MR Imaging of Recurrent Prostate Cancer After Radical Prostatectomy

Klaus Kubin, MD
University Clinics Salzburg
Address for correspondence:

Klaus Kubin, MD Senior Radiologist
Department of Radiology
University Clinics Salzburg (www.salk.at)
Müllner Hauptstraße 48
A-5020 Salzburg
Tel: +43 662 4482 58910
Email: k.kubin@salk.at


Introduction
Radical prostatectomy (RPE) is the most common treatment option for prostate cancer, especially in early stage disease. Retropubic prostatectomy, transperineal prostatectomy, laparoscopic prostatectomy, and robotic prostatectomy are surgical techniques that are available as potential cures. In all these surgical techniques, removal of the prostate gland is mandatory; in many patients the seminal vesicles are also removed. Depending on the local staging, a bilateral- or unilateral- nerve-sparing surgical technique can be used, especially in patients with local T2 staging.

Within 21 to 30 days after RPE, serum prostate-specific antigen (PSA) should decrease to an undetectable level (<0.1 ng/mL) and remain undetectable if the surgery provided a potential cure. Patient follow-up is based on serial measurements of serum PSA levels to monitor tumour recurrence after RPE. Digital rectal examination is a controversial issue in the literature, and Lightner and colleagues even describe it as being inadequate to detect local recurrence[1].

Biochemical relapse is defined as an increase in blood serum PSA levels in three consecutive measurements, and has been reported to occur in 15% to 53% of cases after RPE.2 Four main categories of recurrence are possible: PSA-only relapse, local recurrence in the prostatectomy bed, predominantly nodal or osseous distant metastasis, or a combined local and distant recurrence. The category of recurrence is often difficult to distinguish, especially if clinical examination tools (PSA measurements, digital rectal examination) alone are used. It should be noted that an increasing PSA level rarely is associated with symptoms or findings at physical examinations[2].

In many centres, urologists rely on different nomograms to differentiate between local recurrence and distant metastasis. These nomograms are based on clinical parameters, such as pathologic stage and tumour grade at the time of prostatectomy, PSA doubling time, and time interval between surgery and PSA relapse, among others. A palpable abnormality is not a reliable finding because postoperative fibrosis often mimics recurrent malignancy. Transrectal ultrasonography (TRUS) is more effective for detecting local, recurrent tumours; it lacks specificity, however[3, 4].

Currently, TRUS-guided biopsy of the prostatectomy bed is the most efficient and cost-effective way to prove local recurrence after RPE. However, the likelihood of proving local recurrence after RPE with this type of biopsy is relatively low and has been reported to vary between 38% and 54%. About one third of patients require two or more TRUS-guided biopsy sessions of the prostatectomy bed to obtain a final diagnosis[5].

Other imaging methods, therefore, are necessary to differentiate between local recurrent tumours and distant metastases. Computed tomography and technetium 99m bone scan, immunoscintigraphy, and 11C-acetate positron emission tomography (PET) are widely used modalities. TRUS and CT are neither very sensitive nor very specific in identifying local recurrent tumours or in differentiating them from postsurgical scarring.

Additional methods which show promise include elastography and colour Doppler and/or contrast media-enhanced ultrasound[6]. The literature[2, 5, 7, 8] also indicates that magnetic resonance imaging (MRI) is a promising technique for evaluating the prostatectomy bed after RPE. Targeted, high-resolution imaging, excellent soft-tissue differentiation, and different contrast media enhancement characteristics of benign and malignant tissue types are well known features of MRI. Consequently, MRI is among the most important imaging methods being developed to detect and evaluate local tumour recurrence within the prostatectomy bed after RPE.

Indications for MR Imaging of the Prostatectomy Bed

The diagnosis of biochemical relapse after RPE is relatively straightforward. In most cases, the postsurgical serum PSA level drops below 0.1 ng/mL within 4 weeks and remains low. If the serum PSA level does not decrease following RPE, it is likely that either the surgery was incomplete and prostate tissue remained within the prostatectomy bed, or that the patient already had distant metastases at the time of surgery. A serum PSA level above a threshold of 0.2 ng/mL later than 6 to 12 months after RPE suggests treatment failure with a high risk of local recurrence, whereas a PSA increase within a shorter period strongly correlates with the progression of a distant metastasis[9].

