Malignancy in pheochromocytomas

APMIS

Volumn 112, Issue 9, 2004, Pages 551-9

  Salmenkivi, Kaisa ^a,b   Heikkilä, Päivi ^a,b   Haglund, Caj ^b   Arola, Johanna ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Adrenal; Extraadrenal; Malignant; Paraganglioma; Pheochromocytoma

Indexed keywords

TUMOR MARKER;

ADRENAL MEDULLA; BENIGN TUMOR; CARCINOGENESIS; CATECHOLAMINE RELEASE; DIFFERENTIAL DIAGNOSIS; HISTOLOGY; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROGNOSIS; REVIEW; TUMOR LOCALIZATION; TUMOR VOLUME;

EID: 11144346961     PISSN: 09034641     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0463.2004.apm1120901.x     Document Type: Review

References (83)

1. Lack EE. Tumors of the adrenal gland and extraadrenal paraganglia. In: Rosai J, editor. Atlas of Tumor Pathology. Washington DC, AFIP 1997:223-53.
2. Melicow MM. One hundred cases of pheochromocytoma (107 tumors) at the Columbia-Presbyterian Medical Center, 1926-1976: a clinicopathological analysis. Cancer 1977;40:1987-2004.
3. Proye C, Vix M, Goropoulos A, Kerlo P, Lecompte-Houcke M. High incidence of malignant pheochromocytoma in a surgical unit. 26 cases out of 100 patients operated from 1971 to 1991. J Endocrinol Invest 1992;15:651-63.
4. Klingler HC, Klingler PJ, Martin JK Jr, Smallridge RC, Smith SL, Hinder RA. Pheochromocytoma. Urology 2001;57:1025-32.
5. Remine WH, Chong GC, van Heerden JA, Sheps SG, Harrison EG. Current management of pheochromocytoma. Ann Surg 1974;179:740-8.
6. Yoshida S, Hatori M, Noshiro T, Kimura N, Kokubun S. Twenty-six-years' survival with multiple bone metastasis of malignant pheochromocytoma. Arch Orthop Trauma Surg 2001;121:598-600.
7. Järveläinen H, Viikari J. Malignant pheochromocytoma behaving as a benign tumor. Duodecim 2001;117:2045-50.
8. van der Harst E, Bruining HA, Jaap Bonjer H, van der Ham F, Dinjens WN, Lamberts SW, de Herder WW, Koper JW, Stijnen T, Proye C, Lecomte-Houcke M, Bosman FT, de Krijger RR. Proliferative index in pheochromocytomas: does it predict the occurrence of metastases? J Pathol 2000;191:175-80.
9. Clarke MR, Weyant RJ, Watson CG, Carty SE. Prognostic markers in pheochromocytoma. Hum Pathol 1998;29:522-6.
10. Linnoila RI, Keiser HR, Steinberg SM, Lack EE. Histopathology of benign versus malignant sympathoadrenal paragangliomas: clinicopathologic study of 120 cases including unusual histologic features. Hum Pathol 1990;21:1168-80.
11. Medeiros LJ, Wolf BC, Balogh K, Federman M. Adrenal pheochromocytoma: a clinicopathologic review of 60 cases. Hum Pathol 1985;16:580-9.
12. John H, Ziegler WH, Hauri D, Jaeger P. Pheochromocytomas: can malignant potential be predicted? Urology 1999;53:679-83.
13. Plouin PF, Chatellier G, Fofol I, Corvol P. Tumor recurrence and hypertension persistence after successful pheochromocytoma operation. Hypertension 1997;29:1133-9.
14. Goldstein RE, O'Neill JA Jr, Holcomb GW 3rd, Morgan WM 3rd, Neblett WW 3rd, Gates JA, Brown N, Nadeau J, Smith B, Page DL, Abumrad NN, Scott HW Jr. Clinical experience over 48 years with pheochromocytoma. Ann Surg 1999;229:755-64.
15. Pommier RF, Vetto JT, Billingsky K, Woltering EA, Brennan MF. Comparison of adrenal and extraadrenal pheochromocytomas. Surgery 1993;114:1160-5.
