Journal of Hepatology
Volume 46, Issue 3 , Pages 521-527 , March 2007

Pathological diagnosis of liver cell adenoma and focal nodular hyperplasia: Bordeaux update

References 

  1. International Working Party. Terminology of nodular hepatocellular lesions. Hepatology 1995;22:983–93.
  2. Anthony PP. Tumors and tumor-like lesions of the liver and biliary tract: aetiology epidemiology and pathology. In:  MacSween RNM,  Burt AD,  Portmann BC,  Ishak KG,  Scheuer PJ,  Anthony PP editor. Pathology of the liver. 4th ed.. Toronto: Churchill Livingstone; 2002;p. 711–775
  3. Wanless IR. Vascular disorders. In:  MacSween RNM,  Burt AD,  Portmann BC,  Ishak KG,  Scheuer PJ,  Anthony PP editor. Pathology of the liver. 4th ed.. Toronto: Churchill Livingstone; 2002;p. 539–573
  4. Nguyen BN, Flejou JF, Terris B, Belghiti J, Degott C. Focal nodular hyperplasia of the liver: a comprehensive pathologic study of 305 lesions and recognition of new histologic forms. Am J Surg Pathol. 1999;1441–1454
  5. Wanless IR, Mawdsley C, Adams R. On the pathogenesis of focal nodular hyperplasia of the liver. Hepatology. 1985;5:1194–1200
  6. Bioulac-Sage P, Balabaud C, Wanless IR. Diagnosis of focal nodular hyperplasia: not so easy. Am J Surg Pathol. 2001;25:1322–1325
  7. Marini P, Vilgrain V, Belghiti J. Management of spontaneous rupture of liver tumours. Dig Surg. 2002;19:109–113
  8. Ferrell LD. Hepatocellular carcinoma arising in a focus of multilobular adenoma. A case report. Am J Surg Pathol. 1993;17:525–529
  9. Flejou JF, Barge J, Menu Y, Degott C, Bismuth H, Potet F, et al. Liver adenomatosis. An entity distinct from liver adenoma?. Gastroenterology. 1985;89:1132–1138
  10. Chiche L, Dao T, Salame E, Galais MP, Bouvard N, Schmutz G, et al. Liver adenomatosis: reappraisal, diagnosis, and surgical management: eight new cases and review of the literature. Ann Surg. 2000;231:74–81
  11. Vilgrain V, Uzan F, Brancatelli G, Federle MP, Zappa M, Menu Y. Prevalence of hepatic hemangioma in patients with focal nodular hyperplasia: MR imaging analysis. Radiology. 2003;229:75–79
  12. Cherqui D, Mathieu D, Zafrani ES, Dhumeaux D. Hyperplasie nodulaire focale et adénome hépatocellulaire chez la femme. Données actuelles Gastroenterol Clin Biol. 1997;21:929–935
  13. Makhlouf HR, Abdul-Al HM, Goodman ZD. Diagnosis of focal nodular hyperplasia of the liver by needle biopsy. Hum Pathol. 2005;36:1210–1216
  14. Fabre A, Audet P, Vilgrain V, Nguyen BN, Valla D, Belghiti J, et al. Histologic scoring of liver biopsy in focal nodular hyperplasia with atypical presentation. Hepatology. 2002;35:414–420
  15. Lepreux S, Laurent C, Balabaud C, Bioulac-Sage P. FNH-like nodules: possible precursor lesions in patients with focal nodular hyperplasia (FNH). Comp Hepatol. 2003;26:2–7
  16. Wanless IR. Epithelioid hemangioendothelioma, multiple focal nodular hyperplasias, and cavernous hemangiomas of the liver [letter]. Arch Pathol Lab Med. 2000;124:1105–1107
  17. Takayama A, Wanless IR. Three-dimensional angioarchitecture of focal nodular hyperplasia and hypothesis on the pathogenesis. Mod Pathol. 2004;17(suppl):313A
  18. Wanless IR, Albrecht S, Bilbao J, Frei JV, Heathcote EJ, Roberts EA, et al. Multiple focal nodular hyperplasia of the liver associated with vascular malformations of various organs and neoplasia of the brain: a new syndrome. Mod Pathol. 1989;2:456–462
