Genitourinary Imaging Original Research

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1 Genitourinary Imaging Original Research Li et al. MRI of Renal Function Genitourinary Imaging Original Research Qinghai Li 1 Xinying Wu 1 Lingling Qiu 1 Peipei Zhang 1 Minming Zhang 1 Fuhua Yan 2 Li Q, Wu X, Qiu L, Zhang P, Zhang M, Yan F Keywords: chronic renal insufficiency, diffusion-weighted MRI, glomerular filtration rate, prospective acquisition correction DOI: /AJR Received October 10, 2011; accepted after revision June 10, Department of Radiology, The Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China. 2 Department of Radiology, Shanghai Zhongshan Hospital, Shanghai Medical College, Fudan University, Shanghai, China, Address correspondence to F. Yan (zemylife@163.com). AJR 2013; 200: X/13/ American Roentgen Ray Society Diffusion-Weighted MRI in the Assessment of Split Renal Function: Comparison of Navigator-Triggered Prospective Acquisition Correction and Breath-Hold Acquisition OBJECTIVE. The purpose of this study was to ascertain whether prospective acquisition correction (PACE) diffusion-weighted MRI (DWI) is superior to conventional breath-hold DWI in assessment of split renal function. SUBJECTS AND METHODS. Fifty-four subjects underwent coronal breath-hold DWI and PACE DWI with the b value set at 0 and 800 s/mm 2. Isotope renographic glomerular filtration rate (GFR) was used as the reference standard for assessing split renal function. A GFR of 40 ml/min or greater indicated normal and a GFR less than 40 ml/min indicated reduced split renal function. Reduced split renal function was further divided into a mild reduction group (GFR 20 ml/min) and a moderate-to-severe reduction group (GFR < 20 ml/ min). Various comparisons between the imaging methods were conducted. RESULTS. The signal-to-noise and contrast-to-noise ratios of the PACE DW images were greater than those of the breath-hold DW images (p < 0.001). The correlation between the apparent diffusion coefficient (ADC) value and GFR was stronger when the ADC was measured with PACE DWI than with breath-hold DWI (p = 0.033). Area under the receiver operator curve (AUC) analysis revealed that PACE DWI (AUC, ± 0.045; p < 0.001) but not breath-hold DWI (AUC, ± 0.060; p = 0.053) had diagnostic value in predicting a reduction in split renal function. ADC value assessed with PACE DWI was lower in the groups with mild and moderate-to-severe reduction in split renal function than in the group with normal function (p < 0.01). CONCLUSION. Preliminary results imply that PACE DWI is superior to breath-hold DWI in the assessment of split renal function. T hrough in vivo measurement of water molecule diffusion, diffusion-weighted MRI (DWI) is used for analyzing the internal structure and composition of lesions and the functional status of living tissues [1 3]. The DWI technique has been used to evaluate changes in renal function in various diseases, including obstructive nephropathy, diabetic nephropathy, renal graft rejection, and diffuse renal disease. In such cases, the apparent diffusion coefficient (ADC) values of the affected kidneys have been generally lower than those of normal kidneys [2, 4 9]. A few studies have shown a positive correlation between ADC values and renal function [10, 11]. However, previous DWI studies of kidneys have been conducted with singleshot spin-echo echo-planar imaging [12], and the signal-to-noise ratio (SNR) and spatial resolution were low because of the limitation of the breath-hold time. Use of high b values further limited the accuracy of the ADC measurement. As a technique for suppression of respiratory motion artifacts, navigator-triggered prospective acquisition correction (PACE) has had satisfactory results in the upper abdomen and heart in related application studies [13 16]. Taouli et al. [17] found that PACE DWI was superior to breath-hold DWI in the evaluation of space-occupying liver lesions. Specifically, PACE DWI had better image quality and SNR, increasing the accuracy of quantitative assessment of ADC. Studies by Thoeny et al. [2] with patients with normal renal graft function and Kataoka et al. [18] with healthy volunteers showed that PACE DWI had good reproducibility for renal ADC measurements. However, the value of PACE DWI in the assessment of split renal function requires further study. The purpose of this study was to ascertain whether PACE DWI is superior to the AJR:200, January

