Neither one-time negative screening tests nor negative colposcopy provides absolute reassurance against cervical cancer
Corresponding Author
Philip E. Castle
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Fax: +301-402-0916.
Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd. Room 5030, EPS MSC 7234, Bethesda, MD 20892-7234, USASearch for more papers by this authorAna C. Rodríguez
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorRobert D. Burk
Departments of Pediatrics, Microbiology and Immunology, Obstetrics & Gynecology and Women's Health, and Epidemiology and Population Health, Albert Einstein College of Medicine, Yeshiva University, Bronx, NY
Search for more papers by this authorRolando Herrero
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorAllan Hildesheim
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorDiane Solomon
Division of Cancer Prevention, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorMark E. Sherman
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorJose Jeronimo
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Program for Appropriate Technology in Health, Seattle, WA
Search for more papers by this authorMario Alfaro
Laboratorio Nacional de Citología, Caja Costarricense de Seguro Social, San Jose, Costa Rica
Search for more papers by this authorJorge Morales
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorDiego Guillén
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorMartha L. Hutchinson
Department of Pathology and Laboratory Medicine, Women and Infants' Hospital of Rhode Island, Providence, RI
Search for more papers by this authorSholom Wacholder
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorMark Schiffman
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorCorresponding Author
Philip E. Castle
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Fax: +301-402-0916.
Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd. Room 5030, EPS MSC 7234, Bethesda, MD 20892-7234, USASearch for more papers by this authorAna C. Rodríguez
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorRobert D. Burk
Departments of Pediatrics, Microbiology and Immunology, Obstetrics & Gynecology and Women's Health, and Epidemiology and Population Health, Albert Einstein College of Medicine, Yeshiva University, Bronx, NY
Search for more papers by this authorRolando Herrero
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorAllan Hildesheim
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorDiane Solomon
Division of Cancer Prevention, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorMark E. Sherman
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorJose Jeronimo
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Program for Appropriate Technology in Health, Seattle, WA
Search for more papers by this authorMario Alfaro
Laboratorio Nacional de Citología, Caja Costarricense de Seguro Social, San Jose, Costa Rica
Search for more papers by this authorJorge Morales
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorDiego Guillén
Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica
Search for more papers by this authorMartha L. Hutchinson
Department of Pathology and Laboratory Medicine, Women and Infants' Hospital of Rhode Island, Providence, RI
Search for more papers by this authorSholom Wacholder
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorMark Schiffman
Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD
Search for more papers by this authorAbstract
A population sample of 10,049 women living in Guanacaste, Costa Rica, was recruited into a natural history of human papillomavirus (HPV) and cervical neoplasia study in 1993–1994. At the enrollment visit, we applied multiple state-of-the-art cervical cancer screening methods to detect prevalent cervical cancer and to prevent subsequent cervical cancers by the timely detection and treatment of precancerous lesions. Women were screened at enrollment with 3 kinds of cytology (often reviewed by more than one pathologist), visual inspection and cervicography. Any positive screening test led to colposcopic referral and biopsy and/or excisional treatment of CIN2 or worse. We retrospectively tested stored specimens with an early HPV test (hybrid capture tube test) and for >40 HPV genotypes using a research PCR assay. We followed women typically 5–7 years and some up to 11 years. Nonetheless, 16 cases of invasive cervical cancer were diagnosed during follow-up. Six cancer cases were failures at enrollment to detect abnormalities by cytology screening; 3 of the 6 were also negative at enrollment by sensitive HPV DNA testing. Seven cancers represent failures of colposcopy to diagnose cancer or a precancerous lesion in screen-positive women. Finally, 3 cases arose despite attempted excisional treatment of precancerous lesions. Based on this evidence, we suggest that no current secondary cervical cancer prevention technologies applied once in a previously under-screened population is likely to be 100% efficacious in preventing incident diagnoses of invasive cervical cancer. © 2009 UICC
Supporting Information
Additional Supporting Information may be found in the online version of this article.
Filename | Description |
---|---|
IJC_24525_sm_supptab1.doc125 KB | Supporting Table 1. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1 Kitchener HC,Castle PE,Cox JT. Chapter 7: achievements and limitations of cervical cytology screening. Vaccine 2006; 24 ( Suppl 3): S63–S70.
