Eur Radiol (2015) 25:617–623 DOI 10.1007/s00330-014-3449-6
INTERVENTIONAL
Evaluation of percutaneous biopsies of renal masses under MRI-guidance: a retrospective study about 26 cases J. Garnon & A. Schlier & X. Buy & G. Tsoumakidou & M. de Mathelin & E. Breton & A. Gangi
Received: 31 March 2014 / Revised: 11 July 2014 / Accepted: 22 September 2014 / Published online: 15 October 2014 # European Society of Radiology 2014
Abstract Objective To determine whether MRI allows safe and accurate guidance for biopsies of renal masses. Materials and methods Between May 2010 and September 2013, 26 patients (15 men and 11 women) with 26 renal masses underwent MRI-guided percutaneous biopsy. For each patient, we retrospectively collected the epidemiological, procedural and histopathological data. Results Mean size of tumour was 3.6 cm (range 0.6 – 9 cm). Mean procedure time was 48 minutes (range 37 – 70 min). Malignancy was found in the percutaneous samples in 81 % (21/26) of the masses. All these cases were considered as true positive biopsies. Benignity was found in the percutaneous samples in 5/26 (19 %) of the masses but was confirmed only in 3 cases. The other 2 cases included one false negative case and one undetermined biopsy, as patient was lost to follow-up. The sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy of this study were 95.4 %, 100 %, 100 %, 75 % and 96 %, respectively Conclusion MRI-guidance is safe and accurate to target renal masses.
J. Garnon (*) : A. Schlier : G. Tsoumakidou : A. Gangi Department of Interventional Radiology, Nouvel Hôpital Civil, Strasbourg, France e-mail: [email protected] X. Buy Department of Radiology, Institut Bergonié, Bordeaux, France M. de Mathelin : E. Breton : A. Gangi ICube, University of Strasbourg, CNRS, Strasbourg, France
Key Points • Percutaneous interventions can be performed with MRIguidance • MRI offers real-time multiplanar imaging capabilities without radiation • MRI-guidance allows to target renal tumours Keywords Percutaneous biopsy . Renal masses . Interventional MRI . Real-time guidance . MRI guidance Abbreviations MRI magnetic resonance imaging US ultrasound CT computed tomography CBCT cone beam computed tomography SRMs small renal masses NPV negative predictive value PPV positive predictive value TP true positive TN true negative FP false positive FN false negative
Introduction Renal masses are increasingly found incidentally on abdominal imaging performed for other indications [1]. Preoperative histology is usually not required as imaging, especially magnetic resonance imaging (MRI), allows the characterization of most renal masses [2]. However, image-guided biopsies may be performed in some selected cases, such as atypical features on imaging. Moreover, since up to 30 % of small renal masses
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(SRMs) are benign and may have unspecific characteristics on imaging [2, 3], there are more and more publications suggesting that percutaneous biopsies should be performed for tumours measuring less than 4 cm in order to avoid unnecessary surgery [4]. Clinical decision to treat SRMs with ablative therapies may also be impacted by histological results [5]. Percutaneous biopsies of renal masses have a high accuracy for the diagnosis of malignancy (>90 % in most recent studies) [6] and to determine the subtype of tumour [7]. It also has a very low rate of complications [8]. Ultrasound (US) [9], X-ray computed-tomography [10], MRI [11] and cone-beam CT (CBCT) [12] may be used to guide percutaneous biopsies of SRMs with high rates of accuracy. Compared to other imaging modalities, MRI offers high intrinsic soft-tissue contrast and real-time multi-planar imaging capabilities, which is expected to be very useful when targeting SRMs or lesions requiring complex needle paths, tilted relative to system axes. Additionally, MRI is a non-ionizing imaging modality, which is a strong advantage over CT and CBCT. The objective of this retrospective study is to assess the efficacy and safety of MRI-guided percutaneous biopsies of renal masses.
Material and methods Patients All percutaneous MRI-guided biopsies of renal masses performed in the department of interventional imaging between May 2010 and September 2013 were retrospectively reviewed. This study was conducted in accordance with the institutional review board at our hospital. Patients were referred from the departments of urology or oncology for histological diagnosis of renal masses before treatment decision. All masses were predominantly solid, without visible fat on imaging (MRI, US or CT). All patients gave informed consent for the biopsy. They were asked to stop all anticoagulation medications 5 days before the procedure and blood clotting parameters were tested the day before the biopsy. MRI-guidance was used as the firstline imaging modality as we have a dedicated interventional MRI suite (shared by interventional radiologists and scientists), in which most of percutaneous abdominal interventions are performed. All renal biopsies were therefore referred to MRI in first intention without considering the level of difficulty of the procedure. Patients with contra-indications to MRI or those who could not lie down for at least 30 minutes inside the MRI bore were biopsied using either US or CT-guidance and were therefore not included in this study. Procedures Biopsies were performed in a large bore 1.5 Tesla MRI (MAGNETOM Aera, Siemens, Germany) by four different
