Radiología. 2011;53(1):47-55 ISSN: 0033-8338
RADIOLOGÍA
RADIOLOGÍA
Publicación Oficial de la Sociedad Española de Radiología Médica Incluida en Index Medicus/MEDLINE
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ORIGINAL
Quadrature coils for magnetic resonance spectroscopy in the detection of prostate cancer: Single voxel acquisition does not improve the diagnostic accuracy of multivoxel images M.C. Martínez-Bisbala,b, B. Martínez-Granadosa, A.I. Catalá-Gregoric, J. Sánchezd, B. Celdaa,b, L. Martí-Bonmatíc,* CIBER, Bioingeniería, Biomateriales y Nanomedicina, ISCIII, Madrid, Spain Departamento de Química-Física, Universitat de Valencia, Burjassot, Valencia, Spain c Servicio de Radiología, Hospital Universitario Dr. Peset, Valencia, Spain d Clinical Science, Philips Cuidados de la Salud España, Madrid, Spain a
b
Received 31 July 2009; accepted 30 June 2010
KEYWORDS Prostate cancer; Quadrature body coil; Proton MR spectroscopy; Citrate
Abstract Objective: To determine the viability of quadrature coils for detecting prostate cancer using single voxel and multivoxel spectroscopy images. Material and methods: We used a quadrature coil on a 1.5T MR scanner to evaluate 23 patients with suspected prostate cancer and prostate specific antigen levels greater than 4 ng/ml (mean 12 ± 8 ng/ml), independently of findings at digital rectal examination. We acquired T2-weighted images and MR spectroscopy images. We also acquired single voxel studies in areas in which the T2-weighted images or the multivoxel images were altered. We used a citrate solution to verify the spectroscopic calibration. Results: Using spectroscopy images and a (Cho + Cr)/Cit cutoff of 1.40 in single voxel spectroscopy, we achieved a sensitivity of 92 %, specificity of 55 %, a negative predictive value of 86 %, and a positive predictive value of 69 %. Using a cutoff of 0.75 decreased specificity slightly (45 %). The (Cho + Cr)/Cit ratio calculated for the single volume obtained from the most abnormal area in the T2-weighted images and in the multivoxel spectroscopy slices was not significantly different between cancerous and non-cancerous tissues (ANOVA, p = 0.1), although there was a clear trend toward increased coefficients with hyperplasia and neoplastic degeneration. Conclusion: The quadrature coil enables multivoxel and single voxel spectroscopic images of clinically and technically acceptable quality to be obtained. Using single voxel spectroscopy does not improve the diagnostic performance of multivoxel spectroscopy and T2-weighted images. © 2009 SERAM. Published by Elsevier España, S.L. All rights reserved.
*Corresponding author. E-mail:
[email protected] (L. Martí-Bonmatí). 0033-8338/$ - see front matter © 2009 SERAM. Published by Elsevier España, S.L. All rights reserved.
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PALABRAS CLAVE Cáncer de próstata; Bobina de cuerpo de cuadratura; Espectroscopía de protón por RM; Citrato
Complementariedad de la espectroscopía univóxel y la imagen de espectroscopía multivóxel obtenidas mediante bobina de cuadratura para la detección del carcinoma de próstata Resumen Objetivo: Demostrar la viabilidad de la bobina de cuadratura para la detección del cáncer de próstata mediante espectroscopía univóxel e imagen multivóxel. Material y métodos: Se evaluaron 23 pacientes con sospecha de carcinoma de próstata, con niveles del antígeno específico de próstata superior a 4 ng/ml, (media 12 ± 8 ng/ml), independientemente del tacto rectal, estudiados en un equipo de RM de 1,5 T con la bobina de cuadratura. Se adquirieron imágenes potenciadas en T2 e imágenes de espectroscopía. También se adquirieron estudios univóxel en aquellas zonas donde la imagen T2 o la imagen multivóxel estaban alteradas. Se realizó un control metodológico de espectroscopía con una disolución patrón de citrato. Resultados: Con la imagen espectroscópica y un punto de corte [(Cho + Cr)/Cit] de 1,40 en el vóxel único se alcanzan unos valores de sensibilidad del 92 %, especificidad del 55 %, predictivo negativo del 86 % y predictivo positivo del 69 %. Con un punto de corte de 0,75, la especificidad disminuye discretamente (45 %). La relación [(Cho + Cr)/Cit] calculada para el volumen único obtenido del área más anormal en el T2 y en los cortes de espectroscopía multivóxel no mostró diferencias significativas entre tejidos no tumorales y carcinomas (ANOVA, p = 0,1), aunque se observó una clara tendencia a aumentar el cociente con la hiperplasia y la degeneración neoplásica. Conclusión: La bobina de cuadratura permite obtener imagen multivóxel y espectros univóxel con una calidad técnica y clínicamente aceptables. El empleo de la espectroscopía univóxel no mejora la rentabilidad diagnóstica de la espectroscopía multivóxel y la imagen T2. © 2009 SERAM. Publicado por Elsevier España, S.L. Todos los derechos reservados.