2 Li et al. TABLE 1: Basic Clinical Characteristics of Patients and Subjects Stage of Chronic Kidney Disease Characteristic conventional breath-hold DWI technique in the assessment of split renal function. Renal scintigraphy was performed as the reference standard for grouping subjects according to glomerular filtration rate (GFR). Subjects and Methods Subjects Fifty-four consecutively registered subjects (32 men, 22 women; mean age, 42 ± 12 years) underwent both DWI and isotope renography. Of the 54 subjects, 12 were healthy living related kidney donors, and 42 were patients with chronic kidney disease (CKD). The study protocol was approved by the local ethics committee, and informed consent was obtained from all donors and patients. The inclusion criteria for CKD patients were meeting the clinical diagnostic criteria for CKD [19], completing all of the MRI examinations with sufficient image quality, and having no serious disease of other organs or serious systemic disease. In all cases, the CKD stage was consistent with the isotope GFR stage. Split renal function was categorized as normal (GFR 40 ml/min) or reduced (GFR < 40 ml/min). The reduced split renal function group was further divided into a mild reduction group (GFR < 40 ml/min) and a moderate-tosevere reduction group (GFR < 20 ml/min). The exclusion criteria were a medical history of a disorder that could affect renal function, such as gout, diabetes, and primary hypertension; serious disease of another organ or serious systemic disease; not having undergone an MRI examination or having undergone an MRI examination with poor image quality; malignant renal space-occupying lesions or multiple benign renal space-occupying lesions (e.g., angioleiomyolipoma and cysts); other renal lesions, including kidney stones; hydronephrosis; congenital variation; urinary tract tumors; Normal Renal Function 1 (GFR 90 ml/min) 2 (GFR, ml/min) 3 (GFR, ml/min) 4 (GFR, ml/min) No. of subjects Sex (no.) Men Women Age (y) 41.5 ± ± ± ± 8 42 ± 12 Serum creatinine concentration (µmol/l) 74.1 ± ± ± ± ± GFR (ml/min) Total ± ± ± ± ± 2.9 Left kidney 63.0 ± ± ± ± ± 0.8 Right kidney 67.5 ± ± ± ± ± 2.3 Note Data are number or mean ± SD. GFR = glomerular filtration rate. and contraindications to MRI. The clinical characteristic of the included patients are listed in Table 1. MRI Technique and Methods of Isotopic Determination of Glomerular Filtration Rate A 1.5-T MRI system (Avanto, Siemens Healthcare) and abdominal phased-array surface coil were used for obtaining images. On the day of the examination, the subjects consumed a normal diet and remained hydrated. They underwent a positioning acquisition while in the supine position. The unenhanced acquisition included a HASTE sequence (TR/TE, 1000/83; slice thickness, 7.0 mm; FOV, mm; matrix, ; bandwidth, 391 Hz; single breath-hold) and a coronal FLASH 2D gradient-echo T1-weighted sequence (TR/TE, 233/2.52; slice thickness, 7.0 mm; FOV, mm; matrix, ; bandwidth, 260 Hz; frequency-selective fat suppression; single breath-hold). The acquisition range covered the entire kidney. The DWI acquisition simultaneously entailed a breath-hold single-shot spin-echo echo-planar imaging sequence and a PACE spin-echo echo-planar imaging sequence. The navigation bar of the PACE spin-echo echo-planar imaging sequence was located at the right diaphragm (coronal section; slice thickness, 10 mm; FOV, mm; acquisition window width, ± 2 mm). Thus a coronal acquisition was adopted for both DWI sequences. The acquisition range covered the entire kidney. Specific imaging parameters are listed in Table 2. Within 1 5 days after the MRI examination, isotope renography was performed by the rapid method reported by Goates et al. [20] and Gates [21]. The GFR was measured with a SPECT scanner TABLE 2: Diffusion-Weighted MRI Parameters (b = 0 and 800 s/mm 2 ) Parameter Breath-Hold Prospective Acquisition Correction TR TE No. of signals acquired 1 2 No. of samplings 1 2 Matrix FOV (mm) Slice thickness (mm) 5 5 Interval (mm) Bandwidth (Hz) Generalized autocalibrating partially parallel acquisitions 2 2 Fat-suppression method Frequency selective saturation Frequency selective saturation Sampling time (s) AJR:200, January 2013

3 MRI of Renal Function factor were identical in the PACE and breath-hold DWI sequences. Therefore, any difference in SNR could be attributed to the sequence itself and not to these potentially confounding variables. Ratio Value p = SNR Breath-hold DWI PACE DWI p = CNR (Millennium VG3, GE Healthcare). On the day of the examination, subjects consumed a normal diet and remained hydrated. Height and body weight were measured while the subject was wearing only light clothing. An IV bolus of 296 MBq 99m Tc diethylenetriamine pentaacetic acid was acid administered. Renal dynamic blood flow and functional images were developed within 0 20 minutes. The curves were plotted, and the split renal GFR was calculated in milliliters per minute. MRI Analysis All imaging analyses were performed at an MRI workstation (1.5-T Avanto with Leonardo Syngo, Siemens Healthcare). Two abdominal radiologists with 5 and 6 years of experience in abdominal MRI evaluated the DW images. These radiologists had access to all routine MR images but were blinded to the clinical details. When they had different opinions, they