Immunohistochemical staining for diagnosis and prognostic assessment of hydatidiform moles: Current evidence and future directions

Journal of Reproductive Medicine for the Obstetrician and Gynecologist

Volumn 55, Issue 5-6, 2010, Pages 236-246

  Sebire, Neil J ^a   Seckl, Michael J ^a  

^a CHARING CROSS HOSPITAL   (United Kingdom)

Author keywords

Expression; Hydatidiform mole; Immunostaining; Prognosis

Indexed keywords

BIOLOGICAL MARKER; CATHEPSIN D; COLLAGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; INTERLEUKIN 1; LAMININ; MYC PROTEIN; NUCLEOSIDE DIPHOSPHATE KINASE NM23; OCCLUDIN; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN MLH1; PROTEIN MSH2; PROTEIN P53; PROTEIN P57; PROTEINASE INHIBITOR; PROTEINASE INHIBITOR 9; SOMATOMEDIN C; TELOMERASE; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG; TUMOR MARKER;

GENE EXPRESSION PROFILING; HUMAN; HYDATIDIFORM MOLE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; FEMALE; PREGNANCY; UTERUS CANCER;

FEMALE; HUMANS; HYDATIDIFORM MOLE; IMMUNOHISTOCHEMISTRY; PREGNANCY; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL; UTERINE NEOPLASMS;

EID: 77957663778     PISSN: 00247758     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (104)

