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A Comparison of Arterial Spin Labeling Perfusion MRI and DCEMRI In Research article Received: 25 December 2012, Revised: 21 March 2014, Accepted: 21 March 2014, Published online in Wiley Online Library: 9 May 2014 (wileyonlinelibrary.com) DOI: 10.1002/nbm.3124 A comparison of arterial spin labeling perfusion MRI and DCE-MRI in human prostate cancer Wenchao Caia, Feiyu Lia, Jing Wangb,c, Huarui Dub, Xiaoying Wanga,c*, Jue Zhangb,c, Jing Fangb,c and Xuexiang Jianga Perfusion MRI has the potential to provide pathophysiological biomarkers for the evaluating, staging and therapy monitoring of prostate cancer. The objective of this study was to explore the feasibility of noninvasive arterial spin labeling (ASL) to detect prostate cancer in the peripheral zone and to investigate the correlation between the blood trans flow (BF) measured by ASL and the pharmacokinetic parameters K (forward volume transfer constant), kep (reverse reflux rate constant between extracellular space and plasma) and ve (the fractional volume of extracellular space per unit volume of tissue) measured by dynamic contrast-enhanced (DCE) MRI in patients with prostate cancer. Forty-three consecutive patients (ages ranging from 49 to 86 years, with a median age of 74 years) with pathologi- cally confirmed prostate cancer were recruited. An ASL scan with four different inversion times (TI = 1000, 1200, trans 1400 and 1600 ms) and a DCE-MRI scan were performed on a clinical 3.0 T GE scanner. BF, K , kep and ve maps were calculated. In order to determine whether the BF values in the cancerous area were statistically different from those in the noncancerous area, an independent t-test was performed. Spearman’s bivariate correlation was used to trans assess the relationship between BF and the pharmacokinetic parameters K , kep and ve. The mean BF values in the cancerous areas (97.1 ± 30.7, 114.7 ± 28.7, 102.3 ± 22.5, 91.2 ± 24.2 ml/100 g/min, respectively, for TI = 1000, 1200, 1400, 1600 ms) were significantly higher (p < 0.01 for all cases) than those in the noncancerous regions (35.8 ± 12.5, 42.2 ± 13.7, 53.5 ± 19.1, 48.5 ± 13.5 ml/100 g/min, respectively). Significant positive correlations (p < 0.01 trans for all cases) between BF and the pharmacokinetic parameters K , kep and ve were also observed for all four TI values (r = 0.671, 0.407, 0.666 for TI = 1000 ms; 0.713, 0.424, 0.698 for TI = 1200 ms; 0.604, 0.402, 0.595 for TI = 1400 ms; 0.605, 0.422, 0.548 for TI = 1600 ms). It can be seen that the quantitative ASL measurements show significant differences between cancerous and benign tissues, and exhibit strong to moderate correlations with the parameters obtained using DCE-MRI. These results show the promise of ASL as a noninvasive alternative to DCE-MRI. Copyright © 2014 John Wiley & Sons, Ltd. Keywords: arterial spin labeling (ASL); prostate cancer; DCE-MRI; perfusion imaging; blood flow (BF) INTRODUCTION Prostate cancer (PCa) is the second most frequently diagnosed * Correspondence to: X. Wang, Department of Radiology, Peking University First malignancy and the sixth leading cause of cancer-related mor- Hospital, Peking University, Beijing, China. tality in males worldwide (1). Angiogenesis plays a vital role in E-mail: [email protected] the growth, progression and metastasis processes of malignant tumors (2–6). Through histopathologic (7,8) and dynamic con- a W. Cai, F. Li, X. Wang, X. Jiang trast-enhanced (DCE) MRI findings (9–19), PCa has been shown Department of Radiology, Peking University First Hospital, Peking University, Beijing, China to be a hypervascular tumor. Unlike highly controlled normal physiologic vessels, the tumor vasculatures are chaotic and b J. Wang, H. Du, J. Zhang, J. Fang permeable, making them excellent targets for early detection, Department of Biomedical Engineering, Peking University, Beijing, China accurate localization and curative therapy (4,6,20). Noninvasive c J. Wang, X. Wang, J. Zhang, J. Fang MR biomarkers that are sensitive to angiogenic changes can Center for Functional Imaging, Advanced Academy of Interdisciplinary be good candidates for evaluating therapeutic effects (2,20). Sciences, Peking University, Beijing, China DCE-MRI has been used widely to acquire pharmacokinetic vascular characteristics of prostate cancerous tissues (such as time Abbreviations used: AIF, arterial input function; ASL, arterial spin labeling; fl to peak, speed of contrast uptake, Ktrans, k and v )(9–19,21), but it BF, blood ow; CNR, contrast-to-noise ratio; DCE, dynamic contrast enhanced; ep e DESPOT1, driven equilibrium single pulse observation of T1; EES, extravascular requires venous cannulation and administration of a gadolinium extracellular space; EPI, echo planar imaging; FAIR, flow-sensitive alternating fi chelate contrast agent. Nephrogenic systemic brosis (NSF) has inversion recovery; FOV, field of view; FSE, fast spin echo; kep, reverse reflux rate recently been linked to gadolinium-based contrast agents constant between extracellular space and plasma; Ktrans, forward volume fi (22–25). In this respect, DCE-MRI is not suitable for patients transfer constant; NSF, nephrogenic systemic brosis; PASL, pulsed arterial spin fi labeling; PCa, prostate cancer; PZ, peripheral zone; ROI, region of interest; SE, with renal insuf ciency and is especially inconvenient for spin echo; SNR, signal-to-noise ratio; SSFSE, single-shot fast spin echo; TI, inver- PCa patients who are required to have repeated follow-ups sion time; TRUS, transrectal ultrasound; ve, the fractional volume of extracellu- for therapeutic effect monitoring. lar extravascular space. 