reached consensus through discussion. The ADC value was calculated as: ln(s 1 / S 0 ) / (b 0 b 1 ), where ln is the natural logarithm, S 1 is the signal intensity during breath-hold DWI and PACE DWI at b 1 = 800 s/mm 2, and S 0 is the signal intensity with b 0 = 0 s/mm 2. The ADC values were measured from the fitted ADC map. The central slice of the renal parenchyma at the level of A C Fig year-old woman who is a healthy living related kidney donor. A and B, Breath-hold (A) and prospective acquisition correction (PACE) (B) diffusion-weighted MR images (DWI) with b value of 800 s/mm 2. C, Graph shows results of quantitative comparison of signal-to-noise (SNR) and contrast-to-noise (CNR) ratios of two methods. SNR and CNR values of breath-hold DWI were 3.3 and 1.2 and of PACE DWI were 6.6 and 4.5 (both p < 0.001). the renal hilum was selected. The region of interest (ROI), including the renal cortex and medulla, was manually delineated. The ADC values of the renal parenchyma of both kidneys were measured; artifacts and renal sinuses were avoided. Noise measurement in parallel imaging is tricky. In addition to depending on the coil geometry and acceleration factor, the signal and noise vary spatially throughout the MR image. As a result, the conventional method of measuring noise, in which the ROI is placed in air, cannot be used in parallel imaging. As recommended in the literature [22, 23], the SD of normal liver signal intensity was used as an estimate of the local noise. The following parameters were calculated from the PACE and breath-hold DW images at a b value of 800 s/mm 2 : SNR = SI kidney / noise, where SI is signal intensity, and contrast-to-noise ratio (CNR) = SI kidney SI liver / noise. The spatial location of the ROI, coil geometry, and acceleration B Statistical Analysis Statistical software packages (SPSS13.0, SPSS; MedCalc v10.3.0, MedCalc) were used for data analysis. Independent samples Student t tests were used to compare the SNR and CNR of the PACE and breath-hold DWI methods and to compare ADC values between the normal and reduced split renal function groups. Single-factor analysis of variance was used to compare the renal ADC values between the normal, mild reduction, and moderate-to-severe reduction groups. Pairwise comparisons were performed with the least significant difference method. Associations between the split renal GFR and the renal ADC values were analyzed by Spearman correlation analysis. The diagnostic value of renal ADC values in predicting reduction of split renal function was estimated with the receiver operating characteristic curve (ROC). MedCalc v was used to compare correlation coefficients. Differences with p < 0.05 were considered statistically significant. Results Effects of Prospective Acquisition Correction Technique on Quality of Diffusion-Weighted MRI and Association Between Renal Apparent Diffusion Coefficient and Glomerular Filtration Rate The SNR and CNR of the PACE DW images were higher than those of images acquired during breath-hold DWI (p < 0.001) (Fig. 1 and Table 3). A positive correlation was found between the renal ADC values and GFR and was verified by Spearman correlation analysis. As shown in Figure 2, the correlation coefficient between the renal ADC values and GFR measured with PACE DWI (γ = 0.490, p < 0.001) was higher than that measured with breath-hold DWI (γ = 0.238, p = 0.013) (Z = 2.126, p = 0.033). Effects of the Prospective Acquisition Correction Technique on Prediction of Split Renal Function With Apparent Diffusion Coefficient Values Split renal function was categorized as normal (GFR 40 ml/min) in 74 kidneys and TABLE 3: Comparisons of Signal- and Contrast-to-Noise Ratios Ratio Breath-Hold Prospective Acquisition Correction p Signal to noise 3.3 ± ± a Contrast to noise 1.2 ± ± a Note Except for p, values are mean ± SD. a p < AJR:200, January

4 Li et al. Renal ADC Values ( 10 5 mm 2 /s) Split Renal GFR (ml/min) reduced (GFR < 40 ml/min) in 34 kidneys according to split renal GFR. Although there were no significant differences in age (t = 0.765, p = 0.448) or sex (χ 2 = 0.234, p = 0.628) between the two groups, the ADC value was lower in the reduced split renal function group than in the group with normal function (p < 0.05) (Fig. 3 and Table 4). The area under the ROC curve (AUC) in the PACE DWI group (AUC, ± 0.045; p < 0.001) was greater than that in the breathhold DWI group (AUC, ± 0.060; p = 0.053) (Fig. 4). The results indicated that PACE DWI had fair diagnostic value in prediction of a reduction in split renal function (sensitivity, 74.3%; specificity, 73.5%) when the ADC value was mm 2 /s. In contrast, the results for breath-hold DWI did not reach statistical significance for prediction of a reduction in split renal function. Value of the Prospective Acquisition Correction Technique in Assessing Mild Reduction in Split Renal Function The split