Numerous procedures are currently available for the treatment of ureteral obstruction in feline patients, including ureterotomy, neoureterocystostomy, ureteral stenting, and subcutaneous ureteral bypass.1–10 Although the techniques are chosen partially on the basis of clinician preference, the cause and location of obstruction are also deciding factors.11–15 Preoperative knowledge of this information is therefore critical to the veterinary surgeon deciding on the best treatment option for a patient with upper urinary tract obstruction.
Abdominal ultrasonography is a readily accessible and noninvasive method for evaluating the upper urinary tract in cats.1,11,13,16,17 At our institution when the present study was performed, ultrasonography was used not only to diagnose the presence of ureteral obstruction but also to identify the type of lesion and its approximate location within the ureter, which are major factors in determining the type of intervention recommended. However, information regarding the accuracy of abdominal ultrasonography for these uses in cats is currently limited. Adin et al16 reported that in 11 cats that had a diagnosis of ureteral obstruction at the time of exploratory laparotomy or necropsy, ultrasonography had 100% sensitivity and 33% specificity for identifying ureteral obstructions; correct anatomic localization of the obstruction was found in 9 of 15 ultrasonographic examinations. However, in addition to the small number of cats, that study16 included only 1 cat that had obstruction due to ureteral stricture. In human medicine, the reported sensitivity of ultrasonography for detecting obstructive ureteral disease is only 45%, with positive and negative predictive values of 78% and 62%, respectively.18–22
The goal of the study reported here was to determine the utility of ultrasonography for identifying the cause and location of ureteral obstruction in cats. Additionally, we sought to determine factors that could be associated with diagnostic agreement between ultrasonographic and surgical findings.
Materials and Methods
Case selection
Electronic and hard copy medical records of cats evaluated at the University of Pennsylvania Matthew J. Ryan Veterinary Hospital between January 1, 2010, and June 30, 2016, were reviewed to identify client-owned cats with a diagnosis of ureteral obstruction. Keywords for electronic searches included ureter, ureteral obstruction, ureterotomy, ureteral stent, subcutaneous ureteral bypass, ureteral stone, and stricture. The following criteria had to be met for study inclusion: diagnosis of ureteral obstruction determined with abdominal ultrasonography performed by a board-certified veterinary radiologist or by a radiology resident directly supervised by a board-certified veterinary radiologist, direct visual observation of the cause and location of ureteral obstruction during laparotomy performed by or under direct supervision of a board-certified veterinary surgeon < 24 hours after ultrasonography was performed, and a complete medical record that included ultrasonographic and surgery reports available for review. Cats that had undergone prior surgical intervention for ureteral disease (eg, ureterotomy, neoureterocystostomy, ureteral stent placement, or subcutaneous ureteral bypass) were excluded.
Medical records review
Signalment information collected from the medical records included age, breed, sex, and weight. Ultrasonographic reports prepared by a board-certified veterinary radiologist were reviewed to identify the ureter affected (left vs right), cause (ureterolith, stricture, or other) and location (proximal, middle, or distal aspect of the ureter or multiregional involvement) of the ureteral obstruction, and presence or absence of retroperitoneal effusion. Surgery reports prepared by a board-certified veterinary surgeon or surgical resident were also reviewed to determine the ureter affected and the cause and location of ureteral obstruction as well as the type of surgical procedure performed. Location was recorded as indicated in the records for each method.
Ultrasonographic examinations
Full abdominal ultrasonography or focused assessment of the urinary tract was performed for each cat; procedure selection was at the discretion of the primary clinician. The ultrasonographic examination was performed with cats in lateral recumbency; hair on the ventral aspect of the abdomen was shaved, and ultrasound gel was used. Cats were sedated only if deemed necessary by the primary clinician or radiologist. Ultrasonography was performed by use of an imaging systema with convex (8-MHz) and linear (10- to 12-MHz) transducers, a systemb with convex (10-MHz) and linear (8- to 18-MHz or 6- to 15-MHz) transducers, or a systemc with convex (5- to 8-MHz) and linear (5- to 12-MHz or 5- to 18-MHz) transducers.
