American Journal of Obstetrics & Gynecology
Volume 197, Issue 4 , Pages 346-355 , October 2007

2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests

  • Thomas C. Wright Jr, MD

      Affiliations

    • Department of Pathology, College of Physicians and Surgeons of Columbia University, New York, NY
    • Corresponding Author InformationReprints: Thomas C. Wright Jr, MD, Department of Pathology, College of Physicians and Surgeons of Columbia University, Room 16-404, P&S Building, 630 West 168th St, New York, NY 10032
  • ,
  • L. Stewart Massad, MD

      Affiliations

    • Department of Obstetrics and Gynecology, Washington University School of Medicine, St Louis, MO
  • ,
  • Charles J. Dunton, MD

      Affiliations

    • Department of Obstetrics and Gynecology, Lankenau Hospital, Wynnewood, PA
  • ,
  • Mark Spitzer, MD

      Affiliations

    • Department of Obstetrics and Gynecology, Brookdale University Hospital and Medical Center, Brooklyn, NY
  • ,
  • Edward J. Wilkinson, MD

      Affiliations

    • Department of Pathology, University of Florida College of Medicine, Gainesville, FL
  • ,
  • Diane Solomon, MD

      Affiliations

    • National Institutes of Health and National Cancer Institute, Bethesda, MD.
  • ,
  • 2006 American Society for Colposcopy and Cervical Pathology–sponsored Consensus Conference

Received 6 April 2007 ,Revised 28 June 2007 ,Accepted 29 July 2007.

