• View in gallery
    Figure 1

    Schematic representation of procedural timelines for CT urography (CTU; A), magnetic resonance urography (MRU; B), and excretory MRU (C) performed on 9 healthy Beagles between January 2020 and October 2020. Urography images evaluated by reviewers were obtained at 3 minutes and 7 minutes after furosemide administration in each urography technique.

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    Figure 2

    Representative postcontrast dorsal plane reconstructed maximum intensity projection (MIP) CTU of 1 of the 9 Beagles described in Figure 1 showing the 3 sections considered by reviewers for each ureter: proximal ureter (A), defined as the segment from the renal pelvis to the caudal level of the given kidney; middle ureter (B), defined as the segment from the caudal level of the given kidney to the cranial level of the aortic bifurcation; and distal ureter (C), defined as the segment from the aortic bifurcation to the ureterovesical junction. The dog’s right side is toward the left of the image, and the right distal ureter is obscured by the urinary bladder because of the MIP reconstruction used to obtain the image. The image is displayed in a mediastinum kernel, with a window width of 1,500 HU, window level of 450 HU, and slice thickness of 1 mm.

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    Figure 3

    Representative postcontrast reconstructed dorsal oblique plane (A and E) and reconstructed dorsal (B and F), MIP (C and G), and volume-rendered (D and H) CTU images of 1 of the 9 dogs described in Figure 1 obtained at 3 minutes (A through D) and 7 minutes (E through H) after furosemide administration. Only reconstructed dorsal plane images (B and F) were used in analysis; the other images were generated to show each ureter along its path (A and E) and the urinary tract at a glance. The renal pelvises and most of the lengths of the ureters are clearly visualized; however, parts of the ureters have incomplete opacification, consistent with peristalsis. The dog’s right side is toward the left in all images.

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    Figure 4

    Representative 3-D T2-weighted static-fluid MRU images of 1 of the 9 dogs described in Figure 1 obtained at 3 minutes (A through D) and 7 minutes (E through H) after furosemide administration and displayed in a reconstructed dorsal oblique plane (A and E) and reconstructed dorsal (B and F; used in analysis), MIP (C and G), and volume-rendered (D and H) images. The left ureter is indistinct and blurred; the right ureter is not evident at 3 minutes after furosemide administration, and only the proximal portion of it is evident at 7 minutes after furosemide administration.

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    Figure 5

    Representative 3-D T1-weighted excretory MRU images of 1 of the 9 dogs described in Figure 1 obtained at 3 minutes (A through D) and 7 minutes (E through H) after furosemide administration and displayed in a reconstructed dorsal oblique plane (A and E) and reconstructed dorsal (B and F; used in analysis), MIP (C and G), and volume-rendered (D and H) images. The renal pelvises and ureters are clearly visualized.

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    Figure 6

    Representative reconstructed 3-D T2-weighted dorsal plane static-fluid MRU images of 2 of the 9 dogs described in Figure 1 obtained 7 minutes after administration of furosemide. Ghosting artifacts are observed due to urinary bladder distension (arrows; A) or ureteral peristalsis (arrowheads; B).

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Comparison of static-fluid or excretory magnetic resonance urography with computed tomography urography for visualization of nondilated renal pelvises and ureters in healthy Beagles

Sang-Kwon LeeCollege of Veterinary Medicine, Kyungpook National University, Daegu, South Korea

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Seongjae HyeongCollege of Veterinary Medicine and BK21 Plus Project Team, Chonnam National University, Gwangju, South Korea

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Soyeon KimCollege of Veterinary Medicine and BK21 Plus Project Team, Chonnam National University, Gwangju, South Korea

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Chang-Yeop JeonNational Primate Research Center (NPRC), Korea Research Institute of Bioscience and Biotechnology (KRIBB), Cheongju, South Korea

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Kyung-Seob LimFuturistic Animal Resource & Research Center (FARRC), Korea Research Institute of Bioscience and Biotechnology (KRIBB), Cheongju, South Korea

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Jihye ChoiCollege of Veterinary Medicine, Kyungpook National University, Daegu, South Korea

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Abstract

OBJECTIVE

To assess the usefulness of magnetic resonance urography (MRU) for the visualization of nondilated renal pelvises and ureters in dogs and to compare our findings for MRU versus CT urography (CTU).

ANIMALS

9 healthy Beagles.

PROCEDURES

Dogs underwent CTU, static-fluid MRU, and excretory MRU, with ≥ 7 days between procedures. Contrast medium was administered IV during CTU and excretory MRU, whereas urine in the urinary tract was an intrinsic contrast medium for static-fluid MRU. For each procedure, furosemide (1 mg/kg, IV) was administered, and reconstructed dorsal plane images were acquired 3 minutes (n = 2) and 7 minutes (2) later. Images were scored for visualization of those structures and for image quality, diameters of renal pelvises and ureters were measured, and results were compared across imaging techniques.

