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Genitourinary Imaging |
1 From the Department of Radiology, University Hospitals Leuven, Leuven, Belgium. Received March 25, 2004; revision requested June 4; revision received July 15; accepted August 13. H.C.T. supported by the Kurt and Senta Hermann Foundation, Vaduz, Liechtenstein. Address correspondence to H.C.T., Department of Diagnostic, Interventional, and Pediatric Radiology, University Hospital of Bern, Inselspital, Freiburgstrasse 10, CH-3010 Bern, Switzerland (e-mail: harriet.thoeny@insel.ch).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Study protocol was approved by local ethics committee; informed consent was obtained. Eighteen healthy volunteers and 15 patients underwent transverse fat-saturated echo-planar DW MR imaging of the kidneys during normal breathing. Freehand regions of interest were delineated in the cortex and medulla of the kidneys. The following apparent diffusion coefficient (ADC) values were calculated: ADC of all b values (ADCavg), ADC of low b values (b = 0, 50, 100 sec/mm2; ADClow), and ADC of high b values (b = 500, 750, 1000 sec/mm2; ADChigh). These values were calculated to differentiate influence of perfusion and diffusion. Reproducibility was assessed by repeating the same protocol in five randomly selected volunteers after 6 months. For statistical analysis, Student t tests were used.
RESULTS: In all volunteers, ADCavg and ADChigh were significantly higher in the cortex than in the medulla (P < .001). No difference between the cortex and medulla could be observed for ADClow. Patients with renal failure had significantly lower ADCavg (P < .001, P = .004), ADClow (P = .02, P = .03), and ADChigh (P = .02, P = .04) of cortex and medulla, respectively, than did volunteers. In the patient with pyelonephritis, all ADC values of cortex and medulla were substantially lower compared with the contralateral side, whereas patients with ureteral obstruction showed varying degrees of difference in all ADC values compared with the contralateral side. No statistically significant changes were found in the repeat study of the volunteers.
CONCLUSION: DW MR imaging is feasible and reproducible in the assessment of renal function, as shown in our initial experience with a small number of patients and volunteers.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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The apparent diffusion coefficient (ADC), as a quantitive parameter calculated from the DW MR images, combines the effects of capillary perfusion and water diffusion in the extracellular extravascular space (1). Thus, DW MR imaging provides information on perfusion and diffusion simultaneously in any organ, it can be used to differentiate normal and abnormal structures of tissues better, and it might help in the characterization of various abnormalities.
DW MR imaging is already an established method used routinely at several institutions in the diagnosis of acute stroke (2).
Only in recent years has DW MR imaging been used in extracranial organs; for example, it has been used both to monitor treatment response and tissue characterization and to perform functional evaluation of different organs, such as the parotid glands or kidneys (3–12). DW MR imaging of abdominal organs is much more difficult to perform as a result of physiologic motion artifacts and heterogeneous composition of the organs (10,13). The kidneys are one of the most interesting organs in which to measure ADC values. With their complex anatomic structure and physiology, they are extremely challenging for DW MR imaging. Previous studies generally involved the use of breath-holding sequences (9,11,13–15). This made it difficult to use DW MR imaging in severely ill or dyspneic patients. Furthermore, only a few MR sections were obtained through the kidneys (9,11,13). This harbors the inherent risk of missing small focal lesions.
Thus, the aim of our study was to prospectively evaluate (a) the feasibility of DW MR imaging in the assessment of renal function in healthy volunteers and in patients with various renal abnormalities and (b) the reproducibility of DW MR imaging in volunteers.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Serum creatinine values were obtained from all patients on the day of the MR examination.
The study protocol was approved by the local ethics committee, and informed consent was obtained from all volunteers and patients.
MR Imaging
MR imaging was performed with a 1.5-T MR imager (Sonata; Siemens, Erlangen, Germany) with a 40 mT/m maximum gradient capability with a combination of an anterior and a posterior six-channel body coil. Five randomly selected volunteers (three men and two women; median age, 29 years; age range, 25–36 years) underwent a repeat study with the identical protocol after a mean time of 6 months ± 1 (standard deviation) to determine the reproducibility of the DW MR imaging results.