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interventional radiologists (A.G, X.B, G.T, J.G), each one having at least one year of experience in MR-guided interventions. Patients were positioned in prone or supine position, depending on the localization of the tumour. There was no specific immobilization of the patient. No intravenous or oral medication (such as pain-killer or anxiolytic) was administrated before the biopsy. A free-breath T2-weighted fast spin echo sequence with radial k-space filing (T2 BLADE sequence, TE/TR 178/3420 ms, flip angle 150°, 30 slices, field-of-view 400 mm×400 mm, reconstructed in-plane resolution 2 mm× 2 mm, slice thickness 4 mm, total acquisition time 96 s) was acquired using the body coil in the axial plane in order to localize the lesion, determine the puncture point, plan the needle path, and evaluate the distance between the skin and the renal mass. When the lesion was poorly seen with the body coil alone, and when technically feasible (i.e. the coil could be positioned without covering the puncture site), an 8-element body matrix coil was used in combination with the spine coil to improve image quality. No intravenous contrast agent was injected. After proper skin disinfection and sterile draping, local anaesthesia was administrated to the skin, subcutaneous fat and muscles. A 16G guiding cannula (MRI coaxial puncture needle®, Somatex medical, Teltow, Germany) was inserted in the tumour with the patient lying inside the bore, under real-time MR-fluoroscopic guidance (Fig. 1), using a free-breath interactive, multi-slice balanced SSFP pulse sequence (BEAT-IRTTT sequence, Siemens Corporate Research & Technology, Center for Applied Medical Imaging, Baltimore, MD, USA) (TE/ TR 2.2/5.35 ms, flip angle 50°, field-of-view 400 mm× 400 mm, reconstructed in-plane resolution 1.8 mm × 1.8 mm, slice thickness 4 mm, acquisition time per slice 815 ms). Typically two real-time image planes were manually oriented by the technician in the axis of the needle and orthogonal to each other (Fig. 2). Samplings were done coaxially through the guiding cannula with an 18G semi-automatic needle (MRI biopsy handy®, Somatex medical, Teltow, Germany). Whenever possible, necrotic areas of the tumour were not targeted. Before performing the sampling, precise position of the cutting needle was always checked with either a T2 BLADE sequence or a real-time sequence in the axis of the needle (Fig. 3). Most frequently, 2 samples were taken per tumour. A complementary cyto-aspiration was performed when the samples were fragmented. Track embolization using injection of gelatine sponge (Curaspon®, Curamedical, Assendelft, the Netherlands) through the coaxial needle was used when bleeding was seen in the guiding cannula after the biopsies. Once the needle was removed, another axial T2 sequence was performed to rule out any immediate bleeding. After the procedure, patients stayed under observation in the hospital for one night, as this is the standard of care in our hospital.
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as the greatest axial diameter on pre-procedural imaging performed no more than 2 months before the biopsy (CT or MRI). Tumour location was evaluated on the same examinations and classified as exophytic if more than 50 % of the tumour was visible out of the renal parenchyma, intraparenchymatous if more than 50 % of the tumour was inside the parenchyma and endophytic if more than 50 % of the tumour was in the central part of the kidney. Total duration of the procedure was calculated by reviewing the time between the first (pre-biopsy) and the last (post-biopsy) T2-weighted axial acquisitions. This time includes: T2-weighted planning acquisition, biopsy path planning, patient preparation, needle insertion, biopsies and patient post-operative banding. Regarding histology, a biopsy was defined as true positive (TP) when histopathological examination revealed malignancy (i.e. renal carcinoma, metastasis or lymphoma). A biopsy was considered true negative (TN) when benignity was found on histology and there was no suspicion of malignancy during a follow-up with imaging period of at least 12 months [13], or if benignity was surgically proven. The result of a biopsy was defined as false positive (FP) if histological examination concluded to malignancy on the percutaneous samples, but there was no evidence of malignancy after surgical removal. A biopsy was classified as false negative (FN) if histological examination concluded to benignity, but there was evidence of malignancy on follow-up imaging, or if malignancy was proven after surgical removal.
Fig. 1 a-b: Overview of the MRI suite during a percutaneous renal biopsy a the patient is covered with sterile drapes. The needle is inserted superficially outside the bore b the needle is then advanced under realtime MR fluoroscopy with the patient lying inside the tunnel. The radiologist looks continuously on the screen while he is advancing the needle towards the tumour
Data collection and analysis All epidemiological, radiological and histological data were retrospectively collected for each procedure to determine age, sex, tumour size, tumour location, procedure duration, complications and histological findings. Tumour size was defined Fig. 2 Puncture of a renal mass under real-time guidance using the multi-slice balanced SSFP pulse sequence. The two planes are orthogonal to each other and display both the needle and the mass. Note that MRI-guidance is not limited by a double-angulated approach, as shown in this case.
