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Role of CEUS in the diagnosis of gallbladder disease

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Review

2012, Vol. 14, no. 4, 326-330

Abstract

Conventional ultrasound (US) is the first imaging investigation recommended for diagnosis of gallbladder pathology.

However, it has an important limit of ability to depict microcirculation of some biliary lesions which may lead to failure in diagnosis. The use of contrast-enhanced US (CEUS) seems to overcome these limits and allows a more confident diagnosis.

In this review, the methodology, image interpretation, enhancement pattern, clinical usefulness, and indications for CEUS in gallbladder lesions are summarized. CEUS may be indicated under the following circumstances: 1) For differentiation diag- nosis between a malign tumor or a benign tumor of the gallbladder; 2) to make a distinction between motionless sludge and gallbladder carcinoma; 3) to assess the extension of gallbladder carcinoma in adjacent hepatic parenchyma; 4) patients with impaired renal function.

Keywords: gallbladder tumors, ultrasound, contrast enhanced

Role of CEUS in the diagnosis of gallbladder disease

Zeno Spârchez, Pompilia Radu

3rd Medical Department, “Iuliu Hatieganu” University of Medicine and Pharmacy, Institute of Gastroenterology and Hepatology, Department of Ultrasound, Cluj Napoca, Romania

Received 20.09.2012 Accepted 30.09.2012 Med Ultrason

2012, Vol. 14, No 4, 326-330

Corresponding author: Assoc.Prof.Zeno Spârchez 3rd Medical Deaprtment, 19-21 Croitorilor str Cluj Napoca, Romania E-mail:[email protected]

Introduction

B mode ultrasound (US) is the first imaging investi- gation performed for the diagnosis of biliary pathology.

It has a high sensitivity to detect gallbladder stones and intra-hepatic or extra-hepatic bile duct dilatation. The main limitation of ultrasound is a low ability to assess vascularity and therefore to establish the nature of gall- bladder and biliary ducts tumors [1].

In generally gallbladder cancers present as either a solid mass that occupy the whole gallbladder or a focal polypoid lesion on conventional US. Also a motionless biliary sludge can generate similar US images with gall- bladder cancer [2]. In these cases the presence of vessels can make the differential diagnosis between a benign le-

sion and gallbladder cancer. Color and power Doppler US have been developed to overcome these limitations but several limits still remained: a slow flow or deeply located blood vessels [1,2].

The introduction of micro-bubble contrast agents (UCA) and the development of contrast-specific imaging techniques have improved the performance of B mode US. Microbubble contrast agents have diameters in the range of 1–10 mm (median 2 mm) that do not allow fil- tering by the lungs or the entering into the interstitial flu- id. Therefore, they are completely intravascular contrast agents. Having this feature they give an accurate assess- ment of the blood flow within a lesion and permit the diagnosis of the nature of that lesion. Another important feature is that micro-bubbles agents are not radioactive.

SonoVueTM micro- bubbles are composed of a sulphur hexafluoride gas with a phospholipids shell. The contrast agents are metabolized by the liver and the sulphur hex- afluoride gas is exhaled via the lungs.

After several studies showed that the utilization of contrast-enhanced ultrasound (CEUS) substantially im- proves the detection and the characterization of gallblad-

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der lesions [2-5], in 2011 CEUS was accepted in the Guidelines and good clinical practice recommendations for CEUS - update 2011, for clinical practice [6].

Scanning method

Each patient has to be fasted for least 8 hours before examination. Before performing a CEUS examination, the gallbladder and adjacent liver parenchyma should be examined using conventional gray-scale US and the target lesion identified. After identification of the target lesion, the transducer is kept in a stable position and the imaging mode is changed to low mechanical in- dex (MI<0.2). The tissue signals are eliminated and the depth, gain and focus are carefully adjusted. UCA is ad- ministered intravenously through the antecubital vein as a bolus (within 1-2 s), followed by a flush of 10 ml 0.9%

sodium chloride solution. The timer should be activated from the beginning of contrast agent administration and the lesion is observed intermittently for at least 3 min. It is important that the entire CEUS process for the intrahe- patic biliary system should performed with reference to the adjacent liver parenchyma [2].

