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Keywords:

  • prostate cancer;
  • surveillance;
  • magnetic resonance imaging;
  • sensitivity and specificity

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

What's known on the subject? and What does the study add?

  • Up to 35% of men on active surveillance (AS) for clinically localized prostate cancer will experience biopsy reclassification during follow-up. Currently, annual prostate biopsy is recommended in AS programmes. Multiparametric MRI has shown promise in identifying men at risk for immediate reclassification at the time of entry into AS; however, the MRI characteristics of men already enrolled in AS who may be at low risk for disease reclassification have not been fully described.
  • In the present study, we describe the MRI findings of a cohort of men enrolled within AS, with extended follow-up. Among these men, multiparametric MRI demonstrated excellent specificity (0.974) and negative predictive value (0.897) for the detection of pathological index lesions (determined on serial biopsies). These results suggest that men enrolled in AS with a non-suspicious MRI are unlikely to harbour an index cancerous lesion.

Objective

  • To assess the performance of multiparametric magnetic resonance imaging (MRI) in identifying pathological-index (path-index) lesions, defined as cancer present in the same prostate sextant in two separate surveillance biopsies, in men followed within an active surveillance (AS) programme for low-risk prostate cancer (CaP) with extended follow-up.

Materials and Methods

  • A total of 50 men, representing >215 person-years of follow-up in an AS programme, who were referred for prostate MRI were randomly chosen to have their images reviewed by a radiologist with expertise in prostate MRI, who was blinded to biopsy results.
  • Index lesions on MRI were defined as a single suspicious lesion ≥10 mm or >2 lesions in a given prostate sextant. Lesions on MRI were considered suspicious if ≥2 abnormal parameters co-registered anatomically. Path-index lesions were defined as cancer present in a given prostate sextant on two separate biopsy sessions.
  • Sensitivity and specificity were calculated to test the performance of MRI for identifying path-index lesions.
  • Clinical and pathological features were compared between men with and without a MRI-index lesion.

Results

  • A total of 31 path-index and 13 MRI-index lesions were detected in 22 and 10 patients, respectively.
  • Multiparametric MRI demonstrated excellent specificity and negative predictive value (0.974 and 0.897, respectively) for the detection of path-index lesions. Sensitivity (0.19) and positive predictive value (0.46) were considerably lower.
  • Patients with an index lesion on MRI were younger and less likely to have met the ‘Epstein’ criteria for very low-risk CaP.
  • Compared with men without an MRI lesion, a significant increase in biopsy reclassification was noted for men with a MRI lesion (40 vs 12.5%, P = 0.04).

Conclusions

  • A non-suspicious MRI was highly correlated with a lack of path-index lesions in an AS population.
  • Multiparametric MRI may be useful in both the selection and monitoring of patients undergoing AS.

Abbreviations
path-index

pathological index

AS

active surveillance

CaP

prostate cancer

RP

radical prostatectomy

FOV

field of view

DW

diffusion-weighted

3D

three-dimensional

DCE

dynamic contrast-enhanced

ADC

apparent diffusion coefficient

PPV

positive predictive value

NPV

negative predictive value

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Widespread adoption of PSA screening has led to a significant downward risk migration in prostate cancer (CaP) over the past two decades [1]. Many of these cancers are diagnosed in older men and may have little impact on patient survival. As a result, active surveillance (AS) has emerged as an effective management option allowing many of these men to delay or possibly avoid definitive treatment and its associated side effects [2].

Despite careful patient selection, up to 35% of men in AS will experience biopsy reclassification during follow-up [3, 4]. Non-invasive methods of cancer surveillance, including PSA and PSA kinetics assessments, are not considered reliable triggers for intervention in this population, and annual prostate biopsy is currently recommended by some for monitoring men undergoing AS [5]; however, serial prostate biopsies are associated with potentially serious infectious and quality-of-life sequelae [6, 7]. Improved patient selection and less invasive methods of cancer surveillance are needed to improve the safety of AS in the management of low-risk CaP.

