Pathology of the adrenal cortex: A reappraisal of the past 25 years focusing on adrenal cortical tumors

Endocrine Pathology

Volumn 25, Issue 1, 2014, Pages 35-48

  Papotti, Mauro ^a   Duregon, Eleonora ^a   Volante, Marco ^a   McNicol, Anne Marie ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Adenoma; Adrenal cortex; Carcinoma; Diagnostic criteria; Pathology; Update

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; DNA; INHIBIN A; KI 67 ANTIGEN; MELAN A; MICRORNA; PRIMARY PIGMENTED NODULAR ADRENOCORTICAL DISEASE; STEROIDOGENIC FACTOR 1; UNCLASSIFIED DRUG;

ADRENAL CORTEX CARCINOMA; ADRENAL CORTEX TUMOR; ARTICLE; BECKWITH WIEDEMANN SYNDROME; CANCER DIAGNOSIS; CARNEY COMPLEX; CHROMOSOME ABERRATION; DIAGNOSTIC PROCEDURE; DNA METHYLATION; FAMILIAL CANCER; FAMILIAL CANCER SUSCEPTIBILITY SYNDROME; GARDNER SYNDROME; GENE MUTATION; HUMAN; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; MIXED CORTICO MEDULLARY ADRENAL TUMOR; MULTIPLE ENDOCRINE NEOPLASIA; MYXOID ADRENAL CORTICAL TUMOR; NEUROFIBROMATOSIS; ONCOCYTIC ADRENAL CORTICAL TUMOR; PEDIATRIC ADRENAL CORTICAL TUMOR; PRIORITY JOURNAL; PROGNOSIS; SCORING SYSTEM; TRANSCRIPTOMICS; ADRENAL CORTEX; ADRENAL CORTEX ADENOMA; HISTORY; PATHOLOGY;

ADRENAL CORTEX; ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL ADENOMA; ADRENOCORTICAL CARCINOMA; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS;

EID: 84900315939     PISSN: 10463976     EISSN: 15590097     Source Type: Journal    
DOI: 10.1007/s12022-013-9291-6     Document Type: Article

References (117)

1. Weiss LM (1984) Comparative histologic study of 43 metastasizing and nonmetastasizing adrenocortical tumors. Am J Surg Pathol 8 (3):163-169
2. Weiss LM, Medeiros LJ, Vickery AL, Jr. (1989) Pathologic features of prognostic significance in adrenocortical carcinoma. Am J Surg Pathol 13 (3):202-206
3. Aubert S, Wacrenier A, Leroy X, Devos P, Carnaille B, Proye C, Wemeau JL, Lecomte-Houcke M, Leteurtre E (2002) Weiss system revisited: a clinicopathologic and immunohistochemical study of 49 adrenocortical tumors. Am J Surg Pathol 26 (12):1612-1619
4. Lau SK, Weiss LM (2009) The Weiss system for evaluating adrenocortical neoplasms: 25 years later. Hum Pathol 40 (6):757-768. doi: 10.1016/j.humpath. 2009.03.010
5. Blanes A, Diaz-Cano SJ (2007) Histologic criteria for adrenocortical proliferative lesions: value of mitotic figure variability. Am J Clin Pathol 127 (3):398-408. doi: 10.1309/MCGUQ3R4A4WWN3LB
6. Volante M, Bollito E, Sperone P, Tavaglione V, Daffara F, Porpiglia F, Terzolo M, Berruti A, Papotti M (2009) Clinicopathological study of a series of 92 adrenocortical carcinomas: from a proposal of simplified diagnostic algorithm to prognostic stratification. Histopathology 55 (5):535-543. doi: 10.1111/j.1365-2559.2009.03423.x
7. Papotti M, Volante M, Duregon E, Delsedime L, Terzolo M, Berruti A, Rosai J (2010) Adrenocortical tumors with myxoid features: a distinct morphologic and phenotypical variant exhibiting malignant behavior. Am J Surg Pathol 34 (7):973-983. doi:10.1097/PAS.0b013e3181e2b726
8. Duregon E, Volante M, Cappia S, Cuccurullo A, Bisceglia M, Wong DD, Spagnolo DV, Szpak-Ulczok S, Bollito E, Daffara F, Berruti A, Terzolo M, Papotti M (2011) Oncocytic adrenocortical tumors: diagnostic algorithm and mitochondrial DNA profile in 27 cases. Am J Surg Pathol 35 (12):1882-1893. doi:10.1097/PAS.0b013e31822da401
9. Tissier F, Aubert S, Leteurtre E, Al Ghuzlan A, Patey M, Decaussin M, Doucet L, Gobet F, Hoang C, Mazerolles C, Monges G, Renaudin K, Sturm N, Trouette H, Vacher-Lavenu MC, Viallon V, Baudin E, Bertagna X, Coste J, Libe R (2012) Adrenocortical tumors: improving the practice of the Weiss system through virtual microscopy: a National Program of the French Network INCa-COMETE. Am J Surg Pathol 36 (8):1194-1201. doi:10.1097/PAS.0b013e31825a6308
