Differences in Radiation Exposure of CT-Guided Percutaneous Manual and Powered Drill Bone Biopsy

Purpose Apart from the commonly applied manual needle biopsy, CT-guided percutaneous biopsies of bone lesions can be performed with battery-powered drill biopsy systems. Due to assumably different radiation doses and procedural durations, the aim of this study is to examine radiation exposure and establish local diagnostic reference levels (DRLs) of CT-guided bone biopsies of different anatomical regions. Methods In this retrospective study, dose data of 187 patients who underwent CT-guided bone biopsy with a manual or powered drill biopsy system performed at one of three different multi-slice CT were analyzed. Between January 2012 and November 2019, a total of 27 femur (A), 74 ilium (B), 27 sacrum (C), 28 thoracic vertebrae (D) and 31 lumbar vertebrae (E) biopsies were included. Radiation exposure was reported for volume-weighted CT dose index (CTDIvol) and dose–length product (DLP). Results CTDIvol and DLP of manual versus powered drill biopsy were (median, IQR): A: 56.9(41.4–128.5)/66.7(37.6–76.2)mGy, 410(203–683)/303(128–403)mGy·cm, B: 83.5(62.1–128.5)/59.4(46.2–79.8)mGy, 489(322–472)/400(329–695)mGy·cm, C: 97.5(71.6–149.2)/63.1(49.1–83.7)mGy, 627(496–740)/404(316–515)mGy·cm, D: 67.0(40.3–86.6)/39.7(29.9–89.0)mGy, 392(267–596)/207(166–402)mGy·cm and E: 100.1(66.5–162.6)/62.5(48.0–90.0)mGy, 521(385–619)/315(240–452)mGy·cm. Radiation exposure with powered drill was significantly lower for ilium and sacrum, while procedural duration was not increased for any anatomical location. Local DRLs could be depicted as follows (CTDIvol/DLP): A: 91 mGy/522 mGy·cm, B: 90 mGy/530 mGy·cm, C: 116 mGy/740 mGy·cm, D: 87 mGy/578 mGy·cm and E: 115 mGy/546 mGy·cm. The diagnostic yield was 82.4% for manual and 89.4% for powered drill biopsies. Conclusion Use of powered drill bone biopsy systems for CT-guided percutaneous bone biopsies can significantly reduce the radiation burden compared to manual biopsy for specific anatomical locations such as ilium and sacrum and does not increase radiation dose or procedural duration for any of the investigated locations. Level of Evidence Level 3.


Introduction
CT-guided percutaneous bone biopsies play a key role for the diagnostic work-up of skeletal lesions such as inflammatory and malignant processes. Compared with standard open biopsy, CT-guided approaches are less invasive and provide a sufficient specimen yield [1][2][3]. Furthermore, CT-guided biopsies have a lower complication rate and are generally well tolerated [4,5]. These procedures can be performed either with a manual approach by placing a bone needle within the skeletal lesion, possibly achieved by hammering technique to perforate the cortical bone, or with a powered drill bone biopsy system such as the commercially available ArrowÒ OnControlÒ powered bone access system. For this battery-powered drill, decreased procedural duration, improved user-friendliness and lower pain perception were reported [6,7]. Furthermore, the powered drill approach provides a higher diagnostic yield for sclerotic lesions [4]. Alongside these benefits of manual and powered drill CT-guided bone biopsies, CT entails a radiation burden and is a high-dose imaging technique, which causes the major part of collective effective dose of all medical imaging [8,9]. While some recent studies reported radiation doses of CT-guided bone biopsies [4,[10][11][12], further detailed dose assessment and comparison between different anatomical regions are needed to optimize radiation protection. Additionally, specific reports of diagnostic reference levels (DRL) are rare [13]. For various indications, DRLs were established to limit radiation exposure of radiological imaging modalities [14]. To compare and evaluate local radiation exposure distributions and optimize radiation protection, 75 th percentiles of dose metric distributions are often used as DRL [15].
The aim of this study was to evaluate the radiation exposure and procedural duration of CT-guided percutaneous manual and powered drill bone biopsies and to establish local DRLs.

Patient Cohort
Between January 2012 and November 2019, dose data of all CT-guided percutaneous bone biopsies at our center were included, which provided full information for dose metrics, precisely reported anatomical location as well as technical and procedural duration information. Patients were identified using the radiological information system (RIS). Following anatomical locations were included: femur, ilium, sacrum, thoracic and lumbar vertebrae. Clinical information was extracted from the report archived in the RIS. Ethical approval for this retrospective singlecenter study was granted by the institutional review board and the requirement to obtain informed consent was waived .