Recently, MRI has shown promise in identifying men entering AS who are at risk of immediate pathological upgrading after repeat biopsy or radical prostatectomy (RP) [8, 9], but the MRI characteristics of men within AS programmes who are at low risk of disease reclassification have not been fully described. Identification of these men through MRI has the potential to reduce a man's exposure to serial prostate biopsies without compromising cancer surveillance. In the present study, we report our experience with multiparametric MRI in identifying pathological index (path-index) lesions, defined as cancer present in the same prostate sextant in two separate surveillance biopsies, in an AS cohort with extended follow-up.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Study Population

At our institution, older men with very low-risk CaP, as defined by Epstein et al. [10], are counselled that AS is a viable alternative to immediate treatment. Younger men and those not meeting the criteria for very low-risk CaP may choose AS through personal preference or because of comorbidities if their biopsy Gleason score is ≤6. Most men in AS undergo yearly 12-core, systematic biopsies of the peripheral zone of the prostate with or without two additional cores taken from the transition zone. Details of our AS programme have been described previously [4]. Beginning in September 2010, all men enrolling in AS and those already followed within our AS programme were offered prostate MRI for improved cancer characterization. Men preferring not to undergo MRI and those with contraindications to entering a magnetic field were not imaged.

As of 1 August 2011 88 men had undergone MRI. Of these men, 50 (56.8%) were randomly selected to have their images anonymized and reviewed by a single radiologist with >10 years experience in prostate MRI (K.J.M). The radiologist was aware that the patient was enrolled in AS, but was blinded to previous biopsy results and patient clinical information. The performance of multiparametric MRI to identify index cancerous foci was evaluated as detailed below.

Prostate MRI Technique

We performed MRI examinations on a 3-tesla whole-body TRIO scanner (Siemens Medical Solutions USA, Malvern, PA, USA) using the TIM body matrix coil and endorectal coil (Medrad, Inc, Warrendale, PA, USA) filled with barium solution (Liquid Polibar). Patients were scanned in the supine position ≥6 weeks after their last biopsy, as biopsy-related haemorrhage can cause artifacts mimicking cancer on T2 images; however, the use of a multiparametric protocol has been shown to reliably distinguish between haemorrhage and CaP [11, 12]. The following sequences were obtained (total imaging time 45 min):

  1. Thin-section high-resolution axial, coronal and sagittal T2-weighted fast spin-echo images of the prostate and seminal vesicles (Repetition Time (TR)/Echo Time (TE) = 2500/111 ms, slice thickness 3 mm, interslice gap 0–1 mm, field of view [FOV] 20–25 cm).
  2. Three-dimensional (3D) isometric T2-weighted SPACE acquisition for multiplanar reformations (TR/TE = 1850/115, slice/space 1/0 mm, FOV 35–38 cm).
  3. Diffusion-weighted (DW) imaging with a two-dimensional multislice single-shot DW Echo Planar (EP) sequence (TR/TE = 4200/76 ms, section thickness = 3 mm, FOV 20–25 cm, b values 50, 500, 800).
  4. 3D Chemical Shift Imaging (CSI)/Number of Repetitions (NEX) spectroscopy (TR = 750 ms; TE = 145 ms; NEX = 4). The volume of interest, excitation volume, and FOV were adjusted per patient, as prostate size varied; spectroscopy analysis performed on a Leonardo Workstation (Siemens Medical Solutions USA, Malvern, PA, USA).
  5. Dynamic contrast-enhanced (DCE)-MRI was performed after the T1-weighted high-resolution sequence (mask) was acquired (3D Gradient Echo (GRE) TR/TR 6.5/2.5, slice/space 4/0 mm, number of excitations 4, flip angle 10, matrix 256 × 256, FOV 20 cm). An i.v. single-dose bolus injection (0.1 mmol/kg, injection rate 3 mL/s) of gadopentetate dimeglumine-DTPA (Magnevist®, Bayer Healthcare Pharmaceuticals Inc, Wayne, NJ, USA) was performed using a power injector (Medrad), followed by a 20-mL saline flush.