Introduction Prostate cancer is the fifth most common cancer in the world and the second most common in men. 1-3 Mortality rates for prostate cancer have declined since the 1990s in developed countries, probably as a result of the early detection provided by screening programs in asymptomatic patients with elevated PSA (prostate specific antigen), as well as an improvement in the treatment. 4 PSA levels, digital rectal examination and, in particular, transrectal ultrasound guided biopsy are used to differentiate the healthy tissue of benign prostatic hyperplasia from neoplasm. 5-9 Conventional magnetic resonance (MR) imaging allows us to delimit the peripheral extent of the tumor but sometimes provides an inaccurate diagnosis and a limited ability to differentiate between benign hyperplasia and cancer. 10 However, precise evaluation of the presence, localization and tumor aggressiveness are actually required for correct therapeutic planning and prognostic prediction. Combined use of MR imaging and local biochemical evaluation by MR spectroscopy, especially by multivoxel imaging, 10 improves the ability to identify prostate t u m o r s , 11 p a r t i c u l a r l y i n t h e p e r i p h e r a l g l a n d . Metabolomically, prostate cancer is characterised by reduced regional citrate levels and increased choline and its derivates. 12-14 . Tumors are identified based on increased (choline + creatine)/citrate ratio. 15 Even though citrate levels also change in benign hyperplasia, this ratio does not appear as altered as in carcinoma due
to the interposed glandular tissue. 16 As prostate cancer may involve different zones of the gland, evaluation of the whole gland through a regional voxel-by-voxel analysis, and not limited to a single area, seems indispensable. For this reason, single voxel spectroscopy is considered as a secondary diagnostic tool. MR spectroscopic imaging (multivoxel) is a non-invasive technique able to assess the regional metabolomic characteristics of the prostate when a matrix providing enough spatial resolution and adequate field homogeneity is used. Most MR spectroscopy studies are performed with endorectal coils in order to obtain spectra of sufficient quality. 11,16-18 Unfortunately, the use of endorectal coils increases the cost of the studies and causes discomfort and even patient refusal. 19 For this reason, attempts have been made to assess the feasibility of surface coils in MR spectroscopic imaging. In this sense, linear coils for spine imaging 20 and circular surface coils 10,21-24 have been used in MR spectroscopic studies of the prostate. All these studies performed with surface coils obtain a quality of spectra considered acceptable and reproducible although with limitations due to the small size and deep location of the gland. 25 Although the diagnostic ability of multivoxel MR spectroscopy performed with surface coils has been reported to be similar to that with endorectal coils, 19 it seems well established that the use of the latter improves significantly the overall diagnostic accuracy of the technique. 26,27 The use of quadrature coils for spectroscopic imaging acquisition of the prostate has
Quadrature coils for magnetic resonance spectroscopy in the detection of prostate cancer
not been evaluated. Given the possibility that some MR units may lack dedicated coils for the acquisition of these spectra, or they might be out of order, it seems justified to carry out a study to assess the quality of the spectroscopic imaging obtained using quadrature coils. The present work analyzes the feasibility and complementarity of multi and single voxel MR spectroscopic imaging using the quadrature coil integrated into a 1.5T scanner. Our purpose is to know whether, despite their limited spatial resolution, the quality of the spectra obtained with quadrature coils, present in all RM units, allows adequate detection of tumors in the peripheral zone of the prostate.
Materials and methods Subjects A total of 28 patients with ages between 56–82 years (mean 68 ± 6 years) were evaluated, after signing informed consent. All the patients had elevated PSA levels (mean 12 ± 8ng/ml). Spectroscopic studies could not be performed in 18 % of cases (5/28), thus, 23 patients remained in the study group. Digital rectal examination was not considered an inclusion criterion. The mean time between MR imaging and biopsy was 44 ± 2 months.
