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Keywords:

  • prostate MRI;
  • MRI/US fusion;
  • targeted biopsy;
  • MRI/US fusion platforms

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

Prostate MRI is currently the best diagnostic imaging method for detecting PCa. Magnetic resonance imaging (MRI)/ultrasonography (US) fusion allows the sensitivity and specificity of MRI to be combined with the real-time capabilities of transrectal ultrasonography (TRUS). Multiple approaches and techniques exist for MRI/US fusion and include direct ‘in bore’ MRI biopsies, cognitive fusion, and MRI/US fusion via software-based image coregistration platforms.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

Prostate cancer (PCa) is the second most common malignancy found in men, with an estimated 903 500 new cases worldwide per year [1]. In the pre-PSA era, screening for PCa consisted primarily of the DRE; however, inherent in the use of DRE was the understanding that diagnosis was operator-dependent and that it preferentially detected larger tumours located posteriorly in the gland. Biopsies were then directed to the palpable lesion using finger guides [2]; however, controlled studies failed to show a reduction in PCa mortality after routine DRE alone [3]. As a consequence, after its discovery as a serum marker, PSA was adopted in the late 1980s as a screening tool. Threshold values of PSA were used to determine the need for random biopsies of the prostate. Since the 1980s, the number of samples obtained per biopsy session has gradually increased.

After the introduction of PSA testing, the incidence of PCa rose dramatically, with the greatest increases seen in local-regional disease and a relative decrease in diagnoses of metastatic disease [4].

Although initially introduced as a potential screening technique, TRUS proved to have too many false-negative results. Initially, TRUS was used to guide biopsies to hypoechoic areas, which resulted in a 66% PCa detection rate [5]. Eventually TRUS was adopted as a method to systematically sample the prostate gland using a needle guide coupled to a TRUS probe; thus, a systematic sextant biopsy technique in conjunction with sampling of hypoechoic lesions has traditionally been the preferred biopsy method, yielding 9% greater detection of PCa compared with biopsy of palpable or sonographic abnormalities alone [6].

Further refinement and evolution of the systematic sextant technique has continued in efforts to improve biopsy yield, with schemes that increase the number of systematic cores ranging from 10 to 18 per prostate, and some have even adopted ‘saturation biopsies’ (≥20 systematic cores per biopsy session) technique [7]; however, there continues to be much debate over the idealized schema for TRUS biopsy as PCa detection rates are low and range anywhere from 33 to 44%, and many of these tumours are not clinically significant [8-10]. Recently, concern over the increasing risk of antibiotic-resistant infection has prompted a re-evaluation of patient preparation, as well as the number and frequency of prostate biopsies [11].

MRI as a Diagnostic Technique in PCa

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

MRI was introduced as a staging method for PCa staging in the early 1990s, and was primarily used to assess extracapsular extension or seminal vesicle invasion [12, 13], but actual detection of prostate cancers within the gland was considered limited. With improved technology, MRI with an endorectal coil (ERC) was found to be increasingly useful in identifying and characterizing lesions in the prostate as well as in detecting recurrent disease after treatment [14, 15]. T2-weighted (T2W) scans seemed particularly useful and dynamic contrast-enhanced (DCE) MRI was also considered helpful in confirming tumours. More recently, the ability of MRI to detect central and anterior prostate cancers has enabled the diagnosis of large tumours that went undetected on random biopsies [16]. The addition of magnetic resonance spectroscopic imaging (MRSI), a functional method that detects relative levels of choline and citrate within tumours, added to the specificity of MRI [17]. Over the past few years, diffusion-weighted imaging (DWI) has also been added to the list of parameters that are useful in detecting PCa. The inclusion of two or more MRI parameters – T2W, DWI, MRSI and DCE MRI – became known as multiparametric MRI (mpMRI), and many studies showed improved detection and localization of prostate cancers when two or more of these parameters were positive [18, 19]; because each individual MRI technique has its own shortcomings, mpMRI combines the benefits of each individual MRI sequence and provides the greatest sensitivity and specificity for cancer foci (Fig. 1A–D).

figure

Figure 1. Images from a 65 year old male with serum PSA 8.7 ng/mL and four previously negative TRUS biopsies who underwent a multiparametric MRI (mpMRI). The axial T2W MR image (A) demonstrates an anterior hypointense lesion in the right apical central gland (yellow asterisk); an ADC map of DW-MRI (B) shows a hypointense focus (yellow asterisk) indicating restricted diffusion; quantitative mapping from DCE-MRI (C) localizes the tumor (yellow box); and MRSI (D) (yellow box) demonstrates an increased choline-to-citrine ratio within the lesion. This patient underwent a MRI/US fusion-guided biopsy following mpMRI demonstrating Gleason 4+4 = 8 (90% in 2 targeted cores) in the right anterior lesion.

