Dynamic behavioural interpretation of cervical intraepithelial neoplasia with molecular biomarkers

Journal of Clinical Pathology

Volumn 59, Issue 10, 2006, Pages 1017-1028

  Baak, J P A ^a,b,c   Kruse, A J ^a,d   Robboy, S J ^e   Janssen, E A M ^a   Van Diermen, B ^a   Skaland, I ^a  

^a STAVANGER UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CELL CYCLE PROTEIN; CYTOKERATIN 13; CYTOKERATIN 14; EOSIN; HEMATOXYLIN; KI 67 ANTIGEN; PROTEIN P16; PROTEIN P53; RETINOBLASTOMA PROTEIN; VIRUS PROTEIN;

CANCER GRADING; CANCER GROWTH; CANCER REGRESSION; CANCER RISK; GENOTYPE; HOST; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MICROSCOPE; MORPHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PUNCH BIOPSY; REVIEW; UTERINE CERVIX CARCINOMA IN SITU; UTERINE CERVIX EPITHELIUM; WART VIRUS;

CERVICAL INTRAEPITHELIAL NEOPLASIA; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DISEASE PROGRESSION; FEMALE; HUMANS; KI-67 ANTIGEN; PAPILLOMAVIRUS INFECTIONS; TUMOR MARKERS, BIOLOGICAL; UTERINE CERVICAL NEOPLASMS;

EID: 33750020052     PISSN: 00219746     EISSN: None     Source Type: Journal    
DOI: 10.1136/jcp.2005.027839     Document Type: Review

References (101)

