Abstract
Purpose
The USA has a well-established network of central cancer registries (CCRs) that collect data using standardized definitions and protocols to provide population-based estimates of cancer incidence. The addition of cervical cancer precursors in select CCR operations would facilitate future studies measuring the population-level impact of human papillomavirus (HPV) vaccine. To assess the feasibility of collecting data on cervical cancer precursors, we conducted a multi-site surveillance study in three state-wide CCRs, to obtain annual case counts and compare rates of precursor lesions to those for invasive cervical cancer.
Methods
We developed standardized methods for case identification, data collection and transmission, training and quality assurance, while allowing for registry-specific strategies to accomplish surveillance objectives. We then conducted population-based surveillance for precancerous cervical lesions in three states using the protocols.
Results
We identified 5,718 cases of cervical cancer precursors during 2009. Age-adjusted incidence of cervical cancer precursors was 77 (Kentucky), 60 (Michigan), and 54 (Louisiana) per 100,000 women. Highest rates were observed in those aged 20–29 years: 274 (Kentucky), 202 (Michigan), and 196 (Louisiana) per 100,000. The variable with the most missing data was race/ethnicity, which was missing for 13 % of cases in Kentucky, 18 % in Michigan, and 1 % in Louisiana. Overall rates of cervical cancer precursors were over sixfold higher than invasive cervical cancer rates [rate ratios: 8.6 (Kentucky), 8.3 (Michigan), and 6.2 (Louisiana)].
Conclusions
Incorporating surveillance of cervical cancer precursors using existing CCR infrastructure is feasible and results in collection of population-based incidence data. Standardized collection of these data in high-quality registry systems will be useful in future activities monitoring the impact of HPV vaccination across states. As a result of this study, ongoing surveillance of these lesions has now been conducted in four CCRs since 2010.
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References
Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger ER (2007) Quadrivalent human papillomavirus vaccine. Recommendations of the Advisory Committee on Immunization Practices (ACIP). Morb Mortal Wkly Rep 56(RR-02):1–24
Centers for Disease Control and Prevention (2010) FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP). Morb Mortal Wkly Rep 59:626–629
Brotherton JML, Kaldor JM, Garland SM (2010) Monitoring the control of human papillomavirus (HPV) infection and related diseases in Australia: towards a national HPV surveillance strategy. Sex Health 7:310–319
Fairley CK, Donovan B (2010) What can surveillance of genital warts tell us? Sex Health 7:325–327
Markowitz LE, Hariri S, Unger ER, Saraiya M, Datta SD, Dunne EF (2010) Post-licensure monitoring of HPV vaccine in the United States. Vaccine 28:4731–4737
Schuchat A, Bell BP (2008) Monitoring the impact of vaccines postlicensure: new challenges, new opportunities. Expert Rev Vaccines 7:437–456
Wong CA, Saraiya M, Hariri S et al (2011) Approaches to monitoring biological outcomes for HPV vaccination: challenges of early adopter countries. Vaccine 29:878–885
Egelkrout EM, Galloway DA (2008) The biology of genital human papillomaviruses. In: Holmes KK, Sparling PF, Stamm WE et al (eds) Sexually transmitted diseases, 4th edn. McGraw Hill Medical, New York City, pp 463–487
Winer RL, Kiviat NB, Hughes JP et al (2005) Development and duration of human papillomavirus lesions, after initial infection. J Infect Dis 191:731–738
Moscicki AB, Hills N, Shiboski S et al (2001) Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA 395:2995–3002
Woodman CBJ, Collins S, Winter H et al (2001) Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 357:1831–1836
Baseman JG, Koutsky LA (2005) The epidemiology of human papillomavirus infections. J Clin Virol 32S:S16–S24
National Program of Cancer Registries (NPCR), Centers for Disease Control and Prevention. http://www.cdc.gov/cancer/npcr/about.htm. Accessed 02/04/2013
National Cancer Institute. Surveillance, Epidemiology and End Results (SEER) Program. http://www.seer.cancer.gov/. Accessed 02/04/2013
[North] American Association of Central Cancer Registries (1993) Working group on pre-invasive cervical neoplasia and population-based cancer registries: final subcommittee report. [N]AACCR conference held 5–6 Apr 1993, Rockville, MD. Subsequently adopted by the [N]AACCR Executive Board May 1993 and amended November 1993
