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. Author manuscript; available in PMC: 2025 Sep 23.
Published in final edited form as: Ultrasound Med Biol. 2025 May 28;51(8):1336–1342. doi: 10.1016/j.ultrasmedbio.2025.04.021

Feasibility of Contrast-Enhanced Ultrasound Fusion With Pretreatment MR/CT for Recurrence Detection in Renal Cell Carcinoma Patients During Post-Ablation Surveillance

Aylin Tahmasebi a, Tania Siu Xiao a, Corinne E Wessner a, Cristina M Kuon Yeng Escalante a, Andrej Lyshchik a, Flemming Forsberg a, Ji-Bin Liu a, Christopher G Roth a, Shuchi K Rodgers a,b, Leann M Kania a, Kevin Anton a, Anju Yadav c, Costas D Lallas d, Stephen R Topper a, Edouard J Trabulsi e, John R Eisenbrey a,*
PMCID: PMC12452136  NIHMSID: NIHMS2111386  PMID: 40436663

Abstract

Objective:

Contrast enhanced ultrasound (CEUS) is a cost-effective, safe, and accurate modality for monitoring renal cell carcinoma (RCC) recurrence following percutaneous ablation. However, ultrasound delineation of treated tumor borders can be challenging post-ablation. Here, we demonstrate the feasibility of using post-treatment CEUS fused to preablation MR/CT to detect RCC recurrence during long term follow up.

Methods:

This study was performed as part of a larger ongoing prospective clinical trial for patients with biopsy-proven RCC treated with percutaneous ablation and receiving contrast enhanced (CE) -CT or -MRI for treatment response monitoring. CEUS with preablation CT/MR fusion was performed within 4 weeks of recurrence screening, and CE-CT/MRI was used as the reference standard. After intravenous injection of an ultrasound contrast agent, CEUS imaging of a single target lesion was performed with ultrasound fused to the patient’s pretreatment CT or MRI. RCC recurrence was diagnosed at the bedside based on the presence of iso- to hyper-enhancement within the margins of the ablation cavity compared to normal renal parenchyma.

Results:

To date, 50 participants have been recruited (76% male and 24% female). All participants tolerated the contrast injections without adverse events. CEUS was successfully fused to the participant’s pretreatment cross-sectional imaging in all cases and was found to aid in the delineation of the original treatment zone. Additionally, CEUS correlated perfectly (100% agreement) with CE-CT/MRI findings for all the participants.

Conclusion:

Preliminary results demonstrate that post-treatment CEUS fused with a pretreatment CT/MRI is feasible and may aid in the correct localization of the treated tumor margins during long-term post-ablation monitoring.

Keywords: Contrast-enhanced ultrasound—CEUS; Renal cell carcinoma; Cryoablation; Microwave ablation, Fusion imaging; Surveillance imaging; Ultrasound; Contrast agent

Introduction

Renal cell carcinoma (RCC) is the most common type of kidney cancer in adults, accounting for 80%–85% of all primary renal neoplasms and is the 13th most common cause of cancer death worldwide [1,2]. RCC is often found incidentally on imaging. A minimally invasive treatment option for T1a renal cancer (≤4.0 cm), which accounts for approximately 25% of all RCCs, is percutaneous thermal ablation [3,4]. Imaging surveillance following ablation typically includes abdominal contrast enhanced (CE) computed tomography (CT) or magnetic resonance imaging (MRI) after 3–6 months. Long-term surveillance utilizes annual CE-CT or -MRI (preferred) or ultrasound for 5 years or longer as clinically indicated [5]. However, a significant proportion of these patients have a contraindication to conventional contrast and serial CE-CT/MRI due to chronic kidney disease, nephrectomy status, contrast allergy or kidney transplants [6–8]. Although the new generation of Gadolinium agents has a better safety profile and requires smaller doses, they may still not be universally available or applicable for patients who need serial imaging during surveillance [9]. Additionally, these procedures often incur substantial cost and administrative barriers, such as preauthorizations, which occasionally present obstacles for these patients. Contrast enhanced ultrasound (CEUS), which uses stabilized gas microbubbles as a contrast agent is an ideal tool for post-ablation recurrence monitoring in this patient population. CEUS can alleviate challenges such as body habitus precluding MRI in some cases and degrading CT image quality through photon starving and higher kVp technique. CEUS like B-mode imaging has depth limitations due to attenuation [10]. Other challenges with CT and MRI include breath holding compliance leading to poor image quality, claustrophobia, and implanted devices, which may preclude MRI entirely or cause MRI or CT artifacts limiting lesion evaluation. Ultrasound contrast agents, unlike intravascular iodinated- and gadolinium-based agents, do not diffuse out of circulation, provide potential cost savings, and can be injected repeatedly to increase diagnostic confidence when necessary [11,12]. CEUS also provides better spatial and superior temporal resolution compared to MRI and CT, mitigating the occasional contrast-timing errors that occur with other modalities and providing a better visual illustration of contrast enhancement [13,14]. Specific imaging software for CEUS is commercially available across most manufacturers. This includes nonlinear imaging pulses to maximize ultrasound contrast agent signal generation and low mechanical index (MI; typically < 0.3) scanning to minimize microbubble destruction.