10. Duregon E, Fassina A, Volante M, Nesi G, Santi R, Gatti G, Cappellesso R, Dalino Ciaramella P, Ventura L, Gambacorta M, Dei Tos AP, Loli P, Mannelli M, Mantero F, Berruti A, Terzolo M, Papotti M (2013) The Reticulin Algorithm for Adrenocortical Tumor Diagnosis: A Multicentric Validation Study on 245 Unpublished Cases. Am J Surg Pathol. doi:10.1097/PAS.0b013e31828d387b
11. Kakimoto S, Yushita Y, Sanefuji T, Kondo A, Fujishima N, Kishikawa M, Matsumoto K (1986) Non-hormonal adrenocortical adenoma with oncocytoma-like appearances. Hinyokika Kiyo 32 (5):757-763
12. Bisceglia M, Ludovico O, Di Mattia A, Ben-Dor D, Sandbank J, Pasquinelli G, Lau SK, Weiss LM (2004) Adrenocortical oncocytic tumors: report of 10 cases and review of the literature. Int J Surg Pathol 12 (3):231-243
13. Wong DD, Spagnolo DV, Bisceglia M, Havlat M, McCallum D, Platten MA (2011) Oncocytic adrenocortical neoplasms - a clinicopathologic study of 13 new cases emphasizing the importance of their recognition. Hum Pathol. doi: 10.1016/j.humpath.2010.08.010
14. Lewis PD, Baxter P, Paul Griffiths A, Parry JM, Skibinski DO (2000) Detection of damage to the mitochondrial genome in the oncocytic cells of Warthin's tumour. J Pathol 191 (3):274-281. doi:10.1002/1096-9896(2000)9999: 9999〈::AID-PATH634〉3.0.CO;2-U
15. Lewis PD, Fradley SR, Griffiths AP, Baxter PW, Parry JM (2002) Mitochondrial DNA mutations in the parotid gland of cigarette smokers and non-smokers. Mutat Res 518 (1):47-54.
16. Tang CK, Harriman BB, Toker C (1979) Myxoid adrenal cortical carcinoma: a light and electron microscopic study. Arch Pathol Lab Med 103 (12):635-638
17. Weissferdt A, Phan A, Suster S, Moran CA (2013) Myxoid adrenocortical carcinoma: a clinicopathologic and immunohistochemical study of 7 cases, including 1 case with lipomatous metaplasia. Am J Clin Pathol 139 (6):780-786. doi :10.1309/AJCPCDZLC13RSXRZ
18. Okazumi S, Asano T, Ryu M, Nagashima T, Odaka M, Isono K, Nishizawa T (1987) [Surgical resection of adrenal carcinoma extending into the vena cava, right atrium and ventricle: case report and review of the literature]. Nippon Geka Gakkai Zasshi 88 (2):231-238
19. Collina G, Maldarizzi F, Betts CM, Eusebi V (1989) Primary sarcomatoid carcinoma of the adrenal gland. First case report. Virchows Arch A Pathol Anat Histopathol 415 (2):161-167
20. Lee MS, Park IA, Chi JG, Ham EK, Lee KC, Lee CW (1997) Adrenal carcinosarcoma - a case report. J Korean Med Sci 12 (4): 374-377
21. Sturm N, Moulai N, Laverriere MH, Chabre O, Descotes JL, Brambilla E (2008) Primary adrenocortical sarcomatoid carcinoma: case report and review of literature. Virchows Arch 452 (2):215-219. doi:10.1007/s00428-007-0536-y
22. Coli A, Di Giorgio A, Castri F, Destito C, Marin AW, Bigotti G (2010) Sarcomatoid carcinoma of the adrenal gland: A case report and review of literature. Pathol Res Pract 206 (1):59-65. doi: 10.1016/j.prp.2009.02.012
23. Barksdale SK, Marincola FM, Jaffe G (1993) Carcinosarcoma of the adrenal cortex presenting with mineralocorticoid excess. Am J Surg Pathol 17 (9):941-945
24. Bertolini F, Rossi G, Fiocchi F, Giacometti M, Fontana A, Gibertini MC, Roncucci L, Luppi G, Torricelli P, Rossi A, Conte PF (2011) Primary adrenal gland carcinosarcoma associated with metastatic rectal cancer: a hitherto unreported collision tumor. Tumori 97 (5): 27e-30e. doi:10.1700/989.10734
25. Decorato JW, Gruber H, Petti M, Levowitz BS (1990) Adrenal carcinosarcoma. J Surg Oncol 45 (2):134-136
26. Fischler DF, Nunez C, Levin HS, McMahon JT, Sheeler LR, Adelstein DJ (1992) Adrenal carcinosarcoma presenting in a woman with clinical signs of virilization. A case report with immunohistochemical and ultrastructural findings. Am J Surg Pathol 16 (6):626-631
27. Sasaki K, Desimone M, Rao HR, Huang GJ, Seethala RR (2010) Adrenocortical carcinosarcoma: a case report and review of the literature. Diagn Pathol 5:51. doi: 10.1186/1746-1596-5-51
