British Journal of Radiology 74 (2001),455-457 © 2001 The British Institute of Radiology
Hypoechoic area as an ultrasound finding suggesting subserosal invasion in polypoid carcinoma of the gall bladder
T Fujimoto, MD, SJSUM
1
Y Kato, MD
2
T Kitamura, MD, FJSUM
1 and
T Hiratsuka, MD
1
1 Department of Surgery, Hiratsuka Gastroenterological Hospital, 3-2-16 Nishi-Ikebukuro. Toshima-ku, Tokyo 171-0021
2 Department of Pathology, Cancer Institute, 1-37-1 Kami-Ikebukuro, Toshima-ku, Tokyo 170-8455, Japan
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Abstract
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Ultrasound studies have demonstrated the gall bladder wall to consist of two or more (usually three) layers. Gall bladder tumours with neither a thinned nor split outermost hyperechoic layer are confined to the mucosa or muscle layer, or have only invaded the shallow subserosa. Differentiation of these two types of tumour has posed difficulties. We report a case of polypoid gall bladder carcinoma invading the shallow subserosa with a thickened outermost hyperechoic layer but a hypoechoic area in the deeper part of the tumour. Ultrasound and pathological correlation in this case demonstrated that the hypoechoic area represented an adenocarcinoma invading the subserosa accompanied by abundant fibrosis.
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Introduction
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Ultrasound and histological correlation in gall bladder wall lesions began in the 1980s and produced a consensus on interpretation of vertical extension of gall bladder carcinomas by ultrasound, namely that gall bladder tumours with a thinned or split outermost hyperechoic layer have invaded the subserosa or serosa, respectively [1]. In contrast, those with neither a thinned nor split outermost hyperechoic layer are confined to the mucosa or muscle layer, or have only invaded the shallow subserosal fibrous layer adjacent to the muscle coat (hereafter termed the subserosal fibrous layer). However, differentiation of these latter two types has posed difficulties [2].
We present a case of polypoid gall bladder carcinoma invading the shallow subserosa with a thickened outermost hyperechoic layer but a hypoechoic area in the deeper part of the tumour on transabdominal ultrasound. We indicate the significance of the hypoechoic area in the deeper part of the tumour from ultrasound and pathological correlation.
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Case report
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An apparently healthy 83-year-old man was found to have symptomless gall stones on ultrasound during an annual physical check-up. He was referred to hospital for further examination. There was no significant past medical history. No physical or laboratory abnormalities were found. In particular, there was no elevation of carcinoembryonic antigen or carbohydrate antigen 19-9.
Transabdominal ultrasound using a Toshiba SSA-340A unit with a 3.7 MHz convex transducer (Toshiba, Tokyo, Japan) demonstrated a small amount of biliary sludge in the gall bladder and two small elevated lesions on the gall bladder neck, with slight mural thickening of the body and fundus (Figure 1
). CT demonstrated localized thickening of the wall at the neck, at a site where endoscopic retrograde cholangiography disclosed a filling defect.
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Figure 1. Transabdominal ultrasound shows an elevated lesion (white arrowheads), 25 mm x 20 mm x 11 mm in size, on the liver bed side of the gall bladder neck. Its shallow part is unevenly hyperechoic but its deep part is irregularly hypoechoic with an outermost hyperechoic layer thickened beneaththe lesion. At the peritoneal side of the neck there is another small elevated lesion (black arrows), 3–4 mm in height, with a normal outermost hyperechoic layer. The gall bladder contains a small amount of biliary sludge (black arrowheads) moving freely with changes in position.
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A polypoid gall bladder carcinoma was suspected from the ultrasound findings. Cholecystectomy with liver bed fatty tissue extirpation and regional lymph node dissection was then performed. Macroscopically, two elevated lesions were evident in the neck of the resected gall bladder, against a background of coarsely granular mucosa. Histologically, two carcinomas of the gall bladder neck were found: a mucosal carcinoma on the peritoneal side and another invading the shallow subserosa on the liver bed side, accompanied by widespread mucosal dysplasia (Figure 2). The former was a well differentiated papillary adenocarcinoma, while the latter consisted mainly of well differentiated papillary elements occupying the luminal side of the tumour and a poorly differentiated region involving the shallow subserosa accompanied by abundant fibrosis, lymphocytic infiltration and hyperplastic lymph follicles (Figure 3). Lymphatic permeation and vascular involvement were moderate, and neither perineural invasion nor other tissue involvement were found.
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Figure 2. Fixed resected specimen. The left side is the neck. There are two elevated carcinomas, 12 mm (white arrows) and 30 mm (black arrowheads) in largest diameter, respectively, with a background of coarsely granular mucosa. The smaller represents a mucosal carcinoma on the peritoneal side, and the larger lesion is a carcinoma invading the shallow subserosa on the liver bed side. A black line (A) shows the maximum section of the lesion corresponding to the section in Figure 3 . Coarsely granular mucosa represents dysplasia.
