Paul S. Sidhu, MRCP

Ultrasound is often the preliminary investigation for many diseases affecting the kidney. The examination is safe, inexpensive, and widely available. Most investigators will refer the patient for CT or MRI if a focal abnormality is found. Contrast-enhanced ultrasound, however, may be a feasible alternative as a problem-solving tool when suspected renal pathology is found.

Contrast-enhanced ultrasound has become established in routine clinical practice for liver disease and its use is expanding into other areas. Published guidelines are available on the modality’s use for the characterization of focal liver lesions as well as its role in other intra-abdominal organs, including the kidney.

This imaging method offers several practical advantages. Ultrasound contrast agents are simple to use and are well tolerated by patients.

 Real-time imaging often allows a diagnosis to be made promptly. No ionizing radiation is involved, there is no risk of patients suffering claustrophobia, and the cost of the examination is lower than that for CT or MRI. Contrast-enhanced ultrasound may also provide supplementary information not evident on other modalities.

Ultrasound contrast agents consist of air or perfluorocarbon gas microbubbles that are stabilized by a protein, lipid, or polymer shell. The microbubbles typically measure less than 7 ìm in diameter, making them small enough to cross capillary beds but too large to enter interstitial fluid. These properties enable the microbubbles to serve as blood pool agents.

Microbubble contrast agents survive passage through the cardiopulmonary circulation and typically remain in the vascular compartment for six to eight minutes after intravenous injection. This stability allows sufficient time for imaging. The principal agent used in Europe is SonoVue (Bracco), which is composed of a sulfur hexafluoride gas with a phospholipid shell. The microbubbles are metabolized by the liver and the gas is exhaled via the lungs. Other available agents include Definity (Bristol-Myers Squibb), composed of octafluoropropane gas encapsulated in an outer lipid shell, and Optison (GE Healthcare), which has an albumin shell and an octafluoropropane gas core.

We use SonoVue for our contrast-enhanced renal ultrasound work. The microbubbles are administered in a suspension of saline which, once prepared, remains stable for several hours. An adult patient will typically receive 2.4 mL of the microbubble/saline solution, injected manually through an arm vein. This is followed by a 5 to 10 mL saline flush. Further doses of 2.4 mL may be administered as required, and there is no recommended maximum dose. In a phase I study, doses of up to 56 mL of SonoVue were administered to normal volunteers without adverse events, and no signs or symptoms of overdose have been identified to date. Although we have experience using contrastenhanced ultrasound in pediatric liver lesions, currently we do not use the technique for assessment of pediatric renal lesions.

Examinations are performed on an Acuson Sequoia (Siemens Medical Solutions) machine, using the cadence contrast pulse sequence (CPS), low mechanical index (MI) technique. Examinations of the kidney are quick, continuous, and can be repeated for several minutes. The examination is not associated with nephrotoxicity and can be used safely in cases of renal failure and obstruction.

Some understanding of the dynamics of ultrasound contrast within the kidney is essential when using this modality. Microbubble agents remain entirely intravascular, unlike iodinated and paramagnetic contrast agents. Because they are not excreted by the kidneys, there is no nephrographic or excretory phase.

The enhancement pattern of the kidney, which has a single afferent blood supply, is different from that seen in the liver, which has a dual blood supply. Distinct enhancement phases may be identified in the renal parenchyma. The early arterial corticomedullary phase with corticomedullary differentiation lasts 20 to 40 seconds. A late corticomedullary phase, in which homogenous enhancement is seen in both the renal cortex and medulla, lasts 45 to 120 seconds.

The low MI technique is used almost exclusively when generating renal images. This technique minimizes microbubble destruction, allowing real-time observation throughout the period that microbubbles are present in the blood pool. Low MI pulse inversion imaging causes normal tissue echoes to be suppressed. The baseline precontrast image appears dark and echoes from the microbubble contrast are enhanced. All postcontrast echogenicity is consequently attributed to the presence of microbubbles.

Highly vascular lesions appear echogenic with respect to the adjacent renal parenchyma, reflecting the increased number of microbubbles in their vascular pool. Nonvascular lesions appear black.

