Abstract
Objective:
To compare the diagnostic value of contrast-enhanced ultrasonography (CEUS) with baseline ultrasound (B-US) in ureteral neoplasms.
Methods:
Retrospective analysis, comprising clinical presentation, image appearances, and diagnostic results on B-ultrasound and CEUS, considering pathological result as a gold-standard, was conducted on the clinical information of 39 patients with ureteral neoplasms. CT urography was used to detect and confirm the presence of ureteral neoplasms. Both B-ultrasound and CEUS investigations of those 39 patients under study were performed by a senior radiologist.
Results:
Pathological outcomes established 27 ureteral malignancies and 12 ureteral benignancies. Ureteral malignancies were observed to occur in older patients than benignancies (p = 0.002). Only the morphological indicator of the ureteric wall on B-ultrasound was different in ureteral malignancies and benignancies (p = 0.030). Tumors with hyperenhancement, larger width, and hyperenhanced ureteric wall were easily diagnosed as malignant on CEUS, whereas iso-/hypoenhanced, narrower, and iso-/hypoenhanced ureteric wall indicated benign tumors. Moreover, the lesion widths, enhanced morphologies of the ureteric wall, and the ureteral wall’s linear boundaries on CEUS were different between high- and low-stage ureteral urothelial carcinomas (p = 0.012, 0.002, 0.001, respectively).
Conclusion:
The display of microvessels in ureteral neoplasms was significantly enhanced by CEUS, thus contributing to the differential diagnosis of ureteral neoplasms while assisting the staging of ureteral urothelial carcinoma.
Advances in knowledge:
The imaging features of different ureteral neoplasms on CEUS were analyzed in this study. The diagnostic performances of CEUS and B-ultrasound in ureteral urothelial carcinomas were also explored.
Introduction
Urothelial carcinoma is the fourth most commonly occurring carcinoma globally; while 5–10% of them occurred in the upper urinary tract,1 a very few are detected only in the ureter.2 Although the occurrence of ureteral malignancy is infrequent, its detection at an earlier stage is difficult, resulting in a poor prognosis.3–6 An accurate imaging diagnosis is critical in concluding the treatment; nevertheless, the imaging presentation of ureteral malignancy possibly gets overlapped by benign malignancy.7,8
Swift advancements of ultrasonographic apparatus have rendered ultrasonography to serve as the first-line investigation of patients with hematuria owing to advantages, for instance, non-radiation, low cost, dynamic imaging, and operational comfort.9 Nevertheless, ultrasonographic image quality may be influenced by factors such as the patient’s body size, bowel gas interference, and the radiologist’s operational expertise. Consequently, the dilated ureteral tract may appear as a mass-like or cloudy appearance, and the margin or the vessel signal is not adequately revealed. These limitations cause low accuracy of detecting and diagnosing ureteral lesions.7,10,11
Contrast-enhanced ultrasonography (CEUS) functions as a novel tool for dynamically demarcating intratumoral microvessels, the diameter of which is around <40 µm. The ultrasound contrast agent (UCA) is a phospholipid-coated microbubble containing an inert gas, and their half-life in vivo is only 15 min, which is safely expelled through respiration. UCA is also a pure blood pool radiotracer that is incapable of passing through the interstitial tissue; therefore, it can capture the entire process of microcirculation perfusion in the lesion.12 From its first application 10 years ago, CEUS has been used as a potent tool for differential analysis of tumors in multiple organs including diagnosing renal parenchymal tumors and renal pelvic lesions.13–16 Upper urinary tract masses have been reportedly assessed using CEUS. This technique allows the distinction between high- and low-grade tumors and differentiation of the tumor from the surrounding structures, and accurate mass measurements.17 However, there were few studies conducted to explore the diagnostic performance of CEUS in ureteral malignancies and benignancies, which will be investigated in this study.
Methods and materials
Patients
The Institutional Ethics Committee of Shanghai General Hospital sanctioned this investigation. Consecutive patients hospitalized between December 2012 and May 2019 suspected to have ureteral neoplasms were included in this study. The lesions were detected earlier by way of CT urography (CTU). Written informed consent was provided by each patient. Usually intravenous use of ultrasound contrast agent (SonoVue, Bracco) is contraindicated in patients with right-to-left shunts, severe pulmonary hypertension (pulmonary artery pressure >90 mmHg), uncontrolled systemic hypertension, and adult respiratory distress syndrome. In this study, none of the patients was contraindicated to SonoVue.