RESULTS

Excretory MRU and CTU allowed good visualization of the renal pelvises and ureters, whereas static-fluid MRU provided lower visualization of the ureters. Distention of the renal pelvises and ureters was good in excretory MRU and CTU. Distention of the ureters in static-fluid MRU was insufficient compared with that in CTU and excretory MRU. Distinct artifacts were not observed in CTU and excretory MRU images. Static-fluid MRU images had several mild motion artifacts.

CLINICAL RELEVANCE

Our findings indicated that excretory MRU with furosemide administration was useful for visualizing nondilated renal pelvises and ureters of dogs in the present study. When performing MRU for the evaluation of dogs without urinary tract dilation, excretory MRU may be more suitable than static-fluid MRU.

Abstract

OBJECTIVE

To assess the usefulness of magnetic resonance urography (MRU) for the visualization of nondilated renal pelvises and ureters in dogs and to compare our findings for MRU versus CT urography (CTU).

ANIMALS

9 healthy Beagles.

PROCEDURES

Dogs underwent CTU, static-fluid MRU, and excretory MRU, with ≥ 7 days between procedures. Contrast medium was administered IV during CTU and excretory MRU, whereas urine in the urinary tract was an intrinsic contrast medium for static-fluid MRU. For each procedure, furosemide (1 mg/kg, IV) was administered, and reconstructed dorsal plane images were acquired 3 minutes (n = 2) and 7 minutes (2) later. Images were scored for visualization of those structures and for image quality, diameters of renal pelvises and ureters were measured, and results were compared across imaging techniques.

RESULTS

Excretory MRU and CTU allowed good visualization of the renal pelvises and ureters, whereas static-fluid MRU provided lower visualization of the ureters. Distention of the renal pelvises and ureters was good in excretory MRU and CTU. Distention of the ureters in static-fluid MRU was insufficient compared with that in CTU and excretory MRU. Distinct artifacts were not observed in CTU and excretory MRU images. Static-fluid MRU images had several mild motion artifacts.

CLINICAL RELEVANCE

Our findings indicated that excretory MRU with furosemide administration was useful for visualizing nondilated renal pelvises and ureters of dogs in the present study. When performing MRU for the evaluation of dogs without urinary tract dilation, excretory MRU may be more suitable than static-fluid MRU.

Introduction

Urography is essential for the evaluation of the presence, severity, and cause of upper urinary tract disorders including ureteral calculi, stricture, inflammation, iatrogenic ureteral obstruction, retroperitoneal masses, retroperitoneal fluid, ectopic ureter, retrocaval ureter, and ureterocele.1,2,3,4,5,6,7 Traditionally, radiographic urography and ultrasonography have been used to evaluate the urinary tracts of veterinary patients.8,9 Recently, the use of CT urography (CTU) has increased because CTU can allow visualization of the entire urinary tract without superimposition and provide multiplanar and 3-D reconstruction techniques, such as maximum intensity projection (MIP) and volume rendering.1,2,3,4,5,10,11,12 In addition, renal perfusion13 or glomerular filtration rate14 or can be estimated by quantifying the concentration of the contrast media in renal tissue with the use of CT software.13,14 In CTU, sufficient filling of the renal pelvis and ureter with contrast media during the excretory phase is essential for the detection of small lesions and for the assessment of the patency of the ureters.15,16 However, incomplete opacification of ureters may occur because of peristalsis, resulting in missed lesions in the nonopacified regions.10,17,18

Magnetic resonance urography (MRU) can be used to evaluate the urinary tract without the risk of radiation exposure or the use of nephrotoxic iodinated contrast media. Therefore, it has evolved as an alternative or complementary imaging modality in human medicine when results of CTU are nondiagnostic or when the procedure is contraindicated, such as in children, pregnant women, and patients with renal insufficiency.2426 Static-fluid and excretory MRU are the 2 techniques mainly performed.10,2231 Static-fluid MRU uses urine in the urinary tract as an intrinsic contrast medium and acquires T2-weighted (T2W) images with heavy T2W sequences such as single-shot fast spin echo, single-shot turbo spin echo, or half-Fourier rapid acquisition single-shot turbo spin echo without administration of contrast media. The long T2 relaxation time of the fluid provides high signal intensity of the urinary tract on static-fluid MRU. Thin-slice24,2931 or thick-slice24,2831 urography images are obtained with the breath-hold technique or 3-D respiratory-triggered sequence24,26,31 can be used to acquire thin-slice images with higher spatial resolution and to create MIP or volume-rendered images. Because static-fluid MRU allows for the visualization of urine in the urinary tracts, it does not depend on renal function and can be used for the evaluation of the urinary tracts in patients with renal dysfunction. However, static-fluid MRU is not sufficient for the visualization of nondilated ureters or assessment of renal function.29,31