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As advancements in prostate mpMRI, such as endorectal coils and high field strength magnets to improve signal-to-noise ratios, continue, there has been growing recognition that mpMRI can risk stratify suspicious lesions before biopsy. For instance MRI results, such as the apparent diffusion coefficient (ADC) values calculated from DWI, provide quantitative correlation between MRI results and tissue histology. Such prognostication could potentially allow fewer biopsies if patients could be confidently stratified into low- or high-risk disease categories based upon imaging findings [20]. Successful PCa detection requires high specificity in addition to high sensitivity, and MRI provides both.

Conception of MRI-Guided Biopsy Techniques

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

With the increased recognition of the capabilities of prostate mpMRI for detecting cancers, attempts were made to incorporate MRI into routine prostate biopsies. It has been explored as a sole imaging technique for targeting biopsies or in conjunction with TRUS biopsy, a procedure that is already in the armamentarium of urologists. Three approaches have emerged that use MRI information for guiding targeted prostate biopsies: (1) direct ‘in bore’ MRI biopsies; (2) cognitive fusion; and (3) MRI/US fusion via software-based image coregistration without requiring the MRI to be physically present. In the sections below, we have reported briefly on the published clinical data for direct ‘in-bore’ MRI and cognitive fusion techniques and then focused in detail on all software fusion platforms that have published clinical data, with reporting of all currently available clinical results via the PUBMED, EMBASE and Cochrane databases.

Direct ‘In-Bore’ MRI

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

Initial attempts to use MRI to guide biopsies involved direct ‘in bore’ approaches. The patient is typically placed prone in the MRI scanner and MRI is performed to localize lesions found previously on a diagnostic MRI. Using either a transrectal or transperineal approach, needles are introduced into the visible lesions and samples are obtained with serial MRI scans to confirm biopsy needle placement. For this method, only suspicious lesions are targeted [21-23]. The advantages of this method include a reduction in the number of biopsy cores, precise recording of biopsy needle locations, as well as selecting only those patients with significant lesions. Disadvantages include relatively lengthy procedures that can be uncomfortable for the patient and often require sedation. Moreover, the inability for real-time intervention, because of the limited space inside a MRI machine, the specialized equipment and the costs and availability of this technique, has limited its use. Additionally, the stringent safety requirements of the magnetic environment place constraints on the type of needles and monitoring equipment that can be used. A high level of awareness regarding the environment must be observed by every member of the team or serious injury can result to the patient.

The number of studies reporting results with direct in-bore biopsies is limited. Many do not incorporate mpMRI for lesion identification or do not use a comparator such as systematic TRUS biopsy. As such, detection rates for clinically insignificant disease (small-volume Gleason score ≤6) ranges anywhere from 19.2 to 78.6% [23-26]. Notable, however, is work from Hambrock et al. [27] which incorporates mpMRI (T2W, DCE and DWI) and a 10-core TRUS comparator and found that in-bore MRI-guided biopsies performed significantly better than TRUS-guided biopsies (88 vs 55%, P = 0.001) for PCa detection when assessing radical prostatectomy specimens.

Cognitive Fusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

Conceptually, cognitive fusion is the simplest of the MRI-guided biopsy methods. It requires no additional equipment but requires that an experienced operator estimate lesion location based on the MRI. The operator first reviews magnetic resonance images for suspicious areas and then plans and performs a systematic TRUS-guided biopsy, trying to biopsy the general location of the suspicious lesions identified on diagnostic MRI. Because this technique requires no additional equipment, it can be immediately used in urology offices; however, a primary disadvantage is that it depends on the ability of the operator to translate the MRI findings onto the US images. This requires experience and training and leads to inaccuracies, subjectivity, variability and lack of reproducibility. Furthermore, regardless of operator experience, magnetic resonance images are acquired in an axial plane while two-dimenstional (2D) TRUS endfire biopsy is obtained at multiple differing oblique planes, which increases variability and potential inaccuracy of tissue acquisition. Additionally, unlike the other approaches, not all cognitive approaches will have the ability to record and archive biopsy location, which can be important for repeat biopsies and active surveillance.

Initial comparative studies of cognitive fusion vs systematic 10–12-core TRUS-guided biopsy demonstrate that this targeting method increases PCa detection, accuracy and representation of disease burden as well as Gleason grade identified on biopsy pathology [28-31]. Results of cognitive fusion using a transperineal approach vs a TRUS approach have also demonstrated similar results, but may potentially minimize the oblique sampling plane of TRUS biopsies and allow biopsy location documentation [32]. Two additional studies have compared cognitive fusion with software-based MRI/US fusion platforms (Urostation, Koelis Virtual Navigator and Esaote) and presented conflicting results on performance vs systematic biopsy [33, 34], thus indicating the need for further studies.

MRI/US Fusion via a Software Platform

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

The next step in the evolution of MRI-targeted prostate biopsies was to fuse mpMRI to a real-time TRUS image. In this way MRI can be used to localize a tumour but TRUS can be used to guide the needle, enabling prostate biopsy to be performed in outpatient centres or doctors' offices, much like the cognitive technique. Furthermore, because TRUS is already used to guide systematic biopsies, MRI/US fusion does not alter the normal workflow of urologists who typically perform the biopsy. The patient is in a far more comfortable environment and often only local anaesthetic is required.