References 

  1. ASCUS-LSIL Triage Study (ALTS) Group. Results of a randomized trial on the management of cytology interpretations of atypical squamous cells of undetermined significance. Am J Obstet Gynecol. 2003;188:1383–1392
  2. ASCUS-LSIL Triage Study (ALTS) Group. A randomized trial on the management of low-grade squamous intraepithelial lesion cytology interpretations. Am J Obstet Gynecol. 2003;188:1393–1400
  3. Wright TC, Schiffman M, Solomon D, et al. Interim guidance for the use of human papillomavirus DNA testing as an adjunct to cervical cytology for screening. Obstet Gynecol. 2004;103:304–309
  4. Wright TC, Cox JT, Massad LS, Twiggs LB, Wilkinson EJ. 2001 consensus guidelines for the management of women with cervical cytological abnormalities. JAMA. 2002;287:2120–2129
  5. Wright TC, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ, Solomon D. 2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests. J Low Genit Tract Dis. 2007;in press.
  6. Solomon D, Davey D, Kurman R, et al. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA. 2002;287:2114–2119
  7. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F. Carcinogenicity of human papillomaviruses. Lancet Oncol. 2005;6:204
  8. Wright TC, Schiffman M. Adding a test for human papillomavirus DNA to cervical-cancer screening. N Engl J Med. 2003;348:489–490
  9. In: SEER Cancer Statistics Review 1975-2003. Vol 2006:Bethesda, MD: National Institutes of Health; 2006;
  10. Insinga RP, Glass AG, Rush BB. Diagnoses and outcomes in cervical cancer screening: a population-based study. Am J Obstet Gynecol. 2004;191:105–113
  11. Moscicki AB, Schiffman M, Kjaer S, Villa LL. Updating the natural history of HPV and anogenital cancer (Chapter 5). Vaccine. 2006;24(Suppl 3):S42–S51
  12. Burchell AN, Winer RL, de Sanjose S, Franco EL. Epidemiology and transmission dynamics of genital HPV infection (Chapter 6). Vaccine. 2006;24(Suppl 3):S52–S61
  13. Stoler MH, Schiffman M. Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study. JAMA. 2001;285:1500–1505
  14. Confortini M, Carozzi F, Dalla Palma P, et al. Interlaboratory reproducibility of atypical squamous cells of undetermined significance report: a national survey. Cytopathology. 2003;14:263–268
  15. Gatscha RM, Abadi M, Babore S, Chhieng D, Miller MJ, Saigo PE. Smears diagnosed as ASCUS: interobserver variation and follow-up. Diagn Cytopathol. 2001;25:138–140
  16. Jones BA, Novis DA. Follow-up of abnormal gynecologic cytology: a college of American pathologists Q-probes study of 16132 cases from 306 laboratories. Arch Pathol Lab Med. 2000;124:665–671
  17. Manos MM, Kinney WK, Hurley LB, et al. Identifying women with cervical neoplasia: using human papillomavirus DNA testing for equivocal Papanicolaou results. JAMA. 1999;281:1605–1610
  18. Lonky NM, Felix JC, Naidu YM, Wolde-Tsadik G. Triage of atypical squamous cells of undetermined significance with hybrid capture II: colposcopy and histologic human papillomavirus correlation. Obstet Gynecol. 2003;101:481–489
  19. Bergeron C, Jeannel D, Poveda J, Cassonnet P, Orth G. Human papillomavirus testing in women with mild cytologic atypia. Obstet Gynecol. 2000;95:821–827
  20. Pretorius RG, Peterson P, Novak S, Azizi F, Sadeghi M, Lorincz AT. Comparison of two signal-amplification DNA tests for high-risk HPV as an aid to colposcopy. J Reprod Med. 2002;47:290–296
  21. Guyot A, Karim S, Kyi MS, Fox J. Evaluation of adjunctive HPV testing by Hybrid Capture II in women with minor cytological abnormalities for the diagnosis of CIN2/3 and cost comparison with colposcopy. BMC Infect Dis. 2003;3:23
  22. Dalla Palma P, Pojer A, Girlando S. HPV triage of women with atypical squamous cells of undetermined significance: a 3-year experience in an Italian organized programme. Cytopathology. 2005;16:22–26
  23. Cox JT, Schiffman M, Solomon D. Prospective follow-up suggests similar risk of subsequent cervical intraepithelial neoplasia grade 2 or 3 among women with cervical intraepithelial neoplasia grade 1 or negative colposcopy and directed biopsy. Am J Obstet Gynecol. 2003;188:1406–1412
  24. Guido R, Solomon D, Schiffman M, Burke L. Comparison of management strategies for women diagnosed as CIN 1 or less, postcolposcopic evaluation: data from the ASCUS and LSIL Triage Study (ALTS), a Multicenter randomized trial. J Low Genit Tract Dis. 2002;6:176
  25. Arbyn M, Buntinx F, Van Ranst M, Paraskevaidis E, Martin-Hirsch P, Dillner J. Virologic versus cytologic triage of women with equivocal Pap smears: a meta-analysis of the accuracy to detect high-grade intraepithelial neoplasia. J Natl Cancer Inst. 2004;96:280–293
  26. Kulasingam SL, Kim JJ, Lawrence WF, et al. Cost-effectiveness analysis based on the atypical squamous cells of undetermined significance/low-grade squamous intraepithelial lesion Triage Study (ALTS). J Natl Cancer Inst. 2006;98:92–100
  27. Kim JJ, Wright TC, Goldie SJ. Cost-effectiveness of alternative triage strategies for atypical squamous cells of undetermined significance. JAMA. 2002;287:2382–2390