renal function reduction group was further divided into a mild reduction group (GFR < 40 ml/min; 24 kidneys) and a moderate-to-severe reduction group (GFR < 20 ml/ min; 10 kidneys). The renal ADC values in these groups were compared with those of the normal split renal function group. There were A Renal ADC Values ( 10 5 mm 2 /s) Split Renal GFR (ml/min) Fig. 2 Scatterplots of renal apparent diffusion coefficient (ADC) values and split renal glomerular filtration rate (GFR). A, Breath-hold diffusion-weighted MRI (g = 0.238). B, Prospective acquisition correction diffusion-weighted MRI (g = 0.490). no differences in age (F = 0.325, p = 0.724) or sex (χ 2 = 0.334, p = 0.846) among the three groups. However, the ADC values measured with PACE DWI differed among the groups (p < 0.001), lower ADC values corresponding to a decrease in split renal function. Analysis by least significant difference showed that the renal ADC values measured with PACE DWI in the normal function group were different from those in the mild and moderate-to-severe reduction groups (p < 0.01) (Table 5). Discussion As a 2D navigation-triggered respiratory motion artifact suppression technique [24], PACE entails use of FLASH 2D gradient-echo sequences to monitor the real-time movement of the right apex of the diaphragm during the respiratory cycle. As the diaphragm moves B into the preset collection window, the navigation pulse stops and signal acquisition is performed. Because signals are always acquired at the same position in the respiratory cycle (at end expiration) [13, 24 26], PACE effectively minimizes the effect of respiratory motion artifacts and the need for patients to hold their breath and significantly increases SNR [13, 27]. This study is the first, to our knowledge, to apply PACE DWI to the assessment of split renal function. Use of PACE DWI resulted in significantly higher SNR and CNR results than did use of breath-hold sequences, consistent with the results of Kandpal et al. in the liver [28]. This finding was due to acquisition of a greater number of signals, although the TR, TE, and bandwidth used for PACE DWI had adverse effects on image quality. The image quality of PACE DWI was superior to that of breath-hold DWI. This advantage ensures the accurate measurement of renal ADC values and may improve the assessment of split renal function. In addition, because patients do not need to hold their breath during a PACE DWI examination, the procedure is suitable for patients who are unable to hold their breath for extended durations. We observed a linear positive correlation between renal ADC values and GFR with both breath-hold DWI and PACE DWI. The ADC values of subjects with normal split renal function were significantly greater than those of subjects with reduced renal function, consistent with previous observations of breath-hold DWI [10]. Furthermore, the significantly greater correlation between renal TABLE 4: Comparison of Renal Apparent Diffusion Coefficient Values Between Split Glomerular Filtration Rate (GFR) Groups Diffusion-Weighted MRI Technique Apparent Diffusion Coefficient ( 10 5 mm 2 /s) Normal GFR Reduced GFR Breath hold ± ± a Prospective acquisition correction ± ± b Note Data are mean ± SD. a p < 0.05 b p < TABLE 5: Comparisons of Apparent Diffusion Coefficient Values Between Split Renal Function Groups Diffusion-Weighted MRI Technique Apparent Diffusion Coefficient ( 10 5 mm 2 /s) Normal Function Mild Reduction Moderate-to-Severe Reduction Breath-hold ± ± ± Prospective acquisition correction ± ± ± a Note Data are mean ± SD. a p < p p 116 AJR:200, January 2013

5 MRI of Renal Function ADC values and GFR measured with PACE DWI compared with those measured with breath-hold DWI suggested an advantage of PACE DWI in the assessment of split renal function. This finding could be attributed to the better quality of DW images obtained with the PACE technique and, correspondingly, more accurate measurement of ADC values. The ROC curve analysis also showed that the ADC values obtained via PACE DWI were significant predictors of a reduction in split renal function, whereas those obtained via breath-hold DWI were not. Altogether these findings indicated that PACE DWI has advantages over breath-hold DWI in the assessment of split renal function. We divided the reduced split renal function group into mild and moderate-to-severe reduction subgroups. The ADC values showed a decreasing trend with a progressive decline in split renal function. Subsequent least significant difference analysis showed that the ADC values of the mild reduction in split renal function group were significantly lower than those of the group with normal function, suggesting that PACE DWI may have clinical value in prediction of early-stage reduction in split renal function. Interestingly, in a 2010 preliminary study, Binser et al. [29] found that respiratorycardiac