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European Urology
Volume 52, issue 4, pages 939-1280, October 2007[Editorial Comments by V. Scattoni and by B. Rocco]
Prostate Biopsies Guided by Three-Dimensional Real-Time (4-D) Transrectal Ultrasonography on a Phantom: Comparative Study versus Two-Dimensional Transrectal Ultrasound-Guided Biopsies
Jean-Alexandre Long a b 
, Vincent Daanen b, Alexandre Moreau-Gaudry c, Jocelyne Troccaz b, Jean-Jacques Rambeaud a, Jean-Luc Descotes a.
Accepted 14 November 2006, Published online 27 November 2006, pages 1097 - 1105
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Abstract
Objective
This study evaluated the accuracy in localisation and distribution of real-time three-dimensional (4-D) ultrasound-guided biopsies on a prostate phantom.
Methods
A prostate phantom was created. A three-dimensional real-time ultrasound system with a 5.9 MHz probe was used, making it possible to see several reconstructed orthogonal viewing planes in real time. Fourteen operators performed biopsies first under 2-D then 4-D transurethral ultrasound (TRUS) guidance (336 biopsies). The biopsy path was modelled using segmentation in a 3-D ultrasonographic volume. Special software was used to visualise the biopsy paths in a reference prostate and assess the sampled area. A comparative study was performed to examine the accuracy of the entry points and target of the needle. Distribution was assessed by measuring the volume sampled and a redundancy ratio of the sampled prostate.
Results
A significant increase in accuracy in hitting the target zone was identified using 4-D ultrasonography as compared to 2-D. There was no increase in the sampled volume or improvement in the biopsy distribution with 4-D ultrasonography as compared to 2-D.
Conclusion
The 4-D TRUS guidance appears to show, on a synthetic model, an improvement in location accuracy and in the ability to reproduce a protocol. The biopsy distribution does not seem improved.
Keywords: Biopsy guidance, Prostate cancer, Prostate phantom, 3-D ultrasonography, TRUS.
Article Outline
1. Introduction
This study assessed the value of three dimensions and real-time (4-D mode) ultrasonography in transrectal ultrasound-guided (TRUS) prostate biopsies. We wanted to determine whether the ability to visualise simultaneously orthogonal planes allows a more accurate and more reproducible sampling and whether the biopsies are more evenly distributed within the prostate volume. We compared traditional two-dimensional (2-D) TRUS with three-dimensional (3-D) real-time (4-D) TRUS-guided biopsy sessions on a synthetic model (phantom).
Sextant biopsies resulted in a better cancer detection rate than biopsies focusing on ultrasound abnormalities [1]. However, it was shown that cancer was detected in 20% of the cases studied, during a second set following a negative sextant biopsy. Many biopsy schemes have been described to improve the sensitivity of biopsies while limiting the number of samples. The trend is now towards an increase in the number of biopsies and sampling the peripheral zone [2]. Additional morbidity resulting from extensive protocols remains controversial [3].
Three-dimensional ultrasonography is commercially available for routine clinical use and has been used on some devices since 1994. Rather than producing an anatomic section, image acquisition is performed as a volume of data with nearly immediate reconstruction and simultaneous display of sectional anatomy in three orthogonal planes (sagittal, transverse or coronal plane, or any arbitrary oblique). The scanning time varies from 3 to 10 s, depending on the volume and quality desired. It is also possible to use endocavity probes.
A 3-D volume acquisition of an organ can also be performed, such that the images can be manipulated and the coordinates of all volume points stored in the memory. The latest developments have led to real-time 3-D acquisition, also called 4-D. It consists of displaying, simultaneously, three orthogonal viewing planes in real time. This guiding mode has proven its effectiveness in terms of accuracy in biopsies on breast tumours [4], liver tumours [5], and pancreatic pseudocysts [6]. We wish to study its potential benefits in prostate biopsy.
