Current Oncology Reports

, Volume 6, Issue 6, pp 497–506 | Cite as

Cervical cancer screening

  • Dorothy J. Wiley
  • Bradley J. Monk
  • Emmanuel Masongsong
  • Kristina Morgan


Although primary prevention of human papillomavirus (HPV) infections that are causally associated with invasive cervical cancer may be within our grasp, it is unlikely that these approaches will replace existing cervical cancer screening strategies for many years. Experts agree and data support periodic cytology screening for young-adult women using one of several technologies. Recent analyses of cost-effectiveness suggest that the addition of molecular HPV DNA testing for women aged over 30 years may allow the screening interval to be lengthened to 3 years for most women. Women at high risk for HPV infection and its associated cellular atypias warrant closer monitoring and follow-up. These patients would include organ transplant recipients, women exposed to diethylstilbestrol (DES), and HIV-infected women.


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References and Recommended Reading

  1. 1.
    American Cancer Society: Cancer Facts & Figures: 2003. Atlanta, GA: American Cancer Society; 2003.Google Scholar
  2. 2.
    Papanicolaou GN: Cytological evaluation of smears prepared by the tampon method for the detection of carcinoma of the uterine cervix. Cancer 1954, 7:1185–1190.PubMedCrossRefGoogle Scholar
  3. 3.
    Papanicolaou G: New cancer diagnosis. In Third Race Betterment Conference, 1928. Battle Creek, MI: Race Betterment Foundation; 1928:528–534.Google Scholar
  4. 4.
    US Census Bureau C: Census 2000 Summary File 1 (SF 1) 100-Percent Data: Sex by Age for Total Population. Washington, DC: US Department of Commerce, Economics and Statistics Administration; 2000.Google Scholar
  5. 5.
    US Department of Health and Human Services: Behavioral Risk Factor Surveillance System: Trend Data for No Pap Smear Within Three Years, Nationwide. Washington, DC: Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion; 2004.Google Scholar
  6. 6.
    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. Cost-effectiveness estimates were made for risk of cervical cancer associated with various screening strategies for women older than 30 years: no screening, conventional and liquid-based cytology, and molecular HPV testing at a variety of intervals. Triannual liquid-based Pap until age 30 followed by HPV DNA testing and liquid-based Pap thereafter would reduce ICC by 91.9% at a life-time cost of $1647, and conventional Pap until age 30 with addition of HPV testing (with cytology) would reduce ICC by 91.3% at a cost of $1453. Conventional Pap alone performed every 3 years should reduce ICC by 84.6% at a lifetime cost of $1196.PubMedGoogle Scholar
  7. 7.
    de Villiers EM: Human papillomavirus: introduction. Semin Cancer Biol 1999, 9:377.PubMedCrossRefGoogle Scholar
  8. 8.
    zur Hausen H: Papillomavirus infections: a major cause of human cancers. Biochimica et Biophysica Acta 1996, 1288:F55-F78.PubMedGoogle Scholar
  9. 9.
    zur Hausen H: Immortalization of human cells and their malignant conversion by high risk human papillomavirus genotypes. Semin Cancer Biol 1999, 9:405–411.PubMedCrossRefGoogle Scholar
  10. 10.
    Los Alamos National Laboratory, Bioscience Division, The Regents of the University of California: PV Types and Hosts. University of California under Contract No. W-7405-ENG-36 with the U.S. Department of Energy; 1997.Google Scholar
  11. 11.
    Koutsky L: Epidemiology of genital human papillomavirus infection. Am J Med 1997, 102:3–8.PubMedCrossRefGoogle Scholar
  12. 12.
    Walboomers JM, Jacobs MV, Manos MM, et al.: Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999, 189:12–19.PubMedCrossRefGoogle Scholar
  13. 13.
