Primary Liver Carcinoma Arising in People Younger Than 30 Years
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1 Anatomic Pathology / PRIMARY LIVER CARCINOMA Primary Liver Carcinoma Arising in People Younger Than 30 Years Walter M. Klein, MD, 1 Ernesto P. Molmenti, MD, 2 Paul M. Colombani, MD, 2 Davinder S. Grover, 2 Kathleen B. Schwarz, MD, 3 John Boitnott, MD, 1 and Michael S. Torbenson, MD 1 Key Words: Hepatocellular carcinoma; Fibrolamellar carcinoma; Cytokeratin 7; Foci of altered hepatocytes DOI: /TT0R7KAL32228E99 Abstract Primary liver carcinomas in children and young adults are uncommon and poorly described. We examined primary liver carcinomas in people younger than 30 years and performed immunostains for markers of biliary (cytokeratin [CK] 7, CK19, CD56) and hepatocellular (HepPar) differentiation. We found 23 primary liver carcinomas: 13 hepatocellular carcinomas (HCCs), 9 fibrolamellar carcinomas (FLCs), and 1 cholangiocarcinoma. Most HCCs showed compact (n = 7) or trabecular (n = 4) growth patterns. The Edmondson grades were as follows: 1, 3 tumors; 2, 8 tumors; and 3, 2 tumors. All HCCs and FLCs were HepPar+. All FLCs and 7 of 9 HCCs were CK7+. In contrast, a control group of 65 adult HCCs showed less CK7 positivity (24 [37%]; P =.03). CK19 was positive in 2 HCCs and CD56 in 1 HCC. No chronic background liver disease was seen, although 3 cases showed foci of altered hepatocytes. HCCs are the most common primary liver carcinoma in children and young adults, followed by FLCs. They are morphologically similar to adult HCC, but more likely to be CK7+. Primary hepatic carcinomas are rare in children and young adults, accounting for approximately 1% of tumors in people younger than 20 years. 1 Of these, approximately two thirds are hepatoblastomas, whereas most of the remainder are primary hepatocellular carcinomas (HCCs). 1 Unlike HCC in adults, the risk factors for pediatric HCC are poorly understood. Although case reports have described pediatric HCC in association with a wide variety of congenital anomalies and metabolic diseases, a recent, large, epidemiologic study found that underlying liver or metabolic disease was absent in most cases of pediatric HCC. 1 Furthermore, epidemiologic evidence strongly suggests that risk factors for HCC in children and young adults are different from those in adults. 1 It is unclear, however, whether histologic differences can be found between HCC arising in children and young adults and those arising in adults. Thus, we undertook a retrospective study to examine the histologic features of these tumors. In addition, we carefully examined sections of background nonneoplastic liver samples for evidence of chronic liver disease. We anecdotally had noted immunophenotypic differences in pediatric HCC, with pediatric cases frequently showing strong cytokeratin (CK) 7 positivity, and further studied these tumors with immunostains for CK7, CK19, CD56, and HepPar. CK7 and CK19 are well-recognized markers of biliary differentiation, but numerous studies also have demonstrated positivity in a modest proportion of adult HCCs. 2-5 CD56 is expressed in biliary epithelium in some biliary tract diseases 6 and in approximately 25% of cholangiocarcinomas 7 but not in hepatocytes. HepPar is a marker of hepatocyte differentiation. 512 Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99
2 Anatomic Pathology / ORIGINAL ARTICLE Materials and Methods Tissue Sample Selection All available cases of primary liver carcinoma from January 1984 to January 2003 at the Johns Hopkins Hospital, Baltimore, MD, in persons younger than 30 years were examined. We decided to include all people younger than 30 years based on epidemiologic findings that demonstrate a steady baseline incidence of liver carcinoma before age 40, when the incidence increases dramatically as a consequence of chronic liver disease. 8 Hepatoblastomas were excluded. H&E-stained sections and multiple 5-µm unstained sections for subsequent immunohistochemical analysis were cut from formalin-fixed, paraffin-embedded sections. The morphologic features of the HCCs were determined by using the World Health Organization classification (trabecular/macrotrabecular, pseudoglandular/acinar, compact, and scirrhous), and the tumors were graded using the modified Edmondson nuclear grading system. 