This method is rapidly evolving, with the major technical hurdle involving the ‘registration’ of the MRI to the US image. Because the prostate on MRI (with or without an endorectal coil) often differs in shape and deformation from the same prostate on TRUS, some method of image registration must take place for successful fusion. This process can involve the identification of landmarks (e.g. points, curves and surfaces) which can be recognized on both corresponding images, thereby allowing the two images to become aligned through either a ‘rigid’ or ‘elastic’ transformation. Rigid transformations do not change the images themselves, but allow translation and rotational variations between images, while elastic transformations account for the addition of local deformation, warping or scale changes as well (Fig. 2A). It is important to note that elastic methods stretch or warp one of the image volumes so data is also stretched and moved; therefore, rigid registration-derived images may look less pleasing to the eye when looking at image borders, but the data integrity is greater, because anatomy is not artificially altered by the computer in order to create the appearance of a ‘match’. Furthermore, operator input may often adjust or correct for rigid registration error or offset, with either manual correction, or manual adjustment of targeting, or even adjustment of the manual insertion depth or pressure from the TRUS transducer (Fig. 2B). The registration step is probably the biggest opportunity for operator error.

figure

Figure 2. Elastic and Rigid Software Image Registration Methods. Pre-biopsy MR data is registered with real-time TRUS images by aligning landmarks (e.g. points, curves, surfaces,) in corresponding images via rigid or elastic transformations. (A) represents MRI/US registration when there is minimal TRUS deformation and use of an endorectal coil (ERC) for MR images, and (B) demonstrates increased manual TRUS deformation that can mimic ERC deformation. As seen above, a simple overlay of TRUS and MRI models (middle images in panels A and B) results in reduced correlation between imaging modalities. A rigid registration method can account for translational and rotational differences between models while an elastic registration method has the additional ability to account for local deformations (e.g. caused by an endorectal coil or TRUS probe). However, elastic warping can move or alter relative anatomic location despite more matched borders. ERC, endorectal coil.

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Kaplan et al. [35] described a transperineal biopsy using a rigid stereotactic stepper device, commonly used for deployment of brachytherapy seeds in 2002. Since then, multiple MRI/US software platforms have been developed. The existing platforms with published clinical data to date are summarized in Table 1 [33-45]. The general workflow of all platforms first requires a pre-biopsy diagnostic MRI to identify and annotate lesions suspicious for cancer based on imaging characteristics, with interpretation by a prostate-trained radiologist. Then, depending on the particular platform, targets are delineated before or after MRI data have been loaded onto the software platform. TRUS-guided biopsy of the prostate is performed and MRI and real-time TRUS images are superimposed and displayed side-by-side, thus creating an easily navigable three-dimensional (3D) prostate reconstruction. Because MRI and US images have been colocalized and coregistered, they allow blending back and forth between MRI and TRUS.

Table 1. Summary of MRI/US fusion platform specifications
Fusion System – Trade Name (Manufacturer)Principle investigator locationMRIUSBiopsy
MRIParameters used to define targetEndorectal/pelvic coilUS image acquisitionMethod of image registrationTracking mechanismBiopsy route# Cores per MRI lesionComparator
UroNav (In Vivo Corp./Philips)Bethesda, MD, USA [36-39]3T PhilipsT2W, DCE, DWI, MRSIYes/YesManual US 2D sweep. Freehand manipulation of US probe.RigidElectromagnetic tracking USTransrectalMinimum 212-core TRUS
Artemis (Eigen)Los Angeles, CA, USA [40, 41]3T SiemensT2W, DCE, DWINo/NoManual rotation along a fixed axis (US probe on a tracking arm)ElasticMechanical arm with encoded jointsTransrectalMean 2.212-core TRUS
Urostation (Koelis)Paris, France [34]1.5T SiemensT2W, DCE, DWIYes/YesAutomatic US probe rotation, three different volumes elastically registeredElasticImage-based registrationTransrectalMinimum 210–12-core TRUS
Oslo, Norway [42]1.5 SiemensT2W, DWIYes/NoMinimum 212-core TRUS
Grenoble, France [43]3T PhilipsT2W, DCE, DWINo/No212-core TRUS
BiopSee (Pi Medical/MedCom)Heidelberg, Germany [44]3T SiemensT2W, DCE, DWINo/NoCustom-made biplane TRUS probe mounted on a stepperRigidStepper with two built-in encodersTransperinealMedian 412-core TRUS
Virtual Navigator (Esaote)Paris, France [34]1.5T SiemensT2W, DCE, DWIYes/YesManual US sweep. Freehand rotation of US probe.RigidElectromagnetic tracking US and needleTransrectalMinimum 210–12-core TRUS
Lille, France [33]1.5T PhilipsT2W, DCE, DWINo/YesMinimum 212-core TRUS
HI RVS/Real-Time Virtual Sonography (Hitachi)Chiba, Japan [45]1.5T PhilipsT2W, DCE, DWINo/YesReal-time biplanar TRUSRigidElectromagnetic trackingTransrectal or transperineal1–210-core TRUS

