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Gastrointestinal Imaging |
1 From the Department of Radiology, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo 181, Japan (H.H., A.N., J.H.); and Department of Radiology, Yamanashi Medical University School of Medicine, Japan (T.I., H.S., T.Y., T.A.). Received August 9, 2001; revision requested October 10; revision received May 9, 2002; accepted July 24. Address correspondence to H.H. (e-mail: haradome@ff.iij4u.or.jp).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: MRCP findings and those of a combination of unenhanced and arterial phase computed tomography (CT) and arterial phase MR imaging were retrospectively compared in 29 patients who were pathologically proven to have adenomyomatosis of the gallbladder and in 18 patients with pathologically proven gallbladder carcinoma. Receiver operating characteristic (ROC) analysis was used with a five-point confidence scale. The relative sensitivity, specificity, and accuracy of each imaging modality were also calculated. The pearl necklace sign was defined on MRCP images as small round foci, with the same markedly high signal intensity as bile, within the thickened wall of the gallbladder.
RESULTS: The mean area under the ROC curve of MRCP alone and that of the combination of MRCP and arterial phase MR imaging was significantly higher than that of combined CT (unenhanced and arterial phase) and arterial phase MR imaging alone (P < .01). The relative sensitivities in the diagnosis of adenomyomatosis of the gallbladder were 24% for the combined CT, 29% for arterial phase MR imaging, 62% for MRCP, and 57% for the combination of MRCP and arterial phase MR imaging. The mean relative sensitivity, specificity, and accuracy of the pearl necklace sign on MRCP images were 62%, 92%, and 74%, respectively. In eight (28%) of 29 patients with adenomyomatosis of the gallbladder, the pearl necklace sign was not identified by all three readers on the MRCP images.
CONCLUSION: The pearl necklace sign, which indicates the presence of Rokitansky-Aschoff sinuses within the thickened gallbladder wall, was specifically detected at MRCP for adenomyomatosis of the gallbladder.
© RSNA, 2003
Index terms: Computed tomography (CT), comparative studies, 762.12111, 762.12112 • Gallbladder, adenomyomatosis, 762.3119 • Gallbladder, neoplasms, 762.31, 762.32 • Magnetic resonance (MR), cholangiopancreatography • Magnetic resonance (MR), comparative studies, 762.121411, 762.121412, 762.121416, 762.12143
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Ultrasonography (US) is the most widely used method for evaluating suspected gallbladder diseases. It is well known that diffuse or segmental thickening of the gallbladder wall and anechoic intramural diverticula with or without cometlike echo are characteristic findings in the diagnosis of adenomyomatosis of the gallbladder (7–9). However, US is also limited by subjective evaluation, small field of view, or beam interruption by bowel gas and obesity.
Opacification of the Rokitansky-Aschoff sinus is depicted on drip-infusion cholecystographic images, specifically in the diffuse type of adenomyomatosis of the gallbladder, and is called the "pearl necklace" sign (10). However, opacification of the Rokitansky-Aschoff sinus is not always depicted on drip-infusion cholecystographic images because the gallbladder may not be consistently filled with a contrast agent.
Heavily T2-weighted fast spin-echo (SE) magnetic resonance (MR) images have been investigated for their usefulness in the diagnosis of adenomyomatosis of the gallbladder because Rokitansky-Aschoff sinuses filled with bile within the thickening wall of the gallbladder manifest as markedly hyperintense spots on the images (11,12). Owing to the fast scanning time, MR cholangiopancreatography (MRCP) with single-shot fast SE sequences may be more reliable for this purpose than the heavily T2-weighted fast SE MR imaging that is frequently used to image Rokitansky-Aschoff sinuses (13,14). We hypothesized that if MRCP images can frequently reveal the pearl necklace sign in patients with adenomyomatosis of the gallbladder and not in patients with a diagnosis of gallbladder carcinoma, these images would then be useful for identifying adenomyomatosis of the gallbladder (Fig 1). Therefore, the purpose of our study was to evaluate the demonstration of the pearl necklace sign on MRCP images in patients with proven adenomyomatosis and carcinoma of the gallbladder.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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All imaging studies were performed for clinical reasons, possible presence of gallbladder diseases suspected at US, or both. The patient’s age at diagnosis ranged from 33 to 80 years (mean age, 57 years) for the 29 patients with adenomyomatosis of the gallbladder and from 41 to 87 years (mean age, 64 years) for the 18 patients with gallbladder carcinoma. There were no significant differences in patient age (Mann-Whitney test, P > .1) and the male-female ratio (
2 test, P > .1) between adenomyomatosis of the gallbladder and gallbladder carcinomas.