2. Methods
The device used is a VOLUSON® 730 Pro (General Electric) equipped with an RIC5-9 (5.9 MHz) endorectal probe, which can be used in the 2-D, 3-D, or 4-D mode. The biopsy needle was a Tru-Cut 18-gauge needle, with a cutting length of 23 mm. It appears important to specify that the expected benefit of 4-D ultrasound does not lie primarily in high-accuracy guidance toward a materialised zone but rather in better sampling of the gland. Our purpose was not to assess the protocol but rather the effectiveness in guiding the biopsy towards the zones theoretically set out by the protocol. Testing the device on a synthetic model appeared a necessary preliminary step.
2.1. Design of a synthetic prostate model (phantom)
In a square plastic box (10 × 10 cm), a circular hole spanning 6 cm in diameter was cut, so that a probe could be inserted. Inside the orifice, a cylinder intended to simulate the rectal wall was placed. The ultrasound propagation environment was made of Aquasonic® ultrasound gel (750 ml/phantom). The prostate was made by squeezing candle gel into a silicon mould. The model was the equivalent of a 40-ml prostate (Fig. 1).
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After biopsy execution, air was brought in the phantom by the needle. Biopsies left trails in the phantom, which made it possible to assess the biopsy path using ultrasonographic volume acquisition (3-D). But this also constituted a possible bias by helping the operator to spread the biopsies within the phantom. Considering the bias that would have been created by the trails from the previous biopsies, it was essential that one phantom be produced per biopsy (Fig. 2). The procedure was different from the clinical use because another phantom was used after each biopsy.
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2.2. Modelling the biopsy path
The air incorporated into the phantom when the needle entered left a hyperechogenic trail that was easily detectable by ultrasonography (Fig. 3). A 3-D volume acquisition of the entire phantom was performed after each biopsy and recorded.
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2.3. Biopsy scheme
The protocol used was a 12-biopsy scheme. For that reason, 12 phantoms were produced, making it possible to perform a single uninterrupted session. The phantoms were replaced after each biopsy and 336 phantoms were produced (14 operators, 2 modalities, 12 biopsies/session). The procedure was different from that used clinically. In comparison with the real clinic procedure, a bias may have been introduced.
Despite that replacement, all the phantoms were similar. We assumed that an operator needed to be able to reconstruct mentally the anatomy of the phantom before performing each biopsy. Each operator performed the first biopsy session using the VOLUSON 730® with the 2-D mode then with the 4-D mode.
2.4. Processing the acquired ultrasonographic data
The first step in processing the biopsy data was to create software to visualise the reference volume of the phantom (template). The reference volume was produced after segmentation of an ultrasonographic volume using the image-processing software Analyze®. Then the different biopsies of each session were superimposed in the reference prostate using manual registration (alignment of the different volumes).
Attempts at automatic registration did not yield any results, due to the significant noise and significant variations in interface contrast between the various phantoms.
The 12 biopsies carried out in one session were collected and shown in the reference (Fig. 4, and Fig. 5). The methodology is summarised in Fig. 6.
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Fig. 4 Visualisation of a biopsy path in the reference volume. The green ball shows the entry point. The blue ball shows the target hit.
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2.5. Assessing biopsy results
A quality biopsy assessment protocol was established. Three parameters were studied:
2.5.1. Entry zone
Based on the anatomic and protocol schemes for the 12 biopsies, a point located on the prostate surface was chosen as the ideal insertion point for the needle in each biopsy. Considering that there was no clear recommendation or obvious target, an entry zone spanning 7 mm in diameter (sphere) around the said puncture point was deemed suitable. Beyond that zone the error distance was measured. The 7-mm diameter was chosen because it would allow the entry zones to be juxtaposed on the phantom surface without overlapping.
2.5.2. Target zone
The biopsy tip was also compared to an ideal target zone of 7 mm in diameter. The error was defined as the distance separating the biopsy tip and the sphere (Fig. 7).
