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DOI: 10.1148/radiol.2361021463
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(Radiology 2005;236:189-195.)
© RSNA, 2005

Genitourinary Imaging

Functional Renal Volume: Quantitative Analysis at Gadolinium-enhanced MR Angiography—Feasibility Study in Healthy Potential Kidney Donors1

Sjoerd W. van den Dool, MSc, Martin N. Wasser, MD, Johan W. de Fijter, MD, Jan Hoekstra, MD and Rob J. van der Geest, MSc

1 From the Departments of Radiology (S.W.v.d.D., M.N.W., J.H.) and Nephrology (J.W.d.F.), and Laboratory for Clinical and Experimental Image Processing (R.J.v.d.G.), Leiden University Medical Center, Albinusdreef 2, 2233 ZA Leiden, the Netherlands. Received November 8, 2002; revision requested January 15, 2003; final revision received August 31, 2004; accepted October 1. Address correspondence to M.N.W. (e-mail: m.n.j.m.wasser{at}lumc.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To assess the feasibility of quantifying functional renal volume with gadolinium-enhanced magnetic resonance (MR) angiography.

MATERIALS AND METHODS: Institutional review board approval was obtained, and all subjects gave informed consent. A contour-detection three-dimensional algorithm for determining renal volumes was developed. The method was validated in 18 cadaveric pig kidneys by measuring the water displacement caused by the kidneys. The kidney lengths and volumes in 19 consecutive potential kidney donors who underwent gadolinium-enhanced MR angiography of the renal arteries also were determined. Differences in volume measurements between men and women and between left and right kidneys were analyzed by using the Student t test. The volume of perfused renal cortex was calculated by extracting voxels on the basis of the cortex signal intensity threshold. The relevance of renal function parameters—namely, creatinine clearance rates—in the donor candidates was assessed by using a linear regression model. Intra- and interobserver variabilities of the measurements were determined by using the Bland-Altman method.

RESULTS: Volume measurements of the cadaveric pig kidneys obtained by using MR angiography and the water displacement method were strongly correlated (r = 0.99). The mean total renal volume in the donor candidates was 196 mL (range, 136–295 mL). No significant differences in total renal volume between the men and women or between the left and right kidneys were found. The correlation between calculated renal cortex volumes (mean, 67 mL; range, 40–105 mL) and creatinine clearance rates was good (r = 0.69). Inter- and intraobserver variabilities were lower than 7%.

CONCLUSION: Quantification of functional renal volume with three-dimensional gadolinium-enhanced MR angiography seems feasible with use of the described semiautomatic method.

© RSNA, 2005


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In patients with renovascular disease, renal size is an important parameter in the decision of whether to perform an interventional procedure such as angioplasty or surgical revascularization. Long-standing renal artery stenosis causes ischemia of the kidney followed by parenchymal loss and thus results in progressive renal failure. Beyond a certain level, this parenchymal loss becomes irreversible and therapeutic interventions are no longer effective. Therefore, renal parenchymal size may be regarded as an indicator of the potential functional residual capacity of a given kidney.

Ultrasonography (US) is usually performed to measure renal length or parenchymal thickness. However, in renal length and width measurements that serve as parameters of renal size, the variable shapes of the kidneys are not taken into account because kidneys of a certain length can have a wide range of parenchymal thicknesses (1) and volumes (2). US measurement of renal volume, on the other hand, has limited repeatability and accuracy (3). It was shown that renal volume can be accurately and reproducibly measured on magnetic resonance (MR) images by using the voxel-count method (3,4).