1. Sebire NJ, Fisher RA, Rees HC: Histopathological diagnosis of partial and complete hydatidiform mole in the first trimester of pregnancy. Pediatr Dev Pathol 2003;6:69-77
2. Sebire NJ, Makrydimas G, Agnantis NJ, et al: Updated diagnostic criteria for partial and complete hydatidiform moles in early pregnancy. Anticancer Res 2003;23:1723-1728
3. Hinshaw K, Fayyad A, Munjaluri P: RCOG Guideline. The Management of Early Pregnancy Loss. RCOG, London, 2006
4. Dulay AT, Copel JA: First-trimester ultrasound: Current uses and applications. Semin Ultrasound CT MR 2008;29: 121-131
5. Fowler DJ, Lindsay I, Seckl MJ, et al: Routine pre-evacuation ultrasound diagnosis of hydatidiform mole: Experience of more than 1000 cases from a regional referral center. Ultrasound Obstet Gynecol 2006;27:56-60
6. Kerkmeijer LG, Massuger LF, Ten Kate-Booij MJ, et al: Earlier diagnosis and serum human chorionic gonadotropin regression in complete hydatidiform moles. Obstet Gynecol 2009;113:326-331
7. Hancock BW, Nazir K, Everard JE: Persistent gestational trophoblastic neoplasia after partial hydatidiform mole incidence and outcome. J Reprod Med 2006;51:764-766
8. Seckl MJ, Fisher RA, Salerno G, et al: Choriocarcinoma and partial hydatidiform moles. Lancet 2000;356:36-39
9. Sebire NJ, Seckl MJ: Gestational trophoblastic disease: Current management of hydatidiform mole. BMJ 2008;337: a1193. doi: 10.1136/bmj.a1193
10. Cheung AN, Srivastava G, Chung LP, et al: Expression of the p53 gene in trophoblastic cells in hydatidiform moles and normal human placentas. J Reprod Med 1994;39:223-227
11. Cheville JC, Robinson RA, Benda JA: p53 expression in placentas with hydropic change and hydatidiform moles. Mod Pathol 1996;9:392-396
12. Qiao S, Nagasaka T, Harada T, et al: p53, Bax and Bcl-2 expression, and apoptosis in gestational trophoblast of complete hydatidiform mole. Placenta 1998;19:361-369
13. Petignat P, Laurini R, Goffin F, et al: Expression of matrix metalloproteinase-2 and mutant p53 is increased in hydatidiform mole as compared with normal placenta. Int J Gynecol Cancer 2006;16:1679-1684
14. Hussein MR: Analysis of p53, BCL-2 and epidermal growth factor receptor protein expression in the partial and complete hydatidiform moles. Exp Mol Pathol 2009;87:63-69
15. Yang X, Zhang Z, Jia C, et al: The relationship between expression of c-ras, c-erbB-2, nm23, and p53 gene products and development of trophoblastic tumor and their predictive significance for the malignant transformation of complete hydatidiform mole. Gynecol Oncol 2002;85:438-444
16. Yazaki-Sun S, Daher S, de Souza Ishigai MM, et al: Correlation of c-erbB-2 oncogene and p53 tumor suppressor gene with malignant transformation of hydatidiform mole. J Obstet Gynaecol Res 2006;32:265-272
17. Balaram P, John M, Enose S, et al: Demonstration of TGFalpha- EGFR and EGF-EGFR autocrine loops and their relation to proliferation in complete hydatidiform moles (CHM). Int J Gynecol Cancer 2001;11:397-402
18. Castrillon DH, Sun D, Weremowicz S, et al: Discrimination of complete hydatidiform mole from its mimics by immunohistochemistry of the paternally imprinted gene product p57KIP2. Am J Surg Pathol 2001;25:1225-1230
19. Xiong Y, Cao Y, Li H: Low and maternal-specific expression of p57KIP2 in hydatidiform mole and its clinical implication. J Huazhong Univ Sci Technolog Med Sci 2002;22:121-122
20. Genest DR, Dorfman DM, Castrillon DH: Ploidy and imprinting in hydatidiform moles: Complementary use of flow cytometry and immunohistochemistry of the imprinted gene product p57KIP2 to assist molar classification. J Reprod Med 2002;47:342-346
21. Fukunaga M: Immunohistochemical characterization of p57(KIP2) expression in early hydatidiform moles. Hum Pathol 2002;33:1188-1192
22. Jun SY, Ro JY, Kim KR: p57kip2 is useful in the classification and differential diagnosis of complete and partial hydatidiform moles. Histopathology 2003;43:17-25