Excretory MRU uses contrast media, similar to CTU, and allows visualization of the urinary tract after enhancement with gadolinium-based contrast media which reduces T1 relaxation time. Thus, MRU images obtained with the use of T1-weighted (T1W) sequences can show the urinary tract with high signal intensity. Excretory MRU is most commonly performed with the use of a 3-D T1W gradient-echo sequence obtained with the breath-hold technique, given that the entire urinary tract can be scanned within a short duration.24,28,31,32 Excretory MRU is considered better for visualizing nondilated urinary tracts than is static-fluid MRU, and excretory MRU provides functional information about the urine flow. However, like CTU, it is difficult to use excretory MRU when contrast medium is not excreted because of renal dysfunction or obstruction.

In human medicine, studies have been performed for the development of a comprehensive MRU protocol to facilitate the simultaneous evaluation of the renal parenchyma, upper urinary tracts, renal vasculature, urinary bladder, and surrounding structures by combining MRU with morphological sequence and functional MRI.19,23,28,33 However, to the best of our knowledge, no study has evaluated the feasibility and usefulness of MRU in veterinary medicine, and only 1 case report34 describes the use of MRU in a dog. Therefore, the objectives of the study reported here were to assess the usefulness of static-fluid and excretory MRU for the visualization of nondilated renal pelvises and ureters in healthy dogs and to compare our findings for MRU versus CTU. We hypothesized that MRU could be used to visualize nondilated renal pelvises and ureters in dogs and that excretory MRU would provide better visualization than would static-fluid MRU.

Materials and Methods

The study protocol was approved by the Institutional Animal Care and Use Committee at Chonnam National University. The protocol for the care of dogs adhered to the Guidelines for Animal Experiments of Chonnam National University (CNU IACUC-YB-2020-31).

Animals

In this prospective, method comparison, preliminary study, purpose-bred Beagles housed at the Chonnam National University laboratory animal research facility between January 2020 and October 2020 were eligible. Inclusion criteria were that dogs had to have been younger than 5 years, weigh between 8 and 15 kg, and healthy on the basis of results from physical examination, blood pressure measurement, a CBC, urinalysis (including urine dipstick and urine specific gravity), serum biochemical analyses, thoracic and abdominal radiography, and abdominal ultrasonography. All dogs were housed individually, fed commercial dry food, and had access to tap water ad libitum.

Preparation for urography

Each dog underwent CTU, static-fluid MRU, and excretory MRU on different days with an interval of ≥ 7 days in between procedures (Figure 1). The preparation, anesthesia, and positioning of dogs were consistent for all urography procedures. A CBC, serum biochemical analyses, and urinalysis (including urine dipstick and urine specific gravity) were repeated 24 hours before each scan. For urinalysis, urine was collected by ultrasound-guided cystocentesis. For each dog before each scan, food was withheld for 12 hours, and then 250 mL of a polyethylene glycol laxative solution (Colyte; Taejoon Pharmaceutical) was administered orally to prevent the ureter from being obscured by the feces during CTU and to prevent the susceptibility artifacts in MRU. At 12 hours after oral administration of the laxative, a 20-gauge catheter was placed in the cephalic vein. Anesthesia was induced with alfaxalone (3 mg/kg, IV), an endotracheal tube was placed, and anesthesia was maintained with 1% to 3% (vaporizer settings) isoflurane delivered in oxygen (flow rate, 1 to 2 L/min). Urethral catheterization was performed, and the urinary bladder was emptied through the urethral catheter. Cefazolin sodium (20 mg/kg, IV) was administered to prevent urinary tract infection from the urinary catheter. The dog was positioned in dorsal recumbency and equipped for patient monitoring, including heart rate, respiratory rate, and oxygen saturation of hemoglobin (Spo2). Additionally, before each scan, clinical signs including urinary tract signs, change in heart rate, and rectal temperature were recorded. Intravenous fluids were not administered.

Figure 1
Figure 1

Schematic representation of procedural timelines for CT urography (CTU; A), magnetic resonance urography (MRU; B), and excretory MRU (C) performed on 9 healthy Beagles between January 2020 and October 2020. Urography images evaluated by reviewers were obtained at 3 minutes and 7 minutes after furosemide administration in each urography technique.

