Prostatic neoplasia is a debilitating disease in dogs. Early detection of prostatic neoplasia is uncommon, and there is often local extension of tumor into the urinary tract or adjacent organs.1 Metastasis is also common, which contributes to a guarded prognosis.1
Imaging of tumors in the lower urinary tract of canine patients is most commonly performed with TAUS2,3 owing to the minimally invasive nature of this technique, relative ease of accessibility to the equipment, and lack of requirement for anesthesia of patients, which is often necessary to perform CT and MRI. Transabdominal ultrasonography is an insensitive diagnostic tool in the assessment of bladder tumor size, especially when 2-D ultrasonography is used.4,5 In a recent study,6 CT was used to calculate volume of bladder tumors, and results indicated that the calculated volume was dependent on the technique used for measurement, which again confirmed that variability exists in the assessment of tumor response to treatment.6
Magnetic resonance imaging is an excellent imaging modality for the assessment of neoplasia in the lower urinary tract of human patients.7–10 Although MRI may be considered the criterion-referenced standard imaging modality for assessment of the size and location of tumors in the lower urinary tract, clinical application of MRI in veterinary medicine is limited because of expense and the need for veterinary patients to be anesthetized. For these reasons, evaluation of additional imaging modalities is justified.
Transrectal ultrasonography is commonly used as part of the diagnostic and treatment plan for men with suspected prostatic disease.11–13 Transrectal ultrasonography has several benefits, including placement of a transducer in the rectum adjacent to the organs of interest and the ability to evaluate the abdominal and intrapelvic portions of the urethra without interference from the pelvic bones.11,14 Although TRUS can be used to perform a general ultrasonographic assessment of the prostate gland and adjacent structures, it is more often used to guide transrectal procedures (eg, biopsy and injection of the prostate gland).11 Additionally, newer technologies can be used to evaluate the fusion of images obtained by use of TRUS and other imaging modalities.15,16
The objectives of the study reported here were to describe the use of TRUS in the assessment of prostatic tumors in dogs, evaluate prostatic tumors by the use of various diagnostic imaging modalities (TAUS, TRUS, fluoroscopy, and MRI), and compare measurements obtained with TAUS, TRUS, and fluoroscopy with measurements obtained with MRI. Our hypothesis was that TRUS would have superior agreement with MRI for measurement of size and identification of the precise location of prostatic tumors, compared with agreement of TAUS and fluoroscopy with MRI.
Materials and Methods
Dogs
Client-owned dogs with prostatic carcinoma (identified via cytologic or histologic examination) were enrolled in the study. Owner consent was obtained for inclusion of each dog, and an animal use committee approved the study.
Experimental procedures
Food was withheld from dogs for 24 hours before imaging procedures were performed. Dogs were anesthetized by use of protocols established by the clinical anesthesiology service. Dogs were placed in right lateral recumbency, and the prepuce was clipped and prepared with an aseptic technique. A urethral cathetera was introduced into the penis and passed through the urethra and into the bladder. All urine was drained from the bladder, and sterile saline (0.9% NaCl) solution (5 mL/kg) was infused into the bladder to allow for consistent measurements during MRI, TAUS, and TRUS; other procedures were used during fluoroscopy.
All 4 imaging procedures were performed during the same anesthetic episode. Dogs were monitored after anesthesia by recording heart rate and body temperature during recovery. None of the dogs had any anesthetic complications or complications secondary to the imaging procedures.
MRI
Imaging with MRIb was performed, and T1-weighted fast spin echo and T2 fast spin echo sequences were obtained in the sagittal, transverse, and dorsal planes. A dose of contrast medium (gadolinium-diethylenetriamine pentaacetic acidc; 0.2 mL/kg) was administered IV, and the T1-weighted sequences were repeated. Tumor length and height were measured in a sagittal plane; additionally, tumor height and width were measured in a transverse plane. Regional lymph nodes (medial iliac and hypogastric lymph nodes) were assessed to detect lymphadenomegaly, which was considered a lymph node > 1 cm in length.