Three-dimensional (3D) gadolinium-enhanced MR angiography has rapidly become the method of choice for screening patients who have hypertension and renal failure for renovascular disease (5–7). Gadolinium-enhanced MR angiography yields information about not only the patency of the renal artery (8) but also the perfusion of the renal parenchyma (9). The purpose of our study was to assess the feasibility of quantifying functional renal volume with gadolinium-enhanced MR angiography.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Human Study Subjects
Between April 2001 and January 2002, 19 consecutive healthy, living, related potential kidney donors (11 men, eight women; mean age, 46 years; age range, 28–65 years; mean age of men, 46.2 years; mean age of women, 45.8 years; P = .15) were referred for routine 3D contrast material–enhanced MR angiography before kidney donation. None of the donor candidates had a history of renal or renovascular disease. Results of physical examination, blood pressure measurement, and urinalysis were normal in all donor candidates. This study was part of a larger study involving kidney donors, for which we obtained institutional review board approval. All subjects gave informed consent for the MR imaging postprocessing procedures.

MR Angiography
Breath-hold 3D gradient-echo MR angiograms were obtained by using a 1.5-T unit (ACS-NT; Philips Medical Systems, Best, the Netherlands) with a phased-array body coil for signal reception. The 3D volume was imaged after 0.2 mmol of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) per kilogram of body weight was intravenously injected at a rate of 2 mL/sec by using a power injector (Spectris; Medrad, Indianola, Pa). In all subjects, the same standard sequence was used: a coronal T1-weighted sequence performed by using 4.3/1.3 (repetition time msec/echo time msec), a 400-mm field of view, a 40° flip angle, one signal acquired, a 256 x 512 matrix, a 2.6-mm section thickness interpolated to 1.3 mm, sequential k-space acquisition, and an imaging time of 24 seconds per acquisition.

To evaluate parenchymal enhancement, MR angiograms were obtained during four phases. One breath cycle was allowed between the first and second phases. The third and fourth phases each were preceded by an interval of 1 minute. A volume from the anterior side of the aorta to the posterior side of both kidneys was included in the imaging slab. The imaging delay was determined by measuring the arrival of a 2-mL test bolus of contrast material. In all subjects, the start of the MR imaging examination began with the start of enhancement of the suprarenal aorta. All image data were stored on a CD-ROM for further analysis.

Quantitative Analysis
Only those subjects with normal renal arteries at MR angiography were included in the study and had their data further analyzed. The MR angiographic data of all subjects were downloaded into a computer software program (MASS for UNIX, version 4.0; Medis, Leiden, the Netherlands) (10). This program allows the volumetric analysis of 3D MR image data sets with use of drawn contours. A new protocol was designed to maximize the computer-automated action and to minimize observer variation. This protocol consisted of two steps: First, for renal volume measurements, renal contours were drawn by the semiautomated contour recognition feature of the MASS program—after we located the kidneys for the computer program by drawing a global contour around them—with care taken to exclude the renal arteries and veins and the collecting system (Fig 1, left).



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  		Figure 1. Measurement of total renal and renal cortex volumes on coronal 3D gadolinium-enhanced gradient-echo MR angiograms (4.3/1.3, 40° flip angle, 400-mm field of view, one signal acquired, 256 x 512 matrix, 2.6-mm section thickness) Left: Image shows the contour drawn around a kidney by the computer algorithm after exclusion of the renal hilum. Summation of all voxels within the contour yields the total renal volume. Right: After thresholding, the cortex volume can be measured by adding the enhancing voxels of the cortex. The small squares do not represent the actual pixel size.

 
In the second step, we added a new feature to the MASS program that enabled us to include or exclude image pixels within a contour according to a given signal intensity that served as the minimum signal intensity threshold (Fig 1, right). To calculate the renal cortex volume, a specific signal intensity threshold has to be chosen. Figure 2 shows the percentage of renal volume at each threshold value in a plot of signal intensity gray value compared with renal volume. The higher the chosen signal intensity threshold is, the smaller the cortex volume will be. This graph represents a renal "footprint" that is based on the specific enhancement of renal tissue at gadolinium-enhanced MR angiography. Previously, at visual inspection of the coverage of deep cortical rays by the algorithm at different signal intensity thresholds in a pilot study involving five healthy individuals, we found that in these subjects, approximately 40% of the renal volume was made up of early-enhancing cortex. We therefore used this percentage as the initial threshold for all of the subjects in the current study. We further defined this threshold by averaging this threshold value with use of 1.0-mm2 region-of-interest measurements obtained at three locations in the kidney: the upper, middle, and lower poles.