The major differences between fusion platforms are the registration method, operator input and their original intended use. Electromagnetic tracking fusion was primarily designed for prospectively navigating a needle to an MRI target, and later adapted to archive locations or previous biopsies. Image-based fusion was originally designed to track, document and archive the location of biopsy, and was later adapted to prospectively target MRI-defined targets. Image-processing-based fusion may have limitations in speed or accuracy of prospective needle guidance, but is significantly less cumbersome. Cognitive fusion is also limited in accuracy which means it may be difficult for small targets. Learning curves and degree of automation may vary. Automatic organ edge detection, automatic segmentation (outlining of the organ), and motion compensation are facilitating tools to help account for differences in TRUS insertion depth. Some image-based registration platforms may require a several-second pause with the needle in place to track and archive the location. The platforms also differ greatly in the degree to which they are seamlessly integrated to the MRI workstations. Less human input translates into faster methods with less room for error.

The platforms also differ with regard to steps for manual input (or operator-refinement or ‘tweaking’) of an automatic registration, which is the art of fusion biopsy. Will all platforms be reproducible, standardized and able to normalize the procedure? The platforms differ also in terms of how the 3D ultrasound volumes are built. Some build a 3D volume from a 2D ‘sweep’ with the TRUS transducer fanning out sequentially obtaining 2D images from known perspectives defined by electromagnetic tracking, for example. Others are able to use a biplane probe or a 3D probe that can acquire the data in 3D, rather than reconstruct it. At present, all systems also vary in terms of their ultrasound vendor requirements, with some limited to one vendor, and others relatively vendor-agnostic to varying degrees.

The graphical user interfaces also differ markedly, with some displaying side-by-side ‘co-displayed’ MRI and US separately, and others displaying a blended fusion image where the US and MRI can both be seen on the same image in different colours or grey scale. The TRUS guidance can be primarily relied upon with modifications based upon fusion information, or alternatively the fusion can be relied upon with TRUS input for modifications. Needle depth can be estimated based upon visual feedback from TRUS, and automatic needle detection algorithms are available that automatically detect the distal-most tip of the biopsy needle.

UroNav

The UroNav platform (In Vivo Corp., Gainesville, FL, USA) was the first office-based fusion biopsy platform and was developed at the National Institutes of Health in Bethesda, MD, USA in collaboration with Philips Healthcare. Patient recruitment began in 2004 and has since continued to undergo clinical testing and development. Research done at the National Cancer Institute has largely employed a diagnostic mpMRI performed at 3T (Philips Achieva MRI) using four MRI parameters (T2W, DCE, DWI, MRSI) to identify lesions and individually assign them as low, moderate, or high suspicion for PCa based on their imaging characteristics and abnormal MRI parameters [36]. Biopsy needle localization and tracking data are recorded via an external magnetic field generator but the biopsy uses existing freehand US technology. The biopsies are performed transrectally. Once the MRI data is loaded onto the software platform and an initial TRUS sweep has been performed, rigid image fusion is performed and clinicians are able to see both the MRI and US images move in real time. This allows a lesion to be targeted on MRI but monitored via TRUS for the course and depth of the needle to ensure that it enters the suspicious area. Because biopsy still uses familiar freehand TRUS technology, training for this platform is primarily software-based and can be gained after only a few biopsy sessions.

Initial data for the first 101 men who underwent biopsy on a research-based iteration of UroNav demonstrated that 89.5% of men with high-suspicion lesions on MRI were diagnosed with PCa, with targeted cores detecting more PCa than standard 12-core TRUS cores [37]. Findings have since been updated to more closely assess the utility of the MRI lesion suspicion scoring for PCa detection. Results of 582 patients have shown an increasing correlation between mpMRI suspicion and Gleason score with detection for Gleason score ≥8 PCa showing a 98% sensitivity at the low to moderate threshold and a 91% negative predictive value at the moderate to high threshold [38]. Overall PCa detection rates are nearly equivalent for targeted vs systematic (80 vs 81%; Table 2 [33, 34, 36-45]), but the addition of targeted cores to systematic cores markedly increased the detection rates of intermediate- to high-risk disease, with 32% of patients upgraded after targeted biopsy (TB). Furthermore, targeted cores detected clinically significant disease (biopsy Gleason score ≥4 + 3) in 18% of patients with negative systematic biopsies, while systematic cores detected 8% of Gleason ≥4 + 3 cases missed by targeted biopsy [39]. Thus, stratification of patients with low-risk vs high-risk PCa is possible and may help minimize the number of biopsy sessions a patient undergoes while also strengthening confidence in biopsy results, which is also important for active surveillance; however, more research is warranted to assess patients with low to moderate MRI lesion suspicions as well as further clarifying whether the improved performance of targeted biopsy cores in diagnosing PCa is attributable to improved sampling techniques or to improved localization from the imaging findings.