double-triggered DWI had better reproducibility of ADC measurements than respiratory-triggered DWI alone. They suggested that these potential advantages for assessing split renal function require further study. We used a b value of 800 s/mm 2 for DWI. Although the SNR values of the images were somewhat decreased at this setting, use of this b value can effectively minimize the effect of extraneous movement factors (e.g., perfusion and flow phenomena) in the voxels and better reflect the dispersion state of the kidney [30]. The ADC value measurement method used in this study was previously recommended by Fukuda et al. [31]. Because the ROI was delineated manually in the renal parenchyma in the central slice of the kidney, the perfusion effect may have been further reduced. Xu et al. [32] also found that the aforementioned ADC measurement method was reliable and appropriate in longitudinal studies. In addition, Thoeny et al. [2] reported that PACE DWI had good reproducibility in patients with normal renal graft function. Kataoka et al. [18] performed a study using renal diffusion-tensor imaging (DTI) of healthy volunteers and found good reproducibility for PACE DTI. The current DWI method cannot be used to separate the medulla from the cortex, and A C E Fig. 3 Comparison of images of subjects with normal and those with reduced split renal function. A H, Breath-hold diffusion-weighted (DW) images (A and B), corresponding apparent diffusion coefficient (ADC) maps (C and D), prospective acquisition correction (PACE) DW images (E and F), and their corresponding ADC maps (G and H) of subjects with normal (A, C, E, and G) and reduced (B, D, F, and H) split renal function. Left and right renal glomerular filtration rates of subjects with normal renal function were 65.5 and 57.0 ml/min and in subjects with reduced renal function were 9.4 and 14.9 ml/min. ADC values ( 10 5 mm 2 /s) decreased with decreasing split renal function, evidenced by increased signal intensity of renal parenchyma on DW images. Quality of PACE DW images significantly improved, indicating even greater trend toward decrease. (Fig. 3 continues on next page) B D F AJR:200, January

6 Li et al. G H Fig. 3 (continued) Comparison of images of subjects with normal and those with reduced split renal function. A H, Breath-hold diffusion-weighted (DW) images (A and B), corresponding apparent diffusion coefficient (ADC) maps (C and D), prospective acquisition correction (PACE) DW images (E and F), and their corresponding ADC maps (G and H) of subjects with normal (A, C, E, and G) and reduced (B, D, F, and H) split renal function. Left and right renal glomerular filtration rates of subjects with normal renal function were 65.5 and 57.0 ml/min and in subjects with reduced renal function were 9.4 and 14.9 ml/min. ADC values ( 10 5 mm 2 /s) decreased with decreasing split renal function, evidenced by increased signal intensity of renal parenchyma on DW images. Quality of PACE DW images significantly improved, indicating even greater trend toward decrease. Sensitivity Source of the Curve Breath-hold DWI PACE DWI Reference line Specificity manual division by ROI is even more difficult. We attempted to use two kinds of DWI to separate the medulla from the cortex and did not succeed. Therefore, we included both the medulla and the cortex when we manually delineated the ROI. Future studies should address separate evaluation of the medulla and cortex through the improved resolution of DWI or DTI and improvement of kidney image quality through the use of PACE DTI. The study had several inherent limitations. First, our use of the mean ADC value of the central slice of the renal parenchyma to represent the ADC value of the entire kidney might have caused bias. Nevertheless, because CKD is generally regarded as a diffuse disease, and the lesions at various regions are basically uniform, this is a reasonable and acceptable estimation. Second, we manually delineated Fig. 4 Graph shows results of receiver operating characteristic curve analysis for renal apparent diffusion coefficient values predictive of reduction in split renal function. Area under curve obtained with prospective acquisition correction (PACE) DWI (0.790, p < 0.001) was greater than that obtained with breath-hold DWI and indicated that PACE DWI had fair diagnostic value in prediction of reduction in split renal function. the ROI to measure the ADC values, and this practice involved a degree of subjectivity. Automated ROI delineation methods with better accuracy are needed. Third, the acquisition time of PACE DWI was longer than that of breath-hold DWI; however, in our opinion, the benefits justified this additional time. The difference in ADC value between the two methods was due to the difference in TR, which has been discussed in detail in the literature [33]. 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