Results Patients and procedures The study population consisted of 26 patients (15 men and 11 women) with a mean age of 68 years (range 23–89 years). 17 patients were referred for percutaneous biopsy before considering thermal-ablation. Other indications included: suspicion of renal metastasis (n=2), atypical features on MRI (n=3) and need for a histological result before treatment decision (n=4). A total of 9 of the renal masses were located in the right kidney, the other 17 in the left kidney. Mean size of tumour
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Fig. 3 a-b: a 45 man with an intraparenchymatous tumour not visible on US and unenhanced CT. The biopsy was performed under MRI-guidance a an axial T2 BLADE sequence is performed to confirm the proper position of the guiding cannula in the posterior part of the tumour (the guiding cannula was advanced with real-time sequences) b a real-time sequence confirms that the cutting biopsy needle is inside the tumour and that the sample is correctly located
was 3.6 cm (range 0.6 – 9 cm). There were 17 masses measuring less than 4 cm with a mean size of 2.2 cm, and 9 masses measuring more than 4 cm with a mean size of 6 cm. Location of the tumour was exophytic in 14 cases (54 %), intraparenchymatous in 10 cases (38 %) and endophytic in 2 cases (8 %). Access to the tumour was judged difficult in 6 cases, because of the close proximity of the colon (n=2) or the location in the upper pole of the kidney with the need of a steep pathway (n=4). Mean total duration of the MR-guided renal biopsy procedure was 48 minutes (range 37 – 70 min). Technical success rate was 100 %. Data of our study population are shown in Table 1. Histopathological results Malignancy was found in the percutaneous samples in 81 % (21/26) of renal masses. All these cases were considered as true positive biopsies. It included 13 clear renal cell carcinomas, 3 papillary carcinomas, 3 chromophobe carcinomas, and 2 metastasis (one from lung cancer, the other from cholangiocarcinoma). The 9 nodules measuring more than 4 cm were all
Table 1 characteristics of the study population (26 mass Characteristic
Value
Age Male/Female
68 y.o (mean value) 15/11
Right/Left kidney Greatest axial diameter: -all masses -masses 4 cm Location: -Exophytic • 4 cm -Intraparenchymatous • 4 cm Endophytic • 4 cm
9/17 3.6 cm (mean value) 2.2 cm (mean value) 6 cm (mean value) 14 7 7 10 9 1 2 1 1
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malignant. Over the 17 SRMs, 12 (71 %) turned out to be malignant on histology. When biopsy showed renal cell carcinoma (19 cases), consequent therapy decision were 14 percutaneous cryoablations, 2 radical nephrectomies, one systemic therapy with antiangiogenic drug and one watchful waiting. Benignity was found in the percutaneous samples in 19 % (5/26) of the masses, all measuring less than 4 cm. 3 of these lesions (2 oncocytomas and one chronic inflammation) were considered as true negative because follow-up imaging (range: 12 – 18 months) showed stability of the size and aspect of the masses. One case (normal renal parenchyma on histology) was considered as a false negative because the nodule grew up from 1 cm to 1.3 cm on the follow-up MRI at 3 months. The patient, who had a history of Von-HippelLindau disease, underwent percutaneous cryoablation without any histological proof as it was highly suspicious for clear cell carcinoma. The last case (clot) could not be classified as true or false negative because the patient was lost to follow-up just after the biopsy. Thus, neither benignity nor malignancy could be proved and this case could not be included in the statistical analysis. Note that the lesions for both the false negative and the lost-to follow up unconfirmed benign biopsy cases measured 1 and 0.6 cm, respectively. Given all these data, the sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy in this study were 95.4 %, 100 %, 100 %, 75 % and 96 % respectively (Table 2).
Complications There was no complication following the MRI-guided biopsies of renal masses, especially no case of clinically relevant bleeding. No track seeding was observed, neither for patients followed by imaging (with a mean follow-up of 18 months), nor for those who were operated.
Table 2 outcome of MRI-guided percutaneous biopsies of renal masses Lesson type
Histological diagnosis on biopsies
Final diagnosis (based on follow-up imaging or surgery)
Malignant
21
22
-RCC -metastasis Benign -oncocytoma -chronic inflammation -normal renal parenchyma -clot Total
19 2 5 2 1 1 1 26
20 2 3 2 1 0 undetermined 25
Discussion MRI has been used to guide percutaneous interventions for more than 10 years [14]. Since then, several reports outlined the interest of MRI to target lesions in various locations such as the abdominal cavity (especially in the liver) [15] or the breast [16]. However, to our knowledge, there is no publication focusing specifically on the use of MRI to target renal masses. In our institute, we have an easy access to MRI-guidance as there is a dedicated interventional MRI suite. Thus, almost all abdominal biopsies (including kidney) are performed under MRI-guidance except if there is a contra-indication to MRI. Our technical success rate was 100 %: all biopsy procedures led to the collection of biopsy samples. There was no case of patient refusing to continue the procedure because of claustrophobia, which is a well-known cause of premature termination for MRI although it is rare [17]. The absence of claustrophobia related procedure termination was probably favoured by the use of a short and wide bore MRI system. The MRI bore used in this study is 145 cm long and 70 cm large, which allows the physician to manually guide the needle under real-time MR-fluoroscopy with the patient lying inside the tunnel [18, 19]. Open-bore MRI systems are also used in interventional radiology, with very good results [20, 21]. To date, there is no prospective comparison of wide and open-bore MRI systems. Guidance using a standard closed MRI bore has also been reported in the literature [22] but its use seems to be marginal, mainly because of poor spatial access to the patient during the intervention. In this study, there was no immediate or delayed complication, even minor, related to the MRI-guided biopsy procedure. These results are in accordance with those in the literature. The NPV (75 %) is relatively low compared to recent studies but it may be explained by the small size of the group of benign masses (5/26 masses). Sensitivity (95.4 %), PPV (100 %) and accuracy (96 %) are similar to other recent publications using other image guidance modality such as ultrasound [9], CT-scan [23] or CBCT [12]. In our study, the diagnostic accuracy was satisfactory not only for masses with a large diameter (more than 4 cm) but also for SRMs, even the intraparenchymatous ones. This suggests that MRI-guidance is accurate and safe to target renal masses. The precise navigation of MRI-guidance may explain these encouraging results. In diagnostic imaging, MRI is considered superior to US and CT for the evaluation of renal masses [24]. For percutaneous biopsies, the highintrinsic soft tissue contrast resolution of MRI enables to see the masses without the need for intravenous contrast injection, even for lesions that are predominantly intraparenchymatous or endophytic (respectively 38 % and 8 % in this study). This advantage of MRI has already been outlined for liver lesions not visible on ultrasound
