Yield of Urinary Tract Cancer Diagnosis With Repeat CT Urography in Patients With Hematuria

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1 Genitourinary Imaging Original Research Mullen et al. CT Urography in Urinary Tract Cancer Genitourinary Imaging Original Research Katherine M. Mullen 1 V. nik Sahni Cheryl. Sadow Stuart G. Silverman Mullen KM, Sahni V, Sadow C, Silverman SG Keywords: CT urography, hematuria, urinary system, urothelial cancer DOI: /JR Received March 3, 2014; accepted after revision June 2, Presented at the Society of bdominal Radiology 2013 annual meeting, Maui, HI. 1 ll authors: Division of bdominal Imaging and Intervention, Department of Radiology, righam and Women s Hospital, Harvard Medical School, 75 Francis St, oston, M ddress correspondence to V.. Sahni (vsahni@partners.org). This article is available for credit. JR 2015; 204: X/15/ merican Roentgen Ray Society Yield of Urinary Tract Cancer Diagnosis With Repeat CT Urography in Patients With Hematuria OJECTIVE. The purpose of this study was to evaluate the yield of repeat CT urography (CTU) in detecting urinary tract malignancies in patients with hematuria. MTERILS ND METHODS. review of 5525 patients who underwent CTU between 2000 and 2011 revealed 751 (13.6%) patients who underwent repeat CTU. We excluded 127 patients with more than 3 years between examinations, 409 with nonhematuria indications, and 13 with less than 1 year of follow-up from a negative repeat examination. n additional 54 patients with malignancy diagnosed on the initial evaluation were excluded, leaving 148 patients in the study cohort (77 men and 71 women; mean age, 57 years). Patients were categorized on the basis of the presence or absence of findings suspicious for malignancy on initial CTU reports. Repeat CTU reports were correlated with cystoscopy, pathology, and clinical follow-up to determine the incidence of malignancy. Examinations negative for malignancy were confirmed with at least 1 year of clinical follow-up. CTU examinations of patients diagnosed with malignancy on repeat examination were reviewed by two radiologists in consensus. RESULTS. Initial CTU showed no findings suspicious for malignancy in 103 (70%) of 148 patients; of these, none had malignancy identified on repeat CTU. mong 45 (30%) patients with suspicious initial CTU findings, four malignancies were identified on repeat CTU (8.9%). Three were incidental to the initial suspicious finding; in retrospect, two were present on the initial CTU examination. CONCLUSION. In patients with hematuria, repeat CTU within 3 years is unlikely to show a urinary tract malignancy. These results support currently published guidelines. H ematuria is a common problem, affecting % of the population [1]. lthough most often due to benign causes, even small amounts of blood in the urine may signal a life-threatening malignancy [2 5]. Nevertheless, the yield of the evaluation of hematuria is often low; in up to 80.6% of patients presenting with hematuria, the initial evaluation fails to identify a cause for the patient s hematuria [5 8]. The diagnostic approach to patients with asymptomatic hematuria has evolved with advances in imaging beyond conventional excretory IV urography (IVU) [9 12]. Cystoscopy has been the mainstay diagnostic test of the lower tract, but on the basis of more than a decade of experience with CT urography (CTU), the 2012 merican Urologic ssociation (U) guidelines now recommend that after glomerular and tubulointerstitial diseases of the kidney and other benign conditions are excluded, all patients 35 years and older with hematuria be evaluated with CTU in addition to cystoscopy [13]. When the initial evaluation is negative or yields a benign cause, it is uncertain whether patients need to be reevaluated and when. The 2012 U guidelines recommend repeating CTU and cystoscopy within 3 5 years, guided in part by the clinical presentation. However, these recommendations are broad and are based on data derived from studies of patients largely examined with IVU [14 17]. lthough CTU has been shown to be superior to IVU [12], to our knowledge, the value of repeat CTU has not been investigated. CTU is a more expensive examination [18] and involves a higher radiation exposure to the patient [19]. dditional concerns regarding the use of CTU include potential nephrotoxic or allergic adverse reactions to IV contrast material and the cost and potential morbidity related to incidental findings [20, 21]. Patients with hematuria who have under- 318 JR:204, February 2015