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2.5.3. Biopsy distribution in the volume
Assessing the appropriate biopsy distribution within the prostate volume was not easy. According to Epstein, cancer is significant above 0.5 ml [7]. We therefore tried to find a method that would make it possible to show the volume “explored” by the biopsies (depending on biopsy length in the prostate and, above all, overlapping between the biopsies). We therefore hypothesised that a biopsy “explored” a volume within a 1.2-mm diameter cylinder (18-gauge needle diameter), in addition to which there was a “security zone” of 10 mm diameter (the diameter of a 0.5-cc ball is 10 mm).
Fig. 8 shows the oversampling of a zone, in which two cylindrical volumes are covered by bringing together two biopsies. As a result, the adjacent regions of the prostate are undersampled.
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In other words, the biopsy-explored prostate volume was equal to the length of the biopsy needle multiplied by the surface of a 5.6-mm radius disk. The points that overlapped with the adjacent biopsy cylinders were counted only once.
We opted for a ratio that indirectly reflected the distribution, by identifying the ability of each operator to allocate the biopsies so that they would not overlap (volume explored in the prostate/volume that should have been explored if the biopsies did not overlap).
During each session, it was possible to determine the volume identified by the series within the prostate.
2.6. Statistical analysis
Statistical analysis of the data was performed using STATVIEW 5.0® software. The quantitative variables were described by their mean and standard deviation (mean ± SD) with median and interquartile range. Mean comparisons were performed by using suitable parametric tests once the application conditions where satisfied. When the said conditions were not satisfied, suitable nonparametric tests were used. As usual, tests results were considered statistically significant for p < 0.05.
Accuracy analysis was performed on each 2-D and 4-D TRUS-guided biopsy by analysing distances at the ideal entry zones and ideal theoretical target zones (paired t test). The differences of distances at the entry zones (and then at the ideal target zones) between the 2-D and 4-D approaches were analysed taking account of location factors in the sagittal (apex, middle, and base) and transversal (paramedian, lateral) sections (one-factor ANOVA). Biopsy reproducibility analysis was performed by looking at the deviation from the mean (paired t test). A nonparametric test (Mann-Whitney test) was performed to determine the statistical influence of each biopsy guidance mode on the percentage of the prostate covered by only one biopsy.
The standard biopsy protocol was explained to each operator using a summary scheme. The 2-D procedure was carried out first. The second session was held within 3 h to 3 wk. Time required for each guidance modality was comparable and depended on the experience of the operator.
3. Results
In total, 336 biopsies were performed by 14 operators on 12 phantoms per session. The paired series tests involved 158 paired biopsies.
An increase in accuracy in hitting the target zone was identified significantly in 4-D as compared to 2-D procedures (p = 0.0042). In contrast, no significant improvement in biopsy accuracy was found for the entry zone (Fig. 9 and Table 1).
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Fig. 9 Mean distances from entry and target zones in ideal protocol, in 2- and 4-dimensional modes.
Table 1 Summary of biopsy accuracy in reaching ideal theoretical protocol
| No. | Procedure | Mean (mm) ± SD | Paired Student t test | |
|---|---|---|---|---|
| Distance from ideal target zone | 158 | 2-D | 6.79 ± 6.18 | S |
| 4-D | 5.1 ± 4.8 | |||
| Distance from ideal entry zone | 158 | 2-D | 5.28 ± 5.71 | ns |
| 4-D | 5.19 ± 4.83 | |||
2-D = two dimensional; 4-D = four dimensional; S = significant; ns = not significant.
The accuracy in hitting target and entry zones was not statistically different at each prostate location, as shown by one factor analysis (Fig. 10, and Fig. 11).
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Fig. 10 Interaction curve between differences in accuracy in hitting target zone in 2- and 4-dimensional procedures by location on prostate.
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Fig. 11 Interaction curve between differences in accuracy at the entry zone in 2- and 4-dimensional procedures by prostate zone.