28. Thway K, Olmos D, Shah C, Flora R, Shipley J, Fisher C (2012) Oncocytic adrenal cortical carcinosarcoma with pleomorphic rhabdomyosarcomatous metastases. Am J Surg Pathol 36 (3):470-477. doi:10.1097/PAS.0b013e31824517d9
29. Wieneke JA, Thompson LD, Heffess CS (2003) Adrenal cortical neoplasms in the pediatric population: a clinicopathologic and immunophenotypic analysis of 83 patients. Am J Surg Pathol 27 (7):867-881
30. Magro G, Esposito G, Cecchetto G, Dall'Igna P, Marcato R, Gambini C, Boldrini R, Collini P, D'Onofrio V, Salfi N, d'Amore E, Ferrari A, Bisogno G, Alaggio R (2012) Pediatric adrenocortical tumors: morphological diagnostic criteria and immunohistochemical expression of matrix metalloproteinase type 2 and human leucocyte-associated antigen (HLA) class II antigens. Results from the Italian Pediatric Rare Tumor (TREP) Study project. Hum Pathol 43 (1):31-39. doi:10.1016/j.humpath.2011.04.016
31. Turk AT, Asad H, Trapasso J, Perilli G, LiVolsi VA (2012) Mixed corticomedullary carcinoma of the adrenal gland: a case report. Endocr Pract 18 (3):e37-42. doi:10.4158/EP11222.CR
32. Lam KY, Lo CY (2002) Metastatic tumours of the adrenal glands: a 30-year experience in a teaching hospital. Clin Endocrinol (Oxf) 56 (1):95-101.
33. Gaffey MJ, Traweek ST, Mills SE, Travis WD, Lack EE, Medeiros LJ, Weiss LM (1992) Cytokeratin expression in adrenocortical neoplasia: an immunohistochemical and biochemical study with implications for the differential diagnosis of adrenocortical, hepatocellular, and renal cell carcinoma. Hum Pathol 23 (2):144-153
34. Jorda M, De MB, Nadji M (2002) Calretinin and inhibin are useful in separating adrenocortical neoplasms from pheochromocytomas. Appl Immunohistochem Mol Morphol 10 (1):67-70
35. Browning L, Bailey D, Parker A (2008) D2-40 is a sensitive and specific marker in differentiating primary adrenal cortical tumours from both metastatic clear cell renal cell carcinoma and phaeochromocytoma. J Clin Pathol 61 (3):293-296. doi: 10.1136/jcp.2007.049544
36. Schroder S, Niendorf A, Achilles E, Dietel M, Padberg BC, Beisiegel U, Dralle H, Bressel M, Kloppel G (1990) Immunocytochemical differential diagnosis of adrenocortical neoplasms using the monoclonal antibody D11. Virchows Arch A Pathol Anat Histopathol 417 (2):89-96
37. Schroder S, Padberg BC, Achilles E, Holl K, Dralle H, Kloppel G (1992) Immunocytochemistry in adrenocortical tumours: a clinicomorphological study of 72 neoplasms. Virchows Arch A Pathol Anat Histopathol 420 (1):65-70
38. Tartour E, Caillou B, Tenenbaum F, Schroder S, Luciani S, Talbot M, Schlumberger M (1993) Immunohistochemical study of adrenocortical carcinoma. Predictive value of the D11 monoclonal antibody. Cancer 72 (11):3296-3303
39. Komminoth P, Roth J, Schroder S, Saremaslani P, Heitz PU (1995) Overlapping expression of immunohistochemical markers and synaptophysin mRNA in pheochromocytomas and adrenocortical carcinomas. Implications for the differential diagnosis of adrenal gland tumors. Lab Invest 72 (4):424-431
40. Busam KJ, Iversen K, Coplan KA, Old LJ, Stockert E, Chen YT, McGregor D, Jungbluth A (1998) Immunoreactivity for A103, an antibody to melan-A (Mart-1), in adrenocortical and other steroid tumors. Am J Surg Pathol 22 (1):57-63
41. Ghorab Z, Jorda M, Ganjei P, Nadji M (2003) Melan A (A103) is expressed in adrenocortical neoplasms but not in renal cell and hepatocellular carcinomas. Appl Immunohistochem Mol Morphol 11 (4):330-333
42. Arola J, Liu J, Heikkila P, Voutilainen R, Kahri A (1998) Expression of inhibin alpha in the human adrenal gland and adrenocortical tumors. Endocr Res 24 (3-4):865-867
43. McCluggage WG, Burton J, Maxwell P, Sloan JM (1998) Immunohistochemical staining of normal, hyperplastic, and neoplastic adrenal cortex with a monoclonal antibody against alpha inhibin. J Clin Pathol 51 (2):114-116
44. Munro LM, Kennedy A, McNicol AM (1999) The expression of inhibin/activin subunits in the human adrenal cortex and its tumours. J Endocrinol 161 (2):341-347.