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Figure 3. Photomicrographs of the resected specimen (H&E). (a) Panoramic view of section A (Figure 2) shows a well differentiated papillary adenocarcinoma invading the shallow subserosa accompanied by abundant fibrosis and hyperplastic lymph follicles. Note that the subserosal adipose layer beneath the lesion is thickened and free from carcinoma, fibrosis or lymph follicles. (b) High power view of the shallow subserosa demonstrates small nests of adenocarcinoma accompanied by lymphocytic infiltration and fibrosis.
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The patient has remained well and without evidence of recurrence 4 years later.
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Discussion
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Since many benign lesions, dysplasias, adenomas and early carcinomas of the gall bladder can now be cured by laparoscopic cholecystectomy [3], it is important to predict the depth of invasion of the tumour as precisely as possible to proceed with appropriate treatment. Ultrasound is an accepted method for such prediction.
Ultrasound studies have demonstrated the gall bladder wall to be composed of two or more (usually three) layers [1, 4, 5]: an innermost hyperechoic layer, a middle hypoechoic layer and an outermost hyperechoic layer. There has been much discussion in regard to the interpretation of the middle hypoechoic layer. In 1986, Morita et al [1] reported that the three layers correspond to the mucosa, the muscle layer and the subserosa plus serosa, respectively. However, Aibe et al [4] considered the middle hypoechoic layer to consist not only of the muscularis propria but also the perimuscular connective tissue of the subserosa (the subserosal fibrous layer). This has been supported by Watanabe et al [5] and Yagi et al [6].
In addition, Morita and colleagues [1, 7] reported that endoscopic ultrasound could depict gall bladder carcinomas invading the subserosa with a thinned outermost hyperechoic layer. However, Fujita et al [2] considered that gall bladder carcinomas with neither a thinned nor a split outermost hyperechoic layer consisted not only of tumours confined to the mucosa or muscle layer but also those invading the subserosal fibrous layer, since the middle hypoechoic layer includes the muscle layer plus the subserosal fibrous layer. Hence, they concluded that differentiation of these two types of carcinomas was difficult. The disagreement between these two groups depends not only on the different interpretations of the middle hypoechoic layer but also on different gall bladder carcinomas invading the subserosa: Morita and colleagues [1, 7] dealt with carcinomas invading the deep subserosa composed of the adipose tissue (hereafter the subserosal adipose layer), whereas Fujita et al [2] discussed carcinomas invading the shallow subserosa. In fact, there have been few ultrasound analyses of the latter. In our case, the thickened outermost hyperechoic layer represented a subserosal adipose layer free from carcinoma. The shallow hyperechoic part of the tumour corresponded to well differentiated papillary adenocarcinoma. The deep hypoechoic area, in contrast, represented a poorly differentiated region involving the shallow subserosa accompanied mainly by abundant fibrosis. This ultrasound and pathological correlation coincides with Aibe et al's [4] interpretation and demonstrates that transabdominal ultrasound can facilitate the pre-operative evaluation of vertical extension of certain polypoid gall bladder carcinomas that have neither a thinned nor a split outermost hyperechoic layer. Thus, it does not support the conclusion of Fujita et al [2].
The ultrasound finding of a hypoechoic area within the deeper part of the tumour is not rare but is occasionally noted when gall bladder carcinoma invades the subserosa. In fact, a carcinoma invading the deep subserosa and causing a shallow hyperechoic and deep hypoechoic area with a thinned outermost hyperechoic layer is demonstrated in the cases of Mitake et al [7] and Fujita et al [2]. While they discussed only the thinned outermost hyperechoic layer and overlooked the significance of the deep hypoechoic area, we have highlighted the hypoechoic area for the first time. Mitake et al [7] presented both an ultrasound image and histology of his case, which we suspect represents a papillary adenocarcinoma invading the subserosa accompanied by abundant fibrosis. In addition, we note that a carcinoma comprises a shallow hyperechoic area and a deep hypoechoic area in the case of Pandey et al [8], whereas they neither drew attention to this dual structure nor provided an ultrasound and pathological correlation in this case.
While a polypoid gall bladder carcinoma confined to the mucosa or muscle layer with lymphocytic infiltration or fibrosis beneath the carcinoma might theoretically be overestimated on ultrasound as invading the shallow subserosa, this does not appear to be a real problem.
We therefore conclude that a polypoid gall bladder tumour with neither a thinned nor a split outermost hyperechoic layer but a hypoechoic area within the deeper part of the tumour on ultrasound should be considered as a papillary adenocarcinoma invading the shallow subserosa accompanied by abundant fibrosis.
Received for publication June 27, 2000.
Accepted for publication February 15, 2001.
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References
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Abstract
Introduction