    Bosch FX, Manos MM, Munoz N, et al.: Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International Biological Study on Cervical Cancer (IBSCC) Study Group. J Natl Cancer Inst 1995, 87:796–802.PubMedCrossRefGoogle Scholar
  14. 14.
    Munoz N: Human papillomavirus and cancer: the epidemiological evidence. J Clin Virol 2000, 19:1–5. This report summarizes findings from the International Agency for Research on Cancer case-control studies, serial cross-sectional surveys, and cohort studies of the relationship between HPV and ICC. Pooled estimates suggest that women diagnosed with ICC are 70 times more likely to test positive for HPV DNA than are controls (95% CI, 57%-88%); however, the range of odds ratio estimates varies from 18 to 200 across studies collectively composed of approximately 2000 cases and approximately 2000 control subjects. HPV-16 (53%) and HPV-18 (15%) accounted for 68% of cases.PubMedCrossRefGoogle Scholar
  15. 15.
    Clifford GM, Smith JS, Plummer M, et al.: Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer 2003, 88:63–73. This meta-analysis of data gathered from 10,058 subjects in 85 studies worldwide showed that 79.3% to 88.1% of tumors were associated with HPVs, adjusting for the effect of histologic type, region, DNA specimen, and polymerase chain reaction primers. Cervical squamous cell carcinomas were more likely than adenocarcinomas to be associated with HPVs. HPV-16 was associated with 45% to 63% of cervical squamous cell carcinomas, whereas HPV-18 was associated with 10% to 14%. HPV-18 was more commonly isolated from adenocarcinomas (37.2%) than from squamous cell carcinomas (12.3%).PubMedCrossRefGoogle Scholar
  16. 16.
    Stone KM, Karem KL, Sternberg MR, et al.: Seroprevalence of human papillomavirus type 16 infection in the United States. J Infect Dis 2002, 186:1396–1402. This report presents serial cross-sectional survey data for 7218 males and females aged from 12 to 59 years. National Health and Nutrition Examination Survey respondents were analyzed in combination with simultaneously collected blood samples using HPV-16 enzyme-linked immunosorbent assay. Women more often than men tested positive for HPV-16 IgG (18% vs 8%); additionally, the odds of testing positive increased with the number of lifetime sex partners and generally increased with age for women. HPV-16 IgG positivity was associated with being sexually active more than 10 years, having ever had sex with a man, age, and race/ethnicity for men.PubMedCrossRefGoogle Scholar
  17. 17.
    Rios L, Cosary C, Hankey B, et al.: SEER Cancer Statistics Review 1973–1996. Bethesda, MD: National Cancer Institute; 1999.Google Scholar
  18. 18.
    Ylitalo N, Josefsson A, Melbye M, et al.: A prospective study showing long-term infection with human papillomavirus 16 before the development of cervical carcinoma in situ. Cancer Res 2000, 60:6027–6032.PubMedGoogle Scholar
  19. 19.
    Ylitalo N, Sorensen P, Josefsson 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, 355:2194–2198. HPV-16 viral load, using reverse-transcriptase polymerase chain reaction, for a subset of case and control specimens, was estimated for a population-based cohort of greater than 146,000 women. The estimated cumulative risk for ICC was 23% over 15 years for women with high viral load, compared with nearly 7% for women with “medium” viral load. Pair specimens showed that, for women who tested positive for HPV-16 at their first and last Pap test, viral load increased over the interval.PubMedCrossRefGoogle Scholar
  20. 20.
    Wallin KL, Wiklund F, Angstrom T, et al.: Type-specific persistence of human papillomavirus DNA before the development of invasive cervical cancer. N Engl J Med 1999, 341:1633–1638. Overall, women with ICC were 16 times more likely to test positive for HPV-16 using polymerase chain reaction than were controls and were nearly 23 times more likely to test positive less within 3 years of their diagnosis than were controls matched (to cases) by the date of specimen acquisition. Women who tested persistently positive, at the baseline and the index diagnostic specimen, were 213 times more likely to be diagnosed with ICC than were women who tested negative at both Pap test visits.PubMedCrossRefGoogle Scholar
  21. 21.
