Cancer Causes & Control

, Volume 29, Issue 1, pp 43–50 | Cite as

Uptake of HPV testing and extended cervical cancer screening intervals following cytology alone and Pap/HPV cotesting in women aged 30–65 years

  • Michelle I. Silver
  • Anne F. Rositch
  • Darcy F. Phelan-Emrick
  • Patti E. Gravitt
Original paper



To evaluate the adoption of HPV testing and recommended extended cervical cancer screening intervals in clinical practice, we described yearly uptake of Pap/HPV cotesting and estimated length of time between normal screens by patient characteristics.


We examined 55,575 Pap/HPV records from 27,035 women aged 30–65 years from the Johns Hopkins Hospital Pathology Data System between 2006 and 2013. Cotest uptake and median times to next screening test for cotests and cytology only were calculated. Adjusted hazard ratios were estimated using Cox proportional hazards models, with random effects adjustment for clustering within clinic.


Cotest usage increased from < 10% in 2006 to 78% in 2013. The median time to next screening test following normal cytology alone remained constant around 1.5 years. Screening intervals following a dual-negative cotest increased from 1.5 years in 2006/2007 to 2.5 years in 2010, coincident with increases in the proportion of women cotested. Intervals following a dual negative cotest were longer among Medicare patients (3 years) compared with privately insured women (2.5 years), and shorter among black (2 years) compared with white women (2.8 years).


By mid-2013 we observed broad adoption of Pap/HPV cotesting in routine screening in a large academic medical center. Increased screening intervals were observed only among cotested women, while those screened by cytology alone continued to be screened almost annually. The influence of different combinations of race and insurance on screening intervals should be further evaluated to ensure balance of screening risks and benefits in the U.S. population.


Cervical cancer screening Cytology HPV cotest Screening guidelines Screening interval Implementation Dissemination 



The authors wish to thank Amy Tatsas, John Boitnott and the Johns Hopkins Hospital Department of Pathology. They also thank Nicole A. Patterson for assistance with the graphics.


This work was supported by the Agency for Healthcare Research and Quality (R36 HS022199 to MIS), the National Cancer Institute (Specialized Program of Research Excellence in Cervical Cancer- 2P50-CA098252-11 to AFR and R01 CA123467 to PEG). This work was also supported by the Maryland Cigarette Restitution Fund Research Grant to the Johns Hopkins Medical Institutions (FY15 to AFR) and the Johns Hopkins Individualized Health Initiative (Hopkins inHealth to DFP).

Author contributions

Conceptualization: MS, PG; Methodology: MS, AR, DPE, PG; Software: MS; Validation: MS, PG; Formal Analysis: MS; Investigation: MS; Resources: MS, DPE, PG; Data Curation: MS; Writing-original draft: MS; Writing- review & editing: MS, AR, DPE, PG; Visualization: MS, PG; Supervision: PG; Project Administrator: MS; Funding Acquisition: MS, PG.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

10552_2017_976_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 28 KB)


