British Journal of Radiology (2005) 78, S103-S111
© 2005 British Institute of Radiology
doi: 10.1259/bjr/11253478
MR imaging and MR spectroscopic imaging in the pre-treatment evaluation of prostate cancer
H Hricak, MD, PhD
Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue C278, New York, NY 10021 USA
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Abstract
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Magnetic resonance imaging (MRI) and proton magnetic resonance spectroscopy (1H MRSI) are emerging as the most sensitive tools for the non-invasive, anatomic and metabolic evaluation of prostate cancer. This article reviews the current applications of MRI and 1H MRSI in clinical practice and discusses the promise of these modalities for improving prostate cancer management. MRI demonstrates zonal anatomy with excellent contrast resolution and can reveal tumours in areas not routinely sampled on biopsy and not palpable on digital rectal examination. In addition, MR images allow assessment of local extent (including extracapsular extension and seminal vesicle invasion) and thus can assist in local staging while providing surgeons and radiation therapists with a visual road-map for treatment planning. The addition of 1H MRSI to MRI can improve prostate cancer detection and assessment of tumour volume; it also contributes indirectly to improved local staging. In addition, 1H MRSI metabolic and volumetric data correlate with pathological Gleason grade and thus may offer a non-invasive means to better predict prostate cancer aggressiveness. Combined MRI/1H MRSI is currently of greatest value for high-risk patients. With greater understanding of the relationship between spectroscopic data and tumour biology, it may become possible to use MRI/1H MRSI to achieve more precise stratification of patients in clinical trials, to monitor the progress of patients who select watchful waiting or minimally aggressive cancer therapies, and to guide and assess emerging local prostate cancer therapies.
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Introduction
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The high incidence of prostate cancer (it is now the most commonly diagnosed cancer in men in the UK and the USA), combined with earlier detection, downstaging at the time of diagnosis, and the slow natural progression of this disease, has made its management a complex and controversial issue [1, 2]. Depending on patient age at diagnosis, the stage and aggressiveness of the tumour, the potential side-effects of the treatment, and patient comorbidity [3–5], the options for treatment may include deferred therapy, androgen ablation, radical surgery, and various forms of radiation therapy (brachytherapy, external beam irradiation, including intensity-modulated radiation therapy (IMRT), and combinations) [6, 7]. Radical prostatectomy is still the most commonly recommended treatment for patients with a life expectancy of at least 10 years [8]. Because the most common treatment side-effects – erectile dysfunction and urinary incontinence – are serious, there is a growing demand for patient-specific therapies that can reduce treatment morbidity while maximizing treatment benefits.
Although reports on the value of MRI in prostate cancer management have been contradictory, there is no doubt that MRI has an essential role to play in making safer, more individualized therapies possible. By revealing the anatomical location of prostate tumours, MRI can aid in staging and also provide a road-map for surgery or for radiation treatment. Moreover, the addition of proton MR spectroscopic imaging (1H MRSI) to MRI can further improve cancer localization while enhancing the assessment of tumour aggressiveness, volume and extent. This article will review the role of MRI and 1H MRSI in prostate cancer management, presenting guidelines for appropriate usage; it will also discuss the potential of these modalities for improving prostate cancer management in the future.
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MRI and 1H MR spectroscopic imaging techniques
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Although the "optimal" choice of equipment (specifically, magnet strength) and imaging sequences depends on the instruments available, this section presents general guidelines for diagnostic MR examination of the prostate. Because a combination of MRI and spectroscopic imaging is desirable, a magnet strength of at least 1.5 T is required. The combined use of an endorectal coil with a pelvic phased-array coil and the generation of faster imaging sequences are advisable. Scanning parameters depend on the type of scanner and the field strength, but in general, the following imaging sequences are recommended: (1) T1 weighted axial images of the pelvic region are used for the detection of nodal disease and post-biopsy intraglandular haemorrhage; (2) thin-section (3 mm) T2 weighted images with a smaller field of view ( 
14 cm) in the axial, sagittal and coronal planes are used for tumour detection, localization and staging. The use of dynamic contrast-enhanced MRI is optional [9–11]. Post-biopsy haemorrhage may hamper tumour detection in the prostate, leading to either under- or over-estimation of the tumour presence and local extent. Therefore, MRI should be delayed for at least 4 to 8 weeks after prostate biopsy [12, 13].