Copeland G, Datta SD, Spivak G, Garvin AG, Cote ML (2008) Total burden and incidence of in situ and invasive cervical carcinoma in Michigan, 1985–2003. Cancer 113(10 suppl):2946–2954
National Cancer Institute. Surveillance, Epidemiology and End Results Program. International classification of diseases for oncology, 3rd edn, Coding materials. http://seer.cancer.gov/icd-o-3/. Accessed 02/11/2013
National Center for Health Statistics, Centers for Disease Control and Prevention. International classification of disease, 9th revision, Clinical modification. http://www.cdc.gov/nchs/icd/icd9cm.htm. Accessed 05/10/2012
International Health Terminology Standards Development Organisation. Systematized nomenclature of medicine clinical terms. http://www.ihtsdo.org/snomed-ct/. Accessed 02/11/2013, 2:43 PM EST
National Institutes of Health. US National Library of Medicine. Systematized nomenclature of medicine reference terminology. http://www.nlm.nih.gov/research/umls/Snomed/snomed_faq.html. Accessed 02/04/2013, 2:20 PM EST
Artificial Intelligence in Medicine (AIM) E-Path software. http://www.aim.ca/cancer-surveillance/. Accessed 02/25/2014
National Cancer Institute. Surveillance, Epidemiology and End Results Program data management system. SEER*DMS user manual and tutorials. Chapter 22: Managing follow-back. http://seer.cancer.gov/seerdms/manual/chap22.followback.pdf. Accessed 02/14/2013
North American Association of Central Cancer Registries. Standards for cancer registries, vol II, 13th edn. http://www.naaccr.org/LinkClick.aspx?fileticket=xSH32ZzIzGI%3d&tabid=268&mid=746. Accessed 02/01/2013
Centers for Disease Control and Prevention. National Program of Cancer Registries. GenEdits Plus version 1.2.5. http://www.cdc.gov/cancer/npcr/tools/edits/versionanddownload.htm. Accessed 02/01/2013
Centers for Disease Control and Prevention. National Center for Health Statistics. Bridged-race intercensal estimates of the resident population of the United States for July 1, 2000–July 1, 2009, by year, county, single-year of age (0, 1, 2, …, 85 years and over), bridged race, Hispanic origin, and sex. Prepared under a collaborative arrangement with the US Census Bureau. http://www.cdc.gov/nchs/nvss/bridged_race.htm as of December 20, 2010, following release by the US Census Bureau of the revised unbridged intercensal estimates by 5-year age group on July 23, 2010
North American Association of Central Cancer Registries. NAACCR Guideline for enhancing Hispanic-Latino identification: revised NAACCR Hispanic/Latino identification algorithm [NHIA v2.2.1]. Revised 12 Sept 2011. http://www.naaccr.org/LinkClick.aspx?fileticket=6E20OT41TcA%3d&tabid=118&mid=458. Accessed 02/11/2013
National Cancer Institute. Surveillance, Epidemiology and End Results (SEER) Program. Standard populations (millions) for age-adjustment. http://www.seer.cancer.gov/stdpopulations/. Accessed 01/15/2014
Centers for Disease Control and Prevention. National Program of Cancer Registries. United States Cancer statistics data: all data combined 1999–2009. http://www.cdc.gov/cancer/npcr/uscs/download_data.htm. Accessed 03/18/2013
Koss LG (1990) The new Bethesda system for reporting results of smears of the uterine cervix. J Natl Cancer Inst 82:988–991
Solomon D, Davey D, Kurman R et al (2002) The 2001 Bethesda system. Terminology for reporting results of cervical cytology. JAMA 287:2114–2119
Darragh TM, Colgan TJ, Cox J et al (2012) The lower anogenital squamous terminology standardization project for HPV-associated lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. J Low Genit Tract Dis 16:205–242
Harmon ML, Cooper K (2009) Cervical neoplasia. In: Nucci MR, Oliva E (eds) Gynecologic pathology. Churchill Livingstone Elsevier, Philadelphia
McCredie MRE, Sharples KJ, Paul C, Baranyai J, Medley G, Jones RW, Skegg DCG (2008) Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol 9:425–434
Stoler MH, Schiffman M (2001) Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL triage study. JAMA 185:1500–1510
Dalla Palma P, Giorgi Rossi P, Collina G et al (2009) The reproducibility of CIN diagnoses among different pathologists. Data from histology reviews from a multicenter randomized study. Am J Clin Pathol 132:125–132
Solomon D, Castle PE (2005) Findings from ALTS: impact on cervical cytology screening, triage, and patient management. Pathol Case Rev 10:128–137
Snijders PJF, Steenbergen RDM, Heideman DAM, Meijer CJLM (2006) HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 208:152–164