Detection result of ureteral lesions on baseline ultrasonography by junior and senior radiologist
The detection rates of ureteral lesions obtained from the B-ultrasound investigation outcomes recorded by a junior radiologist with ≤5 years' experience were compared with those of a senior radiologist with16 years of experience. First, all the hospitalized patients underwent a routine sonographic physical examination to detect the abdominal irregularities, including urinary system on their admission by junior radiologists. The senior radiologist further assessed them for specific ureteral examinations.
Further B-ultrasound and CEUS assessment for ureteral lesions performed by the senior radiologist
Following are the data regarding the ultrasound equipment, transducer, and CEUS mode with corresponding mechanical index (MI): Acuson Sequoia 512 ultrasound machine (Siemens, Germany) with 4C1-S transducer and cadence contrast pulse sequencing technique (MI = 0.15); Logiq E9 (GE) with C1-6 and coded contrast imaging technique (MI = 0.12), and MyLab Twice (Easote, Italy) with CA541 and contrast tuned imaging technology (MI = 0.05).
All data and images were documented on B-ultrasound, whereas the best plane to present the ureteric lesion’s entire length opted for CEUS imaging. In case the plane was inadequate to display the lesion, another segment was chosen for the repeated CEUS. SonoVue (Bracco, Milano, Italy) of the dosage 2.4 ml was administered as a bolus via the antecubital vein. The perfusion of the lesion was assessed in real-time by pressing the time marker. It was observed for 2 min. The images were captured in the “Live-Dual” display modality that displays CEUS images and gray-ultrasound images simultaneously on the screen. The outcomes of the investigations were stored in a DVD in the DICOM format.
All patients were on an empty stomach for 8 h before ultrasound examination full bladder (>200 ml). The radiologist cautiously traced the entire ureter from end to end diagonally and longitudinally, using the zoom function, adjusting focusing, and/or dynamic range for a better display of the lesion in the ureteric lumen. The patients were positioned in the supine position to scan the middle and lower parts of the ureter. The investigator pressed the probe in their lower abdomen and pushed the ventral side several times to avoid bowel gas. Applying pressure is particularly crucial for exposing the middle part of the ureter. On selecting the best plane, the radiologist may utilize the strength of her shoulder and both hands to fix the plane to observe the complete perfusion process of the contrast agent in the lesion.
Ultrasonographic image analysis
The B-ultrasound and CEUS diagnostic outcomes documented by the senior radiologist were classified into malignant and benign neoplasms. The following features were recorded. The specific operative steps were as follows:
Among the gray-ultrasonographic images, the neoplasm echogenicity was classified as slightly hyper-, iso-, and hypoechoic in relation to the renal parenchyma.18 The ureteric wall morphology at the site of neoplasm was studied. If the ureteral wall was observed to be either expanded or constricted and linearly appeared thicker, its echogenicity diminished with an unclear margin with the intraluminal lesion, labeled as “irregular and thickened.” If the ureter wall persisted in having the regular shape and linearly hyperechoic appearance, it was considered “regular and smooth.” If it was neither, it was titled as “atypical.”
The intratumoral blood flow of the neoplasm was evaluated with a color Doppler flow image (CDFI). The “abdominal” mode was set, and the focus at the level of the area of interest. The power and gain were tuned to gain a good signal for flow and reduce the adjacent tissue signals. Comparatively, low-pulse repetition frequencies were opted to display the vessels with low velocities.
The length and width of the neoplasm were measured via CEUS images. The boundary of ureteric neoplasm was more clearly exhibited by CEUS than gray ultrasonography; thus, the lesion’s maximal length and width on the best longitudinal plane were recorded. In the case of a clear margin of the intraluminal lesion with the ureteral wall, the lesion’s width was measured from the ureteral wall’s inner margin and the outer margin of the ureteral wall if the margin of the lesion was unclear with the ureteral wall. The high intensities of the ureteral neoplasm and the ureteric wall at the tumor site in the arterial phase (3–30 s after contrast agent injection) were assessed by visual observation. They were then categorized into hyper-, iso-, and hypoenhancement in relation to the adjacent tissues.