    Stenkvist B, Bergstrom R, Eklund G, Fox CH: Papanicolaou smear screening and cervical cancer. What can you expect? JAMA 1984, 252:1423–1426. This early population-based study showed 75% reduction of ICC in three Swedish counties where Pap test screening was implemented.PubMedCrossRefGoogle Scholar
  22. 22.
    Paintsil J, Muller M, Picken M, et al.: Carboxyl terminus of bovine papillomavirus type-1 L1 protein is not required for capsid formation. Virology 1996, 223:238–244.PubMedCrossRefGoogle Scholar
  23. 23.
    Koutsky LA, Ault KA, Wheeler CM, et al.: A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002, 347:1645–1651. This phase II, double-blind, randomized, placebo-controlled clinical trial of HPV-16 VLP vaccine showed no cases of infection among vaccine recipients, compared with 3.8 cases/100 person years for women who received placebo. Even where intent-to-treat analyses were modified to include women otherwise excluded from the primary analysis, women who received placebo were statistically more likely to become infected than were vaccine recipients. These preliminary data suggest that the vaccine prevented HPV-16 infections during a median followup time of approximately 17 months.PubMedCrossRefGoogle Scholar
  24. 24.
    Christensen ND, Kirnbauer R, Schiller JT, et al.: Human papillomavirus type-6 and type-11 have antigenically distinct strongly immunogenic conformationally dependent neutralizing epitopes. Virology 1994, 205:329–335.PubMedCrossRefGoogle Scholar
  25. 25.
    Strickler HD, Schiffman MH, Shah KV, et al.: A survey of human papillomavirus 16 antibodies in patients with epithelial cancers. Eur J Cancer Prev 1998, 7:305–313.PubMedCrossRefGoogle Scholar
  26. 26.
    Sun Y, Eluf-Neto J, Bosch FX, et al.: Serum antibodies to human papillomavirus 16 proteins in women from Brazil with invasive cervical carcinoma. Cancer Epidemiol Biomarkers Prev 1999, 8:935–940.PubMedGoogle Scholar
  27. 27.
    Combita AL, Bravo MM, Touze A, et al.: Serologic response to human oncogenic papillomavirus types 16, 18, 31, 33, 39, 58 and 59 virus-like particles in Colombian women with invasive cervical cancer. Int J Cancer 2002, 97:796–803.PubMedCrossRefGoogle Scholar
  28. 28.
    Goldstone SE, Palefsky JM, Winnett MT, Neefe JR: Activity of HspE7, a novel immunotherapy, in patients with anogenital warts. Dis Colon Rectum 2002, 45:502–507.PubMedCrossRefGoogle Scholar
  29. 29.
    Chu NR, Wu HB, Wu TC, et al.: Immunotherapy of a human papillomavirus type 16 E7-expressing tumor by administration of fusion protein comprised of Mycobacterium bovis BCG Hsp65 and HPV16 E7. Cell Stress Chaperones 2000, 5:401–405.PubMedCrossRefGoogle Scholar
  30. 30.
    Chu NR, Wu HB, Wu T, et al.: Immunotherapy of a human papillomavirus (HPV) type 16 E7-expressing tumour by administration of fusion protein comprising Mycobacterium bovis bacille Calmette-Guerin (BCG) hsp65 and HPV16 E7. Clin Exp Immunol 2000, 121:216–225.PubMedCrossRefGoogle Scholar
  31. 31.
    Hsu KF, Hung CF, Cheng WF, He L, Slater LA, Ling M, et al. Enhancement of suicidal DNA vaccine potency by linking Mycobacterium tuberculosis heat shock protein 70 to an antigen. Gene Ther 2001, 8:376–383.PubMedCrossRefGoogle Scholar
  32. 32.