A number of different 1H MR spectroscopic techniques have been described. The spectroscopic imaging techniques that are at present commercially available include chemical shift imaging [14] with point resolved spectroscopy (PRESS) voxel excitation and band selective inversion with gradient dephasing (BASING) for water and lipid suppression [15]. Chemical shift imaging refers to the multi-voxel technique allowing the acquisition of voxels in single or multiple slices. The PRESS technique generates a cubic or rectangular voxel by the acquisition of three orthogonal slice selective pulses, i.e. a 90-degree pulse followed by two 180-degree pulses. The setup for spectroscopic imaging is the same as for morphological imaging, and both data sets are usually acquired in the same examination in order to overlay metabolic information directly on the corresponding anatomic display. The combined MRI/1H MRSI examination takes approximately 1 h.
Recognition of prostate cancer on MRI
The signal intensity and detection of prostate cancer on MRI depend on the type of imaging sequence used. On T1 weighted images, the prostate demonstrates homogeneous medium signal intensity. On T2 weighted MR images, the zonal anatomy of the prostate can be seen, and cancer most commonly demonstrates decreased signal intensity within the high-signal-intensity normal peripheral zone [16] (Figure 1
). However, low signal intensity in the peripheral zone can also be seen in several benign conditions such as haemorrhage, prostatitis, hyperplastic nodules, or sequelae resulting from radiation or hormonal treatment.
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Figure 1. Clinical stage T2b prostate cancer. (a) Axial T2 weighted MR image demonstrates a large low signal intensity area in the left peripheral zone with obliteration of the rectoprostatic angle (arrow), indicating left side extracapsular invasion. (b) MR spectra show large-volume disease (all eight voxels are abnormal) with absence of citrate and marked elevation of choline, indicating high-grade disease. (c) Step-section pathology confirms large-volume tumour with left side extracapsular extension. Pathology stage pT3a, Gleason grade 4+3.
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Recognition of prostate cancer on MR spectroscopy
MRSI provides metabolic information about prostatic tissue by displaying the relative concentrations of chemical compounds within contiguous small volumes of interest (voxels). Currently, three-dimensional (3D) proton MRSI metabolic mapping of the entire gland is possible with a resolution of 0.24 ml or smaller, depending on the parameters used. Proton MRSI displays concentrations of citrate, creatine, choline and polyamines. Normal prostate tissue contains high levels of citrate—higher in the peripheral zone than in the central and transition zones. Glandular hyperplastic nodules, however, can demonstrate citrate levels as high as those observed in the peripheral zone. In the presence of prostate cancer, the citrate level is diminished or not detectable because of a conversion from citrate-producing to citrate-oxidating metabolism. The choline is elevated due to a high phospholipid cell membrane turnover in the proliferating malignant tissue. Hence the method for depicting tumours is based on an increased choline to citrate ratio. Because the creatine peak is very close to the choline peak in the spectral trace, the two may be inseparable; therefore, for practical purposes, the choline+creatine/citrate ratio ([Cho+Cr]/Cit) is used for the spectral analysis in the clinical setting (Figure 1
). With the latest spectroscopic sequence, polyamine peaks can be resolved as well. The polyamine peak decreases in the presence of prostate cancer.
Although spectral interpretation is still in its early stage, the classification described by Kurhanewicz et al [17] is often used; it classifies a voxel as normal, suspicious for cancer, or very suspicious for cancer. Furthermore, a voxel may contain non-diagnostic levels of metabolites or artefact that obscures the metabolite frequency range. Voxels are considered suspicious for cancer if (Cho+Cr)/Cit is at least 2 standard deviations above the average ratio for the normal peripheral zone, and voxels are considered very suspicious for cancer if (Cho+Cr)/Cit is more than 3 standard deviations above the average ratio [18] (Figure 1). Voxels considered non-diagnostic contain no metabolites with signal-to-noise ratios greater than 5. In voxels where only one metabolite is detectable, the other metabolites are assigned a value equivalent to the noise standard deviation. 1H MRSI permits analysis of metabolism in the entire prostate gland.
