Dose Patient Irradiation Results of the patient radiation dose analysis were available for 23 patients in the FP-CBCT-guidance group and 23 for the conventional CT-guidance group (Table 4). The peak skin radiation doses, using TLD dosimeters, were significantly lower for FP-CBCT-guidance procedures (median dose: 45 vs. 136 mGy, p \ 0.0001). Lesion characteristics (location, size, depth, sclerotic, or lytic appearance) did not affect the radiation dose. Machine dose indices also were documented. Using FPCBCT-guidance, mean procedure Dose area product (DAP) was 48.6 ± 58.8 Gycm2, of which 26.8 ± 22.8 Gycm2 was attributed to 3D acquisitions. Under CT-guidance mean dose length product (DLP) was 1,289 ± 385 mGycm, and helical acquisitions were responsible for 977 ± 324 mGycm. Operator Irradiation Operator whole body irradiation analyzed for 33 procedures using FP-CBCT-guidance (1 intervention was interrupted due to patient’s pain before any irradiation of the operator), and for all procedures with CT-guidance, was significantly lower using FP-CBCT. The percentage of procedures that demonstrated an operator’s irradiation below the dosimeter detection limit was 73 % using FPCBCT-guidance and 41 % CT-guidance (p = 0.01). Lesions characteristics were not significantly associated with operator irradiation. Operator hand radiation dose reached a mean of 0.332 mSv/procedure with FP-CBCTguidance and 0.319 mSv/procedure using CT-guidance. Complications No major complication occurred for any patient. The procedure was interrupted once in the FP-CBCT group because of pain and the patient’s instability to remain still.
Pathological Results FP-CBCT-guided biopsies were diagnostic in 29 of 33 cases (88 %), when at least 1 sample was obtained (1 procedure was interrupted because of pain) and in 30 of 34 cases (88 %) for CT-guidance (p = 1). Contributive biopsies (when the pathologist was able to make a diagnosis) include 34 malignant lesions (58 %): metastasis or malignant primitive bone tumors, and 25 lesions without malignant characteristics (42 %), such as pseudotumors, post-radiochemotherapy alterations, or benign primitive tumors.
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Discussion Three-dimensional FP-CBCT imaging was initially developed for angiography. More recently such systems have been used for guidance of percutaneous needle interventions [20, 21]. Guiding and fusion software and novel detector technology have increased procedure accuracy, facilitate guidance, and visibility for lesion sampling and tend to reduce irradiation, which is one of medical imaging community’s major concern [22].
L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
Due to greater availability, facility of use, real-time fluoroscopy and CT-scan–like imaging combination [18] and a more comfortable workspace, FP-CBCT-guidance is being used increasingly for percutaneous procedures instead of CT-guidance [16]. It has been evaluated for renal [23, 24] and lung [25] biopsies, for thoracic and lumbar vertebroplasty [17] and for percutaneous radiofrequency ablation of osteoid osteomas [26] and hepatocarcinomas [27] with excellent results. However, few studies have compared FP-CBCT-guidance and CT-guidance in terms of accuracy and radiation dose [15, 25, 28–30]. As reported in previous studies [15], feasibility and technical success of FP-CBCT-guidance is excellent. In this study, we demonstrate that FP-CBCT-guidance with real-time 3D image fusion software increases accuracy of bone biopsy compared to CT-guidance. Error distance was less than 1 cm for all procedures, which is consistent with results reported by Tam [17] for CBCTguided vertebroplasty and Leschka et al. series [29]. Thanks to the good visibility of bony structures under X-ray, registration between FP-CBCT images and fluoroscopy is easy to control [20] and to correct when there is a mismatch, due to patient’s movement, in order to increase accuracy. It is interesting to notice that 67 % of FP-CBCT guided puncture-paths were ‘‘out of plane’’ with angulations in z contrarily to CT-guidance where all procedures (100 %) were ‘‘in-plane.’’ Most biopsies are currently performed in an axial plane under CT-guidance for obvious practical reasons, but it does not always correspond to the best access. This is explained by the difficulty to realize puncture with double obliquity using conventional CT-scans, even if gantry angling and recently developed software could improve such approach under CT-guidance. Several studies have report benefits in terms of patient irradiation exposure [30], but results remain controversial [31], without any specific data for operator irradiation exposure. In our study, the radiation dose reduction was significant for both. We chose to compare ‘‘measured’’ as opposed to ‘‘calculated’’ radiation doses, even if calculation methods for the evaluation of the effective dose during needle procedures are widely accepted [21, 32]. A previous study reported an effective dose reduction of 13–42 % for patients having a thoracic needle puncture using CBCT compared with CT scan [28]. In order to be able to compare with other studies, using the ‘‘dose area product (DAP) to the effective dose conversion factor’’ of 0.29 mSv(Gy-1cm-2) described by Suzuki et al. [32], under FP-CBCT-guidance, a mean effective dose per procedure of 14.1 mSv was calculated, which is very close to the radiation doses reported (14.7 mSv for musculoskeletal procedures for Braak et al. [15] series and 19.2 mSv for Leschka et al. [29] study).
Hand irradiation per procedure appears to be similar using both guidance modalities (0.033 mSv per procedure using FP-CBCT and 0.032 using CT guidance), even though it was not possible to compare them statistically. The duration of the guidance procedure is the same as reported by Braak et al. [15] for musculoskeletal procedures (34 min) and shorter than reported by Leschka et al. [29] (58 min). The difference might be explained by the anesthesia procedure (general anesthesia) and the use of a needle biopsy guidance device. The main limitation for the comparison of accuracy was that we could not overlay the predefined biopsy trajectory image with sequential-CT images in the conventional CTguidance group. This image was displayed on the same screen close to the imaging of needle progression. Consequently, the operator had to mentally apply it to the nearly real-time imaging instead of just follow it, as it was with FP-CBCT guidance. Two other potential limitations for the measurement of accuracy were: (1) the artifact caused by the needle-tip could be a source of systematic errors (we systematically measured distances from the center of the artifact to the predefined target); and (2) we used a rigid registration protocol that assumes linear deformation of the whole volume, which is not always the case. We focused our registration on the bone tumor location to minimize this error. Further limitations of our study were: the relatively small number of patient analyzed for ‘‘patient irradiation’’ and the positioning of the TLD dosimeters that measured patient dose. Patient irradiation exposure might be underestimated if the dosimeters were not centered on the correct z-axis in the CT-guidance group, and not in the beam of the FP-CBCT during some parts of the procedure; this was the reason why we decided to compare peak skin doses, using the TLD with the highest value for each procedure. This study confirms previous studies that demonstrated encouraging results for FP-CBCT imaging in interventional oncology. It is now legitimate to perform bone biopsies under FP-CBCT-guidance. Recent detection and postprocessing developments seem promising for the reduction of irradiation exposure using cone-beam-CT or multidetector-CT. Even more revolutionary technics, such as multimodality imaging registration and fusion or novel tracking techniques (electromagnetic, ultra-red, optical), may heighten precision, facilitate the procedure, and reduce patient and physician irradiation exposure [33].
Conclusions FP-CBCT is accurate for bone biopsies and reduces patient and operator radiation doses compared with conventional
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L. Tselikas et al.: Bone biopsies: CBCT vs. CT-scan guidance
CT-guidance. FP-CBCT should be considered for percutaneous intervention, especially for ‘‘bone procedures.’’ Acknowledgments for editing.
Authors would like to thank Lorna Saint Ange
Conflict of interest L. Tselikas, J. Joskin, G. Farouil, S. Dreuil, A. Hakime´, C. Teriitehau, A. Auperin, T. de Baere, and F. Deschamps have no financial disclosures relative to this study.
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