Curr Urol Rep (2014) 15:392 DOI 10.1007/s11934-013-0392-z

NEW IMAGING TECHNIQUES (A ATALA AND A RASTINEHAD, SECTION EDITORS)

Real-Time Elastography for the Detection of Prostate Cancer Georg Salomon & Jonas Schiffmann

# Springer Science+Business Media New York 2014

Abstract The lack of reliable imaging tools in detecting prostate cancer makes a random biopsy still the standard of care to detect prostate cancer. To reduce the number of cores during a biopsy and therefore the risk of biopsy-related complications, an imaging tool which provides reliable guided biopsies is required. Transrectal real-time elastography has shown to have the ability to visualize prostate cancer foci to some extent. In addition to the conventional B-mode image of transrectal ultrasound, it adds information about the stiffness of the prostate tissue. This review highlights the most important studies on elastography to follow the improvements in techniques and to outline the ability to detect prostate cancer and guide biopsies. Keywords Prostate cancer . Imaging . Elastography . Real-time elastography . Guided biopsy . Targeted biopsy . Detection . Shear wave . Multiparametric MRI . Sonoelastography

Introduction The technique of elastography (ELA) (Fig. 1a) was introduced in 1991 [1]. Due to the fact that tumor tissue has a higher cell density, this can lead to a better differentiation of benign and malignant tissues. This can be displayed on the video screen next to the B-mode image in different colors. One of the major This article is part of the Topical Collection on New Imaging Techniques G. Salomon (*) : J. Schiffmann Martini-Clinic, Prostate Cancer Center, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany e-mail: [email protected] J. Schiffmann e-mail: [email protected]

benefits of ELA compared to other imaging techniques is its ability to have a real-time visualization. Since 1991 there have been some technical improvements which make ELA an interesting imaging tool that has proven helpful during daily clinical work to guide biopsies or potentially avoid them. At this stage, according to recent publications, real-time elastography (RTE) increases the detection rate of prostate cancer (PCA). In combination with systematic biopsies, it also might decrease the number of necessary biopsy cores. More than 150 original or review articles are dealing with ultrasound ELA in PCA detection. The majority of these publications show a benefit of PCA detection using ELA, although multi-center studies are missing. This review highlights the most important studies on ELA to follow the technical improvements and to outline the ability to detect prostate cancer and guide biopsies.

Elastography in Comparison with Radical Prostatectomy Specimens There are several studies comparing ELA results with final histopathology from radical prostatectomy (RP) specimens [2, 3•, 4••, 5–7, 8••, 9–11] (Table 1). Results in these studies slightly differ and attest to the RTE technology’s good accuracy in tumor detection. The largest study adressing this issue [4••] includes 109 patients and reported sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of 75.4 %, 76.6 %, 87.8 % and 59.0 %, respectively. Since these patients had a proven PCA with ELA prior to RP, a selection bias has to be taken into account regarding the reported results. The ranges for sensitivity and specificity throughout all studies were 49.0 % to 88.0 % [2, 8••] and 65.0 % to 89.5 % [7, 11], respectively. There is a consistency in recent studies that the detection rate increases with the size of the tumor and higher Gleason

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Fig. 1 a Real-Time Elastography (Hitachi), stiff areas are displayed in dark blue areas. In this case the dark blue, reproducible portion on the right side of the image is supposed to be cancerous tissue. b Shear wave

Elastography (Supersonic, Aixplorer), stiffness of the tissue is displayed in different colors. The region of interest is circled and the stiffness of the tissue is calculated in kPa

grades [11]. Zhu et al. [11] reported a better detection for Gleason >7 (80.4 %) compared to Gleason 5 mm vs. 20 ng/ml: 93.0 96.2

86.9 Per patient: 51.0 Per core: 36.0 Only peripheral zone: 66.0 72.6 Per patient: 84.6 Per sextant: 57.7 67.9 51.1 68.0 Per patient: 25.0 Per core: * 74.0 * *

Sensitivity (%)

* Per patient: 86.8 Per core: 100.0 65.7 65.1 PSA: 20 ng/ml: 93.0 96.2

62.2 66.5 81.0 Per patient: 86.0 Per core: * 60.0 * *

71.9 Per patient: 75.0 Per core: 93.0 Only peripheral zone: 78.0 * *

Specificity (%)

