Hepatocellular adenomas are benign liver tumors,
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1 Case Report Hepatobiliary & Pancreatic Diseases International Pigmented well-differentiated hepatocellular neoplasm with β-catenin mutation Lara Neves Souza, Rodrigo Bronze de Martino, Richard Thompson, Sandra Strautnieks, Nigel D Heaton and Alberto Quaglia London, UK ABSTRACT: According to the most recent WHO classification of hepatocellular adenomas, a small percentage of inflammatory hepatocellular adenomas presents with mutation in the β-catenin gene and are at higher risk of malignant transformation. It has been recognized that adenoma-like hepatocellular neoplasms with focal atypia, or in unusual clinical context present with similar cytogenetic and immunohistochemistry characteristics to well-differentiated hepatocellular carcinomas. We report a case of a well-differentiated hepatocellular neoplasm with Dubin-Johnson-like pigment displaying histological features overlapping with a β-catenin mutated inflammatory adenoma and a well-differentiated hepatocellular carcinoma in a non-cirrhotic liver. The patient was a 48-year-old woman, who was asymptomatic, and had a clinical history of intra-uterine exposure to diethylstilbestrol, previous cancers and past oral contraceptive use. The recently proposed term "well-differentiated hepatocellular neoplasm of uncertain malignant potential" should be applied in such cases to highlight the different pathogenesis and risk of malignancy compared to the typical adenomas, and to suggest a careful and customized clinical management. (Hepatobiliary Pancreat Dis Int 2015;14: ) KEY WORDS: hepatocellular adenoma; hepatocellular carcinoma; β-catenin; glutamine synthetase; diethylstilbestrol Author Affiliations: Institute of Liver Studies, King's College Hospital, Denmark Hill, SE5 9RS, London, UK (Neves Souza L, de Martino RB, Thompson R, Strautnieks S, Heaton ND and Quaglia A); Department of Gastroenterology, Discipline of Liver and Gastrointestinal Transplantation, Hospital das Clínicas, University of São Paulo, São Paulo, Brazil (de Martino RB) Corresponding Author: Nigel D Heaton, Professor, Institute of Liver Studies, King's College Hospital, Denmark Hill, SE5 9RS, London, UK (Tel: ; Fax: ; nigel.heaton@nhs.net) 2015, Hepatobiliary Pancreat Dis Int. All rights reserved. doi: /S (15) Published online May 21, Introduction Hepatocellular adenomas are benign liver tumors, which usually arise in women following oral contraceptive use. [1] Adenomas are known to be at risk of bleeding and malignant transformation, and for that reason they are usually treated with resection. [2] Inflammatory or telangiectatic adenomas comprise more than 50% of hepatocellular adenomas, usually affect women, and are associated with obesity and fatty liver disease. β-catenin mutated hepatocellular adenomas usually display more atypical features than other subtypes and their differentiation from well-differentiated hepatocellular carcinoma (HCC) is often difficult. [3] Pigmented hepatocellular adenomas, so called black adenomas, are a rare variant of hepatocellular adenoma, with few cases reported in the literature. [4-11] Macroscopically, pigmented adenomas are characteristically dark grey or black in color, due to the presence of pigment granules in hepatocyte cytoplasm resembling the pigment observed in patients with Dubin-Johnson syndrome. [12] Of the 9 cases of pigmented hepatocellular lesions previously reported, 4 were classified as benign, 2 as malignant, and in the remaining 3 malignancy could not be excluded. [4-11] Herein we report a case of pigmented hepatocellular neoplasm with histological features overlapping a β-catenin mutated inflammatory adenoma and a well-differentiated HCC, arising in a patient with a peculiar clinical history including intra-uterine exposure to diethylstilbestrol, previous cancers, and oral contraceptive use. Case report Clinical features and laboratory findings A 48-year-old woman was referred with an incidental radiologic finding of a liver lesion. She had been treated by laparoscopic hysterectomy for an endometrial carcinoma 2 years earlier. In addition, she had been found to have 660 Hepatobiliary Pancreat Dis Int,Vol 14,No 6 December 15,2015