  1. 1.
    Howlader NNA, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA: SEER Cancer Statistics Review, (1975–2011), National Cancer Institute. Bethesda, MD,, based on November 2013 SEER data submission, posted to the SEER web site, April 2014. 2014
  2. 2.
    CDC (2012) behavioral risk factor surveillane system survey data. In. Edited by Services DoHaH. Atlanta: Centers for Disease Control and PreventionGoogle Scholar
  3. 3.
    Phelan DF, Boitnott J, Clark DP, Dubay L, Gravitt P (2011) Trends of human papillomavirus testing in cervical cancer screening at a large academic cytology laboratory. Obstetrics Gynecol 118(2):289–295CrossRefGoogle Scholar
  4. 4.
    Tatsas AD, Phelan DF, Gravitt PE, Boitnott JK, Clark DP (2012) Practice patterns in cervical cancer screening and human papillomavirus testing. Am J Clin Pathol 138(2):223–229CrossRefPubMedGoogle Scholar
  5. 5.
    Bekker JB, John TS, Leiman G (2013) Confirming suboptimal adherence to hpv cotesting guidelines in an academic center in Vermont. Am J Clin Pathol 139(2):259–260CrossRefPubMedGoogle Scholar
  6. 6.
    Saslow D, Solomon D, Lawson HW, Killackey M, Kulasingam SL, Cain J, Garcia FAR, Moriarty AT, Waxman AG, Wilbur DC 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. Am J Clin Pathol 137(4):516–542CrossRefPubMedGoogle Scholar
  7. 7.
    Moyer VA (2012) Screening for Cervical Cancer: U.S. preventive services task force recommendation statement. Ann Intern Med 156(12):880–891CrossRefPubMedGoogle Scholar
  8. 8.
    ACOG: Practice Bulletin No. 131 (2012) Screening for cervical cancer. Obstetrics Gynecol 120(5):1222–1238Google Scholar
  9. 9.
    Proctor E, Brownson R (2012) Chap. 13: Measurement issues in dissemination and implementation research. Dissemination and implementation research in health: translating science to practice. edn. Edited by Brownson R, Colditz G, Proctor E. New YorkGoogle Scholar
  10. 10.
    Zhao C, Li Z, Nayar R, Levi AW, Winkler BA, Moriarty AT, Barkan GA, Rao J, Miller F, Fan F et al (2014) Prior high-risk human papillomavirus testing and papanicolaou test Results of 70 invasive cervical carcinomas Diagnosed in 2012: Results of a Retrospective Multicenter Study. Arch Pathol Lab Med 139:184–188Google Scholar
  11. 11.
    Weinmann S, Williams AE, Kamineni A, Buist DSM, Masterson EE, Stout NK, Stark A, Ross TR, Owens CL, Field TS et al (2015) Cervical cancer screening and follow-up in 4 geographically diverse US health care systems, 1998 through 2007. Cancer 121:2976–2983CrossRefGoogle Scholar
  12. 12.
    Cuzick J, Myers O, Hunt WC, Saslow D, Castle PE, Kinney W, Waxman A, Robertson M, Wheeler CM, on behalf of the New Mexico HPVPRSC, (2014) Human papillomavirus testing 2007–2012: co-testing and triage utilization and impact on subsequent clinical management. Int J Cancer 136:2854–2863Google Scholar
  13. 13.
    Hogarth S, Hopkins MM, Rodriguez V (2012) A molecular monopoly? HPV testing, the Pap smear and the molecularisation of cervical cancer screening in the USA. Sociol Health Illn 34(2):234–250CrossRefPubMedGoogle Scholar
  14. 14.
    Saslow D, Runowitz C, Solomon D, Moscicki A-B, Smith R, Eyre H, Cohen C (2002) American Cancer Society Guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin 52(6):342–362CrossRefPubMedGoogle Scholar
  15. 15.
    ACOG (2003) ACOG Practice Bulletin: clinical management guidelines for obstetrician-gynecologists. Number 45., August 2003. Cervical cytology screening (replaces committee opinion 152, March 1995). Obstet Gynecol 102(2):417–427Google Scholar
  16. 16.
    Wright TCJ, Schiffman M, Solomon D, Cox JT, Garcia F, Goldie S, Hatch K, Noller KL, Roach N, Runowicz C et al (2004) Interim guidance for the use of human papillomavirus DNA testing as an adjunct to Cervical cytology for screening. Obstetrics Gynecol 103(2):304–309. CrossRefGoogle Scholar
  17. 17.
    Smith-McCune K (2014) Choosing a screening method for cervical cancer: papanicolaou testing alone or with human papillomavirus testing. JAMA Internal Med 174:1027–1028CrossRefGoogle Scholar
  18. 18.
    Feldman S (2014) CAn the new cervical cancer screening and management guidelines be simplified? JAMA Internal Med 174(7):1029–1030CrossRefGoogle Scholar
  19. 19.