2 CT Urography in Urinary Tract Cancer gone one initial negative evaluation with cystoscopy and IVU or CTU have as low a rate of malignancy as do patients without hematuria [17]. Knowledge of the diagnostic yield of repeat CTU in this population is important so that the benefits of repeating CTU can be weighed against the concerns described. lthough hematuria may be caused by clinically important benign diseases, in general, the most important clinical concern when evaluating patients with hematuria is diagnosing a urinary tract cancer. The purpose of this study was to evaluate the yield of repeat CTU in detecting urinary tract malignancies in patients with hematuria. Materials and Methods HIP-compliant retrospective single-center study was performed. Institutional review board approval was obtained for review of medical records before initiation of the project. Informed consent was waived. Subjects The electronic medical records of all patients who underwent CTU examinations at our institution between March 2000 and December 2011 were reviewed. total of 6747 CTU examinations were performed in 5525 patients in this time period. Of these, 751 patients underwent two or more CTU examinations, totaling 1973 CTU examinations (mean, 2.6 examinations per patient). Patients were excluded from the study on the basis of certain criteria (Fig. 1). First, 127 patients whose second CTU had been performed greater than 3 years after the initial examination were excluded. 3-year period was chosen to correspond with the 2012 U recommendations [13]. lso, to evaluate accurately the value of a CTU examination negative for malignancy, the interval of time was chosen to be short enough to reflect disease that was likely present at the time of the initial examination. Repeat examinations performed after intervals longer than 3 years are likely evaluating new episodes of hematuria rather than the pathologic entities responsible for the initial episode. Second, 409 patients were excluded whose initial CTU examinations were performed for indications other than hematuria. Third, 13 patients who did not have at least 1 year of follow-up beyond the repeat CTU examination and did not have a urinary tract malignancy diagnosed on the repeat CTU examination were excluded. Follow-up consisted of clinic notes, repeat abdominal imaging, cystoscopy and procedure notes, and pathology reports identified through a search of the electronic medical record. Finally, 54 patients whose initial evaluation led to a diagnosis of a cancer of the kidneys, ureters, or bladder were excluded. We did not exclude patients diagnosed with ll CTU Repeat CTU Study cohort 5525 patients (6747 examinations) 751 patients (1973 examinations) 148 patients (341 examinations) prostate cancer because the diagnosis is not typically made with CTU. The final study cohort consisted of 148 patients (77 men and 71 women; mean age, 57 years; range, years). t initial presentation, 75 patients presented with gross hematuria, 40 with microscopic hematuria, and 33 with an unspecified type of hematuria. Cystoscopy was performed at our institution in 96 patients (65%) within 6 months of the initial CTU examination and in 55 patients (37%) within 6 months of the repeat CTU examination. Imaging Technique CTU examinations were performed with MDCT scanners Somatom Volume Zoom, Somatom Sensation 16, Somatom Sensation 64, and Definition S 128, (all Siemens Healthcare); and quilion 64 and quilion 320 (both Toshiba merica Medical Systems). Patients were asked to void immediately before the examination and to drink 900 ml of water. Patients then were scanned using a three-phase protocol, including unenhanced imaging of the abdomen and pelvis ( mm collimation, 120 kvp, and variable tube current); nephrographic phase imaging of the kidneys ( mm collimation, 120 kvp, and variable tube current) 100 seconds after administration of iopromide (100 ml of Ultravist 300 or 80 ml of Ultravist 370, erlex Laboratories & ayer Healthcare) or iopamidol (100 ml of Isovue 300 or 80 ml of Isovue 370, racco Diagnostics) at 3 ml/s; and excretory phase imaging of Exclusions Delay > 3 y between examinations 127 patients (285 examinations) Indication other than hematuria 409 patients (1156 examinations) < 1 y follow-up available from repeat examinations 13 patients (27 examinations) Kidney, ureter, or bladder cancer diagnosed on initial evaluation 54 patients (164 examinations) Fig. 1 Flow diagram shows how study cohort was defined, beginning with all patients examined with CT urography (CTU) from March 2000 to December Patients undergoing repeat CTU examination were identified. Patients were excluded if interval between