Neda Gholizadeh1, Peter B Greer2,3, John Simpson2,3, Jonathan Goodwin2,3, Peter Lau4,5, Arend Heerschap6, and Saadallah Ramadan1,5
1Health Science, The University of Newcastle, Newcastle, Australia, 2Radiation Oncology, Calvary Mater Newcastle, Newcastle, Australia, 3Physics and mathematics, The University of Newcastle, Newcastle, Australia, 4Radiology, Calvary Mater Newcastle, Newcastle, Australia, 5Imaging Centre, Hunter Medical Research Institute (HMRI), Newcastle, Australia, 6Radiology and Nuclear Medicine, Radboud University Medical Center, Nijmegen, Nijmegen, Netherlands
Synopsis
Due
to histological heterogeneity of the central gland, accurate detection of central
gland prostate cancer remains a challenge. A reliable and non-invasive imaging
technique could increase the sensitivity and specificity for identification of
central gland lesions missed by PI-RADS V2 or biopsies. This study evaluates the diagnostic
performance of individual and combined parameters of an mp-MRI exam, employed
for PI-RADS evaluations (T2WI, DWI, DCE) and advanced GOIA-sLASER MRSI using an
external phased-array coil for central gland prostate cancer detection,
localization and grading. The results demonstrate that MRSI using GOIA-sLASER considerably
improves central gland prostate cancer detection and localization.
Introduction
Clinical applications of mp-MRI including T2-weighted
imaging (T2WI), diffusion weighted imaging (DWI) and dynamic contrast enhanced
(DCE) imaging as defined by the Prostate Imaging Reporting and Data System
(PI-RADS V2.1) has shown poor to moderate diagnostic performance for the
central gland prostate cancer.1 The diagnostic potential of proton
MR spectroscopic imaging (MRSI) in combination with anatomical and functional
MRI for the improvement of prostate cancer detection, localization and
characterization has been demonstrated.2-4 MRSI provides important information
on metabolites such as, citrate (Cit), choline (Cho), creatine (Cr) and
polyamines, mostly spermine (Spm).5 However, MRSI has been excluded from routine
clinical mp-MRI mainly due to long acquisition times and lack of robustness.1,6,7 Recently, a gradient-modulated offset-independent adiabatic (GOIA)
semi-localized adiabatic selective refocusing (sLASER) sequence was introduced wich
shows much better robustness then previously used sequences and does not need
an endorectal coil, 8,9 which may lead to a renewed prominent role
for MRSI in prostate cancer management, especially in classification of central
gland prostate cancer tissue where diagnosis remains challenging.2
In this study we evaluated the diagnostic performance
of different combinations of conventional mp-MRI protocols (T2WI, DWI and
quantitative DCE) with and without MRSI GOIA-sLASER for central gland prostate
cancer detection and localization.Methods
Mp-MRI was
performed on 36 patients with biopsy-proven central gland prostate cancer (age
range: 53-72years) using a 3T MRI scanner (Skyra, Siemens) with external
phase-array coil. To evaluate the capability of mp-MRI parameters for
discriminating between different cancer grades, the mean values of apparent
diffusion coefficient (ADC) map of DWI, Ktrans,
Kep and the area under gadolinium curve (iAUGC) of DCE and (Cho+Spm+Cr)/Cit
and Cho/Cit and Cho/Cr metabolite ratios of MRSI were calculated for each
voxel within the ROIs. The cancer tissues were further sub-divided into
low-risk (GS=3+3; 97ROIs), intermediate-risk (GS=3+4; 31ROIs) and high-risk
(GS≥4+3; 69ROIs). Support vector machine (SVM) classifications with a radial
basis function (RBF) kernel (RBF SVM) method and area under receiver operator
characteristic (ROC) using an in-house Matlab routine (Matlab 2017b; The
MathWorks Inc, Natick, MA) were used to describe and compare the diagnostic
performance of different combinations of T2WI, T2WI+DWI, T2WI+DCE,
T2WI+DWI+DCE, T2WI+MRSI, T2WI+DWI+MRSI, T2WI+DCE, and T2WI+DWI+DCE+MRSI. Mp-MRI
parameters with a statistically significant difference between two groups were
used to develop each model (p<0.05). The sensitivity, specificity and
overall accuracy of each classifier were measured. Furthermore, Spearman
correlation coefficient (r) was used to measure the correlation between risk
groups (low-risk, intermediate-risk and high risk) and mp-MRI parameters (IBM
SPSS statistics version 0.24.0).Results and Discussion
In patients with central
gland prostate cancers, tumor tissue commonly presented as low signal intensity
on T2WI and ADC maps and high signal intensity on pharmacokinetic parameter
maps of DCE exams (Figure 1A-F). MRSI spectral maps of the entire prostate
showed low signal intensity levels for Cit and high intensity levels for Cho in
tumor areas, whereas benign central gland tissue showed relatively high levels
of Cit and low levels of Cho (Figure 1G). The mean (±SD) values of mp-MRI
parameters in cancer and benign ROIs for all patients were calculated (Table 1).