TAUS
The TAUSd examinations were performed with a 5− to 8-MHz transducer. Length of a prostatic mass was measured by use of a sagittal approach during TAUS. One veterinary radiologist (EGJ) obtained measurements while viewing the prostate gland in a sagittal plane (long axis of the gland). Length of the prostatic mass was defined as the maximum distance in a cranial-to-caudal direction (Figure 1). Additionally, tumor height was measured in a sagittal plane, and tumor height and width were measured in a transverse plane. Distance between the tumor and the UVJs was measured in a parasagittal plane (Figure 2). Extension of the tumor into the urinary bladder and urethral penetration (identification of abnormal tissue within the urethral lumen) were also assessed in a parasagittal plane. Finally, the regional lymph nodes (medial iliac and hypogastric lymph nodes) were assessed to detect lymphadenomegaly. All images obtained throughout the TAUS procedure were recorded.
Images obtained in the sagittal plane with TAUS (A), TRUS (B and C), MRI (D), and fluoroscopy (E) of an 11-year-old West Highland White Terrier with a prostate tumor. The longest unidimensional measurement was used for comparisons among images A through C. In panels A, B, and C, dots on the dotted lines between the calipers (plus signs) are at intervals of 1 mm.
Citation: American Journal of Veterinary Research 80, 11; 10.2460/ajvr.80.11.1012
Images obtained in the sagittal plane by use of TAUS (A) and TRUS (B and C) of a 10-year-old Border Collie. Notice the location of the UVJ (arrow) in panels A and B. In panel C, the tumor (area within dashed line) extends to the level of the UVJ (region between plus signs).
Citation: American Journal of Veterinary Research 80, 11; 10.2460/ajvr.80.11.1012
TRUS
The TRUS examination was performed by the same veterinary radiologist immediately after completion of TAUS. The TRUSe was performed with a 7-MHz rigid, endocavitary uniplanar (sagittal) transducer. Material was digitally evacuated from the rectum, a syringe was introduced into the rectum, and the rectum was filled with ultrasound gel.f The TRUS transducer was then inserted into the rectum and passed cranially until the bladder was visually identified. Tumor length and height were measured in a sagittal plane (Figure 1). Additionally, distance between the tumor and the UVJs was measured (Figure 2). Extension of the tumor into the bladder and urethral penetration were assessed. Finally, the regional lymph nodes (medial iliac and hypogastric lymph nodes) were assessed to detect lymphadenomegaly. All images for TRUS obtained throughout the procedure were recorded.
Fluoroscopy
For fluoroscopy,g dogs were placed in lateral recumbency, similar to the position used for urethral stent placement.17–19 A marker catheterh was introduced into the rectum to allow for calibration during measurements. The urinary bladder was filled by injection of a 50:50 mixture of saline solution and positive contrast mediumi through the previously placed urethral catheter. Volume of the mixture injected was not standardized; the bladder was filled until the trigone was clearly visible and the bladder was distended. A 0.035-inch, hydrophilic guidewirej was introduced via the urethral catheter, and the urethral catheter was removed. A 4F angled catheterk was introduced into the bladder over the guidewire, and the guidewire then was removed. Positive contrast cystourethrography was performed by slowly extracting the angled catheter while injecting the 50:50 mixture of saline solution and positive contrast medium. All images for the fluoroscopic procedure were recorded.
Image evaluation
Maximum length, height, and width of the tumor were determined by use of TAUS. Because the TRUS transducer was uniplanar (sagittal), only the length and height of the prostatic tumor could be measured. Measurements were determined by placing calipers at the edges of the region of interest. The ultrasound machine then calculated the distance between the 2 calipers and registered a numeric value. In some dogs with large tumors, it was necessary to splice 2 images together to determine tumor length. When splicing was required, the location where the measurement ended in one image was marked to enable identification of the exact same location of the tumor in the adjacent image, which allowed for accurate assessment of the length across 2 images.
For TAUS and TRUS, a UVJ was identified as visible jets of urine exiting from the ureter into the urinary bladder. Distance from the UVJs to the cranial aspect of the tumor was recorded for comparison with the distance on MRI images. Location of the UVJs on MRI images was identified by tracing the ureters to the site of insertion in the bladder.