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  		Figure 2. Graph of renal cortex volume compared with signal intensity gray value shows percentage of enhancing voxels (% count) that make up the renal cortex at each specific gray value used as a threshold.

 
Both the anterior and the posterior sections of the kidney contained a relatively large amount of renal cortex tissue compared with sections through the center of the kidneys, approximately 30% of which consisted of cortical tissue (Fig 3). Finally, to prevent foreshortening, the length of the kidneys was measured by using multiplanar reformations of the 3D volume.



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  		Figure 3. Selected coronal gadolinium-enhanced 3D gradient-echo MR angiograms (4.3/1.3, 40° flip angle, 400-mm field of view, one signal acquired, 256 x 512 matrix, 2.6-mm section thickness) obtained through the kidneys, from anterior (upper left) to posterior (lower right) regions, in the same patient. After signal intensity thresholding, the cortices of the right kidneys are highlighted in red.

 
All computer measurements were performed by two observers (S.W.v.d.D., J.H.) to assess inter- and intraobserver variabilities. Both observers had more than 3 years experience in MR imaging postprocessing techniques.

Reference Standard for Volume Measurements
Because, to our knowledge, no other methods to accurately measure renal volume in vivo exist, an alternative reference standard was used to evaluate the accuracy of the volumetric measurements. We incubated 18 kidneys, from adult pig cadavers, that were obtained from a slaughterhouse and from which the hilar structures were removed in a 0.05 mol/L solution of gadopentetate dimeglumine for 7–8 hours at room temperature to coat the kidney surface with gadolinium. Then, MR images of these kidneys were obtained by using the same MR angiographic sequence (during one dynamic phase) that was used in the donor candidate examinations with use of the phased-array body coil.

Immediately after MR angiography, one author (S.W.v.d.D.) determined the true volume of the kidneys by using the so-called water displacement method (2)—that is, by submersing the kidneys in water. Afterward, computer measurements of the renal volumes were obtained by another author (J.H.) without knowledge of the true volumes.

Analysis of Renal Function
Serum creatinine levels and creatinine clearance rates served as reference-standard laboratory parameters of the actual renal function of the subjects. The creatinine clearance rate (CC, in milliliters per minute) was calculated by using the Cockcroft-Gault equation (11): CC = [(140 – Ag) · Wt]/(72 · SC), where Ag is the subject's age (in years); Wt, the subject's weight (in kilograms); and SC, the serum creatinine level (in milligrams per 100 milliliters). This equation is used to calculate the creatinine clearance rate in male subjects. To calculate this value for female subjects, the creatinine clearance rate calculated for male subjects is multiplied by 0.85. To compare the new volumetric MR angiographic parameters (total renal volume, renal cortex volume, and renal length) with these laboratory parameters of renal function, the MR imaging values for the left and right kidneys were combined.

Statistical Analyses
To assess the variability of total renal volume and renal cortex volume measurements, the Bland-Altman method (12) was used. Inter- and intraobserver variabilities were calculated. The mean difference between two repeated measurements obtained by one observer or between the data sets of the two observers represents the observer variation. We compared inter- and intraobserver variations in renal cortex and total renal volume measurements with these variations in renal length measurements (a frequently used parameter in clinical practice).

To test for measurement differences between men and women and between the left and right kidneys, the Student t test was used. P < .05 was considered to indicate a significant difference. Pearson correlation coefficients for differences between the MR angiographic and fluid displacement volume measurements of cadaveric pig kidneys were calculated.

