Mucinous Tumor of the Gallbladder With a Separate Nodule of Anaplastic Carcinoma
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1 Mucinous Tumor of the Gallbladder With a Separate Nodule of Anaplastic Carcinoma Tsutomu Mizuno, MD; Tadaaki Eimoto, MD; Toyohiro Tada, MD; Hisashi Tateyama, MD; Hiroshi Inagaki, MD; Takayuki Murase, MD A case of mucinous tumor of the gallbladder with a separate nodule of anaplastic carcinoma is reported. The patient was an 83-year-old Japanese man who underwent cholecystectomy under the preoperative diagnosis of a mucus-producing gallbladder tumor. A mucinous tumor was found in the neck and distal body of the gallbladder, associated with a separate nodule in the fundus. The latter nodule was initially diagnosed as a benign xanthogranulomatous lesion. However, the immunohistochemical study revealed that the atypical cells in the superficial part of the nodule were positive for cytokeratin and epithelial membrane antigen, confirming the diagnosis of anaplastic carcinoma. Although the occurrence of mural nodules in mucinous cystic tumors of the ovary and pancreas is well reported, to our knowledge, this is the first report on the occurrence of a mucinous tumor with a nodule of anaplastic carcinoma in the gallbladder. (Arch Pathol Lab Med. 1999;123: ) Mucinous tumor of the gallbladder is extremely uncommon. We report herein a case of mucinous tumor of the gallbladder with a separate nodule of anaplastic carcinoma. The occurrence of such a nodule in mucinous cystic tumors of the ovary and pancreas is well described Although the nodule of anaplastic carcinoma was outside the mucinous tumor in the present case, an analogy can be made between this tumor and those of the ovary and pancreas. This case may provide helpful insights regarding the histogenesis of this unusual combination of tumors. REPORT OF A CASE An 83-year-old Japanese man was admitted to Johsai Hospital (Nagoya, Japan) on August 28, 1992, complaining of general fatigue. He had undergone a sigmoid colectomy in March 1991, at which time well-differentiated adenocarcinoma with submucosal invasion but no lymph node metastasis was diagnosed. Laboratory studies on admission revealed mild liver dysfunctions (glutamic oxaloacetic transaminase, 48 U/L; glutamic pyruvic transaminase, 108 U/L; alkaline phosphatase, 435 U/L; and -gluta- Accepted for publication April 28, From the Department of Pathology, School of Medicine, Nagoya City University, Nagoya, Japan. Reprints: Tsutomu Mizuno, MD, Second Department of Pathology, School of Medicine, Nagoya City University, Kawasumi 1, Mizuho-cho, Mizuho-ku, Nagoya , Japan. myl transpeptidase, 225 U/L) with elevated total bilirubin level. The chest x-ray film revealed no tumor shadows in the lung field. An abdominal ultrasound echogram and an abdominal computed tomogram revealed a tumorlike shadow in the neck and body of the gallbladder. No tumor shadow was detected among the other abdominal organs, including the pancreas. An endoscopic retrograde cholangiogram revealed a dilated common bile duct with a radiolucent filling defect. The papilla of Vater was swollen, and a mucinous secretion could be seen originating from it. Cholecystectomy was performed on October 28, 1992, based on a preoperative diagnosis of a mucus-producing gallbladder tumor. The peritoneum was found to be unremarkable at that time. The postoperative course was uneventful, but abdominal pain appeared during February Surgical exploration on April 26, 1993, revealed peritoneal dissemination of the tumor. The patient died on May 1, 1993; no autopsy was performed. PATHOLOGIC FINDINGS The resected gallbladder was dilated and filled with thick adhesive mucus. The mucus was washed out, and a cm yellowish-gray tumor was found occupying the neck and distal body of the gallbladder. The cut surface of the tumor was mucinous and solid. In addition, a cm nodule was found beneath the depressed mucosa in the fundus (Figure 1). In the neck and distal body of the gallbladder, the tumor showed columnar epithelial cells with basally situated nuclei, and the cells formed microcysts and papillae and produced abundunt mucus. No cellular or structural atypia was found in the epithelial cells on multiple sections. A pathologic diagnosis of mucinous tumor was made (Figure 2). In the fundus of the gallbladder, the separate nodule was located in the wall and partly covered with regenerative nonneoplastic epithelium. The entire nodule was initially diagnosed as a benign xanthogranulomatous lesion that showed a mixed infiltrate of foamy histiocytes and other inflammatory cells (Figure 3, A and B). For immunohistochemical study, the paraffin-embedded sections were stained using the avidin-biotin-peroxidase complex method. The primary antibodies used in the present study were as follows: cytokeratin AE1/AE3 (Dako Corporation, Copenhagen, Denmark), epithelial membrane antigen (EMA) (Dako), carcinoembryonic antigen (Dako), KP-1 (CD68) (Dako), vimentin (Dako), desmin (Dako), and HHF35 (muscle-specific actin) (Dako). The epithelial cells of the mucinous tumor were positive for cytokeratin and EMA. Staining for cytokeratin, EMA, 1280 Arch Pathol Lab Med Vol 123, December 1999 Mucinous Tumor of the Gallbladder Mizuno et al