Statistical analysis
Descriptive statistics were calculated for all measured variables. For cats with bilateral ureteral disease, 1 ureter was randomly selected for inclusion in the statistical analysis. Data were evaluated for normal distribution with the Shapiro-Wilk test. Categorical data were reported as numbers and percentages. Continuous data were reported as mean ± SD or as medians and range (for data with and without normal distribution, respectively). The κ statistic was used to assess the degree of agreement between ultrasonographic and surgical findings. Agreement was interpreted on the basis of κ values as slight (< 0.2), fair (> 0.2 and < 0.4), moderate (> 0.4 and < 0.6), substantial (> 0.6 and < 0.8), or near perfect (> 0.8). A Student t test was used to determine whether patient age or weight was associated with agreement between ultrasonographic and surgical findings, and the Pearson χ2 test was used to determine whether patient sex, ureter affected, or presence of retroperitoneal effusion was associated with intermethod agreement. Values of P < 0.05 were considered significant for all comparisons. Sensitivities, specificities, and positive predictive values for ultrasonographic detection of ureteroliths and ureteral strictures were calculated. Statistical analyses were performed with statistical software programs.d,e
Results
Seventy-one cats were included in the study. Most (56/71 [79%]) were domestic shorthair cats. Other breeds represented in the study population included domestic longhair (7 [10%]), Siamese (2 [3%]), and Persian, Maine Coon Cat, Tonkinese, Russian Blue, Burmese, and Egyptian Mau (1 [1%] each). Thirty-four (48%) cats were castrated males and 37 (52%) were spayed females. Median age of the cats was 9 years (range, 1 to 18 years), and median body weight was 4.7 kg (10.3 lb; range, 2.0 to 9.8 kg [4.4 to 21.6 lb]).
Five board-certified veterinary radiologists performed ultrasonography or supervised various residents who performed the task during the data collection period. Unilateral (50/71 [70%] cats) or bilateral (21 [30%] cats) obstruction was identified (total, 92 obstructed ureters), with ureteroliths diagnosed in 79 of 92 (86%) ureters and strictures diagnosed in 11 (12%) ureters by this method. The cause of obstruction was not determined ultrasonographically for 2 of 92 (2%) affected ureters. On the basis of ultrasonographic reports, obstruction was localized to the proximal aspect of 41 of 92 (45%) ureters, the midregion of 29 (32%) ureters, and the distal aspect of 8 (9%) ureters. In 2 (2%) ureters, the location of obstruction was not determined ultrasonographically. Twelve of 92 (13%) ureters had > 1 site of obstruction seen on ultrasonographic images. Retroperitoneal effusion was visualized around 35 of 92 (38%) ureters.
Six board-certified veterinary surgeons performed surgical procedures or supervised the residents who performed the surgeries during the data collection period. Ureteroliths were identified in 59 of 92 (64%) ureters, and strictures were identified in 22 (24%) ureters. Seven of 92 (8%) ureters were diagnosed as containing solidified blood clots, and diffuse ureteritis causing obstruction was diagnosed in 1 (1%) ureter on the basis of marked diffuse ureteral thickening palpated along the entire ureteral length. In 3 of 92 (3%) ureters, no obstruction was found intraoperatively. Obstruction was localized to the proximal aspect of 48 of 92 (52%) ureters, the midregion of 10 (11%) ureters, and the distal aspect of 19 (21%) ureters. Obstruction was multiregional in 12 of 92 (13%) ureters. Surgical intervention performed included ureterotomy (36/92 [39%]), ureteral stent placement (22 [24%]), ureterotomy with concurrent ureteral stent placement (5 [5.4%]), subcutaneous ureteral bypass (13 [14%]), neoureterocystostomy (8 [9%]), modified Baori flap (1 [1%]), and ureteronephrectomy (3 [3%]). In 3 of 92 (3%) ureters, no intervention was performed owing to lack of an identified obstruction, which was confirmed by intraoperative pyelography. Owing to difficulty of attempted stent placement and the owner declining any other method of intervention, euthanasia was elected for 1 cat with a proximal ureteral stricture. Of the 41 ureterotomies performed, ureteroliths from 36 (88%) were submitted for mineral composition analysis; most (35/36 [97%]) were composed of calcium oxalate.