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and unenhanced CT-scan [25]. Real-time MRI visualization of the renal mass and the needle in two crosssectional image planes allows to target precisely the tumour and to improve the confidence in the position of the needle tip. Thus, MRI may overcome some known technical difficulties of US-guidance, such as poor visualization of the needle’s tip and/or poor visualization of the tumour [26], especially in corpulent patients. Moreover, cross-sectional images are not limited to axial, coronal or sagittal planes and can be tilted in any direction. This is very useful to target “hard to reach” locations such as the upper pole of the kidney (4 biopsies in our study, all positive), where a double angulated approach is usually necessary. The gantry of the CT-scan can be inclined, but only in the caudo-cranial plane and it is usually limited to 25° maximum, which is not sufficient for steep pathways. CBCT may provide direct guidance for complex, double angulated puncture [12]. However, contrary to MRI, CBCT-guidance requires a complete immobilization of the patient (because of fusion imaging) and does not display the tumour during the puncture. This may lead to non-diagnostic biopsies, especially for SRMs measuring less than 2.5 cm [27]. Finally, another important advantage of MRI-guidance over CT- and CBCT- guidance is the absence of radiation for both the patient and the radiologist. MRI-guidance also presents some drawbacks. Duration of the procedure is longer than for procedures led under CT or US guidance. Preparation is time-consuming and can correspond to up to 60 % of the whole procedure time in liver biopsies [28]. In our study, mean procedure time was 48 minutes, which is in the range of the latest publication that was predominantly evaluating liver biopsies [11]. Interestingly, in our experience, the duration of the first ten procedures (51 minutes on average) is longer than the duration of the other 16 interventions (45 minutes on average). This difference may be explained by the learning curves for both the interventional radiologists and the technicians. Technician’s role is crucial in MRI-guided percutaneous procedures as the technician is constantly adjusting the axis of the real-time images in order to display the needle and the lesion on both cross-sectional planes. Thus, technician’s experience may also strongly influence the duration of the procedure. Magnetic susceptibility induced signal void artefacts around the needle are another drawback of MRI-guidance. Needle artefacts can vary in size from a factor 9 depending on the inclination between the needle and the main magnetic field [11]. Therefore, when targeting lesions measuring 1 cm or less, the lesion “disappears” within the artefact when the needle approaches the tumour. At that point, the position of the needle tip can be more precisely evaluated with the T2-weighted fast spin echo sequence than with the real-time gradient echo sequence, but it should be noted that the accuracy of MRI-guidance is
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probably limited for lesions measuring less than 1 cm. In this study, there was one case of false negative biopsy, for a very small lesion measuring 1 cm, which highlights the limitation of MRI-guidance for accurate biopsies of very small lesions. Finally, procedure cost is a major limiting factor of MRIguidance. To our knowledge, there is no comparison of the cost of a percutaneous core biopsy with US, CT and MRIguidance. However, it has been shown that the cost of MRIguided nerve root injection is twice the cost of the same procedure under CT-guidance [29]. This includes the price of the specific non-ferromagnetic needles (which is higher than for standard needles) but also the costs of the personnel and of the MRI-room occupation. One can assume that this cost ratio is at least the same for renal core biopsy, if not superior. This retrospective study has some limitations. The most important one is the absence of surgical confirmation for the majority of biopsies that revealed malignancy. In our department, most patients are referred for MRI-guided biopsy when surgery is not considered the best therapeutic option, i.e. usually when thermal-ablation is potentially indicated. In this study, when malignancy of a SRM was shown on percutaneous biopsy, patients underwent percutaneous cryoablation in a second session. Thus, no histological evaluation of the surgical specimen was possible. However, the correlation of histological evaluation of renal malignancy and subtype of RCC between percutaneous biopsy and surgical specimen approaches 100 % [7, 12, 30]. The use of immunohistochemical staining methods, which was systematic in this study, has increased the diagnostic precision of percutaneous biopsies [31] and may explain this high correlation rate. We believe that surgical confirmation of the histological results obtained with percutaneous samples would not have substantially changed our results. Finally, one patient with a benign biopsy was lost to follow-up and was therefore not included in the statistical analysis: his inclusion may have modified the statistical analysis (mainly the NPV). In conclusion, this retrospective study in 26 patients shows that MRI is accurate and safe to target renal masses, including small intraparenchymatous lesions. However, the use of MRIguidance for percutaneous biopsy of renal masses may currently stay restricted given its time and its cost. Acknowledgments Authors would like to thank Marion VAZEL for her help in coordinating the clinical study. The scientific guarantor of this publication is Afshin Gangi. 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. This study has received funding by French state funds managed by the ANR within the Investissements d'Avenir programme (Labex CAMI) under reference ANR-11-LABX-0004. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Methodology: retrospective, observational, performed at one institution.