Statistical analysis
The IBM SPSS statistics 20.0 system was used for all statistical tests; χ2 test was carried out for comparative analyzes of sex distribution, infected side, and ultrasonographic characteristics between malignant and benign neoplasms. The localization and symptoms distribution were compared using Fisher’s exact test, whereas the age of the patient and the tumor size were compared with a t-test. The diagnostic performances were compared with receiver operating characteristic (ROC) curve analysis; the values of area under the ROC curve, sensitivity, specificity, and accuracy were evaluated; and pathological outcomes were considered a reference standard. p-values < 0.05 were considered statistically significant for intergroup comparisons.
Results
Pathological result of ureteric neoplasms
27 urothelial carcinomas were established using the histopathological reports following radical nephroureterectomy of 18 cases and partial ureterectomy of 9 cases. Of these 27 malignant cases, 3 were associated with renal pelvic urothelial carcinomas (UCs), and one with bladder UC. Multiple lesions in the ureter were observed in the one accompanied with renal pelvic UC, and the rest were with a single lesion in the ureter.
Among 12 ureteral benignancies, radical nephroureterectomy established a case of ureteral endometriosis and a case of tuberculous granulomatous inflammation; partial ureterectomy confirmed two cases of fibroepithelial polyps; pathological results from ureteroscopy verified seven cases of chronic infections and one of the ureteritis cystica.
Clinical features of patients with ureteric neoplasms
The patients with ureteric malignancies were older than patients with benignancies as per the outcomes (p < 0.05; Table 1). The number of male patients with ureteric malignancies was higher than that of female patients, whereas patients with benignancies exhibited an equal distribution of the male and female patients. The distribution of localization and affected side were not found to be significantly different. The most common symptom in patients with ureteric malignancy was hematuria, whereas flank pain was common among patients with benignancy.
Table 1.
Clinical features of patients with ureteral neoplasms.
| Information | Malignancy (N = 27) | Benignancy (N = 12) | p-value |
|---|---|---|---|
| Mean age (years) | 69.5 ± 10.7 | 51.3 ± 11.6 | 0.002 |
| Gender distribution (N%) | 0.194 | ||
| Male | 19 (70.4%) | 6 (50.0%) | |
| Female | 8 (29.6%) | 6 (50.0%) | |
| Side (N%) | 0.491 | ||
| Left ureter | 13 (48.2%) | 5 (41.7%) | |
| Right ureter | 14 (51.8%) | 7 (58.3%) | |
| Localization in ureter (N%) | 0.893 | ||
| Upper segment | 9 (33.3%) | 5 (41.7%) | |
| Middle segment | 6 (22.2%) | 2 (16.7%) | |
| Lower segment | 12 (44.4%) | 4 (33.3%) | |
| Entire segment | 0 (0.0%) | 1 (8.3%) | |
| Symptoms (N%) | 0.080 | ||
| Hematuria | 20 (74.1%) | 4 (33.3%) | |
| Flank pain | 5 (18.5%) | 6 (50.0%) | |
| Not specific | 2 (7.4%) | 2 (16.7%) |
p＜0.05: Significant different.
Ultrasonographic features of ureteric neoplasms on B-ultrasound and CEUS
The morphology of the ureteric wall on the tumor site on B-ultrasound appeared to be different (p < 0.05), which was more irregular and thickened in malignancy (Table 2). Nevertheless, the difference between tumoral echogenicity and tumoral blood flow was indistinguishable.
Table 2.
Characteristics of ureteral neoplasms on B-ultrasound and CEUS.
| Malignancy (N = 27) | Benignancy (N = 12) | p-value | |
|---|---|---|---|
| Echogenicity of neoplasm on gray-US | |||
| Hypoechoic | 21 | 9 | 0.849 |
| Iso-/Slight hyperechoic | 6 | 3 | |
| Intratumoral blood flow of neoplasm on CDFI | |||
| Yes | 9 | 1 | 0.099 |
| No | 18 | 11 | |
| The morphology of ureteric wall at the site of neoplasm on gray-ultrasound | |||
| Irregular or thickened | 18 | 3 | 0.030 |
| Regular or smooth | 9 | 8 | |
| Atypical | 0 | 1 | |
| The width of the neoplasm on CEUS | |||
| Size (mm) | 12.59 ± 3.68 | 7.14 ± 3.18 | 0.007 |
| The length of neoplasm on CEUS | |||
| Size (mm) | 33.70 ± 20.38 | 23.29 ± 9.96 | 0.119 |
| Enhanced intensity of neoplasm in arterial phase on CEUS | |||
| Hyperenhanced | 27 | 2 | 0.000 |
| Isoenhanced | 0 | 5 | |
| Hypoenhanced | 0 | 5 | |
| Enhanced intensity of ureteric wall at the site of neoplasm on CEUS | |||
| Hyperenhanced | 25 | 2 | 0.000 |
| Iso-/hypoenhanced | 2 | 10 | |
CDFI, color Doppler flow image; CEUS, contrast-enhanced ultrasound.
p＜0.05: Significant different.