There was moderate agreement between ultrasonographic and surgical reports for identification of ureteroliths (κ = 0.55; P < 0.001) and strictures (κ = 0.50; P < 0.001). Representative ultrasonographic images of findings that were considered indicative of ureterolithiasis and were or were not subsequently confirmed by surgery are provided (Figures 1 and 2). There was moderate agreement between ultrasonographic and surgical reports for location of ureteral obstruction as proximal (κ = 0.51; P < 0.001), midregion (κ = 0.42; P < 0.001), or distal (κ = 0.55; P < 0.001). Among the 79 ureters diagnosed as having ureteroliths by ultrasonography, 58 (73%) were confirmed to have ureteroliths by surgery, whereas 12 (15%) had strictures, 5 (6%) had solidified blood clots, 1 (1%) had diffuse ureteritis, and 3 (4%) had no obstructive disease identified. Among the 11 ureters diagnosed as having strictures by ultrasonography, 9 were confirmed to have strictures by surgery and 2 had solidified blood clots. Of the 2 ureters in which no discrete cause of obstruction could be identified ultrasonographically, 1 was found to have ureterolithiasis at surgery and 1 was found to have a stricture.
Comparison of results for the affected ureter of 50 cats with unilateral obstruction and a randomly selected ureter of 21 cats with bilateral obstruction revealed that agreement between ultrasonographic and surgery reports for cause of ureteral obstruction was not associated with patient age, sex, or weight; presence of retroperitoneal effusion; or whether the obstruction was in the left or right ureter (P > 0.05 for all comparisons). The sensitivity, specificity, and positive predictive values of ultrasonography for identifying ureteroliths were 98%, 96%, and 98%, respectively (Table 1). For ultrasonographic detection of ureteral strictures, the sensitivity, specificity, and positive predictive values were 44%, 98%, and 88%, respectively.
Sensitivity, specificity, and positive predictive values of ultrasonography for the detection of ureteroliths and strictures in 71 cats with ureteral obstruction.
Sensitivity | Specificity | PPV | ||||
---|---|---|---|---|---|---|
Diagnosis | TP/(TP + FN) | % | TN/(TN + FP) | % | TP/(TP + FP) | % |
Ureterolith | 47/48 | 98 | 22/23 | 96 | 47/48 | 98 |
Stricture | 7/16 | 44 | 54/55 | 98 | 7/8 | 88 |
Surgical findings were used as the reference standard for the assessments. Surgery took place < 24 hours after ultrasonographic examination. For cats that had bilateral lesions (n = 21), 1 ureter was randomly selected for inclusion in the analysis. Eleven cats were found to have other obstructive lesions (blood clots [n = 7] or ureteritis [1]) or did not have the cause identified surgically (3).
FN = False negative. FP = False positive. PPV = Positive predictive value. TN = True negative. TP = True positive.
Discussion
Results of the present study suggested that ultrasonography can be used to identify the cause and location of ureteral obstruction in feline patients, as there was moderate but significant agreement between the ultrasonographic diagnosis and surgical findings. However, whereas ultrasonography was highly sensitive for detection of ureteroliths (98%), sensitivity was poor for detecting ureteral strictures (44%). In fact, when all affected ureters were considered, 12 of 22 (55%) ureteral strictures identified surgically had been incorrectly diagnosed as ureteroliths in the preoperative ultrasonographic examination. The imaging modality was even less useful for detecting solidified blood clots; 5 of 7 ureters with blood clots identified during surgery had been inaccurately diagnosed as ureteroliths, and the remaining 2 had been incorrectly diagnosed as strictures on ultrasonographic examination.
There are many factors that may make determining the cause of ureteral obstruction difficult on ultrasonographic examination in cats, including small patient size, small ureteral diameter, and patient motion during the procedure. Furthermore, the ultrasonographer's view of a ureter may be obscured by surrounding structures (eg, retroperitoneal fat, mesenteric fat, and intestinal loops).18,23 Importantly, although ureteroliths with distinct echogenicity and acoustic shadowing can be readily apparent and easily distinguishable from other ureteral lesions on ultrasonographic examination, not all ureteroliths have these characteristics.23,24 Thus, it may be difficult for a radiologist to differentiate a small ureterolith that lacks acoustic shadowing from a blood clot or stricture. It may be similarly difficult to differentiate sediment and debris accumulation proximal to a stricture from a ureterolith. Because the echogenicity of blood clots can vary, especially when acute, they may be missed entirely on ultrasonographic evaluation. These factors may have contributed to the discrepancy between ultrasonographic and surgical findings in the present study.