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623 16. Brennan SB (2014) Breast magnetic resonance imaging for the interventionalist: magnetic resonance imaging–guided vacuumassisted breast biopsy. Tech Vasc Interv Radiol 17:40–48 17. Eshed I, Althoff CE, Hamm B, Hermann K-GA (2007) Claustrophobia and premature termination of magnetic resonance imaging examinations. J Magn Reson Imaging JMRI 26:401–404 18. Ahrar K, Ahrar JU, Javadi S et al (2013) Real-time magnetic resonance imaging-guided cryoablation of small renal tumors at 1.5 T. Investig Radiol 48:437–444 19. Stattaus J, Maderwald S, Forsting M et al (2008) MR-guided core biopsy with MR fluoroscopy using a short, wide-bore 1.5-Tesla scanner: feasibility and initial results. J Magn Reson Imaging JMRI 27:1181–1187 20. Miki K, Shimomura T, Yamada H et al (2006) Percutaneous cryoablation of renal cell carcinoma guided by horizontal open magnetic resonance imaging. Int J Urol 13:880–884 21. Fischbach F, Bunke J, Thormann M et al (2011) MR-guided freehand biopsy of liver lesions with fast continuous imaging using a 1.0-T open MRI scanner: experience in 50 patients. Cardiovasc Intervent Radiol 34:188–192 22. Rofsky NM, Yang BM, Schlossberg P et al (1998) MR-guided needle aspiration biopsies of hepatic masses using a closed bore magnet. J Comput Assist Tomogr 22:633–637 23. Schmidbauer J, Remzi M, Memarsadeghi M et al (2008) Diagnostic accuracy of computed tomography-guided percutaneous biopsy of renal masses. Eur Urol 53:1003–1011 24. Kang SK, Kim D, Chandarana H (2011) Contemporary imaging of the renal mass. Curr Urol Rep 12:11–17 25. Schmidt AJ, Kee ST, Sze DY et al (1999) Diagnostic yield of MRguided liver biopsies compared with CT- and US-guided liver biopsies. J Vasc Interv Radiol JVIR 10:1323–1329 26. Krücker J, Xu S, Venkatesan A et al (2011) Clinical utility of realtime fusion guidance for biopsy and ablation. J Vasc Interv Radiol JVIR 22:515–524 27. Kroeze SGC, Huisman M, Verkooijen HM et al (2012) Real-time 3D fluoroscopy-guided large core needle biopsy of renal masses: a critical early evaluation according to the IDEAL recommendations. Cardiovasc Intervent Radiol 35:680–685 28. Hoffmann R, Thomas C, Rempp H et al (2012) Performing MRguided biopsies in clinical routine: factors that influence accuracy and procedure time. Eur Radiol 22:663–671 29. Maurer MH, Schreiter N, de Bucourt M et al (2013) Cost comparison of nerve root infiltration of the lumbar spine under MRI and CT guidance. Eur Radiol 23:1487–1494 30. Lee SW, Lee MH, Yang HJ et al (2013) Experience of ultrasonography-guided percutaneous core biopsy for renal masses. Korean J Urol 54:660–665 31. Reichelt O, Gajda M, Chyhrai A et al (2007) Ultrasound-guided biopsy of homogenous solid renal masses. Eur Urol 52:1421–1426
INTERVENTIONAL
Evaluation of percutaneous biopsies of renal masses under MRI-guidance: a retrospective study about 26 cases J. Garnon & A. Schlier & X. Buy & G. Tsoumakidou & M. de Mathelin & E. Breton & A. Gangi
Received: 31 March 2014 / Revised: 11 July 2014 / Accepted: 22 September 2014 / Published online: 15 October 2014 # European Society of Radiology 2014
Abstract Objective To determine whether MRI allows safe and accurate guidance for biopsies of renal masses. Materials and methods Between May 2010 and September 2013, 26 patients (15 men and 11 women) with 26 renal masses underwent MRI-guided percutaneous biopsy. For each patient, we retrospectively collected the epidemiological, procedural and histopathological data. Results Mean size of tumour was 3.6 cm (range 0.6 – 9 cm). Mean procedure time was 48 minutes (range 37 – 70 min). Malignancy was found in the percutaneous samples in 81 % (21/26) of the masses. All these cases were considered as true positive biopsies. Benignity was found in the percutaneous samples in 5/26 (19 %) of the masses but was confirmed only in 3 cases. The other 2 cases included one false negative case and one undetermined biopsy, as patient was lost to follow-up. The sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy of this study were 95.4 %, 100 %, 100 %, 75 % and 96 %, respectively Conclusion MRI-guidance is safe and accurate to target renal masses.
J. Garnon (*) : A. Schlier : G. Tsoumakidou : A. Gangi Department of Interventional Radiology, Nouvel Hôpital Civil, Strasbourg, France e-mail: [email protected] X. Buy Department of Radiology, Institut Bergonié, Bordeaux, France M. de Mathelin : E. Breton : A. Gangi ICube, University of Strasbourg, CNRS, Strasbourg, France
Key Points • Percutaneous interventions can be performed with MRIguidance • MRI offers real-time multiplanar imaging capabilities without radiation • MRI-guidance allows to target renal tumours Keywords Percutaneous biopsy . Renal masses . Interventional MRI . Real-time guidance . MRI guidance Abbreviations MRI magnetic resonance imaging US ultrasound CT computed tomography CBCT cone beam computed tomography SRMs small renal masses NPV negative predictive value PPV positive predictive value TP true positive TN true negative FP false positive FN false negative
Introduction Renal masses are increasingly found incidentally on abdominal imaging performed for other indications [1]. Preoperative histology is usually not required as imaging, especially magnetic resonance imaging (MRI), allows the characterization of most renal masses [2]. However, image-guided biopsies may be performed in some selected cases, such as atypical features on imaging. Moreover, since up to 30 % of small renal masses
618
(SRMs) are benign and may have unspecific characteristics on imaging [2, 3], there are more and more publications suggesting that percutaneous biopsies should be performed for tumours measuring less than 4 cm in order to avoid unnecessary surgery [4]. Clinical decision to treat SRMs with ablative therapies may also be impacted by histological results [5]. Percutaneous biopsies of renal masses have a high accuracy for the diagnosis of malignancy (>90 % in most recent studies) [6] and to determine the subtype of tumour [7]. It also has a very low rate of complications [8]. Ultrasound (US) [9], X-ray computed-tomography [10], MRI [11] and cone-beam CT (CBCT) [12] may be used to guide percutaneous biopsies of SRMs with high rates of accuracy. Compared to other imaging modalities, MRI offers high intrinsic soft-tissue contrast and real-time multi-planar imaging capabilities, which is expected to be very useful when targeting SRMs or lesions requiring complex needle paths, tilted relative to system axes. Additionally, MRI is a non-ionizing imaging modality, which is a strong advantage over CT and CBCT. The objective of this retrospective study is to assess the efficacy and safety of MRI-guided percutaneous biopsies of renal masses.