2 Pigmented hepatocellular neoplasm and β-catenin mutation an incidental transitional cell carcinoma of the bladder. There was no history of smoking or chronic liver disease. She had a history of asthma and received a variety of inhaled medications and one short course of oral steroid therapy. Furthermore, she took oral contraceptive medication for 2 years, approximately at 14 years before presenting with the liver lesion. Of note, her mother was prescribed diethylstilbestrol during her pregnancy. The physical examination was unremarkable. Laboratory values included serum α-fetoprotein: 8 kiu/l (reference <7 kiu/l), total bilirubin: 4 μmol/l (reference 3-20 μmol/l), AST: 19 IU/L (reference IU/L), hemoglobin: 142 g/l (reference g/l), and platelets count: /L (reference /L). CT scan showed a neoplasm suggestive of adenoma of 3.5 cm in segment VII of the liver. The patient had a biopsy of the liver lesion prior to the referral, which showed a hepatocellular proliferation, with features that overlapped with hepatocellular adenoma, focal nodular hyperplasia, and well-differentiated HCC. Non-anatomical hepatectomy was performed to remove the lesion with the majority of segments VII and VIII. The postoperative clinical course was uneventful and the patient was discharged without any complication. Histological findings The liver specimen revealed a 3.0 cm subcapsular nodule, well-demarcated and non-encapsulated. The lesion exhibited a black homogeneous soft cut surface, and presented a thin ridge of horizontal spread beneath the liver capsule, 1-2 mm thick. No satellite tumors were identified. The background liver showed a homogeneous light tan, soft smooth parenchymal surface. Microscopically, the lesion was composed of pigmented, often steatotic hepatocytes, surrounded by a fibrous capsule (Fig. 1). Some areas displayed one to two cell-thick hepatocyte plates, with maintained reticulin framework, and minimal hepatocyte atypia, whilst other portions showed thick plates of hepatocytes with markedly rarefied reticulin framework (Fig. 2), and obvious atypical, sometimes multinucleated hepatocytes. Both areas coexisted throughout the tumor and seemed to merge diffusely. Two mitotic figures were identified (Fig. 3). The lesion included fibrous septa with thick-walled, unpaired arteries (with no correspondent bile ducts) and a mainly lymphocytic inflammatory infiltrate (Fig. 4). Some areas of hemorrhage were observed. There was no sinusoidal dilatation or confluent necrosis. The fibrous capsule surrounding the tumor presented focal discontinuity, where tumor hepatocytes blended with nearby non-lesional liver. The subcapsular peripheral ridge observed macroscopically corresponded to an area of horizontal spread of the neoplasm. No vascular invasion or satellite nodules were identified. The resection margin was free. Masson-Fontana stained in dark brown the coarse cytoplasmic pigment within tumor hepatocytes (Fig. 5). The background liver showed preserved lobular architecture, moderate steatosis, scattered clusters of neutrophils and many hepatocytes featuring vacuolated nuclei. Fig. 1. Neoplasm comprising hepatocytes with brown pigment and steatosis, surrounded by a fibrous capsule (arrowheads) containing ectatic vessels (arrow) and unpaired arteries (asterix) (HE, original magnification 40). Fig. 2. Reticulin stain demonstrating distinct patterns in the neoplasm: normal one-cell-thick to two-cell-thick hepatocyte cords (left), and irregularly thickened cords (right) (original magnification 10). Fig. 3. Some areas showed tumor hepatocytes arranged in thick-cell plates, displaying atypical, multinucleated nuclei (arrows), steatosis, and cytoplasmic pigment (HE, original magnification 100). The inset shows a mitotic figure in a different area of the tumor (original magnification 400). Hepatobiliary Pancreat Dis Int,Vol 14,No 6 December 15,
3 Hepatobiliary & Pancreatic Diseases International Glutamine synthetase immunohistochemistry revealed diffuse and strong positivity in the cytoplasm of tumor hepatocytes in contrast to the background hepatocytes, which presented the normal pattern of glutamine synthetase positivity restricted to perivenular areas (Fig. 6). Fig. 4. The neoplasm displayed fibrous septa with thick-walled, unpaired arteries (arrow), and permeating inflammatory infiltrate (HE, original magnification 100). The inset shows the inflammatory cells were predominantly lymphocytes (original magnification 400). Fig. 5. The coarse pigment within lesional hepatocytes appeared dark brown on Masson-Fontana stain (original magnification 200). Fig. 6. Glutamine synthetase expression was strong and diffuse throughout neoplastic