Fusion imaging allows for real-time and synchronous association of ultrasound images with one or more cross-sectional studies such as CT, MR, or positron emission tomography (PET), which are instantly reconstructed to fuse in the corresponding ultrasound plane. Fusion imaging can also be associated with other imaging technologies such as elastography, color Doppler and CEUS for better localization and characterization. While CEUS fusion to other imaging modalities is still experimental in renal studies, it has been widely used in the liver for both treatment guidance and post-ablation monitoring [15–20].

Our group has previously demonstrated the excellent sensitivity of CEUS for detecting RCC recurrence post-ablation [21,22]. However, the specificity was suboptimal given poor delineation of treated tumor boundaries and difficulties identifying the treatment cavity margins. Consequently, the goal of this work was to evaluate the feasibility of using post-treatment CEUS fused to a patient’s preablation CT/MR to detect RCC recurrence.

Materials and methods

As part of this institutional review board approved ongoing trial, all participants provided written informed consent to undergo a series of CEUS exams within 4 weeks of a clinically scheduled CE-CT/MRI. Standard of care surveillance imaging CE-CT/MR exams were collected at approximately 6- and 12-month intervals as part of a larger ongoing clinical trial (NCT05641935) investigating the use of CEUS for RCC recurrence screening.

The study enrolled patients with biopsy-proven RCC, aged 18 years or older, who had undergone prior treatment with either microwave ablation (MWA) or cryoablation therapy. Patients were consecutively approached and excluded if they were pregnant, terminally ill, medically unstable, or had a known allergy to components of ultrasound contrast agents. All patients were confirmed to have available MR or CT imaging prior to the ablative therapy. CEUS scans were compared with reference standard cross-sectional imaging combined with biopsy confirmation in cases of diagnosed recurrence.

In this study, scanning was performed by three trained sonographers with extensive CEUS experience using a Logiq E10 scanner (GE HealthCare, Waukesha, WI, USA) with a C1–6 probe and Lumason (Bracco Diagnostics, Monroe Township, NJ) as the ultrasound contrast agent.

Fusion imaging was performed with a magnetic console placed approximately 5–12 cm above the patient’s subxiphoid region, while the patient was in either a supine or lateral decubitus position (depending on the lesion location). The magnetic field was then used to recognize the ultrasound transducer and create 3D spatial position and orientation [23]. Digital Imaging and Communications in Medicine (DICOM) datasets of the patient’s pretreatment noncontrast CT or MRI (3 months to 7 years prior to CEUS) were retrieved directly from the Picture Archiving and Communication System (PACS) and uploaded manually onto the ultrasound scanner. Once the images were uploaded, the real-time ultrasound images and prior cross-sectional imaging could be viewed side-by-side or in an overlay mode [24]. The sonographer selected three points in the kidney that were of interest and matched each of these points to the corresponding noncontrast CT or MR images to fuse the imaging plane. Our study team found that incorporating the upper and lower margins of the kidney in a longitudinal plane instead of arbitrary upper, mid, and lower pole regions resulted in a more accurate fusion. An additional co-registration point was then added if an anatomical landmark was present in both imaging modalities. Once the ultrasound and CT/MR examinations were fused and optimized, CEUS was ready to be performed using the coded harmonic imaging contrast package on the scanner.

An intravenous catheter was placed in the patient’s upper extremity by a registered nurse for the Lumason injection. A low MI of <0.13 was used to minimize microbubble destruction during imaging. Similarly, no flash modes or destructive pulses are employed during CEUS exams. The gain settings were adjusted to minimize nonlinear signals prior to contrast injection. The focal zone was placed at or immediately below the approximate depth of the ablation cavity to maximize the generation of nonlinear signals during CEUS. With the cross-sectional imaging acquisition already fused with the ultrasound (VolumeNav, GE HealthCare), patients received a bolus of 1.0–1.6 mL of Lumason followed by 10 mL of normal saline. Real-time CEUS was performed with fused cross-sectional MR/CT. During the early phase of CEUS, the tumor midline was imaged until complete renal enhancement was observed (approximately 30 seconds post-injection), followed by imaging sweeps to evaluate the entire treatment cavity. Sweeps were acquired and imaging continued until either the onset of contrast washout in the renal parenchyma was observed or 90 seconds after the contrast injection if no definite contrast washout was observed. The ablated cavity was intermittently imaged until near complete contrast dissipation was determined 5–7 minutes after contrast injection.