Multislice DCE images of the prostate were acquired using the 3D GRE sequence at lower spatial but high temporal resolution 8.1 s (TR/TE 6.5/2.2 ms, flip angle 10, matrix 128 × 128, FOV 20 cm, number of excitations 1). We imaged the prostate during 30 phases of post-contrast administration, over a period of 6 min, to monitor contrast uptake. DCE images were analysed on a computer-assisted diagnosis workstation (iCAD, Inc., Nashua, NH, USA).

Prostate MRI Analysis

Magnetic resonance images were assessed and diagrams depicting prostate sextants were used to designate regions of abnormality within the prostate. Findings in the prostate were assigned to one of three categories: (i) no tumour; (ii) indeterminate (1 abnormal MRI parameter); and (iii) suspicious (≥two abnormal parameters co-registering anatomically). Prostate lesions were measured along their longest diameter on T2-weighted images, or if not visible on T2-weighted images, on DW images.

Magnetic resonance imaging parameters were considered abnormal based on the following qualitative criteria:

  1. A discrete homogeneous low-signal-intensity focus in the peripheral and/or central zones on T2-weighted images.
  2. A focal region of restricted diffusion, exhibiting high intensity on DW images (b-value of 800) and low intensity on apparent diffusion coefficient (ADC) maps calculated from the DW image data set.
  3. For MR spectroscopy, voxels with elevated levels of choline and lower levels of citrate relative to the background prostate.
  4. For DCE MRI analysis, focal regions showing early and intense enhancement and rapid washout, and ‘hot-spots’ on colour-coded parametric maps generated by computer-assisted diagnosis software (using four-compartment pharmacokinetic analysis), reflecting increased vascular permeability and decreased extracellular volume fraction.

Study Design and Statistical Analysis

The primary outcome was to determine the performance of MRI for detecting path-index cancerous foci found on surveillance biopsies in an AS population. Pathological index lesions were defined as cancer present in a given prostate sextant on two time-separated surveillance biopsy sessions. This has been shown to correlate with index lesions from RP specimens [13]. MRI index lesions were defined as a single suspicious lesion ≥10 mm or >2 suspicious lesions in a given prostate sextant. This diameter was chosen as it correlates with a spherical volume of 0.5 mL which has been proposed as the limit of a clinically significant CaP focus [14]. Patients in the study had been enrolled in AS before undergoing MRI, and path-index lesions were determined by retrospective review of patient's biopsies.

The demographic, biopsy and imaging characteristics of participating men are reported. Sensitivity and specificity analysis was performed to describe multiparametric MRI's performance in identifying path-index lesions within the prostate sextants; therefore, 300 sextants (six sextants per patient) were available for analysis. Sensitivity, specificity, positive (PPV) and negative predictive value (NPV), together with 95% CIs are reported. The sensitivity of MRI was the proportion of sextants with a path-index lesion and an anatomically concordant MRI-index lesion, and specificity was the proportion of sextants without a path-index lesion with no MRI-index lesion. The PPV for MRI was the proportion of sextants with a MRI-index lesion that had a path-index lesion in the same location, and the NPV was the proportion of sextants without a MRI-index lesion that did not have a path-index lesion in that location.

The analysis was performed based on a sextant scheme and then on a prostate lobar scheme (right vs left) to account for biopsy imprecision. Two men had a single prostate biopsy and were excluded on repeat analysis.

Finally, to assess the potential patient management implications of MRI findings, clinical characteristics as well as biopsy reclassification status were compared between men with and without MRI-index lesions. Biopsy reclassification was defined as any individual biopsy Gleason pattern >3 or sum >6 and/or an increase in biopsy cancer volume (>2 cores involved or >50% core involvement). The t-test, chi-squared test, and Wilcoxon rank-sum tests were used to compare patient and cancer characteristics between the groups. A P value < 0.05 was considered to indicate statistical significance for all analyses. Statistical analyses were performed using Stata version 11.0 (Stata Corp LP, College Station, TX, USA).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Patient Characteristics

The median age of the cohort was 67 years, and 37 (74%) men met all AS criteria. Of those not meeting the criteria, nine (18%) had a PSA density > 0.15 ng/mL/cm3, three (6%) had >3 cores involved or >50% involvement of a single core, and one (2%) man had cT2a disease. The cohort had a median follow-up of 47.5 months representing 215.8 person-years. The median time from initial positive biopsy to MRI was 45.5 months. A total of nine men (18%) experienced biopsy reclassification at a median time of 24 months from entry into AS. Of these men, two were reclassified after upgrading of Gleason score. Full clinical and demographic data are listed in Table 1.