    Jochmus I, Schafer K, Faath S, et al.: Chimeric virus-like particles of the human papillomavirus type 16 (HPV 16) as a prophylactic and therapeutic vaccine. Arch Med Res 1999, 30:269–274.PubMedCrossRefGoogle Scholar
  33. 33.
    Breitburd F, Kirnbauer R, Hubbert NL, et al.: Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J Virol 1995, 69:3959–3963.PubMedGoogle Scholar
  34. 34.
    Christensen ND, Hopfl R, DiAngelo SL, et al.: Assembled baculovirus-expressed human papillomavirus type 11 L1 capsid protein virus-like particles are recognized by neutralizing monoclonal antibodies and induce high titres of neutralizing antibodies. J Gen Virol 1994, 75:2271–2276.PubMedGoogle Scholar
  35. 35.
    Harro CD, Pang YY, Roden RB, et al.: Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 viruslike particle vaccine. J Natl Cancer Inst 2001, 93:284–292.PubMedCrossRefGoogle Scholar
  36. 36.
    Rose RC, White WI, Li M, et al.: Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. J Virol 1998, 72:6151–6154.PubMedGoogle Scholar
  37. 37.
    Pinto LA, Edwards J, Castle PE, et al.: Cellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 viruslike particles. J Infect Dis 2003, 188:327–338.PubMedCrossRefGoogle Scholar
  38. 38.
    Embers ME, Budgeon LR, Pickel M, Christensen ND: Protective immunity to rabbit oral and cutaneous papillomaviruses by immunization with short peptides of L2, the minor capsid protein. J Virol 2002, 76:9798–9805.PubMedCrossRefGoogle Scholar
  39. 39.
    ACOG Practice Bulletin: Clinical management guidelines for obstetrician-gynecologists. Number 45, August 2003. Cervical cytology screening (replaces committee opinion 152, March 1995). Obstet Gynecol 2003, 102:417–427.CrossRefGoogle Scholar
  40. 40.
    Fahey MT, Irwig L, Macaskill P: Meta-analysis of Pap test accuracy. Am J Epidemiol 1995, 141:680–689.PubMedGoogle Scholar
  41. 41.
    Walter SD, Irwig L, Glasziou PP: Meta-analysis of diagnostic tests with imperfect reference standards. J Clin Epidemiol 1999, 52:943–951.PubMedCrossRefGoogle Scholar
  42. 42.
    Goldie SJ, Freedberg KA, Weinstein MC, et al.: Cost effectiveness of human papillomavirus testing to augment cervical cancer screening in women infected with the human immunodeficiency virus. Am J Med 2001, 111:140–149.PubMedCrossRefGoogle Scholar
  43. 43.
    Goldie SJ, Kuhn L, Denny L, et al.: Policy analysis of cervical cancer screening strategies in low-resource settings: clinical benefits and cost-effectiveness. JAMA 2001, 285:3107–3115.PubMedCrossRefGoogle Scholar
  44. 44.
    Kim JJ, Wright TC, Goldie SJ: Cost-effectiveness of alternative triage strategies for atypical squamous cells of undetermined significance. JAMA 2002, 287:2382–2390.PubMedCrossRefGoogle Scholar
  45. 45.
    Wright TC, Goldie SJ, Cain JM, Howett MK: Screening for cervical cancer. Science 2000, 290:1651.PubMedCrossRefGoogle Scholar
  46. 46.
    Goldie SJ. Chapter 15: Public health policy and cost-effectiveness analysis. J Natl Cancer Inst Monogr 2003, 2003:102–110.Google Scholar
  47. 47.
    Wright TC Jr, 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.PubMedGoogle Scholar
  48. 48.
    de Boer CJ, van Dorst E, van Krieken H, et al.: Changing roles of cadherins and catenins during progression of squamous intraepithelial lesions in the uterine cervix. Am J Pathol 1999, 155:505–515.PubMedGoogle Scholar
  49. 49.