To evaluate the feasibility and demonstrate proof of concept, bedside interpretation of the CEUS findings was made by the study team based on the presence of arterial phase iso- or hyper-enhancement within the ablation cavity being indicative of a recurrent tumor. These findings were compared to the cross-sectional imaging findings obtained as the standard of care.

Results

To date, 50 cases (76% male and 24% female) have been successfully enrolled and scanned. The average participant age was 70.7 ± 9.8 years. Ablative treatment of the RCC consisted of MWA (52%) or cryoablation (48%). The average time between post-treatment CE-CT/MRI (used as the reference standard) and CEUS was 9.4 ± 8.4 days. The average time between ablation and CEUS was 30.5 ± 23.1 months (range 1.2–87 months).

All participants tolerated the contrast injections with no adverse events. Contrast enhancement of the surrounding renal parenchyma was observed in all patients approximately 20–25 seconds post-injection and lasted roughly 5 minutes before full washout.

Of the examined patients, only 1 patient (1/50 patients, 2%) to date has demonstrated hyper-enhancement within the treatment cavity, indicating RCC recurrence. The recurrence was also detected on an MRI and later confirmed by pathology. The other 49 cases (49/50 patients, 98%) showed no evidence of recurrent or residual disease by CEUS which matched with the CE-CT/MRI findings. These preliminary CEUS results suggest 100% agreement among the 50 recruited patients to date in identifying RCC recurrence during post-ablation surveillance.

Fusion of real-time CEUS with the patient’s pretreatment CT/MRI was found to be feasible, albeit with varying degrees of registration alignment. Figure 1a displays a B-mode image of the ablation cavity and accurate fusion alignment of CEUS and MRI (Fig. 1b, 1c, 1d). Tracking through the region of interest following fusion demonstrated consistent and accurate fusion of both the treatment cavity and surrounding kidney. Alternatively, Figure 2 demonstrates a challenging case in which the region of interest on CEUS and CT did not correctly match. This was a failed case in which the treated tumor cavity could not be well visualized on CEUS because of artifacts from rib shadowing and scanning challenges due to the patient’s larger body habitus. Figure 3 displays examples of accurate and poor fusion alignment of CEUS and preablation MRI in two participants. In both cases, pretreatment cross-sectional imaging was obtained 3 years prior to CEUS.

Figure 1.

Figure 1.

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B-mode and fusion imaging of CEUS and a patient’s preablation MRI. (a) Displays an example B-mode image of the previously ablated cavity. (b) An example image from the arterial phase at 26 seconds post-injection showing no intratumoral enhancement. (c) Example image from the beginning of the renal washout at 2:18, and (d) Near complete renal washout at 3:21.

Figure 2.

Figure 2.

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An example of a challenging case in which the region of interest on CEUS did not correctly match the patient’s preablation CT for fusion imaging. Note, that while the tumor is visualized well on the pretreatment MRI, the ablation cavity is not well appreciated on CEUS.

Figure 3.

Figure 3.

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(a) An example of an excellent overlay of patient’s CEUS and preablation MRI from 4 years prior. (b) An example of a challenging fusion of patient’s CEUS and preablation CT three years prior.

Figure 4 presents imaging of a case of post-ablation recurrence, in a 63-year-old male participant with a history of clear cell RCC and cryoablation 3 years prior to CEUS imaging. Recurrence was detected on both CE-MRI (Fig. 4b) and CEUS (Fig. 4d, 4e, 4f, 4g) and confirmed as a recurrence by tissue sampling obtained during retreatment. While based on a very limited sample size, this study demonstrates the potential of CEUS to diagnose cases of RCC recurrence.

Figure 4.

Figure 4.

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B-mode, MRI, CT and CEUS fusion imaging of a patient with disease recurrence. (a) Displays patient’s ultrasound B-mode image of the recurrent lesion in the previously ablated location with dimensions of 3.8 cm × 2.9 cm, (b) Patient’s most recent CE-MRI displaying the recurrent lesion (c) Displays patient’s preablation CT in, which was used for fusion imaging three years later Example of CEUS with fusion acquired (d) 6 seconds post-injection, (e) 20 seconds post-injection showing the arterial phase iso-enhancement, (f) 2 minutes post-injection at the start of wash out, and (g) 2 minutes and 43 seconds post-injection showing early mild washout.

In some cases, pseudo-enhancement or delayed hypo-enhancement was observed, but this was not indicative of true RCC recurrence. Examples of this delayed enhancement are provided in Figure 5, reflecting the importance of using dynamic imaging to rule out static artifacts.

Figure 5.

Figure 5.

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Example of a well-fused case but with the potentially misleading appearance of intratumoral enhancemnt. In the case of residual or recurrent tumor, contrast enhancement is seen in the arterial phase. In this case, intratumoral enhancement was static, which indicates an artifact likely from tissue necrosis.