Table 2. Patient-based histological biopsy outcomes by fusion platform
Fusion system: trade name (manufacturer)Principle investigator locationPatient inclusion criteriaMRIBiopsy ResultsAdditional/notable study conclusions
Defining lesion suspicion for PCaNo. patients with MRI-suspicious lesionsProstate cancer detection in patients with MRI lesion (no. patients)Prostate cancer detection: TBProstate cancer detection: SBP
  1. TB, targeted biopsy; SB, systematic biopsy.

UroNav (In Vivo/Philips)Bethesda, USA [36-39]August 2007 to August 2012Low, moderate, or highLow – 123 (21%); Moderate – 370 (64%); High – 89 (15%)315/582 (54%)253/315 patients (80)255/315 patients (81)TB upgrades and detects higher Gleason score in 36% of patients compared with TRUS. Lesions with high suspicion on mpMRI associated with higher rate of Gleason upgrading on target vs 12-core biopsy
Artemis (Eigen)Los Angeles, CA, USA [40, 41]March 2010 to September 2011Score 1 to 5 (normal to highly suspicious)151/171 (88%)84/151 (56%)101/486 cores (20.8%)127/1741 cores (7.3%)0.001TB is three times more likely to identify disease than SB (20.8 vs 7.3%, P = 0.001) with greater detection of intermediate- to high-risk disease (36 vs 24%, P = 0.037). Biopsy findings correlate with level of MRI suspicion.
Urostation (Koelis)Paris, France [34]January 2011 to March 2012Yes/No82/133 (62%)71/82 (87%)62/82 patients (76%)44/133 patients (33%)TB PCa detection was significantly higher than SB (P = 0.002). Cognitive TB not different from SB (P = 0.66)
Oslo, Norway [42]December 2010 to May 2011Low, medium, or high80/90 (89%) patients. Lesions – High (55), Medium (6), Low (4)54/80 (67.5%)60/115 targets (52%)6/42 patients (14%)10 patients negative MRI all negative SB. 112/115 (97%) MRI targets successful, 50/115 (52%) positive for cancer.
Grenoble, France [43]November 2011 to August 2012Prostate Imaging-Reporting and Data System (PI-RADS)20/30 (67%)11/20 (55%)Urostation has good accuracy for targeting suspicious areas on MRI
BiopSee (Pi Medical/MedCom)Heidelberg, Germany [44]June 2010 to December 2011Highly suspicious, questionable or not suspiciousHighly suspicious: 104/347 (30%). Questionable: 149 (43%). Not suspicious: 94 (27%)Overall: 200/347 (58% patients). Highly suspicious: 82.6% patients. Questionable: 67% patients. Not suspicious: 14.8% patients386/1281 (30%) cores523/6326 (8.2%) cores0.01TB detects significantly more cancer than SB (30 vs 8.2%) P = 0.01 and of greater significance (41% had significant PCa). Patients without cancer-suspicious MRI lesions, 11.7% (11/94) were diagnosed with intermediate-risk disease. 50.6% (152/300 patients) reported mild haematuria, 26% temporary erectile dysfunction.
Virtual Navigator (Esaote)Paris, France [34]January 2011 to March 2012Yes/No78/131 (59%)78/78 (100%)64/78 (82%) patients60/131 (46%) patientsRigid system TB were significantly higher than SB (P = 0.007). Cognitive TB not different from SB (P = 0.66)
Lille, France [33]May 2009 to January 20111–5 (unlikely to highly likely)95/95 (100%)66/95 (69%) patients *combination of cognitive and Vnav fusion cores56/95 (56%) patients0.033Clinically significant PCa 49/95 (52%) SB patients, 64/95 (67%) TB patients (P = 0.001). Cognitive vs platform fusion not significantly different in PCa detection or Gleason score assessment (47 vs 53%, P = 0.16)
HI RVS/Real-Time Virtual Sonography (Hitachi)Chiba, Japan [45]February 2007 to August 2009Yes/No85/85 (100%)52/85 (61%)62/192 (32%) cores75/833 (9%) cores<0.01TB cores revealed more cancer than SB (32 vs 9%, P < 0.01)

Artemis

The Artemis platform (Eigen, Grass Valley, CA, USA) received US Food and Drug Administration approval in 2008 with patient recruitment beginning in September 2009 at the University of California, Los Angeles (UCLA). The general software features of the Artemis system are similar to the other platforms mentioned (Table 1); however, ultrasound images are acquired along a fixed axis using an articulated mechanical arm so the biopsy is limited by the rotation of the articulated arm. Needle tracking information is recorded based on encoders at each joint of the mechanical arm. A 3T MRI (Siemens Somatom Trio; Siemens, Erlangen, Germany) using T2W, DCE and DWI parameters was used to identify MRI lesions and define the suspicion for each lesion on a 1–5 (normal to highly suspicious) scale [40]. Image registration is carried out via an elastic method. Training for use of this platform requires not only familiarity with the software, but also time to acclimate to TRUS biopsy using manual rotation of the mechanical arm as opposed to the freehand techniques commonly used in urological practice.