Material and methods Patients All percutaneous MRI-guided biopsies of renal masses performed in the department of interventional imaging between May 2010 and September 2013 were retrospectively reviewed. This study was conducted in accordance with the institutional review board at our hospital. Patients were referred from the departments of urology or oncology for histological diagnosis of renal masses before treatment decision. All masses were predominantly solid, without visible fat on imaging (MRI, US or CT). All patients gave informed consent for the biopsy. They were asked to stop all anticoagulation medications 5 days before the procedure and blood clotting parameters were tested the day before the biopsy. MRI-guidance was used as the firstline imaging modality as we have a dedicated interventional MRI suite (shared by interventional radiologists and scientists), in which most of percutaneous abdominal interventions are performed. All renal biopsies were therefore referred to MRI in first intention without considering the level of difficulty of the procedure. Patients with contra-indications to MRI or those who could not lie down for at least 30 minutes inside the MRI bore were biopsied using either US or CT-guidance and were therefore not included in this study. Procedures Biopsies were performed in a large bore 1.5 Tesla MRI (MAGNETOM Aera, Siemens, Germany) by four different
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interventional radiologists (A.G, X.B, G.T, J.G), each one having at least one year of experience in MR-guided interventions. Patients were positioned in prone or supine position, depending on the localization of the tumour. There was no specific immobilization of the patient. No intravenous or oral medication (such as pain-killer or anxiolytic) was administrated before the biopsy. A free-breath T2-weighted fast spin echo sequence with radial k-space filing (T2 BLADE sequence, TE/TR 178/3420 ms, flip angle 150°, 30 slices, field-of-view 400 mm×400 mm, reconstructed in-plane resolution 2 mm× 2 mm, slice thickness 4 mm, total acquisition time 96 s) was acquired using the body coil in the axial plane in order to localize the lesion, determine the puncture point, plan the needle path, and evaluate the distance between the skin and the renal mass. When the lesion was poorly seen with the body coil alone, and when technically feasible (i.e. the coil could be positioned without covering the puncture site), an 8-element body matrix coil was used in combination with the spine coil to improve image quality. No intravenous contrast agent was injected. After proper skin disinfection and sterile draping, local anaesthesia was administrated to the skin, subcutaneous fat and muscles. A 16G guiding cannula (MRI coaxial puncture needle®, Somatex medical, Teltow, Germany) was inserted in the tumour with the patient lying inside the bore, under real-time MR-fluoroscopic guidance (Fig. 1), using a free-breath interactive, multi-slice balanced SSFP pulse sequence (BEAT-IRTTT sequence, Siemens Corporate Research & Technology, Center for Applied Medical Imaging, Baltimore, MD, USA) (TE/ TR 2.2/5.35 ms, flip angle 50°, field-of-view 400 mm× 400 mm, reconstructed in-plane resolution 1.8 mm × 1.8 mm, slice thickness 4 mm, acquisition time per slice 815 ms). Typically two real-time image planes were manually oriented by the technician in the axis of the needle and orthogonal to each other (Fig. 2). Samplings were done coaxially through the guiding cannula with an 18G semi-automatic needle (MRI biopsy handy®, Somatex medical, Teltow, Germany). Whenever possible, necrotic areas of the tumour were not targeted. Before performing the sampling, precise position of the cutting needle was always checked with either a T2 BLADE sequence or a real-time sequence in the axis of the needle (Fig. 3). Most frequently, 2 samples were taken per tumour. A complementary cyto-aspiration was performed when the samples were fragmented. Track embolization using injection of gelatine sponge (Curaspon®, Curamedical, Assendelft, the Netherlands) through the coaxial needle was used when bleeding was seen in the guiding cannula after the biopsies. Once the needle was removed, another axial T2 sequence was performed to rule out any immediate bleeding. After the procedure, patients stayed under observation in the hospital for one night, as this is the standard of care in our hospital.
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as the greatest axial diameter on pre-procedural imaging performed no more than 2 months before the biopsy (CT or MRI). Tumour location was evaluated on the same examinations and classified as exophytic if more than 50 % of the tumour was visible out of the renal parenchyma, intraparenchymatous if more than 50 % of the tumour was inside the parenchyma and endophytic if more than 50 % of the tumour was in the central part of the kidney. Total duration of the procedure was calculated by reviewing the time between the first (pre-biopsy) and the last (post-biopsy) T2-weighted axial acquisitions. This time includes: T2-weighted planning acquisition, biopsy path planning, patient preparation, needle insertion, biopsies and patient post-operative banding. Regarding histology, a biopsy was defined as true positive (TP) when histopathological examination revealed malignancy (i.e. renal carcinoma, metastasis or lymphoma). A biopsy was considered true negative (TN) when benignity was found on histology and there was no suspicion of malignancy during a follow-up with imaging period of at least 12 months [13], or if benignity was surgically proven. The result of a biopsy was defined as false positive (FP) if histological examination concluded to malignancy on the percutaneous samples, but there was no evidence of malignancy after surgical removal. A biopsy was classified as false negative (FN) if histological examination concluded to benignity, but there was evidence of malignancy on follow-up imaging, or if malignancy was proven after surgical removal.
Fig. 1 a-b: Overview of the MRI suite during a percutaneous renal biopsy a the patient is covered with sterile drapes. The needle is inserted superficially outside the bore b the needle is then advanced under realtime MR fluoroscopy with the patient lying inside the tunnel. The radiologist looks continuously on the screen while he is advancing the needle towards the tumour
Data collection and analysis All epidemiological, radiological and histological data were retrospectively collected for each procedure to determine age, sex, tumour size, tumour location, procedure duration, complications and histological findings. Tumour size was defined Fig. 2 Puncture of a renal mass under real-time guidance using the multi-slice balanced SSFP pulse sequence. The two planes are orthogonal to each other and display both the needle and the mass. Note that MRI-guidance is not limited by a double-angulated approach, as shown in this case.