Discussion

This study demonstrates the feasibility of fusing post-ablation CEUS to preablation MRI/CT to improve the delineation of the tumor boundary based on 50 cases. This ongoing clinical trial plans to recruit 210 cases and if successful, may reduce the number of cross-sectional imaging exams required for RCC recurrence surveillance following percutaneous ablation. This approach is possible given the relative stability of both the normal renal parenchyma and the ablation cavity for years following treatment [25].

CEUS with and without fusion has been used in renal tumor studies mainly for renal mass classification [16,24,26–31], intervention guidance [32–35], and treatment response evaluation [36–47]. Our 100% concordance between CE-CT/MR and CEUS supports previous studies, which also reported high inter-modality concordance with CEUS after percutaneous RFA or cryoablation. Kong et al. performed paired CEUS and CE-CT 1 month after RFA in 64 RCCs to evaluate ablation success. Among 62 complete and 2 incomplete ablations, concordance between imaging modalities was 100% [44]. Similarly, Meloni et al. compared CEUS to CE-CT/MRI retrospectively in 28 RCCs after RFA and observed concordance among 27 of 28 tumors. CEUS failed to detect tumor recurrence in 1 tumor, which was noted preprocedurally to be hypovascular and minimally enhancing on CE-CT [38]. Allard et al. also found perfect concordance between CEUS and CE-CT (kappa = 1.0; p < 0.0001) with a diagnostic rate of 94.6% in post-RFA surveillance of renal tumors [39]. Their group suggested CEUS for post-ablation surveillance, should always have a pretreatment CE-CT/MR of the lesion, which is identical to our study design fusing the preablation cross-sectional imaging with CEUS.

Eisenbrey et al. studied harmonic and subharmonic CEUS for renal mass characterization and post-cryoablation treatment response in 12 tumors. Harmonic and subharmonic CEUS showed accuracies of 75% and 83%, respectively in predicting treatment outcome [21]. Zeccolini et al. also reported 100% concordance between CEUS and CE-MRI in surveillance of 25 small renal tumors treated by cryoablation [42]. In a study by Li et al., CEUS showed accuracy of 97.6% in long-term surveillance post-MWA in comparison to CT/MRI [46]. Calio et al. studied the efficacy of 2D and 3D CEUS for recurrence detection in RCC post-ablation surveillance. CEUS successfully identified all cases of recurrence by enhancement of the full ablation cavity with equal arrival times and intensities compared to the renal cortex. They mentioned that some patients with complete response to treatment developed delayed enhancement at the periphery of the ablation cavity over time, which corresponds to fat necrosis, scarring or granulation tissue within the ablation cavity. In this study, early enhancement was a criterion for recurrence of disease [22]. Chandrasekar et al. proposed fractional velocity, a metric extracted from 2D and 3D CEUS data for risk stratification and malignancy prediction of complex renal cysts [48]. Eisenbrey et al. also retrospectively investigated the long-term impact in patients with indeterminate renal masses. CEUS provided definitive diagnosis in 71.6% of cases of which 15.6% underwent surgical resection with pathology proven malignancy in 87.5% of specimens [11]. Furthermore, King et al. studied different CEUS features in subtypes of RCC and found that peak enhancement greater than that of the renal cortex and rapid time to peak intensity were indicative of clear cell RCC, while hypo-enhancement with respect to the renal cortex and slower time to peak enhancement were more characteristic of papillary RCC [49]. The pseudo-enhancement observed in few cases in our study was also reported in another CEUS study assessing the therapeutic response of RCC to radiofrequency ablation (RFA) [44]. Yet another study evaluated the frequency of false positive enhancement after RCC ablation on CE-MR and found it occurs commonly during the first month post-ablation [50]. This indicates the importance of dynamic evaluations when screening for recurrence and waiting at least 3 months before initial imaging to evaluate treatment response.

While CEUS for RCC recurrence has shown promise in these preliminary studies, limitations and challenges should be addressed. Fusion can be challenging if the ideal ultrasound scanning plane is different from the classical orthogonal CT or MR image. When there is more than one imaging modality from different time points, co-registration must be performed to fuse the imaging modalities to create a matching 3D plane. Co-registration points are placed on all corresponding images at the exact locations to fuse the imaging modalities correctly. Since the ideal ultrasound scanning plane can be difficult to achieve in all patients, our group has found that adding multiple anatomical landmarks can improve fusion. For renal fusion imaging, studies have suggested choosing anatomical landmarks such as a renal artery or vein, hilum, a simple renal cyst or even the main portal vein in the liver for fusing multiple imaging modalities. However, our group has found that the most accurate anatomical landmark for renal fusion imaging is matching the upper and lower renal poles as well as an additional anatomical landmark (such as a renal cyst or hilum). In this clinical trial, preablation cross-sectional imaging was used. This delay in imaging results in longer intervals between the preablation CT/MRI and follow-up CT/MRI imaging (time of the CEUS examination), which may make co-registration using anatomical landmarks more challenging (for example, 7 years passed between post-treatment CEUS and preablation imaging for 2 of the cases in this study). Moreover, breathing and displacement of the abdominal structures due to previous abdominal surgeries or pressure from the ultrasound probe can affect the process of registration. CEUS, like conventional ultrasound imaging, is limited in obese patients as demonstrated in one case in this study (Fig. 2) [51]. Moreover, the efficacy of CEUS in deep sitting and hypovascular tumors needs future studies [38,39]. A crucial aspect of interpreting CEUS imaging is the recognition of artifacts and artifactual enhancement. Techniques such as destruction-replenishment may help differentiate true lesion enhancement from calcifications or fat in the ablated cavity. Adjusting the patient’s position and optimizing the acoustic window can also reduce the transducer-to-target distance, helping to eliminate intervening enhancing structures and mitigate these artifacts. Moreover, true enhancement will display dynamically moving microbubbles, while pseudo-enhancement will present stationary microbubbles [52].