All images of the entire fluoroscopic procedure were evaluated to identify the images that most effectively revealed the length of urethral obstruction. Length of the tumor and length of the suspected obstruction were measured to allow for comparison with results for images obtained with MRI, TAUS, and TRUS. Length of the tumor was determined by identifying the region of the prostate gland that had uptake of contrast medium after contrast cystourethrography was performed. Length of obstruction was considered the region of the urethra in which the contrast medium was irregular or suspected to be attenuated by the tumor. Additionally, distance from the tumor to the UVJs was measured when possible. The UVJs were identified via fluoroscopy (when possible) by tracing the ureters to the site of insertion in the bladder.
The MRI images were evaluated, and measurements were determined on a workstationl with viewing softwarem by 1 author, who also obtained measurements for TAUS and TRUS. The author who performed the MRI measurements was not aware of the TAUS and TRUS results, and images were randomly ordered before review. Maximum tumor length was determined in the sagittal plane, and maximum tumor height and width were determined in the transverse plane by use of information provided on both precontrast and postcontrast imaging sequences.
Statistical analysis
Absolute agreement between results of MRI, fluoroscopy, TAUS, and TRUS was estimated for continuous variables by use of intraclass correlation coefficients and 95% confidence intervals on the basis of 2-way random-effects models. Raw absolute agreement between results of MRI, TAUS, and TRUS was reported for dichotomous variables, and the McNemar nonparametric test for marginal homogeneity was used to test the hypothesis of equality among ratings. Analyses were performed with computer software,n and values of P < 0.05 were considered significant. Intraclass correlation coefficients were interpreted in accordance with a previously described method20 whereby values < 0.50 indicated poor agreement, values between 0.50 and 0.74 indicated moderate agreement, values between 0.75 and 0.90 indicated good agreement, and values > 0.90 indicated excellent agreement.
Results
Ten dogs were enrolled in the study. Dog breeds comprised 3 Labrador Retrievers, 1 Belgian Malinois, 1 Border Collie, 1 Dachshund, 1 Leonberger, 1 Rottweiler, 1 Welsh Corgi, and 1 West Highland White Terrier. All dogs were castrated. Median body weight was 26.3 kg (range, 9.4 to 49.5 kg).
The TRUS transducer was successfully positioned within the rectum of all dogs, and visualization of the bladder, urethra, and lymph nodes was considered excellent. Injection of ultrasound gel into the rectum was considered by the authors to be essential for assessment assessment of the prostate gland. No complications were encountered during or after TRUS.
Median length of the prostatic tumors as measured in a sagittal plane with MRI was 58.5 mm (range, 10 to 88 mm), and median height was 45 mm (range, 11 to 45 mm). Median height of the prostatic tumors measured in a transverse plane with MRI was 33 mm (range, 13 to 44 mm), and median width was 37 mm (range, 13 to 47 mm). Median distance from the left UVJ to the tumor as measured with MRI was 8.5 mm (range, 0 to 20 mm), and median distance from the right UVJ to the tumor as measured with MRI was 7.5 mm (range, 0 to 18 mm). Of the 20 UVJs (2 UVJs/dog) evaluated with MRI, the tumor was located at the level of the UVJ (distance, 0 mm) for 8.
Median length of the prostatic tumor measured in a sagittal plane with TAUS was 55 mm (range, 13 to 71 mm), and median height was 37 mm (range, 11 to 48 mm). Median height of the prostatic tumor measured in a transverse plane with TAUS was 34 mm (range, 8 to 46 mm), and median width was 39 mm (range, 7 to 41 mm). Median distance from the left UVJ to the tumor as measured with TAUS was 7.1 mm (range, 0 to 27.4 mm), and median distance from the right UVJ to the tumor as measured with TAUS was 8.9 mm (range, 0 to 27.4 mm). Of the 20 UVJs evaluated with TAUS, the tumor was located at the level of the UVJ (distance, 0 mm) for 7.