Contrast-enhanced ultrasound may be of value when evaluating anomalies in lobar anatomy that simulate tumors on baseline ultrasound. The column of Bertin is a good example. This normal renal structure comprises nonreabsorbed polar parenchyma of one or both subkidneys that fuse to form a normal kidney. Its location between overlapping regions of two renal sinus systems, the presence of normal renal tissue, and the observation of a smooth surface contiguous with adjacent parenchyma should enable differentiation from tumor.

Fetal lobulation and lobar dysmorphism may also be misinterpreted as focal lesions.

 The suspicious area should remain isoreflective to normal renal parenchyma in all phases of enhancement following administration of microbubble contrast (Figure 1), reassuring physicians and patients alike.

Renal cysts are generally assessed by radiologists and urologists according to the Bosniak classification, which is based on the analysis of specific CT features.

 Simple (type I) or minimally complicated (type II) cysts appear on B-mode ultrasound as unilocular, echofree structures of varying size, either within the substance or at the margin of the kidney. Simple cysts remain dark after microbubble contrast enhancement, even if they contain echoes on baseline ultrasound. The result is that simple cysts, and particularly small ones, are more conspicuous on contrastenhanced ultrasound. This suggests that microbubble contrast could be useful in the early detection of conditions such as polycystic kidney disease.

Another practical role for renal contrast- enhanced ultrasound is to evaluate lesions that are equivocal on CT and cannot be distinguished from malignant tumors (Bosniak type III cysts), namely by aiding the delineation of internal architecture. Microbubbles can be visualized in real-time within the fine capillaries that supply the cyst walls and internal septa. This allows suspicious features that may not be evident on CT, such as septations or mural nodule enhancement, to become more apparent. 

Contrast-enhanced ultrasound is also superior to unenhanced ultrasound and contrast-enhanced CT in the diagnosis of malignancy in complex cystic renal masses.

The main advantage of contrastenhanced ultrasound in overtly malignant cysts (Bosniak type IV) is to add to CT or MRI findings. Microbubbles can be employed to further characterize the tumor, and to distinguish solid components from cystic and necrotic parts that do not enhance (Figure 2).

The value of contrast-enhanced ultrasound in renal tumor characterization is currently limited. Benign and malignant tumors can exhibit varying enhancement patterns, and there are no exact criteria to distinguish between the two groups. This task continues to be performed predominately on CT and/or MRI.

True tumors usually show a disparity in enhancement after administration of microbubble contrast, unlike pseudotumors that have homogenous enhancement patterns identical to the adjacent renal parenchyma.

Solid renal cell carcinomas less than 3 cm in diameter often show diffuse, heterogeneous enhancement during the early corticomedullary phase, frequently with a hypervascular appearance. Enhancement may, alternatively, be homogenous, though this is less common.9 Cystic or avascular necrotic components appear black, making them more noticeable (Figure 3).

Microbubble agents are limited in the assessment of renal cell carcinoma. RCC can have arterial-phase contrast enhancement similar to adjacent renal parenchyma, making the tumors less evident after microbubble injection. Renal hypovascular metastases, on the other hand, have a persistent hypoech-oic appearance after microbubble injection that might aid diagnosis.

Contrast-enhanced ultrasound may be used to distinguish between lesions that may be characterized on ultrasound alone, such as minimally complicated cysts, hyperechoic or hemorrhagic cysts simulating a renal tumor, pseudotumors, and those lesions that will need additional investigation on cross-sectional imaging.

Contrast-enhanced ultrasound allows renal perfusion defects to be interpreted with confidence. Perfusion defects appear as single- or multifocal, wedgeshaped areas of absent, diminished, or delayed enhancement when compared with adjacent renal parenchyma (Figure 4).

This technique may be of particular use after renal transplantation. Microbubble imaging can also facilitate the diagnosis of arterial and venous thrombosis as well as postinterventional complications such as hematomas, arteriovenous shunts, and false aneurysms.

Abscesses formed by renal infection can be identified by the central liquid portion of the abscess and will show a lack of enhancement as intralesional vessels are destroyed or displaced by the colliquative process. Fine internal septa may develop as the abscess evolves, and they become more obvious on ultrasound following contrast administration (Figure 5).

CT is undoubtedly the modality of choice for assessment of visceral and skeletal injuries in high-velocity trauma. Contrast-enhanced ultrasound may have a role, however, in stable patients with low-energy blunt trauma as an aid to FAST scanning and for followup. The absence of ionizing radiation means that this strategy may be especially useful in pediatric patients.