Lastly, this study was designed to calculate inter-modality agreement between CEUS and CE-CT/MR, but not other test characteristics such as sensitivity, specificity, and positive or negative predictive values. We cannot definitively rule out false negative results among CEUS and CE-CT/MR, since renal biopsy was not performed in patients with negative CE-CT/MR. Also, histopathology confirmed RCC recurrence in one patient with arterial enhancement, excluding the possibility of false positive results from either modality.

CEUS is a cost-effective and safe imaging modality for detecting recurrent or residual RCC following percutaneous ablation. The role of renal CEUS has previously demonstrated important cost-savings and direct benefit to patient management in several retrospective studies [11,12]. Additionally, CEUS provides improved temporal and spatial resolution, and no concerns of nephrotoxicity. However, it is not suitable for whole-body imaging and may not be ideal for surveillance of new tumors, suggesting an optimal surveillance strategy could include alternating modalities. Our future studies from this ongoing clinical trial will include a larger sample size with an extended follow-up period and readings of both modalities to fully evaluate these approaches.

Conclusion

Initial results demonstrate the feasibility of using post-treatment CEUS fused with pretreatment CT/MRI for monitoring RCC recurrence post-ablation. Preliminary results show complete concordance between CEUS and CE-CT/MRI for detecting RCC recurrence following percutaneous ablation and fusion with pretreatment CT/MRI was found to be useful for correct localization of the prior tumor boundaries on CEUS.

Acknowledgments

The authors would like to thank Kristen Bradigan for her continuous nursing and coordinator support throughout the project. Grant support R01 CA269750. Equipment support from GE HealthCare. Drug support from Bracco.

Conflict of interest

CEW is a consultant for Bracco, SonoSim and Speaking bureau for Canon Medical Systems USA. JRE received Grant, equipment and drug support from GE HealthCare; Drug support from Bracco; Equipment support from Siemens; Drug support and member of scientific advisory board of Lantheus Medical Imaging. Royalties from Elsevier; Consultant for SonoSim. FF received Equipment loan and/or grant support from The Butterfly Network, Canon Medical Systems USA, GE HealthCare, and Siemens Healthineers; Contrast agent from Bracco Diagnostics, GE HealthCare and Lantheus Medical Imaging; Advisory Board/Consultant/Author for Elsevier, Exact Therapeutics AS, GE HealthCare, Lantheus Medical Imaging, Longeviti Neuro Solutions, and SonoThera. AL is GE Healthcare advisory Board Member; has a Consulting agreement and Research support; Bracco Diagnostic—Advisory Board Member, Consulting agreement, and Research support, and received royalties from Elsevier. The rest of authors declare no conflict of interests.

Data availability statement

All data are available upon request.

