Contrast-enhanced ultrasound (CEUS) in renal imaging at an interdisciplinary ultrasound centre: Possibilities of dynamic microvascularisation and perfusion

Abstract

OBJECTIVE: To identify the indications for CEUS in renal imaging in an interdisciplinary ultrasound department.

METHODS: 102 CEUS examinations of the kidney in 82 patients between September 2014 and July 2016 were analysed regarding the indication for ultrasound. CEUS was performed by one experienced sonographer agent after bolus injection of 1.0 up to 2.4 ml sulphur hexafluoride microbubbles using multifrequency probes with Contrast Harmonic imaging.

RESULTS: CEUS of the kidney was performed in patients from 20 to 87 years. 44% of the patients had a stage 3 of chronic kidney disease and higher 38% of the patients had undergone a renal transplantation. No adverse events were observed. 54% of examinations were requested by nephrologists. The remaining by surgeons, oncologists or gastroenterologists. In 47% the objectives were the evaluation of complex renal cysts, in 31% the analysis of kidney perfusion, in 19% the assessment of solid renal masses. The remaining were perirenal tumours (2%) and infection (1%).

CONCLUSIONS: CEUS is a good diagnostic alternative for patients with impaired renal function, complicated cysts, infections, solid renal lesions and after renal transplant.

Keywords

CEUS kidney interdisciplinary ultrasound department imaging possibilities

1 Introduction

In nephrology, ultrasound diagnostics plays an important role as the method of further investigation following the initial examination. It is used to detect pathologies as well as to assess restriction of renal function based on morphologic criteria. As first line imaging, ultrasound is indispensable in many cases. The additional use of Colour Coded Doppler Sonography (CCDS) and Power Doppler Sonography (PD) provides important information on many diseases, especially in the evaluation of perfusion. Nevertheless, conventional ultrasound (digital methods and Colour Coded Doppler Ultrasound) has its limits, and further diagnostics are often necessary.

In kidney imaging, contrast enhanced ultrasound (CEUS) plays an increasing role. In the DEGUM study, the role of CEUS in the assessment of liver tumours was put on the same level with CT and MRI. Therefore, CEUS was recommended as the first additional modality for clarifying an unidentified liver mass [1, 2].

According to the current EFSUMB guidelines [3], CEUS is used increasingly in kidney imaging in our interdisciplinary ultrasound department at the University Hospital of Regensburg. The “kidney imaging” team consists of experienced sonographers and nephrologists. Initially, primary indications were mainly the assessment of simple and complicated renal cysts. Using CEUS successfully for many cases in our ultrasound centre (e.g. free flaps, liver lesions, thyroid tumour) [4 –8], indications were quickly expanded to include more complex cases. As the centre deals with many transplant cases, the assessment of kidney transplants has become more important.

The aim of this study is to determine the status of CEUS in kidney imaging and to describe the diagnostic value of CEUS in preselected cases of patients with suspicious renal findings in ultrasound evaluation by experienced nephrologists.

2 Material and methods

In this study, all CEUS examinations of the kidney in our interdisciplinary ultrasound department at the University Hospital of Regensburg between September 2014 and July 2016 were analysed. Patients were admitted by all departments of the University Hospital of Regensburg for CEUS with the Ethical board permission of the University Hospital. Ultrasound examinations were performed by an experienced radiologist (more than 5000 ultrasound examinations per year) and a nephrologist. The examination was performed independently. In cases of disagreements in terms of a common final judgment, additional analyses were performed together. Each examination was performed using high-resolution multifrequency convex probes (1–5 MHz, 1–6 MHz). B-Mode images, CCDS and PD were performed and stored in an analyzable format before CEUS.

After given written informed consent, patients received a peripheral venous bolus injection of 1.0–2.4 ml of ultrasound contrast agent (sulphur hexafluoride microbubbles, SonoVue^®, Bracco, Italy) followed by a 10 ml saline flush. The mechanical index was adjusted to values <0.2, which enabled the “low MI-technique” Contrast Harmonic Imaging of CEUS [3, 9]. Raw images were stored digitally as loops from early wash-in to the late wash-out time in PACS (DICOM format). Perfusion time intensity curve (TIC) analysis [8] was performed using the integrated computer workstation (LOGIQ E9, GE). Clinical and biochemical data were retrieved from a clinical database. Data collection was permitted by the ethical review committee of the University Hospital of Regensburg.