1. Ostor AG. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 1993;12:186-92.
2. Heatly MK. How should we grade CIN? Histopathology 2002;40:377-90.
3. Keenem SJ, Diamond J, McCluggage WG, et al. An automated machine vision system for the histological grading of cervical intraepithelial neoplasia (CIN). J Pathol 2000;192:351-62.
4. McCluggage WG, Bharucha H, Caughley LA, et al. Interobserver variation in the reporting of cervical colposcopic biopsy specimens: comparison of grading systems. J Clin Pathol 1996;49:833-5.
5. Ismail SM, Colclough AB, Dinnen JS, et al. Reporting cervical intra-epithelial neoplasia (CIN): intra and inter-pathologist variation and factors associated with disagreement. Histopathology 1990;16:371-6.
6. Ismail SM, Colclough AB, Dinnen JS, et al. Observer variation in histopathological diagnosis and grading of cervical intraepithelial neoplasia. BMJ 1989;298:707-10.
7. Robertson AJ, Anderson JM, Swanson Beck J, et al. Observer variability in histopathological reporting of cervical biopsy specimens. J Clin Pathol 1989;42:231-8.
8. Stoler MH, Schiffman M. Atypical Squamous Cells of Undetermined Significance-Low-grade Squamous Intraepithelial Lesion Triage Study (ALTS) Group. Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study, JAMA 2001;285:1500-5.
9. Grenko RT, Abendroth CS, Frauenhoffer EE, et al. Variance in the interpretation of cervical biopsy specimens obtained for atypical squamous cells of undetermined significance. Am J Clin Pathol 2000;114:735-40.
10. Al Nafussi AI, Colquhoun MK. Mild cervical intraepithelial neoplasia (CIN-1)-a histological overdiagnosis. Histopathology 1990;17:557-61.
11. Creagh T, Bridger JE, Kupek E, et al. Pathologist variation in reporting cervical borderline epithelial abnormalities and cervical intraepithelial neoplasia. J Clin Pathol 1995;48:59-60.
12. Kruse AJ, Baak JP, Janssen EA, et al. Ki-67 predicts progression in early CIN: validation of a multivariate progression-risk model. Cell Oncol 2004;26:13-20.
13. Kruse AJ, Buhr-Wildhagen S, Janssen EA, et al. The relationship between syntactic structure analysis features, histological grade and high-risk HPV DNA in cervical intraepithelial neoplasia. Cell Oncol 2004;26:135-41.
14. Kruse AJ, Gudlaugsson E, Helliesen T, et al. Evaluation of prospective, routine application of Ki-67 immunoquantitation in early CIN for assessment of short-term progression risk. Anal Quant Cytol Histol 2004;26:134-40.
15. Kruse AJ, Skaland I, Janssen EA, et al. Quantitative molecular parameters to identify low-risk and high-risk early CIN lesions: role of markers of proliferative activity and differentiation and Rb availability. Int J Gynecol Pathol 2004;23:100-9.
16. Kruse AJ, Baak JP, Helliesen T, et al. Prognostic value and reproducibility of koilocytosis in cervical intraepithelial neoplasia. Int J Gynecol Pathol 2003;22:236-9.
17. Kruse AJ, Baak JP, Janssen EA, et al. Low- and high-risk CIN-1 and 2 lesions: prospective predictive value of grade, HPV, and Ki-67 immunoquantitative variables. J Pathol 2003;199:462-70.
18. Kruse AJ, Baak JP, Helliesen T, et al. Evaluation of KI-67-positive cell clusters as a diagnostic marker for cervical intraepithelial neoplasia. Am J Surg Pathol 2002;26:1501-7.
19. Kruse AJ, Baak JP, de Bruin PC, et al. Relationship between the presence of oncogenic HPV DNA assessed by polymerase chain reaction and Ki-67 immunoquantitative features in cervical intraepithelial neoplasia. J Pathol 2001;195:557-62.
20. Kruse AJ, Baak JP, de Bruin PC, et al. Ki-67 immunoquantitation in cervical intraepithelial neoplasia (CIN): a sensitive marker for grading. J Pathol 2001;193:48-54.
21. Sono T, Oyama T, Kashiwabara K, et al. Expression status of p16 protein is associated with human papillomavirus oncogenic potential in cervical and genital lesions. Am J Pathol 1998;153:1741-8.
22. Klaes R, Friedrich T, Spitkovsky D, et al. Overexpression of p16(INK4A) as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer 2002;92:276-84.
23. Keating JT, Cviko A, Riethdorf S, et al. Ki-67, cyclin E, and p16INK4A are complimentary surrogate biomarkers for human papilloma virus-related cervical neoplasia. Am J Surg Pathol 2001;25:884-91.