- 2 IARC. Cervix cancer screening, vol. 10. Lyon, France: IARC Press, 2005.
- 3 Cuzick J,Clavel C,Petry KU,Meijer CJ,Hoyer H,Ratnam S,Szarewski A,Birembaut P,Kulasingam S,Sasieni P,Iftner T. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 2006; 119: 1095–1101.
- 4 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): S78–89.
- 5 Schiffman M,Castle PE,Jeronimo J,Rodriguez AC,Wacholder S. Human papillomavirus and cervical cancer. Lancet 2007; 370: 890–907.
- 6 Castle PE,Wheeler CM,Solomon D,Schiffman M,Peyton CL. Interlaboratory reliability of hybrid capture 2. Am J Clin Pathol 2004; 122: 238–45.
- 7 Carozzi FM,Del Mistro A,Confortini M,Sani C,Puliti D,Trevisan R,De Marco L,Tos AG,Girlando S,Palma PD,Pellegrini A,Schiboni ML, et al. Reproducibility of HPV DNA testing by hybrid capture 2 in a screening setting. Am J Clin Pathol 2005; 124: 716–21.
- 8 Mayrand MH,Duarte-Franco E,Rodrigues I,Walter SD,Hanley J,Ferenczy A,Ratnam S,Coutlee F,Franco EL. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 2007; 357: 1579–88.
- 9 Naucler P,Ryd W,Tornberg S,Strand A,Wadell G,Elfgren K,Radberg T,Strander B,Forslund O,Hansson BG,Rylander E,Dillner J. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007; 357: 1589–97.
- 10 Bulkmans N,Berkhof J,Rozendaal L,van KF,Boeke A,Bulk S,Voorhorst F,Verheijen R,van GK,Boon M,Ruitinga W,van BM, et al. Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia grade 3 and cancer: 5-year follow-up of a randomised controlled implementation trial. Lancet 2007; 370: 1764–72.
- 11 Wright TC,Jr,Massad LS,Dunton CJ,Spitzer M,Wilkinson EJ,Solomon D. 2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests. Am J Obstet Gynecol 2007; 197: 346–55.
- 12 Wright TC,Jr,Schiffman M,Solomon D,Cox JT,Garcia F,Goldie S,Hatch K,Noller KL,Roach N,Runowicz C,Saslow D. Interim guidance for the use of human papillomavirus DNA testing as an adjunct to cervical cytology for screening. Obstet Gynecol 2004; 103: 304–9.
- 13 Sherman ME,Lorincz AT,Scott DR,Wacholder S,Castle PE,Glass AG,Mielzynska-Lohnas I,Rush BB,Schiffman M. Baseline cytology, human papillomavirus testing, and risk for cervical neoplasia: a 10-year cohort analysis. J Natl Cancer Inst 2003; 95: 46–52.
- 14 Kjaer S,Hogdall E,Frederiksen K,Munk C,van den BA,Svare E,Meijer C,Lorincz A,Iftner T. The absolute risk of cervical abnormalities in high-risk human papillomavirus-positive, cytologically normal women over a 10-year period. Cancer Res 2006; 66: 10630–6.
- 15 Gage JC,Hanson VW,Abbey K,Dippery S,Gardner S,Kubota J,Schiffman M,Solomon D,Jeronimo J. Number of cervical biopsies and sensitivity of colposcopy. Obstet Gynecol 2006; 108: 264–72.
- 16 Jeronimo J,Schiffman M. Colposcopy at a crossroads. Am J Obstet Gynecol 2006; 195: 349–53.
- 17 Pretorius RG,Zhang WH,Belinson JL,Huang MN,Wu LY,Zhang X,Qiao YL. Colposcopically directed biopsy, random cervical biopsy, and endocervical curettage in the diagnosis of cervical intraepithelial neoplasia II or worse. Am J Obstet Gynecol 2004; 191: 430–4.
- 18 Herrero R,Castle PE,Schiffman M,Bratti MC,Hildesheim A,Morales J,Alfaro M,Sherman ME,Wacholder S,Chen S,Rodriguez AC,Burk RD. Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis 2005; 191: 1796–807.