At presentation, the 29 patients with adenomyomatosis of the gallbladder had complaints of abdominal pain (n = 15), elevated levels of biliary enzymes (n = 8), or elevated levels of tumor makers (n = 6). All 29 patients underwent histologic evaluation by means of surgery (n = 7) or laparoscopic cholecystectomy (n = 22) because the presence of cholecystolithiasis (n = 15) with abdominal pain or a possible gallbladder carcinoma was suggested as a preoperative diagnosis. In the 29 patients, the whole gallbladder was resected and histopathologic findings were used to classify the adenomyomatosis into three morphologic subtypes: diffuse (six patients), segmental (13 patients), and fundal (10 patients). In all of the patients, Rokitansky-Aschoff sinuses of various sizes were identified in the specimens.
All 18 gallbladder adenocarcinomas were completely resected at surgery and were pathologically diagnosed. Histopathologically, the tumors were morphologically classified into two subtypes: a diffuse wall-thickening type (n = 7) and a polypoid type (n = 11). All seven tumors of the diffuse wall-thickening type had invaded the subserosal layer of the wall of the gallbladder. The 11 tumors of the polypoid type had invaded the mucosal layer (five patients), the muscular layer (four patients), or the subserosal layer (two patients). None of the tumors involved other organs, such as the liver or duodenum.
Imaging
All MR imaging examinations were performed with commercially available 1.5-T superconducting MR units (Signa Horizon, GE Medical Systems, Milwaukee, Wis; and Magnetom Vision, Siemens Medical Systems, Erlangen, Germany) with phased-array multicoils. First, coronal T1-weighted test images with gradient-echo sequences (fast spoiled gradient-echo or fast low-angle shot, 120–170/1.8–6, 90° flip angle) were obtained to confirm the optimal scanning range of the gallbladder. In all patients, MRCP images were obtained with half-Fourier single-shot fast SE or with half-Fourier single-shot turbo SE (HASTE; Siemens Medical Systems) sequence. The imaging parameters were as follows: 2,000–30,000/90–600, 180° flip angle, echo spacing of 8.6 msec, echo train length of 168, matrix of 320–256 x 256, and acquisition time of 2 seconds per section with the single-shot fast SE sequence and 
/87, 180° flip angle, echo spacing of 10.9 msec, echo train length of 128, matrix of 256 x 240, and acquisition time of 2 seconds per section with the single-shot turbo SE sequence. All MRCP images included single-shot images with a section thickness of 2–5 cm and multishot images with a section thickness of 3–5 mm obtained with sequential scanning during a breath hold of 10–30 seconds. The MRCP images were obtained in the coronal, transverse, and oblique planes and included a single-shot image with section thickness of 2–5 cm and 9–13 contiguous images with a section thickness of 5 mm obtained with sequential scanning during a breath hold of about 18–26 seconds.