Therefore MR imaging is the preferred imaging modality to differentiate between

  • residual prostate tissues
  • local recurrent tumour
  • distant metastasis (not necessarily displayed locally when the prostatectomy bed is examined by MR, but inferred when the prostatectomy bed shows no abnormalities)

As already mentioned, TRUS and TRUS-guided biopsy of the prostatic fossa are accurate methods to detect local tumour recurrence. Unfortunately, biopsy results positive for local recurrence are strongly correlated with serum PSA levels. In patients with a serum PSA level <0.5 ng/mL, no positive TRUS biopsies were found; in patients with a serum PSA level <1.0 ng/mL, almost 30% of biopsies were positive[3, 10, 11]. Therefore, it would seem useful to perform MRI prior to targeted TRUS- or transperineal MR-guided biopsy[12].

Additional fusion imaging can be essential for the final diagnosis of recurrence. 11C-acetate PET and MR imaging results are superimposed by dedicated software applications, and functional information and morphological information are combined[13].

Figure 1A

Figure 1B
Figure 1. 73-year-old patient 9 years after RPE (T3a), serum PSA level 2.18 ng/mL. Recurrent tumour with invasion of the rectal wall (white arrows) prior to (Figure 1a) and 6 months after (Figure 1b) HIFU; Small icons show evaluation of dynamic contrast enhancement by CADvue (iCAD, USA).

MR imaging of the prostatectomy bed is suitable for follow-up examinations. Treatment response of a local, recurrent tumour (for example, after external beam radiation or high-intensity focused ultrasound) can be visualised very effectively with MR (Figure 1)[14,15]. Additionally, MR imaging shows great promise as a planning tool for different treatment options[12, 16].

MR Imaging Technique

The prostate region can be visualised with 1.5- and 3-Tesla MR systems. However, imaging of the prostatectomy bed after RPE is reported in the literature only with 1.5-Tesla MR systems[2, 5, 8, 17]. A pelvic phased-array coil is used in combination with a balloon-covered expandable endorectal coil (ERC) for signal reception in all the major studies that are cited in this article. Although no comparative studies have been reported, results from studies using different techniques suggest that, on the basis of image quality, the combination of surface coil and ERC or ERC only is the preferred method[18, 19]. Heijmink et al evaluated image quality, localisation, and staging performance of 3-Tesla exams with body-array coil (BAC) versus ERC and reported significantly better performance among experienced radiologists using an ERC[20]. Most of the commercially available ERCs must be filled with air; if permitted by the manufacturer, liquid filling is recommended. Alternatively, smaller surface coils (such as cardiac coils), or combinations of different surface coils can be used.

About 1 hour prior to the examination a clysma/enema is necessary to clean the rectum. An oral preparation prior to the exam is not necessary. To prevent artifacts due to rectum peristalsis, an intramuscular injection of 1 mL scopolamine-N-butylbromide (eg, Buscopan, Boehringer Ingelheim Germany) or 1 mg glucagon (eg, Glucagen, Novo Nordisk A/S Gentofte, Denmark) is recommended. Finally, a delay of at least 3 weeks after biopsy of the prostatectomy bed is necessary to avoid restricted image quality[21].

MR Imaging Acquisition Protocol

T1-weighted imaging

T1-weighted images obtained from the aortic bifurcation to the symphysis are mandatory to get an overview of the anatomical situation of the pelvis and to exclude pathological lymph nodes. A slice thickness of 4 to 5 mm and a larger field of view (FOV) (12-16 cm) are recommended[2, 17]. In more than half of the studies describing MR of the prostatectomy bed, no T1-weighted images were obtained. There are several possible reasons for this, including the fact that not all institutions include nodal staging in their imaging protocols, while others include additional CT scans of the abdomen, excluding metastases. The size of the surface coil used can also determine whether images of the prostatectomy bed are obtained. For example, cardiac imaging using a small coil would not extend to cover the pelvic nodes.