    Carico E, French D, Bucci B, et al.: Integrin beta 4 expression in the neoplastic progression of cervical epithelium. Gynecol Oncol 1993, 49:61–66.PubMedCrossRefGoogle Scholar
  50. 50.
    Vessey CJ, Wilding J, Folarin N, et al.: Altered expression and function of E-cadherin in cervical intraepithelial neoplasia and invasive squamous cell carcinoma. J Pathol 1995, 176:151–159.PubMedCrossRefGoogle Scholar
  51. 51.
    Felix JC, Lonky NM, Tamura K, et al.: Aberrant expression of Ecadherin in cervical intraepithelial neoplasia correlates with a false-negative Papanicolaou smear. Am J Obstet Gynecol 2002, 186:1308–1314.PubMedCrossRefGoogle Scholar
  52. 52.
    Felix JC: The science behind the effectiveness of in vivo screening. Am J Obstet Gynecol 2003, 188(Suppl):S8-S12.PubMedCrossRefGoogle Scholar
  53. 53.
    Christopherson WM, Scott MA: Trends in mortality from uterine cancer in relation to mass screening. Acta Cytolo 1977, 21:5–9.Google Scholar
  54. 54.
    Kim K, Rigal RD, Patrick JR, et al.: The changing trends of uterine cancer and cytology: a study of morbidity and mortality trends over a twenty year period. Cancer 1978, 42:2439–2449.PubMedCrossRefGoogle Scholar
  55. 55.
    National Center for Health Statistics, Centers for Disease Control and Prevention: US Mortality Public Use Data Tapes, volumes 1930–1959 and 1960–1996. Atlanta, GA: American Cancer Society; 1999.Google Scholar
  56. 56.
    Koutsky LA, Galloway DA, Holmes KK: Epidemiology of genital human papillomavirus infection. Epidemiol Rev 1988, 10:122–163.PubMedGoogle Scholar
  57. 57.
    Myers ER, McCrory DC, Nanda K, et al.: Mathematical model for the natural history of human papillomavirus infection and cervical carcinogenesis. Am J Epidemiol 2000, 151:1158–1171.PubMedGoogle Scholar
  58. 58.
    National Institutes of Health Consensus Development Conference statement on cervical cancer. April 1–3, 1996. Gynecol Oncol 1997, 66:351–361.Google Scholar
  59. 59.
    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.PubMedCrossRefGoogle Scholar
  60. 60.
    Screening for cervical cancer: recommendations and rationale. Am Fam Physician 2003, 67:1759–1766.Google Scholar
  61. 61.
    Ferenczy A, Robitaille J, Franco E, et al.: Conventional cervical cytologic smears vs. ThinPrep smears: a paired comparison study on cervical cytology. Acta Cytol 1996, 40:1136–1142.PubMedGoogle Scholar
  62. 62.
    Bur M, Knowles K, Pekow P, et al.: Comparison of ThinPrep preparations with conventional cervicovaginal smears: practical considerations. Acta Cytologica 1995, 39:631–642.PubMedGoogle Scholar
  63. 63.
    Hutchinson ML, Zahniser DJ, Sherman ME, et al.: Utility of liquid-based cytology for cervical carcinoma screening: results of a population-based study conducted in a region of Costa Rica with a high incidence of cervical carcinoma. Cancer 1999, 87:48–55.PubMedCrossRefGoogle Scholar
  64. 64.
    Papillo JL, Zarka MA, St John TL: Evaluation of the ThinPrep Pap test in clinical practice: a seven-month, 16,314-case experience in northern Vermont. Acta Cytol 1998, 42:203–208.PubMedGoogle Scholar
  65. 65.
    Sherman ME, Mendoza M, Lee KR, et al.: Performance of liquid-based, thin-layer cervical cytology: correlation with reference diagnoses and human papillomavirus testing. Mod Pathol 1998, 11:837–843.PubMedGoogle Scholar
  66. 66.
