Acute and subacute prostate MRI findings after MRI-guided transurethral ultrasound ablation of prostate cancer

Abstract

Background

Magnetic resonance imaging (MRI)-guided transurethral ultrasound ablation (TULSA) is an emerging method for treatment of localized prostate cancer (PCa). TULSA-related subacute MRI findings have not been previously characterized.

Purpose

To evaluate acute and subacute MRI findings after TULSA treatment in a treat-and-resect setting.

Material and Methods

Six men with newly diagnosed MRI-visible and biopsy-concordant clinically significant PCa were enrolled and completed the study. Eight lesions classified as PI-RADS 3–5 were focally ablated using TULSA. One- and three-week follow-up MRI scans were performed between TULSA and robot-assisted laparoscopic prostatectomy.

Results

TULSA-related hemorrhage was detected as a subtle T1 hyperintensity and more apparent T2 hypointensity in the MRI. Both prostate volume and non-perfused volume (NPV) markedly increased after TULSA at one week and three weeks after treatment, respectively. Lesion apparent diffusion coefficient values increased one week after treatment and decreased nearing the baseline values at the three-week MRI follow-up.

Conclusion

The optimal timing of MRI follow-up seems to be at the earliest at three weeks after treatment, when the post-procedural edema has decreased and the NPV has matured. Diffusion-weighted imaging has little or no added diagnostic value in the subacute setting.

Keywords

Prostate magnetic resonance imaging primary neoplasms ablation procedures

Introduction

Prostate cancer (PCa) has the highest prevalence of all cancers among men worldwide (1). Multiparametric magnetic resonance imaging (mpMRI) is increasingly used in the diagnosis and local staging of PCa and has a high sensitivity in detecting clinically significant PCa (2).

Prostate-specific antigen (PSA) screening of asymptomatic patients has led to an increased incidence of low-risk PCa (3). However, older patients are more likely to have high-risk PCa and they are less likely to receive local treatments, which may partially explain the higher cancer-specific mortality rates (4). There is a need for less invasive, but locally radical, options alongside the traditional curative treatments.

Different types of focal treatments for PCa have been used since the 1990s. The most extensively studied methods have been transrectal high-intensity focused ultrasound (HIFU), cryotherapy, photodynamic therapy, and brachytherapy (5). Preliminary studies of a novel MRI-guided transurethral ultrasound therapy system (TULSA) have demonstrated that it is a safe and feasible treatment method for PCa (6 –8).

Both transrectal HIFU and TULSA are based on the thermal energy delivered by high-intensity ultrasound. The extent of acute thermal damage, which is thought to represent acute coagulation necrosis, is evaluated as the non-perfused volume (NPV) in contrast-enhanced fat-saturated T1-weighted (T1W) images. The rim of enhancement surrounding the NPV has been reported to represent inflammation and partial necrosis (9 –13). Some studies have evaluated post-treatment MRI findings of transrectal HIFU (14 –20), but there is a limited number evaluating post-TULSA outcomes (21). In studies assessing post-HIFU MRI, the main findings include the obscure delineation of the transitional and peripheral zones of prostate, the reduction of the T2 signal intensity (SI) of prostate tissue, and the presence of hemorrhage and necrosis in the surrounding tissue. There are no previous studies reporting subacute MRI findings after TULSA treatment with a correlation to histology, except for our previous study, where clinical and safety aspects of this same study population have been covered (22).

The aim of the present study was to evaluate the acute and subacute MRI findings in a three-week period after TULSA treatment before robot-assisted laparoscopic prostatectomy (RALP).

Material and Methods

Study design and patient selection

This was a prospective, registered, ethics-approved, clinical phase-one trial with a treat-and-resect study setting with a three-week follow-up between TULSA treatment and RALP. Between August 2017 and May 2018, six men with newly diagnosed MRI-visible and biopsy-proven clinically significant PCa were enrolled and completed the study (apart from one patient who could not participate in the one-week MRI follow-up due to scheduling problems). Patients underwent targeted biopsies with cognitive registration from MRI-visible lesions with PI-RADS version 2.0 ≥3 in addition to systematic transrectal 10–12-core ultrasound-guided biopsies. Eight PI-RADS 3–5 lesions were treated with TULSA. MRI was carried out one and three weeks after TULSA, followed by RALP. Clinical and lesion characteristics are shown in Table 1.