69.4

21.9 75.8 *

57.6 49.0 68.0 Per patient: 20.0 Per core: 24.0 39.0 12.7 Per patient: 56.5 Per lesion: 59.1 22.4 *

61.6 Per patient: 64.0 Per core: 72.0 Only peripheral zone: 77.0 * *

PPV (%)

99.6

68.6 * *

* *

91.4 Per patient: 64.0 Per core: 74.0 Only peripheral zone: 67.0 * Per patient: 86.7 Per sextant: 93.6 71.9 49.9 81.0 Per patient: 88.0 Per core: * 93.0 * *

NPV (%)

*

* 0.75 *

* *

* * *

* * 82.0 *

*

53.9 73.6 *

* *

* * *

* * 76.0 *

* *

*

* *

77.0

*

Accuracy

*

AUC

PPV: positive predictive value, NPV: negative predictive value, AUC: Area under the receiver operating curve, *: not stated, ELA: Elastography, vs: versus, RTE: Real-Time Elastography, SWE: Shear Wave Elastography

Study design

Author

Table 2 Elastography in comparision to biopsy and / or targeted biopsies

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sufficient enough for an accurate prediction. To get more precise information, studies analyzing targeted biopsies are necessary.

Real-Time Elastography Targeted Biopsies RTE provides the ability to perform targeted biopsies (Table 2). First generation ELA scanners cannot compete with the modern techniques currently in use. König et al. [19] reported in 2005 on the potential benefit of ELA compared to conventional B-mode ultrasound. The detection rate for PCA per patient was higher for ELA (84.1 %) compared to B-mode ultrasound (32.5 %). However, regarding the per core detection for ELA, the sensitivity, specificity, PPV, and NPV were 51.1 %, 66.5 %, 49.0 % and 49.9 %, respectively. Around half of the patients (48.3 %) had a positive digital rectal examination (DRE), which does not reflect today’s cohort of patients. In addition, the reference test was a positive biopsy, which cannot rule out the real prevalence of prostate cancer in this cohort of patients. Eggert et al. [20], also using a first generation ELA scanner, could not confirm these results and showed no benefit for ELA vs. B-mode sonography (40.2 % vs. 37.7 %) in overall detection rates of PCA. Using actual ELA scanner technology, several studies are addressing this issue [13, 21•, 22••, 23, 24•, 25–29]. The range of sensitivity, specificity, PPV, and NPV in predicting positive targeted biopsies by ELA were 24.4 % to 92.3 %, 60.0 % to 100.0 %, 12.2 % to 75.8 % and 68.6 % to 93.6 %, respectively. Reported AUCs for predicting PCA in the peripheral zone of the prostate were between 0.85 and 0.96 [13, 25]. Pallwein et al. analyzed 230 men with 1109 targeted biopsy cores and reported about a PPV of 12.2 % [29], whereas Zhang et al. [13] analyzed 148 men with RTE targeted biopsies and reported about a sensitivity, specificity, PPV, and AUC of 92.3 %, 77.1 %, 75.8 % and 0.85, respectively. Here the detection rate was superior for the RTE targeted biopsies compared to TRUS targeted biopsies (75.8 % vs. 65.6 %). Recently Salomon et al. reported about an incremental detection of about 7.1 % when adding 4 ELA targeted biopsy cores to a 10-core random biopsy examination within 1,024 patients [30]. In addition Aigner et al. [21•] reported about a sensitivity, specificity, PPV, and NPV in RTE targeted biopsies of 74.0 %, 60.0 %, 39.0 % and 93.0 %, respectively. Compared to a random 10-core biopsy, the per core detection rate was 4.7-fold higher within the RTE targeted biopsy cores. Ganzer et al. [24•] reported about a better PPV for RTE targeted biopsies compared to random biopsies (22.4 % vs. 9.2 %). Also, the mean percentage of prostate cancer per core

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from corresponding areas was significantly higher in RTE targeted compared to random biopsy cores (21.5 % vs. 16.4 %). Recently Taverna et al. [26] reported about a sensitivity, specificity, PPV, NPV, and accuracy for ELA targeted biopsies of 24.4 %, 65.7 %, 21.9 %, 68.6 % and 53.9 %, respectively. Only one patient’s condition (0.9 %) was detected exclusively by ELA targeted biopsies. In this study two experienced sonographers performed a double-blinded RTE to reduce the interpretative subjectivity of the images. Interestingly, patients with a positive DRE or trans-rectal ultrasound were excluded from this study. In our eyes, this does not reflect clinical reality since the aim of RTE should be to optimize the diagnosis of PCA on a clinically routine basis. This study used a scoring system, previously described by Kamoi et al. [27] and Itoh et al. [31], which ranges from score I to V. The best result, i.e. to detect cancerous tissue, was a score of 5. &

The majority of the studies show a better PPV for targeted biopsies compared to systematic biopsies.