45. Arola J, Liu J, Heikkila P, Ilvesmaki V, Salmenkivi K, Voutilainen R, Kahri AI (2000) Expression of inhibin alpha in adrenocortical tumours reflects the hormonal status of the neoplasm. J Endocrinol 165 (2):223-229.
46. Sasano H, Shizawa S, Suzuki T, Takayama K, Fukaya T, Morohashi K, Nagura H (1995) Transcription factor adrenal 4 binding protein as a marker of adrenocortical malignancy. Hum Pathol 26 (10): 1154-1156
47. Figueiredo BC, Cavalli LR, Pianovski MA, Lalli E, Sandrini R, Ribeiro RC, Zambetti G, DeLacerda L, Rodrigues GA, Haddad BR (2005) Amplification of the steroidogenic factor 1 gene in childhood adrenocortical tumors. J Clin Endocrinol Metab 90 (2):615-619. doi: 10.1210/jc.2004-0942
48. Pianovski MA, Cavalli LR, Figueiredo BC, Santos SC, Doghman M, Ribeiro RC, Oliveira AG, Michalkiewicz E, Rodrigues GA, Zambetti G, Haddad BR, Lalli E (2006) SF-1 overexpression in childhood adrenocortical tumours. Eur J Cancer 42 (8):1040-1043. doi: 10.1016/j.ejca.2006.01.022
49. Sbiera S, Schmull S, Assie G, Voelker HU, Kraus L, Beyer M, Ragazzon B, Beuschlein F, Willenberg HS, Hahner S, Saeger W, Bertherat J, Allolio B, Fassnacht M (2010) High diagnostic and prognostic value of steroidogenic factor-1 expression in adrenal tumors. J Clin Endocrinol Metab 95 (10):E161-171. doi: 10.1210/jc.2010-0653
50. Sangoi AR, Fujiwara M, West RB, Montgomery KD, Bonventre JV, Higgins JP, Rouse RV, Gokden N, McKenney JK (2011) Immunohistochemical distinction of primary adrenal cortical lesions from metastatic clear cell renal cell carcinoma: a study of 248 cases. Am J Surg Pathol 35 (5):678-686. doi:10.1097/PAS.0b013e3182152629
51. Duregon E, Volante M, Giorcelli J, Terzolo M, Lalli E, Papotti M (2013) Diagnostic and prognostic role of steroidogenic factor 1 in adrenocortical carcinoma: a validation study focusing on clinical and pathologic correlates. Hum Pathol 44 (5):822-828. doi:10.1016/j.humpath.2012.07.025
52. Weissferdt A, Phan A, Suster S, Moran CA (2013) Adrenocortical Carcinoma: A Comprehensive Immunohistochemical Study of 40 Cases. Appl Immunohistochem Mol Morphol. doi:10.1097/PAI.0b013e31828a96cf
53. McNicol AM, Struthers AL, Nolan CE, Hermans J, Haak HR (1997) Proliferation in Adrenocortical Tumors: Correlation with Clinical Outcome and p53 Status. Endocr Pathol 8 (1):29-36.
54. Iino K, Sasano H, Yabuki N, Oki Y, Kikuchi A, Yoshimi T, Nagura H (1997) DNA topoisomerase II alpha and Ki-67 in human adrenocortical neoplasms: a possible marker of differentiation between adenomas and carcinomas. Mod Pathol 10 (9): 901-907
55. Nakazumi H, Sasano H, Iino K, Ohashi Y, Orikasa S (1998) Expression of cell cycle inhibitor p27 and Ki-67 in human adrenocortical neoplasms. Mod Pathol 11 (12):1165-1170
56. Arola J, Salmenkivi K, Liu J, Kahri AI, Heikkila P (2000) p53 and Ki67 in adrenocortical tumors. Endocr Res 26 (4):861-865
57. Terzolo M, Boccuzzi A, Bovio S, Cappia S, De Giuli P, Ali A, Paccotti P, Porpiglia F, Fontana D, Angeli A (2001) Immunohistochemical assessment of Ki-67 in the differential diagnosis of adrenocortical tumors. Urology 57 (1):176-182.