Citation: American Journal of Veterinary Research 83, 3; 10.2460/ajvr.21.03.0041

CTU

Each CTU was performed with a 16-row multi-detector CT scanner (SOMATOM Emotion 16; Siemens Medical Solutions Inc) with the settings of slice thickness = 1 mm, pitch = 0.8, rotation time = 600 milliseconds, tube voltage = 120 kV, and tube current = 120 mA. For each dog, after precontrast CT, iohexol (2 mL/kg, IV; Omnipaque 300; GE Healthcare) was delivered at a rate of 3 mL/s with a power injector (Optivantage DH; Mallinckrodt). Immediately after complete administration of the contrast medium, furosemide (1 mg/kg, IV) was administered and followed with a flush of sterile saline (0.9% NaCl) solution (5 mL, IV). The CTU images were acquired at 3 and 7 minutes after furosemide administration. The breath-hold technique with hyperventilation was performed during each scan. All CTU images were reconstructed in the dorsal plane with a 1-mm slice thickness, mediastinum kernel, window width of 1,500 HU, and a window level of 450 HU.

MRU

Each MRU was performed with a 3.0T whole-body scanner (Achieva; Philips Healthcare) with a 32-channel SENSE torso and cardiac coil (Philips Healthcare). After obtaining 3 orthogonal plane images with a 3-D T1W fast-field echo scan as a localizer, dorsal plane images of the urinary tract were obtained with static-fluid MRU or excretory MRU protocols (Appendix 1).

Static-fluid MRU 3-D T2W turbo spin echo sequence was performed 3 times for each dog: immediately before (baseline) and at 3 and 7 minutes after administration of furosemide (1 mg/kg, IV) immediately followed with a sterile saline (5 mL, IV) flush. All static-fluid MRU images were reconstructed with 2-mm thickness in the dorsal plane.

Excretory MRU was performed with a 3-D T1W turbo field echo sequence. After the precontrast scan, 0.1 mmol/kg of meglumine gadoterate (Dotarem; Guerbet) was administered IV at a rate of 3 mL/s with the use of a power injector (Optistar Elite; Mallinckrodt). Immediately after complete administration of the contrast medium, furosemide (1 mg/kg, IV) was administered and followed by a flush of saline solution (5 mL, IV). Excretory MRU images were then acquired 3 and 7 minutes later.

Image analysis

For each dog, images acquired at 3 and 7 minutes after administration of furosemide during each procedure were reconstructed to dorsal plane images with 2-mm slice thicknesses. Because a single image could not show both kidneys and ureters entirely, the evaluation from each kidney to the ureterovesical junction involved the use of more than 30 consecutive reconstructed dorsal plane images: 6 series (2 CTU, 2 static-fluid MRU, and 2 excretory MRU) of dorsal plane images for each dog. Additionally, images of each ureter were reconstructed in oblique planes along the path of the ureters, and MIP and volume-rendered images were obtained to show the urinary tract at a glance; however, only the dorsal plane images were used in the analysis. All MRU images were evaluated by a radiologist (JHC) and a fourth-year PhD student (SKL) using a DICOM-enabled workstation (PACS; Infinitt Healthcare). A set of 2 urography series (serial images acquired 3 and 7 minutes after administration of furosemide) obtained with each technique (CTU, static-fluid MRU, and excretory MRU) were presented to each observer in random order, and image assessment was performed by evaluating the 2 series in each set together. The observers could not be blinded to the technique because of the inherent signal characteristics of the MRU images and the differences between the CTU and MRU images.

For the analysis, reviewers considered the imaged ureters in 3 anatomic segments: proximal ureter (spanned from the renal pelvis to the level of the caudal pole of the given kidney), middle ureter (from the level of the caudal pole of the given kidney to the cranial level of the aortic bifurcation), and distal ureter (from the cranial level of the aortic bifurcation to the ureterovesical junction; Figure 2). For each imaging series, the pelvises and the 3 ureteral segments were comprehensively evaluated by 2 observers separately. Visualization of the renal pelvises and ureters and image quality in terms of artifacts were assessed qualitatively. The diameter of the pelvis on each image was measured perpendicular to the long axis of each kidney. The diameters of the ureteral segments on each image were measured at the level of the caudal pole of the ipsilateral kidney for each proximal ureter, at the midpoint of the middle ureter length, and at the caudal level of the aortic bifurcation for the distal ureter. For each set of 2 images, the larger measurement for each anatomic site of interest was used for further analysis. For analysis, a mean value of the measurements between 2 observers was used. In addition, a 4-point scale based on the opacification of the urinary tract (Appendix 2) was used to subjectively score visualization of each renal pelvis and ureteral segment, and the overall image quality was evaluated on a 4-point scale (Appendix 3) based on motion artifacts (eg, caused by respiratory motion, motion of the urinary bladder, peristalsis of the ureter) in CTU or MRU, beam hardening artifacts in CTU, and susceptibility artifact in MRU. For the scoring of the visualization and image quality of images, consensus was reached between 2 observers through discussion.