Scoring System The utilization for a classification or interpretation system of images is mandatory to minimize intra-observer and interobserver variability. In case of mpMRI, the prostate imaging reporting and data system (PI-RADS) classification is getting more and more popular. Not only will this make results more objective, but it will lead to a better acceptance of this method. In the case of ELA, which is a very subjective method, there are some existing approaches for scoring systems. König et al. [19] introduced a three-criterion decision tool: 1) the suspicious area should reveal stiff tissue; 2) it has to be reproducible; and 3) there is no correlation with a benign lesion, e.g. a node with benign prostate hyperplasia, in TRUS. This was described by Zhang et al. [13] as failing to some extent, because there were overlaps between benign and malignant lesions. A more detailed five-point scoring system was used by Itoh et al.[31] and Kamoi et al.[27] in which lesions are classified according to the tissue´s stiffness and reproducibility as follows: benign, probably benign, indeterminate, probably malignant, and definitely malignant. The Hamburg group [32••] used the three criteria scores in a prospective study in which more than 400 patients were judged according to the ELA as low (no elastographic signs of PCA,), intermediate (5 mm and reproducible) suspicion for PCA. The reference was a positive biopsy, which followed after the examination. About 20 % of patients classified in the low suspicion group exhibited PCA in the biopsy, although most of them were Gleason 3+3 tumors. In turn, the high suspicion group had a PPV >75 % for a positive biopsy, with more aggressive tumors.

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Developments in Elastography The ELA technique was first described 20 years ago. Since that time, there have been new developments in the techniques of ELA. Whereas the first generation scanners, which were used in one of the initial studies [19], did not show to be beneficial over conventional B-mode images and systematic biopsies [20], the new scanners not only improved in the quality of ELA but also in the image quality itself. Different ultrasound companies offer the ELA technique. In principle, there are two approaches to the ultrasound ELA technique: strain ELA and shear wave ELA. The shear wave elastography (SWE) (Fig. 1b) technology might be benefical for the inexperienced user, since the elastograms are being produced without any manual assistance of the examiner. There is an automated generation of the elastograms by the calculation of shear wave velocity. In contrast, for the strain ELA, the examiner has to manually compress and decompress the tissue. The elastographic findings will be displayed in different colors in regards to the stiffness of the tissue on the video screen. Most of the studies have been performed using the Hitachi RTE (HI-RTE).

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array coils in patients with proven PCA prior to RP. Sensitivity and specificity, according to 16 different parts of the prostate gland were between 44.1 % to 58.9 % and 83.0 % to 74.8 % for RTE and 36.7 % to 43.1 % and 85.9 % to 79.8 % for MRI. Whereas RTE had a better detection rate in apical and middle parts in contrast to MRI (66.7 %-80.0 % vs. 41.7 %-60.0 %), MRI had superior results in the gland´s base (14.9 % vs. 19.4 %) and transitional zone (29.6 % vs. 34.7 %). Sensitivity and specificity were not different when comparing RTE and MRI in detecting capsular involvement (79.2 % vs. 80.8 % and 80.0 % vs. 70.0 %), and both techniques seem to be equal. A new tool which provides a fusion of B-mode sonography, ELA, and mpMRI is now available, but first results are still awaited. & &

Elastography showed similar results in the detection of PCA in the prostate compared to multiparametric MRI. Advantages for MRI or ELA for different regions have been described; therefore, a fusion of both modalities might increase the accuracy in the diagnosis of PCA.