  19. Paradis V, Laurent A, Flejou JF, Vidaud M, Bedossa P. Evidence for the polyclonal nature of focal nodular hyperplasia of the liver by the study of X-chromosome inactivation. Hepatology. 1997;26:891–895
  20. Paradis V, Bieche I, Dargere D, Laurendeau I, Nectoux J, Degott C, et al. A quantitative gene expression study suggests a role for angiopoietins in focal nodular hyperplasia. Gastroenterology. 2003;124:651–659
  21. Bioulac-Sage P, Rebouissou S, Sa Cunha A, Jeannot E, Lepreux S, Blanc JF, et al. Clinical, morphological and molecular features defining so called telangiectatic focal nodular hyperplasias of the liver. Gastroenterology. 2005;128:1211–1218
  22. Zucman-Rossi J, Jeannot E, Tran Van Nhieu J, Scoazec JY, Guettier C, Rebouissou S, et al. Genotype–phenotype correlation in hepatocellular adenoma: new classification and relationship with HCC. Hepatology. 2006;43:515–524
  23. Paradis V, Benzekri A, Dargere D, Bieche I, Laurendeau I, Vilgrain V, et al. Telangiectatic focal nodular hyperplasia: a variant of hepatocellular adenoma. Gastroenterology. 2004;126:1323–1329
  24. Bluteau O, Jeannot E, Bioulac-Sage P, Marques JM, Blanc JF, Bui H, et al. Bi-allelic inactivation of TCF1 in hepatic adenomas. Nat Genet. 2002;32:312–315
  25. Bioulac-Sage P, Rebouissou S, SaCunha A, Jeannot E, Rullier A, le Bail B, et al. So-called telangiectatic focal nodular hyperplasia (TFNH): a subgroup of inflammatory and/or telangiectatic adenoma – experience of a single french center. Hepatology. 2005;42(Suppl.):300A
  26. Libbrecht L, De Vos R, Cassiman D, Desmet V, Aerts R, Roskams T. Hepatic progenitor cells in hepatocellular adenomas. Am J Surg Pathol. 2001;25:1388–1396
  27. Roskams T, De Vos R, Desmet V. ’Undifferentiated progenitor cells’ in focal nodular hyperplasia of the liver. Histopathology. 1996;28:291–299
  28. Lepreux S, Laurent C, Le Bail B, Saric J, Balabaud C, Bioulac-Sage P. Multiple telangiectatic focal nodular hyperplasia: vascular abnormalities. Virchows Arch. 2003;442:226–230
  29. Sadowski DC, Lee SS, Wanless IR, Kelly JK, Heathcote EJ. Progressive type of focal nodular hyperplasia characterized by multiple tumors and recurrence. Hepatology. 1995;21:970–975
  30. Laurent C, Trillaud H, Lepreux S, Balabaud C, Bioulac-Sage P. Association of adenoma and focal nodular hyperplasia: experience of a single French academic center. Comp Hepatol. 2003;2:6
  31. Socas L, Zumbado M, Perez-Luzardo O, Ramos A, Perez C, Hernandez JR, et al. Hepatocellular adenomas associated with anabolic androgenic steroid abuse in bodybuilders: a report of two cases and a review of the literature. Br J Sports Med. 2005;39:e27
  32. Kawakatsu M, Vilgrain V, Erlinger S, Nahum H. Disappearance of liver cell adenoma: CT and MR imaging. Abdom Imaging. 1997;22:274–276
  33. Aseni P, Sansalone CV, Sammartino C, Benedetto FD, Carrafiello G, Giacomoni A, et al. Rapid disappearance of hepatic adenoma after contraceptive withdrawal. J Clin Gastroenterol. 2001;33:234–236
  34. Ohmoto K, Honda T, Hirokawa M, Mitsui Y, Iguchi Y, Kuboki M, et al. Spontaneous regression of focal nodular hyperplasia of the liver. J Gastroenterol. 2002;37:849–853
  35. Leconte I, Van Beers BE, Lacrosse M, Sempoux C, Jamart J, Materne R, et al. Focal nodular hyperplasia: natural course observed with CT and MRI. J Comput Assist Tomogr. 2000;24:61–66