58. Stojadinovic A, Brennan MF, Hoos A, Omeroglu A, Leung DH, Dudas ME, Nissan A, Cordon-Cardo C, Ghossein RA (2003) Adrenocortical adenoma and carcinoma: histopathological and molecular comparative analysis. Mod Pathol 16 (8):742-751. doi:10.1097/01.MP.0000081730.72305.81
59. Soon PS, Gill AJ, Benn DE, Clarkson A, Robinson BG, McDonald KL, Sidhu SB (2009) Microarray gene expression and immunohistochemistry analyses of adrenocortical tumors identify IGF2 and Ki-67 as useful in differentiating carcinomas from adenomas. Endocr Relat Cancer 16 (2):573-583. doi:10.1677/ERC-08-0237
60. Schmitt A, Saremaslani P, Schmid S, Rousson V, Montani M, Schmid DM, Heitz PU, Komminoth P, Perren A (2006) IGFII and MIB1 immunohistochemistry is helpful for the differentiation of benign from malignant adrenocortical tumours. Histopathology 49 (3):298-307. doi: 10.1111/j.1365-2559.2006.02505.x
61. Duregon E, Molinaro L, Volante M, Ventura L, Righi L, Bolla S, Terzolo M, Sapino A, Papotti M (2013) Comparative diagnostic and prognostic performances of morphological and phospho-histone H3-based mitotic count and Ki-67 proliferation index in adrenocortical carcinoma. Mod Pathol. (in press)
62. Libe R, Groussin L, Tissier F, Elie C, Rene-Corail F, Fratticci A, Jullian E, Beck-Peccoz P, Bertagna X, Gicquel C, Bertherat J (2007) Somatic TP53 mutations are relatively rare among adrenocortical cancers with the frequent 17p13 loss of heterozygosity. Clin Cancer Res 13 (3):844-850. doi: 10.1158/1078-0432.CCR-06-2085
63. Vargas MP, Vargas HI, Kleiner DE, Merino MJ (1997) Adrenocortical neoplasms: role of prognostic markers MIB-1, P53, and RB. Am J Surg Pathol 21 (5):556-562
64. Morimoto R, Satoh F, Murakami O, Suzuki T, Abe T, Tanemoto M, Abe M, Uruno A, Ishidoya S, Arai Y, Takahashi K, Sasano H, Ito S (2008) Immunohistochemistry of a proliferation marker Ki67/MIB1 in adrenocortical carcinomas:Ki67/MIB1 labeling index is a predictor for recurrence of adrenocortical carcinomas. Endocr J 55 (1):49-55.
65. Dohna M, Reincke M, Mincheva A, Allolio B, Solinas-Toldo S, Lichter P (2000) Adrenocortical carcinoma is characterized by a high frequency of chromosomal gains and high-level amplifications. Genes Chromosomes Cancer 28 (2):145-152. doi:10.1002/(SICI)1098-2264(200006)28:2〈145::AID-GCC3〉3. 0.CO;2-7
66. Gaujoux S, Grabar S, Fassnacht M, Ragazzon B, Launay P, Libe R, Chokri I, Audebourg A, Royer B, Sbiera S, Vacher-Lavenu MC, Dousset B, Bertagna X, Allolio B, Bertherat J, Tissier F (2011) Beta-catenin activation is associated with specific clinical and pathologic characteristics and a poor outcome in adrenocortical carcinoma. Clin Cancer Res 17 (2):328-336. doi: 10.1158/1078-0432.CCR-10-2006
67. Ronchi CL, Sbiera S, Leich E, Tissier F, Steinhauer S, Deutschbein T, Fassnacht M, Allolio B (2012) Low SGK1 Expression in Human Adrenocortical Tumors Is Associated with ACTH-Independent Glucocorticoid Secretion and Poor Prognosis. J Clin Endocrinol Metab. doi: 10.1210/jc.2012-2669
68. Volante M, Sperone P, Bollito E, Frangipane E, Rosas R, Daffara F, Terzolo M, Berruti A, Papotti M (2006) Matrix metalloproteinase type 2 expression in malignant adrenocortical tumors: Diagnostic and prognostic significance in a series of 50 adrenocortical carcinomas. Mod Pathol 19 (12):1563-1569. doi: 10.1038/modpathol.3800683
69. Fenske W, Volker HU, Adam P, Hahner S, Johanssen S, Wortmann S, Schmidt M, Morcos M, Muller-Hermelink HK, Allolio B, Fassnacht M (2009) Glucose transporter GLUT1 expression is an stage-independent predictor of clinical outcome in adrenocortical carcinoma. Endocr Relat Cancer 16 (3):919-928. doi: 10.1677/ERC-08-0211
70. Carney JA, Hruska LS, Beauchamp GD, Gordon H (1986) Dominant inheritance of the complex of myxomas, spotty pigmentation, and endocrine overactivity. Mayo Clin Proc 61 (3):165-172