Figure 2
Figure 2

Representative postcontrast dorsal plane reconstructed maximum intensity projection (MIP) CTU of 1 of the 9 Beagles described in Figure 1 showing the 3 sections considered by reviewers for each ureter: proximal ureter (A), defined as the segment from the renal pelvis to the caudal level of the given kidney; middle ureter (B), defined as the segment from the caudal level of the given kidney to the cranial level of the aortic bifurcation; and distal ureter (C), defined as the segment from the aortic bifurcation to the ureterovesical junction. The dog’s right side is toward the left of the image, and the right distal ureter is obscured by the urinary bladder because of the MIP reconstruction used to obtain the image. The image is displayed in a mediastinum kernel, with a window width of 1,500 HU, window level of 450 HU, and slice thickness of 1 mm.

Citation: American Journal of Veterinary Research 83, 3; 10.2460/ajvr.21.03.0041

Statistical analysis

Data were reported as mean and SD. Statistical analyses were performed by 1 author (SKL) using SPSS Statistics version 25 (IBM Corp). The Kolmogorov-Smirnov test was performed to determine the normality of the data. The comparison of results among the 3 different urography techniques was performed with the use of 1-way repeated-measures ANOVA with Bonferroni correction for normally distributed data or Friedman test with Wilcoxon signed-rank test for nonnormal distributed data. The level of significance for the tests was set at P < 0.05.

Results

Animals

Nine purpose-bred Beagles (4 sexually intact males and 5 sexually intact females) were included. The sample size was based on convenience sampling of dogs available at the Chonnam National University laboratory animal research facility that met the inclusion criteria during the period from January 2020 to October 2020. The dogs’ median age and weight were 2 years (range, 1 to 3 years) and 10.0 kg (range, 8.7 to 12.6 kg). All 9 dogs underwent CTU and MRU successfully, without any complications or abnormal changes in results for CBC, serum biochemical analyses, or urinalyses.

Image analysis

On CTU, the renal pelvises and most of the ureteral segments were clearly visualized in all dogs (Figure 3). Although incomplete opacification of some ureteral segments was observed due to peristalsis, filling of the ureteral lumen could be confirmed by comprehensive assessment of the respective paired image of each set.

Figure 3
Figure 3

Representative postcontrast reconstructed dorsal oblique plane (A and E) and reconstructed dorsal (B and F), MIP (C and G), and volume-rendered (D and H) CTU images of 1 of the 9 dogs described in Figure 1 obtained at 3 minutes (A through D) and 7 minutes (E through H) after furosemide administration. Only reconstructed dorsal plane images (B and F) were used in analysis; the other images were generated to show each ureter along its path (A and E) and the urinary tract at a glance. The renal pelvises and most of the lengths of the ureters are clearly visualized; however, parts of the ureters have incomplete opacification, consistent with peristalsis. The dog’s right side is toward the left in all images.

Citation: American Journal of Veterinary Research 83, 3; 10.2460/ajvr.21.03.0041

On static-fluid MRU before furosemide administration, neither the renal pelvises nor ureters were visualized. After furosemide administration, the renal pelvis and ureters were visualized as bright signals; however, most of the ureters were indistinct and blurred (Figure 4).

Figure 4
Figure 4

Representative 3-D T2-weighted static-fluid MRU images of 1 of the 9 dogs described in Figure 1 obtained at 3 minutes (A through D) and 7 minutes (E through H) after furosemide administration and displayed in a reconstructed dorsal oblique plane (A and E) and reconstructed dorsal (B and F; used in analysis), MIP (C and G), and volume-rendered (D and H) images. The left ureter is indistinct and blurred; the right ureter is not evident at 3 minutes after furosemide administration, and only the proximal portion of it is evident at 7 minutes after furosemide administration.

Citation: American Journal of Veterinary Research 83, 3; 10.2460/ajvr.21.03.0041

On excretory MRU, only the proximal ureter could be identified, albeit indistinctly, in some precontrast images. After administration of the contrast medium and then furosemide, consistent and clear visualization of the renal pelvises and ureters was achieved; however, some ureteral segments were incompletely opacified, likely due to peristalsis (Figure 5).

Figure 5
Figure 5

Representative 3-D T1-weighted excretory MRU images of 1 of the 9 dogs described in Figure 1 obtained at 3 minutes (A through D) and 7 minutes (E through H) after furosemide administration and displayed in a reconstructed dorsal oblique plane (A and E) and reconstructed dorsal (B and F; used in analysis), MIP (C and G), and volume-rendered (D and H) images. The renal pelvises and ureters are clearly visualized.

Citation: American Journal of Veterinary Research 83, 3; 10.2460/ajvr.21.03.0041

The mean ± SD visualization scores for the renal pelvis and the proximal, middle, and distal ureteral segments were compiled (Table 1). The mean visualization scores for the ureteral segments were significantly (P < 0.05) lower in static-fluid MRU images than in CTU or excretory MRU images. The mean visualization score of the renal pelvis in static-fluid MRU was lower than that in CTU or excretory MRU; however, the difference was not statistically significant. There was no substantial difference in the mean visualization score for excretory MRU versus CTU images.