MR imaging MR imaging and single and multivoxel spectrometry were performed in a 1.5T MR unit (Intera Philips Medical Systems, Netherland). The surface coil was used for image acquisition and the quadrature coil integrated into the MR unit was used for the spectroscopic analyses. At the beginning of the study, each patient received a subcutaneous dose of butylscopolamine (20 mg) in order to reduce intestinal peristalsis and image noise. 28 In addition, an inextensible abdominal belt placed around the pelvis was used to reduce respiratory motion artifacts. In all patients, MR imaging protocol included the acquisition of axial and sagittal T2-weighted TSE images (TR = 3400 ms, TE eff = 140 ms) using a multielement surface coil. The field of view (FOV) was 350 mm with a matrix size of 480 × 512. Section thickness was 3 mm with 0.3 mm intersection gap. The axial image was perpendicular to the central axis of the prostate. Any focal region of nodular morphology located in the peripheral zone and hypointense relative to the hyperintense rest of the gland was considered abnormal.
Spectroscopy In order to verify the spectroscopic calibration of the unit and the adequate assignment of the citrate peak, several measurements of a standard solution were performed to check the effect of the J coupling of the citrate signal on the single voxel studies obtained with the quadrature coil. To this end, a 300 ml glass sphere
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was filled with 200 mM of citrate solution buffered with phosphate and 2,2-dimethyl-2-silapentane-5-sulfonate (DSS) sodium salt used as reference for the chemical shift. The standard solution was studied following the same protocol applied to the patients and using the same coil. In this spectroscopic imaging the repetition of the 180° pulse and of the gradient of the last echo allow us to generate a series of echoes (three in the proposed protocol) for each TR reducing the acquisition time. Measurement of the citrate signal from the standard solution enabled the assessment of the evolution of the multiplet at 2.66 ppm with the TE for its correct identification in both single (TE 136 ms) and multi voxel (TE 272 ms) imaging techniques, with an acceleration factor of 3. Citrate signal appears inverted in multivoxel spectroscopic imaging (TE 272 ms) and positive in single voxel imaging, in both the standard solution and patients. Previous studies 29-31 confirm the complex behaviour of the citrate signal. In the patients, the axial spectroscopic images were obtained in the same angle as the T2 imaging and covering the same FOV in order to facilitate data overlaid (fig. 1). Two adjacent slices with a 24 × 24 matrix and 20 mm thickness were obtained generating voxels of 13 × 13 × 20 mm. Optimization of the magnetic field homogeneity was adjusted over a region of interest (ROI) of 65 × 65 mm, that in all cases included the central and peripheral areas of the prostate. The PRESS acquisition sequence (TR = 2700 ms, TE = 272 ms) with parallel imaging (turbo acceleration factor of 3) was used. Outer volume suppression was minimized using saturation bands (12-16) around the prostate, to prevent contamination from fat and susceptibility artifacts from adjacent tissues. Overall acquisition time was 9.5 min. Any region with a choline peak (3.2 ppm) equal or greater than to that of citrate (2.6 ppm) was considered abnormal. Finally, single voxel spectroscopic sequences (PRESS, TR = 1800 ms, TE = 136 ms) were acquired with the quadrature coil from those zones with an abnormal T2 signal or suspicious in multivoxel spectroscopy of containing tumor tissue (fig. 2 — healthy prostate tissue and figure 3 — malignant prostate tissue). In order to increase the signal-to-noise ratio, 256 acquisitions were obtained with a total acquisition time of 8.3 min.
Post-processing and analysis j M R U I 3 2 ( s i n g l e v o x e l s p e c t r o s c o p y ) a n d S I Vi e w 3 3 (multivoxel spectroscopy) software were used in the post-processing of the spectra and both the real and imaginary parts of the signal were analyzed to check citrate coupling inversion at 2.6 ppm (fig. 4). Single voxel spectra were quantified using jMRUI, measuring citrate (Cit), choline (Cho) and creatine (Cr) signals. Based on these values, the [(Cho + Cr)/Cit] ratios were calculated for each voxel. For the classification of normal voxels, at a first stage, voxels with a [(Cho + Cr)/Cit] ratio > 1.40 were considered pathologic and, at a second stage, a cutoff value > 0.75 was established. 34 Multivoxel spectroscopic imaging data were analyzed voxel-by-voxel by means of qualitative visual analysis of the spectra. Spectra with a choline
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the histopathological results. Biopsies were not performed under MR or spectroscopic (single or multivoxel) guidance.
Statistical analysis The diagnostic accuracy of MR was calculated by means of 2 × 2 contingency tables. The ANOVA StudentNewman-Keuls test was used to assess the differences based on the [(Cho+Cr)/Cit] ratios.