Table 1.

Baseline patient, disease, and tumor characteristics as assessed by MRI.

Patient and disease characteristics					Primary lesion					Secondary lesion
	Age (years)	PSA	cT	EAU risk group	PI-RADS	Max diameter (mm)	Volume (mL)	MRI-TBx histology (GS)	Location	PI-RADS	Max diameter (mm)	Volume (mL)	MRI-TBx histology (GS)	Location
1	70	10	T2	Intermediate	3	16	0.6	4 + 3 = 7	L/PZ/apex-mid/post	NA
2	70	4.6	T2	Intermediate	5	24	3	3 + 3 = 6	L(+R)/TZ/apex-base/ant	NA
3	66	7.5	T3	High	5	19	1.5	3 + 4 = 7	R/TZ/mid-base/ant	NA
4	70	36	T3	High	5	29	5.1	4 + 3 = 7	L/PZ/apex-base/post	NA
5	72	12	T2	High	4	8	0.4	4 + 4 = 8	L/PZ/mid/post	4	9	0.2	4 + 4 = 8	L/PZ/apex/post
6	54	7.8	T2	Intermediate	4	10	1	3 + 4 = 7	R/PZ/mid/post	4	9	0.7	3 + 4 = 7	L/PZ/mid/post

ant, anterior; cT, clinical tumor category; EAU, European Association of Urology; GS, Gleason Score; L, left; MRI-TBx, magnetic resonance imaging-targeted biopsies; NA, not applicable; post, posterior; PZ, peripheral zone; R, right; TZ, transitional zone.

MRI-guided TULSA

Thermal ablation of the prostate was delivered using the TULSA system (TULSA-PRO, Profound Medical Corp., Mississauga, Canada) integrated into a 3-T MR system (Ingenia 3T, Philips Healthcare, Koninklijke, Netherlands).

The treatment plan aimed to ablate all MRI-visible (PI-RADS 3-5) and biopsy-proven PCa lesions (eight lesions in total) with a 5-mm margin when feasible. Due to safety aspects of the study with regard to post-TULSA RALP, the TULSA ablation was conservative in the vicinity of neurovascular bundles with a safety margin of up to 3 mm.

Imaging protocol

All images were obtained on a 3-T MR system with 32-channel torso coil (Ingenia 3T, Philips Healthcare). The intravenous contrast media used in these protocols was gadoterate meglumine (Dotarem®, Guerbet, Villepinte, France).

Diagnostic baseline MRI studies were performed at 49–106 days (mean = 75 days) before TULSA. Axial, coronal, and sagittal T2-weighted (T2W) turbo spin-echo (TSE), three-dimensional (3D) T1W fat-saturated (FS) turbo field echo (TFE) and axial diffusion-weighted (DW) images (b-values 0, 100, 200, 350, 500, 1000, 1500, 2000 and 2500 s/mm²) with apparent diffusion coefficient (ADC) mapping. Five of the six patients were imaged with this biparametric MRI protocol used in our institution (23); the other patient underwent an additional 3D T1W FS TFE dynamic contrast-enhanced series.

MRI acquired immediately after treatment (ultrasound applicator still in place in the patient) included axial T2W TSE images, axial DW images with ADC mapping (b-values 0, 100, 200, 350, 500, 1500, 2000, 2500 s/mm²), 3D T1W FS TFE images without contrast media and with dynamic contrast enhancement and axial T1W FS TFE with contrast media.