References

  • [1].Capitanio U, Bensalah K, Bex A, Boorjian SA, Bray F, Coleman J, et al. Epidemiology of renal cell carcinoma. Eur Urol 2019;75(1):74–84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [2].Atkins MB, El Bakouny Z, Choueiri TK. UpToDate. Epidemiology, pathology, and pathogenesis of renal cell carcinoma. 2024. [accessed 15.01.25]. https://www.upto-date.com/contents/epidemiology-pathology-and-pathogenesis-of-renal-cell-carci-noma.
  • [3].Campbell SC, Clark PE, Chang SS, Karam JA, Souter L, Uzzo RG. Renal mass and localized renal cancer: evaluation, management, and follow-up: AUA guideline: part I. J Urol 2021;206(2):199–208. [DOI] [PubMed] [Google Scholar]
  • [4].Campbell SC, Uzzo RG, Karam JA, Chang SS, Clark PE, Souter L. Renal mass and localized renal cancer: evaluation, management, and follow-up: AUA guideline: part II. J Urol 2021;206(2):209–18. [DOI] [PubMed] [Google Scholar]
  • [5].Expert Panel on Urological I, Purysko AS, Nikolaidis P, Dogra VS, Ganeshan D, Gore JL, et al. ACR appropriateness criteria(R) post-treatment follow-up and active surveillance of clinically localized renal cell cancer. J Am Coll Radiol 2019;16(11S): S399–416. [DOI] [PubMed] [Google Scholar]
  • [6].Abbas FM, Julie BM, Sharma A, Halawa A. “Contrast nephropathy” in renal transplantation: Is it real? World J Transplant 2016;6(4):682–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [7].Abu Jawdeh BG, Leonard AC, Sharma Y, Katipally S, Shields AR, Alloway RR, et al. Contrast-induced nephropathy in renal transplant recipients: a single center experience. Front Med (Lausanne) 2017;4:64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [8].Davenport MS, Perazella MA, Yee J, Dillman JR, Fine D, McDonald RJ, et al. Use of intravenous iodinated contrast media in patients with kidney disease: consensus statements from the American College of Radiology and the National Kidney Foundation. Radiology. 2020;294(3):660–8. [DOI] [PubMed] [Google Scholar]
  • [9].Bashir MR, Thomas KL. A new generation of gadolinium-based MRI contrast agents: higher relaxivity, lower dose. Radiology 2023;308(1):e231454. [DOI] [PubMed] [Google Scholar]
  • [10].Fetzer DT, Vijay K, Caserta MP, Patterson-Lachowicz A, Dahiya N, Rodgers SK. Artifacts and technical considerations at contrast-enhanced US. Radiographics 2023;43 (2):e220093. [DOI] [PubMed] [Google Scholar]
  • [11].Eisenbrey JR, Kamaya A, Gummadi S, Bird K, Burrowes D, Arias D, et al. Effects of contrast-enhanced ultrasound of indeterminate renal masses on patient clinical management: retrospective analysis from 2 institutions. J Ultrasound Med 2021;40 (1):131–9. [DOI] [PubMed] [Google Scholar]
  • [12].Streb JW, Tchelepi H, Malhi H, Deurdulian C, Grant EG. Retrospective analysis of contrast-enhanced ultrasonography effectiveness in reducing time to diagnosis and imaging-related expenditures at a single large United States County Hospital. Ultrasound Q 2019;35(2):99–102. [DOI] [PubMed] [Google Scholar]
  • [13].Velasquez-Botero FBA, Tang Y, Lu Q, Liu JB, Eisenbrey JR. Renal contrast-enhanced ultrasound: clinical applications and emerging research. Advanced Ultrasound in Diagnosis and Therapy 2022;6(4):129–46. [Google Scholar]
  • [14].Kuon Yeng Escalante CM, Siu Xiao T, Nagaraj RU, Savsani E, Mohammed A, Li J, et al. Evaluation of the contrast-enhanced ultrasound nonradiation treatment response assessment LI-RADS v2024 using data from a multi-center transarterial chemoembolization study. Acad Radiol 2024;31(12):5078–86. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [15].Savsani E, Shaw CM, Forsberg F, Wessner CE, Lyshchik A, O’Kane P, et al. Contrast-enhanced US evaluation of hepatocellular carcinoma response to chemoembolization: a prospective multicenter trial. Radiology 2023;309(1):e230727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [16].Schwarze V, Rubenthaler J, Marschner C, Fabritius MP, Rueckel J, Fink N, et al. Advanced fusion imaging and contrast-enhanced imaging (CT/MRI-CEUS) in oncology. Cancers (Basel) 2020;12(10). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Nam K, Stanczak M, Lyshchik A, Machado P, Kono Y, Forsberg F, et al. Evaluation of hepatocellular carcinoma transarterial chemoembolization using quantitative analysis of 2D and 3D real-time contrast enhanced ultrasound. Biomed Phys Eng Express 2018;4(3):035039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [18].Lu MD, Yu XL, Li AH, Jiang TA, Chen MH, Zhao BZ, et al. Comparison of contrast enhanced ultrasound and contrast enhanced CT or MRI in monitoring percutaneous thermal ablation procedure in patients with hepatocellular carcinoma: a multi-center study in China. Ultrasound Med Biol 2007;33(11):1736–49. [DOI] [PubMed] [Google Scholar]