The relevance of various parameters (total renal volume; renal cortex volume; renal length; and subject age, sex, and weight) in terms of how they affect creatinine clearance was determined by using a backward linear regression model with a computer software program (SPSS for Windows, version 10; SPSS, Chicago, Ill) to exclude the nonsignificant or less significant parameters within this model.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Cadaveric Pig Kidneys
We observed a significant linear correlation between the MR angiographic and water displacement volume measurements of the cadaveric pig kidneys (r = 0.98; relative mean difference, 9.13%) (Fig 4). Coating the surfaces of the cadaveric kidneys with gadopentetate dimeglumine enabled adequate contour detection with the postprocessing algorithm (Fig 5).



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  		Figure 4. Graph illustrates correlation between renal volumes (in milliliters) measured with MR angiography and those measured by using the water displacement method. Good correlation (R2 = 0.9781 [r = 0.98]) was observed between the two sets of measurements.

 


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  		Figure 5. Coronal 3D gradient-echo MR angiographic midsection (4.3/1.3, 40° flip angle, 400-mm field of view, one signal acquired, 256 x 512 matrix, 2.6-mm section thickness) obtained through a cadaveric pig kidney coated with gadopentetate dimeglumine.

 
Human Study Subjects
All 19 potential kidney donors were included in the study, because none of them showed signs of renovascular disease at MR angiography. Table 1 shows the renal length, renal cortex volume, and total renal volume measurements obtained by using MR angiography. Results were different between the male and female subjects, but these differences were not significant. Individual total renal volume and renal cortex volume measurements of all 38 kidneys are presented in Figure 6. In this figure, renal cortex volume and total renal volume values for each left kidney and each right kidney are separately shown for comparison. Mean lengths of the left and right kidneys were 11.3 cm ± 0.8 (standard deviation) and 10.8 cm ± 0.8, respectively. This 5-mm difference in renal length was small but significant (P = .005). Intra- and interobserver variations in renal length measurements were lower than 1%. As can be seen in Figure 7, kidneys of similar lengths can have a wide range of volumes.


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  		TABLE 1. Mean Cortex Volume, Total Renal Volume, and Renal Length Measurements in 19 Healthy Potential Kidney Donors

 


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  		Figure 6. Bar graph shows total renal volumes and renal cortex volumes measured with MR angiography in all potential donors. For each subject, values for the left kidney are presented first (marked by odd numbers on x-axis) and are followed by values for the right kidney.

 


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  		Figure 7. Graph shows correlations between renal length and renal volume. One particular length may correspond to a large variety of volumes.

 
Differences in total renal volume and renal cortex volume between the left and right kidneys were not significant. The inter- and intraobserver variabilities of these measurements, expressed as relative mean differences, are given in Table 2. All variations were within an acceptable range (<7%). The renal cortex volume was different in each kidney, with a mean volume of 34.6% ± 3.


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  		TABLE 2. Intraobserver and Interobserver Variability of Total Renal Volume and Renal Cortex Volume Measurements

 
The renal cortex volume (of two kidneys combined) was correlated with the calculated creatinine clearance (r = 0.69, P = .001). This correlation with the renal cortex volume was higher than those with the total renal volume and the renal length (for two kidneys combined) (r = 0.66 and r = 0.63, respectively; P < .004). At backward linear regression analysis, renal length was excluded, and this exclusion indicated that renal length, in contrast to total renal volume and renal cortex volume, was not an important factor in creatinine clearance. Renal cortex volume and creatinine clearance were inversely correlated with subject age (r = 0.51 and r = 0.59, respectively). The cortical thicknesses of the 38 kidneys ranged from 10 to 12 mm, but focal differences in cortical thickness within the kidneys could be seen, as shown in Figure 3.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
On the basis of the voxel-count technique, we developed a method for quantifying total renal volume and renal cortex volume by using the contrast-enhanced MR angiographic data of 19 healthy potential kidney donors. At present, no other accurate method of measuring human kidney volume in vivo exists, to our knowledge. Therefore, we could not use a reference standard for our in vivo measurements. Measuring the volumes of ex vivo kidneys by means of fluid displacement—for example, during the harvesting of the organs for transplantation—introduces errors such as the inclusion of ureters, vessels, and variable amounts of perinephric fat. Also, differences in volume between normally perfused in vivo kidneys and harvested ex vivo kidneys may exist. To ensure identical physiologic conditions, we used cadaveric pig kidneys to compare our method of MR volume measurement with fluid displacement analysis. We observed a strong correlation between the two methods (r = 0.98), with a mean difference of 9.13%. Bakker et al (3) measured a mean renal volume of 180 mL in healthy volunteers with two-dimensional spin-echo MR imaging. This value compares favorably to the mean volume of 196 mL that we measured in our study.