The neoplasm size was more precisely measurable on CEUS images than on B-ultrasound images. The malignant ureteric lesions were significantly wider than benign lesions (p < 0.05) but not longer. The heightened intensity of neoplasms was observed to be significantly dissimilar (p < 0.05). The ureteric malignancy (27/27, 100.0%) and most of their surrounding ureters (25/27, 92.6%) revealed intensive hyperenhancement in the arterial phase (Figure 1). In contrast, the majority (10/12, 83.3%) of benignancy displayed mild isoenhancement or sparse hypoenhancement, including seven chronic infections and one of ureteritis cystica, ureteral endometriosis (Figure 2), and fibroepithelial polyps. One case of tuberculous granulomatous inflammation and one case of fibroepithelial polyps presented hyperenhancement, similar to malignancy appearance (Figure 3 and Supplementary Video).
Figure 1.
Two cases of ureteral malignancies. (a) An isoechoic mass (white arrow) in the lower part of the left ureter on baseline ultrasonography. (b) Same case shown in Fig. a. No obvious vessel signal was detected in the mass and ureteric wall on CDFI. (c) Same case shown in Fig. a. The mass and ureteric wall was obviously hyperenhanced on CEUS, and the size of the neoplasms could be measured more accurately than that on B-ultrasonography (white arrow) and the pattern of ureteric wall was swollen at the tumor site. The pathological proved the mass to be high grade invasive urothelial carcinoma in T4 tumor stage. (d) A hypoechoic mass in the upper segment of the left ureter on B-ultrasonography (white arrow). The difference of echogenicity between the tumor and the ureteric wall on the tumor site was not obvious. (e) Same case shown in Fig. c. No obvious vessel signal was detected in the mass and ureteric wall on CDFI. (f) Same case shown in Fig. c. The mass appeared to be hyper-enhanced in the arterial phase on CEUS (white arrow). The morphology of the ureteric wall on the tumor site was irregular and thickened. The pathological proved the mass to be high grade invasive urothelial carcinoma in T2 tumor stage. CDFI, color Doppler flow imaging; CEUS, contrast-enhanced ultrasonography.
Figure 2.
A case of ureteric benignancy. (a, b) A hypoechoic mass in the right ureter, with no obscure boundary with the uterus. No obvious vessel signal was detected in the mass on CDFI (white arrow). (c, d) The mass showed hypoenhanced in the arterial phase and venous phase on CEUS (white arrow). The diagnostic result was ureteral benignancy. *The pathological proved the mass to be endometriosis. CDFI, color Doppler flow imaging; CEUS, contrast-enhanced ultrasonography.
Figure 3.
A case of ureteral benignancy. (a) An isoechoic mass in the middle and lower segments of the right ureteric lumen on the grayscale image (white arrow). (b) The mass was hyperenhanced in the arterial phase on CUES (white arrow), and the ureteric wall was regular, smooth, and hyperenhanced. The pathological proved the mass to be fibroepithelial polyp. CEUS, contrast-enhanced ultrasonography.
In one case of multiple ureteral lesions, a large lesion (Length × Width 23 × 9 mm) was detected on ultrasound by the senior radiologist, but the remaining small lesions (2–4 mm) were not.
All the ureteral lesions were detected by the senior radiologist, whereas the junior radiologist’s detection rate was 79.49% (31/39), including missing three chronic infections and five ureteral malignancies.
The 39 cases enrolled in this study were previously scanned by CTU and the presence of the lesions was first confirmed. 34r cases had a definitive diagnosis of CTU, while 5 cases were undetermined to be malignant or benign. Following CEUS showed that two cases were hyperenhanced in CEUS, indicating that they were malignancies (pathologically proved to be ureteral urothelial carcinomas), and the other three cases showed sparse hypoenhancement in CEUS, according to benignancy (pathologically proven to be a chronic inflammation change) (Supplementary Figure 1).