Post-treatment MRI was performed at one and three weeks after TULSA, except for one patient. The MRI protocol consisted of axial, coronal, and sagittal T2W TSE, axial DW images (b-values 0, 100, 200, 350, 500, 1000, 1500, 2000, and 2500 s/mm²) with ADC mapping, axial T2W FS TSE, 3D T1W FS TFE images without contrast media and with dynamic contrast enhancement, axial T1W FS TFE with contrast media.

All MRI images were analyzed by the same radiologist experienced in prostate MRI and ultrasound therapy of the prostate. Detailed MRI sequence parameters are presented in supplemental material.

Measurement of NPV

The NPV was defined on 3D T1W FS gadolinium-enhanced images (slice thickness = 1 mm) visually as the non-enhancing area within the surrounding rim of enhancement. NPVs were measured using the AW Server 3.2 (GE Healthcare, Chicago, Illinois, United States) volume-rendering tool where the manually contoured area was multiplied by plane thickness.

T1 and T2 signal intensity ratio and measurement of hemorrhage volume

We evaluated the NPV for MRI signal of hemorrhage. T1 SI was measured using 3D T1W FS images (Carestream PACS Version 12.1.5.5151., Carestream Health Inc., Rochester, New York, United States). A region of interest (ROI) of 0.2 cm² was drawn covering the area of highest intensity within the NPV and a reference ROI was drawn on the same slice in a contralateral non-hemorrhagic area of the prostate. The T1 SI ratio (SIR) was calculated by dividing the SI in the hemorrhagic area by the SI in a non-hemorrhagic area of the prostate. The T2 SIR was measured similar to the T1 SIR, except that the hemorrhagic area SI was measured in the most T2 hypointense area within the NPV.

Hemorrhage volumes were measured using the AW Server volume rendering tool by manually contouring regions of T1 hyperintensity in the treatment area.

Measurement of prostate volume

Axial T2W images with a slice thickness of 3 mm were used in the volume assessment. Prostate volumes were measured manually by contouring the prostate boundaries and using the AW Server volume-rendering tool in the volume calculation.

Measurement of ADC values

ADC values were measured from ADC maps obtained from high b-value DW imaging (DWI; b-value = 1500 s/mm²). A ROI of 0.2 cm² was drawn in the lowest signal in the lesion area. A reference ROI was drawn in a homogenous region in prostate outside the treatment area.

RALP and histopathology

The RALPs were performed three weeks after the TULSA treatment by the same experienced urologist. The prostate specimens including seminal vesicles were fixed in formalin and cut into sections of 5 mm. Whole-mount hematoxylin and eosin (H&E)-stained sections of 5 µm were examined by the same experienced uropathologist.

Results

Evolution of NPV

One of our six patients did not participate in the one-week control MRI. In four patients, the NPV expanded between the immediate post-treatment MRI scan and the one-week follow up. In one patient, the NPV decreased by 29%. The mean change in the NPV was +2.0 ± 1.8 mL (+23% ± 34%).

Between the one- and three-week MRI follow-ups, the NPV increased in three patients, but slightly decreased in two patients. The mean change was +0.8 ± 1.5 mL (+24% ± 44%).

The NPV had increased in all six patients when we compared the MRI scans taken immediately after treatment with those at the three-week follow-up (mean = +2.9 ± 1.7 mL [+41% ± 21%]).

The representative evolution of the NPV for patient 4 is shown in Fig. 1 with the average NPV volumes presented in Fig. 2.

Fig. 1.

Evolution of the non-perfused volume in patient 4. Axial T1-weighted fat-saturated images with contrast media administered immediately and then at 1 week and 3 weeks after treatment.

Fig. 2.

Average non-perfused volumes.

Detection and evolution of hemorrhage within NPV

In the histopathologic evaluation, signs of hemorrhagic necrosis were identified in the treatment region in all patients (see Fig. 3 for hemorrhagic coagulation necrosis in patient 6). We analyzed the presence of hemorrhage within NPV as changes in T1 and T2 images with the SI being compared to a non-hemorrhagic area of prostate. These changes were quantitatively defined as the T1 and T2 SIRs.

Fig. 3.