23. Crisp H, Burton JL, Stewart R, et al: Refining the diagnosis of hydatidiform mole: Image ploidy analysis and p57KIP2 immunohistochemistry. Histopathology 2003;43:363-373
24. Popiolek DA, Yee H, Mittal K, et al: Multiplex short tandem repeat DNA analysis confirms the accuracy of p57(KIP2) immunostaining in the diagnosis of complete hydatidiform mole. Hum Pathol 2006;37:1426-1434
25. Maggiori MS, Peres LC: Morphological, immunohistochemical and chromosome in situ hybridization in the differential diagnosis of hydatidiform mole and hydropic abortion. Eur J Obstet Gynecol Reprod Biol 2007; 135:170-176
26. LeGallo RD, Stelow EB, Ramirez NC, et al: Diagnosis of hydatidiform moles using p57 immunohistochemistry and HER2 fluorescent in situ hybridization. Am J Clin Pathol 2008;129:749-755
27. McConnell TG, Murphy KM, Hafez M, et al: Diagnosis and subclassification of hydatidiform moles using p57 immunohistochemistry and molecular genotyping: Validation and prospective analysis in routine and consultation practice settings with development of an algorithmic approach. Am J Surg Pathol 2009;33:805-817
28. Ishikawa N, Harada Y, Tokuyasu Y, et al: Re-evaluation of the histological criteria for complete hydatidiform mole: Comparison with the immunohistochemical diagnosis using p57KIP2 and CD34. Biomed Res 2009;30:141-147
29. Fisher RA, Hodges MD, Rees HC, et al: The maternally transcribed gene p57(KIP2) (CDNK1C) is abnormally expressed in both androgenetic and biparental complete hydatidiform moles. Hum Mol Genet 2002;11:3267-3272
30. Kihara M, Matsui H, Seki K, et al: Genetic origin and imprinting in hydatidiform moles: Comparison between DNA polymorphism analysis and immunoreactivity of p57KIP2. J Reprod Med 2005;50:307-312
31. McConnell TG, Norris-Kirby A, Hagenkord JM, et al: Complete hydatidiform mole with retained maternal chromosomes 6 and 11. Am J Surg Pathol 2009;33:1409-1415
32. Sebire NJ, Rees HC, Peston D, et al: p57(KIP2) immunohistochemical staining of gestational trophoblastic tumours does not identify the type of the causative pregnancy. Histopathology 2004;45:135-141
33. Qiao S, Nagasaka T, Nakashima N: Numerous vessels detected by CD34 in the villous stroma of complete hydatidiform moles. Int J Gynecol Pathol 1997;16:233-238
34. Yoshida K, Nagasaka T, Nakashima N, et al: Elucidation of vascular structure of molar villi in complete hydatidiform mole by CD-34 antibody. Int J Gynecol Pathol 2000;19:212-218
35. Lisman BA, Boer K, Bleker OP, et al: Vasculogenesis in complete and partial hydatidiform mole pregnancies studied with CD34 immunohistochemistry. Hum Reprod 2005;20: 2334-2339
36. Dickson-Gonzalez SM, Garcia de Barriola V, Barbella-Aponte RA, et al: Histopathologic and immunohistochemical evaluation of blood vessels in complete and partial hydatidiform mole. J Reprod Med 2006;51:933-937
37. Kim MJ, Kim KR, Ro JY, et al: Diagnostic and pathogenetic significance of increased stromal apoptosis and incomplete vasculogenesis in complete hydatidiform moles in very early pregnancy periods. Am J Surg Pathol 2006;30:362-369
38. Fu JJ, Lin P, Lv XY, et al: Low molecular mass polypeptide-2 in human trophoblast: Over-expression in hydatidiform moles and possible role in trophoblast cell invasion. Placenta 2009;30:305-312
39. Wong SY, Ngan HY, Chan CC, et al: Apoptosis in gestational trophoblastic disease is correlated with clinical outcome and Bcl-2 expression but not Bax expression. Mod Pathol 1999;12:1025-1033
40. Kim KR, Park BH, Hong YO, et al: The villous stromal constituents of complete hydatidiform mole differ histologically in very early pregnancy from the normally developing placenta. Am J Surg Pathol 2009;33:176-185