initial and repeat CTU examination was greater than 3 years, if CTU examination was performed for indications other than hematuria, if less than 1 year of follow-up was available from time of repeat CTU examination, or if urinary tract cancer was diagnosed on initial evaluation. the abdomen and pelvis ( mm collimation, 120 kvp, and variable tube current) minutes after contrast material injection. Excretory phase scans were reconstructed at 3- to 5-mm sections in the axial plane and 3-mm sections in the coronal plane. These examinations were supplemented with either an infusion of 250 ml of IV normal saline administered after the contrast material, 10 mg of IV furosemide (Lasix, bbott Laboratories) administered 2 3 minutes before the contrast material, or both. eginning in January 2004, patients under the age of 40 years were scanned using a two-phase split bolus protocol. This included unenhanced imaging of the abdomen and pelvis ( mm collimation, 120 kvp, and variable tube current) followed by combined nephrographic and excretory phase imaging of the abdomen and pelvis ( mm collimation, 120 kvp, and variable tube current) performed after an initial IV administration of iopromide (100 ml of Ultravist 300 or 80 ml of Ultravist 370) or iopamidol (100 ml of Isovue 300 or 80 ml of Isovue 370) at 3 ml/s and a 6 8 minute delay followed by a second injection of iopromide (50 ml Ultravist 300 or 40 ml Ultravist 370) or iopamidol (50 ml Isovue 300 or 40 ml Isovue 370) at 3 ml/s; scanning was performed at 100 seconds after the second injection. Report Review Radiology reports of the initial CTU examination of the study cohort were reviewed. On the ba- JR:204, February

3 Mullen et al. sis of the reports, patients were placed into categories according to the presence or absence of findings suspicious for malignancy (Fig. 2). Findings suspicious for malignancy included indeterminate cystic renal mass, focal thickening of the ureter or renal pelvis, focal thickening or mass of the bladder, potentially solid renal mass, calyceal compression, and calyceal filling defect. Examinations with no findings suspicious for malignancy included those with findings with clinical significance but without malignant potential (but generally requiring treatment or follow-up), findings without clinical significance, and examinations with no findings. Reports of repeat CTU examinations were then evaluated for findings suspicious for malignancy. ll patients with pathology-proven malignancy on repeat CTU examination were identified through review of the medical records. Images of the CTU examinations performed in patients with malignancy diagnosed subsequent to the second imaging examination were reviewed by two abdominal radiologists in consensus to confirm the accuracy of the findings described in the report. True-negative examinations were confirmed by verifying that no urinary tract malignancies were diagnosed in the medical record within 1 year of follow-up after the examination. 1-year followup was chosen because diagnoses of cancer more than 1 year after the repeat CTU may not reflect disease that was present at the time of the examination, and may instead represent malignancy that developed after the repeat CTU. The median length of clinical follow-up from the repeat examination in patients without malignancy was 6.3 years (range, 1 12 years). Study cohort (n = 148 patients) Initial CTU Findings Suspicious for malignancy Indeterminate cystic renal mass Focal thickening of ureter or renal pelvis Focal bladder thickening or mass Potentially solid renal mass Calyceal compression Calyceal filling defect No suspicious findings Clinically significant findings Insignificant findings Negative examination Results Of the initial CTU examinations in 148 patients, 103 (70%) showed no findings suspicious for malignancy. Of these 103 examinations, 57 revealed clinically significant findings, 30 revealed clinically insignificant findings, and 16 had no findings. Examples of findings with clinical significance included urolithiasis, enlarged prostate gland, urinary tract obstruction, renal artery aneurysm, diffuse bladder wall thickening, nephrocalcinosis, and large (> 4 cm) angiomyolipomas. Clinically insignificant findings included simple renal cysts, small angiomyolipomas, renal scar, or postsurgical appearance. None of these patients was diagnosed with malignancy at repeat CTU. No Repeat CTU Findings 4 malignancies (8.9%) 0 malignancies (0%) Fig. 2 Flow diagram shows findings of initial and repeat CT urography (CTU) at evaluation for hematuria. Initial CTU examinations were categorized