A biopsy reproducibility test was performed by looking at the variance in distances at the entry and target points. It showed that reproducibility increased significantly in biopsies towards the target zone with 4-D ultrasound mode (p = 0.0385). However, there is no statistical link, but a trend towards improvement in reproducibility in needle entry points in the phantom (p = 0.0623; Table 2).
Table 2 Biopsy reproducibility study by deviation from mean2 (variance)
| No. | Procedure | Deviation from mean (mm) | Student t test | |
|---|---|---|---|---|
| Variance in distance compared to ideal target zone | 158 | 2-D | 37.95 | 0.0385 S |
| 4-D | 22.9 | |||
| Variance in distance compared to ideal entry zone | 158 | 2-D | 32.43 | 0.0623 ns |
| 4-D | 23.18 | |||
2-D = two dimensional; 4-D = 4 dimensional; S = significant; ns = not significant.
The biopsy distribution data did not show any significant difference in the prostate volume explored under 2-D and 4-D ultrasound guidance (p = 0.44). The sampled volume percentage through which only one biopsy runs was 56.9% under 2-D guidance, as compared to 56.7% under 4-D guidance (p = 0.98; Table 3).
Table 3 Study of biopsy dispersion by measuring volume per biopsy and percentage of the prostate sampled by only one biopsy
| No. | Procedure | Median, (interquartile range) | Mean ± SD | Minimum | Maximum | p | |
|---|---|---|---|---|---|---|---|
| Volume sampled per biopsy | 14 | 2-D | 963 (209) | 971 ± 166 mm3 | 751 mm3 | 1271 mm3 | ns |
| 4-D | 907 (258) | 1025 ± 184 mm3 | 777 mm3 | 1490 mm3 | |||
| Percentage of sampled prostate through which only one biopsy runs | 14 | 2-D | 0.576 (0,168) | 0.567 ± 0.093 | 0.46 | 0.707 | ns |
| 4-D | 0.582 (0,199) | 0.571 ± 0.117 | 0.42 | 0.782 | |||
2-D = two dimensional; 4-D = four dimensional; ns = not significant.
4. Discussion
We have observed that, on a phantom model, biopsy accuracy on the zones to be sampled improved with 4-D guidance. This illustrates the fact that multidimensional visualisation improves the operator's ability to hit the virtual target. The improved reproducibility in execution shows the robustness of the guidance. In contrast, no benefits were found, when 3-D real-time reconstruction was used, in volume sampled by the set and in biopsy dispersion. A number of biases were found throughout the work methodology. The most important was introduced by the registration. We saw that only biopsy was performed per phantom, to prevent the operator from being able to see his previous biopsies and benefiting from their guidance. For that reason, at each session, 12 registrations had to be performed. As a result, the risk of bad alignment was increased. Finally, manual registration does not allow for a perfectly reproducible method. Moreover, we saw that the procedure was different from the clinical procedure because of the replacement of the phantom after each biopsy. However, those biases should cancel each other out in that they are present whatever the guidance method.
The various automatic registration techniques developed have not, for the time being, yielded significant results. A registration algorithm is still being developed and could make this analysis more reliable.
It is not easy to find quality criteria for a set of prostate biopsies; the purpose of the biopsies is to detect the tumours. The current TRUS-guided biopsy technique involves randomising biopsies inside the prostate. We set out two objectives: to be as accurate as possible in producing a selected biopsy protocol and to scatter the biopsies so that they would not overlap. We assumed that a biopsy explored a volume equal to the inside of a 5.6-mm radius cylinder. This volume reflects clinical reality, that is, a cancer specimen of significant volume, as currently defined by Epstein (volume of 0.5 cc, Gleason score >6). Our distribution assessment technique explores coverage but does not actually look at how the biopsies spread across the volume. Consequently, a biopsy session should be judged first on accuracy in placing the needle where planned and, second, on the ability to have no needles entering through the same points. This study showed that the first point was improved under 4-D guidance, but not the second.