    Wang N, Emancipator SN, Rose P, et al.: Histologic follow-up of atypical endocervical cells: liquid-based, thin-layer preparation vs. conventional Pap smear. Acta Cytol 2002, 46:453–457.PubMedGoogle Scholar
  67. 67.
    Herrero R, Hildesheim A, Bratti C, et al.: Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst 2000, 92:464–474.PubMedCrossRefGoogle Scholar
  68. 68.
    Sellors JW, Karwalajtys TL, Kaczorowski JA, et al.: Prevalence of infection with carcinogenic human papillomavirus among older women. CMAJ 2002, 167:871–873.PubMedGoogle Scholar
  69. 69.
    Martin-Hirsch P, Jarvis G, Kitchener H, Lilford R: Collection devices for obtaining cervical cytology samples. Cochrane Database Syst Rev 2000 (3):CD001036.Google Scholar
  70. 70.
    Martin-Hirsch P, Lilford R, Jarvis G, Kitchener HC: Efficacy of cervical-smear collection devices: a systematic review and meta-analysis. Lancet 1999, 354:1763–1770.PubMedCrossRefGoogle Scholar
  71. 71.
    Celasun B: Presence of endocervical cells and number of slides in cervicovaginal smears: differences in performance between gynecologists. Acta Cytol 2001, 45:730–734.PubMedGoogle Scholar
  72. 72.
    Lewis D, Mitchell H: An evaluation of cervical screening in general practice. Med J Aust N Z 1994, 160:628–632.Google Scholar
  73. 73.
    Moscicki AB, Hills N, Shiboski S, et al.: Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA 2001, 285:2995–3002.PubMedCrossRefGoogle Scholar
  74. 74.
    Mount SL, Papillo JL: A study of 10,296 pediatric and adolescent Papanicolaou smear diagnoses in northern New England. Pediatrics 1999, 103:539–545.PubMedCrossRefGoogle Scholar
  75. 75.
    Deligdisch L, de Resende Miranda CR, Wu HS, Gil J: Human papillomavirus-related cervical lesions in adolescents: a histologic and morphometric study. Gynecol Oncol 2003, 89:52–59.PubMedCrossRefGoogle Scholar
  76. 76.
    Sellors JW, Karwalajtys TL, Kaczorowski J, et al.: Incidence, clearance and predictors of human papillomavirus infection in women. CMAJ 2003, 168:421–425.PubMedGoogle Scholar
  77. 77.
    Ho GY, Bierman R, Beardsley L, et al.: Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998, 338:423–428.PubMedCrossRefGoogle Scholar
  78. 78.
    Richardson H, Kelsall G, Tellier P, et al.: The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 2003, 12:485–490.PubMedGoogle Scholar
  79. 79.
    Screening for squamous cervical cancer: duration of low risk after negative results of cervical cytology and its implication for screening policies. IARC Working Group on evaluation of cervical cancer screening programmes. BMJ (Clin Res ed) 1986, 293:659–664.Google Scholar
  80. 80.
    Sawaya GF, Kerlikowske K, Lee NC, et al.: Frequency of cervical smear abnormalities within 3 years of normal cytology. Obstet Gynecol 2000, 96:219–223.PubMedCrossRefGoogle Scholar
  81. 81.
    Nguyen T, McPhee S, Lam T, Mock J: Predictors of cervical Pap smear screening awareness, intention, and receipt among Vietnamese-American women. Am J Prev Med 2002, 23:207–214.PubMedCrossRefGoogle Scholar
  82. 82.
    Cyrus-David MS, Michielutte R, Paskett ED, et al.: Cervical cancer risk as a predictor of Pap smear use in rural North Carolina. J Rural Health 2002, 18:67–76.PubMedCrossRefGoogle Scholar
  83. 83.