9 Nonneoplastic liver tissue samples were evaluated for underlying liver disease. Reticulin stains were performed on cases with H&E findings that suggested nodular regenerative hyperplasia. The medical records and laboratory findings also were reviewed for causes of chronic liver disease. Immunohistochemical Analysis Antigen retrieval was performed for 5 minutes in 0.01 mol/l of sodium citrate buffer. Sections then were treated with monoclonal antibodies against CK7 (dilution 1:500; DAKO, Carpinteria, CA), CK19 (dilution 1:10; DAKO), CD56 (dilution 1:100; Zymed, San Francisco, CA), and HepPar (dilution 1:100; DAKO). Ki-67 immunostains also were performed on selected sections (dilution 1:1,000; DAKO). The Envision kit (DAKO) was used according to the manufacturer s instructions. The sections stained for CK7, CK19, and CD56 were evaluated in a semiquantitative scoring system of 0 to 3 based on the percentage of tumor cells labeled: 0, no labeling or focal positivity less than 5%; 1+, 5% to 33% of cells; 2+, 34% to 66% of cells; and 3+, greater than 66% of cells. Intensity of staining was scored as weak (1+), moderate (2+), and strong (3+). Control Groups As a control group for the frequency of CK7 staining, tissue arrays containing 65 HCCs from adults older than 40 years also were stained for CK7 as described. The tissue arrays were constructed at Johns Hopkins from formalin-fixed, paraffin-embedded tissue samples from the surgical pathology archives. The average ± SD age at resection for these adult cases was 63 ± 13 years (range, years). The distribution of the modified Edmondson nuclear grades was as follows: 1, 12 (18%); 2, 24 (37%); 3, 25 (38%); and 4, 4 (6%). Fibrolamellar carcinomas (FLCs) were excluded from this control group. When studying the background liver samples of cases with HCC, we noted discrete foci of altered hepatocytes (FAH). To betters understand these FAH, we examined 4 separate control groups for the presence of FAH: colon carcinoma metastatic to the liver with no underlying liver disease (n = 25), HCCs in adults older than 40 years with cirrhotic background liver samples (n = 25), HCCs in adults older than 40 with background liver samples showing no significant fibrosis (n = 25), and hepatoblastomas (n = 15). Results We identified 23 cases of primary liver carcinoma, including 13 HCCs (57%), 9 FLCs (39%), and 1 intrahepatic cholangiocarcinoma (4%). There was a slight male predominance (13 males, 10 females). No cases were associated with congenital anomalies or metabolic or other recognized inherited diseases. At the initial examination, the serum α-fetoprotein level was elevated in 6 (46%) of 13 cases Table 1. Three patients with typical HCC had known chronic hepatitis B virus (HBV) infection (Table 1), whereas none of the remaining patients had identifiable chronic liver disease at the clinical or histologic level. In 1 case (case 11), the HCC was associated with and seemed to arise out of a hepatic adenoma. The available records for this case did not indicate use of oral contraceptive pills or other exposure to exogenous estrogens or androgens. Histologic Features of HCC The 13 patients with HCC included 8 males and 5 females with a mean age of 19.3 years (range, 4-27 years). Of these 13 cases, 10 specimens were obtained from resections and 3 from needle biopsies. The architectural growth patterns were compact (n = 7), trabecular (n = 4), macrotrabecular (n = 1), and combined trabecular/compact (n = 1). The modified Edmondson grades were as follows: 1, 3; 2, 8; and 3, 2. Three HCCs had areas of tumor composed of small, round-to-oval clusters of hepatocytes embedded in fibrous stroma somewhat resembling biliary-type differentiation Image 1A. Extensive necrosis was seen in 4 cases and angiolymphatic invasion in 4 cases. Histologic Features of Cholangiocarcinoma The 1 intrahepatic cholangiocarcinoma was from a resection specimen from a 25-year-old man with no evidence of chronic biliary tract disease. The histologic findings were those of a typical cholangiocarcinoma. Tumor necrosis and angiolymphatic invasion were present. Immunohistochemical Findings in HCC Sufficient tissue for immunohistochemical analysis was present in 9 of 13 HCC cases. All 9 HCCs were strongly (3+) Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99 513