Results of 171 men undergoing fusion biopsy from March 2010 to September 2011at UCLA have shown that 94% (16/17 patients) with MRI lesion suspicion of grade 5 have had biopsy-positive PCa, with targeted cores three times more likely to detect disease than systematic cores (20.8 vs 7.3%, P = 0.001). Furthermore, a 38% detection rate was found for intermediate- to high-risk PCa detected only on targeted biopsy, with targeted cores more likely to detect intermediate- to high-risk disease vs systematic biopsy (SB) (36 vs 24%, P = 0.037), as well as a correlation between MRI suspicion and biopsy findings (Table 2) [41].

One notable difference in the UCLA approach to fusion biopsy is their five-point semi-quantitative scoring system for assessment of MRI-identified lesion suspicion for PCa. Scores are based on levels of variation in T2 characteristics, quantitative ADC maps of the DWI parameter, and DCE curve analysis as opposed to a binary evaluation of abnormal vs normal for individual parameters for a given lesion. The utility of the different scoring systems in direct comparison with one another has yet to be investigated and fully defined.

Urostation

Urostation (Koelis, Grenoble, France) has been studied clinically at centres in France and Norway as well as preclinically at the University of Southern California in Los Angeles, California, USA (Table 1) [34, 42, 43, 46]. Because there are multiple independent centres using this platform, they have each chosen different MRI parameters and thus varying definitions of what qualifies as a suspicious lesion on MRI (Tables 1, 2). The fusion process is performed via elastic registration and similar to the UroNav platform with the exception that confirmation of biopsy needle placement is done retrospectively and requires a 3–5-s delay for each needle for 3D TRUS acquisition. Training on this system is otherwise software-based as the biopsy guidance uses a standard freehand approach.

Experience with the Urostation platform has shown targeting accuracy to be as high as 97% (112/115 MRI targets) in clinical models [46] with PCa detection rates for MRI-suspicious lesions that vary from 55 to 87% of patients [34, 42, 43]. Furthermore, Delongchamps et al. [34] have shown improved PCa detection in targeted cores vs 12-core systematic TRUS biopsy (76 vs 33% patients, P = 0.002) with greater clinically significant disease (biopsy Gleason score >6) detected in targeted cores (33 vs 14% patients, P = 0.01). Results from Rud et al. [42] also highlight findings that higher-suspicion MRI lesions have a greater propensity to contain PCa on targeted biopsy sampling (91% high-suspicion lesions were positive for PCa vs a 10% positivity rate for low-suspicion lesion targets [Table 2]).

BiopSee

The BiopSee Platform (Pi Medical, Athens, Greece) is a system whose main clinical development has been performed at University Hospital Heidelberg in Heidelberg, Germany. Unlike other fusion platforms (Table 1), BiopSee is the only platform in which the prostate biopsy is performed via a transperineal route. An endorectal US probe is still used for guidance and is attached to a custom-made mechanical stepper fixed to the operating table. This TRUS probe has two degrees of freedom that allow adjustments in probe depth and rotation along the main axis. These movements and rotations are tracked by two built-in encoders. Biopsy needles are guided through a grid mounted to the mechanical stepper.

MRI was obtained at 3T (Magnetom Trio; Siemens) with T2W, DWI and DCE sequences to define lesion suspicion for PCa based on a three-point scale (not suspicious, questionably suspicious or highly suspicious). A rigid image registration process is employed. Training with this system requires not only familiarity with the software aspect of BiopSee, but also experience in handling the US probe along fixed degrees of movement and rotation while also aligning it via software prompts (virtual needle insertion lines) to ensure correct needle placement and penetration as designed by the system. According to Kuru et al. [44], the learning curve for platform is ∼10 patients.

Patient recruitment for BiopSee began in June 2010 and by March 2012 it had enrolled 347 patients [44]. Overall PCa detection was 58% of patients with targeted biopsy cores accounting for 51% of cases, of which 41% had clinically significant disease. When looking at performance on a per core analysis, targeted cores detected significantly more PCa than 12-core systematic TRUS biopsy (30 vs 8.2%, P = 0.01). A correlation between higher lesion suspicion and PCa detection was found, with 82.6% of highly suspicious lesions demonstrating PCa (72% of which demonstrated biopsy Gleason score ≥7), while questionably suspicious lesions had a PCa detection rate of 67%.

BiopSee data appear similar to those of other methods, but the study design creates biases favouring targeted cores and sometimes omitted sampling of systematic cores and thus data should be interpreted with caution.

Virtual Navigator

Virtual Navigator (Esaote, Genoa, Italy) is a fusion platform that was initially released in 2004 for percutaneous interventional guidance procedures and thus was capable of image fusion between real-time US and either previous diagnostic CT or MRI studies. Its use for prostate biopsy has only recently been explored, particularly in France, and is currently not commercialized in the USA. MRI targets are selected after uploading MRI studies into the software platform and then via rigid registration fused to real-time, freehand TRUS images. Studies reporting the use of suspicious lesions found using Virtual Navigator have been defined by 1.5T MRI using T2W, DCE and DWI parameters.

