Steatotic hepatocellular carcinoma: a variant associated with metabolic factors and late tumour relapse

Histopathology

Volumn 69, Issue 6, 2016, Pages 971-984

  Chan, Anthony W H ^a   Yu, Shuangni ^b   Yu, Yau Hei ^a   Tong, Joanna H M ^a,c   Wang, Lei ^d,e   Tin, Edith K Y ^a   Chong, Charing C N ^c   Chan, Stephen L ^a,c   Wong, Grace L H ^c   Wong, Vincent W S ^c   Chan, Henry L Y ^c   Lai, Paul B S ^c   To, Ka Fai ^a,c  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

fatty liver; hepatocellular carcinoma; relapse; steatohepatitis; steatosis

Indexed keywords

FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 1; PATATIN LIKE PHOSPHOLIPASE 3; PHOSPHOLIPASE; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; ADIPONUTRIN, HUMAN; MEMBRANE PROTEIN; TRIACYLGLYCEROL LIPASE; TUMOR MARKER;

ADULT; ARTICLE; CANCER RECURRENCE; CLINICAL FEATURE; COHORT ANALYSIS; DIABETES MELLITUS; DIABETIC PATIENT; DISEASE FREE SURVIVAL; DNA POLYMORPHISM; FATTY LIVER; FEMALE; FOLLOW UP; GENOTYPE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MULTIPLE CANCER; NON INSULIN DEPENDENT DIABETES MELLITUS; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SINGLE NUCLEOTIDE POLYMORPHISM; STEATOSIS; TUMOR CELL; TUMOR RECURRENCE; TUMOR VOLUME; AGED; COMPLICATION; GENETICS; HYPERLIPIDEMIAS; KAPLAN MEIER METHOD; LIVER TUMOR; MORTALITY; PATHOLOGY; POLYMERASE CHAIN REACTION; PROPORTIONAL HAZARDS MODEL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RISK FACTOR; TISSUE MICROARRAY;

ADULT; AGED; BIOMARKERS, TUMOR; CARCINOMA, HEPATOCELLULAR; DIABETES MELLITUS; FATTY LIVER; FEMALE; HUMANS; HYPERLIPIDEMIAS; HYPERTENSION; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LIPASE; LIVER NEOPLASMS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PROPORTIONAL HAZARDS MODELS; RETROSPECTIVE STUDIES; RISK FACTORS; TISSUE ARRAY ANALYSIS;

EID: 84987786110     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/his.13029     Document Type: Article

References (40)