CT Scanners and Biopsy Equipment
All interventions were performed by experienced interventional radiologists at one of three commercially available, modern multi-slice CT scanners: single-source 128-slice SOMATOM Definition AS ? , dual-source 128-slice SOMATOM Definition Flash and dual-source 192-slice SOMATOM Force (all: Siemens Healthineers, Erlangen, Germany). At dual-source CT scanners, only one tube was used. For all scans, the tube voltage was 120 kV and the rotation time 0.5 s. Further technical settings according to CT scanner are shown in Table 1. For manual bone biopsy, commercially available 10-, 11-or 13-gauge bone biopsy needles such as the OstycutÒ bone biopsy needle (Bard, Covington, USA) and other bone biopsy sets (Stryker, Kalamazoo, USA) were used. For battery-powered drill bone biopsy, the ArrowÒ On ControlÒ powered bone access system with attachable 11-gauge biopsy needle (Teleflex, Wayne, USA) was applied, which is a handheld powered drill with electric drive and manual guidance of the drilling channel (Fig. 1).

Definitions
To determine the diagnostic yield of the CT-guided bone biopsies, the pathology reports were checked to see if a diagnosis could be made from the specimen. A biopsy was considered diagnostic if the specimen was eligible for histological evaluation.
To investigate the dose difference between bone biopsies of osteolytic and osteoblastic lesions, the average density of the lesion was determined. An average density below 250 HU was considered osteolytic, above that osteoblastic.
Bone biopsies were divided into superficial and deep biopsies according to the depth of the lesion, which was measured from the skin puncture site to the site of the tip of the biopsy needle or drill bit within the bone lesion. A depth up to 70 mm was considered superficial, above that depth was considered deep.
The assessed procedural duration refers to the period between the start of the intra-procedural, i.e., biopsyguiding sequence with acquisition of the first scan after puncture to its end with successful placement of the biopsy needle in the lesion but before acquisition of the postbiopsy scan for documentation and recording of possible complications.

Bone Biopsy Procedure
First, a prebioptic scan was obtained for biopsy planning. Subsequently, the area of the planned puncture site was locally anesthetized. The manual system contains a disposable biopsy cannula with internal stylet. Intraosseously, the inner stylet was removed and the biopsy needle advanced through the lesion to the desired depth using rotary motion or hammering technique using a mallet. Subsequently, the system was completely removed and the specimen was carefully extruded from the needle using an obturator. The powered drill system includes a handheld reusable electric drill with a sealed lithium-ion battery to which a disposable bone biopsy needle is attached. The drill does not have a hammer function and the attachable 11-gauge biopsy needle is available in a length of 4 or six inches (102 mm or 152 mm) and is coaxial in design with an outer cannula and an inner stylet with a beveled tip [12]. The non-sterile drill was wrapped in a sterile bag prior to biopsy and connected to the biopsy needle via a connector. Once the needle tip was placed immediately in front of the bone lesion, the drill was removed from the connector and the inner stylet was removed from the biopsy needle. The drill was then reconnected and the biopsy needle was used to drill through the bone lesion to the desired depth. The system was then completely removed and the specimen in the biopsy needle was carefully pushed out using the stylet. In both approaches, intermittent biopsy-guiding CT scans were taken for positional control. As soon as the biopsy needle could be delineated intralesionally, the internal stylet was removed and the tissue sample was collected. The biopsy system was then removed and a post-bioptic scan was performed for documentation and to exclude complications.

Dose Assessment
For dose assessment, examination data and dose measurements were extracted from the Digital Imaging and Communications in Medicine (DICOM) header and from the Radiation Dose Structured Report stored in the Picture Archiving and Communication System (PACS). Dose assessments referred to the 32 cm diameter standard polymethyl methacrylate (PMMA) CT dosimetry phantom. Assessed radiation exposure indices were the volumeweighted CT dose index (CTDI vol ) and dose-length product (DLP). Although they do not directly represent the  (right), which was wrapped in a sterile bag prior to biopsy, and an associated disposable 11-gauge 4 inch (102 mm) biopsy needle (center) and an obturator (left) for pushing the specimen out of the needle dose to an individual patient, CTDI vol and DLP quantify the radiation dose output of a CT scanner and may help to ensure lower radiation exposures. DRLs were set at the 75 th percentile of dose distribution. Both the manual and powered drill bone biopsies were performed under CT guidance in step-and-shoot technique. For both approaches, multiple CT scans were needed to monitor the location of the biopsy needle, respectively, the drill tip during the biopsy-guiding scans. All DLP values of the biopsy-guiding scans were added to a total DLP, so that all scans necessary for the biopsy and possibly acquired CT spirals were included in the total DLP. To emphasize the differences of radiation dose contributed to the application of manual versus powered drill bone biopsy system, radiation doses of biopsy-guiding scans were analyzed additionally with exclusion of pre-and post-bioptic scans. Dose assessment was also performed for different subgroups in relation to characteristics of the bone lesions, that is, in terms of density, depth, anatomical location, suspected etiology, and technical parameters such as needle diameter and protocols on CT scanners.