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Role of MRI and 1H MRSI in prostate cancer detection and localization
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Prostate cancer is a multifocal and histologically heterogeneous disease. Although biopsy is considered the preferred method for prostate cancer detection and characterization, estimates suggest that even with a threshold PSA value of 4.1 ng ml–1, biopsy will miss 82% of cancers in men less than 60 years old and 65% of cancers in men 60 years of age or older [19]. In fact, when biopsy results were compared with radical prostatectomy for sextant tumour localization, the positive predictive value of biopsy was 83.3%, and the negative predictive value was 36.4% [20]. In another study, sextant biopsies missed up to 30% of cancers [21] and were not accurate for defining the location and extent of prostatic carcinoma [22]. While combined MRI/1H MRSI is not used as a first approach to diagnose prostate cancer, it can be useful for directing targeted biopsy, especially for patients with PSA levels indicative of cancer but with negative previous biopsy results; this situation occurs most frequently with lesions in the anterior peripheral or transition zones (i.e. regions not palpable by digital rectal examination (DRE) and often not sampled during biopsy) [23, 24]. Combined MRI/1H MRSI has shown excellent sensitivity and specificity for detecting cancer in the peripheral zone (though with only modest interobserver agreement) [25]. In a recent study comparing DRE, transrectal ultrasound (TRUS) and endorectal MRI in the detection and localization of prostate cancer [26], MRI performed significantly better than DRE in detecting cancer in the apex, mid-gland, and base, and significantly better than TRUS-guided biopsy in the mid-gland and base (Figure 2). Unlike either DRE or TRUS-guided biopsy, MRI is also capable of detecting tumour in the transition zone, a capability that is enhanced by the use of MRSI (Figure 3) [23]. The use of MRI/1H MRSI may reduce the rate of false-negative biopsies and hence decrease the need for more extensive biopsy protocols and multiple repeat biopsy procedures [27]. Moreover, combined MRI/1H MRSI can estimate the tumour volume within the prostate gland better than MRI alone.
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Figure 2. Clinical stage T1c prostate cancer (non-palpable, biopsy-detected cancer). (a) Axial T2 weighted MR image show a large tumour on the left side of the peripheral zone with a focal bulge and asymmetry of the neurovascular bundle (arrowhead). (b) Sagittal T2 weighted MR image shows a large volume mid-to-base tumour with direct extension into the left seminal vesicle (arrow). On MRI, tumour stage is T3b. Corresponding step-section pathology shows sites of focal extracapsular extension (c) and left seminal vesicle invasion (d, arrowhead) (pathology stage pT3b), confirming the MRI tumour stage.
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Figure 3. Clinical stage T1c prostate cancer. (a) Axial T2 weighted MR image shows a large tumour (T) in the transition zone. There is interruption of the low signal fibromuscular stroma (arrows) suggestive of anterior extracapsular extension and thus indicating T3a disease. Corresponding step-section pathology (b) shows the tumour in the transition zone and site of established extracapsular extension. Pathology stage pT3A.
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One of the most challenging characteristics of prostate cancer is its variability in biological aggressiveness. Biopsy specimens are also not accurate in the prediction of Gleason grade. Studies of 226 and 449 patients found that biopsy correctly predicted radical prostatectomy Gleason grade in 31% and 58% of cases, respectively [28, 29]. Proton MRSI has the potential to provide a non-invasive means of improving the assessment of prostate cancer aggressiveness. It has been shown that the ratio of (Cho+Cr) to Cit in the lesion correlates with the Gleason grade, with the elevation of choline and reduction of citrate indicating increased cancer aggressiveness (Figures 1 and 4) [30]. Since Gleason grade is an important predictor of patient outcome, this finding provides an important rationale for adding MRI/1H MRSI to the pre-treatment evaluation of prostate cancer patients.
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Figure 4. Clinical stage T1c prostate cancer, Gleason grade 3+3. (a) Axial T2 weighted MR image shows foci of low-signal-intensity areas in the right and left sides of the peripheral zone. The tumour is organ-confined. In the region of cancer, MR spectra (b) show that citrate, although decreased, is still present, while choline is moderately elevated, indicating low-grade tumour. (c) Step-section pathology shows scattered organ-confined disease and confirms Gleason grade 3+3, pT2b.
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Role of MRI and 1H MRSI in prostate cancer staging
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While historically, the staging of prostate cancer was based on Jewett classification, in the last 10 years TNM staging has prevailed. At present, however, both staging systems are in common use particularly in the USA. TNM staging of prostate cancer has undergone a number of modifications, the latest ones having been made in 2002. The 2002 revised TNM system, shown in Table 1, is clinically useful and precisely stratifies newly diagnosed patients [31].