- 19 Schiffman M,Herrero R,Desalle R,Hildesheim A,Wacholder S,Cecilia RA,Bratti MC,Sherman ME,Morales J,Guillen D,Alfaro M,Hutchinson M, et al. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005; 337: 76–84.
- 20 Herrero R,Schiffman MH,Bratti C,Hildesheim A,Balmaceda I,Sherman ME,Greenberg M,Cardenas F,Gomez V,Helgesen K,Morales J,Hutchinson M, et al. Design and methods of a population-based natural history study of cervical neoplasia in a rural province of Costa Rica: the Guanacaste Project. Rev Panam Salud Publica 1997; 1: 362–75.
- 21 Bratti MC,Rodriguez AC,Schiffman M,Hildesheim A,Morales J,Alfaro M,Guillen D,Hutchinson M,Sherman ME,Eklund C,Schussler J,Buckland J, et al. Description of a seven-year prospective study of human papillomavirus infection and cervical neoplasia among 10 000 women in Guanacaste, Costa Rica [Descripcion de un estudio prospectivo de siete anos sobre la infeccion por el virus del papiloma humano y el cancer cervicouterino en 10 000 mujeres de Guanacaste, Costa Rica]. Rev Panam Salud Publica 2004; 15: 75–89.
- 22 Castle PE,Schiffman M,Gravitt PE,Kendall H,Fishman S,Dong H,Hildesheim A,Herrero R,Bratti MC,Sherman ME,Lorincz A,Schussler JE, et al. Comparisons of HPV DNA detection by MY09/11 PCR methods. J Med Virol 2002; 68: 417–23.
- 23 Qu W,Jiang G,Cruz Y,Chang CJ,Ho GY,Klein RS,Burk RD. PCR detection of human papillomavirus: comparison between MY09/MY11 and GP5+/GP6+ primer systems. J Clin Microbiol 1997; 35: 1304–10.
- 24 de Sanjose S,Diaz M,Castellsague X,Clifford G,Bruni L,Munoz N,Bosch FX. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis 2007; 7: 453–9.
- 25 Smith JS,Lindsay L,Hoots B,Keys J,Franceschi S,Winer R,Clifford GM. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 2007; 121: 621–32.
- 26 Schiffman M,Rodriguez AC. Heterogeneity in CIN3 diagnosis. Lancet Oncol 2008; 9: 404–6.
- 27 McCredie MR,Sharples KJ,Paul C,Baranyai J,Medley G,Jones RW,Skegg DC. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol 2008; 9: 425–34.
- 28 Herrero R,Hildesheim A,Bratti C,Sherman ME,Hutchinson M,Morales J,Balmaceda I,Greenberg MD,Alfaro M,Burk RD,Wacholder S,Plummer M, et al. Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst 2000; 92: 464–74.
- 29 Mosher WD,Chandra A,Jones J. Sexual behavior and selected health measures: men and women 15–44 years of age, United States, 2002. Adv Data 2005; 362: 1–55.
- 30 Smith HO,Padilla LA. Adenocarcinoma in situ of the cervix: sensitivity of detection by cervical smear: will cytologic screening for adenocarcinoma in situ reduce incidence rates for adenocarcinoma. Cancer 2002; 96: 319–22.
- 31 Bray F,Carstensen B,Moller H,Zappa M,Zakelj MP,Lawrence G,Hakama M,Weiderpass E. Incidence trends of adenocarcinoma of the cervix in 13 European countries. Cancer Epidemiol Biomarkers Prev 2005; 14: 2191–9.
- 32 Wang SS,Sherman ME,Hildesheim A,Lacey JV,Jr,Devesa S. Cervical adenocarcinoma and squamous cell carcinoma incidence trends among white women and black women in the United States for 1976–2000. Cancer 2004; 100: 1035–44.
- 33 Ferreccio C,Bratti MC,Sherman ME,Herrero R,Wacholder S,Hildesheim A,Burk RD,Hutchinson M,Alfaro M,Greenberg MD,Morales J,Rodriguez AC, et al. A comparison of single and combined visual, cytologic, and virologic tests as screening strategies in a region at high risk of cervical cancer. Cancer Epidemiol Biomarkers Prev 2003; 12: 815–23.