For morphologic evaluation of the kidneys, a coronal T2-weighted half-Fourier rapid acquisition with relaxation enhancement—or RARE—sequence (HASTE; Siemens) was used, with an early and late echo. A transverse T1-weighted fast low-angle shot (or FLASH) gradient-echo sequence was also used, and both in-phase and out-of-phase images were acquired. The early echo T2-weighted images were acquired with the following parameters: section thickness, 4.0 mm; intersection gap, 1 mm; field of view, 400 x 400 mm; matrix size, 220 x 256; one signal acquired; voxel size, 1.8 x 1.6 x 4.0 mm; repetition time msec/echo time msec, 1040/63; partial Fourier factor, 5/8; 20 sections acquired; total acquisition time, 22 seconds. The late-echo T2-weighted images were acquired with identical parameters, except for an echo time of 361 msec and a partial Fourier factor of 7/8, which resulted in a total acquisition time of 23 seconds. For the T1-weighted images, the following parameters were used: section thickness, 5.0 mm; intersection gap, 1 mm; field of view, 380 x 380 mm; matrix size, 179 x 256; one signal acquired; voxel size, 2.1 x 1.5 x 5.0 mm; repetition time, 101 msec; in-phase echo time, 4.76 msec; out-of-phase echo time, 2.38 msec; flip angle, 70°; bandwidth, 350 Hz per pixel; parallel imaging with modified sensitivity encoding (or mSENSE) with a parallel imaging reduction factor of two; number of sections acquired, 25; acquisition time, 20 seconds.
Transverse DW multisection echo-planar MR imaging was performed with the following diffusion gradient b values: 0, 50, 100, 150, 200, 250, 300, 500, 750, and 1000 sec/mm2. These were applied in three orthogonal directions and subsequently averaged to minimize the effects of diffusion anisotropy. The following parameters were used for this sequence by applying modified sensitivity encoding: parallel imaging reduction factor of two; 3200/71; section thickness, 5 mm; intersection gap, 1 mm; voxel size, 3.0 x 3.0 x 5.0 mm; matrix size, 128 x 128; field of view, 380 x 380 mm; partial Fourier factor, 6/8; bandwidth, 1502 Hz per pixel; six signals acquired. Fat saturation was used to avoid chemical shift artifacts, and two presaturation slabs were positioned perpendicular to the anterior and posterior sections, respectively, to suppress motion influences. The whole sequence consisted of 25 sections, with an acquisition time of 9 minutes 22 seconds. The study was performed during normal respiration. ADC maps were calculated automatically with the MR system. Calculated ADC values are expressed in square millimeters per second.
Image Analysis
Image analysis was performed off-line at a Linux workstation (Dell, Round Rock, Tex) with dedicated software (Biomap; Novartis, Basel, Switzerland). No major distortion artifacts due to susceptibility or eddy currents or N/2 ghosting artifacts were observed in the DW images of all subjects.
Morphologic evaluation of the images was performed in consensus by two experienced radiologists who were blinded to the DW MR images and data (H.C.T., R.H.O.). The presence and size of parenchymal lesions, focal or diffuse parenchymal signal alteration, corticomedullary differentiation (normal, reduced, absent), perirenal changes, and dilatation of the collecting system (mild, moderate, marked) were noted.
In the transverse ADC map, circular regions of interest (ROIs) were placed in the cortex and medulla on several sections (upper, middle, and lower poles) in each kidney by means of consensus of two observers (H.C.T., F.D.K.). For each kidney, the ROIs in the cortex were merged into a single ROI, and the same procedure was performed for the medulla. This yielded four ROIs per subject (one ROI for cortex [on average, 3.2 cm3± 1.1] and one ROI for medulla [on average, 2.7 cm3± 0.7] for each kidney), from which the average ADC values were calculated. Afterward, these ROIs were copied on the original DW images, from which the average intensities for each b value could be obtained.
In addition, ADCs of the kidneys were calculated separately for the low (ADClow; b = 0, 50, and 100 sec/mm2) and high (ADChigh; b = 500, 750, and 1000 sec/mm2) b values to enable differentiation of the relative influence of the perfusion fraction and true diffusion (1). ADChigh reflects almost only diffusion, whereas ADClow is composed of both diffusion and perfusion (1).
The ADC values were calculated by using a least squares solution of the following system of equations: S(i) = S0 · exp(–bi · ADC), where S(i) is the signal intensity measured on the ith b value image and bi is the corresponding b value. S0 is a variable estimating the exact (without noise induced by the MR measurement) signal intensity for a b value of 0 sec/mm2. To reduce the influence of the noise in the measured signal intensity of the original DW MR images in the ADC calculations, the diffusion images obtained with three b values were used (0, 50, and 100 sec/mm2 for ADClow; 500, 750, and 1000 sec/mm2 for ADChigh) when calculating the ADC values.