3 Results

In all 82 patients (102 cases), image quality was high enough for independent reading of US and CEUS. In 51 cases the ultrasound conditions were rated as complicated, due to meteorism in 32 cases and/or obesity in 26 cases (BMI >30). The average age was 57.9±13.6 years (20 to 87 years). The majority were men (62.4% –64 cases). There were no patients with contrast agent incompatibility. The average quantity of contrast agent used was 1.7±0.4 ml (1.0 to 2.4 ml). No patient needed multiple applications. There were no adverse reactions to the ultrasound contrast agent application. The proportion of cases of patients with kidney transplants was 38.2% (39 cases). In 75.2% (78 cases) the pathology was found in the native kidney, in 23.5% (24 cases) in the transplanted kidney. On average CEUS was performed after 5.4 years after transplantation (14 days up to 19 years) (Table 1).

Table 1
Baseline characteristics: Patient characterization of all cases undergoing CEUS at an interdisciplinary ultrasound centre between September 2014 and July 2016

Men (%) 62.7

Age (years) 58.0±13.6

Kidney transplantation (%) 38.2

Median creatinine (mg/ml) 2.14±2.25

Median GFR (CKD-EPI, ml/min/1,73 m²) 56.8±32.9

Stage of chronic kidney disease (n/%)

- Stadium 1 20 (19.6)

- Stadium 2 24 (23.5)

- Stadium 3 22 (21.6)

- Stadium 4 12 (11.8)

- Stadium 5 11 (10.8)

In 52.9% (54 cases) of the cases CEUS of the kidney was requested by nephrologists, in other cases by specialists of the surgery department (14.7% –15 cases), gastroenterology (6.9% –7 cases), oncology (4.9% –5 cases) and in 20.6% (21 cases) by other departments. Outpatient treatments comprised 49.0% of the cases and 51.0% were treated in hospital. 4 examinations were performed at the intensive care unit.

In 70 cases (68.6%) CEUS was the first examination following previous ultrasound diagnostics, in 32 cases (31.4%) CEUS served as confirmatory diagnostics after previous CT or MRI.

The patients’ renal function was assessed on the basis of creatinine concentration and glomerular filtration rate, GFR (CKD-EPI). In all cases laboratory findings were available. The mean creatinine was 2.14±2.25 mg/dl, the mean GFR was 56.8±32.9 ml/min/1.73 m². 44% of patients had a stage 3 of chronic kidney disease and higher (Fig. 1).

Fig.1

Kidney function of patients undergoing CEUS imaging: Kidney function of patients was assessed on the basis of creatinine and GFR (CKD-EPI). The mean creatinine was 2.14±2.25 mg/dl, the mean GFR was 56.8±32.9 ml/min/1.73 m². 44% of patients had a stage 3 of chronic kidney disease and higher.

The objective in 49 cases (47%) was to use CEUS to evaluate cysts, in 20 cases (19%) to investigate a suspected solid tumour, in 32 cases (31%) to clarifying a perfusion deficit or a suspected inflammatory event in one case (1%), in two cases (2%) the task was to assess a perirenal mass.

The evaluated cysts were classified according to the Bosniak classification of renal cysts [10 –12]. The median size of the evaluated cysts was 21.1±11.8 mm (9 mm to 60 mm). No cysts of category I were evaluated with CEUS, Bosniak cysts of category II were found in 8 cases. Most cysts were classified as category IIF (32 cases, Fig. 2). In 6 cases cysts were distributed to group III, category IV was described in 3 cases. Because of the high rate of malignancy in categories III and IV, patients were recommended to undergo invasive evaluation (Fig. 3).

Fig.2

Renal cysts (Bosniak I and IIF): A) Subcapsular renal cyst of a 69-year-old patient in B-Mode ultrasound image (white arrow) and CEUS perfusion imaging of same patient (black arrow). The cyst shows no septa, calcifications or enhancement of the walls. (Bosniak I). B) B-Mode ultrasound image (white arrow) of a 70-year-old patient. The correspondent CEUS perfusion image reveals more thin septa and small nods, which are hidden in the B-Mode ultrasound image (Bosniak IIF).