Delongchamps et al. [34] reported that this platform was 100% accurate for PCa detection in 78 patients with a suspicious MRI lesion, of which targeted biopsy detected 82% (64/78 patients). When assessing targeted vs systematic biopsy performance, targeted cores detected an additional 9% (7/78) of patients with intermediate- to high-risk disease, while systematic biopsy detected an additional 18% of patients (14/78) with Gleason 6 disease. Puech et al. [33] have also published results with the Virtual Navigator platform and found significant differences in overall PCa in favour of targeted biopsy (69 vs 59% patients, P = 0.033) with more clinically significant disease detected by targeted biopsy vs systematic biopsy (67 vs 52% patients, P = 0.001); however, it is important to note that their evaluation of targeted cores includes results from both cognitive targeting as well as Virtual Navigator targeting, with not all patients undergoing both targeting procedures.

Overall, results such as these are consistent with those of the other platforms mentioned in the present review (UroNav, Artemis, Koelis and BiopSee) [34, 39, 41, 44] and indicate targeted biopsy has greater utility not only in detecting PCa, but in avoiding the diagnosis of nonsignificant disease.

Real-Time Virtual Sonography

Real-Time Virtual Sonography (HI RVS; Hitachi, Tokyo, Japan) is another general fusion platform that has been customized for prostate biopsy and, as such, has image fusion capabilities between US and MRI as well as between US and CT. The HI RVS platform was developed in Japan and uses freehand TRUS with a electromagnetic sensor for motion-tracking. Research on this platform at Hitachi General Hospital used a 1.5T MRI (Philips Interna) with T2W, DCE and DWI parameters to define MRI lesions as positive or negative for PCa suspicion (Table 1) after MRI data were loaded onto the HI RVS biopsy platform. Rigid registration is then used between MRI and TRUS images.

In 2010, results from an 85-patient study conducted between February 2007 and August 2009 on the HI RVS platform showed an overall PCa detection rate of 61% of patients (52/85), of which 87% (45/52) were detected by targeted cores. Per-core analysis showed that targeted cores detected significantly more cancer than systematic cores (32 vs 9%, P < 0.01) [45]. These results are again congruent with other platform detection rates; however, no further comments were made about the ability of this biopsy platform to track needle cores or histological correlation between targets vs systematic biopsy locations at the current time.

Fusion Biospy: How Does It Compare with Current Standards?

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

Because of the relative novelty of these fusion biopsy platforms, there have been few studies that have performed comparisons between the different platforms, much less between MRI-guided biopsy techniques [33, 34]; however, as seen on a per-platform analysis, targeted biopsy appears to have improved PCa detection rates compared with systematic TRUS biopsies alone and demonstrates a greater detection rate of clinically relevant disease (Table 2). A systematic review by Moore et al. [47] assessed the accuracy of all three MRI-guided biopsy techniques (in-bore, cognitive, and fusion platform) compared with systematic TRUS-guided biopsy for the detection of clinically significant disease and concluded that MRI guidance vs systematic TRUS biopsy detected the same amount of cancer; however, further analysis showed that targeted cores resulted in less tissue sampling (7% systematic cores [368/5441] positive vs 30% targeted cores [375/1252] positive) with an additional one-third of men detected on targeted biopsy vs systematic biopsy (48% for targeted biopsy vs 36% for systematic biopsy). Additionally, targeted biopsy missed a diagnosis of clinically insignificant disease in ∼10% (53/555) of men in their investigation.

While the present systematic review provides an excellent overall perspective on MRI-guided techniques, further studies are needed to elucidate the roles of individual targeted biopsy techniques compared with current standards. Also unclear is whether new techniques with new sensitivities will alter the core criteria for ‘significant disease’ Additionally, as described previously, because of the lack of standardization in MRI parameters (e.g. 1.5 vs 3T, use of functional parameters including spectroscopy, use of endorectal and/or surface coils) and variations in definitions for MRI lesion suspicion, it is difficult to form consensus guidelines for MRI at this time. Finally, as targeted biopsies typically yield a higher tumour-positive percentage of the core, new guidelines will need to be established for the management of cancers detected by MRI/US fusion technology.

Future Directions of Prostate Fusion Biopsy

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

As the use of fusion biopsy platforms becomes more widespread, the implications for how it will change current diagnostic and management decisions are yet to be fully understood. Perhaps one of the most potentially promising outcomes is higher PCa detection rates, particularly of clinically significant disease, along with the potential to minimize the number of repeat biopsy sessions and cores sampled per session. With earlier and more accurate diagnosis of PCa, not only does this have the potential to improve patient quality of life but could also potentially affect mortality outcomes for men with intermediate- to high-risk disease at the time of initial diagnosis. As present studies indicate, while there is certainly measurable utility in the use of targeted cores, systematic biopsy methods cannot be dismissed because they continue to diagnose a small but measurable number of significant lesions that are missed on targeted biopsy [39, 41, 44, 45]. Whether this is attributable to limitations of MRI to detect lesions below a certain size threshold, non-imageable cancer foci, or misplaced targeted cores because of poor co-registration of MRI with the TRUS used for guidance is unclear at this point, but MRI technology improvements may potentially shed light on these questions, as MRI strives to shed light on PCa detection and characterization.