Statistical Analysis
Statistical analysis was performed with the Excel 9.0 (Microsoft, Seattle, Wash) and Analyse-It, version 1.68 (Analyse-It Software, Leeds, England) software packages. The ADC values of the volunteers and patients with renal failure are reported as the mean ± standard deviation.
The group of patients with renal failure was divided into two groups according to their serum creatinine level by using an arbitrary threshold of 2.5 mg/dL (221 µmol/L) to compare diffusion differences at different serum creatinine levels. The serum creatinine level was below this level in 11 patients and above this level in nine.
Statistical analysis was performed by using two-tailed paired Student t tests for the comparison of cortex and medulla in the volunteers. Two-tailed unpaired Student t tests were used when comparing the patients with renal failure with the volunteers. A P value of less than .05 was considered to indicate a statistically significant difference.
For the patients with unilateral abnormalities, the reported values are the percentage differences between the normal and the abnormal kidney. Differences of more than 10% were arbitrarily chosen as substantial.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Of the three patients with ureteral obstruction, two had ureteral calculi, and one had transitional cell carcinoma in the left proximal ureter, with moderate dilatation of the collecting system and some perirenal fluid. One patient had a calculus in the left proximal ureter, with moderate dilatation of the collecting system. The other had a calculus in the right proximal ureter, with only a slightly dilated collecting system, but perirenal fluid surrounded the lower pole because of fornix rupture.
The patient with acute unilateral multifocal pyelonephritis showed slight enlargement of the affected left kidney.
Eleven patients had renal failure of various causes (Table 1). Four patients had normal findings at morphologic analysis of the kidneys (patients 1–4); two of these patients had a fresh hematoma at the lower pole of the left kidney less than 7 days after biopsy (patients 3 and 4). Patient 5 had enlarged kidneys: The left kidney measured 149 x 66 mm, and the right kidney measured 145 x 53 mm. One patient (patient 6) who abused an analgesic (phenacetin nephropathy) had a small irregular right kidney and a shrunken hydronephrotic left kidney; the shrunken left kidney was caused by external compression of the ureter by a huge tumor mass and was therefore not included in DW MR analysis. One patient had undergone nephrectomy on the left side 50 years previously for renal tuberculosis. The right kidney was reduced in size, with reduced corticomedullary differentiation and perirenal stranding. In addition, a 7-cm-diameter cortical cyst at the middle pole and a 1-cm-diameter cyst at the upper pole were visible (patient 7). Another patient had reduced corticomedullary differentiation, perirenal stranding, and a small (1 cm in diameter) cortical cyst at the lower pole on the right side (patient 8).
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Functional Evaluation
The group of volunteers used for analysis of reproducibility had ADCavg values of (2.00 ± 0.07) x 10–3 mm2/sec and (1.89 ± 0.07) x 10–3 mm2/sec, ADClow values of (3.50 ± 0.47) x 10–3 mm2/sec and (3.71 ± 0.43) x 10–3 mm2/sec, and ADChigh values of (1.67 ± 0.11) x 10–3 mm2/sec and (1.54 ± 0.09) x 10–3 mm2/sec for the cortex and medulla, respectively, in the first examination. After 6 months ± 1, these same volunteers underwent a repeat MR examination, which resulted in ADCavg values of (1.98 ± 0.07) x 10–3 mm2/sec and (1.85 ± 0.06) x 10–3 mm2/sec, ADClow values of (3.40 ± 0.50) x 10–3 mm2/sec and (3.73 ± 0.62) x 10–3 mm2/sec, and ADChigh values of (1.63 ± 0.10) x 10–3 mm2/sec and (1.52 ± 0.08) x 10–3 mm2/sec for the cortex and medulla, respectively (Fig 1). No significant differences were found when comparing any of the corresponding areas and the different ADC values with a paired Student t test.
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Patients
Unilateral abnormality.—The results for the patients with a unilateral abnormality are listed in Table 3.