Clinical T-staging is largely dependent on imaging. Compared with CT, ultrasound and DRE, MRI has higher accuracy in the assessment of unilateral or bilateral disease (stage T2), extracapsular extension and seminal vesicle invasion (stage T3), and the invasion of adjacent structures (stage T4). However, the literature shows a wide range (from 50% to 92%) in the accuracy of local staging by MRI [32]. Despite the high specificity of MRI in identifying organ-confined disease and extracapsular extension, due to lower sensitivity and substantial interobserver variability, the routine use of MRI in local staging of prostate cancer remains controversial.
A recent study by Wang et al has shown that MRI contributes significant incremental value to clinical variables in the prediction of extracapsular extension [33]. On endorectal MRI, the criteria for extracapsular extension include a contour deformity with a step-off or angulated margin; an irregular bulge or edge retraction; a breach of the capsule with evidence of direct tumour extension; obliteration of the recto-prostatic angle (Figure 1); and asymmetry of the neurovascular bundles (Figure 2) [34, 35]. While transaxial planes of section are essential in the evaluation of extracapsular invasion, the combination of transaxial and coronal plane images facilitates the diagnosis of extracapsular extension. The addition of volumetric data from 1H MRSI to the anatomical display of MRI significantly improves the evaluation of extracapsular extension and decreases interobserver variability [36].
MRI is also useful for demonstrating seminal vesicle invasion. The criteria for seminal vesicle invasion on endorectal MRI include contiguous low signal-intensity tumour extension from the base of the gland into the seminal vesicles; tumour extension along the ejaculatory duct (non-visualization of the ejaculatory duct); asymmetric decrease in the signal intensity of the seminal vesicles; and decreased conspicuity of the seminal vesicle wall on T2 weighted images (Figure 5). Combined axial, coronal and sagittal planes of section facilitate evaluation of seminal vesical and bladder neck invasion [37].
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Figure 5. Clinical stage T2b prostate cancer. MRI (section not shown) demonstrated large volume cancer. Axial T2 weighted image shows gross left seminal vesicle invasion (arrow) indicating MR stage T3b disease, which was confirmed at surgical pathology.
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In a secondary study of the same data analysed by Wang et al [33], Mullerad et al demonstrated that the incremental value of endorectal MRI in predicting extracapsular extension was only significant when interpretation was performed by genitourinary radiologists with substantial experience in endorectal MRI [38]. This suggests that the recent improvement in the performance of MRI can be attributed to increased reader experience as well as to the maturation of MRI technology (e.g. faster imaging sequences, more powerful gradient coils, and post-processing image correction), and better understanding of morphological criteria used to diagnose extracapsular extension or seminal vesicle invasion.
In the evaluation of lymph node metastases, efficacy data for MRI and CT are similar, with both modalities having low sensitivity. Promising results have been reported for the use of ultra-small, super-paramagnetic iron oxide particles as an aid to diagnosing lymph node metastases by MRI [39, 40]. These particles are taken up by normal nodal tissue but not by metastatic tissue, providing tissue contrast within the lymph node and allowing detection of metastases. The sensitivity of MRI for metastases may be increased through use of these compounds, since they appear to permit detection of metastases in normal-sized nodes [39, 40].
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The use of MRI and combined MRI/1H MRSI in treatment planning
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Risk-adjusted, patient-specific therapy designed to maximize cancer control while minimizing the risks of complications is being mandated. Such an approach requires accurate characterization of the cancer location and extent. Optimal treatment for prostate cancer is best selected based on clinical TNM stage, Gleason grade and PSA level. The decision to treat should also be made in the context of the patient's age, disease stage, and associated medical illnesses, as well as on his personal preferences.
As we have seen, the inclusion of MRI/1H MRSI findings in clinical nomograms improves prediction of cancer extent, thereby improving patient selection for local therapy. Furthermore, as described below, information from MRI/1H MRSI can assist in planning how best to apply the treatment chosen, whether it be surgery or a form of radiation therapy.