Statistics and Data Analysis
Descriptive statistics were performed using GraphPad Prism 5.01 (GraphPad Software, San Diego, USA). To determine normal distribution Kolmogorov-Smirnov, Shapiro-Wilk and D'Agostino-Pearson test were applied.
Normally distributed data are reported as mean ± standard deviation (SD), non-normally distributed data as median and interquartile range (IQR). Mann-Whitney U test was applied to compare radiation indices between manual and powered drill approaches. Kruskal-Wallis test with Dunn-Bonferroni post hoc test was performed to compare procedural durations and DLP values of manual biopsies with different needle diameters. A p value lower than 0.05 was considered statistically significant.

Patient Cohort
In our retrospective study, 187 patients who underwent a CT-guided percutaneous bone biopsy between January 2012 and November 2019 could be included for evaluation.  (Tables 2 and 3). Similar to the radiation dose distribution of the whole procedure, the major part of median CTDI vol and DLP values as well as IQRs of the biopsy-guiding scans were lower with the powered-drill approach (Fig. 2). Statistical analysis revealed significantly lower CTDI vol for biopsy-guiding scans of powered-drill biopsies of ilium (p \ 0.0001) and sacrum (p = 0.0232). Likewise, radiation exposure in terms of DLP for biopsyguiding sequences was significantly lower for both anatomical regions: ilium (p = 0.0008), sacrum (p = 0.0178). No statistical significant difference was found for other biopsy regions.

Comparison Between Different Protocols on the CT Scanners
Because of the higher tube current product on the SOMATOM Force, a subgroup analysis was performed with all manual versus powered drill biopsies on SOMA-TOM AS ?

Procedural Duration of CT-guided Percutaneous Bone Biopsies
Lowest median procedural duration of the CT-guided bone biopsy with exclusion of pre-and post-bioptic scans was depicted for ilium with 21.0 (IQR 16.6-27.7) minutes, highest for lumbar vertebrae with 23.3 (IQR 17.5-32.1) minutes (Table 4). Comparing manual and powered drill approaches, median procedural durations were between 2.2 (A) and 6.6 min (E) less for powered drill approaches. Nonetheless, Kruskal-Wallis test revealed no significant difference between subgroups (p = 0.512). No significant difference in duration was also found with respect to the density of the bone lesion (p = 0.1477).