Another important downstream effect of MRI/US fusion technology is the improved ability to correlate histological outcomes with radiological findings, both qualitatively and quantitatively. Lesions visible on MRI can be linked to their corresponding biopsy cores with greater confidence because fusion platforms are able to track needle placement and create a biopsy map (‘mapping’) for post-biopsy session reference (‘archiving’). This mapping will be increasingly vital for patients undergoing active surveillance who receive repeat imaging with or without biopsy. The radiology-to-pathology correlation is a powerful tool for validation of imaging screening tools, such as research MRI sequences, contrast agents or specific indications. Work such as this has been pursued with small patient cohorts e.g. that of Turkbey et al. [48], who found a significant negative correlation between ADC values, Gleason score and D'Amico clinical risk scores; however, there is an urgent need for standardizing reporting of MRI-suspicious lesions so that risk assessments do not suffer from wide interobserver variations (Table 1). In an effort to accomplish this, an international working group has recently released recommendations for MRI-targeted biopsy results which may prove helpful in the future by allowing the interpretation of data from a variety of different centres worldwide [49].

Perhaps one of the most interesting effects of fusion platforms and the use of targeted cores is how it will affect the management of PCa, both from the perspective of active surveillance as well as focal therapy. Not only should needle tracking allow more precise re-biopsy of previously diagnosed known cancer foci, but it should increase confidence that MRI-visible lesions can be histologically and radiographically followed for disease progression. One questionthat remains unanswered, however, is the potential effect of targeted cores upon current biopsy interpretation, which is based on less efficient TRUS-guided sampling. More ‘efficient’ targeted cores are more likely to have a greater proportion of positive cores (more cancer represented per core because of their targeted nature). Since current guidelines with regard to the ‘per cent of core’ involved assume a ‘tip of the iceberg’ underestimation of disease extent, this new, more accurate information, will need to be incorporated into decision algorithms for PCa management and prognosis. Biopsy needle tracking may also prove beneficial in the arena of focal therapy for imageable and localized PCa. Although further investigations are warranted with regard to appropriate patient selection for focal therapy, the ability to confirm and follow foci of PCa becomes critical when undergoing lesion-directed or partial gland therapies vs the classic radiation whole-gland surgical and radiation treatments currently in use today.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

Improvements in imaging technology and screening methods have changed the way clinicians approach not only PCa, but solid tumours in general. Resulting expanded capabilities for real-time tumour targeting and risk stratification may minimize unnecessary intervention. Each commercial platform has its own optimum application, workflow, strengths and weaknesses. Awareness of the differences of each is vital to understanding how to make optimum use of these tools. The fact that there are many commercial options for fusion biopsy will drive future applications and refinement of the technology, but the strengths and weaknesses of each platform remain opinions and are largely anecdotal, and there is no clear consensus on which methodology is optimal for screening, detection or surveillance, nor on the specific indications (vs standard TRUS guidance or MRI in-bore guidance). When fusion is useful in any specific clinical setting also remains somewhat speculative. What is clearer now, more than ever, is that the era of fusion biopsy is here, and this will involve radiologists and urologists working in multidisciplinary teams, so as to fully realize the potential of this powerful approach.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References

This research was supported by the Intramural Research Program of the NIH, National Cancer Institute, Center for Cancer Research and the Center for Interventional Oncology. NIH and Philips Healthcare have a cooperative research and development agreement. NIH and Philips share intellectual property in the field. This research was also made possible through the National Institutes of Health (NIH) Medical Research Scholars Program, a public-private partnership supported jointly by the NIH and generous contributions to the Foundation for the NIH from Pfizer Inc, The Doris Duke Charitable Foundation, The Alexandria Real Estate Equities, Inc. and Mr. and Mrs. Joel S. Marcus, and the Howard Hughes Medical Institute, as well as other private donors.

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  1. Top of page
  2. Abstract
  3. Introduction
  4. MRI as a Diagnostic Technique in PCa
  5. Conception of MRI-Guided Biopsy Techniques
  6. Direct ‘In-Bore’ MRI
  7. Cognitive Fusion
  8. MRI/US Fusion via a Software Platform
  9. Fusion Biospy: How Does It Compare with Current Standards?
  10. Future Directions of Prostate Fusion Biopsy
  11. Conclusions
  12. Acknowledgements
  13. Conflict of Interest
  14. References
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Abbreviations
PCa

prostate cancer

DCE

dynamic contrast-enhanced

MRSI

magnetic resonance spectroscopic imaging

T2W

T2-weighted

DWI

diffusion-weighted imaging

mpMRI

multiparametric MRI

ADC

apparent diffusion coefficient

2D

two-dimensional

3D

three-dimensional

UCLA

University of California Los Angeles

SB

systematic biopsy

TB

targeted biopsy

ERC

endorectal coil