24. Nucci MR, Castrillon OH, Bai H, et al. Biomarkers in diagnostic obstetric and gynecologic pathology: a review. Adv Anat Pathol 2003;10:55-68.
25. Pirog EC, Baergen RN, Soslow RA et al. Diagnostic accuracy of cervical low-grade squamous intraepithelial lesions is improved with Ki-67 immunostaining. Am J Surg Pathol 2002;26:70-5.
26. Kiviat N. Natural history or cervical neoplasia: overview and update. Am J Obstet Gynecol 1996;175:1099-104.
27. Koutsky LA, Holmes KK, Critchlow CW, et al. A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl J Med 1992;327:1271-8.
28. Woodman CBJ, Collins S, Winter H, et al. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 2001;357:1831-6.
29. Saito K, Saito A, Fu YS, et al. Topographic study of cervical condyloma and intraepithelial neoplasia. Cancer 1987;59:2064-70.
30. Schneider V. CIN prognostication: will molecular techniques do the trick? Acta Cytol 2003;47:115-6.
31. El Hamidi A, Kocjan G, Du M-Q. Clonality analysis of archival cervical smears. Correlation of monoclonality with grade and clinical behavior of cervical intraepithelial neoplasia. Acta Cytol 2003;47:117-23.
32. Crum CP, Abbott DW, Quade BJ. Cervical cancer screening: from the papanicolaou smear to the vaccine era. J Clin Oncol 2003;21:224-30.
33. Sun CA, Lai HC, Chang CC, et al. The significance of human papillomavirus viral load in prediction of histologic severity and size of squamous intraepithelial lesions of uterine cervix. Gynecol Oncol 2001;83:95-9.
34. Clovel C, Masure M, Levert M, et al. Human papillomavirus detection by the hybrid capture II assay: a reliable test to select women with normal cervical smears at risk for developing cervical lesions. Diagn Mol Pathol 2000;9:145-50.
35. Nobbenhuis MAE, Walboomers JMM, Helmerhorst ThJM, et al. Relation of human papillomavirus status to cervical lesions and consequences for cervical-cancer screening: a prospective study. Lancet 1999;354:20-5.
36. Bosch FX, Lorincz A, Munoz N, et al. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002;55:244-65.
37. Cuschieri KS, Cubie HA, Whitley MW, et al. Persistent high risk HPV infection associated with development of cervical neoplasia in a prospective population study. J Clin Pathol 2005;58:946-50.
38. Schiffman M, Herrero R, Hildesheim A, et al. HPV DNA testing in cervical cancer screening: results from women in a high-risk province or Costa Rica. JAMA 2000;283:87-93.
39. Healey SM, Aronson KJ, Mao Y, et al. Oncogenic human papillomavirus infection and cervical lesions in aboriginal women of Nunavut, Canada. Sex Transm Dis 2001;28:694-700.
40. Sherman ME, Schiffman M, Cox JT. Effects of age and HPV viral load on colposcopy triage: data from the randomized atypical squamous cells of undetermined significance/low-grade squamous intraepithelial lesion triage study (ALTS). J Natl Cancer Inst 2002;94:102-7.
41. Van Duin M, Snijders PJ, Schrijnemakers HF, et al. Human papillomavirus 16 load in normal and abnormal cervical scrapes: an indicator of CIN II/III and viral clearance. Int J Cancer 2002;98:590-5.
42. Daistein V, Riethmuller D, Pretet JL, et al. Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int J Cancer 2003;106:396-403.
43. Koutsky IA, Ault KA, Wheeler CM, et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002;347:1645-51.
44. Fairley CK, Robinson PM, Chen S, et al. The detection of HPV DNA, the size of tampon specimens and the menstrual cycle. Genitourin Med 1994;70:171-4.
45. Robboy SJ, Anderson MC, Morse A, et al. Cervical precancer (intraepithelial neoplasia). In: Robboy SJ, Anderson MC, Russell P, eds. Pathology of the female reproductive tract. London: Churchill Livingstone, 2002:165-93.
46. Hildesheim A, Schiffman MH, Gravitt PE, et al. Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis 1994;169:235-40.
47. Hinchlife SA, van Velzen D, Korporaal, et al. Transience of cerical HPV infection in sexually active, young women with normal cervicavaginal cytology. Br J Cancer 1995;72:943-5.
48. Wheeler C, Greer CE, Becker TM, et al. Short-term fluctuations in the detection of cervical human papillomvirus DNA. Obstet Gynecol 1996;88:261-8.
49. Moscicki A, Shiboski S, Broering J, et al. The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr 1998;132:277-84.
50. Ho GYF, Bierman R, Beardsly L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998;338:423-8.