on basis of presence or absence of findings suspicious for malignancy, and repeat CTU examinations were analyzed for diagnoses of malignancy. Of the initial CTU examinations in 148 patients, 45 (30%) had findings that were suspicious for malignancy. Fourteen had an indeterminate cystic renal mass, 11 had focal thickening of the ureter or renal pelvis, 10 had focal thickening or mass of the bladder, eight had a potentially solid renal mass, and one each had calyceal compression and a calyceal filling defect (Fig. 2). Of 45 patients with findings suspicious for malignancy, four (8.9%) patients had a urinary tract malignancy diagnosed on repeat CTU. These included urothelial carcinoma of the bladder, urothelial carcinoma of the right renal pelvis, renal cell carcinoma, and squamous cell carcinoma of the kidney. C Fig year-old man with urothelial carcinoma diagnosed on repeat CT urography (CTU). and, On initial CTU in 2004, axial nephrographic phase image () shows left-sided 4.8-cm indeterminate cystic renal mass (circle, ) with minimally thickened septations and wall calcification. xial excretory phase image () from same examination shows filling defect in right upper renal calyx (arrow, ). This finding was not described in initial report. C, On repeat CTU in 2005, axial, excretory phase image shows slight increase in size of calyceal filling defect (arrow). Left cystic renal mass was unchanged (not shown). Urothelial carcinoma was diagnosed at right nephroureterectomy. 320 JR:204, February 2015

4 CT Urography in Urinary Tract Cancer C D Fig year-old man with history of prostate cancer treated with brachytherapy who was diagnosed with urothelial carcinoma of bladder on repeat CT urography (CTU). C, Initial CTU in 2005 revealed bilateral small enhancing renal masses (circles) on axial images ( and ) and normal bladder is shown on coronal excretory phase image (C). rachytherapy seeds are seen throughout prostate (arrow, C). D, Repeat CTU in 2006 showed new 2.9-cm mass in bladder dome on coronal excretory phase image (arrowhead). Foley catheter balloon is in bladder (asterisk). There was only slight interval growth of renal masses (not shown). Urothelial carcinoma was diagnosed on transurethral resection of bladder tumor and confirmed on radical cystectomy. rachytherapy seeds are seen throughout prostate (arrow). Fig year-old man with renal cell carcinoma diagnosed on repeat CT urography (CTU)., On initial CTU in 2005, axial, nephrographic phase image shows right-sided 1.6-cm hypodense cystic renal mass that was described as benign complicated cyst but in retrospect shows indistinct inferior border and possible solid component (arrow)., On repeat CTU in 2007, axial, nephrographic phase image shows growth of mass to 2.2 cm and more solid components (arrow). Renal cell carcinoma was diagnosed at right partial nephrectomy. Image review revealed that two of these malignancies were present on the initial CTU examination but were not detected or were misinterpreted as likely benign. The initial CTU in a 77-year-old man who presented with an unspecified type of hematuria was reported to have an indeterminate cystic renal mass (Fig. 3), which remained stable and was proven benign. However, a calyceal filling defect in the contralateral kidney was not detected. The filling defect increased in size and was detected with repeat CTU 9 months later. The patient underwent right nephroureterectomy and was diagnosed with urothelial carcinoma. n indeterminate cystic renal mass on the initial CTU examination of a 69-year-old man with gross hematuria (Fig. 4) was reported as likely benign. In retrospect, this mass had an indistinct inferior margin and possible solid component. Repeat CTU 2 years later showed increased size and solid components of the mass, and renal cell carcinoma was diagnosed at partial right nephrectomy. Two other patients had malignancies diagnosed with repeat CTU; both patients findings were new and located apart from the suspicious finding on the initial examination. In the first patient, a high-grade urothelial carcinoma of the bladder was diagnosed with repeat CTU in a 74-year-old man with an unspecified type of hematuria after bilateral small renal masses were detected on initial CTU (Fig. 5). The patient underwent radical cystectomy with ileal conduit urinary diversion. lthough the renal masses grew slightly and were concerning for renal cell carcinoma, pathology was never performed. In the second patient, a left-sided solid renal mass with ipsilateral retroperitoneal lymphadenopathy was detected with repeat CTU JR:204, February