We found no significant difference in total renal volume between the men and the women, but this may have been due to the limited number of subjects. We also observed no significant difference in total renal volume but a small yet significant difference in renal length between the left and right kidneys: The left kidney was, on average, 5 mm longer than the right kidney. We found that kidneys of similar lengths had a wide range of volumes; this finding indicates that renal length is not a reliable indicator of renal size.

Because there is, to our knowledge, no other technique for accurately measuring human renal cortex volume in vivo, a true reference standard for the measurement of this parameter also was not available. In experimental animals, after injection of radiolabeled microspheres (13), radiography of sliced kidneys may yield an estimation of cortical thickness but not of total cortical volume. Because the total renal volume decreases after kidneys are sliced, extrapolation of the amount of cortical tissue per slice probably does not yield an adequate measurement of cortical volume in vivo. Because the renal cortex is made up largely of glomeruli, proximal tubuli, and afferent and efferent arterioles, it becomes enhanced rapidly after contrast agent injection. Therefore, by calculating the portion of the kidney that becomes enhanced during the arterial phase of MR angiography, it is possible to determine the volume of perfused functioning cortex. To test this hypothesis, we performed this study by examining a homogeneous group of potential kidney donors who did not have cardiovascular, renal, or renovascular disease. To obtain reproducible results, it was essential to use a similar MR angiographic protocol, with standardized timing of the start of the acquisitions and a standardized imaging duration, in all individuals.

No clear-cut border between the renal cortex and the medulla is depicted on MR angiograms. However, at histologic analysis, one can observe a relatively gradual transition (13,14). We therefore had to choose a cutoff point to demarcate these structures that was based on the signal intensity of the pixels. This threshold value was determined in a standardized way in all donor candidates. We found that in healthy individuals aged 28–65 years, the proportion of the kidney that is cortical tissue remains fairly constant (34.6% ± 3), irrespective of the subject's age or sex. The mean thickness of the cortex of these kidneys ranged from 10 to 12 mm, which is consistent with data in the literature (13).

An advantage of using gadolinium-enhanced MR angiography for these measurements is that frequently encountered anomalies such as cysts, which contribute to renal mass and volume but not to renal function, are excluded from the quantification of the functional renal cortex volume.

Since glomerular filtration is an important component of renal function and is determined according to the number and quality of glomeruli, renal cortex volume should, in theory, be directly related to renal function. Indeed, we observed a good correlation between renal function (estimated according to the calculated creatinine clearance) and cortex volume (r = 0.69), and this correlation was better than that between renal function and either total renal volume or renal length. Linear regression analysis revealed a nonsignificant relationship between renal length and creatinine clearance.

Because we used standardized imaging and postprocessing methods, the intra- and interobserver variabilities of all measurements were lower than 7%. The method that we developed is semiautomatic: Operator-dependent interactions are limited to manual drawing of global contours around the kidneys to locate them for the computer algorithm and region-of-interest measurements at three predefined points in the kidney. In the future, fully automatic segmentation and thresholding that facilitate even further reductions in interstudy variation may be feasible.