3 Klein et al / PRIMARY LIVER CARCINOMA Table 1 Histologic and Immunohistochemical Findings in 13 HCCs and 1 Cholangiocarcinoma Case No./ Specimen Growth Nuclear Serum AFP HBV CK7 CK19 Sex/Age (y) Type Pattern Grade (ng/ml) * Test Result Other Findings (I/D) (I/D) Hepatocellular carcinoma 1/F/4 Resection Compact 2 500,000 Fatty change in nonneoplastic 2+/2+ 0/0 liver; s/p embolization 2/M/10 Resection Compact 2 78,000 Fatty change in nonneoplastic 0/0 0/0 liver; tumor necrosis, s/p radiation and chemotherapy, ALI 3/M/13 Resection Compact 2 Normal Nonneoplastic liver with nodular NA NA regenerative hyperplasia; tumor with necrosis, ALI 4/M/13 Needle biopsy Macrotrabecular 1 2,202,600 HBsAg+;HBeAg ; NA NA HBeAb+ 5/M/16 Resection Trabecular 2 437,015 Tumor with necrosis, ALI 0/0 0/0 6/F/22 Resection Compact 1 ND ND 3+/2+ 0/0 7/M/22 Needle biopsy Compact 1 380,000 HBsAg+; HBeAg+; Cirrhosis NA NA HBeAb 8/F/23 Resection Trabecular and 3 644,000 HBsAg+; HBeAg ; FAH in nonneoplastic liver; s/p 3+/3+ 1+/1+ compact HBeAb+ radiation and chemotherapy 9/M/25 Resection Compact 2 Normal Tumor CD56+ 1+/1+ 1+/1+ 10/F/25 Resection Trabecular 2 Normal 3+/2+ 0/0 11/F/25 Resection Trabecular 3 Normal Tumor seems to have developed 3+/3+ 0/0 out of hepatic adenoma 12/M/26 Resection Compact 2 Normal s/p chemoembolization 1+/1+ 0/0 13/M/27 Needle biopsy Trabecular 2 ND s/p chemotherapy NA NA Cholangiocarcinoma 14/M/25 Resection Cholangio- Normal FAH in nonneoplastic liver; tumor 3+/3+ 2+/1+ carcinoma necrosis, ALI ALI, angiolymphatic invasion; AFP, α-fetoprotein; CK, cytokeratin; FAH, focus of altered hepatocytes; HBeAb, hepatitis B e antibody; HBeAg, hepatitis B e antigen; HBsAg hepatitis B surface antigen; HBV, hepatitis B virus; I/D, intensity/distribution (see text); NA, no tissue available for immunohistochemical analysis; ND, not done; s/p, status post; +, positive;, negative. * Results are given in conventional units; to convert to Système International units (µg/l), multiply by 1.0. and diffusely positive for HepPar. Of the 9 typical HCCs, 7 (78%) were positive for CK7 Image 1B. Immunohistochemical staining for CK7 was weak (n = 2 cases), moderate (n = 1 case), and strong (n = 4 cases). In contrast, CK7 positivity was less common in control adult HCCs, 24 of 65 (37%; P =.03; Yates-corrected χ 2 ). In the adult samples, CK7 staining did not correlate with the degree of background liver fibrosis. CK7 was positive in 15 (38%) of 39 with advanced fibrosis or cirrhosis and 9 (35%) of 26 without significant fibrosis (P =.11). Immunohistochemical staining for CK19 was positive in 2 (22%) of 9 HCCs with weak intensity Image 1C. One HCC was strongly and diffusely positive for CD56 in a membranous manner Image 1D. Immunohistochemical Findings in Cholangiocarcinoma The intrahepatic cholangiocarcinoma was negative for HepPar and CD56 but was strongly positive for CK7 in a diffuse distribution and moderately positive for CK19 in a patchy distribution. Fibrolamellar Carcinoma We identified 9 FLCs Image 1E in 4 males and 5 females with a mean age of 20.0 years (range, years). Of these 9 cases, 4 were obtained from resection specimens, 4 from wedge biopsies, and 1 from a needle biopsy. Significant necrosis was seen in 2 of 9 cases. All FLCs were strongly and diffusely positive for HepPar. CK7 was moderately to strongly positive in all 9 cases (100%) of FLC Image 1F. Immunohistochemical staining for CK19 and CD56 was negative in all cases. Histologic Features of the Background Liver Samples Sections were available to review the background liver samples in 7 of 14 HCC cases, the cholangiocarcinoma case, and 3 of 9 FLC cases. Three cases of typical HCC were known to arise in the setting of chronic HBV infection (Table 1). Sections of background liver were available in 2 of 3 of the HBV-associated cases and showed minimal chronic inflammation and no fibrosis. In the third HBVassociated case (case 7), the surgical pathology report indicated that the background liver was cirrhotic, although slides and blocks were not available for confirmation. An additional 2 cases showed patchy mild fatty change in the nonneoplastic liver samples. The background liver samples showed mild nodular regenerative hyperplasia in 1 case of HCC and 2 cases of FLC. None of the remaining cases showed chronic hepatitis or fibrosis. 