817 NMR Biomed. 2014; 27: 817–825 Copyright © 2014 John Wiley & Sons, Ltd. W. CAI ET AL. Arterial spin labeling (ASL) perfusion MRI is a noninvasive, Table 1. The clinical characteristics of 43 patients with PCa nonradioactive and non-contrast-enhanced method capable of quantitatively measuring microvascular perfusion characteristics Characteristics Value of tissues by tagging arterial water (26–29), significantly ben- – efitting PCa patients with renal dysfunction or other contraindi- Median patient age (years)* 74 (49 86) cations to MR contrast agents. Recently, a feasibility study Median PSA level (ng/ml)*↑ 22.9 (5.67–-5000) showed that normal prostate perfusion can be measured with Pathologic tumor stage♂ the ASL technique (30). To the best of our knowledge, ASL has T2a 5 not yet been used for human PCa detection and staging. T2b 7 The application of traditional ASL for PCa is limited by the intrin- T2c 1 sically low signal-to-noise ratio (SNR), and this is further exacer- T3a 13 fl bated by the relatively slow ow of blood into the prostate from T3b 11 multiple feeding vessels (31). On the other hand, the pulsed arterial T4 6 spin labeling (PASL) method provides a better balance between Gleason score♂ tagging efficiency and SNR, and has been proven to be effective 66 and repeatable in many studies of cerebral diseases (28,32,33) 712 and renal function (29). However, arrival times differ between path- 813 ological and physiological neovascularization settings, and this 912 necessitates the optimization of inversion times (TI) (26,30,33,34). In this study, we sought to explore the feasibility of the PASL *Numbers in parentheses are range. ↑PSA, prostate specific antigen. technique with an imaging readout that is different from the ♂ one that was employed in the previous feasibility study of Data are numbers of patients. prostate ASL perfusion imaging (30). The results were compared The staging was according to the AJCC 7th ed. (2010) (54). with those of DCE-MRI. Furthermore, in order to investigate possible transit time differences between benign and malignant tissues, we used four distinct inversion times. eight-channel pelvic phased-array coil. RF transmission was provided by the body coil. METHODS Transverse and coronal T2-weighted fast spin-echo (FSE) images (TR/TE = 3000/130 ms, NEX = 4 and matrix = 320 × 224), Patient population transverse T1-weighted FSE images (TR/TE = 620/7 ms, NEX = 1 The prospective study was approved by the institutional review and matrix = 320 × 224), diffusion-weighted spin-echo/echo board of the local ethics committee and informed consent was planar imaging (SE/EPI) images (TR/TE = 1000/57.3 ms, NEX = 4 obtained from all patients prior to MRI. Fifty-three consecutive and matrix = 128 × 128) were acquired. All sequences mentioned patients with PCa confirmed by transrectal ultrasound (TRUS)- above were performed using a 4 mm section thickness with an guided systemic biopsy (12 or more cores) were recruited between intersection gap of 1 mm. The field of view (FOV) was 26 cm July 2011 and October 2012. All of the patients underwent MR and the number of slices was 16. The phase encoding gradient examination before biopsy. The time between the MRI examina- was from right to left in order to reduce the motion artifacts tion and the biopsy was less than 1 month. caused by the bladder and the rectum. Inclusion and exclusion criteria T1 mapping Inclusion criteria were as follows: (a) patients with histologically The baseline T1 mapping was performed via the driven equilibrium proven PCa; (b) visible PCa lesion on the MR images; (c) no prior single pulse observation of T1 (DESPOT1) method (35). A pair of history of PCa treatment (such as antiandrogen treatment, radia- spoiled gradient recalled echo images were acquired at optimized tion therapy or chemotherapy). flip angles before DCE-MRI scan. Other parameters were as follows: Exclusion criteria were as follows: (a) presence of a cardiac 3D spoiled gradient recalled echo sequence, TR/TE = 6.0/2.8 ms, pacemaker or other electronic implant; (b) known allergy to flip angle = 3°/12°, matrix = 256 × 256, FOV = 26 cm, section gadolinium-based contrast agents; (c) known renal insuffi- thickness = 5.0 mm, 26 slices, NEX = 2 and bandwidth = 31.5 kHz. ciency; (d) reported claustrophobia; (e) failure to give written informed consent.
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