Results Patients and procedures The study population consisted of 26 patients (15 men and 11 women) with a mean age of 68 years (range 23–89 years). 17 patients were referred for percutaneous biopsy before considering thermal-ablation. Other indications included: suspicion of renal metastasis (n=2), atypical features on MRI (n=3) and need for a histological result before treatment decision (n=4). A total of 9 of the renal masses were located in the right kidney, the other 17 in the left kidney. Mean size of tumour
620
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Fig. 3 a-b: a 45 man with an intraparenchymatous tumour not visible on US and unenhanced CT. The biopsy was performed under MRI-guidance a an axial T2 BLADE sequence is performed to confirm the proper position of the guiding cannula in the posterior part of the tumour (the guiding cannula was advanced with real-time sequences) b a real-time sequence confirms that the cutting biopsy needle is inside the tumour and that the sample is correctly located
was 3.6 cm (range 0.6 – 9 cm). There were 17 masses measuring less than 4 cm with a mean size of 2.2 cm, and 9 masses measuring more than 4 cm with a mean size of 6 cm. Location of the tumour was exophytic in 14 cases (54 %), intraparenchymatous in 10 cases (38 %) and endophytic in 2 cases (8 %). Access to the tumour was judged difficult in 6 cases, because of the close proximity of the colon (n=2) or the location in the upper pole of the kidney with the need of a steep pathway (n=4). Mean total duration of the MR-guided renal biopsy procedure was 48 minutes (range 37 – 70 min). Technical success rate was 100 %. Data of our study population are shown in Table 1. Histopathological results Malignancy was found in the percutaneous samples in 81 % (21/26) of renal masses. All these cases were considered as true positive biopsies. It included 13 clear renal cell carcinomas, 3 papillary carcinomas, 3 chromophobe carcinomas, and 2 metastasis (one from lung cancer, the other from cholangiocarcinoma). The 9 nodules measuring more than 4 cm were all
Table 1 characteristics of the study population (26 mass Characteristic
Value
Age Male/Female
68 y.o (mean value) 15/11
Right/Left kidney Greatest axial diameter: -all masses -masses 4 cm Location: -Exophytic • 4 cm -Intraparenchymatous • 4 cm Endophytic • 4 cm
9/17 3.6 cm (mean value) 2.2 cm (mean value) 6 cm (mean value) 14 7 7 10 9 1 2 1 1
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malignant. Over the 17 SRMs, 12 (71 %) turned out to be malignant on histology. When biopsy showed renal cell carcinoma (19 cases), consequent therapy decision were 14 percutaneous cryoablations, 2 radical nephrectomies, one systemic therapy with antiangiogenic drug and one watchful waiting. Benignity was found in the percutaneous samples in 19 % (5/26) of the masses, all measuring less than 4 cm. 3 of these lesions (2 oncocytomas and one chronic inflammation) were considered as true negative because follow-up imaging (range: 12 – 18 months) showed stability of the size and aspect of the masses. One case (normal renal parenchyma on histology) was considered as a false negative because the nodule grew up from 1 cm to 1.3 cm on the follow-up MRI at 3 months. The patient, who had a history of Von-HippelLindau disease, underwent percutaneous cryoablation without any histological proof as it was highly suspicious for clear cell carcinoma. The last case (clot) could not be classified as true or false negative because the patient was lost to follow-up just after the biopsy. Thus, neither benignity nor malignancy could be proved and this case could not be included in the statistical analysis. Note that the lesions for both the false negative and the lost-to follow up unconfirmed benign biopsy cases measured 1 and 0.6 cm, respectively. Given all these data, the sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy in this study were 95.4 %, 100 %, 100 %, 75 % and 96 % respectively (Table 2).
Complications There was no complication following the MRI-guided biopsies of renal masses, especially no case of clinically relevant bleeding. No track seeding was observed, neither for patients followed by imaging (with a mean follow-up of 18 months), nor for those who were operated.
Table 2 outcome of MRI-guided percutaneous biopsies of renal masses Lesson type
Histological diagnosis on biopsies
Final diagnosis (based on follow-up imaging or surgery)
Malignant
21
22
-RCC -metastasis Benign -oncocytoma -chronic inflammation -normal renal parenchyma -clot Total
19 2 5 2 1 1 1 26
20 2 3 2 1 0 undetermined 25
Discussion MRI has been used to guide percutaneous interventions for more than 10 years [14]. Since then, several reports outlined the interest of MRI to target lesions in various locations such as the abdominal cavity (especially in the liver) [15] or the breast [16]. However, to our knowledge, there is no publication focusing specifically on the use of MRI to target renal masses. In our institute, we have an easy access to MRI-guidance as there is a dedicated interventional MRI suite. Thus, almost all abdominal biopsies (including kidney) are performed under MRI-guidance except if there is a contra-indication to MRI. Our technical success rate was 100 %: all biopsy procedures led to the collection of biopsy samples. There was no case of patient refusing to continue the procedure because of claustrophobia, which is a well-known cause of premature termination for MRI although it is rare [17]. The absence of claustrophobia related procedure termination was probably favoured by the use of a short and wide bore MRI system. The MRI bore used in this study is 145 cm long and 70 cm large, which allows the physician to manually guide the needle under real-time MR-fluoroscopy with the patient lying inside the tunnel [18, 19]. Open-bore MRI systems are also used in interventional radiology, with very good results [20, 21]. To date, there is no prospective comparison of wide and open-bore MRI systems. Guidance using a standard closed MRI bore has also been reported in the literature [22] but its use seems to be marginal, mainly because of poor spatial access to the patient during the intervention. In this study, there was no immediate or delayed complication, even minor, related to the MRI-guided biopsy procedure. These results are in accordance with those in the literature. The NPV (75 %) is relatively low compared to recent studies but it may be explained by the small size of the group of benign masses (5/26 masses). Sensitivity (95.4 %), PPV (100 %) and accuracy (96 %) are similar to other recent publications using other image guidance modality such as ultrasound [9], CT-scan [23] or CBCT [12]. In our study, the diagnostic accuracy was satisfactory not only for masses with a large diameter (more than 4 cm) but also for SRMs, even the intraparenchymatous ones. This suggests that MRI-guidance is accurate and safe to target renal masses. The precise navigation of MRI-guidance may explain these encouraging results. In diagnostic imaging, MRI is considered superior to US and CT for the evaluation of renal masses [24]. For percutaneous biopsies, the highintrinsic soft tissue contrast resolution of MRI enables to see the masses without the need for intravenous contrast injection, even for lesions that are predominantly intraparenchymatous or endophytic (respectively 38 % and 8 % in this study). This advantage of MRI has already been outlined for liver lesions not visible on ultrasound