T2-weighted imaging

To start the detailed examination of the prostatectomy bed with transversal, coronal, and sagittal T2-weighted images with an FOV reduced to the prostatectomy bed, an optimised high-resolution matrix (range of 256x256 mm to 512x512 mm) and a slice thickness of 3 to 4 mm are recommended.

Spectroscopy

H1-MR spectroscopy (H1-MRS) of the prostatectomy bed after RPE is not commonly described in the literature but is a promising technique when combined with dynamic contrast media-enhanced MR (DCEMR)[8]. Sciarra et al performed H1-MRS using a section-selected box drawn closely around the prostatic fossa. A point-resolved spectroscopic sequence was obtained with the use of a three-dimensional chemical-shift imaging (CSI) sequence with spectral/spatial pulses optimised for quantitative detection of choline and citrate. When H1-MRS is performed, morphological T2-weighted images should be reviewed first to optimise the volume of interest (VOI) and to exclude surrounding structures (eg, muscle, fat, rectal air, or urine).

T1-weighted dynamic contrast medium-enhanced imaging

To the author’s knowledge there are four studies[5, 8, 17, 22] in the literature using a contrast medium-enhanced T1-weighted sequence to evaluate tumour recurrence. Depending on the scanner, protocols vary considerably, especially in the duration of a single sequence (11-40 s). Parameters including 4-mm slice thickness, transversal plane, 12 to 15 section numbers, one sequence prior to injection of contrast medium, and repeated sequences (at least three repetitions) after contrast injection have been described.

However, the protocols in the recent literature have a few things in common. They all administer a single 0.1 mmol/kg body-weight dose of paramagnetic contrast media intravenously (eg, Multihance, Bracco Spa, Mailand, Italy, or Magnevist, Berlex Schering AG, Berlin, Germany). A power injector is not essential but is strongly recommended. An injection rate of 2.5 to 4 mL/s followed by a 15 mL saline flush (2 mL/s injection rate) is advisable.5, 8 In general, contrast medium uptake by recurrent tumour tissue is very similar to that by primary prostate tumour tissue. Accordingly, dynamic contrast media enhancement (DCE) of prostate tumours is also valid for recurrent tumours. The author recommends adopting pre-existing contrast media protocols for prostate imaging.

The number of sequence repetitions needed following injection of contrast medium and the duration of the examination are mostly dependent on the scanner. If evaluation software is not used to visualise wash-in and wash-out of tumour tissue, normal tissue, and scars, only three to four repetitions of 20 s (early arterial phase), 60 s (venous phase), 120 s (equilibrium phase), and 180 s (late wash-out) are suitable. Although dedicated software products are available for evaluating DCE of the prostate, these have not been evaluated for diagnosing recurrent tumours until now. Reports in the literature, however, describe the benefit of evaluating signal enhancement-time curves with or without reference structures (such as pelvic muscle). Consequently, the enhancement curve can be modelled with four parameters: onset time of signal enhancement, time to peak (TTP), peak enhancement, and wash-out.

Diffusion-weighted imaging (DWI)

To the author’s knowledge there are no studies available evaluating the pros and cons of DWI and apparent diffusion coefficient maps within the prostatectomy bed.

MR Imaging Findings

Normal postoperative findings

After surgery, the bladder base and levator sling descend caudally and anteriorly into the prostatectomy bed, but the urogenital diaphragms stay in similar position. There is a notable increase in the volume of fat within the prostatectomy bed. To a variable degree, vas deferens and seminal vesicle remnants are present. These structures show a linear, low/intermediate signal strength on both T1- and T2-weighted images.

Postsurgical fibrosis can be found next to the anterior rectal wall and at the site of the anastomosis of the urethra and bladder. These structures normally show low signal strength in T1- and T2-weighted imaging[7]. In 80% of patients after RPE, TRUS shows a corresponding hypoechoic soft-tissue lesion anterior to the anastomosis.23 In normal postsurgical cases without recurrent disease, there is usually no enhancement of the prostatic bed in the arterial phase and sometimes uniform (but poor) enhancement in the venous phase[7].