There were several limitations to this study. First, no reference standard for in vivo measurement of total renal volume or renal cortex volume measurement was available. However, with use of a standardized imaging protocol and a semiautomatic postprocessing algorithm, it seems possible to compare different measurement technique and subject groups. Second, because of the gradual transition from the renal cortex to the medulla, we had to choose a cutoff signal intensity value to isolate the cortex. As a starting value for our computer algorithm, we chose the signal intensity at which 40% of the total renal volume became enhanced—this value was derived from a pilot experiment—and we averaged this value by using region-of-interest measurements obtained at three locations in the kidney. The thus-measured volume may not exactly correspond to the anatomic cortex, but, again, by using a standardized protocol, it may be possible to compare different measurement technique and subject groups. Third, we compared our MR angiography–based volume measurements with estimated creatinine clearance rates. For ethical reasons, we could not measure glomerular filtration rates, although such measurements would have provided us with a better standard for cortical function. The Cockcroft-Gault equation for estimating creatinine clearance rates, however, is well suited for comparing measurement technique and subject groups, which was the purpose of our study. Finally, because of the limited number of subjects examined, the reported statistical analysis results should be interpreted with caution. Larger studies are needed to confirm our findings.

Additional research is needed to determine the importance of volumetric analysis of the kidneys in patients with renal artery stenosis who are being considered for interventional procedures. In this article, we describe a method for quantifying the functioning renal parenchyma in healthy humans by using MR angiographic data.


   FOOTNOTES
 

Abbreviations: 3D = three-dimensional

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, M.N.W.; study concepts, S.W.v.d.D., M.N.W., R.J.v.d.G.; study design, M.N.W., S.W.v.d.D.; literature research, S.W.v.d.D., J.W.d.F.; clinical studies, S.W.v.d.D., J.H., J.W.d.F.; experimental studies, S.W.v.d.D., J.H.; data acquisition, S.W.v.d.D., J.H.; data analysis/interpretation, S.W.v.d.D., M.N.W.; statistical analysis, S.W.v.d.D., J.H.; manuscript preparation and definition of intellectual content, S.W.v.d.D., M.N.W., R.J.v.d.G.; manuscript editing and final version approval, S.W.v.d.D., M.N.W.; manuscript revision/review, J.W.d.F., R.J.v.d.G.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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  2. Bakker J, Olree M, Kaatee R, de Lange EE, Beek FJ. In vitro measurement of kidney size: comparison of ultrasonography and MRI. Ultrasound Med Biol 1998; 24:683–688.[CrossRef][Medline]
  3. Bakker J, Olree M, Kaatee R, et al. Renal volume measurements: accuracy and repeatability of US compared with that of MR imaging. Radiology 1999; 211:623–628.[Abstract/Free Full Text]
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  5. Marcos HB, Choyke PL. Magnetic resonance angiography of the kidney. Semin Nephrol 2000; 20:450–455.[Medline]
  6. Dong Q, Schoenberg SO, Carlos RC, et al. Diagnosis of renal vascular disease with MR angiography. RadioGraphics 1999; 19:1535–1554.[Abstract/Free Full Text]
  7. Grist TM. Magnetic resonance angiography of renal artery stenosis. Am J Kidney Dis 1994; 24:700–712.[Medline]
  8. Prince MR. Renal MR angiography: a comprehensive approach. J Magn Reson Imaging 1998; 8:511–516.[Medline]
  9. Ros PR, Gauger J, Stoupis C, et al. Diagnosis of renal artery stenosis: feasibility of combining MR angiography, MR renography, and gadopentetate-based measurements of glomerular filtration rate. AJR Am J Roentgenol 1995; 165:1447–1451.[Abstract/Free Full Text]
  10. van der Geest RJ, Buller VG, Jansen E, et al. Comparison between manual and semiautomated analysis of left ventricular volume parameters from short-axis MR images. J Comput Assist Tomogr 1997; 21:756–765.[CrossRef][Medline]
  11. Cockcroft DW, Gault MH. Prediction of creatinine clearance from serum creatinine. Nephron 1976; 16:31–41.[Medline]
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