514 Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99
4 Anatomic Pathology / ORIGINAL ARTICLE A B C D E F Image 1 A, Hepatocellular carcinoma (HCC) with a trabecular growth pattern (H&E, 100); inset from the same case shows a focus with a biliary-like growth pattern (H&E, 200). B, HCC positive for cytokeratin (CK) 7 in a 3+/3+ manner; inset with more focal CK7 staining, 2+/1+ ( 200). C, HCC positive for CK19 in a 2+/1+ manner ( 200). D, HCC with CD56 staining in a membranous manner ( 200). E, Typical fibrolamellar carcinoma (H&E, 200). F, Fibrolamellar carcinoma positive for CK7 in a 3+/3+ manner. Adjacent nonneoplastic bile ducts also are positive ( 200). See the text for an explanation of the scoring for staining. Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99 515
5 Klein et al / PRIMARY LIVER CARCINOMA Despite the lack of chronic hepatitis and fibrosis, the background nonneoplastic liver samples showed discrete FAH in 1 of the 7 HCC cases, 1 of 3 FLC cases, and the intrahepatic cholangiocarcinoma. FAH were microscopically of 2 types: The first (found in the cholangiocarcinoma case) showed large, pale hepatocytes without fatty change Image 2A, essentially identical to those described by Su et al 10 as glycogen storing foci (FAH-GS). The second (found in the HCC and FLC cases) was characterized by circumscribed, nodular foci of smaller hepatocytes with an increased nuclear/cytoplasmic ratio, fatty change, and occasional extramedullary hematopoiesis Image 2B and Image 2C. Both types were demarcated sharply from the surrounding liver and were readily apparent at scanning power magnification. In the HCC and intrahepatic cholangiocarcinoma cases, multiple FAH were found that varied from 0.3 to 0.6 mm. The FLC case revealed a single focus measuring approximately 6 mm. None of these FAH were identified during original gross processing of the specimens. Tissue blocks were available for immunohistochemical analysis for 2 of 3 cases with FAH (HCC and FLC cases). The FLC case demonstrated moderate 2+ staining for CK7 and an increase in proliferation with Ki-67: there was 5% staining in the FAH compared with less than 1% staining of hepatocytes in the background liver Image 2D. The other FAH was CK7 with no increased proliferation. In the 4 control groups, no cases were seen of the second type of foci (with fatty change and smaller hepatocytes). A B C D Image 2 A, Glycogen-storing foci of altered hepatocytes (FAH) are demarcated sharply from the adjacent normal liver tissue (H&E, 40). B, A second type of FAH from a case of fibrolamellar carcinoma demonstrates smaller hepatocytes, an increased nuclear/cytoplasmic ratio, and fatty change (H&E, 100). C, Higher magnification (H&E, 200) of the FAH from B. D, Focal 2+ cytokeratin 7 staining in the FAH from B ( 200). See the text for an explanation of the scoring for staining. 516 Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99
6 Anatomic Pathology / ORIGINAL ARTICLE However, the FAH-GS were found in the background liver tissue samples in 1 (7%) of 15 cases of hepatoblastoma, 2 (8%) of 25 cases of adult HCC arising in the setting of cirrhosis, 5 (20%) of 25 cases of adult HCCs arising in livers with no significant fibrosis, and 5 (20%) of 25 livers resected for metastatic colon carcinoma. Discussion HCC is common in adults, with a worldwide incidence of 450,000 and approximately 10,000 cases diagnosed annually in the United States. The majority of adult cases are due to chronic liver injury from chronic viral hepatitis B or C or other chronic liver disease such as fatty liver disease. 