Surgery
Most cancers treated today are not palpable, and apart from the information obtained by ultrasound and biopsy, the surgeon has limited information about the size, location and extent of the cancer. MRI can help to refine the surgical plan, to maximize the preservation of periprostatic tissues (important for recovery of urinary and sexual function), and to minimize the risk of positive surgical margins. The use of endorectal coil MRI prior to radical prostatectomy has been shown to improve the surgeon's decision regarding whether to spare or to resect the neurovascular bundles [41]. MRI can also be useful in predicting intraoperative blood loss during radical retropubic prostatectomy (i.e. a cutoff value of 4 mm separation from tumour to apical periprostatic veins on MRI is correlated with greater blood loss) [42]. In addition, MRI can help predict urinary incontinence after radical retropubic prostatectomy. In a series of 211 patients, Coakley et al [43] demonstrated that membranous urethral length, as measured on MRI, correlated with the return of urinary continence after surgery. Patients with a longer membranous urethra regain urinary continence significantly more rapidly [43].
Radiotherapy
The most commonly used forms of radiation therapy for prostate cancer are brachytherapy, 3D conformal therapy (3D-CRT), and intensity-modulated radiation therapy (IMRT). The guidelines for the optimal choice of treatment are not well established and the choices are often empirical. Several retrospective analyses and the early results of clinical trials indicate that an increased radiation dose is associated with reduced rates of biochemical failure and may, therefore, increase local control rates and decrease the risk for distant metastasis and the overall mortality rate [44–46]. This observation is important for management of intermediate- and high-risk prostate cancer patients; however, increased radiation doses may be associated with a risk of treatment morbidity [47]. 3D-CRT, IMRT and brachytherapy all offer the possibility of combining very high radiation doses in areas of high tumour-cell density within the prostate gland without significantly increasing the risk of normal tissue damage. Because of its ability to show tumour location and extent, MRI can be of tremendous help in radiation treatment planning, which requires knowledge of tumour location, volume and extent (Figure 6).
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Figure 6. Clinical stage T1c prostate cancer. Coronal T2 weighted image shows tumour (T) in the transition zone; tumour abuts the right wall of the urethra (U). The left wall of the prostatic urethra (arrows) is normal. As a result of imaging, the treatment plan was changed from brachytherapy to IMRT.
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Further implementation of these advanced therapeutic techniques has increased the interest in imaging techniques that are able to map tumour volume or localize more aggressive regions within the tumour, such as highly proliferating or hypoxic foci [48]. Such imaging-optimized dose delivery has shifted radiotherapy treatment planning towards a more individualized treatment approach. MRI is more accurate than CT in defining the prostate volume, with the greatest discrepancy being in the apex and posterior parts of the gland and the seminal vesicles [49–51]. CT-derived prostate volumes are larger than MRI-derived volumes [49]. MRI is also more accurate for the anatomic delineation of surrounding organs, such as the rectal wall, the sigmoid, the urethra and the penile bulb, which are at risk for radiation-induced tissue damage. The dose delivered to the rectal wall and bulb of the penis is significantly reduced with treatment plans based on the MRI-delineated prostate anatomy compared with treatment plans based on the CT-delineated prostate anatomy, decreasing the risk of rectal and urological complications [52]. Metabolic mapping of the prostate gland by 1H MRSI offers the possibility for tumour-targeted radiotherapy (i.e. intraprostatic dose escalation), applicable both by external radiation treatment and brachytherapy [53, 54].
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Summary
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MRI and 1H MRSI are emerging as the most sensitive tools for the anatomical and metabolic evaluation of prostate cancer. The improved performance of MRI/1H MRSI in the last several years is likely due to the maturation of MR technology, including improvements in MRI acquisition techniques, a better understanding of morphological criteria used to diagnose extraprostatic disease, and increased reader experience. The addition of 1H MRSI to MRI has further improved the accuracy of MR in prostate cancer localization, volume estimation and staging [20, 25]. Recent studies have confirmed that 1H MRSI metabolic and volumetric data correlate with pathological Gleason grade and thus may help to non-invasively predict prostate cancer aggressiveness [30]. In clinical practice, MRI/1H MRSI is currently of greatest value for high-risk patients [41, 55]. With greater understanding of the relationship between spectroscopic data and tumour biology, it may become possible to use MRI/1H MRSI to assist all risk groups substantially by improving patient stratification in clinical trials, monitoring the progress of patients who select watchful waiting or other minimally aggressive cancer management options, and assisting in the guidance and assessment of emerging local prostate cancer therapies.
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Abstract
Introduction