hepatocytes (right), and restricted to the perivenular region in background liver (left) (glutamine synthetase immunostain, original magnification 40). The inset depicts the β-catenin immunostain of the same area, showing nuclear expression of β-catenin in tumor hepatocytes (left), contrasting with negative surrounding liver (right). There was strong and diffuse nuclear β-catenin staining throughout the lesion, and the same stain was absent in the surrounding liver (inset Fig. 6). The tumor was diffusely positive for serum amyloid A in contrast to the negative background liver. Expression of fatty acid binding protein was faint and patchy both in lesional and non-lesional hepatocytes. Immunohistochemistry to glypican 3 was completely negative in the neoplasm. CD34 sinusoidal staining was present only in atypical areas of the neoplasm. Multidrug resistance-associated protein 2 was positive in both lesional and non-lesional hepatocytes. Genetic analysis was performed on frozen tissue from both the tumor and background liver, and showed a deletion in β-catenin gene CTNNB1, encompassing intron 2, exon 3, and exon 4. This mutation was present at low level in one sample of background liver. The deleted copy only, was detectable in the tumor. Discussion Hepatocellular adenomas usually affect young women, and are generally considered to have an estimated prevalence of malignant transformation of around 4.2%. [2] The decision between surveillance and resection will depend on tumor size and appearance. Lesions greater than 5 cm are frequently treated with resection, particularly if patients have fatty liver and/or other risk factors for developing HCC. [13] In the current case, the recommendation for surgical resection was based on the inability to exclude HCC on biopsy, in a patient with risk factors for developing malignancy, including history of diethylstilbestrol exposure and two previous cancers. Of 9 pigmented adenomas previously reported in the literature, 4 developed in women and 5 in men, aged from 28 to 65 years old. [4-11] In most cases, the patients were asymptomatic, and the index lesion was incidentally diagnosed on radiological imaging, ranging from 2.5 to 16 cm in diameter. Only 2 cases of HCC containing Dubin-Johnson-like pigment in patients without evidence of Dubin-Johnson syndrome have been recorded in the literature. [7, 14] The case reported by Hechtman et al [7] consisted of a microscopic HCC within a 16 cm inflammatory pigmented adenoma in a 53-year-old male patient, whereas the tumor reported by Roth et al [14] was a 12 cm well circumscribed lesion in a 62-year-old man. Both patients had no history of liver disease, neoplasm or steroid use. Diethylstilbestrol is a synthetic oestrogen considered to have a transplacental carcinogenic activity that targets the uterus, ovaries, urinary bladder and liver. [15] It used to be prescribed until the 1970s in women with high-risk 662 Hepatobiliary Pancreat Dis Int,Vol 14,No 6 December 15,2015
4 Pigmented hepatocellular neoplasm and β-catenin mutation pregnancy to prevent miscarriage. Diethylstilbestrol has been shown to pass through the placenta and has a direct effect on the developing fetus, producing abnormalities which can be present later in life. [16] Although a large follow up study found consistent evidence of increased risk for vaginal, uterine and breast cancer following diethylstilbestrol exposure, [17] the overall carcinogenic impact of this oestrogen still needs to be established. Given the history of previous bladder and uterine cancer, diethylstilbestrol may have contributed to the development of the liver neoplasm in our patient. The current classification of hepatocellular adenomas proposed by Bioulac-Sage et al, and updated by the WHO, divides these tumors in four subtypes according to genotype and histological characteristics: HNF1A mutated, β-catenin mutated, inflammatory and unclassified adenomas. β-catenin mutated hepatocellular adenomas comprise 10% of adenomas, and show strong and diffuse expression of glutamine synthetase and nuclear β-catenin, as a result from the mutation of the β-catenin gene, which upregulates glutamine synthetase expression. This subtype usually affects men with metabolic conditions, such as glycogenosis, or with history of androgens use, and often presents nuclear atypia, and/or pseudoglandular growth pattern on histology. [18] Based on observations of β-catenin mutated HCC displaying well-differentiated