Macroscopic prostate specimen after robot-assisted laparoscopic prostatectomy (patient 6). Regions of hemorrhagic coagulation necrosis (marked with *).

The mean T1 SIR was 1.21 ± 0.12 at the one-week follow-up and 1.26 ± 0.22 at the three-week follow-up (mean increase = 7% ± 11%). The mean T2 SIR was 0.42 ± 0.13 at the one-week control follow-up and 0.31 ± 0.07 at the three-week follow up (mean change = –29% ± 4.8%). The average T1 and T2 SIRs are shown in Fig. 4 and the representative measurements of T1 and T2 SI in patient 1 are illustrated in Fig. 5.

Fig. 4.

Average T1 and T2 signal intensity ratios (SIR).

Fig. 5.

T1 and T2 signal intensity measurements (patient 1). The 1- and 3-week axial T1-weighted fat-saturated non-contrast images (a, b), and the corresponding T2-weighted non-contrast images (c, d).

The mean percentual increase in hemorrhage volumes between the one-week and three-week follow-ups was 110% ± 86%. Hemorrhage volumes are shown in Table 2.

Table 2.

Prostate, planned treatment, NPV, and hemorrhage volumes.

	Patient
Parameter	1	2	3	4	5	6
Prostate volume on baseline MRI (mL)	65	65	42	51	82	55
One-week prostate volume post-TULSA (mL)	75	83	62	68	98	NA
Three-week prostate volume post-TULSA (mL)	73	61	47	61	86	48
Target volume on treatment planning (mL)	16.8	10.5	7.0	13.0	10.1	18.6
Immediate post-TULSA NPV (mL)	11.1	9.1	2.8	6.7	5.7	10
One-week post-TULSA NPV (mL)	13.5	10.9	2	10.8	8.1	NA
Three-week post-TULSA NPV (mL)	15.9	9.6	4	10.7	9.3	13
One-week post-TULSA hemorrhage volume (mL)	3.0	0.8	0.4	1.1	2.8	NA
Three-week post-TULSA hemorrhage volume (mL)	3.4	1.4	0.9	3.8	5.4	5.8
Baseline PSA (ng/mL)	10	4.6	7.5	37	12	7.8
One-week post-TULSA PSA (ng/mL)	33	4.5	8.4	32	NA	NA
Three-week post-TULSA PSA (ng/mL)	24	2.8	3.2	7.3	16	4.4

MRI, magnetic resonance imaging; NA, not applicable; NPV, non-perfused volume; PSA, prostate-specific antigen; TULSA, transurethral ultrasound ablation.

Evolution of prostate volume

Prostate volume increased in all of the patients when the baseline MRI was compared to the one-week follow-up MRI (mean +16 ± 3.8 mL [+29% ± 13%]). Between the one- and three-week MRI follow-ups, the prostate volume decreased in all patients (mean –12 ± 7.6 mL [–15% ± 10%]). When the baseline and three-week follow-up MRIs were compared, it was found that the prostate volume had increased in four out of six patients and decreased in the other two patients (mean change = +3 ± 6.7 mL [+5% ± 12%]). The evolution of prostate volumes is shown in Fig. 6.

Fig. 6.

Average prostate volumes.

Evolution of ADC values

The mean lesion (eight lesions altogether) ADC value in the baseline imaging was 819 ± 185 (10⁻⁶ mm²/s). The corresponding average lesion ADC values in the one- and three-week MRI follow-ups were 970 ± 200 and 769 ± 147, respectively. Between the baseline and one-week follow-up MRIs, the ADC values increased in five out of six lesions (one patient with two lesions did not participate in the one-week MRI follow-up); the mean change was +15% ± 12%. Between the one- and three-week MRI follow-ups, the ADC values decreased in every lesion with an average change of –22% ± 11%. In six out of eight lesions, the ADC value decreased between the baseline and three-week MRI follow-up; the mean change was –4% ± 27%. The lesion ADC values and their evolution are listed in full in Table 3. The reference ADC values showed negligible changes between the MRI studies; the mean reference ADC values were 1454 ± 310 at baseline, 1510 ± 332 at one week, and 1456 ± 295 at three weeks. The mean percentage change in reference ADC values were +0.2% ± 1.1%, –0.2% ± 1.8, +0.4% ± 1.0, respectively.