Microbubble imaging has been shown to be more sensitive than Bmode ultrasound and almost as sensitive as CT in the detection of solid organ injury in blunt abdominal trauma. 

 The renal parenchyma normally enhances intensely following contrast administration. Hematomas or lacerations are avascular and appear as hypoechoic lesions (Figure 6).

In conclusion, contrast-enhanced ultrasound is a valuable addition to radiologists’ armory, enabling increased confidence in the diagnosis of renal pathology. It is a repeatable, real-time, multiplanar imaging modality that uses a completely intravascular contrast agent. The method is noninvasive, involves no exposure to ionizing radiation, and may be used in patients with renal impairment and those who cannot be examined with contrast-enhanced CT and/or MRI. Recognition of specific enhancement features is, however, essential.

Articles

Ultrasound is often the preliminary investigation for many diseases affecting the kidney.

Microbubble agents helppinpoint renal lesions

Ultrasound is the most commonly used abdominal imaging modality. The addition of color and spectral Doppler imaging has been particularly beneficial. When ultrasound findings are nonspecific, however, patients are generally referred to CT or MRI. 

A contrast-enhanced ultrasound examination could alleviate the need for these more expensive imaging investigations, and a number of micro-bubble-based agents exist. The predominant agent used in Europe is SonoVue (Bracco). Other available agents include Definity (Bristol-Myers Squibb) and Optison (GE Healthcare). All microbubbles are filled with gas; sulfur hexachloride in the case of SonoVue, perfluoropro-pane in the case of Definity. The gas-filled bubbles are smaller than red blood cells, so they will undergo pulmonary recirculation. When injected intravenously, the micro-bubbles remain in the blood pool for up to six minutes.

Technological advances, particularly the advent of harmonic and pulse-inversion imaging, have contributed to improvements in microbubble-based imaging. All major manufacturers of ultrasound equipment offer add-on software packages that allow for contrast-enhanced imaging, albeit at an extra cost. Microbubble contrast agents have an excellent safety profile and can be used in patients with renal impairment.

Many clinical radiology departments across Europe now use micro-bubble contrast agents for ultrasound scans of the liver. Published guidelines are available on the characterization of focal liver lesions using contrast-enhanced ultrasound,

 and good concordance with CT and MRI has been demonstrated.

The extension of contrast-enhanced ultrasound into other abdominal structures outside of the liver is on the horizon, though the potential role for microbubble agents in these organs is not as well appreciated at present. The agents may be used to depict disease processes in the spleen, kidneys, gallbladder, bowel, and pancreas.

The kidneys normally are readily accessible on ultrasound. The combination of real-time imaging and patient cooperation yields the best views. Adding microbubble contrast to the renal examination is a logical step if the features of any abnormality require further elucidation.

Several renal pseudotumors may mimic genuine tumors on imaging.

 The column of Bertin, for example, comprises non-reabsorbed polar parenchyma of the subkidneys that fuse to form a normal kidney. It may be misdiagnosed as a renal mass on ultrasound, though its location between overlapping regions of two renal sinus systems, the presence of normal renal tissue, and the observation of a smooth surface contiguous with adjacent parenchyma should be reassuring. The same misdiagnosis can occur in cases of fetal lobulation and lobar dysmorphism.

Ultrasound contrast agents may be of particular value in these patients. The immediate depiction of normal-functioning renal tissue can reassure both the patient and the examining physician (Figure 1). Suspicious areas remain isoreflective to normal renal parenchyma. They exhibit a rapid increase in enhancement during the arterial phase and subsequent wash-out in the later phase, identical to normal tissue.

It is worth remembering that patterns of contrast enhancement in organs with a single afferent blood supply are different from those seen in the liver, which has a unique dual afferent blood supply.

Complex renal cysts account for 10% of renal cell carcinomas, and it is thus vital to diagnose these correctly. The Bosniak renal cyst classification system is an established method of assessing renal cystic lesions from CT findings.

 Ultrasound alone is of limited value in these cases.