CAP/ASCCP lower anogenital squamous terminology for HPV-associated lesions. Summary of consensus recommendations. http://www.cap.org/aps/docs/membership/transformation/new/asccp-sum_last_recom.pdf. Accessed 03/15/2013
Saraiya M, Goodman MT, Datta SD, Chen VW, Wingo PA (2008) Cancer registries and monitoring the impact of prophylactic human papillomavirus vaccines: the potential role. Cancer 113(10 suppl):3047–3057
Saslow D, Solomon D, Lawson HW et al (2012) American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin 62:147–172
American Congress of Obstetricians and Gynecologists. New cervical cancer screening recommendations from the US Preventive Services Task Force and the American Cancer Society/American Society for Colposcopy and Cervical Pathology/American Society for Clinical Pathology. Released 14 March 2012. http://www.acog.org/About_ACOG/Announcements/New_Cervcal_Cancer_Screening_Recommendations. Accessed 03/18/2013
US Preventive Services Task Force. Screening for cervical cancer. Current recommendation. Released March 2012. http://www.uspreventiveservicestaskforce.org/uspstf/uspscerv.htm. Accessed 03/18/2013
Centers for Disease Control and Prevention. Office of Surveillance, Epidemiology, and Laboratory Services. Behavioral risk factor surveillance system, 2008 and 2010. http://www.cdc.gov/brfss/technical_infodata/surveydata.htm. Accessed 02/01/2013
Centers for Disease Control and Prevention. Office of Surveillance, Epidemiology, and Laboratory Services. Behavioral risk factor surveillance system. Prevalence and trends data women’s health—2010. Women aged 18+ who have had a pap test within the past three years. http://apps.nccd.cdc.gov/BRFSS/list.asp?cat=WH&yr=2010&qkey=4426&state=All. Accessed 03/20/2013
Tangka F, Subramanian S, Beebe MC, Trebina D, Michaud F (2010) Economic assessment of central cancer registry operations, part III: results from 5 programs. Journal of Registry Management 37:152–155
Yuan YC (2000) Multiple imputation for missing data: concepts and new development. Paper P267-25. Presented at 25th SAS Users Group International. 9–12 Apr 2000. http://www2.sas.com/proceedigns/sugi25/25/st/25p267.pdf. Accessed 03/18/2013
Hariri S, Unger ER, Powell SE et al (2012) The HPV vaccine impact monitoring project (HPV-IMPACT): assessing early evidence of vaccination impact on HPV-associated cervical cancer precursor lesions. Cancer Causes Control 23:281–288
Wheeler CM, Hunt WC, Cuzick J, Langsfeld E, Pearse A, Montoya GD et al (2013) A population-based study of human papillomavirus genotype prevalence in the United States: baseline measures prior to mass human papillomavirus vaccination. Int J Cancer 132:198–207
About the SEER Program. Research activities. http://seer.cancer.gov/about/. Accessed 02/15/2013
National Cancer Institute. Surveillance, Epidemiology and End Results Program data management system. SEER*DMS user manual and tutorials. Chapter 28: Special studies. http://seer.cancer.gov/seerdms/manual/chap28.special.studies.pdf. Accessed 02/15/2013
Potter R, Copeland G, Datta SD, Saraiya M, Flagg EW (2012) Monitoring the impact of human papillomavirus (HPV) vaccines on precancerous cervical lesions by linking immunization information system and cancer registry data in Michigan. Abstract 30354. Presented at the 1st national immunization conference online. 26–28 March 2012. https://cdc.confex.com/cdc/nic2012/webprogram/Paper30354.html. Accessed 03/18/2013
Gargano JW, Wilkinson EJ, Unger ER, Steinau M, Watson M, Huang Y et al (2012) Prevalence of human papillomavirus types in invasive vulvar cancers and vulvar intraepithelial neoplasia 3 in the United State before vaccine introduction. J Low Genit Tract Dis 16(4):471–479
Steinau M, Unger ER, Hernandez BY, Goodman MT, Copeland G, Hopenhayn C et al (2013) Human papillomavirus prevalence in invasive anal cancers in the United States before vaccine introduction. J Low Genit Tract Dis 17(4). doi:10.1097/LGT.0b013e31827ed372
Acknowledgments
Funding for this work was provided by the Centers for Disease Control and Prevention (Contract No. 200-2008-27956).
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The authors declare that they have no conflict of interest.
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Flagg, E.W., Datta, S.D., Saraiya, M. et al. Population-based surveillance for cervical cancer precursors in three central cancer registries, United States 2009. Cancer Causes Control 25, 571–581 (2014). https://doi.org/10.1007/s10552-014-0362-x
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DOI: https://doi.org/10.1007/s10552-014-0362-x