In all patients, arterial phase MR images were obtained immediately after a bolus injection of 0.1 mmol per kilogram of body weight of a gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany). The fast spoiled gradient-echo or fast low-angle shot sequences for arterial phase MR images were designed with the following imaging parameters: 140–170/4.2–6, 90° flip angle, 256 x 512 matrix, seven to 15 sections acquired, 5-mm section thickness, 50% intersection gap, field of view of 300–350 mm (62.5%–75% rectangular field of view), one signal acquired, and breath-holding time of 26–32 seconds. No fat-saturated techniques were used for the arterial phase MR images. To avoid bowel-related motion artifacts, 7.5 mg of an antiperistaltic drug (timepidium bromide [Buscopan]; Tanabe Pharmaceutical, Osaka, Japan) was injected intravenously before arterial phase MR examinations. MR images were obtained 25–35 seconds after the start of the administration of gadopentetate dimeglumine.
Arterial phase CT images were obtained with commercially available helical CT scanners (X-Vigor, Toshiba Medical, Tokyo, Japan; or Proceed SA, GE Medical Systems). Unenhanced CT scans were obtained in 7- or 10-mm-thick sections. The unenhanced CT series were programmed to include the entire liver and the gallbladder. The upper and lower helical scanning levels were determined from the unenhanced CT images. At arterial phase CT imaging, patients received 100 mL of iopamidol with an iodine concentration of 300 mg/mL (Iopamilon [total dose of iodine, 30 g]; Schering). The contrast material was administrated at rates of 3.0 mL/sec with a 20-gauge plastic cannula placed into an antecubital vein and with a monophasic rate of injection with a power injector (Autoenhance; Nemotokyorindo, Tokyo, Japan). The arterial phase CT image was obtained 35 seconds after the injection of a bolus of the contrast material. The section thickness was 5 mm, and the table incremental speed was 5 mm/sec (1:1 pitch). The reconstruction intervals were 5 mm. The imaging time for the arterial phase CT and MR images was determined on the basis of the results of the previous studies (15–17). All unenhanced and arterial phase CT and arterial phase MR images were evaluated for image analysis. In this study, unenhanced MR images were not included in image analysis because previous reports have indicated that arterial phase MR images were reliable in the evaluation of adenomyomatosis of the gallbladder (15–17).
Image Analysis
The ability of each imaging modality to differentiate gallbladder carcinoma from adenomyomatosis of the gallbladder was assessed with a receiver operating characteristic (ROC) analysis based on a five-point confidence scale. Two abdominal radiologists (H.S., H.H.), serving as study coordinators, initially reviewed all CT and MR images with knowledge of the pathologic findings. On the basis of pathologic reports, the final diagnosis of each lesion was determined in all patients. If the initial filming was of poor quality, the images were reprinted. All CT and MR images were interpreted independently and randomly by three other experienced abdominal radiologists (T.I., T.Y., K.I.). Each reader was blinded to patient identity, clinical history, results of other imaging examinations, and clinicopathologic information. The pearl necklace sign was defined on MRCP images as small round foci, with a markedly high signal intensity equivalent to that of bile, within the thickened wall of the gallbladder.
In clinical study, MRCP is mainly divided into two acquisition techniques: thick single-section technique and thin multisection technique postprocessed with maximum intensity projection. Moreover, with the multisection technique, thin source images are suitable for evaluating the gallbladder wall. However, multisection MRCP images demonstrate a polypoid solid lesion and gallstone as having the same signal intensity because they are obtained with relatively long echo time, compared with conventional T2-weighted images. Therefore, differentiation of both is difficult on multisection MRCP images. Multisection MRCP images, which are obtained without contrast media and provide only T2 contrast, are also difficult in the differentiation of the wall thickness due to inflammation or malignancy. For these reasons, a different five-point confidence scale was used for the diagnostic reliability of MRCP images and CT and MR images.
For MRCP images, the following five-point confidence scale was defined according to the presence of the pearl necklace sign: score 1, definitely gallbladder carcinoma (absence of the pearl necklace sign); score 2, probably gallbladder carcinoma (probable absence of the pearl necklace sign); score 3, equivocal (indistinct evidence of the pearl necklace sign); score 4, probably adenomyomatosis of the gallbladder (probable presence of the pearl necklace sign); and score 5, definitely adenomyomatosis of the gallbladder (definite presence of the pearl necklace sign).