    Hiatt RA, Pasick RJ, Stewart S, et al.: Community-based cancer screening for underserved women: design and baseline findings from the Breast and Cervical Cancer Intervention Study. Prev Med 2001, 33:190–203.PubMedCrossRefGoogle Scholar
  84. 84.
    Hewitt M, Devesa SS, Breen N: Cervical cancer screening among U.S. women: analyses of the 2000 National Health Interview Survey. Prev Med 2004, 39:270–278.PubMedCrossRefGoogle Scholar
  85. 85.
    Sirovich BE, Welch HG: Cervical cancer screening among women without a cervix. JAMA 2004, 291:2990–2993.PubMedCrossRefGoogle Scholar
  86. 86.
    Janerich DT, Hadjimichael O, Schwartz PE, et al.: The screening histories of women with invasive cervical cancer, Connecticut. Am J Public Health 1995, 85:791–794.PubMedGoogle Scholar
  87. 87.
    Sherman ME, Lorincz AT, Scott DR, et al.: Baseline cytology, human papillomavirus testing, and risk for cervical neoplasia: a 10-year cohort analysis. J Natl Cancer Inst 2003, 95:46–52.PubMedCrossRefGoogle Scholar
  88. 88.
    Schiffman M, Herrero R, Hildesheim A, et al.: HPV DNA testing in cervical cancer screening: results from women in a highrisk province of Costa Rica. JAMA 2000, 283:87–93.PubMedCrossRefGoogle Scholar
  89. 89.
    Arbyn M, Buntinx F, Van Ranst M, et al.: Virologic versus cytologic triage of women with equivocal Pap smears: a metaanalysis of the accuracy to detect high-grade intraepithelial neoplasia. J Natl Cancer Inst 2004, 96:280–293.PubMedCrossRefGoogle Scholar
  90. 90.
    Nieminen P, Kallio M, Anttila A, Hakama M: Organised vs. spontaneous Pap-smear screening for cervical cancer: A casecontrol study. Int J Cancer 1999, 83:55–58.PubMedCrossRefGoogle Scholar
  91. 91.
    Parazzini F, Hildesheim A, Ferraroni M, et al.: Relative and attributable risk for cervical cancer: a comparative study in the United States and Italy. Int J Epidemiol 1990, 19:539–545.PubMedCrossRefGoogle Scholar
  92. 92.
    Jimenez PRM, Thomas DB: Has the use of pap smears reduced the risk of invasive cervical cancer in Guadalajara, Mexico? Int J Cancer 1999, 82:804–809.CrossRefGoogle Scholar
  93. 93.
    Herrero R, Brinton LA, Reeves WC, et al.: Screening for cervical cancer in Latin America: a case-control study. Int J Epidemiol 1992, 21:1050–1056.PubMedCrossRefGoogle Scholar
  94. 94.
    Trends in screening for colorectal cancer: United States, 1997 and 1999. MMWR Morb Mortal Wkly Rep 2001, 50:162–166.Google Scholar
  95. 95.
    Palmer JR, Anderson D, Helmrich SP, Herbst AL: Risk factors for diethylstilbestrol-associated clear cell adenocarcinoma. Obstet Gynecol 2000, 95:814–820.PubMedCrossRefGoogle Scholar
  96. 96.
    Barter JF, Austin JM Jr, Shingleton HM: Endometrial adenocarcinoma after in utero diethylstilbesterol exposure. Obstet Gynecol 1986, 67(Suppl):84S-85S.PubMedGoogle Scholar
  97. 97.
    Mangan CE, Guintoli RL, Sedlacek TV, et al.: Six years’ experience with screening of a diethylstilbestrol-exposed population. Am J Obstet Gynecol 1979, 134:860–865.PubMedGoogle Scholar
  98. 98.
    Welsch CW, Jenkins T, Amenomori Y, Meites J: Tumorous development of in situ and grafted anterior pituitaries in female rats treated with diethylstilbesterol. Experientia 1971, 27:1350–1352.PubMedCrossRefGoogle Scholar
  99. 99.