Results
Figure 1 Axial (top) and sagittal (bottom) T2-weighted images show the location of the sections for the multivoxel imaging. The axial image shows the ROI (dark gray box). Despite the inclusion of some peripheral fat, the signal is saturated due to the use of saturation bands (not shown) perpendicular to the axial plane and long TE (272 ms). The sagittal image shows (light gray dotted box) the full area of the ROI in the centre of the anatomic image, including the two sections (the centres of the two planes appear as two parallel lines) perpendicular to the central axis of the gland.
peak equal or greater than citrate peak amplitude were considered abnormal. Researchers had at least four years of experience in imaging analysis and prostate spectroscopy.
Histopathologic examination In order to determine the presence of abnormalities and classify prostate cancer, the biopsy specimens were all submitted for histopathologic evaluation using the standard histological techniques used in our institution. All the patients underwent ultrasoundguided sextant biopsies of the peripheral gland and six cores were obtained. Radiologists and pathologists were blinded to each other’s reports. An independent radiologist correlated the spectroscopy results with
Five (18 %) of the 28 patients in whom T2-weighted TSE and MR spectroscopic (single and multivoxel) imaging was performed were excluded owing to the presence of artifacts that prevented metabolomic quantification at spectroscopy. Final sample consisted of 23 cases. None of the patients reported local discomfort during the study. Spectra obtained from the citrate solution showed similar scalar coupling (J-coupling) than those obtained from patients (fig. 5), helping in the identification of citrate resonance. This was particularly useful to verify the results from the multivoxel image. Histopathologic findings were: eight patients diagnosed with normal prostate, three with benign hyperplasia and 12 with carcinoma. For this prevalence of carcinoma (52 %) (12 carcinomas in 23 patients), the diagnostic accuracy of multivoxel spectrometry as classification criterion showed a sensitivity of 92 %, a specificity of 55 %, a positive predictive value of 69 % and negative predictive value of 86 %. When complemented with a single voxel study and a 1.40 cutoff value, the overall accuracy of MR was similar to that of multivoxel spectroscopy (92 % sensitivity, 55 % specificity, 69 % positive predictive value and 86 % negative predictive vale) (table 1). When the cutoff value was set at 0.75, the diagnostic accuracy slightly decreased (table 2). The metabolic profiles obtained showed a slight correlation with the histopathological results. The [(Cho+Cr)/Cit] ratio calculated for the single voxel obtained from the most abnormal area in the T2 sequences and in the spectroscopic sections showed no significant differences between the groups (ANOVA Student-Newman-Keuls, p = 0,1); however, a tendency to increased ratio in benign hyperplasia and neoplastic degeneration was found. Thus, the value of the metabolic ratio was 0.57 ± 0.43 for the normal prostate; 0.91 ± 0.55 for benign hyperplasia and 1.16 ± 0.74 for carcinomas (fig. 6).
Discussion The spectroscopic study of the entire prostate involves a multivoxel approach with a good signal-to-noise ratio. Citrate detection is a quality factor in prostate spectroscopy. In order to obtain such a spectrum quality, endorectal coils are normally used although they may cause discomfort to the patient. Studies performed with
Quadrature coils for magnetic resonance spectroscopy in the detection of prostate cancer
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Cit
Cho
3.5
3.25
Cr
3
2.75
2.5
2.25
2
Frequency (ppm)
Figure 2 Single voxel RM spectroscopy of the left part of the peripheral gland in a healthy patient: axial (top left) and sagittal (bottom left) T2-weighted images for localization of the voxel (gray box). On the right, the spectrum of this voxel. Voxel dimensions are 15 × 25 × 25 mm. Signal-to-noise ration allows identification and quantification of the main peaks of Cho, Cr and Cit.
Cho
Cit
Cr
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3
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Frequency (ppm)
Figure 3 Single voxel RM spectroscopy of a prostatic lesion: sagittal (top left) and axial (bottom left) T2-weighted images for localization of the voxel (gray box). On the right, the spectrum of this voxel with Cho, Cr and Cit levels. In comparison with Fig. 2 (healthy tissue), this spectrum shows elevated Cho levels and reduced Cit levels, resulting in a higher [(Cho+Cr)/Cit] ratio.
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Creatine
Citrate
Choline
Figure 4 Spectra of the lower section of the multivoxel image obtained from one patient in our series. Upper and bottom left images show the overlaid ROI grid on the T2-weighted images. On the right, enlarged spectra of the selected voxels from the ROI for better assessment. The upper right image shows the module of the spectra and the bottom image shows the module and the real part of the signal used to evaluate the peak inversion of Cit in comparison with Cho and Cr peaks. This feature allows better identification of the Cit signal within the spectrum.