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When dividing the group of patients with renal failure into two groups according to serum creatinine level (an arbitrary threshold of 2.5 mg/dL [221 µmol/L] was used), the group of patients with a creatinine level lower than this threshold (n = 11) had ADC values lower (except the ADChigh in the medulla) than those in volunteers (Table 2). The reported P values for this group were as follows: .03 and .09 for ADCavg of the cortex and medulla, respectively; .37 and .37 for ADChigh of the cortex and medulla, respectively; and .26 and .61 for ADClow of the cortex and medulla, respectively.
The group of patients with a creatinine level higher than the threshold (n = 9) showed significant differences from the volunteers for all ADC values, except for ADChigh in the medulla (Table 2). In this group, ADCavg values were (1.73 ± 0.24) x 10–3 mm2/sec for the cortex (P = .005) and (1.61 ± 0.26) x 10–3 mm2/sec for the medulla (P = .02). ADClow and ADChigh were (3.07 ± 0.68) x 10–3 mm2/sec (P = .02) and (1.44 ± 0.24) x 10–3 mm2/sec (P = .02) for the cortex and (3.10 ± 0.52) x 10–3 mm2/sec (P = .005) and (1.31 ± 0.26) x 10–3 mm2/sec (P = .06) for the medulla, respectively (Fig 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In several previously published articles, authors analyzed the feasibility of DW MR imaging of the kidneys by using different technical approaches (10,15,16); however, only a few studies were performed in patients (9,11).
The present study was performed to investigate DW MR imaging of the kidneys in healthy volunteers and patients with various diffuse renal abnormalities in a normal hydration state and without breath holding.
DW MR imaging provides information on diffusion and perfusion at the same time (17). When applying only high b values, the influence of perfusion is largely cancelled out, and the ADC value approximates the true diffusion. Low b values are influenced by both perfusion and diffusion. Thus, calculating the ADC of low and high b values separately provides more specific information on kidney function.
The ADCs of the healthy volunteers calculated with all b values and those calculated with high b values (b value of 500, 750, and 1000 sec/mm2) were significantly higher in the cortex than in the medulla. Similar differences were observed in a study in which diffusion tensor imaging was used and gradients were applied in six directions (14) and in a study performed without breath holding in which gradients were applied in three directions (16). In contrast, studies (9,15) in which b values of up to 198 and 300 sec/mm2, respectively, were applied showed the ADC of the medulla to be higher than that of the cortex. In several other studies, no effort was made to differentiate between ADC of the cortex and ADC of the medulla (4,11,16).
When comparing ADClow and ADChigh of the cortex and medulla separately in the current study, a significant difference could only be observed in ADChigh. The difference in ADChigh is probably due to the presence of more free diffusion-inhibiting structures in the medulla than in the cortex. However, the lack of difference between the cortex and medulla in ADClow might be because the effect of higher true diffusion in the cortex is largely cancelled out by the greater anisotropy due to the radial orientation of the structures in the medulla.
A group studying DW MR imaging of the kidneys without breath holding observed high interindividual differences of ADC values in healthy volunteers (16). This finding was attributed to the hydration state. Since no mean age of the subjects was mentioned in this study, however, these differences could also be related to differences in age. Indeed, our results in a relatively homogenous age group of volunteers did not show large differences, even when we disregarded hydration state.
A study by Müller et al (15) showed a significant decrease in ADC in volunteers who were dehydrated compared with volunteers who were hydrated. Under normal conditions, this may be less important, since hydration status in volunteers did not seem to substantially influence the results. The results were reproducible even after an interval of several months. The standard deviation of the ADC values in our group of volunteers was relatively small.
Most of the previously published studies dealing with DW MR imaging of the kidneys were performed with breath holding and covered only portions of the kidneys (9,11,13,15). In contrast, our data do not show major motion artifacts, the image quality was good (even in obese patients), and the examinations were performed during normal respiration. A pilot study was performed in two volunteers; DW MR imaging without and with pulse triggering (in the same individual) did not show substantial differences in calculated ADC values or image quality (data not shown). Thus, our investigation was performed with free breathing and without pulse triggering. Repetition times in a pulse-triggered sequence change in patients who are nervous, have an irregular pulse, or both. This can change the signal intensities of the DW MR images with a possible negative effect on the accuracy and image quality of the ADC maps. Obtaining images during normal respiration is a major advantage in the clinical routine.
In our study protocol, the entire kidneys were covered with a small section thickness. This allows visualization of smaller focal changes and is clinically important in patients with small renal lesions or in the detection of early vascular changes in patients with transplanted kidneys.