16. Mornex R, Badet C, Peyrin L. Malignant pheochromocytoma: a series of 14 cases observed between 1966 and 1990. J Endocrinol Invest 1992;15:643-9.
17. Bravo EL. Evolving concepts in the pathophysiology, diagnosis, and treatment of pheochromocytoma. Endocr Rev 1994;15:356-68.
18. van der Harst E, de Herder WW, de Krijger RR, Bruining HA Bonjer HJ, Lamberts SW, van den Meiracker AH, Stijnen TH, Boomsma F. The value of plasma markers for the clinical behaviour of phaeochromocytomas. Eur J Endocrinol 2002;147:85-94.
19. Proye CA, Vix M, Jansson S, Tisell LE, Dralle H, Hiller W. "The" pheochromocytoma: a benign, intra-adrenal, hypertensive, sporadic unilateral tumor, does it exist? World J Surg 1994;18;467-72.
20. Schlumberger M, Gicquel C, Lumbroso J, Tenenbaum F, Comoy E, Bosq J, Fonseca E, Ghillani PP, Aubert B, Travagli JP, Gardet P, Parmentier C. Malignant pheochromocytoma: clinical, biological, histologic and therapeutic data in a series of 20 patients with distant metastases. J Encocrinol Invest 1992;15:631-42.
21. Tibbett PA, McEwan AJ, Ackery DM. A re-evalution of dopamine excretion in pheochromocytoma. Clin Endocrinol 1986;25:401-10.
22. Plouin PF, Chatellier G, Fofol I, Corvol P. Tumor recurrence and hypertension persistence after successful pheochromocytoma operation. Hypertension 1997;29:1133-9.
23. Vassallo G, Capella C, Solcia E. Grimelius's silver stain for endocrine cell granules, as shown by electron microscopy. Stain Technol 1971;46:7-13.
24. Unger P, Hoffman K, Pertsemlidis D, Thung S, Wolfe S, Kaneko M. s-100 protein-positive sustentacular cells in malignant and locally aggressive adrenal pheochromocytomas. Arch Pathol Lab Med 1991;115:484-7.
25. Achilles E, Padberg BC, Holl K, Kloppel G, Schroder S. Immunocytochemistry of paragangliomas-value of staining for S-100 protein and glial fibrillary acid protein in diagnosis and prognosis. Histopathology 1991;18:453-8.
26. Montresor E, Iacono C, Nifosi F, Zanza A, Modena S, Zamboni G, Bernardello F, Serio G. Retroperitoneal paragangliomas: role of immunohistochemistry in the diagnosis of malignancy and in assessment of prognosis. Eur J Surg 1994;160:547-52.
27. Thompson LD. Pheochromocytoma of the Adrenal gland Scaled Score (PASS) to separate benign from malignant neoplasms: clinicopathologic and immunophenotypic study of 100 cases. Am J Surg Pathol 2002;26:551-66.
28. Salmenkivi K, Heikkilä P, Haglund C, Louhimo J, Arola J. Lack of histopathologically suspicious features, proliferative activity, and p53 expression suggests benign diagnosis in pheochromocytomas. Histopathology 2003;43:62-71.
29. Shibuya M, Saito F, Miwa T, Davis RL, Wilson CB, Hoshino T. Histochemical study of pituitary adenomas with Ki-67 and anti-DNA polymerase alpha monoclonal antibodies, bromodeoxyuridine labeling, and nucleolar organizer region counts. Acta Neuropathol 1992;84:178-83.
30. Katoh R, Bray CE, Suzuki K, Komiyama A, Hemmi A, Kawaoi A, Oyama T, Sugai T, Sasou S. Growth activity in hyperplastic and neoplastic human thyroid determined by an immunohistochemical staining procedure using monoclonal antibody MIB-1. Hum Pathol 1995;26:139-46.