51. Rozendaal L, Walboomers JMM, van der Linden JC, et al. PCR-based high risk HPV test in cervical cancer screening gives objective risk assessment of women with cytomorphologically normal cervical smears. Int J Cancer 1996;68:766-9.
52. Ho GYF, Burk RD, Klein S, et al. Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst 1995;87:1365-71.
53. Koutsky LA, Holmes KK, Critchlow CW, et al. A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl J Med 1992;327:1272-8.
54. Cuschieri KS, Cubie HA, Whitley MW, et al. Multiple high risk HPV infections are common in cervical neoplasia and young women in a cervical screening population. J Clin Pathol 2004;57:68-72.
55. Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005;32:S16-S24.
56. Steenbergen RDM, de Wilde J, Wilting SM, et al. HPV-mediated transformation of the anogenital tract. J Clin Virol 2005;325:S25-33.
57. Milde-Langosch K, Riethdorf S. Role of cell-cycle regulatory proteins in gynecological cancer. J Cell Physiol 2003;196:224-44.
58. Trunk MJ, Wentzensen N, von Knebel Doeberitz M. Molecular pathogenesis of cervical cancer and its first steps. Pathologie 2005;26:283-90.
59. Wright TC, Kurman RJ, Ferenczy A. Precancerous lesions of the cervix. In: Kurman RJ, eds. Blaustein's pathology of the female genital tract. 5th edn. New York: Springer, 2002:278-9.
60. Zur Hausen H. Papillomavirus causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000;92:690-8.
61. von Knebel Doeberitz M. New markers for cervical dysplasia to visualise the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur J Cancer 2002;38:2229-42.
62. Klaes R, Woerner SM, Ridder R, et al. Detection of high-risk cervical intraepithelial neoplasia and cervical cancer by amplification of transcripts derived from integrated papillomavirus oncogenes. Cancer Res 1999;59:6132-6.
63. Nishimura A, Ono T, Ishimoto A, et al. Mechanisms of human papillomavirus E2-mediated repression of viral oncogene expression and cervical cancer cell growth inhibition. J Virol 2000;74:3752-60.
64. Riley RR, Duensing S, Brake T, et al. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res 2003;63:4862-71.
65. Jeon S, Allen-Hoffmann BL, Lambert PF. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J Virol 1995;69:2989-97.
66. Zur Hausen H. Papillomavirus and cancer: from basic studies to clinical application. Nat Rev Cancer 2002;2:342-50.
67. Munger K, Howley PM. Human papillomavirus immortalization and transformation functions. Virus Res 2002;89:213-28.
68. Duensing S, Duensing A, Crum CP, et al. Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res 2001;61:2356-60.
69. Wang SS, Hildesheim A. Viral and host factors in human papillomavirus persistence and progression. J Natl Cancer Inst 2003;31:35-40.
70. Hildesheim A, Wang SS. Host and viral genetics and risk of cervical cancer: a review. Virus Res 2002;89:229-40.
71. Villa LL, Sichero L, Rahal P, et al. Molecular variants of human papillomavirus types 16 and 18 preferentially associated with cervical neoplasia. J Gen Virol 2000;81:2959-68.
72. Chan PK, Lam CW, Cheung TH, et al. Association of human papillomavirus type 58 variant with the risk of cervical cancer. J Natl Cancer Inst 2002;94:1249-53.
73. Ylitalo N, Sorensen P, Josefson AM, et al. Consistent high viral load of human papillomavirus 16 and risk of cervical carcinoma in situ: a nested case-control study. Lancet 2000;355:2194-8.
74. Lorincz AT, Castle PE, Sherman ME. Viral load of human papillomavirus and risk of CIN3 or cervical cancer. Lancet 2002;360:228-9.
75. Schiller JT, Hildesheim A. Developing HPV virus-like particle vaccines to prevent cervical cancer: a progress report. J Clin Virol 2000;19:67-74.
76. Lehtinen M, Dillner J, Knekt P, et al. Serologically diagnosed infection with human papillomavirus type 16 and risk of subsequent development of cervical carcinoma: nested case-control study. BMJ 1996;312:537-9.
77. De Sanjose S, Hamsikova E, Munoz N, et al. Serological response to HPV16 in CIN-III and cervical cancer patients. Case-control studies in Spain and Colombia. Int J Cancer 1996;66:70-4.
78. Sun Y, Eluf-Neto J, Bosch FX, et al. Serum antibodies to HPV16 proteins in women from Brazil with invasive cervical carcinoma. Cancer Epidemiol Biomarkers Prev 1999;8:935-40.