CEUS – enhancement pattern of gallbladder The vascular phases of the gallbladder are different from those of the liver because the blood supply is pro- vided entirely by the cystic artery and not by portal vein branches. Therefore only 2 phases can be followed: arte- rial phase (10–20 s after bolus injection) and late phase (31–180 s after contrast injection). The late phase persists for a short time in comparison with that for the liver [7,8].

Enhancement is assessed by comparing the echogenicity of a lesion with the echogenicity of the liver parenchyma.

Pathology

1. Polypoid lesions of the gallbladder

The majority of polypoid lesions of the gallbladder are cholesterol polyps. US has 90% sensitivity for the de- tection of polypoid lesions. Distinguishing a potentially pre-malignant adenoma from a benign cholesterol polyp is not possible always only on the basis of US. There are several features that can suggest the benign nature of polypoid lesions: size less than 10 mm, multiplicity and an increased echogenicity. By contrast, increasing size on sequential US examinations, focal thickening of the gall- bladder wall or nodularity adjacent to a polypoid mass can suggest malignancy.

The US appearance of cholesterol polyps is that of multiple, non-shadowing, oval lesions attached to the gallbladder wall. The size is usually 2-5 mm and the di- agnosis is made easily with US. Larger lesions (up to 20

Fig 1. Cholesterol polyps. a) Conventional US de- picts one echogenic lesion arising from the gall- bladder wall (<). b) CEUS image at 15 s after CA administration demonstrates vascularity of the le- sion; c) macroscopic specimen.

Fig 2. Gallbladder adenoma. a) B mode US shows an echogenic mass arising from the wall; b) in arte- rial phase the lesion is isoenhanced in respect with the liver; 3) in venous phase the lesion in slightly hypoenhanced.

mm) should be differentiated from adenomas or gallblad- der carcinomas [9].

On CEUS, hyper-enhancement is found in the ma- jority (93%) of the lesions and the remaining 7% show iso-enhancement during the early phase. In cholester- ol polyps, normal-caliber arteries taper normally and subdivide normally into small vessels, thereby the le- sion shows dotted- or branched-type tumor vessels on CEUS. In the late phase, hypo-enhancement is found in 64% and iso-enhancement in 36% of the lesions [2,7]

(fig 1).

2. Gallbladder adenomas

Gallbladder adenomas are relatively uncommon, with an incidence ranging between 0.3% and 0.5% in gallbladders removed [7]. Gallbladder adenoma appears on US as a sessile polypoid mass, with an echogenicity slightly greater or similar to the liver, with a smooth or lobulated surface and a relatively homogeneous internal texture, without infiltration to the adjacent tissue. On CEUS examination adenomas can appear during the ear- ly phase homogeneous hyper-enhanced (78%) and iso- enhanced (22%). In the late phase they appear iso- (56%) and hypo-enhanced (44%) [2] (fig 2).

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3. Gallbladder sludge

Gallbladder sludge is a mixture of particulate matter and bile that occurs when the solutes in bile precipitate.

In the differentiation between gallbladder cancer and mo- tionless biliary sludge CEUS has a sensitivity of 100%

[2,4]. Because of the lack of vessels in the arterial phase the mass will appear non-enhanced. In the late phase it will remain non-enhanced (fig 3).

4. Adenomyomatosis

Adenomyomatosis is a hyperplastic cholecystoses , has no malignant potential and may involve the gallblad- der in a focal, segmental or diffuse form.

It is relatively commonly found in 1-9% of all chole- cystectomy specimens and is characterized pathologi- cally by hyperplasia of the wall with formation of intra- mural mucosal diverticula (Rokitansky-Aschoff sinuses) penetrating into the muscular wall of the gallbladder, with or without gallbladder wall thickening.

On US examination the characteristic feature is the comet tail artifact echogenic intramural foci from which emanate V-shaped “comet tail” reverberation artifacts.