Shear Wave Elastography Real-Time Elastography in Comparison with Magnetic Resonance Imaging Three studies suggest an improved [6] or equal [22••, 33••] detection rate of PCA for RTE compared to T2-weighted endorectal 1.5 Tesla magnetic resonance imaging (MRI), with or without dynamic contrast enhanced imaging [6] (DCEI). Sumara et al. [6] reported about a 74.1 % detection rate for RTE and 42.1 % for T2-weighted endorectal MRI in seventeen patients prior to RP. Aigner et al. [22••] analyzed 33 patients with RTE and MRI prior to systematic biopsy and reported a sensitivity and NPV per patient of 84.6 % and 86.7 % (RTE) and 84.6 % and 83.3 % (MRI), respectively. The per sextant analysis showed a sensitivity and NPV of 57.7 % and 93.6 % (RTE) and 50.0 % and 92.2 % (MRI), respectively. Both studies investigated patients with relatively high mean PSA values (10.5 ng/ml and 9.3 ng/ml), which might not reflect patients in a typical “screening” population, and a number of patients were relatively low. Also, the biopsies were not guided, and the results do not have to reflect findings from the actual suspicious spots from RTE and MRI. Interestingly, the additional use of DCEI [6] with the T2weighted imaging does not improve the MRI results and revealed even worse results than without DCEI [22••]. Currently, the state of the art MRI [34] for the diagnosis of PCA should be at least a 1.5 Tesla MRI with DCEI and diffusion weighted imaging (DWI), using the PI-RADS classification for reporting about suspicious areas. A recent publication [33••] showed equal results comparing RTE with four different modalities at 3.0 T using endorectal and body-phased

Limitations for ELA in the prostate are that it has some inability to differentiate PCA foci from chronic prostatitis [35]. The SWE technology offers a tool to measure the stiffness of the tissue (kPa). It is, to some extent, possible to use these values as cut-offs for benign or malignant tissue. Our group (data not published yet) found a cut-off >55 kPa that the tissue is more likely (accuracy: 78 %) to be prostate cancer rather than benign tissue. Predicting positive cores using SWE prior to a random biopsy with a cut-off of 37 kPA between benign and malignant tissue, Barr et al. [35] reported about a sensitivity, specificity, PPV, and NPV of 96.2 %, 96.2 %, 69.4 % and 99.6 %, respectively. According to Ahmad et al. [36], the sensitivity and specificity in predicting positive biopsy cores by SWE was slightly rising in patients with higher PSA levels (Table 2).

Conclusion Different elastographic techniques exist. Improvements in the techniques have provided better results. Whether SWE technology will yield the benefit of more objective interpretation of lesions in the prostate remains to be shown in larger studies. Promising sensitivity and specificity up to 88.0 % [2] and 89.5 % [11] were reported when comparing ELA results prior to RP with final histopathological results. Detection rates increased according to higher Gleason grades [11] and bigger tumor size [5, 9]. Major drawbacks of these study designs are that 1) all of these patients were scheduled for RP, and the

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investigators knew that the patients had proven PCA; and 2) the transitional zone has not been included in the analysis for most of these studies. Comparing ELA results prior to a random biopsy without using targeted biopsies is a questionable study design. We cannot be sure if the suspicious spots from the ELA examination are really reflected by the non-targeted random biopsy cores. However, the results were promising and justified further studies with targeted RTE biopsies. Regarding RTE targeted biopsies, encouraging results were reported regarding the peripheral zone of the prostate, with a sensitivity and specificity of 92.3 % [13] and 100 % [25], respectively. These exciting results were not always reproducible, and sensitivity and specificity were also reported to be 24.4 % [26] and 60.0 % [21•], respectively. Scoring systems are available to standardize ELA findings and help to increase the detection rates of PCA. Studies which are comparing ELA and MRI results with biopsy or RP findings are sparse and suggest, with a caveat on methodological limitations, comparable results for both techniques. Results have depended on different regions of the prostate. Interesting new tools performing a fusion of mpMRI, TRUS, and ELA are now available, and first results are awaited. In summary, ELA is a promising tool with the potential to assist, especially for additional targeted biopsies. However, the results are still too inconstant and not reliable enough to waive justified random biopsies because of ELA findings. Elastography is not recommended for initial biopsies in the EAU guidelines. This might be due to missing prospective, multicenter evaluations of elastography. A European multicenter study has been launched in the beginning of 2013 and should elucidate the benefit of elastography targeted biopsies. Compliance with Ethics Guidelines Conflict of Interest Dr. Georg Salomon and Dr. Jonas Schiffmann each declare no potential conflicts of interest relevant to this article. Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.

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Real-time elastography for the detection of prostate cancer.

The lack of reliable imaging tools in detecting prostate cancer makes a random biopsy still the standard of care to detect prostate cancer. To reduce ...
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