Median length of the prostatic tumor measured in a sagittal plane with TRUS was 69.1 mm (range, 9.9 to 102.2 mm), and median height was 26.7 mm (range, 10 to 40 mm). Median distance from the left UVJ to the tumor as measured with TRUS was 0 mm (range, 0 to 17.3 mm), and median distance from the right UVJ to the tumor as measured with TRUS was 2.4 mm (range, 0 to 27.4 mm). Of the 20 UVJs evaluated with TRUS, the tumor was located at the level of the UVJ (distance, 0 mm) for 11. There was a significant moderate to good agreement among TAUS, TRUS, and MRI for tumor length and height (Table 1).
Comparisons between imaging modalities for measurements of prostatic tumors and distance from the tumor to the UVJs in 10 dogs.
| 95% CI | |||||
|---|---|---|---|---|---|
| Measurement | Comparison | ICC | Lower | Upper | P value* |
| Length (sagittal plane) | MRI vs TAUS | 0.674 | 0.165 | 0.906 | 0.010 |
| MRI vs TRUS | 0.596 | 0.049 | 0.878 | 0.021 | |
| MRI vs fluoroscopy | 0.615 | 0.065 | 0.886 | 0.020 | |
| Height (sagittal plane) | MRI vs TAUS | 0.836 | 0.483 | 0.956 | < 0.001 |
| MRI vs TRUS | 0.863 | −0.040 | 0.976 | < 0.001 | |
| Height (transverse plane) | MRI vs TAUS | 0.820 | 0.419 | 0.952 | 0.001 |
| Width (transverse plane) | MRI vs TAUS | 0.804 | 0.376 | 0.948 | 0.002 |
| Tumor to left UVJ† | MRI vs TAUS | 0.79 | 1.233 | 0.955 | 0.008 |
| MRI vs TRUS | 0 | −0.604 | 0.647 | 0.509 | |
| Tumor to right UVJ† | MRI vs TAUS | 0.714 | 0.124 | 0.924 | 0.016 |
| MRI vs TRUS | 0.062 | −0.790 | 0.722 | 0.444 | |
Values were considered significant at P < 0.05.
Represents results for only 8 dogs.
CI = Confidence interval. ICC = Intraclass correlation coefficient.
Positive contrast cystourethrograms were obtained with fluoroscopy. Median tumor length was 63 mm (range, 50 to 87 mm), but median length of the region of suspected urethral obstruction was 49.5 mm (range, 13 to 65 mm). The ureters could be visually identified in 6 of 10 fluoroscopic procedures; both ureters could be identified in 5 procedures, and only the left ureter could be identified in 1 procedure. Examination of these 11 ureters revealed that the ureters appeared to be entering the tumor for 6 ureters (distance, 0 mm), whereas the measured median distance from the ureter to the tumor was 19 mm (range, 1 to 21 mm) for the other 5 ureters.
Penetration of tumor into the urethra was identified in all 10 dogs on the basis of MRI, 1 of 10 dogs on the basis of TAUS, and 7 of 10 dogs on the basis of TRUS; absolute agreement was 10% between MRI and TAUS and 70% between MRI and TRUS. Assessments of urethral penetration performed with MRI differed significantly from those performed with TAUS (P = 0.003) but not from those performed with TRUS (P = 0.250).
Extension of tumor into the urinary bladder was identified in 8 of 10 dogs on the basis of MRI, 2 of 10 dogs on the basis of TAUS, and 3 of 10 dogs on the basis of TRUS; absolute agreement was 40% between MRI and TAUS and 50% between MRI and TRUS. Assessments of bladder extension performed with MRI differed significantly from those performed with TAUS (P = 0.03) but not from those performed with TRUS (P = 0.063).
Local lymphadenomegaly (medial iliac and hypogastric lymph nodes) was identified in 4 of 10 dogs on the basis of MRI, 2 of 10 dogs on the basis of TAUS, and 3 of 10 dogs on the basis of TRUS; absolute agreement was 60% between MRI and TAUS and 70% between MRI and TRUS. Assessments of lymphadenomegaly performed with MRI did not differ significantly from those performed with TAUS (P = 0.625) or TRUS (P = 1.000). None of the lymph nodes were cytologically or histologically evaluated to determine the cause of lymphadenomegaly.