5 Mullen et al. C Fig year-old man with bilateral staghorn calculi who was diagnosed with renal squamous cell carcinoma on repeat CT urography (CTU). and, xial, excretory phase images from initial CTU in 2008 show bilateral staghorn calculi (dotted arrow) and thickening of right renal pelvis (solid arrow, ). C, On repeat CTU in 2010, axial nephrographic phase images show interval development of 6.6-cm enhancing left renal mass (asterisk) and left-sided retroperitoneal lymphadenopathy (arrowhead). Thickening of right renal pelvis remained stable (not shown). Percutaneous biopsy of retroperitoneal lymph node revealed squamous cell carcinoma. in a 52-year-old man whose initial CTU performed for microscopic hematuria showed bilateral staghorn calculi, obstructive uropathy, and right-sided renal pelvis thickening with adjacent stranding (Fig. 6). left-sided squamous cell carcinoma was diagnosed by percutaneous retroperitoneal lymph node biopsy. The right renal pelvis thickening and adjacent stranding remained stable over 23 months and were diagnosed as pyelitis secondary to the staghorn calculus. Discussion lthough CTU has become established in clinical practice and is now part of published guidelines in patients with asymptomatic hematuria, the approach to patients with hematuria in whom the initial evaluation is negative or yields only benign findings remains in question. n initial negative examination may leave the clinician (and patient) wondering whether a urinary tract cancer was present but not detected. ecause hematuria may be caused by multiple urinary tract abnormalities, an initial evaluation that reveals benign findings, such as an enlarged prostate gland or urolithiasis, particularly because they are common, may lead to similar concerns about a concomitant cancer that could be present and missed at the time of the initial evaluation. These concerns may lead to repeating the examination. The optimal timing for reevaluating patients with hematuria, however, is not known. The U guidelines offer a broad range of recommendations and suggest that a repeat evaluation including CTU may be performed at any time within 3 5 years. Our data indicate that a repeat CTU examination earlier than 3 years is unlikely to lead to a diagnosis of malignancy in the absence of suspicious findings on the initial examination. Indeed, of the 148 patients in our cohort, no malignancies were diagnosed with repeat CTU in 103 patients who had no suspicious findings on initial CTU. Our findings suggest that from the perspective of diagnosing urinary tract malignancy, CTU had a high negative predictive value (because all negative examinations were true-negative for malignancy). Suspicious findings were detected in less than one third of patients (45/148), and when these patients were reexamined, less than 10% (4/45) were found to have a urinary tract malignancy on repeat CTU. Moreover, of these four patients, two malignancies were detected serendipitously because they were incidental to the initial examination findings. In these two patients, the malignancies may have been present at the time of the initial examination (and simply too small to be detected with CTU) or they may have developed in the interval. The other two malignancies were not detected or misinterpreted and were seen only in retrospect; in both patients, the cancer remained organ confined. Several studies of patients with negative initial evaluations for asymptomatic microscopic hematuria also have found very low (0 0.85%) rates of urinary tract malignancies subsequently diagnosed with long-term clinical follow-up as long as 20 years [14 17]. However, most of these studies were conducted before CTU became established in clinical practice, relying instead on excretory urography (IVU) with or without renal ultrasound for the evaluation of the upper tracts. For example, Murakami et al. [14] reported four malignancies that were found among 809 patients within 3 years of an initial negative evaluation that used IVU and renal ultrasound. Howard et al. [16] found no malignancies in 191 patients with unexplained hematuria over years who were evaluated initially by cystoscopy and renal ultrasound. Mishriki et al. [15] found only one of 292 patients who developed bladder cancer 2 years after a negative initial evaluation that included IVU with or without renal ultrasound. Madeb et al. [17] conducted a prospective study of 234 patients with hematuria who were evaluated with cystoscopy and imaging with either IVU or CTU. fter a negative initial evaluation, only two bladder cancers were diagnosed, with no malignancies diagnosed in the