1. Ferlay J, Soerjomataram I, Ervik M et al. GLOBOCAN 2012 v1.0, Cancer incidence and mortality worldwide: IARC CancerBase no. 11 [internet]. Lyon: International Agency for Research on Cancer, 2013.
2. Roayaie S, Blume IN, Thung SN et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology 2009; 137; 850–855.
3. European Association for the Study of the Liver, European Organisation For Research and Treatment of Cancer. EASL–EORTC clinical practice guidelines: management of hepatocellular carcinoma. J. Hepatol. 2012; 56; 908–943.
4. Chan AW, Chan SL, Wong GL et al. Prognostic Nutritional Index (PNI) predicts tumor recurrence of very early/early stage hepatocellular carcinoma after surgical resection. Ann. Surg. Oncol. 2015; 22; 4138–4148.
5. Theise ND, Curado MP, Franceshi S et al. Hepatocellular carcinoma. In Bosman FT, Carneiro F, Hruban RH, Theise ND eds. WHO classification of tumours of the digestive system. Lyon: International Agency for Research on Cancer, 2010; 205–216.
6. Honeyman JN, Simon EP, Robine N et al. Detection of a recurrent DNAJB1–PRKACA chimeric transcript in fibrolamellar hepatocellular carcinoma. Science 2014; 343; 1010–1014.
7. Mayo SC, Mavros MN, Nathan H et al. Treatment and prognosis of patients with fibrolamellar hepatocellular carcinoma: a national perspective. J. Am. Coll. Surg. 2014; 218; 196–205.
8. Chan AW, Tong JH, Pan Y et al. Lymphoepithelioma-like hepatocellular carcinoma: an uncommon variant of hepatocellular carcinoma with favorable outcome. Am. J. Surg. Pathol. 2015; 39; 304–312.
9. Chan AW, Tong JH, Chan SL, Lai PB, To KF. Expression of stemness markers (CD133 and EpCAM) in prognostication of hepatocellular carcinoma. Histopathology 2014; 64; 935–950.
10. Salomao M, Yu WM, Brown RS Jr, Emond JC, Lefkowitch JH. Steatohepatitic hepatocellular carcinoma (SH-HCC): a distinctive histological variant of HCC in hepatitis C virus-related cirrhosis with associated NAFLD/NASH. Am. J. Surg. Pathol. 2010; 34; 1630–1636.
11. Salomao M, Remotti H, Vaughan R, Siegel AB, Lefkowitch JH, Moreira RK. The steatohepatitic variant of hepatocellular carcinoma and its association with underlying steatohepatitis. Hum. Pathol. 2012; 43; 737–746.
12. Jain D, Nayak NC, Kumaran V, Saigal S. Steatohepatitic hepatocellular carcinoma, a morphologic indicator of associated metabolic risk factors: a study from India. Arch. Pathol. Lab. Med. 2013; 137; 961–966.
13. Shibahara J, Ando S, Sakamoto Y, Kokudo N, Fukayama M. Hepatocellular carcinoma with steatohepatitic features: a clinicopathological study of Japanese patients. Histopathology 2014; 64; 951–962.
14. Kutami R, Nakashima Y, Nakashima O, Shiota K, Kojiro M. Pathomorphologic study on the mechanism of fatty change in small hepatocellular carcinoma of humans. J. Hepatol. 2000; 33; 282–289.
15. Wang G, Bonkovsky HL, de Lemos A, Burczynski FJ. Recent insights into the biological functions of liver fatty acid binding protein 1. J. Lipid Res. 2015; 56; 2238–2247.
16. Charlton M, Viker K, Krishnan A et al. Differential expression of lumican and fatty acid binding protein-1: new insights into the histologic spectrum of nonalcoholic fatty liver disease. Hepatology 2009; 49; 1375–1384.
17. Bioulac-Sage P, Rebouissou S, Thomas C et al. Hepatocellular adenoma subtype classification using molecular markers and immunohistochemistry. Hepatology 2007; 46; 740–748.
18. Inoue M, Takahashi Y, Fujii T, Kitagawa M, Fukusato T. Significance of downregulation of liver fatty acid-binding protein in hepatocellular carcinoma. World J. Gastroenterol. 2014; 20; 17541–17551.
19. Wang B, Tao X, Huang CZ, Liu JF, Ye YB, Huang AM. Decreased expression of liver-type fatty acid-binding protein is associated with poor prognosis in hepatocellular carcinoma. Hepatogastroenterology 2014; 61; 1321–1326.
20. Rangwala F, Guy CD, Lu J et al. Increased production of sonic hedgehog by ballooned hepatocytes. J. Pathol. 2011; 224; 401–410.
21. Lu JT, Zhao WD, He W, Wei W. Hedgehog signaling pathway mediates invasion and metastasis of hepatocellular carcinoma via ERK pathway. Acta Pharmacol. Sin. 2012; 33; 691–700.
22. Shen J, Wong GL, Chan HL et al. PNPLA3 gene polymorphism accounts for fatty liver in community subjects without metabolic syndrome. Aliment. Pharmacol. Ther. 2014; 39; 532–539.
23. Salameh H, Raff E, Erwin A et al. PNPLA3 Gene polymorphism is associated with predisposition to and severity of alcoholic liver disease. Am. J. Gastroenterol. 2015; 110; 846–856.
24. Singal AG, Manjunath H, Yopp AC et al. The effect of PNPLA3 on fibrosis progression and development of hepatocellular carcinoma: a meta-analysis. Am. J. Gastroenterol. 2014; 109; 325–334.
25. Johnson PJ, Berhane S, Kagebayashi C et al. Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J. Clin. Oncol. 2015; 33; 550–558.
26. Farrell GC, Chitturi S, Lau GK, Sollano JD; Asia-Pacific Working Party on NAFLD. Guidelines for the assessment and management of non-alcoholic fatty liver disease in the Asia-Pacific region: executive summary. J. Gastroenterol. Hepatol. 2007; 22; 775–777.
27. Chan AW, Chan SL, Mo FK et al. Albumin-to-alkaline phosphatase ratio: a novel prognostic index for hepatocellular carcinoma. Dis. Markers 2015; 2015; 564057.
28. Chan AW, Kumada T, Toyoda H et al. Integration of albumin–bilirubin (ALBI) score into Barcelona clinic liver cancer (BCLC) system for hepatocellular carcinoma. J. Gastroenterol. Hepatol. 2016; 31; 1300–1306.
29. Ishak K, Baptista A, Bianchi L et al. Histological grading and staging of chronic hepatitis. J. Hepatol. 1995; 22; 696–699.
30. Brunt EM, Kleiner DE, Wilson LA, Belt P, Neuschwander-Tetri BA, Network NCR. Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings. Hepatology 2011; 53; 810–820.
31. Lackner C, Gogg-Kamerer M, Zatloukal K, Stumptner C, Brunt EM, Denk H. Ballooned hepatocytes in steatohepatitis: the value of keratin immunohistochemistry for diagnosis. J. Hepatol. 2008; 48; 821–828.
32. McCarty KS Jr, Miller LS, Cox EB, Konrath J, McCarty KS Sr. Estrogen receptor analyses. Correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies. Arch. Pathol. Lab. Med. 1985; 109; 716–721.
33. Yuen MF, Hou JL, Chutaputti A; Asia Pacific Working Party on Prevention of Hepatocellular Carcinoma. Hepatocellular carcinoma in the Asia pacific region. J. Gastroenterol. Hepatol. 2009; 24; 346–353.
34. Cheng Z, Yang P, Qu S et al. Risk factors and management for early and late intrahepatic recurrence of solitary hepatocellular carcinoma after curative resection. HPB (Oxford) 2015; 17; 422–427.
35. Yeh MM, Liu Y, Torbenson M. Steatohepatitic variant of hepatocellular carcinoma in the absence of metabolic syndrome or background steatosis: a clinical, pathological, and genetic study. Hum. Pathol. 2015; 46; 1769–1775.
36. Yu J, Shen J, Sun TT, Zhang X, Wong N. Obesity, insulin resistance, NASH and hepatocellular carcinoma. Semin. Cancer Biol. 2013; 23; 483–491.
37. Tan PS, Nakagawa S, Goossens N et al. Clinicopathological indices to predict hepatocellular carcinoma molecular classification. Liver Int. 2016; 36; 108–118.
38. Hoshida Y, Nijman SM, Kobayashi M et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res. 2009; 69; 7385–7392.
39. Ando S, Shibahara J, Hayashi A, Fukayama M. Beta-catenin alteration is rare in hepatocellular carcinoma with steatohepatitic features: immunohistochemical and mutational study. Virchows Arch. 2015; 467; 535–542.
40. Grundy SM, Cleeman JI, Daniels SR et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005; 112; 2735–2752.