We know from previously published data that the medulla of the kidney is anisotropic because of the radial orientation of its structures (11,12,14). To our knowledge, there is only one study in which diffusion tensor imaging of the kidneys was performed (14). Performing DW MR imaging in only one direction (z axis direction) because of anisotropy in the medulla might lead to a loss of information under certain conditions. This is an important aspect, for instance, in kidney transplants. Thus, our investigation was performed by averaging the three orthogonal directions and has the following advantages. First, ADC fluctuations due to different kidney positions are avoided. Second, DW MR imaging is easier to perform and postprocess than diffusion tensor imaging. Third, most of the chronic parenchymal renal diseases (eg, glomerulonephritis, glomerulosclerosis, interstitial nephritis) originate in the cortex. Anisotropy is not a main issue there; therefore, diffusion tensor imaging does not provide additional information, and averaging of the three orthogonal directions to minimize the influence of anisotropy seems to be justified.
In patients with high serum creatinine values, Fukuda et al (11) observed a decrease in ADC compared with those with normal values. This is confirmed by the results in the present study. Acute and chronic renal failure, as well as renal artery stenosis, also showed decreased ADC values compared with those of healthy volunteers (9). This corresponds to our findings in the group of patients with renal insufficiency. Independent of the underlying abnormality—which causes chronic renal failure—interstitial fibrosis, tubular atrophy, and scarring of glomeruli are the final results (18). This implies a restriction of free water in the extravascular extracellular space and causes a decrease in ADC. However, an overlap of the ADC in the cortex and medulla between patients and volunteers was observed when only patients with serum creatinine levels below 2.5 mg/dL [221 µmol/L] were analyzed.
A study performed in pigs with renal artery stenosis or ureteral obstruction also showed a decrease in ADC (15). Our investigation in three patients with ureteral obstruction confirms a decrease in ADClow of variable extent. The ADCavg showed only slight changes in all three patients, and the ADChigh changed to a varying extent. Thus, differentiation of ADCavg, ADClow, and ADChigh may allow more subtle analysis of the different abnormalities. These findings are likely to be attributed to differing degrees and durations of the obstruction. This could be important for the clinical care of the patient. Mechanical obstruction to urinary outflow causes a rise in luminal pressure and dilation of the proximal collecting system and consequent increased interstitial pressure in the cortex and medulla, as well as decreased renal blood flow, which is reflected in a decrease in ADClow. However, further investigations in a larger series are necessary to quantify the degree of obstruction.
In the patient with acute pyelonephritis, a lower ADC (ADCavg, ADClow, and ADChigh) value was observed in the cortex and medulla when compared with the opposite side. This corresponds to zones of inflammation involving the papilla and cortex (18).
A combination of conventional MR imaging and DW MR imaging provides information on morphologic and functional changes at the same time. With functional evaluation, DW MR imaging is able to depict even early alterations (9).
Future applications for DW MR imaging of the kidneys might include children with nephritis, follow-up of patients undergoing chemotherapy with nephrotoxic agents or immunosuppressive drugs, and follow-up of patients with glomerulonephritis or tubulointerstitial disease.
There are limitations of our study. First, the number of patients with the same abnormality is small. To analyze different abnormalities in more detail, larger series must be conducted, possibly with histopathologic correlation.
Second, our volunteers are of a homogeneous younger age group, whereas the patients have a wider range of ages. Thus, no age matching between volunteers and patients could be performed. This is important because the ADC of the kidneys probably decreases slightly over the years.
In conclusion, DW MR imaging of the kidneys gives reproducible noninvasive information on renal function in healthy volunteers, and it is also feasible in severely ill patients. It may provide information as to the degree of kidney dysfunction, assist in the differentiation of various renal abnormalities, and be applicable for follow-up of patients with various abnormal conditions. However, larger scale studies are needed for confirmation.
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, H.C.T.; study concepts and design, H.C.T., F.D.K., R.R.P.; literature research, H.C.T., F.D.K., R.R.P.; clinical studies, all authors; data acquisition, H.C.T., F.D.K., R.R.P.; data analysis/interpretation, all authors; statistical analysis, F.D.K., R.R.P.; manuscript preparation, definition of intellectual content, and editing, H.C.T., F.D.K.; manuscript revision/review and final version approval, all authors
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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