Comparison of diagnostic performance between B-ultrasound and CEUS
Here, B-ultrasound and CEUS appropriately diagnosed 23 (18 malignant and five benign) and 37 (27 malignant and 10 benign) lesions, respectively (Table 3). The values of diagnostic accuracy, sensitivity, specificity, and Az of B-ultrasound for ureteric lesions were 58.97%, 66.67%, 41.67%, and 0.542, and which of CEUS were 94.87%, 100.00%, 83.33%, and 0.917, respectively.
Table 3.
Diagnostic performance of ureteral neoplasms on B-ultrasound and CEUS.
| Accuracy | Sensitivity | Specificity | Az | |
|---|---|---|---|---|
| B-ultrasound | 58.97% | 66.67% | 41.67% | 0.543 |
| CEUS | 94.87% | 100.00% | 83.33% | 0.917 |
Az, Area under the ROC curve;CEUS, contrast-enhanced ultrasonography.
CEUS in stage evaluation of ureteral urothelial carcinomas
The appearances among different stages (T) of urothelial cell carcinoma (UCC) were analyzed. The numbers of cases per the T0–T4 tumor stages were confirmed as 2, 6, 7, 10, and 2, respectively. Considering the difficulty of transabdominal ultrasonography to accurately perform subtle stratification of the ureter, patients in the T0–T2 stages were grouped into the low-stage group, and those in the T3–T4 stages were grouped into the high-stage group. The CEUS displayed significant differences in transverse tumor diameters, ureteric wall morphology, and linear boundaries between the low- and high-stage groups (all p < 0.05; Table 4).
Table 4.
CEUS characteristics of UCC between low- and high-stages.
| Low-stage (N = 15) | High-stage (N = 12) | p-value | |
|---|---|---|---|
| The length of the neoplasm(mm) | 27.8 ± 9.38 | 38.0 ± 20.85 | 0.169 |
| The width of the neoplasm(mm) | 9.44 ± 3.64 | 14.58 ± 4.80 | 0.012 |
| The morphology of ureteric wall at the site of neoplasm | |||
| Regular or smooth | 8 | 0 | 0.002 |
| Irregular or thickened | 2 | 5 | |
| Swollen | 5 | 7 | |
| The linear boundary of ureteral wall | |||
| Distinct | 12 | 2 | 0.001 |
| Obscure | 3 | 10 | |
CEUS, contrast-enhanced ultrasonography; UCC, urothelial cell carcinoma.
p＜0.05: Significant different.
Discussion
CEUS demonstrated better diagnostic performance than B-ultrasound in ureteral lesions, which could also assist in evaluating stage of ureteral UCC.
Transabdominal ultrasound is a well-established technique utilized in assessing the urinary tract, especially among patients with renal function impairment or allergy to the radiographic contrast material. The ureteric wall morphology in the neoplastic site varied immensely between malignant and benign groups on B-ultrasound. The intratumoral blood flow displayed on CDFI strongly supported the existence of malignancy. Nevertheless, deeper position and bowel gas intrusion may cause inadequate outcomes. Most ureteral neoplasms were hypoechoic on B-ultrasound, which did not form a clear interface with luminal urine, especially with blood urine, thus diminishing the effectiveness of B-ultrasound diagnosis. These are the limiting factors for the diagnostic performance of B-ultrasound in ureteral abnormalities.19
The microvessel density in the lesion was highly correlated to its malignancy level, which is the basis for its characterization by CEUS, as CEUS is highly sensitive in detecting small vessels and low-speed blood flow. All the ureteral urothelial carcinoma presented as hyperenhanced occupied lesions in the ureteral lumen, contrary to the nonenhanced urine, which eased accurate measurement of the lesions. The diagnostic accuracy of ureteral malignancies was significantly higher in CEUS (27/27, 100%) than in B-ultrasound (18/27, 66.7%). Contrarily, the ureteral benignancies such as chronic inflammation, ureteritis cystica, and ureteral endometriosis displayed iso- or hypoenhancement in CEUS, indicating a very less number of blood vessels.20–23 The indicators of lesion width, and the enhanced pattern of the ureteric wall were also found to support the differential diagnosis. The malignant tumors were observed to be markedly wider than benign ones. The enhanced intensity of the ureteric wall surrounding the malignancies was also higher than that of benignancies, which on a pathological basis might be owing to the aggressiveness of the luminal muscle layer by carcinoma.