Regarding accuracy, the results significantly prove that concurrent visualisation of several viewing planes improves the spatial representation of prostate biopsy. In contrast, the low number (14) of operators makes interpreting the results a thorny task as regards biopsy distribution analysis. No significant difference was shown between 2-D and 4-D guidance.
This commercially available technique is reproducible in clinical use. According to this study, the clinical advantages of 4-D guidance do not lie in better cancer detection rate during a first biopsy session. Indeed, the biopsy dispersion is not improved in the study. This would have been a powerful claim for improving the sensitivity of a set of biopsies. However, for repeated biopsies, the needle is more accurately guided to the target zone under 4-D guidance. Moreover, the accuracy in localisation of the technique permits us to establish an exact mapping of the cancer within the prostate. The potential benefits of 4-D guidance will increase with the record of biopsy paths and the real-time guidance of prostate biopsies.
The clinical benefit of establishing a biopsy mapping is clear in two situations: in a histologic suspicious zone around which additional samples should be performed or repeated biopsies in response to a high or rising prostate-specific antigen when the first biopsies were negative [8], and [9].
TIMC Laboratory is developing a biopsy guidance system to enable the execution of a preprocedure planning. The planning could focus on an optimised protocol [10], and [11] or on areas previously sampled by a first set of biopsies. The aim is to detect cancer specimens that are smaller or less detectable during standard biopsy procedures.
The final step is to be able to carry out preprocedure planning focusing on assessment imaging techniques (spectroscopy and injected magnetic resonance imaging) and to perform real-time ultrasound guidance after data registration. The first attempts at computer-assisted guidance, developed at TIMC Laboratory, is currently being tested at the Grenoble University Hospital Centre [12].
5. Conclusions
The study is a step in preoperative assessment of prostate biopsy paths using 3-D ultrasonography. It also makes it possible to demonstrate that real-time 3-D guidance on phantom biopsies offers greater accuracy in determining the needle target and makes biopsy reproducibility better. No evidence has been shown that biopsy distribution is more even in the prostate volume or that the biopsies were better spread.
Editorial Comment
Vincenzo Scattoni .
The authors have experimentally evaluated the accuracy in localisation and distribution of real-time three-dimensional (4-D) ultrasound-guided biopsies (PBx) on a prostate phantom. The authors have demonstrated that 4-D transurethral ultrasound (TRUS) PBx is able to improve the accuracy of hitting the target zone and the ability to reproduce a protocol compared to two-dimensional (2-D) TRUS PBx. This technology is commercially available and easily reproducible in clinical use.
Even if this study is experimental and the clinical advantages are yet to be defined, 4-D TRUS PBx proves its utility because concurrent visualisation of several viewing planes definitely improves the spatial representation of prostate biopsy. The authors believe that the clinical advantage of 4-D guidance may be achieved during repeated biopsies rather than during a first biopsy session. This point is not necessarily true because prostate cancer is very often multifocal and the precise spatial concordance between cancer with atypical small acinar proliferation and high-grade prostatic intraepithelial neoplasia is found only in about 30% and 50% of the patients, respectively [1], [2], and [3]. On the contrary, in my view, increasing the ability to reproduce a precise biopsy scheme might increase the detection rate for prostate cancer [4]. In a prostate-specific antigen era when hypoechoic lesions have reduced their incidence and lost their clinical relevance [5], to hit a precise zone of the prostate that has the highest density of positivity is becoming of utmost importance. I fully agree with the authors that a better visualisation of the prostate with 4-D TRUS may significantly help to reproduce a protocol compared to 2-D TRUS.
Unfortunately, the authors have also demonstrated that 4-D biopsy distribution is not more even in the prostate volume or that biopsies were not better spread. Because the cancer detection rate is mainly dependent on the number and distribution of cores, the possible improvement in cancer detection is questionable.
Such studies are these deserve and, at the same time, urgently necessitate a clinical verification.
References
- [1] M. Roscigno, V. Scattoni, M. Freschi, et al.. Monofocal and plurifocal high-grade prostatic intraepithelial neoplasia on extended prostate biopsies: factors predicting cancer detection on extend repeat biopsy. Urology 63 (2004) (1105 - 1110) Crossref.