adenoma-like areas, and coexistent HCC and β-catenin mutated adenomas in the same liver, this subtype of hepatocellular adenoma is considered to have a greater risk of malignant transformation. [2] Nonetheless, it is not clear if these tumors occur following malignant transformation of β-catenin mutated adenomas, or if they are HCCs from the beginning. Because of the overlapping histological and molecular features, the distinction between β-catenin mutated hepatocellular adenomas and well-differentiated HCC may be very difficult. [18] Inflammatory or telangiectatic adenomas comprise 55% of all hepatocellular adenomas, and show a strong diffuse expression of inflammatory markers and a combination of inflammation, sinusoidal dilatation, congestion, septa with unpaired, thick-walled arteries and ductular reaction. They occur mostly in obese women with fatty liver disease. Approximately 10% of inflammatory HCCs have been found to have evidence of activating mutation in the β-catenin gene, and therefore overlap with β-catenin mutated hepatocellular adenoma. These cases are considered to be at particular risk of malignant transformation. [18] Adenoma-like hepatocellular neoplasms displaying focal atypical morphological features or occurring in unusual clinical settings, such as in men or women older than 50 years or younger than 15, have been shown to present cytogenetic and immunohistochemical characteristics typical of well-differentiated HCC. Despite morphologically mimicking adenoma, these tumors may recur and metastasize, and therefore may actually represent well-differentiated forms of HCC. [3] A recently published study on HCCs arising within adenomas found the same immunohistochemical and cytogenetic features expressed in both adenoma-like and carcinoma-like areas of neoplasms, and concluded that the adenoma portions of those tumors represent an extremely well-differentiated variant of HCC. [19] Bedossa et al [20] reviewed cases of unusual well-differentiated hepatocellular neoplasms, 3 of which were initially diagnosed as pigmented/black adenomas, and proposed a new diagnostic category to address lesions that cannot be confidently classified as either hepatocellular adenoma or carcinoma: "well-differentiated hepatocellular neoplasm of uncertain malignant potential". Our case presented a distinctive combination of features that overlap with inflammatory adenoma, β-catenin mutated hepatocellular adenoma and well-differentiated HCC. The areas displaying bland hepatocytes, sometimes steatotic, preserved reticulin framework, fibrous septa with thick-walled arteries and inflammatory infiltrate, and expression of serum amyloid A, fit with a typical inflammatory/telangiectatic adenoma. On the other hand, the strong and diffuse glutamine synthetase and β-catenin positivity throughout the tumor, the genetic mutation, and presence of areas with atypical hepatocytes point toward a β-catenin mutated adenoma. Finally, the loss of reticulin framework in some portions, with CD34 sinusoidal expression, focal mitotic activity and loss of a well-defined tumor border, favor the classification of this tumor as an HCC. Unlike the case reported by Hechtman et al, in which the HCC arose in a background of a β-catenin mutated pigmented telangiectatic adenoma as a nodule-withinnodule, [7] in our case adenoma-like and carcinoma-like areas merged diffusely. The underlying complex clinical history suggests that the risk of malignancy in this patient deviates from what is usually observed in conventional adenomas arising in women at reproductive age on oral contraceptives, and the term "well-differentiated hepatocellular neoplasm of uncertain malignant potential" should be applied to highlight the lesion unpredictable nature and suggest a careful and customized clinical management. [20] In summary, pigmented hepatocellular lesions with Dubin-Johnson-like pigment are rare, and for this reason their pathogenesis, risk factors, histological and clinical behaviour, including malignant potential, are not well defined. Well-differentiated hepatocellular neoplasms developing in unusual clinical context or with atypical Hepatobiliary Pancreat Dis Int,Vol 14,No 6 December 15,