Here, to study the high diagnostic sensitivity of CEUS, its application value in stage evaluation of UCC was observed. The ureteral wall was seen to be irregularly thickened and even swollen in high-stage UCC, causing blurring of the boundary wall. In contrast, the ureteral wall in low-stage UCC was more likely to be regular and smooth, with a linear boundary. Correspondingly, the tumor is wider in high-stage UCC than in low-stage tumors.
CEUS prominently enhanced the diagnostic accuracy of ureteral neoplasms as compared with B-ultrasound (94.87% vs 58.97%), especially in high sensitivity (100.00%), yet with limited specificity (83.33%), because the hypervascularized benign lesions may mimic the malignancies. In this study, one case of ureteral polyp and one case of tuberculosis exhibited hyperenhancement on CEUS, similar to malignancies. Nevertheless, certain auxiliary signs for assisting such abnormalities were found. For instance, the specific “worm peristalsis” sign indicating that the lesion moved around in the lumen and was separable from the ureteric wall suggesting the diagnosis of the polyp, whereas a “beaded corkscrew” appearance supported the diagnosis of tuberculosis.24,25 These specific signs could help distinguish them from malignant ones.
All the imaging results analyzed here were obtained from a single senior radiologist. Even if the CTU results of lesion presence were known in advance by a junior and senior radiologist, the less-experienced junior radiologist misdiagnosed certain cases, establishing that identifying ureter neoplasms is operator-dependent. Nevertheless, the possibility of ultrasound in diagnosing ureteral neoplasms through careful scanning and certain experience is not ruled out. The ureteral scanning mainly depends on the anatomical knowledge of the ureter, and according to its route, the operator needs to scan continuously and uninterrupted from the upper to the lower part while applying constant pressure on the patient’s abdomen to avoid bowel gas interference.
CEUS may be more sensitive than CTU in capturing neovascularization. CTU continues to be the first-line imaging technique for urinary tract carcinoma. CTU has been reported to have the highest accuracy in detecting carcinoma of the upper urinary tract among various imaging methods, with a combined sensitivity of 92% and a combined specificity of 95%.2 However, the benign lesion can mimic malignancies in CTU, causing an undetermined diagnosis.26 In this study, the five undetermined cases in CTU had a definitive diagnosis by CEUS examination. Therefore, due to the high sensitivity of CEUS in detection of microvessels, when CTU fails to diagnose ureteral diseases, CEUS may serve as a safe and effective imaging method to help.
Certain of the several limitations of our study should be mentioned. In addition to the small number of patients, patient and operator selection bias, the limitation of B-ultrasound and CEUS in detecting small lesions had to be mentioned. In one case of multiple ureteral lesions, B-ultrasound and CEUS detected the large lesions, while small lesions (2–4 mm) were not diagnosed by observing the gross pathological specimen. Also, tumor grade assessment is essential for the selection of treatment and the determination of patient prognosis. Earlier studies have suggested that low-grade UCC in the bladder were not as hypervascularized as high-grade ones but were similar to the benign lesion.16 Nevertheless, owing to the limited number of low-grade UCC in this study, such differences between low- and high-UCC were not found. All six low-grade UCC were observed to be hyperenhanced on CEUS, and their intensity was much higher than benignancies by visual observation.
Conclusion
CEUS immensely enhanced the neovascularization display in ureteral neoplasms than in B-ultrasound. The indicators of hyperenhancement, wider size, and irregular ureteric wall supported the malignant diagnosis. Moreover, CEUS had a predicating role in staging UCC. In clinical practice, CEUS could serve as a helpful tool for the characterization of ureteral neoplasms.
Footnotes
The authors Yun Bai and Jun Lin contributed equally to the work.
Contributor Information
Yun Bai, Email: baiyang1617@163.com.
Jun Lin, Email: forestsoldier@sohu.com.
An Chen, Email: 258164790@163.com.
Min Bai, Email: baimin101@126.com.
Chunxiao Li, Email: lcx198910@126.com.
Yingyu Cai, Email: kuluta_404@qq.com.
Jie Yu, Email: yuyujiejie2013@163.com.
Wenjie Hu, Email: huwenjie_34@163.com.