Table 1. Clinical and pathological characteristics of 50 men with CaP managed with AS who underwent MRI*.
Variable 
  1. *Information represents patient data upon entry into programme. Johns Hopkins Hospital AS criteria: cT1c, Gleason score 6, PSA density < 0.15 ng/mL/cm3, <3 biopsy cores involved with cancer, and <50% involvement of any biopsy core with cancer. Adverse pathology: Gleason score > 6, >2 biopsy cores involved with cancer, 50% involvement of any biopsy core with cancer.

Median (range) age, years67 (49–80)
Median (range) TRUS prostate volume, mL49.3 (12–151)
Median (range) PSA, ng/mL4.5 (0.4–18.6)
Median (range) PSA density, ng/mL/cm30.09 (0.01–0.32)
Median (range) time from initial biopsy to MRI, months45.5 (2–161)
Median (range) time to reclassification, months24 (13–136)
Race, n (%) 
Caucasian47 (94)
African-American2 (4)
Other1 (2)
JHH AS criteria met, n (%)37 (74)
Criteria not met, n (%) 
Elevated PSA density9 (18)
Adverse pathology3 (6)
Palpable disease1 (2)
Gleason score 6, n (%)50 (100)
Stage T1c, n (%)49 (98)
Biopsy reclassification, n (%)9 (18)
Volume7 (77.8)
Gleason score > 61 (11.1)
Both1 (11.1)
Reclassification in men who met AS criteria5 (13.5)

Considering the entire cohort, 237 prostate biopsy sessions were performed of which 217 (91.6%) occurred before MRI. A total of 130 (54.9%) of these biopsy sessions were positive for CaP. The median number of biopsy sessions and positive biopsy sessions per patient was 4 and 2, respectively. In all, 24 men had >5 consecutive prostate biopsies and 7 had <3 biopsies (Table 2).

Table 2. Biopsy and MRI characteristics of 50 men enrolled in AS for management of clinically localized CaP.
Biopsy characteristics 
Total no. of TRUS-guided prostate biopsy sessions237
Median (range) no. of biopsy sessions per patient4 (1–11)
Total positive biopsy sessions, n (%)130 (54.9)
Median (range) no. of positive biopsy sessions per patient2 (1–9)
Total number of path-index lesions, n31
Total no. of men with path-index lesions, n22
No. of men with one lesion15
No. of men with two lesions5
No. of men with three lesions2
MRI Characteristics 
  1. a

    Positive sextant defined as a prostate sextant with an MRI-index lesion.

Total no. of MRI index lesions13
Total no. of men with MRI-index lesions 10
No. of men with one lesion7
No. of men with two lesions3
Median (range) size of largest lesion, mm12.5 (11–30)
Median (range) no. of foci per positive sextanta2.5 (1–5)

Sensitivity and Specificity Analysis

Out of the 300 prostate sextants analysed, a total of 31 path-index and 13 MRI-index lesions were identified. Multiparametric MRI demonstrated high specificity (0.97, 95% CI: 0.95–0.99) and NPV (0.90) when the analysis was based on the sextant biopsy scheme, but sensitivity (0.19, 95% CI: 0.08–0.38) and PPV (0.46) were considerably lower. After the exclusion of two men with a solitary biopsy, similar specificity (0.98, 95% CI: 0.95–0.99), sensitivity (0.19: 95% CI: 0.08–0.38), NPV (0.91) and PPV (0.55) were found.

Analyses based on a lobar scheme demonstrated similarly high specificity (0.92, 95% CI: 0.82–0.97), but lower NPV (0.65). Sensitivity (0.20, 95% CI: 0.09–0.37) was similar to that found in the analyses based on a sextant scheme while PPV was slightly higher (0.58). Exclusion of two men with a solitary biopsy did not affect sensitivity, but resulted in greater MRI specificity (0.95, 95% CI: 0.85–0.99), NPV (0.67) and PPV (0.70).