11 In contrast, the risk factors for pediatric HCC are not well characterized. Despite the case reports of HCCs found in association with congenital and metabolic diseases, epidemiologic findings indicate that most individuals in the United States do not have a clinically recognized underlying liver disease. 1 Our findings strongly support these epidemiologic observations and show that most HCCs in children and young adults do not arise in the setting of histologically recognizable liver disease. In other nations, however, underlying liver disease is more commonly present. In a study from Poland, 15 (39%) of 39 children had cirrhosis, mostly from chronic HBV infection, 12 as did 68% of 55 children in a study from Taiwan. 13 At the histologic level, HCCs were more common than FLCs, and 1 intrahepatic cholangiocarcinoma was found. The HCCs generally were moderately differentiated with compact or trabecular growth patterns. CK7 was present in 7 (78%) of 9 HCCs. In this regard, HCCs in children and young adults are more similar to FLCs, which are also positive for CK7, compared with adult HCCs that have a lower frequency of CK7 positivity. Strong expression of CK7 has been reported in 2 cases of FLC. 14 The normal hepatocyte has a limited CK expression pattern, composed of CK8 and CK18. Biliary epithelium, in contrast, expresses CK7 and CK19 in addition to CK8 and CK However, CK7 also has been used in some studies as a marker of hepatic stem cells. 16 We do not have sufficient data in the present study to explore whether the CK7 expression is more reflective of biliary differentiation or indicative of stem cell features. Despite the presence of CK7 expression in most cases and focal areas of biliary-type morphologic features in some cases, the HCCs in the present study are distinct from those that we would classify as combined hepatocholangiocarcinomas: combined hepatocholangiocarcinomas lack the diffuse and strong HepPar positivity in the cholangiocarcinoma component, demonstrate areas of true gland formation, and also have dual positivity for CK7 and CK19 in the cholangiocarcinoma component. Several cases in the present study contained FAH in the background liver that were morphologically discrete from the adjacent hepatocytes. These FAH are similar to those described by others in diseased human livers 10,17 and animal models. 18,19 Our findings extend our understanding of these interesting foci by demonstrating their presence in the nonneoplastic and nondiseased livers of children and young adults in whom primary liver carcinoma developed. Although additional studies are needed, the findings from animal and human studies suggest that these foci are a logical place to search for precursor lesions to HCC. Because FAH-GS were found in the background liver samples of all control groups, including the partial hepatectomy specimens resected for metastatic colon carcinoma, these FAH might be less likely to represent direct precursor lesions than the FAH characterized by fatty changes and smaller hepatocytes. These latter FAH have similar morphologic features to some of the HCCs, and 1 of 2 also demonstrated CK7 and a slightly higher proliferative rate. Nevertheless, FAH-GS might still have a role because others have shown that the size and frequency of FAH-GS correlate with neoplasia in the liver. 20 We suspect more cases in the present study also might have demonstrated FAH if the background livers had been sampled more extensively. However, the specimens all were processed in a routine manner for diagnostic purposes and typically had only 1 or 2 sections of nonneoplastic liver. One potential explanation for the development of HCC in young people when no underlying liver disease is identifiable would be the presence of germline mutations in 1 copy of a tumor suppressor gene, as described in a child with adenomatous polyposis. 