Table 1

Mean ± SD visualization scores for the renal pelvises and ureteral segments in 9 healthy purpose-bred Beagles that underwent CT urography (CTU), static-fluid magnetic resonance urography (MRU), and excretory MRU between January and October 2020, stratified by the imaging technique.

Site CTU* Static-fluid MRU* Excretory MRU* P value
Renal pelvis 3.00 ± 0.00 2.44 ± 0.68 2.72 ± 0.42 0.066
Proximal ureter 2.83 ± 0.33b 2.00 ± 0.41a 2.72 ± 0.42b 0.005
Middle ureter 2.44 ± 0.44b 1.28 ± 0.82a 2.83 ± 0.24b 0.001
Distal ureter 2.28 ± 0.58b 1.22 ± 0.11a 2.56 ± 0.55b 0.021

Data are presented as mean ± SD.

Within a row, values with different superscript letters differ significantly (P < 0.05)

The mean diameters of the proximal, middle, and distal ureteral segments were significantly (P < 0.05) smaller in static-fluid MRU images than in CTU or excretory MRU images (Table 2). The mean diameter of the renal pelvis was larger in CTU and excretory MRU images, compared with that in static-fluid MRU images; however, the difference was not significant. There was no substantial difference in the mean diameter of the renal pelvis or any of the ureteral segments for excretory MRU versus CTU images.

Table 2

Comparisons of the mean ± SD diameter (mm) of the renal pelvis and ureter segment measurements obtained with CTU, static-fluid MRU, or excretory MRU.

Site CTU* Static-fluid MRU* Excretory MRU* P value
Renal pelvis (mm) 3.20 ± 0.58 2.53 ± 0.59 2.90 ± 0.59 0.080
Proximal ureter (mm) 2.25 ± 0.38b 1.84 ± 0.20a 2.34 ± 0.16b 0.006
Middle ureter 2.18 ± 0.35b 1.33 ± 0.73a 2.32 ± 0.18b 0.001
Distal ureter 2.13 ± 0.35b 1.37 ± 0.85a 2.31 ± 0.15b 0.011

SeeTable 1 for the key.

All CTU images received image quality scores of 3, and none had motion or beam hardening artifacts. All static-fluid MRU images received 2 points in image quality due to motion artifacts. Motion artifacts were caused by the distention of the urinary bladder in all dogs, and peristalsis-related artifacts were observed in images of 5 of the 9 dogs (Figure 6). However, these artifacts were minor and not sufficient to degrade the visualization of the ureters. Respiratory motion artifact or susceptibility artifact was not observed. All excretory MRU images received image quality scores of 3, and none had any motion or susceptibility artifacts.

Figure 6
Figure 6

Representative reconstructed 3-D T2-weighted dorsal plane static-fluid MRU images of 2 of the 9 dogs described in Figure 1 obtained 7 minutes after administration of furosemide. Ghosting artifacts are observed due to urinary bladder distension (arrows; A) or ureteral peristalsis (arrowheads; B).

Citation: American Journal of Veterinary Research 83, 3; 10.2460/ajvr.21.03.0041

Discussion

In the present study, the usefulness of static-fluid MRU and excretory MRU for the visualization of the renal pelvises and ureters in dogs was evaluated by comparing results for MRU versus CTU in healthy dogs. Excretory MRU provided sufficient visualization and distension of nondilated renal pelvises and ureters and yielded results similar to those of CTU. However, the visualization and distension of the renal pelvises and ureters were less for static-fluid MRU, compared with CTU or excretory MRU. These findings supported our hypothesis that MRU could be used to visualize nondilated renal pelvises and ureters in dogs and that excretory MRU would provide better visualization than would static-fluid MRU.

Excretory MRU performed with a single breath-hold yielded clear images of the renal pelvises and ureters in dogs of the present study. Similarly, in human patients with a high risk of urinary tract malignancy or hydronephrosis, MRU yielded images with visualization scores and ureteral distention similar to those of CTU images and even a higher visualization score in the distal ureteral segment.19 In our study, the visualization scores of the middle and distal ureteral segments were slightly higher in images obtained with excretory MRU versus CTU; however, the difference was not statistically meaningful.

In excretory MRU images, the urinary tract could be observed more consistently with larger renal pelvises and ureters, compared with those in static-fluid MRU images, despite the fact that both techniques used the same dose of furosemide (1 mL/kg, IV), volume of saline flush (5 mL, IV), and time points for obtaining urographic images. Although contrast medium was administered for excretory MRU, the dose administered to each dog was very small (0.2 mL/kg, IV). Similarly, in an aforementioned study28 of people with nondilated urinary tracts, the same dose of furosemide was administered for excretory versus static-fluid MRU, and although visualization of the imaged ureters was similar with both techniques excretory MRU images showed a higher degree of urinary tract distention than did static-fluid MRU images. This finding may relate to the diuretic effect of the contrast agent itself. Another possibility is that the ureteral diameter could be overestimated in excretory MRU due to partial volume effects.