For the CT interpretation, unenhanced CT images were read in addition to the arterial phase CT images for the purpose of detecting calcifications. A five-point confidence scale for CT and MR images was defined according to the status of a soft-tissue masslike lesion (or thickening of the gallbladder wall) with or without extra-wall extensions or possible metastases (ie, enlarged lymph nodes or hepatic hypoattenuating nodules) and with small calcification or Rokitansky-Aschoff sinuses within the gallbladder wall. If a masslike lesion (or thickened gallbladder wall) was found, the size and the enhancement pattern of the lesion were also considered. Score 1 indicated definite gallbladder carcinoma (heterogeneously enhanced masslike lesion or thickened gallbladder wall, >1 cm with possible extension beyond the gallbladder or possible metastases); score 2, probably gallbladder carcinoma (heterogeneously enhanced masslike lesion or thickened gallbladder wall, >1 cm without extra gallbladder extension or metastases); score 3, equivocal (heterogeneously enhanced masslike lesion or thickened gallbladder wall, 1 cm or <1 cm without extra gallbladder extension or metastases, or homogeneously enhanced masslike lesion, or thickened gallbladder wall, 
1 cm without calcification or Rokitansky-Aschoff sinus); score 4, possible adenomyomatosis of the gallbladder (probable presence of calcification or Rokitansky-Aschoff sinus); and score 5, definitely adenomyomatosis of the gallbladder (definite presence of calcification or Rokitansky-Aschoff sinus). Two weeks after the independent interpretation of each type of image was completed, each reader attempted to use the combined imaging criteria to interpret the combination of MRCP and MR images.
Statistical Analysis
The interobserver differences were assessed to establish the reliability of the imaging interpretation. The degree of the interobserver difference between each combination of two readers was also calculated with the chance-corrected 
statistic. Generally, a statistic greater than 0.75 is considered to indicate excellent agreement beyond chance; 0.40–0.75, fair to good agreement; and less than 0.40, poor agreement (18).
For ROC analysis, ROC curves of MRCP, CT, and MR images were created. We also included 23 healthy patients and 24 patients with chronic cholecystitis, which represents benign gallbladder disorders, as the control group. The results were analyzed with the ROCFIT (Metz CE, Department of Radiology, University of Chicago, Ill) maximum likelihood estimation of binomial ROC curve grading data. The diagnostic accuracy of each imaging modality for each reader was evaluated by calculating the area under the ROC curve (Az). Factors with Az values greater than 0.80 were considered to have good diagnostic accuracy (19). The Az values of each imaging modality calculated from ROC curves were compared statistically by using the paired Student t test. P values of less than .05 were considered to indicate statistically significant differences. When a lesion was assigned a grade of 4 or 5 (probably or definitely adenomyomatosis of the gallbladder), it was regarded as positive for the presence of adenomyomatosis of the gallbladder. The relative sensitivity, specificity, and accuracy of each imaging technique in the diagnosis of adenomyomatosis of the gallbladder were calculated. The significance of the differences of these relative sensitivities between each imaging technique was estimated with the McNemar test (20).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The chance-corrected values that indicated the confidence levels among the three readers for image interpretation with ROC analysis are shown in Table 1. With ROC analysis, the values were excellent ( > 0.75) for MRCP and arterial phase CT images between reader 1 and reader 2. The values were fair to good ( = 0.40–0.75) for MRCP and arterial phase CT images between reader 1 and reader 3 and between reader 2 and reader 3 and for arterial phase MR images among all three readers.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Presently, US, which is a noninvasive and convenient modality, is the first choice for the evaluation of gallbladder disorders (7–9). US is also useful as a follow-up examination for adenomyomatosis of the gallbladder because it is a noninvasive modality and is conducted at lower cost. Although US is a sensitive modality for the diagnosis of adenomyomatosis of the gallbladder, it has high interobserver variability because it is dependent on the operator’s skill. Small field of view, interruption of the beam by bowel gas, obesity, or coexisting stones also make it difficult to evaluate the gallbladder wall at US. Therefore, the reported accuracies of US in the diagnosis of adenomyomatosis of the gallbladder were different and relatively low (66%) (8,9,23).