2 Figure 1. Gross photograph of the resected gallbladder. A mucinous tumor (asterisk) is visible in the neck and distal body of the gallbladder. A separate nodule (arrow) is also found in the fundus. and vimentin showed positivity in the atypical cells located in the superficial part of the nodule (Figure 4). Cytokeratin-positive atypical cells were also positive for vimentin. There were some atypical cells that were positive for vimentin but negative for cytokeratin. Macrophages surrounding the atypical foci of the deeper part of the nodule were positive for CD68. Staining for carcinoembryonic antigen, desmin, and HHF35 yielded negative results in both the mucinous epithelial component and the cells in the nodule. Microscopic findings of the separate nodule were reevaluated. In the superficial part of the nodule, tumor cells had bizzare pleomorphic nuclei. Occasionally, tumor cells were multinucleated. Spindle-shaped tumor cells were also seen. A few ill-defined glandular spaces could be seen (Figure 3, A). The infiltration of a single tumor cell or clusters of tumor cells into the surrounding stroma could be seen. The uninvolved gallbladder mucosa was regenerative and occasionally detached. The deeper part of the nodule showed only a xanthogranulomatous reaction (Figure 3, B). Based on these findings, the histologic diagnosis of the separate nodule was changed to anaplastic carcinoma associated with xanthogranulomatous reaction. The specimen from the peritoneum obtained in exploratory surgery revealed that the tumor cells were atypical and had bizzare pleomorphic nuclei with prominent nucleoli and somewhat resembled the atypical cells in the nodule of the gallbladder fundus (Figure 3, C). The tumor cells of the peritoneum specimen were positive for vimentin only. COMMENT Mucinous tumor of the gallbladder is extremely uncommon. In this report, we describe the unusual case of a mucinous tumor having a separate nodule of anaplastic carcinoma. This nodule initially gave the erroneous impression of a benign xanthogranulomatous lesion. Immunohistochemistry, however, demonstrated that the atypical cells in the superficial part of the nodule were positive for cytokeratin and EMA, supporting their epithelial nature. Since the colon cancer in the present patient was histologically well-differentiated adenocarcinoma, the nodule was not considered to be a metastatic focus of colon cancer. The explanation of a metastasis due to a malignant peritoneal tumor, such as malignant mesothelioma, was also discounted, since no tumor had been found in the peritoneum at the time of cholecystectomy. No malignant foci were identified in the multiple sections of the mucinous tumor, so the possibility of intramural metastasis in the gallbladder was also rejected. A metastasis from an un- Arch Pathol Lab Med Vol 123, December 1999 Mucinous Tumor of the Gallbladder Mizuno et al 1281
3 Figure 2. Mucinous tumor. The tumor shows columnar epithelial cells with basally situated nuclei, forming microcysts and papillae and producing abundunt mucus (hematoxylin-eosin, original magnification 40). determined site is unlikely, because, as the result of the clinical examination before cholecystectomy, neither anaplastic carcinoma nor carcinosarcoma was found in the lungs, pancreas, or other abdominal organs. These findings, along with the histologic appearance and the later development of peritoneal metastasis, support the diagnosis of primary anaplastic carcinoma for the nodule. The occurrence of mural nodules in mucinous tumors of the ovary and pancreas is well described As the designation mural implies, the nodules usually occur in the septal walls of multicystic mucinous tumors. Although the nodule in the present case was separate from the mucinous tumor, the coexistence of these 2 types of tumors is similar to cases reported in the ovary and pancreas. The mural nodules are now recognized as a heterogenous group of tumors with associated prognoses closely related to the malignant potential of the nodules. Recently, Baergen and Rutgers 1,2 advocated the classification for mural nodules. The present case may represent an example of a mural nodule of carcinoma and reactive changes as described by Baergen and Rutgers, but the present case showed a somewhat unusual pattern of a mural nodule. Although it is important to distinguish between mural nodule subtypes, they are frequently difficult to separate by histologic methods alone because of their overlapping morphologic features. Several authors 8 12 have pointed out the usefulness of immunohistochemistry in characterizing mural nodules. Nichols et al 8 reported that the immunohistochemical study of the mural nodule revealed the strong coexpression of cytokeratin and vimentin, supporting the diagnosis of anaplastic carcinoma. The carcinomatous nature of the superficial foci of the nodule in the present case was also confirmed by immunohistochemistry. In 1982, Prat et al 5 reported a case of an ovarian mucinous tumor accompanied by cm mural nodules of anaplastic carcinoma, in which the small mural nodules developed