Excretory MRU is used as an essential protocol for urinary tract imaging in humans because it allows superior visualization and provides functional assessment of the urinary tract, whereas static-fluid MRU is an optional, supplementary imaging technique.23,24,26,28 In particular, excretory MRU is indicated for detecting and localizing communication between the renal collecting system and a cystic structure in people with nondilated ureters.24 However, excretory MRU depends on the excretion of the contrast media; thus, it is difficult to use in patients with severe renal dysfunction, and imaging can be delayed in patients with urinary tract obstruction.24 Although, to our knowledge, nephrotoxicity attributed to gadolinium-based contrast media has not been reported in veterinary medicine, it is a concern in human patients with chronic kidney disease.35 In those patients, static-fluid MRU can be used because the imaging technique is independent of renal function.24,27 Additionally, static-fluid MRU is more time-efficient than excretory urography, given that there is no need of delayed imaging for excretion of contrast media. Static-fluid MRU has good sensitivity for detecting cystic lesions, edema, and small volumes of peritoneal fluid.21,28,31 In human patients with obstructive urinary tract disease, static-fluid MRU has similar accuracy to conventional radiographic urography in detecting urinary tract obstruction and is superior in the determining the location and cause of obstruction.36,37 In veterinary medicine, static-fluid MRU yielded clear visualization of a dilated renal pelvis and ureter in a dog with retrocaval ureter.34 However, in the present study, static-fluid MRU provided unsatisfactory visualization and distention of nondilated ureters in dogs even after furosemide administration, which was a finding consistent with previous studies.23,29 Although a recent study28 in human medicine shows that static-fluid MRU with furosemide administration provided similar visualization of nondilated urinary tracts as did excretory urography with furosemide administration, it may be difficult to expect such results in dogs, which have smaller diameter ureters than humans.

Another limitation of static-fluid MRU is that extra-urinary fluids, such as gastric or intestinal contents, exhibit high signal intensity on MRI and may obscure the ureter, especially in a thick-slice image.10,28,31 In our study, small volumes of gastric or intestinal contents exhibited high signal intensity; however, this did not affect the evaluation of the ureters, possibly because of the small slice thickness used and because we withheld food from and administered a laxative to the dogs of the present report before they underwent urography. Also, in the present study, static-fluid MRU images had mild motion artifacts due to distention of the urinary bladder or ureteral peristalsis; however, this did not affect the evaluation of the urinary tracts. The presence of artifacts was possibly attributable to the long scan duration of the 3-D T2 turbo spin echo sequence and respiratory triggering used rather than the intrinsic limitation of static-fluid MRU.18 Scan duration could be shortened, and consequently reduce imaging artifacts, with the use of 2-D single-shot sequence, thick-slice imaging, and a breath-hold technique.18,19,24,28 Although 3-D image acquisition had mild motion artifacts in images of the present study, 3-D image acquisition in very thin slice thicknesses and with high spatial resolution and can provide various useful volumetric reconstructions, such as multiplanar reformation, MIP, and volume-rendered images.38

Although not evaluated, there was no marked difference in scan duration between MRU and CTU in the present study. Therefore, MRU did not have the disadvantage of a longer duration of anesthesia, compared with that of CTU. This finding may not translate to clinical settings because we evaluated only the visualization of the renal pelvises and ureters. For instance, in patients with urinary disorders, CTU can be used to simultaneously evaluate the ureters, kidneys, and adjacent tissues in 1 procedure, whereas MRU requires obtaining additional sequences for evaluating kidneys and adjacent tissues, which would require longer durations of anesthesia for patients than would CTU.

In humans, MRU is generally used as a comprehensive protocol in combination with other sequences (eg, T1W and T2W MRI and various functional imaging procedures), and these combined protocols may provide high contrast among soft tissues and functional information.23,24,30,31 To our knowledge, there have been no studies on comprehensive MRU protocols in veterinary medicine, and although our findings indicated that visualization of nondilated ureters and renal pelvises was similarly superior for excretory MRU and CTU, compared with static-fluid MRU, the value of CTU or MRU in diagnosing urinary disease should not be based solely on urinary tract visualization during urography.