The use of microbubble contrast agents can be an effective addition to the imaging workup when dealing with complex renal cysts, and this approach may supersede the role of CT and MRI. The vascularity of renal cyst walls can be assessed, allowing the suspect lesion to be characterized and its potential malignancy evaluated. Newer imaging techniques make it possible to visualize microbubbles in real-time within the tiny capillaries that supply the cysts' fine septae and walls (Figure 2).

Researchers have shown that the Bosniak renal cyst classification is also applicable to contrast-enhanced ultrasound.

 Replacement of contrast-enhanced CT with micro-bubble ultrasound imaging for complex renal cyst follow-up will have a substantial impact on patient morbidity. The potential for nephrotoxicity from iodinated contrast and the long-term risks associated with ionizing radiation are eliminated.

Renal cell carcinoma is the most common malignant tumor of the kidney. Diagnosis is traditionally established by unenhanced CT followed by contrast-enhanced CT during the corticomedullary and nephrographic phases. Tumor detection is maximal during the nephrographic phase.Microbubble contrast agents are an effective tool for assessing tumor vascularity. A heterogeneous pattern of enhancement is more common than a homogeneous pattern, unlike the pattern seen in normal renal tissue. A renal tumor enhances more than the adjacent parenchyma, and it enhances maximally in the arterial phase (20 to 60 seconds after a bolus injection).

 Contrast-enhanced ultrasound may also evaluate hypovascular solid renal tumors that enhance less than normal renal parenchyma.

Care should be taken in the rare case of patients with multiple focal renal infarcts, which do not enhance with microbubble contrast. Unenhanced ultrasound shows the infarcts as wedge-shaped, low-reflective areas. This illustrates the importance of performing a baseline ultrasound examination prior to contrast administration in all patients.

Ultrasound is an established screening tool for renal artery stenosis, a treatable cause of secondary hypertension. The examination is often time-consuming and operator-dependent, however. Micro-bubble enhancement has been shown to improve the detection of renal artery stenosis and reduce the rate of technical failure. Angiography remains the reference standard. Renal vein examinations using microbubble contrast could potentially be used to differentiate thrombus from tumor thrombus, which shows strong enhancement.

Ultrasound is the most frequently used imaging modality for splenic assessments. The addition of microbubble contrast can help diagnose a wide variety of abnormalities, in-cluding congenital variations, acquired focal lesions (benign and malignant), abscesses, infarctions, and the effects of trauma.

Accessory spleens found in 10% to 30% of the population can be single or multiple. Most occur at the splenic hilum, though they can also be found in the splenorenal or gastrosplenic ligaments. Histopathology of an accessory spleen is similar to that of the parent spleen, as is appearance on ultrasound. Microbubble contrast demonstrates the vascular hilum clearly and shows the sinusoidal blood flow occurring at identical times within the spleen and splenunculus. These imaging features are of value in distinguishing a splenunculus from a pancreatic tail mass or an abnormal lymph node.

Splenic cysts are either primary (parasitic or epithelial) or traumatic. They are normally avascular but may contain debris or demonstrate wall calcification. Microbubble contrast outlines the smooth contour of the cyst and can differentiate the cyst from a solid lesion. Hydatid cysts are the exception. These may have high re-flectivity and demonstrate peripheral but not internal enhancement. 

Benign solid lesions of the spleen include hemangiomas, lymphangiomas, and hamartomas. Cavernous hemangiomas, the most common, are typically detected as an incidental finding measuring less than 2 cm across. Cavernous hemangiomas are characteristically well defined, highly reflective lesions that enhance centripetally with microbubble contrast. This is particularly the case for larger lesions.

Splenic metastases are due mainly to lymphoma and melanoma, although other malignancies can spread to the spleen. Most have low reflectivity and, with microbubble contrast, peripheral irregular enhancement. Additional lesions not seen on the baseline examination are often identified when contrast is added. Differentiation from splenic abscesses may be difficult, though demonstration of enhancing septations and a relevant clinical history can help in such cases (Figure 3).

Solid organ injury in blunt abdominal trauma may be imaged reliably with contrast-enhanced ultrasound,

 though CT is the investigation of choice. An initial FAST (focused assessment with sonography for trauma) evaluation is often performed in the emergency department to rule out obvious solid organ injury and the presence of free fluid.