Those artifacts represent the unique acoustic signature of cholesterol crystals within the lumina of Rokitansky- Aschoff sinuses [1,7,8,10]. At CEUS examination in the arterial phase the gallbladder wall has a characteristic

“moth-eaten” enhancement: the non affected gallbladder wall is normally enhanced and the diverticulum zone will not depict contrast enhancement [8,10].

5. Acute cholecystitis

Acute cholecystitis is an inflammation of the gall- bladder wall typically caused by a calculus obstructing the cystic duct. On CEUS examination during the arterial phase, enhancement of the gallbladder wall will be seen earlier than the enhancement of the adjacent liver paren- chyma. In the late phase the thickened gallbladder wall will have an obvious “wash-out” comparative with the liver parenchyma (Figure 4). CEUS examination has an important role in detecting abscess formation in the sur- rounding liver parenchyma. Interruption of the gallblad- der wall suggests perforation, which can be confirmed by the absence of enhancement of the perforated wall [2,3,8,6] (fig 5).

6. Gallbladder malignant tumors.

Gallbladder carcinoma is the fifth most common malignancy of the gastrointestinal tract and has an as- sociation with gall stones [8]. On US examination it can appear like a polypoid intraluminal lesion, a tissue mass infiltrating the gallbladder wall and the surrounding he- patic parenchyma or a diffuse mural thickening [1,9].

On CEUS examination, the arterial branches that sup- ply the gallbladder carcinoma tend to show irregularly tortuous extension. The late phase washout of the con-

trast agent within 35-60 seconds after administration may be a key for differential diagnosis [2] (fig 6). Improved gallbladder wall visualization following contrast admin- istration and the malignant feature of late-phase hypovas- cularity relative to the hepatic parenchyma may provide sharp demarcation of tumor outline.

Another appearance that can be seen in gallbladder carcinoma is a disruption of the gallbladder wall integ-

Fig 3. Gallbladder sludge. a) B mode US shows a gallbladder with an echogenic mass inside; b) CEUS in arterial phase depicts no enhancement within the mass.

Fig 4. Acute cholecystitis a) B mode US in a pa- tient after endoscopic stent placement shows a thickened , double layer gallbladder wall ; b) in arterial phase the wall is hyperenhanced ; c) in venous phase the wall becomes slightly hypoen- hanced.

Fig 5. Acute cholecystitis with perforation and abscess formation. a) US shows a gallbladder with thickened wall and am irregular anechoic structure in the adja- cent liver; b) CEUS in arterial phase depicts the hy- perenhaced wall and a small disruption of the wall (<).

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rity. On CEUS examination, in the arterial phase the wall disruption is better visualized [8] (fig 7).

Metastases to the gallbladder are very rare, the most common tumor leading to a metastatic tumor of the gall- bladder being malignant melanoma. The lesions are usu- ally multiple, hyperechoic broad base polypoid lesions larger then 10 mm [9]. The lesions are hyperenhancing in arterial phase with a rapid wash out (fig 8).

7. Difference between benign and malignant lesions.

All gallbladder tumors, benign or malign, are sup- plied by arterial vessels from branches of the cystic ar- tery. Therefore in the arterial phase most of the lesions are hyper-enhanced in the early phase of CEUS and no difference between them is detected [2,5]. Hyper- enhancement in the arterial phase was present in 84.8%

of carcinomas and in 70.2% of benign lesions ( 92.2%

cholesterol polyps, 77.8% adenomas and 85.5 % chronic cholecystitis) [7].

The distribution of the vessels inside the lesion may add some diagnostic features. Thus, the benign lesions show dotted vessel enhancement whereas malignant le- sions tortuous vessel enhancement [7].

Although the late phase is important in establishing the nature of the hepatic lesion, for gallbladder this algorithm is not always applicable. Nevertheless wash-out phenom- enon of the contrast agent within 35-60 s after UCA ad- ministration was present mostly in malignant tumors [5].