Comparison of Men with and without MRI-index Lesions

The 31 path-index and 13 MRI-index lesions were diagnosed in 22 (44%) and 10 (20%) men, respectively (Table 2). Five men with a MRI-index lesion had no corresponding path-index lesion. These tumours were located in the mid-prostate (3), the apex (1) and anteriorly (1); however, all of these men previously had one positive biopsy from the corresponding sextant. Likewise, 25 path-index lesions in 21 men did not have a corresponding MRI-index lesion, however, 13 (52%) of these path-index lesions had a corresponding MRI finding including seven lesions considered suspicious but with a diameter <10 mm, five lesions considered indeterminate with a diameter <10 mm, and one lesion considered indeterminate with a diameter >10 mm (Fig. 1).

figure

Figure 1. Flow chart of study results.

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Men with a MRI-index lesion were typically younger (58.5 vs 67 years, P = 0.02) and less likely to have met all AS criteria (50 vs 80%, P = 0.05). Reclassification was more prevalent in men with an MR-index lesion (40 vs 12.5%, P = 0.04); however, when considering only men who met all AS criteria, there was no significant difference in biopsy reclassification based on MRI findings (Table 3).

Table 3. Comparative analysis of men with localized CaP managed with AS, who did and did not have a suspicious lesion ≥ 10 mm or two suspicious lesions in a given prostate sextant on multiparametric prostate MRI.
VariableNon-suspicious MRI N = 40Suspicious MRI N = 10Comparison (P)
  1. a

    Johns Hopkins Hospital Active Surveillance Criteria: cT1c, Gleason score 6, PSA Density < 0.15 ng/mL/cm3, <3 biopsy cores involved with cancer and <50% involvement of any biopsy core with cancer.

Median (range) age, years67 (53–80)58.5 (49–76)0.02
Race, n (%)  0.67
Caucasian37 (92.5)10 
African-American2 (5)- 
Other1 (2.5)- 
JHH criteria meta32 (80)50.05
Median (range) PSA, ng/mL4.7 (0.4–18.6)4.1 (2.6–10.8)0.65
Median (range) PSA density, ng/mL/cm30.09 (0.01–0.32)0.08 (0.02–0.28)0.82
Median (range) maximum no. of cores involved1 (1–3)1.5 (1–5)0.06
Median (range) maximum core involvement, %10 (1–60)20 (5–95)0.04
Path-index lesion, n (%)17 (42.5)50.67
Biopsy reclassification, n (%)5 (12.5)40.04
Reclassification in men meeting AS criteriaa, n (%)4 (12.5)10.65
Median (range) follow-up, months47.5 (12–119)45.5 (2–165)0.59

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

The use of MRI in AS protocols for men with low-risk CaP has not been widely accepted, in part because of conflicting reports on its usefulness in this population. In the present study, there was a low prevalence of MRI-index lesions (20%) as would be expected in men who have remained in a selective AS programme for a median follow-up of 47.5 months. In this population, multiparametric MRI demonstrated high specificity and NPV in correctly classifying those without path-index lesions. Furthermore, when compared with those without a MRI-index lesion, those with a MRI-index lesion were more likely to have experienced biopsy reclassification. These results are among the first to describe the findings of multiparametric prostate MRI in an AS cohort with extended follow-up.

The interpretation of these results must begin by fully understanding the study population, which was a cohort of men at very low risk of cancer reclassification given their acceptance into and maintenance within a highly selective AS programme. In these men, in whom a negative MRI would be expected, the absence of a MRI-index lesion provided reassurance on the indolent nature of their disease. Whether MRI results can be used to follow these men is an interesting question which requires further prospective study, but, even within this population, significant tumours were identified on MRI (Fig. 2). Indeed, these men had higher rates of disease reclassification, underscoring the need for vigilant pathological follow-up in men with a visible tumour on MRI despite favourable disease characteristics on biopsy. In total, these results suggest multiparametric MRI may have an important role in the management of men in AS for low-risk CaP.