71. Kirschner LS, Carney JA, Pack SD, Taymans SE, Giatzakis C, Cho YS, Cho-Chung YS, Stratakis CA (2000) Mutations of the gene encoding the protein kinase A type I-alpha regulatory subunit in patients with the Carney complex. Nat Genet 26 (1):89-92. doi:10.1038/79238
72. Else T (2012) Association of adrenocortical carcinoma with familial cancer susceptibility syndromes. Mol Cell Endocrinol 351 (1):66-70. doi:10.1016/j.mce.2011.12.008
73. Painter TA, Jagelman DG (1985) Adrenal adenomas and adrenal carcinomas in associationwith hereditary adenomatosis of the colon and rectum. Cancer 55 (9):2001-2004
74. Lynch HT, Kimberling W, Albano WA, Lynch JF, Biscone K, Schuelke GS, Sandberg AA, Lipkin M, Deschner EE, Mikol YB, et al. (1985) Hereditary nonpolyposis colorectal cancer (Lynch syndromes I and II). I. Clinical description of resource. Cancer 56 (4):934-938
75. Achatz MI, Hainaut P, Ashton-Prolla P (2009) Highly prevalent TP53 mutation predisposing to many cancers in the Brazilian population: a case for newborn screening? Lancet Oncol 10 (9):920-925. doi:10.1016/S1470-2045(09)70089- 0
76. Custodio G, Parise GA, Kiesel Filho N, Komechen H, Sabbaga CC, Rosati R, Grisa L, Parise IZ, Pianovski MA, Fiori CM, Ledesma JA, Barbosa JR, Figueiredo FR, Sade ER, Ibanez H, Arram SB, Stinghen ST, Mengarelli LR, Figueiredo MM, Carvalho DC, Avilla SG, Woiski TD, Poncio LC, Lima GF, Pontarolo R, Lalli E, Zhou Y, Zambetti GP, Ribeiro RC, Figueiredo BC (2013) Impact of neonatal screening and surveillance for the TP53 R337H mutation on early detection of childhood adrenocortical tumors. J Clin Oncol 31 (20):2619-2626. doi:10.1200/JCO.2012.46.3711
77. Herrmann LJ, Heinze B, Fassnacht M, Willenberg HS, Quinkler M, Reisch N, Zink M, Allolio B, Hahner S (2012) TP53 germline mutations in adult patients with adrenocortical carcinoma. J Clin Endocrinol Metab 97 (3):E476-485. doi:10.1210/jc.2011-1982
78. DeChiara TM, Robertson EJ, Efstratiadis A (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64 (4):849-859.
79. Weksberg R, Shuman C, Smith AC (2005) Beckwith-Wiedemann syndrome. Am J Med Genet C Semin Med Genet 137C (1):12-23. doi:10.1002/ajmg.c.30058
80. Langer P, Cupisti K, Bartsch DK, Nies C, Goretzki PE, Rothmund M, Roher HD (2002) Adrenal involvement in multiple endocrine neoplasia type 1. World J Surg 26 (8):891-896. doi:10.1007/s00268-002-6492-4
81. Bertherat J, Bertagna X (2009) Pathogenesis of adrenocortical cancer. Best Pract Res Clin Endocrinol Metab 23 (2):261-271. doi:10.1016/j.beem.2008.10. 006
82. Heppner C, Reincke M, Agarwal SK, Mora P, Allolio B, Burns AL, Spiegel AM, Marx SJ (1999) MEN1 gene analysis in sporadic adrenocortical neoplasms. J Clin Endocrinol Metab 84 (1):216-219
83. Schulte KM, Mengel M, Heinze M, Simon D, Scheuring S, Kohrer K, Roher HD (2000) Complete sequencing and messenger ribonucleic acid expression analysis of the MEN I gene in adrenal cancer. J Clin Endocrinol Metab 85 (1):441-448
84. Tissier F, Cavard C, Groussin L, Perlemoine K, Fumey G, Hagnere AM, Rene-Corail F, Jullian E, Gicquel C, Bertagna X, Vacher-Lavenu MC, Perret C, Bertherat J (2005) Mutations of betacatenin in adrenocortical tumors: activation of the Wnt signaling pathway is a frequent event in both benign and malignant adrenocortical tumors. Cancer Res 65 (17):7622-7627. doi: 10.1158/0008-5472.CAN- 05-0593
85. Berthon A, Martinez A, Bertherat J, Val P (2012) Wnt/beta-catenin signalling in adrenal physiology and tumour development. Mol Cell Endocrinol 351 (1):87-95. doi:10.1016/j.mce.2011.09.009
86. Bonnet S, Gaujoux S, Launay P, Baudry C, Chokri I, Ragazzon B, Libe R, Rene-Corail F, Audebourg A, Vacher-Lavenu MC, Groussin L, Bertagna X, Dousset B, Bertherat J, Tissier F (2011) Wnt/beta-catenin pathway activation in adrenocortical adenomas is frequently due to somatic CTNNB1-activatingmutations, which are associated with larger and nonsecreting tumors: a study in cortisol-secreting and -nonsecreting tumors. J Clin Endocrinol Metab 96 (2): E419-426. doi: 10.1210/jc.2010-1885