upper tract on follow-up. lthough these studies, like ours, revealed an extremely low (< 1%) rate of malignancies diagnosed on follow-up, even after intervals as long as 20 years [16], the upper tract imaging tests used in the initial evaluation were largely limited to IVU and renal ultrasound. lthough Madeb et al. [17] used CTU to evaluate some patients with hematuria, the study cohort also included patients evaluated only with IVU. In addition, the follow-up method in these studies did not always include reevaluation with imaging. Our study used CTU in both the initial and repeat evaluation. The consistent use of CTU, with its higher sensitivity for detection of malignancy [12], is likely to reduce false-negative initial exam- 322 JR:204, February 2015

6 CT Urography in Urinary Tract Cancer inations and thereby decrease further the need for repeat examinations. However, given the extremely low rate of malignancies diagnosed on repeat evaluation, a large sample size would be necessary to document a statistically significant decrease in yield of repeat examination after an initial evaluation using CTU rather than IVU. Of note, the U guidelines were intended for asymptomatic microhematuria [13]. Our cohort included patients with gross hematuria who have a higher pretest probability of malignancy [22]. Nevertheless, the low rate of subsequently diagnosed malignancy in our study is in keeping with prior reports [14 17]. The low rate of malignancy in our cohort emphasizes the high negative predictive value of CTU even in a higher-risk population. There are several limitations to our study. First, given its retrospective design, the proportion of all patients with hematuria who were reexamined with CTU was not determined, and information about other clinical risk factors for developing a urinary tract malignancy that may have contributed to the decision to reexamine patients with CTU was not collected. The subset of patients in whom repeat CTU was requested may have differed from those who were not reevaluated; for example, they may have presented with more concerning clinical features. If more patients had been evaluated and added to our cohort, the rate of malignancy detected on repeat examinations might have been lower. Indeed, the likelihood of detecting a urinary tract cancer after a negative initial evaluation may depend in part on factors known to increase the risk of a urinary tract malignancy, such as gross hematuria, irritative voiding symptoms, or history of smoking or chemical exposure [13]. We did not evaluate these factors because there was an insufficient positivity rate of malignancy to evaluate their impact on the yield of repeat CTU [13, 23]. Second, the effect of using urine cytology and cystoscopy as part of the initial workup of hematuria on the rate and yield of repeat CTU was not elucidated. Urine cytology and cystoscopy were not used in the evaluations of all patients; this may have decreased the yield of the initial evaluation for detecting malignancy, particularly in the lower tracts. Finally, because we did not review the images in patients who did not develop malignancy between the initial and repeat CTU, it is possible that this cohort included false-negative examinations. However, this is unlikely because the negative repeat CTU examinations were confirmed by 1 year of follow-up. In summary, our study shows the low yield of repeat CTU for diagnosing malignancy within 3 years, supporting the high negative predictive value of CTU as part of the initial evaluation of hematuria. Our data suggest that it is reasonable to delay repeat CTU evaluation for hematuria until 3 5 years, within the range recommended in the recently published U guidelines. References 1. Grossfeld GD, Litwin MS, Wolf JS, et al. Evaluation of asymptomatic microscopic hematuria in adults: the merican Urological ssociation best practice policy. Part I. Definition, detection, prevalence, and etiology. Urology 2001; 57: Carson CC 3rd, Segura JW, Greene LF. Clinical importance of microhematuria. JM 1979; 241: Mohr DN, Offord KP, Owen R, Melton LJ 3rd. symptomatic microhematuria and urologic disease. population-based study. JM 1986; 256: Mariani J, Mariani MC, Macchioni C, Stams UK, Hariharan, Moriera. 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Urology 2001; 57: FOR YOUR INFORMTION This article is available for CME and Self-ssessment (S-CME) credit that satisfies Part II requirements for maintenance of certification (MOC). To access the examination for this article, follow the prompts associated with the online version of the article. JR:204, February