rapidly into a widespread peritoneal metastasis; the patient died 4 months later. In this way, if the mural nodule is malignant, it may develop rapidly and may cause death, even if the nodule is small when detected. The pathogenesis of the mural nodule in mucinous tumors remains unclear, but there have been several hypotheses. Prat and Scully 4 proposed that the concept of a collison tumor, which is the result of a collision between 2 neoplasms that have arisen in adjacent areas, may be the best explanation for the pathogenesis. Fujii et al 6 reported that a sarcomalike mural nodule was one of the reactive products. Czernobilsky et al 7 reported that a mural nodule developed as a result of progressive dedifferentiation of 1282 Arch Pathol Lab Med Vol 123, December 1999 Mucinous Tumor of the Gallbladder Mizuno et al
4 Figure 3. A, Higher magnification of atypical tumor cells in the superficial part of the nodule of the gallbladder fundus. Occasionally, tumor cells are multinucleated. Spindle-shaped tumor cells are also seen. A few ill-defined glandular spaces (arrow) could be seen (hematoxylin-eosin, original magnification 100). B, The deeper part of the nodule shows only a xanthogranulomatous reaction (hematoxylin-eosin, original magnification 100). C, Metastatic tumor of the peritoneum. This shows more atypical and pleomorphic tumor cells than those in the gallbladder nodule (hematoxylin-eosin, original magnification 100). mucinous cells, with a concomitant loss of the ability to produce mucin. The separate nodule in the present case supports the collision hypothesis, with its growth and progression probably stimulated through a paracrine mechanism by the coexisting mucinous tumor. It was also surmised that the tumor cells in the metastatic peritoneal lesions became dedifferentiated and acquired a more mesenchymal character from the carcinomatous cells of the nodule. Additional case studies are necessary before the pathogenesis of this interesting lesion can be fully clarified. In conclusion, the present case of mucinous tumor of Arch Pathol Lab Med Vol 123, December 1999 Mucinous Tumor of the Gallbladder Mizuno et al 1283
5 Figure 4. A, Cytokeratin is positive in the atypical cells and the nonneoplastic mucosal epithelial cells located at the superficial part of the nodule (cytokeratin AE1/AE3, original magnification 200). B, Cytokeratin-positive atypical cells are also positive for vimentin. There are some atypical cells that were positive for vimentin but negative for cytokeratin (vimentin, original magnification 200). the gallbladder with a separate nodule of anaplastic carcinoma is, to our knowledge, the only well-documented example of this unusual combination of tumor types in this location. Its occurrence indicates that the appearance of anaplastic nodules in mucinous tumors is not limited to the ovary and pancreas. References 1. Baergen RN, Rutgers JL. Classification of mural nodules in common epithelial tumors of the ovary. Adv Anat Pathol. 1995;2: Baergen RN, Rutgers JL. Mural nodules in common epithelial tumors of the ovary. Int J Gynecol Pathol. 1994;13: Prat J, Scully RE. Ovarian mucinous tumors with sarcoma-like mural nodules: a report of seven cases. Cancer. 1979;44: Prat J, Scully RE. Sarcomas in ovarian mucinous tumors: a report of two cases. Cancer. 1979;44: Prat J, Young RH, Scully RE. Ovarian mucinous tumors with foci of anaplastic carcinoma. Cancer. 1982;50: Fujii S, Konishi I, Kobayashi F, Okamura H, Yamabe H, Mori T. Sarcomalike mural nodules combined with a microfocus of anaplastic carcinoma in mucinous ovarian tumor. Gynecol Oncol. 1985;20: Czernobilsky B, Dgani R, Roth LM. Ovarian mucinous cystadenocarcinoma with mural nodule of carcinomatous derivation: a light and electron microscopic study. Cancer. 1983;51: Nichols GE, Mills SE, Ulbright TM, Czernobilsky B, Roth LM. Spindle cell mural nodules in cystic ovarian mucinous tumors: a clinicopathologic and immunohistochemical study of five cases. Am J Surg Pathol. 1991;15: Chan YH, Ho HC, Ma L. Ovarian mucinous tumor with mural nodules of anaplastic carcinoma. Gynecol Oncol. 1989;35: Søndergaard G, Kaspersen P. Ovarian and extraovarian mucinous tumors with solid mural nodules. Int J Gynecol Pathol. 1991;10: Tsuruchi N, Kaku T, Kinoshita H, et al. Ovarian mucinous cystadenocarcinoma with sarcoma-appearing mural nodule of anaplastic carcinoma. Gynecol Oncol. 1993;50: Kessler E, Halpern M, Koren R, Dekel A, Goldman J. Sarcoma-like mural nodules with foci of anaplastic carcinoma in ovarian mucinous tumor: clinical, histological, and immunohistochemical study of a case and review of the literature. Surg Pathol. 1990;3: Rego JAG, Ruvira LV, Garcia AA, Freijanes MPS, Penaranda JMS, Soto JMR. Pancreatic mucinous cystadenocarcinoma with pseudosarcomatous mural nodules: a report of a case with immunohistochemical study. Cancer. 1991;67: Tsujimura T, Kawano K, Taniguchi M, Yoshikawa K, Tsukaguchi I. Malignant fibrous histiocytoma coexistent with mucinous tumor of the pancreas. Cancer. 1992;70: Arch Pathol Lab Med Vol 123, December 1999 Mucinous Tumor of the Gallbladder Mizuno et al
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