41. Genest DR, Laborde O, Berkowitz RS, et al: A clinicopathologic study of 153 cases of complete hydatidiform mole (1980-1990): Histologic grade lacks prognostic significance. Obstet Gynecol 1991;78:402-409
42. Horn LC, Kowalzik J, Bilek K, et al: Prognostic value of trophoblastic proliferation in complete hydatidiform moles in predicting persistent disease. Pathol Res Pract 2006;202: 151-156
43. Bulmer JN, Johnson PM, Sasagawa M, et al: Immunohistochemical studies of fetal trophoblast and maternal decidua in hydatidiform mole and choriocarcinoma. Placenta 1988; 9:183-200
44. Wongweragiat S, Searle RF, Bulmer JN. Decidual T lymphocyte activation in hydatidiform mole. J Clin Pathol 1999; 52:888-894
45. Hussein MR, Abd-Elwahed AR, Abodeif ES, et al: Decidual immune cell infiltrate in hydatidiform mole. Cancer Invest 2009;27:60-66
46. Wongweragiat S, Searle RF, Bulmer JN: Expression of Fas/Fas ligand by decidual leukocytes in hydatidiform mole. Biol Reprod 2001;64:784-789
47. Li AS, Siu MK, Zhang H, et al: Hypermethylation of SOX2 gene in hydatidiform mole and choriocarcinoma. Reprod Sci 2008;15:735-744
48. Feng HC, Tsao SW, Ngan HY, et al: Differential gene expression identified in complete hydatidiform mole by combining suppression subtractive hybridization and cDNA microarray. Placenta 2006;27:521-526
49. Kim SJ, Lee SY, Lee C, Kim et al: Differential expression profiling of genes in a complete hydatidiform mole using cDNA microarray analysis. Gynecol Oncol 2006;103:654-660
50. Cui JQ, Shi YF, Zhou HJ, et al: The changes of gene expression profiles in hydatidiform mole and choriocarcinoma with hyperplasia of trophoblasts. Int J Gynecol Cancer 2004; 14:984-997
51. Ma L, Xiang Y, Zhao J, et al: Comparative proteomic analysis between benign and malignant-transformed hydatidiform mole. J Reprod Med 2008;53:623-628
52. Menczer J, Schreiber L, Berger E, et al: Assessment of Her-2/neu expression in hydatidiform moles for prediction of subsequent gestational trophoblastic neoplasia. Gynecol Oncol 2007;104:675-679
53. Chew SH, Perlman EJ, Williams R, et al: Morphology and DNA content analysis in the evaluation of first trimester placentas for partial hydatidiform mole (PHM). Hum Pathol 2000;31:914-924
54. Fukunaga M: Flow cytometric and clinicopathologic study of complete hydatidiform moles with special reference to the significance of cytometric aneuploidy. Gynecol Oncol 2001;81:67-70
55. Pradhan M, Abeler VM, Danielsen HE, et al: A distinct pattern in the DNA ploidy histograms of hydatidiform moles and nonmolar abortuses is caused by accumulation of tro phoblasts in the late s-phase. Int J Gynecol Pathol 2007;26: 432-436
56. Minami S, Yamoto M, Nakano R: Immunohistochemical localization of inhibin-activin subunits in hydatidiform mole and invasive mole. Obstet Gynecol 1993;82:414-418
57. Mylonas I, Makovitzky J, Vogel M, et al: Expression of inhibin/ activin subunits, sialyl-lewis A (CA 19-9, sLea) and sialyl-Lewis X (sLex) carbohydrate antigens in a hydatidiform mole with persistent polymorphic trophoblastic hyperplasia. Anticancer Res 2005;25:1725-1730
58. Mylonas I, Shabani N, Vogl J, et al: Inhibin/activin subunits are immunohistochemically expressed in complete and partial hydatidiform moles. Anticancer Res 2007;27:1995-2000
59. Balaram P, Alex S, Panikkar B, et al: Adhesion-related proteins E-cadherin, P-cadherin, CD44, and CD44v6, and antimetastatic protein nm23H1 in complete hydatidiform moles in relation to invasion potential. Int J Gynecol Cancer 2004;14:532-539
60. Reynolds EA, DuBeshter B, Katzman P, et al: Expression of CD44, E-cadherin, and antimetastatic protein nm23-H1 in complete hydatidiform moles. Gynecol Oncol 2007;104: 451-454
61. Davidson B, Reich R, Risberg B, et al: The biological role and regulation of matrix metalloproteinases (MMP) in cancer. Arkh Patol 2002;64:47-53