The seminal vesicles rarely are completely removed during RPE and therefore the lateral ends can often be seen in postsurgical MR imaging. Their characteristic appearance does not change significantly from presurgical MR imaging and includes high-strength signals in T2-weighted imaging and bilobulated contours, although there may also be some low signal-strength scarring. Scars, fibrosis, and exuberant fibrosis can be found around the vesicourethral anastomosis. The strength of the signal associated with these structures can be low to intermediate in T2-weighted imaging, which can therefore mimic tumour recurrence. DCE or MRS can be helpful in this situation.

Residual gland tissue can mimic recurrent tumours, but typically the residual prostate tissue is shaped like normal gland tissue and is homogeneous and well defined. The tissue is homogenous and hyperintense in T2-weighted imaging and has a “parenchymatous” aspect with regular margins and profile[17]. DCE is often helpful to differentiate between residual gland tissue and recurrent tumours. It should be noted that patients with residual prostate gland tissue after RPE will never show a complete drop in postsurgical PSA levels[7].

Pathological postoperative findings

T2- and T1-weighted imaging

Sella et al[2] studied 42 patients with recurrent tumour nodules that were isointense to muscle in T1-weighted images and slightly hyperintense to muscle on T2-weighted images (Figure 2 a + b). Eleven recurrent tumor nodules (26%) were shown to invade an adjacent pelvic structure (eg, levator ani muscle, bladder, rectum, ureter, or urethra), and these nodules were among the largest recurrences observed.



Figure 1A
Figure 2. T2-weighted images of a 68-year-old patient 12 months after RPE (T3b), serum PSA level 0.39 ng/mL (initial serum PSA level after RPE was 0.01 ng/mL). Well-defined hyperintense nodular lesion left to the perianastomotic region (white arrow – Figure 2 a); 6-month follow-up without therapy; obvious increase in lesion size and therefore indicative of a recurrent tumour (white arrow – Figure 2 b).

Occasionally, differentiation between postoperative fibrosis and recurrent tumour can be difficult. Sella et al reported false negative MR imaging results in 2 of the 42 patients for whom: (i) the tumour recurrence was localised at the perianastomotic site, (ii) the signal intensity of the tumour tissue was similar to that of muscle, and (iii) the tumour margins were irregular[2].



Table 1. Sites of recurrent tumours within the prostatic bed – meta-analysis of three studies[2, 5, 17.]

Table 1
* including lesions next to anterior or lateral surgical margin

Most recurrent tumour lesions occur in a perianastomotic location, although they can occur in retained seminal vesicles or retrovesically. Table 1 summarises tumour localisation evidence from three separate studies[2, 5, 17].

Without using any additional techniques (such as DCE, MRS or DWI) Sella et al showed a sensitivity and specificity of 95% and 100%, respectively[2. However, results from other authors based on T2-weighted images only are not as promising (sensitivity: 48% to 84%; specificity: 52% to 88%), even when combined with DCE[5, 17, 22] or MRS[8].

DCE

The administration of contrast media allows detection of cancerous tissue in cases where morphological anomalies are not evident on unenhanced MR images and differentiation between recurrent tumour tissue and postoperative fibrosis/scarring is not possible[17].

Figure 1A
Figure 3. 64-year-old patient 2 years after RPE with recent, significant serum PSA level increase. Tumour lesion nearly isointense in T2-weighted images (white arrow – figure a) and isointense compared to surrounding structures in T1-weighted imaging (white arrow – Figure 3b); premature enhancement within the early arterial phase (white arrow – Figure 3c).

Recurrent tumour tissue typically shows premature enhancement in comparison with surrounding structures—also called early enhancement (Figure 3 a, b, c). In most cases, the early enhancement can be seen without supportive DCE evaluation software. However, this is not the case for wash-out, or tumour enhancement in the venous and equilibrium phases. Acquisition of several sequences or rapid acquisition of a single sequence will yield more detailed DCE information about suspicious tissues. Although a number of different examination protocols are reported in the literature[5, 8, 17, 22] detailed time resolution (and consequently passable spatial resolution) is necessary. However, this necessitates dealing with quite extensive data sets. Therefore, postprocessing of T1-weighted imaging seems to be useful. There are dedicated software products on the market (Prostate MRI CAD, iCAD, USA; Prostream, Confirma, USA) or, alternatively, the signal intensity evaluation software tools provided by the scanner itself can be used. These analytical tools are definitely helpful when short repetition times (detailed time resolution) are used to summarise results illustrated by colour maps (Figure 4).