    Sherman AI, Goldrath M, Berlin A, et al.: Cervical-vaginal adenosis after in utero exposure to synthetic estrogens. Obstet Gynecol 1974, 44:531–545.PubMedGoogle Scholar
  100. 100.
    Branca M, Delfino A, Rossi E, et al.: Cervical intraepithelial neoplasia and human papillomavirus related lesions of the genital tract in HIV positive and negative women. Eur J Gynaecol Oncol 1995, 16:410–417.PubMedGoogle Scholar
  101. 101.
    Branca M, Garbuglia AR, Benedetto A, et al.: Factors predicting the persistence of genital human papillomavirus infections and PAP smear abnormality in HIV-positive and HIV-negative women during prospective follow-up. Int J STD AIDS 2003, 14:417–425.PubMedCrossRefGoogle Scholar
  102. 102.
    Ellerbrock TV, Chiasson MA, Bush TJ, et al.: Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA 2000, 283:1031–1037.PubMedCrossRefGoogle Scholar
  103. 103.
    Delmas MC, Larsen C, van Benthem B, et al.: Cervical squamous intraepithelial lesions in HIV-infected women: prevalence, incidence and regression. European Study Group on Natural History of HIV Infection in Women. AIDS 2000, 14:1775–1784.PubMedCrossRefGoogle Scholar
  104. 104.
    Frisch M, Biggar RJ, Goedert JJ: Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst 2000, 92:1500–1510.PubMedCrossRefGoogle Scholar
  105. 105.
    Palefsky JM: Cervical human papillomavirus infection and cervical intraepithelial neoplasia in women positive for human immunodeficiency virus in the era of highly active antiretroviral therapy. Curr Opin Oncol 2003, 15:382–388.PubMedCrossRefGoogle Scholar
  106. 106.
    Uberti-Foppa C, Origoni M, Maillard M, et al.: Evaluation of the detection of human papillomavirus genotypes in cervical specimens by hybrid capture as screening for precancerous lesions in HIV-positive women. J Med Virol 1998, 56:133–137.PubMedCrossRefGoogle Scholar
  107. 107.
    Zappa M, Visioli CB, Ciatto S, et al.: Lower protection of cytological screening for adenocarcinomas and shorter protection for younger women: the results of a case-control study in Florence. Br J Cancer 2004, 90:1784–1786.PubMedGoogle Scholar
  108. 108.
    Hemminki K, Li X, Vaittinen P: Time trends in the incidence of cervical and other genital squamous cell carcinomas and adenocarcinomas in Sweden, 1958–1996. Eur J Obstet Gynecol Reprod Biol 2002, 101:64–69.PubMedCrossRefGoogle Scholar
  109. 109.
    Schorge JO, Lea JS, Elias KJ, et al.: P16 as a molecular biomarker of cervical adenocarcinoma. Am J Obstet Gynecol 2004, 190:668–673.PubMedCrossRefGoogle Scholar
  110. 110.
    Dillner J, Lehtinen M, Bjorge T, et al.: Prospective seroepidemiologic study of human papillomavirus infection as a risk factor for invasive cervical cancer. J Natl Cancer Inst 1997, 89:1293–1299.PubMedCrossRefGoogle Scholar
  111. 111.
    Ronnett BM, Manos MM, Ransley JE, et al.: Atypical glandular cells of undetermined significance (AGUS): cytopathologic features, histopathologic results, and human papillomavirus DNA detection. Human Pathol 1999, 30:816–825.CrossRefGoogle Scholar

Copyright information

© Current Science Inc 2004

Authors and Affiliations

  • Dorothy J. Wiley
    • 1
  • Bradley J. Monk
    • 1
  • Emmanuel Masongsong
    • 1
  • Kristina Morgan
    • 1
  1. 1.Division of Primary CareSchool of Nursing, University of California at Los Angeles (UCLA)Los AngelesUSA

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