21 Although no recognizable inherited disease syndromes were evident in the cases described herein, these atypical foci might have added significance as a potential source for identifying early genetic changes in HCC, including tumor suppressor genes. HCCs in children and young adults typically were moderately differentiated and demonstrated compact or trabecular growth patterns. They frequently showed CK7 positivity, and FLCs were uniformly CK7+. In addition, FAH can be identified in the nondiseased background liver samples in some cases and might represent precursor lesions. From the Departments of 1 Pathology, 2 Surgery, and 3 Pediatrics, the Johns Hopkins University School of Medicine, Baltimore, MD. Address reprint requests to Dr Torbenson: the Johns Hopkins University School of Medicine, Room B314, 1503 E Jefferson, Baltimore, MD References 1. Darbari A, Sabin KM, Shapiro CN, et al. Epidemiology of primary hepatic malignancies in U.S. children. Hepatology. 2003;38: Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99 517
7 Klein et al / PRIMARY LIVER CARCINOMA 2. Van Eyken P, Sciot R, Paterson A, et al. Cytokeratin expression in hepatocellular carcinoma: an immunohistochemical study. Hum Pathol. 1988;19: Chu P, Wu E, Weiss LM. Cytokeratin 7 and cytokeratin 20 expression in epithelial neoplasms: a survey of 435 cases. Mod Pathol. 2000;13: Xiao SY, Wang HL, Hart J, et al. cdna arrays and immunohistochemistry identification of CD10/CALLA expression in hepatocellular carcinoma. Am J Pathol. 2001;159: Lau SK, Prakash S, Geller SA, et al. Comparative immunohistochemical profile of hepatocellular carcinoma, cholangiocarcinoma, and metastatic adenocarcinoma. Hum Pathol. 2002;33: Torbenson M, Wang J, Abraham S, et al. Bile ducts and ductules are positive for CD56 (N-CAM) in most cases of extrahepatic biliary atresia. Am J Surg Pathol. 2003;27: Chu PG, Arber DA, Weiss LM. Expression of T/NK-cell and plasma cell antigens in nonhematopoietic epithelioid neoplasms: an immunohistochemical study of 447 cases. Am J Clin Pathol. 2003;120: El-Serag HB, Davila JA, Petersen NJ, et al. The continuing increase in the incidence of hepatocellular carcinoma in the United States: an update. Ann Intern Med. 2003;139: Nzeako UC, Goodman ZD, Ishak KG. Hepatocellular carcinoma in cirrhotic and noncirrhotic livers: a clinicohistopathologic study of 804 North American patients. Am J Clin Pathol. 1996;105: Su Q, Benner A, Hofmann WJ, et al. Human hepatic preneoplasia: phenotypes and proliferation kinetics of foci and nodules of altered hepatocytes and their relationship to liver cell dysplasia. Virchows Arch. 1997;431: Montalto G, Cervello M, Giannitrapani L, et al. Epidemiology, risk factors, and natural history of hepatocellular carcinoma. Ann N Y Acad Sci. 2002;963: Czauderna P. Adult type vs childhood hepatocellular carcinoma: are they the same or different lesions? biology, natural history, prognosis, and treatment. Med Pediatr Oncol. 2002;39: Chen JC, Chen CC, Chen WJ, et al. Hepatocellular carcinoma in children: clinical review and comparison with adult cases. J Pediatr Surg. 1998;33: Van Eyken P, Sciot R, Brock P, et al. Abundant expression of cytokeratin 7 in fibrolamellar carcinoma of the liver. Histopathology. 1990;17: Van Eyken P, Sciot R, Desmet VJ. Immunocytochemistry of cytokeratins in primary human liver tumors. APMIS Suppl. 1991;23: Roskams T, De Vos R, Van Eyken P, et al. Hepatic OV-6 expression in human liver disease and rat experiments: evidence for hepatic progenitor cells in man. J Hepatol. 1998;29: Seki S, Sakaguchi H, Kawakita N, et al. Detection of the preneoplastic lesions of small hepatocellular carcinoma in cirrhotic livers. J Gastroenterol Hepatol. 1993;8: Koen H, Pugh TD, Goldfarb S. Hepatocarcinogenesis in the mouse; combined morphologic-stereologic studies. Am J Pathol. 1983;112: Stout DL, Becker FF. Occurrence of progressive DNA damage coincident with the appearance of foci of altered hepatocytes. Carcinogenesis. 1982;3: Su Q, Bannasch P. Relevance of hepatic preneoplasia for human hepatocarcinogenesis. Toxicol Pathol. 2003;31: Gruner BA, DeNapoli TS, Andrews W, et al. Hepatocellular carcinoma in children associated with Gardner syndrome or familial adenomatous polyposis. J Pediatr Hematol Oncol. 1998;20: Am J Clin Pathol 2005;124: DOI: /TT0R7KAL32228E99
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