Figure 1A
Figure 4. 62-year-old patient 3 months after RPE (T3a), serum PSA level 0.35 ng/mL. T2-weighted axial image of the prostatectomy bed showing slightly hyperintense recurrent tumour at the left seminal vesicle site (white arrow – figure a) and focal hypointense bone marrow signal at the ramus inferior of the left os pubis (open arrow – Figure 4a); both lesions show pathological colour maps after postprocessing T1-weighted DCE series (arrows – Figure 4b).

DCE MR imaging of the prostatectomy bed is unquestionably superior to the use of T2-weighted images only[5, 8, 17, 22]. Combining T2-weighted images with DCE results led to sensitivity and specificity of 84% to 88% and 89% to 100%, respectively[5, 8, 17].

Spectroscopy

Prior to evaluating voxels, those representing the urethra, seminal vesicles, ejaculatory duct and bladder, and rectal wall should be excluded. The remaining voxels must have a signal-to-noise ratio greater than 3:1, and water/fat suppression should be adequate. All voxels that do not fit these criteria should not be considered. For all the other available voxels, the ratio of Choline (Cho) plus Creatine (Cr) to Citrate (Ci) can be calculated. Sciarra et al[8] recommend the following classification:

  • No solid tissue/empty prostatic fossa when Cho+Cr/Ci is not detectable
  • Fibrotic/scar tissue when Cho+Cr/Ci < 0.2
  • Residual healthy prostatic gland tissue when Cho+Cr/Ci > 0.2 and < 0.5
  • Probably recurrent tumour when Cho+Cr/Ci > 0.5 and < 1.0
  • Definitely recurrent tumour when Cho+Cr/Ci > 1.0
    • Sensitivity and specificity were reported as 84% and 88%, respectively, in patients with recurrent tumours proven by biopsy. In another group of patients where recurrent tumour was proven by a decrease of serum PSA levels after external radiation therapy of the prostatectomy bed, sensitivity and specificity were reported as 71% and 83%, respectively[8].

    Conclusion

    Recurrent tumours or distant metastases due to prostatic cancer after RPE cannot be defined by biochemical relapse standards alone. Although imaging plays an important role in the diagnosis of recurrent tumour, morphologic T2-weighted MR images are insufficient to detect these lesions. DCE and MRS are additional MR imaging modalities that provide more diagnostic accuracy. MR imaging of the prostatectomy bed can be used to monitor the success of RPE, and to guide salvage therapy, which ultimately improves patient outcomes.

    Key learning points
    Indications for MR imaging of the prostatectomy bed:
    1. If there is clinical evidence of biochemical relapse, MRI can be used to differentiate between:
      • residual prostate tissues
      • local recurrent tumour
      • distant metastasis
    2. MRI should be performed prior to targeted TRUS- or transperineal MR-guided biopsy
    3. MRI can accurately monitor treatment response of local recurrent tumours
    4. Fusion imaging of MRI with PET or PET/CT can be essential for a definitive diagnosis of recurrence
    5. MRI can be used as a planning tool for different treatment options

    Technical recommendations:
    1. 1.5- or 3-Tesla MR system
    2. Combined endorectal (ERC) – body array coil mandatory in 1.5 Tesla systems and recommended in 3.0 Tesla
    3. Clysma/enema 1 h prior to the examination to clean the rectum
    4. 1 mL scopolamine-N-butylbromide (eg, Buscopan, Boehringer Ingelheim Germany) or 1 mg of glucagon (eg, Glucagen, Novo Nordisk A/S Gentofte, Denmark) i.m. to prevent artifacts due to rectum peristalsis
    5. No biopsy for at least 3 weeks before the MR exam

    MR protocol:
    1. Transverse, coronal, and sagittal high-resolution T2-weighted images
    2. Coronal and/or transverse T1-weighted images covering the pelvis (aortic bifurcation – symphysis)
    3. T1-weighted images prior to and at least three times after contrast media injection – DCE
    4. H1- 3D CSI – MR spectroscopy of the prostatectomy bed

    References
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