62. Li Z, Xiang Y, Dai L: Prediction of malignant transformation of hydatidiform mole by mRNA determination of matrix metalloproteinases and tissue inhibitor of metalloproteinases. Zhonghua Fu Chan Ke Za Zhi 2000;35:547-550
63. Lian SC, Tan PH: CerbB2 status in breast cancer: Pathologic issues. Ann Acad Med Singapore 2002;31:793-798
64. Belgiovine C, Chiodi I, Mondello C: Telomerase: Cellular immortalization and neoplastic transformation: Multiple functions of a multifaceted complex. Cytogenet Genome Res 2008;122:255-262
65. Bae SN, Kim SJ: Telomerase activity in complete hydatidiform mole. Am J Obstet Gynecol 1999;180:328-333
66. Sukcharoen N, Mutirangura A, Limpongsanurak S: Telomerase activity in complete hydatidiform mole. J Reprod Med 1999;44:465-470
67. Amezcua CA, Bahador A, Naidu YM, et al: Expression of human telomerase reverse transcriptase, the catalytic subunit of telomerase, is associated with the development of persistent disease in complete hydatidiform moles. Am J Obstet Gynecol 2001;184:1441-1446
68. Wang F, Huang H, Kang X, et al: Telomerase activity and the subunit of telomerase in hydatidiform mole and their relationship with the development of postmolar tumor. Eur J Gynaecol Oncol 2006;27:473-476
69. Nishi H, Ohyashiki K, Fujito A, et al: Expression of telomerase subunits and localization of telomerase activation in hydatidiform mole. Placenta 1999;20:317-323
70. Lehner R, Bobak J, Kim NW, et al: Localization of telomerase hTERT protein and survivin in placenta: Relation to placental development and hydatidiform mole. Obstet Gynecol 2001;97:965-970
71. Buzza MS, Hosking P, Bird PI: The granzyme B inhibitor, PI-9, is differentially expressed during placental development and up-regulated in hydatidiform moles. Placenta 2006;27:62-69
72. Pal T, Permuth-Wey J, Sellers TA: A review of the clinical relevance of mismatch-repair deficiency in ovarian cancer. Cancer 2008;113:733-742
73. Chen H, Ye D, Xie X, et al: Mismatch repair gene promoter methylation and expression in hydatidiform moles. Arch Gynecol Obstet 2005;272:35-39
74. Chen H, Ye D, Xie X, et al: PTEN promoter methylation and protein expression in normal early placentas and hydatidiform moles. J Soc Gynecol Investig 2005;12:214-217
75. Saxena A, Frank D, Panichkul P, et al: The product of the imprinted gene IPL marks human villous cytotrophoblast and is lost in complete hydatidiform mole. Placenta 2003;24:835-842
76. Thaker HM, Berlin A, Tycko B, et al: Immunohistochemistry for the imprinted gene product IPL/PHLDA2 for facilitating the differential diagnosis of complete hydatidiform mole. J Reprod Med 2004;49:630-636
77. Fukunaga M: Immunohistochemical characterization of cyclin E and p27KIP1 expression in early hydatidiform moles. Int J Gynecol Pathol 2004;23:259-264
78. Batorfi J, Fulop V, Kim JH, et al: Osteopontin is down-regulated in hydatidiform mole. Gynecol Oncol 2003;89:134-139
79. Capparuccia L, Marzioni D, Giordano A, et al: PPARgamma expression in normal human placenta, hydatidiform mole and choriocarcinoma. Mol Hum Reprod 2002;8:574-579
80. Iwase K, Okamoto T, Nui R, et al: Expression of nm23-H1 in hydatidiform mole and its relationship with the development of postmolar disease. Gynecol Obstet Invest 2001;51: 228-232
81. Alex S, Panikkar B, Devi C, et al: Expression of nm23-H1 protein in relation to myometrial invasion in complete hydatidiform moles. J Soc Gynecol Investig 2002;9:111-115
82. Yang X, Zhang Z, Jia C, et al: The relationship between expression of c-ras, c-erbB-2, nm23, and p53 gene products and development of trophoblastic tumor and their predictive significance for the malignant transformation of complete hydatidiform mole. Gynecol Oncol 2002;85:438-444
83. Goldman-Wohl D, Ariel I, Greenfield C, et al: A study of human leukocyte antigen G expression in hydatidiform moles. Am J Obstet Gynecol 2001;185:476-480