A few investigators have addressed the usefulness of CT and MR imaging for the diagnosis of adenomyomatosis of the gallbladder (14,24,25). They have suggested the usefulness of an enhancement pattern with CT and/or MR imaging in differentiating gallbladder carcinoma from adenomyomatosis of the gallbladder or chronic cholecystitis (15,16). For gallbladder carcinoma, marked enhancement is noted in the arterial phase at contrast-enhanced dynamic CT and/or MR imaging, compared with that for chronic cholecystitis. Therefore, this finding may be helpful in the differentiation between gallbladder carcinoma and other benign gallbladder disorders. Moreover, the enhancement of the mucosal layer of the gallbladder is also best shown on arterial phase contrast-enhanced dynamic CT and/or MR images among the other phases. Therefore, outpouching of the mucosa into the thickened muscular layer, which indicates Rokitansky-Aschoff sinus, may be demonstrated most clearly at arterial phase contrast-enhanced dynamic CT and/or MR imaging. For these reasons, only these images were included for imaging analysis in our study.
However, contrary to our expectation, approximately 70% of patients with adenomyomatosis of the gallbladder showed indistinguishable enhancement patterns that were similar to those in the majority of patients with gallbladder carcinoma in our study. The combined CT (unenhanced and arterial phase) and arterial phase MR images also had lower sensitivities of 25% and 29%, respectively, compared with MRCP images (63%) in the depiction of Rokitansky-Aschoff sinuses. The minimum diameter (5 mm) of the Rokitansky-Aschoff sinus, which was identified with arterial phase CT and arterial phase MR imaging, was larger than that (3 mm) identified with MRCP. Rokitansky-Aschoff sinus of less than 5 mm in diameter was not identified with each modality, and there was no interobserver variability in these patients.
In addition to the relatively lower contrast and spatial resolution of arterial phase CT and arterial phase MR imaging for evaluating small sizes of Rokitansky-Aschoff sinuses, relatively many cases (82.7%) with small sizes of Rokitansky-Aschoff sinuses, which were included in our study, may also contribute to very low sensitivities; whereas MRCP images with single-shot fast SE sequences were free from motion or susceptibility artifacts and frequently revealed Rokitansky-Aschoff sinuses within the thickened gallbladder wall. Moreover, these images have superior contrast resolution to other modalities and consistently demonstrate Rokitansky-Aschoff sinuses as high-signal-intensity structures. As a result, the mean Az value of the MRCP images was significantly higher than that of the arterial phase CT and arterial phase MR images in the differentiation of gallbladder carcinoma and adenomyomatosis of the gallbladder.
The mean specificity (92%) of the pearl necklace sign was also sufficiently high in the diagnosis of adenomyomatosis of the gallbladder. Therefore, the pearl necklace sign is specific in both the diagnosis of adenomyomatosis of the gallbladder and the differentiation between gallbladder carcinoma and adenomyomatosis of the gallbladder. In eight of 29 patients with adenomyomatosis of the gallbladder (28%), the pearl necklace sign was not identified on MRCP images. In six of the eight patients, this was due to the small size of the Rokitansky-Aschoff sinuses (<3 mm). Even MRCP images may be unable to show Rokitansky-Aschoff sinuses that are very small. In the remaining two patients, the pearl necklace sign was not found owing to compacted calcifications associated with the Rokitansky-Aschoff sinus.
Although presence of intramural calcifications helps in making a diagnosis of adenomyomatosis of the gallbladder on CT images, they may become a pitfall on MRCP images used for this purpose. In this study, one reader mistook intraduodenal fluid overlapping the gallbladder for a pearl necklace sign. The use of a negative oral contrast agent in MRCP examination may reduce such false-positive identifications.