79. Tsukui T, Hildesheim A, Schiffman MH, et al. Il-2 production by peripheral lymphocytes in response to human papillomavirus-derived peptides: correlation with cervical pathology. Cancer Res 1996;56:3967-74.
80. Kadish AS, Timmins P, Wang Y, et al. Regression of CIN and loss of HPV infection is associated with cell-mediated immune responses to an HPV type 16 E7 peptide. Cancer Epidemiol Biomarkers Prev 2002;11:483-8.
81. Carreon JD, Martin MP, Hildesheim, et al. Human leukocyte antigen class I and II haplotypes and risk of cervical cancer. Tissue Antigens 2005;66:321-4.
82. Hemminki K, Li X, Mutanen P. Familial risk in invasive and in situ cervical cancer by histological type. Eur J Cancer Prev 2001;10:83-9.
83. Magnusson PK, Lichtenstein P, Gyllensten UB. Heritability of cervical tumours. Int J Cancer 2000;88:698-701.
84. Klaes R, Benner A, Friedrich T, et al. p16INK4a immunohistochemistry improves interobserver agreement in the diagnosis of cervical intraepithelial neoplasia. Am J Surg Pathol 2002;26:1389-99.
85. Snijders PJ, Steenbergen RDM, Heideman DA, et al. HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 2006;208:152-64.
86. Kruse AJ. Quantitative biomarkers to identify low- and high-risk early CIN lesions [dissertation]. Vrije Universiteit Amsterdam, 2003.
87. Murphy N, Ring M, Killalea AG, et al. P16ink4a as a marker for cervical dyskaryosis: CIN and cGIN in cervical biopsies and ThinPrep smears. J Clin Pathol 2003;56:56-63.
88. Bulten J, Van der Laak JA, Gemmink JH, et al. Ki-67, a promising marker for the classification of cervical intraepithelial neoplasia. J Pathol 1996;178:268-73.
89. Abadi MA, Ho GYF, Burk RD, et al. Stringent criteria for histological diagnosis of koilocytosis fail to eliminate overdiagnosis of human papillomavirus infection and cervical intraepithelial neoplasia grade 1. Hum Pathol 1998;29:54-9.
90. Reesink-Peters N, Helder MN, Wisman GB, et al. Detection of telomerase, its components, and human papillomavirus in cervical scrapings as a tool for triage in women with cervical dysplasia. J Clin Pathol 2003;56:31-5.
91. Bravaccini S, Sanchini MA, Amadori A, et al. Potential of telomerase expression and activity in cervical specimens as a diagnostic tool. J Clin Pathol 2005;58:911-4.
92. Southern SA, McDicken IW, Herrington CS. Loss of cytokeratin 14 expression is related to human papillomavirus type and lesion grade in squamous intraepithelial lesions of the cervix. Hum Pathol 2001;32:1351-5.
93. Sadlar L, Saftlas A, Wang W, et al. Treatment for cervical intraepithelial neoplasia and risk of preterm delivery. JAMA 2004;291:2100-6.
94. Baak JPA, Kruse A-J, Garland SM, et al. Combined p53 and retinoblastoma protein detection identify persistent and regressive cervical high-grade squamous intraepithelial lesions. Am J Surg Pathol 2005;29:1062-6.
95. Zielinsky GD, Snijders PJF, Rozendaal L, et al. The presence of high-risk HPV combined with specific p53 and p16ink4a expression patterns points to high-risk HPV as the main causative agent for adenocarcinoma in situ and adenocarcinoma of the cervix. J Pathol 2003;201:535-43.
96. Trimble CL, Piantadosi S, Gravitt P, et al. Spontaneous regression of high-grade cervical dysplasia: effects of human papillomavirus type and HLA phenotype. Clin Cancer Res 2005;11:4717-23.
97. Hagen B, Skjeldestad FE. A guide in gynecological oncology 2002. Oslo: The Norwegian Medical Association, 2002.
98. Follen M, Atkinson EN, Schottenfeld D. A randomized clinical trial of 4-hydroxyphenylretinamide for high-grade squamous intraepithelial lesions of the cervix. Clin Cancer Res 2001;7:3356-65.
99. Meyskens FL Jr, Surwit E, Moon TE. Enhancement of regression of cervical intraepithelial neoplasia II (moderate dysplasia) with topically applied all-trans-retinoic acid: a randomized trial. J Natl Cancer Inst 1994;86:539-43.
100. Keefe KA, Schell MJ, Brewer C, et al. A randomized, double blind, phase III trial using oral beta-carotene supplementation for women with high-grade cervical intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev 2001;10:1029-35.
101. Baak JP, Janssen EA, Soreide K, et al. Genomics and proteomics-the way forward. Ann Oncol 2005;16:30-44.