31. Abbona GC, Papotti M, Gasparri G, Bussolati G. Proliferative activity in parathyroid tumors as detected by Ki-67 immunostaining. Hum Pathol 1995;26:135-8.
32. Pelosi G, Bresaola E, Bogina G, Pasini F, Rodella S, Castelli P, Iacono C, Serio G, Samboni G. Endocrine tumors of the pancreas: Ki-67 immunoreactivity on paraffin sections is an independent predictor for malignancy: a comparative study with proliferating-cell nuclear antigen and progesterone receptor protein immunostaining, mitotic index, and other clinicopathologic variables. Hum Pathol 1996;27:1124-34.
33. Goldblum J, Shannon R, Kaldjian EP, Thiny M, Davenport R, Thompson N, Lloyd R. Immunohistochemical assessment of proliferative activity in adrenal cortical neoplasms. Mod Pathol 1993;6:663-8.
34. Nagura S, Katoh R, Kawaoi A, Kobayashi M, Obara T, Omata K. Immunohistochemical estimations of growth activity to predict biological behavior of pheochromocytomas. Mod Pathol 1999;12:1107-11.
35. Castilla-Guerra L, Moreno AM, Fernandez-Moreno MC, Utrilla JC, Fernandez E, Galera-Davison H. Expression and prognostic value of c-erbB-2 oncogene product in human pheochromocytomas. Histopathology 1997;31:144-9.
36. de Krijger RR, van der Harst E, van der Ham F, Stijnen T, Dinjens WN, Koper JW, Bruining HA, Lamberts SW, Bosman FT. Prognostic value of p53, bcl-2, and c-crbB-2 protein expression in pheochromocytomas. J Pathol 1999;188:51-5.
37. Shay JW, Bachetti S. A survey of telomerase activity in human cancer. Eur J Cancer 1997;33:787-91.
38. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW. Specific association of human telomerase activity with immortal cells and cancer. Science 1994;266:2011-5.
39. Kubota Y, Nakada T, Sasagawa I, Yanai H, Itoh K. Elevated levels of telomerase activity in malignant pheochromocytoma. Cancer 1998;82:176-9.
40. Elder EE, Xu D, Hoog A, Enberg U, Hou M, Hou M, Pisa P, Gruber A, Larsson C, Backdahl M. Ki-67 and hTERT expression can aid in the distinction between malignant and benign pheochromocytoma and paraganglioma. Mod Pathol 2003;16:246-55.
41. Boltze C, Mundschenk J, Unger N, Schneider-Stock R, Peters B, Mawrin C, Hoang-Vu C, Roessner A, Lehnert H. Expression profile of the telomeric complex discriminates between benign and malignant pheochromocytoma. J Clin Endocrinol Metab 2003;88:4280-6.
42. Risbridger GP, Schmitt FJ, Robertson DM. Activins and inhibins in endocrine and other tumors. Endocr Rev 2001;22:836-58.
43. Munro LMA, Kennedy A, McNicol AM. The expression of inhibin/activin subunits in the human adrenal cortex and its tumors. J Endocrinol 1999;161:341-7.
44. Spencer SJ, Rabinovici J, Mesiano S, Goldsmith PC, Jaffe RB. Activin and inhibin in the human adrenal gland, regulation and differential effects in fetal and adult cells. J Clin Invest 1992;90:142-9.
45. Salmenkivi K, Arola J, Voutilainen R, Ilvesmäki V, Haglund C, Kahri AI, Heikkilä P, Liu J. Inhibin/activin betaB subunit expression in pheochromocytomas favors benign diagnosis. J Clin Endocrinol Metab 2001;86:2231-5.
46. Hollstein M, Sidransky D, Vogelstein B, Harris C. p53 mutations in human cancers. Science 1991;253:49-53.
47. Dahia PLM, Aguiar RCT, Tsanaclis AM, Bendit I, Bydlowski SP, Abelin NMA, Toledo SPA. Molecular and immunohistochemical analysis of p53 in pheochromocytoma. Br J Cancer 1995;72:1211-3.