Discussion
In this study, the comparison of manual and powered drill CT-guided percutaneous bone biopsies revealed significantly lower radiation exposure for biopsy-guiding scans of ilium and sacrum with a powered drill biopsy system, and radiation exposure indices were also slightly lower for the other evaluated anatomical locations. Furthermore, our study demonstrated that for both osteolytic and osteoblastic bone lesions, as well as for superficial and deep biopsies, radiation exposure was lower with the powered drill system. Hence, further dose reduction in CT-guided bone biopsies is achievable by using powered drill biopsy systems. Furthermore, a slight but not significant decrease in procedural duration could be depicted for the powered drill approaches. Bone biopsies play a key role for several diseases causing skeletal lesions such as infectious or malignant processes [10]. CT guidance is used for biopsies of many anatomical locations within the body as it improves identification of a pathology, enables planning of access route through the body and reduces costs and interventional risks compared with open biopsy [16]. Battery-powered drill bone biopsy systems such as the commercially available ArrowÒ OnControlÒ rotatory drill pose an alternative approach to place a bioptic needle in the desired depth within a skeletal lesion opposed to the manual approach with inserting the needle by manual pressure and hammering technique [7,17]. However, the main objective of a CT-guided percutaneous biopsy, whether using a manual or powered drill biopsy system, is to provide a sufficient amount of biopsy material, and thus the diagnostic yield should be equivalent for both approaches as a matter of priority. In this coherence, several studies reported a sufficient diagnostic yield of both manual and powered drill CT-guided bone biopsies [4,10]. Our results showed that a high diagnostic yield, comparable to other studies, was given for both approaches and was slightly higher for the powered drill biopsies. Nevertheless, differences in radiation burden and procedural duration might optimize patient care and minimize radiation exposure [10]. Therefore, radiation protection aspects of CT-guided bone biopsies are worth to consider. Several studies reported dose assessments: For example, Yang et al. reported radiation exposures with a median DLP of 733 mGyÁcm (IQR 462-1086 mGyÁcm) [11]. Our results, like the study by Lee et al. comparing manual and powered drilling systems (mean ± SD CTDI vol : manual 270 ± 48 mGy, powered drill 164 ± 35 mGy), demonstrated that the radiation exposure was significantly lower with the powered drill approach [12]. In contrast, it also has been reported that radiation exposure was slightly higher with the power drill (DLP 1203 mGyÁcm) than with the manual biopsy system (DLP 971 mGyÁcm) [4].
Various factors such as the anatomical location and etiology of the bone lesion, as well as the choice of biopsy system, influence the diagnostic yield of CT-guided bone biopsies [18][19][20][21]. In this context, different features also influence radiation exposure of the biopsy procedure. For example, densely and sclerotic lesions are more difficult to be attained both with manual needle and powered drill [18,19]. Therefore, more biopsy-guiding CT scans are likely to be required in such cases, increasing the radiation exposure and also procedural duration [10]. Kihira et al. reported radiation exposure of bone biopsies differentiated by density to be higher for manual than for powered drill biopsies with mean DLP values between 752 and 1317 mGyÁcm [10]. In our study, the results demonstrated that the density of a bone lesion, i.e., osteolytic or osteoblastic, had no significant effect on radiation exposure, but the use of the biopsy system did. With regard to an interoperator variability, our study showed no significant differences in the radiation exposures of the bone biopsies. In addition to diagnostic yield and radiation exposure, characteristics of the bone lesion and the biopsy system are also thought to influence procedural duration. Comparable to the results of Cohen et al., our study demonstrated that procedural duration of all evaluated anatomical locations was slightly lower with the powered drill biopsy system, although this time saving was not significant [4]. Although the powered drill approach is reported to offer shorter scanning time for biopsies of densely sclerotic lesions in addition to less specimen artifacts [10,18], no significant difference in procedural duration between biopsies of osteolytic and osteoblastic lesions was observed in our study. Aside from considerations related to radiation exposure and duration, many factors influence the choice of a bone biopsy system such as availability, costs and operator preference [10]. Therefore, not only do local preferences differ with respect to biopsy systems and procedures, but also the radiation exposures of CT examinations can vary significantly by institution [20,21]. Helpful benchmarks for dose monitoring are DRLs which indicate typical ionizing radiation exposure values in a country, region or an institute [22]. Although the establishment of DRLs for CT interventions is more difficult compared to diagnostic examinations due to a wide variation in location and technique, the establishment of DRLs might play a crucial role for dose optimization in interventional radiology. However, not only European and national DRLs for CT-guided bone biopsies are lacking, but also reports of locally established DRLs are rare. Therefore, our local DRLs for CT-guided bone biopsies of the most common anatomical locations might be an another step toward the establishment of national or European DRLs. Limitations of our study are the retrospective design and that there were no equivalent numbers of manual and powered drill biopsies and partly different protocols on the CT scanners. With regard to the CT scanners used, comparison of manual biopsies on SOMATOM Force versus biopsies on SOMATOM AS ? and Flash with same settings showed that DLP values were significantly higher on the SOMATOM Force. Accordingly, comparable settings on all scanners and same number of cases would be a significant optimization factor. Strengths of our study include the detailed dose assessment, which enables detailed evaluation on radiation dose of manual versus powered drill biopsy approaches. Furthermore, several anatomical locations and procedural durations were evaluated.

Conclusion
In conclusion, our study demonstrated that the use of a powered drill bone biopsy system for CT-guided percutaneous bone biopsy can reduce the radiation exposure significantly for specific anatomical locations. For both osteolytic and osteoblastic bone lesions, as well as for superficial and deep biopsies, radiation exposure was lower with the powered drill system. DRLs for CT-guided bone biopsies are needed to optimize radiation protection, and our locally determined DRLs may help as benchmarks.
Funding Open Access funding enabled and organized by Projekt DEAL. This study was not supported by any funding.

Declarations
Conflict of interest D. Bos and J. Haubold were supported as Clinician Scientists and received research grants within the University Medicine Essen Academy (UMEA) program, funded by the German Research Foundation (DFG; Grant FU356/12-1) and the Faculty of Medicine, University of Duisburg-Essen.
Consent for Publication For this type of study, consent for publication is not required.
Ethical Approval All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.
Informed Consent This study has obtained IRB approval from the Faculty of Medicine, University of Duisburg-Essen, and the need for informed consent was waived.
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