Discussion
Transrectal ultrasonography was successfully performed in this cohort of dogs with prostatic neoplasia, and no intraprocedural or postprocedural complications were encountered. There was significant moderate to good agreement among TAUS, TRUS, and MRI for tumor length and height measurements for the dogs of the study reported here. The TRUS assessments of urethral penetration, extension of tumor into the bladder, and lymph node status did not differ significantly from those made with MRI, whereas assessments made with TAUS lacked agreement with those made with MRI.
Reports on the use of TRUS in veterinary patients with spontaneously developing neoplasia are lacking, but use of TRUS in the assessment of prostate glands of healthy dogs17–19 or dogs with experimentally induced diseases of the prostate gland20–23 has been described. The potential uses of TRUS in veterinary patients need further elucidation. Similar to the use in humans, TRUS could be used to perform ultrasonographic evaluations of the lower urinary tract (including the prostate gland) and adjacent organs. Additionally, methods currently used to obtain prostatic biopsy specimens or perform prostatic-specific procedures require a TAUS− or CT-guided approach or an open surgical procedure. Similar to the use of TRUS in humans, TRUS could be considered as an alternative option for some of these procedures.
Transrectal ultrasonography may also be of value for other applications in companion animals, including assessment of tumor response to treatment, evaluation of the lower urinary tract for recurrence or progression of disease after treatment, or evaluation as an adjunctive imaging modality for the performance of minimally invasive surgical or interventional radiology procedures. Transrectal ultrasonography may hold an advantage over other modalities (eg, MRI) in veterinary patients because it requires that animals only be sedated for the procedure; this would allow for tumor assessment to be performed more regularly to help guide future treatments (eg, chemotherapy or radiation therapy) as well as decrease costs to owners. Use of traditional treatments (eg, IV administration of chemotherapeutics) and newer interventional radiology techniques (eg, intra-arterial chemotherapy and prostatic embolization) requires that the available armamentarium of imaging tools needs to expand to allow better assessment of responses.
Growth of prostatic tumors is commonly associated with obstruction of the urethra with subsequent urine retention. Urethral stents have emerged as an effective treatment option for this condition,24–26 and dogs can be treated and discharged to their owners, often within 24 hours. Additionally, patient quality of life can be dramatically improved. The placement of urethral stents is generally performed with digital radiographic or fluoroscopic guidance. A major challenge to urethral stent placement is accurate assessment of tumor location; such assessments must be made accurately to allow precise placement of a stent and ensure urethral patency. Placing a stent in an incorrect location may lead to continued obstruction with no clinical improvement. In the study reported here, there was moderate agreement between fluoroscopy and MRI for evaluation of tumor length. However, although maximum length of prostatic tumors may be determined, it is not always the case that the entire tumor is causing obstruction of the urethra, and it is the area of the obstruction that must be included in the stented region of the urethra. The use of TRUS should be evaluated in future studies to determine whether this modality is a useful adjunctive imaging modality to fluoroscopy during stent placement or could be used alone to guide placement of urethral stents.
Transrectal ultrasonography may be a diagnostic option to consider as an additional aid when planning open surgical treatments. Total prostatectomy has been described as a treatment for prostatic neoplasia in dogs.27,28 It is important that clinicians have a full understanding of tumor location to aid in both case selection and surgical planning with this procedure, especially when the tumor extends into the urethra and bladder. In the present study, there was no significant difference between TRUS and MRI for the determination of urethral penetration and tumor extension into the bladder. In contrast, TAUS differed significantly from MRI for the determination of tumor extension into the bladder and urethral penetration. It is likely that TAUS differed from MRI for determination of tumor extension into the bladder and urethral penetration on the basis of the location of the prostate gland and trigone within the pelvic canal. Diagnostic imaging of pelvic structures requires placing more pressure on the transducer. In addition, images typically are at oblique angles and are not of the same high quality as images obtained outside of the pelvic canal. These deficiencies of TAUS can lead to images that are imperfect, compared with MRI images, which are perfectly planar provided they are acquired correctly.