87. Yu B, Ragazzon B, Rizk-Rabin M, Bertherat J (2012) Protein kinase A alterations in endocrine tumors. Horm Metab Res 44 (10):741-748. doi:10.1055/s-0032-1316292
88. Cibas ES, Medeiros LJ, Weinberg DS, Gelb AB, Weiss LM (1990) Cellular DNA profiles of benign and malignant adrenocortical tumors. Am J Surg Pathol 14 (10):948-955
89. Stephan EA, Chung TH, Grant CS, Kim S, Von Hoff DD, Trent JM, Demeure MJ (2008) Adrenocortical carcinoma survival rates correlated to genomic copy number variants. Mol Cancer Ther 7 (2):425-431. doi:10.1158/1535-7163.MCT-07-0267
90. Kjellman M, Kallioniemi OP, Karhu R, Hoog A, Farnebo LO, Auer G, Larsson C, Backdahl M (1996) Genetic aberrations in adrenocortical tumors detected using comparative genomic hybridization correlatewith tumor size andmalignancy. Cancer Res 56 (18):4219-4223
91. Letouze E, Rosati R, Komechen H, Doghman M, Marisa L, Fluck C, de Krijger RR, van Noesel MM, Mas JC, Pianovski MA, Zambetti GP, Figueiredo BC, Lalli E (2012) SNP array profiling of childhood adrenocortical tumors reveals distinct pathways of tumorigenesis and highlights candidate driver genes. J Clin Endocrinol Metab 97 (7):E1284-E1293. doi:10.1210/jc.2012-1184
92. Giordano TJ, Thomas DG, Kuick R, Lizyness M, Misek DE, Smith AL, Sanders D, Aljundi RT, Gauger PG, Thompson NW, Taylor JM, Hanash SM (2003) Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis. Am J Pathol 162 (2):521-531. doi: 10.1016/S0002-9440(10)63846-1
93. de Fraipont F, El Atifi M, Cherradi N, Le Moigne G, Defaye G, Houlgatte R, Bertherat J, Bertagna X, Plouin PF, Baudin E, Berger F, Gicquel C, Chabre O, Feige JJ (2005) Gene expression profiling of human adrenocortical tumors using complementary deoxyribonucleic acid microarrays identifies several candidate genes as markers of malignancy. J Clin Endocrinol Metab 90 (3):1819-1829. doi: 10.1210/jc.2004-1075
94. Velazquez-Fernandez D, Laurell C, Geli J, Hoog A, Odeberg J, Kjellman M, Lundeberg J, Hamberger B, Nilsson P, Backdahl M (2005) Expression profiling of adrenocortical neoplasms suggests a molecular signature of malignancy. Surgery 138 (6):1087-1094. doi: 10.1016/j.surg.2005.09.031
95. Slater EP, Diehl SM, Langer P, Samans B, Ramaswamy A, Zielke A, Bartsch DK (2006) Analysis by cDNA microarrays of gene expression patterns of human adrenocortical tumors. Eur J Endocrinol 154 (4):587-598. doi: 10.1530/eje.1.02116
96. Giordano TJ, Kuick R, Else T, Gauger PG, Vinco M, Bauersfeld J, Sanders D, Thomas DG, Doherty G, Hammer G (2009) Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling. Clin Cancer Res 15 (2):668-676. doi: 10.1158/1078-0432.CCR-08-1067
97. de Reynies A, Assie G, Rickman DS, Tissier F, Groussin L, Rene-Corail F, Dousset B, Bertagna X, Clauser E, Bertherat J (2009) Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol 27 (7):1108-1115. doi: 10.1200/JCO.2008.18.5678
98. Tombol Z, Szabo PM, Molnar V, Wiener Z, Tolgyesi G, Horanyi J, Riesz P, Reismann P, Patocs A, Liko I, Gaillard RC, Falus A, Racz K, Igaz P (2009) Integrative molecular bioinformatics study of human adrenocortical tumors: microRNA, tissue-specific target prediction, and pathway analysis. Endocr Relat Cancer 16 (3):895-906. doi:10.1677/ERC-09-0096
99. Laurell C, Velazquez-Fernandez D, Lindsten K, Juhlin C, Enberg U, Geli J, Hoog A, Kjellman M, Lundeberg J, Hamberger B, Larsson C, Nilsson P, Backdahl M (2009) Transcriptional profiling enables molecular classification of adrenocortical tumours. Eur J Endocrinol 161 (1):141-152. doi:10.1530/EJE-09- 0068
100. Assie G, Giordano TJ, Bertherat J (2012) Gene expression profiling in adrenocortical neoplasia. Mol Cell Endocrinol 351 (1):111-117. doi:10.1016/j.mce.2011.09.044
101. de Krijger RR, Papathomas TG (2012) Adrenocortical neoplasia: evolving concepts in tumorigenesis with an emphasis on adrenal cortical carcinoma variants. Virchows Arch 460 (1):9-18. doi:10.1007/s00428-011-1166-y