48. Gupta D, Shidham V, Holden J, Layfield L. Prognostic value of immunohistochemical expression of topoisomerase alpha II, MIB-1, p53, E-cadherin, retinoblastoma gene protein product, and HER-2/neu in adrenal and extra-adrenal pheochromocytomas. Appl Immunohistochem Mol Morphol 2000;8:267-74.
49. Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 1989;161:851-8.
50. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 1991;12:1806-14.
51. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992;255:989-91.
52. Semenza GL. HIF-1 and human disease: one highly involved factor. Genes Dev 2000;14:1983-91.
53. Dobbs SP, Hewett PW, Johnson IR, Carmichael J, Murray JC. Angiogenesis is associated with vascular endothelial growth factor expression in cervical intraepithelial neoplasia. Br J Cancer 1997;76:1410-5.
54. Guidi AJ, Abu-Jawdeh G, Tognazzi K, Dvorak HF, Brown LF. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in endometrial carcinoma. Cancer 1996;78:454-60.
55. Favier J, Plouin PF, Corvol P, Gasc JM. Angiogenesis and vascular architecture in pheochromocytomas: distinctive traits in malignant tumors. Am J Pathol 2002;161:1235-46.
56. Takekoshi K, Isobe K, Yashiro T, Kara H, Ishii K, Kawakami Y, Nakai T, Okuda Y. Expression of vascular endothelial growth factor (VEGF) and its cognate receptors in human pheochromocytomas. Life Sci 2004;74:863-71.
57. Zielke A, Middeke M, Hoffmann S, Colombo-Benkmann M, Barth P, Hassan I, Wunderlich A, Hofbauer LC, Duh QY VEGF-mediated angiogenesis of human pheochromocytomas is associated to malignancy and inhibited by anti-VEGF antibodies in experimental tumors. Surgery 2002;132:1056-63.
58. Salmenkivi K, Heikkilä P, Liu J, Haglund C, Arola J. VEGF in 105 pheochromocytomas: enhanced expression correlates with malignant outcome. APMIS 2003;111:458-64.
59. Bull HA, Brickell PM, Dowd PM. Src-related protein tyrosine kinases are physically associated with the surface antigen CD36 in human dermal microvascular endothelial cells. FEBS Lett 1994;351:41-4.
60. Kolomecki K, Stepien H, Bartos M, Kuzdak K. Usefulness of VEGF, MMP-2, MMP-3 and TIMP-2 serum level evaluation in patients with adrenal tumors. Endocr Regul 2001;35:9-16.
61. Eccles S. Heparanase: breaking down barriers in tumors. Nat Med 1999;5:735-6.
62. Quiros RM, Kim AW, Maxhimer J, Gattuso P, Xy X, Prinz RA. Differential heparanase-1 expression in malignant and benign pheochromocytomas. J Surg Res 2002;108:44-50.
63. Mackie EJ, Chiquet-Ehrismann R, Pearson CA, Inaguma Y, Taya K, Kawarada Y, Sakakura T. Tenascin is a stromal marker for epithelial malignancy in the mammary gland. Proc Natl Acad Sci USA 1987;84:4621-5.
64. Iskaros BF, Tanaka KE, Hu X, Kadish AS, Steinberg JJ. Morphologic pattern of tenascin as a diagnostic biomarker in colon cancer. J Surg Oncol 1997;64:98-101.
65. Kusagawa H, Onoda K, Namikawa S, Yada I, Okada A, Yoshida T, Sakakura T. Expression and degeneration of tenascin-C in human lung cancers. Br J Cancer 1998;77:98-102.
66. Salmenkivi K, Haglund C, Arola J, Heikkilä P. Increased expression of tenascin in pheochromocytomas correlates with malignancy. Am J Surg Pathol 2001;25:1419-23.