  • [19].Morimoto M, Nozawa A, Numata K, Shirato K, Sugimori K, Kokawa A, et al. Evaluation using contrast-enhanced harmonic gray scale sonography after radio frequency ablation of small hepatocellular carcinoma: sonographic-histopathologic correlation. J Ultrasound Med 2005;24(3):273–83. [DOI] [PubMed] [Google Scholar]
  • [20].Meloni MF, Andreano A, Franza E, Passamonti M, Lazzaroni S. Contrast enhanced ultrasound: should it play a role in immediate evaluation of liver tumors following thermal ablation? Eur J Radiol 2012;81(8):e897–902. [DOI] [PubMed] [Google Scholar]
  • [21].Eisenbrey JR, Shaw CM, Lyshchik A, Machado P, Lallas CD, Trabulsi EJ, et al. Contrast-enhanced subharmonic and harmonic ultrasound of renal masses undergoing percutaneous cryoablation. Acad Radiol 2015;22(7):820–6. [DOI] [PubMed] [Google Scholar]
  • [22].Calio BP, Lyshchik A, Li J, Stanczak M, Shaw CM, Adamo R, et al. Long term surveillance of renal cell carcinoma recurrence following ablation using 2D and 3D contrast-enhanced ultrasound. Urology 2018;121:189–96. [DOI] [PubMed] [Google Scholar]
  • [23].European Society of R Abdominal applications of ultrasound fusion imaging technique: liver, kidney, and pancreas. Insights Imaging 2019;10(1):6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [24].Rubenthaler J, Paprottka KJ, Marcon J, Reiser M, Clevert DA. MRI and contrast enhanced ultrasound (CEUS) image fusion of renal lesions. Clin Hemorheol Microcirc 2016;64(3):457–66. [DOI] [PubMed] [Google Scholar]
  • [25].Davenport MS, Caoili EM, Cohan RH, Ellis JH, Higgins EJ, Willatt J, et al. MRI and CT characteristics of successfully ablated renal masses: Imaging surveillance after radiofrequency ablation. AJR Am J Roentgenol 2009;192(6):1571–8. [DOI] [PubMed] [Google Scholar]
  • [26].Auer T, Heidegger I, DEZ T, Junker D, Jaschke W, Steinkohl F, et al. Fusion imaging of contrast-enhanced ultrasound with CT or MRI for kidney lesions. In Vivo 2019;33 (1):203–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [27].Rubenthaler J, Wilson S, Clevert DA. Multislice computed tomography/contrast-enhanced ultrasound image fusion as a tool for evaluating unclear renal cysts. Ultrasonography 2019;38(2):181–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [28].Zarzour JG, Lockhart ME, West J, Turner E, Jackson BE, Thomas JV, et al. Contrast-enhanced ultrasound classification of previously indeterminate renal lesions. J Ultrasound Med 2017;36(9):1819–27. [DOI] [PubMed] [Google Scholar]
  • [29].Barr RG, Peterson C, Hindi A. Evaluation of indeterminate renal masses with contrast-enhanced US: a diagnostic performance study. Radiology 2014;271 (1):133–42. [DOI] [PubMed] [Google Scholar]
  • [30].Ignee A, Straub B, Brix D, Schuessler G, Ott M, Dietrich CF. The value of contrast enhanced ultrasound (CEUS) in the characterisation of patients with renal masses. Clin Hemorheol Microcirc 2010;46(4):275–90. [DOI] [PubMed] [Google Scholar]
  • [31].Helck A, D’Anastasi M, Notohamiprodjo M, Thieme S, Sommer W, Reiser M, et al. Multimodality imaging using ultrasound image fusion in renal lesions. Clin Hemorheol Microcirc 2012;50(1–2):79–89. [DOI] [PubMed] [Google Scholar]
  • [32].Carrafiello G, Mangini M, Fontana F, Recaldini C, Piacentino F, Pellegrino C, et al. Single-antenna microwave ablation under contrast-enhanced ultrasound guidance for treatment of small renal cell carcinoma: preliminary experience. Cardiovasc Intervent Radiol 2010;33(2):367–74. [DOI] [PubMed] [Google Scholar]
  • [33].Amalou H, Wood BJ. Multimodality fusion with MRI, CT, and ultrasound contrast for ablation of renal cell carcinoma. Case Rep Urol 2012;2012:390912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [34].Chen Y, Huang J, Xia L, Dong B, Chen W, Xue W, et al. Monitoring laparoscopic radiofrequency renal lesions in real time using contrast-enhanced ultrasonography: an open-label, randomized, comparative pilot trial. J Endourol 2013;27 (6):697–704. [DOI] [PubMed] [Google Scholar]
  • [35].Zhao X, Wang W, Zhang S, Liu J, Zhang F, Ji C, et al. Improved outcome of percutaneous radiofrequency ablation in renal cell carcinoma: a retrospective study of intraoperative contrast-enhanced ultrasonography in 73 patients. Abdom Imaging 2012;37(5):885–91. [DOI] [PubMed] [Google Scholar]