Table 3.

Lesion ADC values.

	Patient
Parameter	1	2	3	4	5a/5b	6a/6b	Mean
Baseline ADC (10^–6 mm²/s)	959	697	718	630	965/1155	755/671	819 ± 185
One-week ADC (10^–6 mm²/s)	1204	818	890	694	1137/1078	NA	970 ± 200
Three-week ADC (10^–6 mm²/s)	894	666	863	558	726/807	640/996	769 ± 147
							Mean change
Change from baseline to 1 week (%)	+26	+17	+24	+10	+18/–7	NA	+15 ± 12
Change from 1 week to 3 weeks (%)	–26	–19	–3	–20	–36/–25	NA	–22 ± 11
Change from baseline to 3 weeks (%)	–7	–4	+20	–11	–25/–30	–26/+48	–4 ± 27

ADC, apparent diffusion coefficient; NA, not applicable.

Discussion

In this prospective clinical phase-one trial with a treat-and-resect study setting, we evaluated the subacute MRI changes after focal TULSA treatment of PCa.

To our knowledge, this is the first study to have evaluated such a broad range of short-term MRI changes after thermal ablation using therapeutic ultrasound. Repeated MRI scans over three weeks and their comparison to the histology of the removed prostates allowed accurate observations to be made regarding temporal changes in the whole gland and lesion area.

Previously, one study of transrectal HIFU reported on average a 19% increase in the prostate volume 2–5 days after treatment, a change most likely attributable to postprocedural edema (9). In a 12-month follow-up-study after whole-gland TULSA treatment, the median prostate volume reduction was 88% (21).

In our study population, there was an increase in the prostate volume in all of the patients at the one-week control MRI (29% on average). Between the one- and three-week MRI follow-ups, the prostate volumes decreased in every patient, apparently due to a reduction in postoperative edema. The mean volume change between baseline and three-week MRI was +5%. These results suggest that the maximal postoperative edema seems to occur at one week after treatment, with this being followed by decreasing edema (at 3–4 weeks back to baseline volume) and later with a gradual shrinkage of the prostate.

In the present study, we observed a significant NPV increase in the period between the immediate post-treatment and three-week follow-up MRIs. These results suggest that significant delayed necrosis occurs after TULSA treatment and this may be evident up to three weeks after the therapy.

Prostate post-biopsy hemorrhage is interpreted as the area of low T2 SI corresponded with T1 hyperintensity. It has been claimed that it takes up to four months for the hemorrhage to resolve (24). The published literature about MRI findings of subacute hemorrhage after HIFU or TULSA treatment is limited to one study, in which the slightly hyperintense T1 foci most likely representing hemorrhage within the treatment area were observed at 2–5 days after transrectal HIFU (9). In that study, increased T2 hypointensity was also detected in the treatment area. In our study, we evaluated the hemorrhage within NPV as changes in the T1 and T2 SI. In the T1 images, the visual hemorrhagic changes were rather subtle. The T2 hypointensity in hemorrhagic areas was more apparent. At the three-week follow-up MRI, the hemorrhage within NPV was more clearly demarcated and larger when compared to one-week images. T1 and T2 SIRs supported the visual observations, i.e. the T1 SI values in the hemorrhagic areas were only slightly higher than those in the non-hemorrhagic area of prostate (average SIR values = 1.26 and 1.21). Furthermore, T2 hypointensity in the hemorrhagic areas was more readily distinguishable (average SIR values = 0.31 and 0.42). We did not find any data in the literature about the post-biopsy hemorrhage SIR, but according to our experience, the post-biopsy hemorrhage is more clearly visualized as T1 hyperintensity even a few months after biopsy. Most likely the relatively subtle T1 hyperintensity after TULSA is due to the thermal coagulation of hemorrhage.