67. Dubois RN, Abramson SB, Crofford L, Gupta RA, Simon LS, van de Putte LBA, Lipsky PE. Cyclooxygenase in biology and disease. FASEB J 1998;12:1063-73.
68. Vane JR, Bakhle VS, Botting RM. Cyclooxygenase 1 and 2. Annu Rev Pharmacol Toxicol 1998;38:97-120.
69. Taketo MM. Cyclooxygenase-2 inhibitors in tumorigenesis (part II). J Natl Cancer Inst 1998;90:1609-20.
70. Tsujii M, Kawano S, Dubois RN. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc Natl Acad Sci USA 1997;94:3336-40.
71. Salmenkivi K, Haglund C, Ristimäki A, Arola J, Heikkilä P. Increased expression of cyclooxygenase-2 in malignant pheochromocytomas. J Clin Endocrinol Metab 2001;86:5615-9.
72. Latif F, Tory K, Gnarra J, Yao M, Duh FM, Orcutt ML, Stackhouse T, Kuzmin I, Modi W, Geil L. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993;260:1317-20.
73. Walther MM, Herring J, Enquist E, Keiser HR, Linehan WM. von Recklinghausen's disease and pheochromocytomas. J Urol 1999;162:1582-6.
74. Mulligan LM, Kwok JB, Healey CS, Elsdon MJ, Eng C, Gardner E, Love DR, Mole SE, Moore JK, Papi L. Germ-line mutations of the RET proto-oncogene in multiple endocrine neoplasia type 2A. Nature 1993;363:458-60.
75. Astuti D, Douglas F, Lennard TW, Aligianis IA, Woodward ER, Evans DG, Eng C, Latif F, Maher ER. Germline SDHS mutation in familial pheochromocytoma. Lancet 2001;357:1181-2.
76. Baysal B, Ferrell RE, Willett-Brozick JE, Lawrence EC, Myssiorek D, Bosch A, van der Mey A, Taschner PE, Rubinstein WS, Myers EN, Richard CW 3rd, Cornelisse CJ, Devilee P, Devlin B. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000;287:848-51.
77. Niemann S, Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 2000;26:268-70.
78. Neumann HPH, Berger DP, Sigmund G, Blum U, Schmidt D, Parmer RJ, Volk B, Kirste G. Pheochromocytomas, multiple endocrine neoplasia type 2, and von Hippel-Lindau disease. New Engl J Med 1993;329:1531-8.
79. Neumann HPH, Bausch B, McWhinney SR, Bender BU, Gimm O, Franke G, Schipper J, Klisch J, Altehoefer C, Zerres K, Januszewicz A, Eng C, Smith WM, Munk R, Manz T, Glaesker S, Apel TW, Treier M, Reineke M, Walz MK, Hoang-Vu C, Brauckhoff M, Klein-Franke A, Klose P, Schmidt H, Maier-Woelfle M, Peczkowska M, Szmigielski C. Germ-line mutations in nonsyndromic pheochromocytoma. N Engl J Med 2002;346:1459-66.
80. Bender BU, Gutsche M, Glasker S, Muller B, Kirste G, Eng C, Neumann HPH. Differential genetic alterations in von Hippel-Lindau syndrome-associated and sporadic pheochromocytomas. J Clin Endocrinol Metab 2000;85:4568-74.
81. Khosla S, Patel VM, Hay ID, Schaid DJ, Grant CS, van Heerden JA, Thibodeau SN. Loss of heterozygosity suggests multiple genetic alterations in pheochromocytomas and medullary thyroid carcinomas. J Clin Invest 1991;87:1691-9.
82. Tsutsumi M, Yokota J, Kakizoe T, Koiso K, Sugimura T, Terada M. Loss of heterozygosity on chromosomes 1p and 11p in sporadic pheochromocytoma. J Natl Cancer Inst 1989;81:367-70.
83. Vargas MP, Shuang Z, Wang C, Vortmeyer A, Linehan WM, Merino MJ. Loss of heterozygosity on the short arm of chromosomes 1 and 3 in sporadic pheochromocytoma and extra-adrenal paraganglioma. Hum Pathol 1997;28:411-5.