Fig.3

Renal cyst (Bosniak IV): A) 67-year-old patient with autosomal-dominant polycystic kidney disease, the B-Mode ultrasound revealed a suspect renal cyst with solid masses (white arrow). B) CEUS perfusion imaging of correspondent cyst reveals enhancement of the solid masses (white arrow –Bosniak IV). C) MRI-image of the suspect cyst. After nephrectomy, a papillary renal cell carcinoma was confirmed by pathology.

A solid tumour could be detected in 19 cases. The median size was 25.5±14.7 mm (8 to 60 mm). CEUS classified 12 lesions as malignant, 6 as benign and 1 lesion remained unclear.

Histology could be retrieved in 10 cases of suspicious lesions (cysts or solid renal masses). Thereby 5 renal cell carcinomas (RCC) were found (3 cases of clear cell renal cell carcinoma, 1 case of a papillary renal cell carcinoma, 1 not classified renal cell carcinoma). In 1 case an oncocytoma was found, in 1 case a biopsy revealed no suspicious cells. 1 angiomyolipoma was diagnosed in a tumour with partial hyperperfusion in the arterial phase and without wash-out in the latephase.

The evaluation of the renal perfusion was requested in 32 cases. The identification of renal infarction and the evaluation of a hypoperfusion was the issue in 21 cases, the assessment of arterio-venous fistula was requested in 4 cases, and the confirmation of an arterial renal transplant stenosis was the aim in 3 cases.

Most of the performed examinations represent the first diagnostic test following previous ultrasound (70,6% –72 cases). In 29.4% of the cases (30 cases), CEUS represents the confirmatory diagnostics following previous complementary imaging. The requested objectives could be answered in all cases. In 24.5% (25 cases) of the cases, the sonographer recommended further diagnostics (MRI in 7 cases, urological evaluation in 16 cases, both in 2 cases) to confirm the findings from CEUS.

4 Discussion

In the diagnosis of liver lesions, CEUS has become important, both scientifically and in daily practice. Patients of all ages are examined with CEUS. There are no relevant limitations for older patients or critically ill patients, and the permission for CEUS is also given for children by the FDA. In Europe, the ultrasound contrast-media injection in children is still off label use, but described in the non-hepatic guidelines [3 , 14].

Using CEUS in renal imaging has many important advantages: due to the fact that the equipment required for the procedure is less complex, experienced examiners can offer a safe diagnostic method that can be applied anywhere, e.g. in the setting of an intensive care unit. Patients are not exposed to radiation or put at risk by nephrotoxic contrast agents and their many side effects, e.g. impairment of renal perfusion [15] or the risk of a nephrogenic systemic fibrosis [16].

56% of the patients showed a normal or mild impairment in renal function (stadium I/II). A major proportion (up to 44%) suffered from an impairment of GFR below 60 ml/min/1,73 m². Therefore, the use of contrast media containing iodine or gadolinium was highly limited [16, 17]. This restricts the available diagnostic tests and opens an avenue for CEUS, which can be safely used with only minor side effects [18].

In our study, cysts were mainly detected via conventional ultrasound examinations and for the tumour’s assessment to differentiate malignant from benign tumours, the patients were transferred to our centre for the CEUS examination. Renal cysts were found, not only in native kidneys but also in transplanted kidneys. Here CEUS can provide additional information if solid lesions and cysts present equivocal (Fig. 2A).

Another objective is the assessment of complicated renal cysts to differentiate malignant from benign cysts (n = 49). The Bosniak classification system, originally developed in 1986 for CT-examinations and modified in 1993 [10, 11], serves to classify cystic lesions in CEUS. The differentiation is made by assessing the cysts in terms of quantity, thickness and enhancement of walls and septations [19, 20]. In the sample group, we examined, it appears that the cyst stages assessed according to the Bosniak system (determined in CT/MRI), were classified “higher” via the CEUS method. (Fig. 2B) This is often traced back to the fact that even the smallest septa can be assessed in terms of perfusion via CEUS [20 –25]. In a recent publication, Rübenthaler et al. recommend using CEUS as a full-value alternative to CT and MRI (Fig. 3) [12, 25].

The diagnosis of a renal tumour that appears to be solid, is frequently the objective of a nephrological ultrasound (n = 20). The diagnostic qualities of CEUS in terms of liver tumours have been evaluated in several multicentre studies [1 , 27]. CCDS and PD have limited sensitivity, especially in the case of obese patients [28, 29]. Here, CEUS provides important diagnostic information [30], also in case of pseudotumour [31].