102. Rana TM (2007) Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 8 (1):23-36. doi: 10.1038/nrm2085
103. Singh P, Soon PS, Feige JJ, Chabre O, Zhao JT, Cherradi N, Lalli E, Sidhu SB (2012) Dysregulation of microRNAs in adrenocortical tumors. Mol Cell Endocrinol 351 (1):118-128. doi:10.1016/j.mce.2011.09.041
104. Soon PS, Tacon LJ, Gill AJ, Bambach CP, Sywak MS, Campbell PR, Yeh MW, Wong SG, Clifton-Bligh RJ, Robinson BG, Sidhu SB (2009) miR-195 and miR-483-5p Identified as Predictors of Poor Prognosis in Adrenocortical Cancer. Clin Cancer Res 15 (24):7684-7692. doi: 10.1158/1078-0432.CCR-09-1587
105. Chabre O, Libe R, Assie G, Barreau O, Bertherat J, Bertagna X, Feige JJ, Cherradi N (2013) Serum miR-483-5p and miR-195 are predictive of recurrence risk in adrenocortical cancer patients. Endocr Relat Cancer 20 (4):579-594. doi:10.1530/ERC-13-0051
106. Gao ZH, Suppola S, Liu J, Heikkila P, Janne J, Voutilainen R (2002) Association of H19 promoter methylation with the expression of H19 and IGF-II genes in adrenocortical tumors. J Clin Endocrinol Metab 87 (3):1170-1176
107. Sidhu S, Martin E, Gicquel C, Melki J, Clark SJ, Campbell P, Magarey CJ, Schulte KM, Roher HD, Delbridge L, Robinson BG (2005) Mutation and methylation analysis of TP53 in adrenal carcinogenesis. Eur J Surg Oncol 31 (5):549-554. doi: 10.1016/j.ejso.2005.01.013
108. Korah R, Healy JM, Kunstman JW, Fonseca AL, Ameri AH, Prasad ML, Carling T (2013) Epigenetic silencing of RASSF1A deregulates cytoskeleton and promotes malignant behavior of adrenocortical carcinoma. Mol Cancer 12:87. doi:10.1186/1476-4598-12-87
109. Fonseca AL, Kugelberg J, Starker LF, Scholl U, Choi M, Hellman P, Akerstrom G, Westin G, Lifton RP, Bjorklund P, Carling T (2012) Comprehensive DNA methylation analysis of benign andmalignant adrenocortical tumors. Genes Chromosomes Cancer 51 (10):949-960. doi:10.1002/gcc.21978
110. Rechache NS, Wang Y, Stevenson HS, Killian JK, Edelman DC, Merino M, Zhang L, Nilubol N, Stratakis CA, Meltzer PS, Kebebew E (2012) DNA methylation profiling identifies global methylation differences and markers of adrenocortical tumors. J Clin Endocrinol Metab 97 (6):E1004-E1013. doi:10.1210/jc.2011-3298
111. Liu-Chittenden Y, Kebebew E (2013) CpG island methylator phenotype in adrenocortical carcinoma: fact or fiction? J Clin Endocrinol Metab 98 (1):48-50. doi:10.1210/jc.2012-4063
112. Barreau O, Assie G, Wilmot-Roussel H, Ragazzon B, Baudry C, Perlemoine K, Rene-Corail F, Bertagna X, Dousset B, Hamzaoui N, Tissier F, de Reynies A, Bertherat J (2013) Identification of a CpG island methylator phenotype in adrenocortical carcinomas. J Clin Endocrinol Metab 98 (1):E174-184. doi:10.1210/jc.2012-2993
113. Barzon L, Sonino N, Fallo F, Palu G, Boscaro M (2003) Prevalence and natural history of adrenal incidentalomas. Eur J Endocrinol 149 (4):273-285
114. Bernard MH, Sidhu S, Berger N, Peix JL, Marsh DJ, Robinson BG, Gaston V, Le Bouc Y, Gicquel C (2003) A case report in favor of a multistep adrenocortical tumorigenesis. J Clin Endocrinol Metab 88 (3):998-1001
115. Trezzi R, Poli F, Fellegara G (2009) "Dedifferentiated" adrenal cortical neoplasm. Int J Surg Pathol 17 (4):343-344. doi:10.1177/ 1066896909335155
116. Heaton JH, Wood MA, Kim AC, Lima LO, Barlaskar FM, Almeida MQ, Fragoso MC, Kuick R, Lerario AM, Simon DP, Soares IC, Starnes E, Thomas DG, Latronico AC, Giordano TJ, Hammer GD (2012) Progression to adrenocortical tumorigenesis in mice and humans through insulin-like growth factor 2 and beta-catenin. Am J Pathol 181 (3):1017-1033. doi:10.1016/j.ajpath.2012.05.026
117. Ronchi CL, Sbiera S, Leich E, Henzel K, Rosenwald A, Allolio B, Fassnacht M (2013) Single nucleotide polymorphism array profiling of adrenocortical tumors - evidence for an adenoma carcinoma sequence? PLoS One 8 (9):e73959. doi:10.1371/journal.pone.0073959