ADC values were significantly lower in cancerous ROIs than benign ROIs (p<0.01). The pharmacokinetic
parameters Ktrans, Kep and iAUGC, derived from DCE MRI,
increased in cancer ROIs compared to benign ROIs (p<0.05). The mean values of (Cho+Spm+Cr)/Cit, Cho/Cit and Cho/Cr
from GOIA-sLASER MRSI examinations in cancer ROIs were significantly higher
than benign ROIs (p<0.01). The area under the curve (AUC) of RBF SVM models demonstrated that adding MRSI to mp-MRI exam substantially
improved the diagnostic performance of detecting cancer in the central gland,
in contrast to DCE MRI (Figure 2 and Table 2)).
The average ADC demonstrated
good correlation with the different aggressiveness groups (r= -0.49, p<0.01) (Figure 3A). A poor
correlation was found for Ktrans (r= 0.26, p=0.05), a parameter
derived from DCE. The (Cho+Spm+Cr)/Cit ratio derived from MRSI had the highest
correlation with tumour aggressiveness (r= 0.57, p<0.01) (Figure 3B). The correlation of Cho/Cit and Cho/Cr with
different risk groups were (r=0.36, p=0.01) and (r=0.30, p=0.02), respectively.
Correlation coefficients for the normalized T2WI, Kep, and iAUGC
parameters with Gleason grade groups were very low and non-significant (| r |
< 0.25, p>0.05).Conclusion
This
study demonstrates that the addition of GOIA-sLASER MRSI to structural T2WI and
DWI substantially enhanced central gland cancer detection. As the inclusion of
DCE did not improve central gland cancer detection and localization accuracy, a
robust MRSI may be an attractive alternative in mp-MRI. Moderate correlation
between cancer aggressiveness and metabolite ratios as well as ADC values was
observed.Acknowledgements
This
study was supported by the Hunter Cancer Research Alliance (HCRA). Authors
would especially like to acknowledge the contribution of the Clinical Research
and Statistical Support unit in Hunter Medical Research Institute (HMRI).References
1.
Turkbey B, Rosenkrantz AB, Haider MA, et al. Prostate Imaging Reporting and
Data System Version 2.1: 2019 Update of Prostate Imaging Reporting and Data
System Version 2. European urology 2019;76(3):340-351.
2. Gholizadeh N, Greer
PB, Simpson J, et al. Supervised risk predictor of central gland lesions in
prostate cancer using (1) H MR spectroscopic imaging with gradient
offset-independent adiabaticity pulses. Journal of magnetic resonance imaging
2019.
3. Kobus T, Wright AJ,
Scheenen TW, et al. Mapping of prostate cancer by 1H MRSI. NMR in biomedicine
2014;27(1):39-52.
4. Kobus T, Wright AJ,
Weiland E, et al. Metabolite ratios in 1H MR spectroscopic imaging of the
prostate. Magnetic Resonance in Medicine 2015;73(1):1-12.
5. Kurhanewicz J,
Vigneron DB, Nelson SJ. Three-Dimensional Magnetic Resonance Spectroscopic
Imaging of Brain and Prostate Cancer. Neoplasia 2000;2(1-2):166-189.
6. Barentsz JO, Weinreb
JC, Verma S, et al. Synopsis of the PI-RADS v2 Guidelines for Multiparametric
Prostate Magnetic Resonance Imaging and Recommendations for Use. European urology;69(1):41-49.
7. Tayari N, Heerschap A, Scheenen TWJ, et al. In
vivo MR spectroscopic imaging of the prostate, from application to
interpretation. Anal Biochem
2017;529:158-170.
8. Steinseifer IK, Philips BW, Gagoski B, et al. Flexible
proton 3D MR spectroscopic imaging of the prostate with low‐power adiabatic
pulses for volume selection and spiral readout. Magnetic resonance in medicine
2017;77(3):928-935.
9. Tayari N, Steinseifer
IK, Selnaes KM, et al. High-Quality 3-Dimensional 1H Magnetic Resonance
Spectroscopic Imaging of the Prostate Without Endorectal Receive Coil Using A
Semi-LASER Sequence. Invest Radiol 2017;52(10):640-646.