Although there was no such case in our study group, some researchers have reported that Rokitansky-Aschoff sinuses were not identified in patients with thick bile, which has a shorter T2 value than does normal bile (14,23). Therefore, the pearl necklace sign may not be identified in these patients, particularly with single-section MRCP technique with long echo time. Thick bile, which has a shorter T1 value, also appears as high signal intensity on T1-weighted images. Additional T1-weighted images may be helpful for demonstrating Rokitansky-Aschoff sinuses.
There are several limitations of our study. The study population was relatively small. There was also bias in this retrospective study because patients with chronic cholecystitis were included as a control group and patients with other kinds of gallbladder diseases were not included. In particular, xanthogranulomatous cholecystitis may show findings similar to the pearl necklace sign because of the presence of intramural abscess or xanthogranuloma (26), although MR or MRCP findings of this disease have not yet been reported. Only images obtained with arterial phase contrast-enhanced dynamic CT and/or MR imaging were included for imaging analysis owing to some reasons described previously, though the optimal phase at contrast-enhanced dynamic CT and/or MR imaging in diagnosis of adenomyomatosis of the gallbladder has been controversial. Therefore, further investigation, including images obtained with other phases with contrast-enhanced dynamic CT and/or MR imaging, is needed to determine the absolute sensitivity, specificity, or accuracy of MRCP, CT, or MR images in the diagnosis of adenomyomatosis of the gallbladder.
Also, there have been reports of coexisting adenomyomatosis of the gallbladder and gallbladder carcinoma (27–29), though there was no such case in our study group and in other groups previously reported (14,23–25). Although cases with coexisting adenomyomatosis of the gallbladder and gallbladder carcinoma may be rare, the existence of these cases limits the ability to use the pearl necklace sign for differentiating adenomyomatosis of the gallbladder and gallbladder carcinoma. However, the majority of the gallbladder carcinomas underlying adenomyomatosis of the gallbladder, as described in the previous studies, are very small and are confined within the mucosal layer of the gallbladder wall, which results in being discovered microscopically (27–29). Therefore, authors using imaging modalities may not be able to make an accurate diagnosis for these cases. While Ootani et al (27) have reported that the prevalence of gallbladder carcinoma in patients with segmental adenomyomatosis of the gallbladder was significantly higher than that in patients with other types of adenomyomatosis of the gallbladder, the mechanism of cancer development has not been clarified. Therefore, especially in patients with segmental adenomyomatosis of the gallbladder, strict follow-up imaging examinations may be needed, even if the pearl necklace sign is demonstrated on MRCP images.
In conclusion, MRCP frequently depicted Rokitansky-Aschoff sinus within the thickened gallbladder wall (the pearl necklace sign) in the majority of patients with all morphologic types of adenomyomatosis of the gallbladder. Moreover, the pearl necklace sign was specific for adenomyomatosis of the gallbladder and was never seen in gallbladder carcinoma in our study. As a result, MRCP images were more useful than CT and arterial phase MR images in the differentiation between gallbladder carcinoma and adenomyomatosis of the gallbladder. A combination of arterial phase MR and MRCP images may be helpful for differentiation between gallbladder carcinoma and adenomyomatosis of the gallbladder when the pearl necklace sign is not identified on the MRCP images or gallbladder carcinoma coexists with adenomyomatosis of the gallbladder, especially the segmental type of adenomyomatosis. Additional prospective studies that include control subjects and patients who have all kinds of gallbladder disorders and who are referred for MRCP imaging are needed to make a more definite conclusion concerning the diagnostic usefulness of the pearl necklace sign.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, T.I.; study concepts and design, T.I.; literature research, H.H.; clinical studies, A.N., T.Y., H.S.; data acquisition, T.I., H.S.; data analysis/interpretation, T.I., T.Y.; statistical analysis, H.S.; manuscript preparation, H.H.; manuscript definition of intellectual content and editing, T.I., H.H.; manuscript revision/review, T.I.; manuscript final version approval, T.A., J.H.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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