  36. Lepreux S, Laurent C, Blanc JF, Trillaud H, Le Bail B, Trouette H, et al. The identification of small nodules in liver adenomatosis. J Hepatol. 2003;39:77–85
  37. Belghiti J, Dokmak S, Paradis V, Vilgrain V, Durand F, Valla D. Specific management for multiple liver cell adenoma: is it justified?. Hepatology. 2005;42(Suppl.):297A
  38. Vilgrain V. Focal nodular hyperplasia. Eur J Radiol. 2006;58:236–245
  39. Mortele KJ, Ros PR. Benign liver neoplasms. Clin Liver Dis. 2002;6:119–145
  40. Gouysse G, Frachon S, Hervieu V, Fiorentino M, d’Errico A, Dumortier J, et al. Endothelial cell differentiation in hepatocellular adenomas: implications for histopathological diagnosis. J Hepatol. 2004;41:259–266
  41. Vander Borght S, Libbrecht L, Blokzijl H, Faber KN, Moshage H, Aerts R, et al. Diagnostic and pathogenetic implications of the expression of hepatic transporters in focal lesions occurring in normal liver. J Pathol. 2005;207:471–482
  42. Chen YW, Jeng YM, Yeh SH, Chen PJ. P53 gene and Wnt signaling in benign neoplasms: beta-catenin mutations in hepatic adenoma but not in focal nodular hyperplasia. Hepatology. 2002;36:927–935
  43. Takayasu H, Motoi T, Kanamori Y, Kitano Y, Nakanishi H, Tange T, et al. Two case reports of childhood liver cell adenomas harboring beta-catenin abnormalities. Hum Pathol. 2002;33:852–855
  44. Torbenson M, Lee JH, Choti M, Gage W, Abraham SC, Montgomery E, et al. Hepatic adenomas: analysis of sex steroid receptor status and the Wnt signaling pathway. Mod Pathol. 2002;15:189–196
  45. Cadoret A, Ovejero C, Terris B, Souil E, Levy L, Lamers WH, et al. New targets of beta-catenin signaling in the liver are involved in the glutamine metabolism. Oncogene. 2002;21:8293–8301
  46. Wilkens L, Bredt M, Flemming P, Schwarze Y, Becker T, Mengel M, et al. Diagnostic impact of fluorescence in situ hybridization in the differentiation of hepatocellular adenoma and well-differentiated hepatocellular carcinoma. J Mol Diagn. 2001;3:68–73
  47. Herman P, Pugliese V, Machado MA, Montagnini AL, Salem MZ, Bacchella T, et al. Hepatic adenoma and focal nodular hyperplasia: differential diagnosis and treatment. World J Surg. 2000;24:372–376
  48. Bacq Y, Jacquemin E, Balabaud C, Jeannot E, Scotto B, Branchereau S, et al. Familial liver adenomatosis associated with hepatocyte nuclear factor 1alpha inactivation. Gastroenterology. 2003;125:1470–1475
  49. Reznik Y, Dao T, Coutant R, Chiche L, Jeannot E, Clauin S, et al. Hepatocyte nuclear factor-1 alpha gene inactivation: cosegregation between liver adenomatosis and diabetes phenotypes in two maturity-onset diabetes of the young (MODY)3 families. J Clin Endocrinol Metab. 2004;89:1476–1480
  50. Yamagata K, Oda N, Kaisaki PJ, Menzel S, Furuta H, Vaxillaire M, et al. Mutations in the hepatocyte nuclear factor-1alpha gene in maturity-onset diabetes of the young (MODY3). Nature. 1996;384:455–458
  51. llard S. Hepatocyte nuclear factor 1 alpha (HNF-1 alpha) mutations in maturity-onset diabetes of the young. Hum Mutat. 2000;16:377–385
  52. Foster JH, Donohue TA, Berman MM. Familial liver-cell adenomas and diabetes mellitus. N Engl J Med. 1978;299:239–241

PII: S0168-8278(06)00678-7

doi: 10.1016/j.jhep.2006.12.007

Journal of Hepatology
Volume 46, Issue 3 , Pages 521-527 , March 2007

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