In terms of localization of obstructions along the ureter, the interval between the onset of ureteral obstruction and ultrasonographic assessment would affect the degree of ureteral dilation present, and this in turn can influence the accuracy of ultrasonographic findings.18 Specifically, it has been suggested that localizing the site of ureteral obstruction is more challenging in cases of early obstruction, given that ureteral dilation begins proximally and then progresses distally toward the site of the obstruction.16,18 Additionally, there can be substantial tortuosity of the feline ureter (particularly proximally) up to the level of obstruction. This may also make localization of an obstruction by ultrasonography challenging. Owing to limitations of the retrospective case series design, we were unable to evaluate these factors in our study population. Future prospective studies evaluating how such factors may contribute to the accuracy of ultrasonography in characterizing ureteral obstructions may help to determine which patients could benefit from evaluation with other imaging modalities during the surgical screening process.
Despite the inherent limitations of ultrasonography, it is still commonly used as the initial imaging modality of choice for human patients with upper urinary tract disease.25 Computed tomography has a reported sensitivity of 95% to 98% and specificity of 96% to 100% in human patients with ureterolithiasis.26–29 Computed tomography allows for improved detection of ureteroliths and more accurate estimation of ureterolith size than does ultrasonography.18 For cats, it has also been suggested that CT is superior to ultrasonography for determining the number and position of ureteroliths.13 However, drawbacks of advanced imaging exist, including greater expense than ultrasonography, the need for heavy sedation or general anesthesia in small animal patients, and exposure to radiation and contrast agents.25,30 Comprehensive studies evaluating CT in the context of feline ureteral abnormalities are needed to determine which patients would benefit most from this advanced imaging modality.
There were several limitations to the present study, including its retrospective nature. It should be noted that location of ureteral obstructions was subjectively assessed during both ultrasonographic examination and surgery; no objective measurements were made, and the terminology used was not standardized. The subjective, nonstandardized nature of these assessments made comparison of ultrasonographic and surgical findings challenging. Additionally, there was an interval of up to 24 hours between ultrasonographic examination and surgery in our study population. Because ureteroliths have been shown to spontaneously migrate in small animals during the perioperative period,31 this time interval may have resulted in discrepancies between ultrasonographic and surgical findings for disease localization. At the time patients in the present study were treated, all ultrasonographic imaging at our institution was performed or directly supervised by a board-certified veterinary radiologist and we had a high caseload of cats that underwent imaging because of suspected ureteral disease. This is not true of all veterinary institutions, and such differences may limit the generalizability of our study results. The fact that ultrasonographic examinations were performed by multiple radiologists likely added a component of intraspecialty variability to our study results. Another limitation was that only cats that underwent exploratory laparotomy because of ureteral obstruction were included; it did not take into account cats with obstructions that were managed medically or for which the owners declined surgical intervention. Given that ultrasonographic results likely had a strong influence on whether surgery was recommended, there was considerable potential for verification bias. Despite these limitations, our results shed light on the diagnostic utility of abdominal ultrasonography in cats with ureteral obstruction and have important implications for veterinary surgeons who may rely on this imaging modality for preoperative patient assessment and surgical planning.
In the present study, ultrasonography appeared to be a useful imaging modality for detection of ureteral obstruction in cats with ureterolithiasis; the method was found to have limitations for detection of other causes of obstruction such as strictures or blood clots. The findings suggested that, minimally, a surgeon must be prepared to adjust the treatment plan for such patients in the event of unexpected surgical findings. Future prospective studies are needed to determine the role of advanced imaging in the assessment of feline patients with ureteral disease.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
Footnotes
LOGIQ 9, General Electric Medical Systems, Milwaukee, Wis.
LOGIQ S8, General Electric Medical Systems, Milwaukee, Wis.
EPIQ 5G, Philips Medical Systems, Bothell, Wash.
Stata for Mac, version 14.0, Stata Corp, College Station, Tex.
XLSTAT for Mac 2015, Addinsoft SARL, New York, NY.
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