- [2] V. Scattoni, M. Roscigno, M. Freschi, et al.. Predictors of prostate cancer after initial diagnosis of atypical small acinar proliferation at 10 to 12 core biopsies. Urology 66 (2005) (1043 - 1047) Crossref.
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Editorial Comment
Bernardo Rocco .
In this paper, the authors compare real-time three-dimensional (4-D) versus two-dimensional (2-D) ultrasound-guided prostate biopsy, using a synthetic prostatic model and simulating biopsy procedures. Investigating the needle trails in the models they found, with the 4-D ultrasonography, a better accuracy in needle placement but no advantages as far as distribution of the sampled volume is concerned.
4-D ultrasonography has been extensively developed as a significant progress in the assessment of fetal behaviour [1]; moreover, better accuracy in biopsy needle guidance for different kinds of tumours has been demonstrated (refs. [4], [5], and [6] in the article). Nevertheless, in contrast to other biopsy procedures, prostate biopsy is mostly a random procedure and the needle is aimed at an area virtually circumscribed rather than a specific target and the need of millimetric precision could be questionable. Furthermore, this paper demonstrates the lack of evidence of better tissue sampling using a 4-D device. Therefore, the cost effectiveness of 4-D ultrasonography in urology could seem unjustified.
Nevertheless, some considerations should be mentioned.
The authors did not report any advantage in terms of tissue distribution due to reduced risk of overlapping needle trails with a 12-biopsy scheme, but this should be assessed even with saturation biopsy schemes that are becoming more common [2]. In fact, with more cores, the increased risk of trails overlapping could be reduced by 4-D guidance.
Moreover, biopsy is gaining a major role as a staging device as well as a diagnostic tool.
Its findings are often considered a significant indicator of disease stage and progression [3]. Therefore, the accurate reproducibility of a biopsy scheme becomes critical when performing a nomogram-based therapeutic strategy, as for a nerve-sparing prostatectomy.
Finally, a more precise guidance would be advantageous for procedures such as brachytherapy or cryotherapy where the accuracy of needle placement can avoid significant risks and complications and even shorten the learning curve.
References
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- [3] M. Graefen, A. Haese, U. Pichlmeier, et al.. A validated strategy for side specific prediction of organ confined prostate cancer: a tool to select for nerve sparing radical prostatectomy. J Urol 165 (2001) (857 - 863)
Conflicts of interest
No commercial relationship.
Sources of funding:
–AFU (French Association of Urology);
–National PHRC prostate-echo 2003.
Acknowledgements
Our thanks to the French Association of Urology (AFU), Sanofi-Aventis for the grant awarded, the national PHRC Prostate Echo 2003 project and ANR (TecSan 2005 program, SMI project). We want to thank Dr P. Mozer, M. Baumann, and A. Leroy for their advice.
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- [8] B. Djavan, Y.K. Fong, V. Ravery, et al.. Are repeat biopsies required in men with PSA levels ≤4 ng/ml? A multiinstitutional prospective European study. Eur Urol 47 (2005) (38 - 44) Abstract, Full-text, PDF, Crossref.
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- [10] M.E. Chen, P. Troncoso, D.A. Johnston, et al.. Optimization of prostate biopsy strategy using computer based analysis. J Urol 158 (1997) (2168 - 2175) Crossref.
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Footnotes
a Urological Surgery and Renal Transplantation Unit, Grenoble University Hospital Centre, Grenoble, France
b TIMC-GMCAO Laboratory (UMR CNRS 5525), domaine de la Merci, Grenoble, France
c Technological Innovative Centre (TIC), Grenoble University Hospital Centre, Grenoble, France
Corresponding author. Urological Surgery and Renal Transplantation Unit, Michallon University Hospital Centre, 38043 Grenoble Cedex 9, France. Fax: +33 4 76 76 56 11.
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