endorectal coils offer a good opportunity to detect changes in citrate, choline and creatine levels; however this equipment is unpleasant as well as expensive. In addition, endorectal coils have to be adequately placed near the ROI to achieve the best possible signal from the prostate. For this purpose, several adjustments of the coil position may be needed. Accordingly, the use of other types of surface coils in spectroscopy is being increasingly evaluated. However, in specific occasions the dedicated surface coils might not be available or in the appropriate conditions for performing spectroscopy. This work confirms that quadrature coils, present in all MR units, may be used for the acquisition of single and multivoxel spectroscopic studies. This approach allows generalization of the spectroscopic studies in case of unavailability of surface coils, as long as we establish a compromise between acquisition time and the metabolic information adequate for clinical use. In order to guarantee adequate citrate identification with quadrature coils, a multivoxel image was acquired from the standard solution of citrate. The acquisition of a reference signal was very useful to ensure the quality of the MR spectroscopic studies obtained with quadrature coils. Multivoxel studies, in our series as well as in previous studies, 35-38 showed choline, creatine and citrate signals
with an adequate resolution of the prostate. Single voxel spectra from our study also showed an adequate resolution for calculation of the [(Cho + Cr)/Cit] ratios. The use of single voxel spectroscopy to improve the classification obtained with T2-weighted sequences and multivoxel spectroscopy does not improve the diagnostic accuracy, thus, this imaging technique is not necessary under these conditions. Loss of specificity and predictive value occur even with a 0.75 cutoff. One of the main limitations of the quadrature coil in prostate spectroscopy is the loss of spatial and spectral resolution in comparison with surface and endorectal coils. The latter are the optimum coils for prostate spectroscopy. As we have demonstrated, quadrature coils allow us to obtain spectra technically and clinically acceptable; however, they should be used only in specific cases, when surface coils are not available. Another source of error is the use of biopsy as the gold standard, because although the histopathologic examination of the entire prostate should be considered the best parameter to establish the diagnostic accuracy of the technique, its use is clearly limited in series that include subjects without tumor. In the present study we demonstrate that quadrature coils allow the acquisition of single and multivoxel spectra technically and clinically acceptable. Multivoxel
Quadrature coils for magnetic resonance spectroscopy in the detection of prostate cancer
53
Figure 5 Combined transverse T2-weighted MR image and corresponding multivoxel spectral grid (top and bottom) of the standard solution with 200 mM citrate concentration. At the top and bottom right, enlargement of the spectra and of the acquisition matrix. Module of the spectra (top right) and module (black) and real part (red) of the spectra (bottom right) depicting the peak inversion of Cit in multivoxel imaging (TE 272 ms).
spectra acquired with quadrature coils show high diagnostic accuracy values. Despite the shorter acquisition time of single voxel spectroscopy in comparison with the multivoxel technique, the lack of
Table 1 Classification using a 1.40 cutoff for the [(Cho+Cr)/Cit] ratio (single voxel spectroscopy) and increased Cho in the multivoxel RM spectroscopy.
EVALUATION + —
diagnostic accuracy of the former makes it inadequate as a complement to T2-weighted and multivoxel imaging when using quadrature coils, thus, this imaging technique is not required under these conditions.
Table 2 Classification using a 0.75 cutoff for the [(Cho+Cr)/Cit] ratio (single voxel spectroscopy) and increased Cho in the multivoxel RM spectroscopy.
Final diagnosis
Final diagnosis
+
—
+
—
11 1
5 6
11 1
6 5
Sensitivity = 92 % Specificity = 55 % PPV = 69 % and NPV = 86 %
PPV: positive predictive value; NPV: negative predictive value.
EVALUATION + —
Sensitivity = 92 % Specificity = 45 % PPV = 65 % and NPV = 83 %
PPV: positive predictive value; NPV: negative predictive value.
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(Cho + Cr)/Cit
3 2.5
6.
2
7.
1.5
8.
1
9. 0.5 0
10. No tumor or HBP HBP Carcinoma Histopathologic findings
Figure 6 Box plot (depicting minimum and maximum values, quartile, median and symmetry of the distribution): results of the [(Cho+Cr)/Cit] ratio from the single voxel spectroscopy correlating with the three possible histopathologic findings (no tumor, benign hyperplasia and carcinoma).
Authorship
11.
12.
The authors have made contributions to the following requirements: • conception and design of the study (MCMB, BMG, BC and LMB); • data acquisition (MCMB, BMG and AICG); • analysis and interpretation (MCMB, BMG, AICG, BC and LMB); • drafting the paper (MCMB, BMG, AICG, JS, BC and LMB); • critical review (MCMB, BMG, AICG, JS, BC and LMB); • guarantor of the overall quality (BC and LMB).
13.
14.
15.
All the authors have read and approved the final version of the manuscript. 16.
Conflict of interest
17.
The authors declare no conflict of interest.
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