figure

Figure 2. MRI of a 71-year-old man followed using AS for >10 years. He had had multiple positive biopsy cores from the location of the tumour visualized by MRI. Although his disease was reclassified owing to the number of biopsy cores involved with cancer (3) he elected to remain on AS because of his age, comorbidities, and low grade cancer. Multiparametric MRI performed at 3 tesla, with the endorectal coil, shows a MRI-index lesion in the right mid posterior peripheral zone. The lesion is 11 mm and shows suspicious features on T2-weighted imaging, DW imaging, DCE imaging and spectroscopy. A, Axial T2-weighted image shows an ill-defined T2 hypointense lesion (arrow). B, Axial ADC map calculated from the DW image data set shows a low signal lesion with restricted diffusion corresponding to A. (arrow), ADC value 0.783 × 10−3 mm2/s. C, Post-contrast axial subtraction image shows a hyperperfusing lesion (arrow) corresponding to A. D, DCE-MRI color-coded map shows a lesion with high vascular permeability (arrow) in the location corresponding to A. E, MR spectroscopy shows high Choline peak (arrow) in the region corresponding to A.

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The use of MRI for the diagnosis and staging of CaP has increased over the past 5 years. Using RP specimens as a reference, early reports demonstrated excellent performance of various MRI sequences in identifying tumours of the peripheral and transition zones as well as anterior tumours [15-17]. Application of this technology has been extended to identify and target tumours for biopsy in men with previous benign biopsies and persistently elevated PSA levels [18, 19]. Despite the increasing use of MRI in CaP diagnosis and management the use of such technology in AS populations remains undefined. The present report adds to a growing body of literature demonstrating that MRI may have an important role in screening patients for entry into AS as well as monitoring their cancer for progression.

There is much controversy concerning the ability of MRI to predict disease reclassification among men in AS. Studies by Margel et al. [8] and Fradet et al. [20] showed that, among men undergoing AS, a suspicious lesion on MRI conferred a significant risk of disease reclassification on repeat biopsy. Conversely, among men undergoing RP, who would have otherwise qualified for AS, Guzzo et al. [21] did not find any correlation between tumour identification on MRI and adverse pathological features. In the present study, we found a significantly greater rate of biopsy reclassification in men who had a MRI-index lesion when compared with those without. Although the present study was not designed to analyse MRI as a prognostic tool, its results suggest that MRI may play an important role in counselling patients regarding both entry into surveillance and cancer monitoring; for example, a non-suspicious MRI may indicate that surveillance is safe for those men with tumour features that do not fit all AS criteria, thus broadening enrolment in the programme. Furthermore, a non-suspicious MRI together with previous favourable biopsy features may allow an increased interval between biopsies for some men.

The present study has several limitations. First, MRI was typically performed after the patient had been enrolled in AS for several years, therefore, only limited conclusions on the prognostic value of MRI can be made without further prospective data. Second, defining a path-index lesion with serial biopsy data provides an estimation of true pathological tumour characteristics. We have previously shown, however, that having two positive biopsies in the same location is associated with an index cancer in the same location at RP [13], so the present results may provide a robust estimate of the performance of MRI in identifying true index lesions which could only be determined after prostatctomy. Nevertheless, such post-prostatectomy results are also inherently biased by different selection of patients. Third, the men included in the study had undergone multiple biopsies at the time of MRI. Despite waiting at least 6 weeks from the last biopsy to perform MRI, biopsy artifact and/or scar may have still influenced image interpretation. Fourth, only one experienced radiologist interpreted the imaging studies and therefore interobserver variability cannot be reported. Finally, the study is limited by its small population size and its retrospective design. Larger, prospective studies are needed to determine the long-term impact of MRI findings in AS populations and are planned by our group.

In conclusion, a non-suspicious multiparametric MRI is associated with an absence of a path-index lesion in an AS population. Furthermore, biopsy reclassification appears to be more common in men with a MRI-index lesion. MRI in conjunction with other patient characteristics may ultimately be useful in selecting patients for AS and for guiding the need for repeat prostate biopsies during surveillance.

Conflict of Interest

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Katarzyna J. Macura is a Clinical Trial Investigator for Siemens AG.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References
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