  28. Guido R, Schiffman M, Solomon D, Burke L. Postcolposcopy management strategies for women referred with low-grade squamous intraepithelial lesions or human papillomavirus DNA-positive atypical squamous cells of undetermined significance: a two-year prospective study. Am J Obstet Gynecol. 2003;188:1401–1405
  29. Sherman ME, Solomon D, Schiffman M. Qualification of ASCUS (A comparison of equivocal LSIL and equivocal HSIL cervical cytology in the ASCUS LSIL Triage Study). Am J Clin Pathol. 2001;116:386–394
  30. Boardman LA, Stanko C, Weitzen S, Sung CJ. Atypical squamous cells of undetermined significance: human papillomavirus testing in adolescents. Obstet Gynecol. 2005;105:741–746
  31. Eltoum IA, Chhieng DC, Roberson J, McMillon D, Partridge EE. Reflex human papilloma virus infection testing detects the same proportion of cervical intraepithelial neoplasia grade 2-3 in young versus elderly women. Cancer. 2005;105:194–198
  32. Sawaya GF, Kerlikowske K, Lee NC, Gildengorin G, Washington AE. Frequency of cervical smear abnormalities within 3 years of normal cytology. Obstet Gynecol. 2000;96:219–223
  33. Sherman ME, Schiffman M, Cox JT, Group TA. Effects of age and HPV load on colposcopic triage: data from the ASCUS LSIL Triage Study (ALTS). J Natl Cancer Inst. 2002;94:102–107
  34. Bruner KS, Davey DD. ASC-US and HPV testing in women aged 40 years and over. Diagn Cytopathol. 2004;31:358–361
  35. Duerr A, Paramsothy P, Jamieson DJ, et al. Effect of HIV infection on atypical squamous cells of undetermined significance. Clin Infect Dis. 2006;42:855–861
  36. Massad LS, Ahdieh L, Benning L, et al. Evolution of cervical abnormalities among women with HIV-1: evidence from surveillance cytology in the women’s interagency HIV study. J Acquir Immune Defic Syndr. 2001;27:432–442
  37. Massad LS, Schneider MF, Watts DH, et al. HPV testing for triage of HIV-infected women with Papanicolaou smears read as atypical squamous cells of uncertain significance. J Womens Health (Larchmt). 2004;13:147–153
  38. Kirby TO, Allen ME, Alvarez RD, Hoesley CJ, Huh WK. High-risk human papillomavirus and cervical intraepithelial neoplasia at time of atypical squamous cells of undetermined significance cytologic results in a population with human immunodeficiency virus. J Low Genit Tract Dis. 2004;8:298–303
  39. Dunn TS, Bajaj JE, Stamm CA, Beaty B. Management of the minimally abnormal Papanicolaou smear in pregnancy. J Low Genit Tract Dis. 2001;5:133–137
  40. Davey DD, Neal MH, Wilbur DC, Colgan TJ, Styer PE, Mody DR. Bethesda 2001 implementation and reporting rates: 2003 practices of participants in the College of American Pathologists Interlaboratory Comparison Program in Cervicovaginal Cytology. Arch Pathol Lab Med. 2004;128:1224–1229
  41. Arbyn M, Sasieni P, Meijer CJ, Clavel C, Koliopoulos G, Dillner J. Chapter 9: clinical applications of HPV testing: a summary of meta-analyses. Vaccine. 2006;24(Suppl 3):S78–S89
  42. Alvarez RD, Wright TC. Effective cervical neoplasia detection with a novel optical detection system: a randomized trial. Gynecol Oncol. 2007;104:281–289
  43. Chute DJ, Covell J, Pambuccian SE, Stelow EB. Cytologic-histologic correlation of screening and diagnostic Papanicolaou tests. Diagn Cytopathol. 2006;34:503–506
  44. Moscicki AB, Shiboski S, Hills NK, et al. Regression of low-grade squamous intra-epithelial lesions in young women. Lancet. 2004;364:1678–1683
  45. Evans MF, Adamson CS, Papillo JL, St John TL, Leiman G, Cooper K. Distribution of human papillomavirus types in ThinPrep Papanicolaou tests classified according to the Bethesda 2001 terminology and correlations with patient age and biopsy outcomes. Cancer. 2006;106:1054–1064
  46. Massad LS, Collins YC, Meyer PM. Biopsy correlates of abnormal cervical cytology classified using the Bethesda system. Gynecol Oncol. 2001;82:516–522
  47. Dunn TS, Burke M, Shwayder J. A ”see and treat” management for high-grade squamous intraepithelial lesion pap smears. J Low Genit Tract Dis. 2003;7:104–106
  48. Jones BA, Davey DD. Quality management in gynecologic cytology using interlaboratory comparison. Arch Pathol Lab Med. 2000;124:672–681
  49. Ko V, Tambouret RH, Kuebler DL, Black-Schaffer WS, Wilbur DC. Human papillomavirus testing using hybrid capture II with surepath collection: initial evaluation and longitudinal data provide clinical validation for this method. Cancer. 2006;108:468–474
  50. Holschneider CH, Ghosh K, Montz FJ. See-and-treat in the management of high-grade squamous intraepithelial lesions of the cervix: a resource utilization analysis. Obstet Gynecol. 1999;94:377–385
  51. Numnum TM, Kirby TO, Leath CA, Huh WK, Alvarez RD, Straughn JM. A prospective evaluation of ”see and treat” in women with HSIL Pap smear results: is this an appropriate strategy?. J Low Genit Tract Dis. 2005;9:2–6
  52. Melnikow J, Nuovo J, Willan AR, Chan BK, Howell LP. Natural history of cervical squamous intraepithelial lesions: a meta-analysis. Obstet Gynecol. 1998;92:727–735
  53. Peto J, Gilham C, Deacon J, et al. Cervical HPV infection and neoplasia in a large population-based prospective study: the Manchester cohort. Br J Cancer. 2004;91:942–953