DWI is an essential part of tumor characterization in prostate MRI. ADC values have an inverse relationship to Gleason grades (25). There is evidence that prostate biopsy hemorrhage affects ADC values (26). In the long term after thermal ablation of the prostate, ADC values of treated lesions should gradually increase in successful treatment (14 –20). There are no prior studies considering the effect of thermal ablation on DWI, and on the use of DWI in treatment outcome assessment in the subacute setting.

In our study, the ADC values increased on average by 15% one week after treatment, which would indicate a favorable treatment outcome. However, at the three-week MRI follow-up, the ADC values did not continue to increase, but, on the contrary, they markedly decreased (mean = –22%). The three-week ADC values were on average slightly decreased (–4%) when compared to baseline values. It is probably that the increase in ADC values at one week is mainly due to post-treatment edema, and as the edema diminishes and post-treatment hemorrhage gets more organized, the ADC values are decreased at the three-week MRI follow-up (27). One might argue that the remaining low ADC values might also represent residual cancer. However, all the measurements were made within NPVs; for example, patient 2, who had no signs of residual cancer in histopathological evaluation, had this above-mentioned one-week increase and three-week decrease in ADC values (Fig. 7). Accordingly, it seems evident that DWI confers no additional value in the assessment of the ablation zone in the subacute setting of post-TULSA.

Fig. 7.

Evolution of lesion ADC values (patient 2). (a) Baseline, (b) 1-week MRI, and (c) 3-week MRI. ADC, apparent diffusion coefficient; MRI, magnetic resonance imaging.

The present study has some significant limitations, most notably the small study population and the disease heterogeneity with both intermediate- and high-risk tumors being included in the study set. There was also some variation in the MRI-visible lesion sizes, prostate baseline volumes, and target volumes on treatment planning. The main reason for the small study population was ethical considerations; due to the study setting, the patients did not gain any extra benefit in their cancer treatment as RALP was also planned. Despite the limited study group, important information concerning subacute changes of prostate after TULSA has been obtained. This information can help to optimize the follow-up protocols after prostate ablation and warrant further investigations with a larger population treated by TULSA.

In conclusion, hemorrhage occurs in the prostate after TULSA treatment, and the presence of hemorrhage is seen on MRI images as subtle T1 hyperintensity and more apparent T2 hypointensity; it is more clearly demarcated and larger at three weeks after the treatment. The prostate volume initially increases after the TULSA treatment, apparently due to post-treatment edema. Based on our results, the maximal edema is reached one week after the treatment, and at three weeks, the prostate size has returned near to the baseline volume. On average, the NPV increases between the immediate post-treatment MRI and the one-week follow-up MRI, and between the one-week and three-week MRI follow-ups. The optimal timing of MRI follow-up seems to be at the earliest after three weeks post-treatment, when the post-procedural edema has decreased and the NPV has matured. DWI seems to have little or no added diagnostic value in the assessment of the ablation zone in the subacute setting of post-TULSA.

Supplemental Material

sj-pdf-1-acr-10.1177_0284185120976931 - Supplemental material for Acute and subacute prostate MRI findings after MRI-guided transurethral ultrasound ablation of prostate cancer

Supplemental material, sj-pdf-1-acr-10.1177_0284185120976931 for Acute and subacute prostate MRI findings after MRI-guided transurethral ultrasound ablation of prostate cancer by Pietari Mäkelä, Mikael Anttinen, Visa Suomi, Aida Steiner, Jani Saunavaara, Teija Sainio, Antero Horte, Pekka Taimen, Peter Boström and Roberto Blanco Sequeiros in Acta Radiologica

Footnotes

Acknowledgements

The authors thank the whole staff at the Turku HIFU Research Centre for their dedicated work.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received the following financial support for the research, authorship, and/or publication of this article: This study was financially supported by a personal research grant from the TYKS-foundation (to MP).

ORCID iDs

Pietari Mäkelä

Visa Suomi

Supplemental material

Supplemental material for this article is available online.

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