5 Hepatobiliary & Pancreatic Diseases International histology should not be considered as conventional adenomas, and the term "well-differentiated hepatocellular neoplasm of uncertain malignant potential" fits with this approach. Future studies regarding such hepatocellular neoplasms should be performed, including clinical, molecular and immunohistochemical correlation, in order to clarify their pathogenesis and allow a more appropriate classification and patient stratification. Contributors: NSL and MRB collected the data and wrote the first draft. TR and SS performed genetic analysis. QA performed histological analysis and reviewed the paper. HND performed the surgery and reviewed the paper. All authors contributed to the design and interpretation of the study and to further drafts. HND is the guarantor. Funding: None. Ethical approval: Not needed. Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. References 1 Reddy KR, Kligerman S, Levi J, Livingstone A, Molina E, Franceschi D, et al. Benign and solid tumors of the liver: relationship to sex, age, size of tumors, and outcome. Am Surg 2001;67: Stoot JH, Coelen RJ, De Jong MC, Dejong CH. Malignant transformation of hepatocellular adenomas into hepatocellular carcinomas: a systematic review including more than 1600 adenoma cases. HPB (Oxford) 2010;12: Evason KJ, Grenert JP, Ferrell LD, Kakar S. Atypical hepatocellular adenoma-like neoplasms with β-catenin activation show cytogenetic alterations similar to well-differentiated hepatocellular carcinomas. Hum Pathol 2013;44: Hasan N, Coutts M, Portmann B. Pigmented liver cell adenoma in two male patients. Am J Surg Pathol 2000;24: Masuda T, Beppu T, Ikeda K, Ishiko T, Chikamoto A, Hayashi H, et al. Pigmented hepatocellular adenoma: report of a case. Surg Today 2011;41: Ye MQ, Suriawinata A, Ben Haim M, Parsons R, Schwartz ME. A 42-year-old woman with liver masses and long-term use of oral contraceptives. Semin Liver Dis 1999;19: Hechtman JF, Raoufi M, Fiel MI, Taouli B, Facciuto M, Schiano TD, et al. Hepatocellular carcinoma arising in a pigmented telangiectatic adenoma with nuclear β-catenin and glutamine synthetase positivity: case report and review of the literature. Am J Surg Pathol 2011;35: Bernard PH, Blanc JF, Paulusma C, Le Bail B, Carles J, Balabaud C, et al. Multiple black hepatocellular adenomas in a male patient. Eur J Gastroenterol Hepatol 2000;12: Vij M, Patra S, Rela M. Pigmented hepatocellular adenoma with complete CD34 immunostaining pattern: a diagnostic dilemma. Indian J Pathol Microbiol 2012;55: Koea JB, Kua H. Pigmented liver cell adenoma: rare but benign. ANZ J Surg 2012;82: Ferko A, Bedrna J, Nozicka J. Pigmented hepatocellular adenoma of the liver caused by long-term use of phenobarbital. Rozhl Chir 2003;82: Thompson RJ, Portmann BC, Roberts EA. Genetic and metabolic liver disease. In: Burt AD, Portmann BC, Ferrell LD, editors. MacSween's Pathology of the Liver. 6th ed. Edinburgh, London, New York, Oxford, Philadelphia, St Louis, Sydney, Toronto: Elsevier; 2012: Terkivatan T, de Wilt JH, de Man RA, van Rijn RR, Zondervan PE, Tilanus HW, et al. Indications and long-term outcome of treatment for benign hepatic tumors: a critical appraisal. Arch Surg 2001;136: Roth JA, Berman E, Befeler D, Johnson FB. A black hepatocellular carcinoma with Dubin-Johnson-like pigment and Mallory bodies: a histochemical and ultrastructural study. Am J Surg Pathol 1982;6: Waalkes MP, Liu J, Ward JM, Diwan BA. Enhanced urinary bladder and liver carcinogenesis in male CD1 mice exposed to transplacental inorganic arsenic and postnatal diethylstilbestrol or tamoxifen. Toxicol Appl Pharmacol 2006;215: Newbold RR. Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 2004;199: Troisi R, Hatch EE, Titus-Ernstoff L, Hyer M, Palmer JR, Robboy SJ, et al. Cancer risk in women prenatally exposed to diethylstilbestrol. Int J Cancer 2007;121: Bioulac-Sage P, Balabaud C, Wanless I. Focal nodular hyperplasia and hepatocellular adenoma. In: Bosman FT, Carneiro F, Hruban RH, Theise ND, editors. WHO Classification of Tumors of the Digestive System. 4th ed. Lyon: WHO; 2010: Kakar S, Grenert JP, Paradis V, Pote N, Jakate S, Ferrell LD. Hepatocellular carcinoma arising in adenoma: similar immunohistochemical and cytogenetic features in adenoma and hepatocellular carcinoma portions of the tumor. Mod Pathol 2014;27: Bedossa P, Burt AD, Brunt EM, Callea F, Clouston AD, Dienes HP, et al. Well-differentiated hepatocellular neoplasm of uncertain malignant potential: proposal for a new diagnostic category. Hum Pathol 2014;45: Received July 25, 2014 Accepted after revision December 8, Hepatobiliary Pancreat Dis Int,Vol 14,No 6 December 15,2015
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