Lianfang Du, Email: lianfang_du@126.com.
Fan Li, Email: medicineli@163.com.
REFERENCES
- 1.Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin 2019; 69: 7–34. doi: 10.3322/caac.21551 [DOI] [PubMed] [Google Scholar]
- 2.Rouprêt M, Babjuk M, Burger M, Capoun O, Cohen D, Compérat EM, et al. European association of urology guidelines on upper urinary tract urothelial carcinoma: 2020 update. Eur Urol 2021; 79: 62–79. doi: 10.1016/j.eururo.2020.05.042 [DOI] [PubMed] [Google Scholar]
- 3.Kardoust Parizi M, Glybochko PV, Enikeev D, Rouprêt M, Fajkovic H, Seebacher V, et al. Risk stratification of upper tract urothelial carcinoma: a review of the current literature. Expert Rev Anticancer Ther 2019; 19: 503–13. doi: 10.1080/14737140.2019.1621753 [DOI] [PubMed] [Google Scholar]
- 4.Moss TJ, Qi Y, Xi L, Peng B, Kim T-B, Ezzedine NE, et al. Comprehensive genomic characterization of upper tract urothelial carcinoma. Eur Urol 2017; 72: 641–9. doi: 10.1016/j.eururo.2017.05.048 [DOI] [PubMed] [Google Scholar]
- 5.Taylor J, Meng X, Ghandour R, Margulis V. Advancements in the clinical management of upper tract urothelial carcinoma. Expert Rev Anticancer Ther 2019; 19: 1051–60. doi: 10.1080/14737140.2019.1698295 [DOI] [PubMed] [Google Scholar]
- 6.Sung Tae H, Deuk Jae S, Kyung Sook Y, Ki Choon S, Na Yeon H, Beom Jin P, et al. Prediction of high-grade ureteral urothelial carcinoma on CT urography. Br J Radiol 2017; 90: 20170159. doi: 10.1259/bjr.20170159 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Froemming A, Potretzke T, Takahashi N, Kim B. Upper tract urothelial cancer. Eur J Radiol 2018; 98(1872-7727): 50–60. doi: 10.1016/j.ejrad.2017.10.021 [DOI] [PubMed] [Google Scholar]
- 8.Baard J, de Bruin DM, Zondervan PJ, Kamphuis G, de la Rosette J, Laguna MP. Diagnostic dilemmas in patients with upper tract urothelial carcinoma. Nat Rev Urol 2017; 14(1759-4820): 181–91. doi: 10.1038/nrurol.2016.252 [DOI] [PubMed] [Google Scholar]
- 9.Unsal A, Calişkan EK, Erol H, Karaman CZ. The diagnostic efficiency of ultrasound guided imaging algorithm in evaluation of patients with hematuria. Eur J Radiol 2011; 79(1872-7727): 7–11. doi: 10.1016/j.ejrad.2009.10.027 [DOI] [PubMed] [Google Scholar]
- 10.Maruschke M, Kram W, Zimpfer A, Kundt G, Hakenberg OW. Upper urinary tract tumors: which diagnostic methods are needed? Urol Int 2017; 98(1423-0399): 304–11. doi: 10.1159/000457133 [DOI] [PubMed] [Google Scholar]
- 11.Chlapoutakis K, Theocharopoulos N, Yarmenitis S, Damilakis J. Performance of computed tomographic urography in diagnosis of upper urinary tract urothelial carcinoma, in patients presenting with hematuria: systematic review and meta-analysis. Eur J Radiol 2010; 73(1872-7727): 334–8. doi: 10.1016/j.ejrad.2008.10.026 [DOI] [PubMed] [Google Scholar]
- 12.Claudon M, Dietrich CF, Choi BI, Cosgrove DO, Kudo M, Nolsøe CP, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver--update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultraschall Med 2013; 34(1438-8782): 11–29. doi: 10.1055/s-0032-1325499 [DOI] [PubMed] [Google Scholar]
- 13.Li F, Bai M, Wu Y, He Y, Gu J, Xing J, et al. Comparative diagnostic performance of contrast-enhanced ultrasound versus baseline ultrasound for renal pelvis lesions. Ultrasound Med Biol 2015; 41(1879-291X): 3109–19. doi: 10.1016/j.ultrasmedbio.2015.07.034 [DOI] [PubMed] [Google Scholar]