- 34 Arbyn M,Bergeron C,Klinkhamer P,Martin-Hirsch P,Siebers AG,Bulten J. Liquid compared with conventional cervical cytology: a systematic review and meta-analysis. Obstet Gynecol 2008; 111: 167–77.
- 35 Nanda K,McCrory DC,Myers ER,Bastian LA,Hasselblad V,Hickey JD,Matchar DB. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med 2000; 132: 810–19.
- 36 Castle PE,Hillier SL,Rabe LK,Hildesheim A,Herrero R,Bratti MC,Sherman ME,Burk RD,Rodriguez AC,Alfaro M,Hutchinson ML,Morales J, et al. An association of cervical inflammation with high-grade cervical neoplasia in women infected with oncogenic human papillomavirus (HPV). Cancer Epidemiol Biomarkers Prev 2001; 10: 1021–7.
- 37 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: 1401–5.
- 38 Pretorius RG,Kim RJ,Belinson JL,Elson P,Qiao YL. Inflation of sensitivity of cervical cancer screening tests secondary to correlated error in colposcopy. J Low Genit Tract Dis 2006; 10: 5–9.
- 39 Kreimer AR,Guido RS,Solomon D,Schiffman M,Wacholder S,Jeronimo J,Wheeler CM,Castle PE. Human papillomavirus testing following loop electrosurgical excision procedure identifies women at risk for posttreatment cervical intraepithelial neoplasia grade 2 or 3 disease. Cancer Epidemiol Biomarkers Prev 2006; 15: 908–14.
- 40 Mitchell MF,Tortolero-Luna G,Cook E,Whittaker L,Rhodes-Morris H,Silva E. A randomized clinical trial of cryotherapy, laser vaporization, and loop electrosurgical excision for treatment of squamous intraepithelial lesions of the cervix. Obstet Gynecol 1998; 92: 737–44.
- 41 Alvarez RD,Helm CW,Edwards RP,Naumann RW,Partridge EE,Shingleton HM,McGee JA,Hall JB,Higgins RV,Malone JM,Jr. Prospective randomized trial of LLETZ versus laser ablation in patients with cervical intraepithelial neoplasia. Gynecol Oncol 1994; 52: 175–9.
- 42 Arbyn M,Paraskevaidis E,Martin-Hirsch P,Prendiville W,Dillner J. Clinical utility of HPV-DNA detection: triage of minor cervical lesions, follow-up of women treated for high-grade CIN—an update of pooled evidence. Gynecol Oncol 2005; 99(3 Suppl ): S7–S11.
- 43 Andrae B,Kemetli L,Sparen P,Silfverdal L,Strander B,Ryd W,Dillner J,Tornberg S. Screening-preventable cervical cancer risks: evidence from a nationwide audit in Sweden. J Natl Cancer Inst 2008; 100: 622–9.
- 44 Cuzick J. Routine audit of large-scale cervical cancer screening programs. J Natl Cancer Inst 2008; 100: 605–6.
- 45 Slater DN,Milner PC,Radley H. Audit of deaths from cervical cancer: proposal for an essential component of the National Screening Programme. J Clin Pathol 1994; 47: 27–8.
- 46
Sung HY,Kearney KA,Miller M,Kinney W,Sawaya GF,Hiatt RA.
Papanicolaou smear history and diagnosis of invasive cervical carcinoma among members of a large prepaid health plan.
Cancer
2000;
88:
2283–9.
10.1002/(SICI)1097-0142(20000515)88:10<2283::AID-CNCR12>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
- 47 Leyden WA,Manos MM,Geiger AM,Weinmann S,Mouchawar J,Bischoff K,Yood MU,Gilbert J,Taplin SH. Cervical cancer in women with comprehensive health care access: attributable factors in the screening process. J Natl Cancer Inst 2005; 97: 675–83.
- 48 Nygard JF,Nygard M,Skare GB,Thoresen SO. Screening histories of women with CIN 2/3 compared with women diagnosed with invasive cervical cancer: a retrospective analysis of the Norwegian Coordinated Cervical Cancer Screening Program. Cancer Causes Control 2005; 16: 463–74.
- 49 Qiao YL,Sellors JW,Eder PS,Bao YP,Lim JM,Zhao FH,Weigl B,Zhang WH,Peck RB,Li L,Chen F,Pan QJ, et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol 2008; 9: 929–36.