  • [36].Sanz E, Hevia V, Arias F, Fabuel JJ, Alvarez S, Rodriguez-Patron R, et al. Contrast-enhanced ultrasound (CEUS): an excellent tool in the follow-up of small renal masses treated with cryoablation. Curr Urol Rep 2015;16(1):469. [DOI] [PubMed] [Google Scholar]
  • [37].Guo F, Hu B, Chen L, Li J. Clinical application of contrast-enhanced ultrasound after percutaneous renal tumor ablation. Br J Radiol 2019;92(1103):20190183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [38].Meloni MF, Bertolotto M, Alberzoni C, Lazzaroni S, Filice C, Livraghi T, et al. Follow-up after percutaneous radiofrequency ablation of renal cell carcinoma: contrast-enhanced sonography versus contrast-enhanced CT or MRI. AJR Am J Roentgenol 2008;191(4):1233–8. [DOI] [PubMed] [Google Scholar]
  • [39].Allard CB, Coret A, Dason S, Tajzler C, Shayegan B, Matsumoto ED, et al. Contrast-enhanced ultrasonography for surveillance of radiofrequency-ablated renal tumors: a prospective, radiologist-blinded pilot study. Urology 2015;86(6):1174–8. [DOI] [PubMed] [Google Scholar]
  • [40].Garbajs M, Popovic P. Contrast-enhanced ultrasound for assessment of therapeutic response after percutaneous radiofrequency ablation of small renal tumors. J BUON 2016;21(3):685–90. [PubMed] [Google Scholar]
  • [41].Barwari K, Wijkstra H, van Delden OM, de la Rosette JJ, Laguna MP. Contrast-enhanced ultrasound for the evaluation of the cryolesion after laparoscopic renal cryoablation: an initial report. J Endourol 2013;27(4):402–7. [DOI] [PubMed] [Google Scholar]
  • [42].Zeccolini G, Del Biondo D, Cicero C, Casarin A, Guarise A, Celia A. Comparison of Contrast-Enhanced Ultrasound Scan (CEUS) and MRI in the follow-up of cryoablation for small renal tumors. Experience on 25 cases. Urologia 2014;81(Suppl 23):S1–8. [DOI] [PubMed] [Google Scholar]
  • [43].Hoeffel C, Pousset M, Timsit MO, Elie C, Mejean A, Merran S, et al. Radiofrequency ablation of renal tumours: diagnostic accuracy of contrast-enhanced ultrasound for early detection of residual tumour. Eur Radiol 2010;20(8):1812–21. [DOI] [PubMed] [Google Scholar]
  • [44].Kong WT, Zhang WW, Guo HQ, Qiu JL, Tang M, Jiang ZM, et al. Application of contrast-enhanced ultrasonography after radiofrequency ablation for renal cell carcinoma: is it sufficient for assessment of therapeutic response? Abdom Imaging 2011;36(3):342–7. [DOI] [PubMed] [Google Scholar]
  • [45].Wink MH, Lagerveld BW, Laguna MP, de la Rosette JJ, Wijkstra H. Cryotherapy for renal-cell cancer: diagnosis, treatment, and contrast-enhanced ultrasonography for follow-up. J Endourol 2006;20(7):456–8. [DOI] [PubMed] [Google Scholar]
  • [46].Li X, Liang P, Yu J, Yu XL, Liu FY, Cheng ZG, et al. Role of contrast-enhanced ultrasound in evaluating the efficiency of ultrasound guided percutaneous microwave ablation in patients with renal cell carcinoma. Radiol Oncol 2013;47(4):398–404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [47].Zhu Q, Shimizu T, Endo H, Kodama Y, Abo D, Miyasaka K. Assessment of renal cell carcinoma after cryoablation using contrast-enhanced gray-scale ultrasound: a case series. Clin Imaging 2005;29(2):102–8. [DOI] [PubMed] [Google Scholar]
  • [48].Chandrasekar T, Clark CB, Gomella A, Wessner CE, Wang S, Nam K, et al. Volumetric quantitative contrast-enhanced ultrasonography evaluation of complex renal cysts: an adjunctive metric to the Bosniak classification system to predict malignancy. Eur Urol Focus 2023;9(2):336–44. [DOI] [PubMed] [Google Scholar]
  • [49].King KG, Gulati M, Malhi H, Hwang D, Gill IS, Cheng PM, et al. Quantitative assessment of solid renal masses by contrast-enhanced ultrasound with time-intensity curves: how we do it. Abdom Imaging 2015;40(7):2461–71. [DOI] [PubMed] [Google Scholar]
  • [50].Takaki H, Nakatsuka A, Cornelis F, Yamanaka T, Hasegawa T, Sakuma H, et al. False-positive tumor enhancement after cryoablation of renal cell carcinoma: a prospective study. AJR Am J Roentgenol 2016;206(2):332–9. [DOI] [PubMed] [Google Scholar]
  • [51].Setola SV, Catalano O, Sandomenico F, Siani A. Contrast-enhanced sonography of the kidney. Abdom Imaging 2007;32(1):21–8. [DOI] [PubMed] [Google Scholar]
  • [52].Elbanna KY, Krishna S, Finelli A, Atri M. Contrast-enhanced ultrasound of the indeterminate renal mass, from the AJR “how we do it” special series. AJR Am J Roentgenol 2024;223(6):e2430817. [DOI] [PubMed] [Google Scholar]

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