- 14.Fan L, Lianfang D, Jinfang X, Yijin S, Ying W. Diagnostic efficacy of contrast-enhanced ultrasonography in solid renal parenchymal lesions with maximum diameters of 5 cm. J Ultrasound Med 2008; 27(0278-4297): 875–85. doi: 10.7863/jum.2008.27.6.875 [DOI] [PubMed] [Google Scholar]
- 15.Nicolau C, Bunesch L, Peri L, Salvador R, Corral JM, Mallofre C, et al. Accuracy of contrast-enhanced ultrasound in the detection of bladder cancer. Br J Radiol 2011; 84(1748-880X): 1091–9. doi: 10.1259/bjr/43400531 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Li Q, Tang J, He E, Li Y, Zhou Y, Wang B. Differentiation between high- and low-grade urothelial carcinomas using contrast enhanced ultrasound. Oncotarget 2017; 8(1949-2553): 70883–9. doi: 10.18632/oncotarget.20151 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Drudi FM, Di Candio G, Di Leo N, Malpassini F, Gnecchi M, Cantisani V, et al. Contrast-Enhanced ultrasonography in the diagnosis of upper urinary tract urothelial cell carcinoma: a preliminary study. Ultraschall Med 2013; 34(1438-8782): 30–7. doi: 10.1055/s-0032-1325548 [DOI] [PubMed] [Google Scholar]
- 18.Guo H, Hamilton M, Offutt SJ, Gloeckner CD, Li T, Kim Y, et al. Ultrasound produces extensive brain activation via a cochlear pathway. Neuron 2018; 98: 1020–30. doi: 10.1016/j.neuron.2018.04.036 [DOI] [PubMed] [Google Scholar]
- 19.Browne RFJ, Meehan CP, Colville J, Power R, Torreggiani WC. Transitional cell carcinoma of the upper urinary tract: spectrum of imaging findings. Radiographics 2005; 25(1527-1323): 1609–27. doi: 10.1148/rg.256045517 [DOI] [PubMed] [Google Scholar]
- 20.Maccagnano C, Pellucchi F, Rocchini L, Ghezzi M, Scattoni V, Montorsi F, et al. Ureteral endometriosis: proposal for a diagnostic and therapeutic algorithm with a review of the literature. Urol Int 2013; 91: 1–9. doi: 10.1159/000345140 [DOI] [PubMed] [Google Scholar]
- 21.Mu D, Li X, Zhou G, Guo H. Diagnosis and treatment of ureteral endometriosis: study of 23 cases. Urol J 2014; 11: 1806–12. [PubMed] [Google Scholar]
- 22.Padilla-Fernández B, Díaz-Alférez F, Herrero-Polo M, Martín-Izquierdo M, Silva-Abuín J, Lorenzo-Gómez M. Ureteritis cystica: important consideration in the differential diagnosis of acute renal colic. Clin Med Insights Case Rep 2012; 5: 29–33. doi: 10.4137/CCRep.S9189 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Potenta SE, D'Agostino R, Sternberg KM, Tatsumi K, Perusse K. Ct urography for evaluation of the ureter. Radiographics 2015; 35: 709–26. doi: 10.1148/rg.2015140209 [DOI] [PubMed] [Google Scholar]
- 24.Georgescu D, Mulţescu R, Geavlete BF, Geavlete P, Vrabie CD, Drăghici IM, et al. Fibroepithelial polyps - a rare pathology of the upper urinary tract. Rom J Morphol Embryol 2014; 55: 1325–30. [PubMed] [Google Scholar]
- 25.Sallami S, Ghariani R, Hichri A, Zrayer O Padilla-Fernández B, Díaz-Alférez F, Herrero-Polo M, Martín-Izquierdo M. Imaging findings of urinary tuberculosis on computerized tomography versus excretory urography: through 46 confirmed cases. Tunis Med 2014; 92: 743–7. [PubMed] [Google Scholar]
- 26.Chlapoutakis K, Theocharopoulos N, Yarmenitis S, Damilakis J. Performance of computed tomographic urography in diagnosis of upper urinary tract urothelial carcinoma, in patients presenting with hematuria: systematic review and meta-analysis. Eur J Radiol 2010; 73: 334–8. doi: 10.1016/j.ejrad.2008.10.026 [DOI] [PubMed] [Google Scholar]
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