Disruption of the gallbladder wall integrity appears in 85% of gallbladder carcinomas and in none of the benign lesions (specificity 100%).

The combination of enhancement pattern (hyper- enhancement or iso-enhancement in the early phase with hypo-enhancement within 35 s after contrast agent administration) and lesion’s size yield a sensitivity of 90.9%, specificity of 87.2% and an accuracy of 88.8 % in diagnosing malignancy [2].

8. Conclusions

In the diagnosis of gallbladder lesions CEUS over- comes the limitations of conventional US and allows an improved ability in the assessment of intralesional vas- cularity. CEUS is a safe method that has proved to have a high accuracy in the diagnosis of gallbladder lesions.

Also it has proved to be a trusted tool in differentiating malignant and benign tumors.

In clinical practice CEUS may be used in the follow- ing settings: 1) For patients with renal impairment for whom the use of contrast agents in CT imaging is not allowed; 2) To make a differential diagnostic between a malign and a benign tumor of gallbladder; 3) To make a differential diagnostic between motionless sludge and gallbladder carcinoma; 4) To assess the extension of gall- bladder carcinoma in adjacent hepatic parenchyma.

References

1. Yarmenitis SD. Ultrasound of the gallbladder and the bil- iary tree. Eur Radiol 2002;12:270-282.

2. Xie XH, Xu HX, Xie XY, et al. Differential diagno- sis between benign and malignant gallbladder diseases Fig 6. Small gallbladder carcinoma. a) conventional

US shows a 2 cm polypoid mass in the gallbladder;

b) in arterial phase CEUS depicts hypervascularity of the mass; c) in venous phase the mass becomes slightly hypoenhanced.

Fig 7. Gallbladder carcinoma with disruption of the wall integrity and invasion in liver parenchyma. a) US depicts a gallbladder full with stones, the walls could not be identified. In the adjacent liver a hypoechoic mass is well seen; b) CEUS shows a hyperenhanced le- sion in arterial phase with c) wash out in venous phase.

Fig 8. Gallbladder metastasis from melanoma. a) US shows a multiple, irregular masses in the gall- bladder lumen; b) CEUS arterial phase, one lesion is hyperenhanced; c) in venous phase there is a clear wash-out.

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with real-time contrast-enhanced ultrasound. Eur Radiol 2010;20:239-248.

3. Adamietz B, Wenkel E, Uder M, et al. Contrast enhanced sonography of the gallbladder: a tool in the diagnosis of cholecystitis? Eur J Radiol 2007;61:262-266.

4. Inoue T, Kitano M, Kudo M, et al. Diagnosis of gallbladder diseases by contrast-enhanced phase inversion harmonic ultrasonography. Ultrasound Med Biol 2007;33:353-361.

5. Numata K, Oka H, Morimoto M, et al. Differential di- agnosis of gallbladder diseases with contrast enhanced harmonic gray scale ultrasonography. J Ultrasound Med 2007;26:763-774.

6. Piscaglia F, Nolsøe C, Dietrich C F, et al. The EFSUMB guidelines and recommendations on the clinical practice

of contrast enhanced ultrasound (CEUS): Update 2011 on non-hepatic applications. Ultraschall Med 2012;33:33-59.

7. Xu HX. Contrast-enhanced ultrasound in the biliary system:

Potential uses and indications. World J Radiol 2009;1:37-44.

8. Meacock LM, Sellars ME, Sidhu PS. Evaluation of gall- bladder and biliary duct disease using microbubble con- trast-enhanced ultrasound. Br J Radiol 2010;83:615-627.

9. Khalili K, Wilson SR. The biliary tree and gallbladder. In:

Diagnostic ultrasound. Rumack CM, Wilson SR, Charbo- neau JW (eds). Mosby Inc 2005:171-212.

10. Haradome H, Ichikawa T, Sou H, et al. The pearl necklace sign: an imaging sign of adenomyomatosis of the gallblad- der at MR cholangiopancreatography. Radiology 2003;227:

80-88.

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