An appropriate dose of contrast media in excretory MRU is essential to provide sufficient enhancement with contrast resolution and adequate dilation of the urinary tract.24,27 A high dose of a contrast medium may cause signal loss due to the susceptibility effect when it is concentrated in the renal collecting system, and a low dose of a contrast medium may reduce contrast resolution and impair the dilation of the collecting system. In humans, generally, 0.05 to 0.1 mmol/kg of gadolinium-based contrast medium is used, with image acquisition starting at 5 minutes after administration of contrast medium.19,20,22,25,28,32 In the present study, a dose of 0.1 mmol/kg was used, consistent with a previous study39 of dynamic MRI nephrography in dogs, and we obtained images at 3 minutes after administration of contrast medium on the basis that opacification of ureter reaches its peak at 3 minutes and persists for approximately 1 hour in dogs.1,2,17,4042 Our second set of images were acquired at 7 minutes after administration of contrast medium, because the duration of static-fluid MRU in the present study exceeded 3 minutes, and we harmonized onsets of imaging across the 3 techniques used. The dose of the contrast medium was considered suitable for clear visualization of the urinary tract without the susceptibility effect associated with the contrast medium.

Furosemide was administered to dilate the ureters and renal pelvises in dogs of the present study. Diuretic effects of furosemide increase urine production, which increases urine volume, which in turn promotes urinary tract distention, and increased urine flow leads to rapid and uniform distribution of the contrast medium in the urinary tract.41,43 Moreover, dilution of the contrast medium by water retention after furosemide administration minimizes beam hardening artifact in CTU and T2* decay in excretory MRU.43

There were limitations in the present study. First, the image evaluation was mainly subjective. However, because of the difference between the properties of CTU and MRU, other quantitative evaluations such as the degree of contrast enhancement were difficult to perform. To compensate for the limitations of subjective evaluation, images were analyzed by the 2 observers and consensus was reached for the scoring of the visualization and image quality of images. Second, the present study focused only on the visualization of nondilated renal pelvises and ureters in healthy dogs. Therefore, further studies are needed to evaluate the usefulness of MRU in dogs with urinary tract diseases and dilated urinary tracts. Third, we did not evaluate the visualization of the ureterovesical junction. Because all dogs in the present study were imaged in dorsal recumbency, the images acquired were not suitable for evaluating ureterovesical junction because of the accumulation of contrast media on the dorsal aspect of the urinary bladder and partial volume artifact. Further studies including analysis of transverse plane images obtained from dogs with ventral recumbency may be necessary to evaluate the feasibility of MRU for the visualization of the ureterovesical junction.

In conclusion, excretory MRU with furosemide administration was feasible for the visualization of nondilated renal pelvises and ureters in dogs, and the quality of acquired images was similar to that provided by CTU. Compared with findings for CTU or excretory MRU, static-fluid MRU images had lower scores for visualization of the renal pelvises and ureters, even after administration of furosemide administration. Therefore, in dogs without renal pelvic or ureteral dilation, excretory MRU may be more suitable than static-fluid MRU for visualization of those structures. The results of the present study could be used as basic data when considering or performing MRU as a supplementary technique to conventional radiographic urography for the evaluation of the urinary system.

Acknowledgments

This study was supported by the Animal Medical Institute of Chonnam National University and the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, ICT, and Future Planning (NRF-2018R1A2B6006775).

The authors declare that there were no conflicts of interest.

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Appendix 1

Detailed imaging parameters of static-fluid magnetic resonance urography (MRU) and excretory MRU performed on 9 healthy Beagles between January 2020 and October 2020.

Parameters Static-fluid MRU Excretory MRU
Sequence 3-D T2W Turbo spin echo 3-D T1W Turbo field echo
TR (ms) 1,570 3.10
TE (ms) 850 1.43
Flip angle (°) 90 10
Matrix size (mm) 300 X 262 268 X 266
Fat suppression Yes Yes
Parallel acceleration factor 2 X 1 2 X 1.5
Motion control Respiratory triggering Breath-hold
FOV (mm) 300 X 300 X 80 400 X 400 X 70
Slice thickness (mm) 2 2
Scan duration (min) 3.65 0.30

FOV = Field of view. T1W = T1-weighted. T2W = T2-weighted. TE = Echo time. TR = Repetition time.

Appendix 2

Visualization scores and corresponding criteria used for evaluation of renal pelvises and ureters on CT urography (CTU) and MRU images of the dogs described in Appendix 1.

Site Score Criteria
Renal pelvis 0 Not visualized as bright
1 Indistinctly visualized as bright
2 Visualized as bright, but the border of the renal pelvis is slightly blurred
3 Visualized as bright with the border of the renal pelvis clearly visible
Ureter 0 Not visualized
1 Visualized as bright for < 50% of the ureteral segment length
2 Visualized as bright for 50% to 99% of the ureteral segment length
3 Visualized as bright for the entire length of the ureteral segment

Appendix 3

Image quality scores and corresponding criteria used for evaluation of the CTU and MRU images of the dogs described in Appendix 1.

Score Criteria
0 Hard to interpret images due to severe artifacts
1 Impeded image quality with distinct artifacts
2 Fairly good images with minor artifacts
3 Optimal urography images with no interference

Contributor Notes

Corresponding author: Dr. Choi (imsono@snu.ac.kr)