Baseline ultrasound imaging features of splenic trauma include subcapsular hematoma, intrasplenic foci of iso- or low reflectivity, and lacerations. These injuries may not be apparent on B-mode imaging in an acute setting. Micro-bubble contrast agents in-crease the conspicuity of these abnormalities, especially complex lacerations, which are visualized surrounded by the enhancing parenchyma (Figure 4). The ability to identify solid organ injury in the emergency setting allows patients to be triaged efficiently. Microbubble contrast-enhanced ultrasound can improve the detection of injury in the spleen, liver, and kidneys.

Microbubble contrast can help differentiate highly reflective bile sludge from a possible tumor or polyp. Biliary sludge shows neither tumor vessels nor tumor enhancement (Figure 5),

 but inflammatory polyps, adenomas, and carcinomas can demonstrate both intralesional vessels and enhancement. Assessment of tumor vessels on contrast-enhanced ultrasound may be useful for distinguishing gallbladder carcinoma from other polypoidal gallbladder lesions. Caution must be taken because the appearances can overlap. Contrast-enhanced ultrasound is also superior to unenhanced color Doppler ultrasound when evaluating the vascularity of gallbladder wall disease. Microbubble contrast demonstrates marked enhancement in the gallbladder wall in acute cholecystitis. 

Contrast-enhanced ultrasound can be used to assess the pancreas, bowel, and ovaries as well.

 The evaluation of pancreatic tumors, particularly cystic tumors and ductal adenocarcinoma, is promising. Intense enhancement may signal the presence of a small insulinoma in the pancreas.

Intense enhancement to thickened bowel wall may indicate ongoing inflammatory changes due to Crohn's disease. It may be more important, however, to search for areas of bowel wall with no enhancement, as these areas are likely to be ischemic.

Microbubble contrast can be used to assess the integrity of an endovascular abdominal aortic stent-graft. This is reported to be the most sensitive method of detecting subtle leaks that result in endotension (persistent or recurrent pressurization of the aneurysm sac).

The incidence of hypersensitivity or adverse events appears to be much lower with the microbubble agents used for ultrasound than with iodine-based CT contrast. Ultrasound is also free from ionizing radiation. Reports of the adverse effects of MR contrast agents, coupled with the claustrophobic nature of MR imaging, make contrast-enhanced ultrasound even more attractive.

A review of 23,188 investigations using microbubble contrast revealed the incidence of adverse events to be 0.0086%. These events were predominantly minor, such as itching, nausea, dizziness, headache, mild hypotension, and a sense of warmth.2 Arrhythmia effects have been reported when using ultrasound contrast during cardiac investigations. These are thought to be attributable to QT prolongation and the induction of premature ventricular contractions.

Contrast-enhanced ultrasound is not performed widely, despite the wealth of scientific data demonstrating the usefulness of microbubble agents. The technique is employed by enthusiastic practitioners at a number of centers, but the overall number of users is growing slowly.Obstacles may be difficult to overcome. In the U.K., for example, ultrasound is perceived as a noninvasive examination, and the need to administer an injection is a major psychological hurdle. Most sonographers operate single-handed. A contrast-enhanced examination would require two practitioners, raising staffing issues.

Radiologists may prefer to direct a CT or MRI examination remotely and report at their convenience. Ultrasound does not lend itself to this practice. Hands-on imaging is the only way to fully appreciate the nuances of the examination and attain the correct conclusion. If the addition of contrast to ultrasound imaging resulted in a definitive answer, and patients were no longer referred for further examinations, then arguments relating to lack of time could perhaps be resolved. Radiologists may then look at the technique more favorably. 

Ultrasound can demonstrate anatomy and pathology with high resolution, and the addition of microbubble-based contrast aids in the diagnosis of disease and subsequent follow-up. The role of such agents outside of the liver is clearly useful. Operators should be encouraged to take this step before requesting further imaging with CT or MRI. 

DR. FERNANDO is a radiology registrar, DR. SELLARS and DR. SIDHU are consultant radiologists, all at King's College Hospital in London.

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Ultrasound is the most commonly used abdominal imaging modality. The addition of color and spectral Doppler imaging has been particularly beneficial. When ultrasound findings are nonspecific, however, patients are generally referred to CT or MRI

Paul S. Sidhu, MRCP

Articles

Microbubble agents helppinpoint renal lesions

Microbubble-based scans reach beyond liver