The differentiation between renal cell carcinoma (RCC) and various other benign entities is difficult. Angiomyolipomas for instance, usually show a hyper echogenic signal due to the high fat content (6 cases) can, however, they can appear to be low in fat, making the differentiation more difficult. The tumour diagnostics for RCC are likewise difficult as there are mixed forms (e.g. hypovascular malignant renal lesions such as papillary RCCs and lipid-poor AMLs). This difficulty has also been confirmed in the case of differentiation of solid renal tumours due to “overlapping features” [32]. The application of perfusion analysis may provide another tool for differentiating precisely between benign and malignant masses [33, 34].

The second most common objective was the diagnosis of perfusion deficit (32 cases). In our centre, it was predominantly requested in the case of transplanted kidneys. In terms of renal infarctions, the CT contrast agent was the “golden standard” [35]. However, in the frequent cases of limited renal function, it cannot be performed. The B-image sonography alone is not appropriate for detecting infarcts [35], Doppler methods have only limited use due to poor sensitivity at low velocities and amplitudes [36]. Further restrictions for the Doppler sonography include decreased sensitivity due to certain assess angles [37] as well as the limited possibility of assessing in cases of overlying intestinal gas or deep organ location [36 , 39]. In 17 cases CEUS represents an effective and reproducible method for detecting acute renal infarcts like Bertolotto et al. described in their publication [40]. In our examinations, infarcts diagnosed via CT were confirmed in 100% via CEUS. In the case of an emergency, this method was used on intensive care unit at the patient’s bedside (4 cases).

The occurrence of AV fistulas is often a secondary finding after renal biopsies [41, 42]. Due to the high rate of spontaneous obstruction, it is clinically not relevant. Occasionally, there are persistent or also progredient findings, in which case the impairment of renal function needs to beassessed.

Another diagnostic procedure for CEUS in the transplant centre was the assessment of renal transplant artery stenosis (3 cases). Often asymptomatic, but sometimes a newly occurred arterial hypertonia is one of most common diseases. According to literature, the CCDS shows a sensitivity of 67–100% and specificity of 66–100%, so the conventional ultrasound plays the biggest role in initial diagnostics [43]. The cause for circulatory disorders can be manifold and it is difficult to differentiate them in the CCDS. Besides anastomoses stenosis (1 case) or dissections (2 cases) of the transplant artery, another cause is also kink stenosis (1 case) that is a result of the renal transplant’s location in the body (Fig. 4). CEUS can provide visual material that can be helpful for further planning of a revision operation or intervention.

Fig.4

Causes for kidney transplant arterial stenosis: A) CEUS renal perfusion imaging of a kidney transplant of a 29-year-old patient with a renal arterial stenosis due to kinking. B) CEUS renal perfusion imaging of a kidney transplant stenosis due to stenosis of the anastomosis in a 51-year-old patient.

Sonography of a transplanted kidney performed immediately after surgery can show reduced perfusion in the CCDS of deeper-lying organ parts and can falsely indicate a hypoperfusion. The contrast agent sonography is crucial in the assessment of renal transplants. It is an easy and uncomplicated examination that can be done anytime at the patient’s bedside, or in an intensive care ward. For examinations, taking place immediately after kidney transplantation, the absence of nephrotoxicity makes CEUS an important tool in cases where problems were detected by conventionalultrasound.

5 Conclusion

Due to progressive deterioration in renal function, many patients cannot receive imaging involving contrast agents containing iodine or gadolinium. CEUS closes this diagnostic gap and is, therefore, recommended for different indications by current EFSUMB guidelines. CEUS provides a valuable addition to the diagnostic spectrum in terms of renal imaging when performed by an experienced examiner.

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Men (%)	62.7
Age (years)	58.0±13.6
Kidney transplantation (%)	38.2
Median creatinine (mg/ml)	2.14±2.25
Median GFR (CKD-EPI, ml/min/1,73 m²)	56.8±32.9
Stage of chronic kidney disease (n/%)
- Stadium 1	20 (19.6)
- Stadium 2	24 (23.5)
- Stadium 3	22 (21.6)
- Stadium 4	12 (11.8)
- Stadium 5	11 (10.8)