  54. Sharpless KE, Schnatz PF, Mandavilli S, Greene JF, Sorosky JI. Dysplasia associated with atypical glandular cells on cervical cytology. Obstet Gynecol. 2005;105:494–500
  55. DeSimone CP, Day ME, Tovar MM, Dietrich CS, Eastham ML, Modesitt SC. Rate of pathology from atypical glandular cell Pap tests classified by the Bethesda 2001 nomenclature. Obstet Gynecol. 2006;107:1285–1291
  56. Tam KF, Cheung AN, Liu KL, et al. A retrospective review on atypical glandular cells of undetermined significance (AGUS) using the Bethesda 2001 classification. Gynecol Oncol. 2003;91:603–607
  57. Derchain SF, Rabelo-Santos SH, Sarian LO, et al. Human papillomavirus DNA detection and histological findings in women referred for atypical glandular cells or adenocarcinoma in situ in their Pap smears. Gynecol Oncol. 2004;95:618–623
  58. Diaz-Montes TP, Farinola MA, Zahurak ML, Bristow RE, Rosenthal DL. Clinical utility of atypical glandular cells (AGC) classification: cytohistologic comparison and relationship to HPV results. Gynecol Oncol. 2006;104:366–371
  59. Krane JF, Lee KR, Sun D, Yuan L, Crum CP. Atypical glandular cells of undetermined significance (Outcome predictions based on human papillomavirus testing). Am J Clin Pathol. 2004;121:87–92
  60. Fetterman B, Shaber R, Pawlick G, Kinney W. Human papillomavirus DNA testing in routine clinical practice for prediction of underlying cervical intraepithelial neoplasia 2,3+ at initial evaluation and in follow-up of women with atypical glandular cell Papanicolaou tests. J Low Genit Tract Dis. 2006;3:179
  61. Greenspan DL, Cardillo M, Davey DD, Heller DS, Moriarty AT. Endometrial cells in cervical cytology: review of cytological features and clinical assessment. J Low Genit Tract Dis. 2006;10:111–122
  62. Simsir A, Carter W, Elgert P, Cangiarella J. Reporting endometrial cells in women 40 years and older: assessing the clinical usefulness of Bethesda 2001. Am J Clin Pathol. 2005;123:571–575
  63. In: Cervix cancer screening IARC handbooks of cancer. Vol 10:Lyons (France): IARC; 2005;
  64. Wright TC. HPV DNA testing for cervical cancer screening. Int J Gynaecol Obstet. 2006;95(Suppl 1):S239–S246
  65. Dunne EF, Unger ER, Sternberg M, et al. Prevalence of HPV infection among females in the United States. JAMA. 2007;297:813–819
  66. Saslow D, Runowicz CD, Solomon D, et al. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin. 2002;52:342–362
  67. Cuzick J, Mayrand MH, Ronco G, Snijders P, Wardle J. New dimensions in cervical cancer screening (Chapter 10). Vaccine. 2006;24(Suppl 3):S90–S97
  68. Koliopoulos G, Arbyn M, Martin-Hirsch P, Kyrgiou M, Prendiville W, Paraskevaidis E. Diagnostic accuracy of human papillomavirus testing in primary cervical screening: a systematic review and meta-analysis of non-randomized studies. Gynecol Oncol. 2007;104:232–246
  69. Cuzick J, Clavel C, Petry KU, et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer. 2006;119:1095–1101
  70. ACOG practice bulletin. Clinical Management Guidelines for Obstetrician-Gynecologists. Number 61, April 2005. Human papillomavirus. Obstet Gynecol. 2005;105:905–918
  71. Hybrid Capture 2 FDA approval letter. Available at: http://www.fda.gov/cdrh/pdf/p890064s009a.pdf. Accessed January 27, 2007.
  72. Kjaer S, Hogdall E, Frederiksen K, et al. The absolute risk of cervical abnormalities in high-risk human papillomavirus-positive, cytologically normal women over a 10-year period. Cancer Res. 2006;66:10630–10636
  73. Khan MJ, Castle PE, Lorincz AT, et al. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J Natl Cancer Inst. 2005;97:1072–1079
  74. Goldie SJ, Kim JJ, Wright TC. Cost-effectiveness of human papillomavirus DNA testing for cervical cancer screening in women aged 30 years or more. Obstet Gynecol. 2004;103:619–631
  75. Ronco G, Segnan N, Giorgi-Rossi P, et al. Human papillomavirus testing and liquid-based cytology: results at recruitment from the new technologies for cervical cancer randomized controlled trial. J Natl Cancer Inst. 2006;98:765–774
  76. Bigras G, de Marval F. The probability for a Pap test to be abnormal is directly proportional to HPV viral load: results from a Swiss study comparing HPV testing and liquid-based cytology to detect cervical cancer precursors in 13,842 women. Br J Cancer. 2005;93:575–581
  77. Cuzick J, Szarewski A, Cubie H, et al. Management of women who test positive for high-risk types of human papillomavirus: the HART study. Lancet. 2003;362:1871–1876
  78. Clavel C, Masure M, Bory JP, et al. Human papillomavirus testing in primary screening for the detection of high-grade cervical lesions: as study of 7932 women. Br J Cancer. 2001;89:1616–1623
  79. Schlecht NF, Kulaga S, Robitaille J, et al. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA. 2001;286:3106–3114
  80. Gross PA, Barrett TL, Dellinger EP, et al. Purpose of quality standards for infectious diseases (Infectious Diseases Society of America). Clin Infect Dis. 1994;18:421
  81. Kish MA. Guide to development of practice guidelines. Clin Infect Dis. 2001;32:8511

PII: S0002-9378(07)00930-1

doi: 10.1016/j.ajog.2007.07.047

American Journal of Obstetrics & Gynecology
Volume 197, Issue 4 , Pages 346-355 , October 2007