84. Iwahashi M, Muragaki Y, Ooshima A, et al: Decreased type III and V collagen expression in chorionic villi of hydatidiform mole. J Clin Endocrinol Metab 2001;86:3346-3350
85. Iwahashi M, Muragaki Y, Ooshima A, et al: Overexpression of type IV collagen in chorionic villi in hydatidiform mole. J Clin Endocrinol Metab 2001;86:2649-2652
86. Marzioni D, Banita M, Felici A, et al: Expression of ZO-1 and occludin in normal human placenta and in hydatidiform moles. Mol Hum Reprod 2001;7:279-285
87. Prabha B, Molykutty J, Swapna A, et al: Increased expression of interleukin-1 beta is associated with persistence of the disease and invasion in complete hydatidiform moles (CHM). Eur J Gynaecol Oncol 2001;22:50-56
88. Molykutty J, Schultz G, Rajalekshmy TN, et al: Immunolocalization and quantitation of transforming growth factor alpha in hydatidiform mole. Tumori 1999;85:183-187
89. Suresh UR, Hale RJ, Fox H, et al: Use of proliferation cell nuclear antigen immunoreactivity for distinguishing hydropic abortions from partial hydatidiform moles. J Clin Pathol 1993;46:48-50
90. Jeffers MD, Grehan D, Gillan JE: Comparison of villous trophoblast proliferation rate in hydatidiform mole and nonmolar abortion by assessment of proliferating cell nuclear antigen expression. Placenta 1994;15:551-556
91. Cheung AN, Ngan HY, Collins RJ, et al: Assessment of cell proliferation in hydatidiform mole using monoclonal antibody MIB1 to Ki-67 antigen. J Clin Pathol 1994;47:601-604
92. Jeffers MD, Richmond JA, Smith R: Trophoblast proliferation rate does not predict progression to persistent gestational trophoblastic disease in complete hydatidiform mole. Int J Gynecol Pathol 1996;15:34-38
93. Neudeck H, Unger M, Hufnagl P, et al: Villous cytotrophoblast proliferating potential in complete and partial hydatidiform mole: Diagnostic value of silver-stained nucleolar organizer region (AgNOR)-associated proteins. Gen Diagn Pathol 1997;143:179-184
94. Watanabe M, Ghazizadeh M, Konishi H, et al: Interphase cytogenetic and AgNOR analyses of hydatidiform moles. J Clin Pathol 1998;51:438-443
95. Ostrzega N, Phillipson J, Liu P: Proliferative activity in placentas with hydropic change and hydatidiform mole as detected by Ki-67 and proliferating cell nuclear antigen immunostaining. Am J Clin Pathol 1998;110:776-781
96. Wihman IL, Carlstrom K, Faxon M: Insulin-like growth factor- I in women with hydatidiform mole and in normal pregnancy. Obstet Gynecol 1998;92:431-434
97. Nomura S, Okamoto T, Matsuo K, et al: Serum and tissue vascular endothelial growth factor levels in hydatidiform mole. Life Sci 1998;63:1793-1805
98. Iwahashi M, Muragaki Y, Ooshima A, et al. Increased laminin-1 expression in hydatidiform mole. Mol Hum Reprod 1997;3:1107-1111
99. Sasa H, Umekage T, Namima M, et al: Expression of Ras GTPase-activating protein (GAP) in human normal chorionic villi and hydatidiform mole. Placenta 1997;18:427-431
100. Cheung AN, Ngan HY, Ng WF, et al: The expression of cathepsin D, oestrogen receptor and progestogen receptor in hydatidiform mole: An immunohistochemical study. Histopathology 1995;27:341-347
101. Brescia RJ, Kurman RJ, Main CS, et al: Immunocytochemical localization of chorionic gonadotropin, placental lactogen, and placental alkaline phosphatase in the diagnosis of complete and partial hydatidiform moles. Int J Gynecol Pathol 1987;6:213-229
102. Danihel L, Porubski J, Zaviacic T, et al: Trophoblastic disease. I. Use of immunohistochemistry in the diagnosis of complete hydatidiform moles. Cesk Patol 1994;30:76-79
103. Cheah PL, Looi LM: Expression of placental proteins in complete and partial hydatidiform moles. Pathology 1994; 26:115-118
104. Cheung AN, Srivastava G, Pittaluga S, et al: Expression of c-myc and c-fms oncogenes in trophoblastic cells in hydatidiform mole and normal human placenta. J Clin Pathol 1993;46:204-207