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and unenhanced CT-scan [25]. Real-time MRI visualization of the renal mass and the needle in two crosssectional image planes allows to target precisely the tumour and to improve the confidence in the position of the needle tip. Thus, MRI may overcome some known technical difficulties of US-guidance, such as poor visualization of the needle’s tip and/or poor visualization of the tumour [26], especially in corpulent patients. Moreover, cross-sectional images are not limited to axial, coronal or sagittal planes and can be tilted in any direction. This is very useful to target “hard to reach” locations such as the upper pole of the kidney (4 biopsies in our study, all positive), where a double angulated approach is usually necessary. The gantry of the CT-scan can be inclined, but only in the caudo-cranial plane and it is usually limited to 25° maximum, which is not sufficient for steep pathways. CBCT may provide direct guidance for complex, double angulated puncture [12]. However, contrary to MRI, CBCT-guidance requires a complete immobilization of the patient (because of fusion imaging) and does not display the tumour during the puncture. This may lead to non-diagnostic biopsies, especially for SRMs measuring less than 2.5 cm [27]. Finally, another important advantage of MRI-guidance over CT- and CBCT- guidance is the absence of radiation for both the patient and the radiologist. MRI-guidance also presents some drawbacks. Duration of the procedure is longer than for procedures led under CT or US guidance. Preparation is time-consuming and can correspond to up to 60 % of the whole procedure time in liver biopsies [28]. In our study, mean procedure time was 48 minutes, which is in the range of the latest publication that was predominantly evaluating liver biopsies [11]. Interestingly, in our experience, the duration of the first ten procedures (51 minutes on average) is longer than the duration of the other 16 interventions (45 minutes on average). This difference may be explained by the learning curves for both the interventional radiologists and the technicians. Technician’s role is crucial in MRI-guided percutaneous procedures as the technician is constantly adjusting the axis of the real-time images in order to display the needle and the lesion on both cross-sectional planes. Thus, technician’s experience may also strongly influence the duration of the procedure. Magnetic susceptibility induced signal void artefacts around the needle are another drawback of MRI-guidance. Needle artefacts can vary in size from a factor 9 depending on the inclination between the needle and the main magnetic field [11]. Therefore, when targeting lesions measuring 1 cm or less, the lesion “disappears” within the artefact when the needle approaches the tumour. At that point, the position of the needle tip can be more precisely evaluated with the T2-weighted fast spin echo sequence than with the real-time gradient echo sequence, but it should be noted that the accuracy of MRI-guidance is
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probably limited for lesions measuring less than 1 cm. In this study, there was one case of false negative biopsy, for a very small lesion measuring 1 cm, which highlights the limitation of MRI-guidance for accurate biopsies of very small lesions. Finally, procedure cost is a major limiting factor of MRIguidance. To our knowledge, there is no comparison of the cost of a percutaneous core biopsy with US, CT and MRIguidance. However, it has been shown that the cost of MRIguided nerve root injection is twice the cost of the same procedure under CT-guidance [29]. This includes the price of the specific non-ferromagnetic needles (which is higher than for standard needles) but also the costs of the personnel and of the MRI-room occupation. One can assume that this cost ratio is at least the same for renal core biopsy, if not superior. This retrospective study has some limitations. The most important one is the absence of surgical confirmation for the majority of biopsies that revealed malignancy. In our department, most patients are referred for MRI-guided biopsy when surgery is not considered the best therapeutic option, i.e. usually when thermal-ablation is potentially indicated. In this study, when malignancy of a SRM was shown on percutaneous biopsy, patients underwent percutaneous cryoablation in a second session. Thus, no histological evaluation of the surgical specimen was possible. However, the correlation of histological evaluation of renal malignancy and subtype of RCC between percutaneous biopsy and surgical specimen approaches 100 % [7, 12, 30]. The use of immunohistochemical staining methods, which was systematic in this study, has increased the diagnostic precision of percutaneous biopsies [31] and may explain this high correlation rate. We believe that surgical confirmation of the histological results obtained with percutaneous samples would not have substantially changed our results. Finally, one patient with a benign biopsy was lost to follow-up and was therefore not included in the statistical analysis: his inclusion may have modified the statistical analysis (mainly the NPV). In conclusion, this retrospective study in 26 patients shows that MRI is accurate and safe to target renal masses, including small intraparenchymatous lesions. However, the use of MRIguidance for percutaneous biopsy of renal masses may currently stay restricted given its time and its cost. Acknowledgments Authors would like to thank Marion VAZEL for her help in coordinating the clinical study. The scientific guarantor of this publication is Afshin Gangi. 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. This study has received funding by French state funds managed by the ANR within the Investissements d'Avenir programme (Labex CAMI) under reference ANR-11-LABX-0004. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Methodology: retrospective, observational, performed at one institution.
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