The TRUS machine used in the study reported here provided excellent image quality and was easy to use. However, as the potential use of TRUS in companion animals increases, a few considerations should be mentioned. First, it is likely that the transducer used in the present study would be too large for certain breeds of dogs. The smallest dog evaluated in the study had a body weight of 9.4 kg, and no difficulty was noted for introduction of the TRUS transducer into that dog's rectum or performance of imaging procedures. Smaller TRUS transducers are available, and investigation into the use of those transducers would be beneficial for veterinary patients. Second, the TRUS machine used in the present study was uniplanar, which limited the assessment of the prostatic masses in the transverse plane. Newer TRUS models are capable of performing multiplanar evaluations. Advancements in ultrasonographic technology and the combination of ultrasonography with Doppler and contrast-enhanced ultrasonography have been evaluated in humans29–33 and companion animals.34–36 For microbubble contrast-enhanced ultrasonography, injected microbubbles respond to the produced ultrasound waves, which increases the amplitude of the scattered signals. These signals are used to better identify blood vessels and to make delineations between benign and malignant lesions. Additionally, the information gained from the administration of microbubbles in conjunction with ultrasonography may improve the ability of clinicians to identify neoplastic invasion.36 These advancements are likely to make the information gained from various ultrasonographic technologies more useful and comprehensive.
The study reported here had several limitations. Only a small number of dogs was included in the study. Because of the small sample size, precision of agreement estimates was low, as indicated by the wide confidence intervals, all of which included values that would be considered poor to good or excellent. Results of agreement estimates may be altered with a larger sample size. Although investigation of TRUS for the evaluation of prostatic neoplasia in veterinary patients is warranted, the study reported here was the first step in that process, and the authors are not aware of any available information for comparison. Additionally, as stated previously, advancements in TRUS technology may yield differing results, and other devices need to be investigated in future studies. Because of the length of the TRUS transducer, measurements of tumor length sometimes had to be acquired with adjacent images. This could have resulted in inaccuracy of the tumor length measurement. Because one of the proposed uses for TRUS is the assessment of response to treatment, accurate measurement of tumor size is of utmost importance to evaluate the efficacy of a particular treatment. As additional evaluations of TRUS are performed, transducers that can be used to measure large masses in 1 image should be evaluated. Finally, the identification of anatomic structures (eg, UVJs and prostatic tumor) with fluoroscopy was imprecise because of the inability to completely visually evaluate these structures radiographically.
In the study reported here, TRUS was successfully and safely used to evaluate prostatic tumors in a cohort of dogs. There was agreement between TRUS and MRI for assessment of tumor length and height, and TRUS was better than TAUS for the determination of urethral penetration and extension of tumor into the bladder. Further investigation into the use of TRUS for the assessment of benign and malignant conditions is necessary to determine the areas where TRUS may be considered as an adjunctive imaging modality for use in companion animals.
Acknowledgments
Supported by the Center for Companion Animal Health, School of Veterinary Medicine, University of California-Davis.
The authors declare there were no conflicts of interest.
ABBREVIATIONS
| TAUS | Transabdominal ultrasonography |
| TRUS | Transrectal ultrasonography |
| UVJ | Ureterovesicular junction |
Footnotes
Red rubber catheter, Bard Medical, Covington, Ga.
HDX 1.5T MR system, GE Co, Milwaukee, Wis.
Magnevist, Bayer HealthCare LLC, Whippany, NJ.
iE 33 ultrasound, Philips, Bothell, Wash.
Prosound Alpha 7 ultrasound, Hitachi-Aloka Medical Ltd, Wallingford, Conn.
Aquasonic 100, Parker Laboratories Inc, Fairfield, NJ.
Omni Diagnost Eleva fluoroscope, Philips, Bothell, Wash.
Marker catheter, Infiniti Medical, Redwood City, Calif.
Isovue 300, Bracco Diagnostics Inc, Princeton, NJ.
Weasel Wire, Infiniti Medical, Redwood City, Calif.
Berenstein catheter, Infiniti Medical, Redwood City, Calif.
21-inch grayscale 3-megapixel medical diagnostic monitor, NEC Logistics America Inc, Itasca, Ill.
Merge Healthcare Inc, Chicago, Ill.
Stata Statistical Software, release 14, StataCorp, College Station, Tex.
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