    Rogers E (2003) Diffusion of innovataions, 5th edn. The Free Press, New YorkGoogle Scholar
  20. 20.
    Gage JC, Schiffman M, Katki HA, Castle PE, Fetterman B, Wentzensen N, Poitras NE, Lorey T, Cheung LC, Kinney WK (2014) Reassurance Against future risk of precancer and cancer conferred by a negative human papillomavirus test. J Natl Cancer Inst 106(8)Google Scholar
  21. 21.
    Katki HA, Kinney WK, Fetterman B, Lorey T, Poitras NE, Cheung L, Demuth F, Schiffman M, Wacholder S, Castle PE (2011) Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice. Lancet Oncol 12(7):663–672CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Dillner J, Rebolj M, Birembaut P, Petry K-U, Szarewski A, Munk C, de Sanjose S, Naucler P, Lloveras B, Kjaer S et al (2008) Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: joint European cohort study. BMJ 337:a1754CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Damschroder L, Aron D, Keith R, Kirsh S, Alexander J, Lowery J (2009) Fostering implementation of health services research findings into practice: a consolidated framework for advancing implementation science. Implement Sci 4(1):50CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Sheppard CS, El-Zein M, Ramanakumar AV, Ferenczy A, Franco EL (2016) Assessment of mediators of racial disparities in cervical cancer survival in the United States. Int J Cancer 138(11):2622–2630CrossRefPubMedGoogle Scholar
  25. 25.
    Collins Y, Holcomb K, Chapman-Davis E, Khabele D, Farley JH (2014) Gynecologic cancer disparities: a report from the health disparities taskforce of the society of gynecologic oncology. Gynecol Oncol 133(2):353–361CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Beavis AL, Gravitt PE, Rositch AF (2017) Hysterectomy-corrected cervical cancer mortality rates reveal a larger racial disparity in the United States. Cancer 123:1044–1050CrossRefPubMedGoogle Scholar
  27. 27.
    Rositch AF, Nowak RG, Gravitt PE (2014) Increased age and race-specific incidence of cervical cancer after correction for hysterectomy prevalence in the United States from 2000 to 2009. Cancer 120(13):2032–2038CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cuzick J, Myers O, Hunt WC, Robertson M, Joste NE, Castle PE, Benard VB, Wheeler CM (2014) A Population-based evaluation of cervical screening in the United States: 2008–2011. Cancer Epidemiol Biomark Prevent 23(5):765–773CrossRefGoogle Scholar
  29. 29.
    Gage JC, Katki HA, Schiffman M, Fetterman B, Poitras NE, Lorey T, Cheung LC, Castle PE, Kinney WK (2015) Age-stratified 5-year risks of cervical precancer among women with enrollment and newly detected HPV infection. Int J Cancer 136(7):1665–1671CrossRefPubMedGoogle Scholar
  30. 30.
    Roland KB, Soman A, Benard VB, Saraiya M (2011) Human papillomavirus and Papanicolaou tests screening interval recommendations in the United States. Am J Obstet Gynecol 205(5):447. CrossRefPubMedGoogle Scholar
  31. 31.
    Saraiya M, Berkowitz Z, Yabroff KR, Wideroff L, Kobrin S, Benard V (2010) Cervical cancer screening with both human papillomavirus and papanicolaou testing vs papanicolaou testing alone: what screening intervals are physicians recommending? Arch Intern Med 170(11):977–986CrossRefPubMedGoogle Scholar
  32. 32.
    Yabroff KR, Saraiya M, Meissner HI, Haggstrom DA, Wideroff L, Yuan G, Berkowitz Z, Davis WW, Benard VB, Coughlin SS (2009) Specialty differences in primary care physician reports of papanicolaou test screening practices: a National Survey, 2006 to 2007. Ann Intern Med 151(9):602–611CrossRefPubMedGoogle Scholar
  33. 33.
    Cooper CP, Saraiya M, Mclean TA, Hannan J, Liesmann JM, Rose SW, Lawson HW (2005) Report from the CDC. Pap Test Intervals Used by Physicians Serving Low-Income Women through the National Breast and Cervical Cancer Early Detection Program. J Womens Health 14(8):670–678CrossRefGoogle Scholar
  34. 34.
    Berkowitz Z, Saraiya M, Benard V, Yabroff KR (2010) Common abnormal results of pap and human papillomavirus cotesting: what physicians are recommending for management. Obstetrics Gynecol 116(6):1332–1340. CrossRefGoogle Scholar
  35. 35.
    Meissner HI, Tiro JA, Yabroff KR, Haggstrom DA, Coughlin SS (2010) Too much of a good thing? Physician practices and patient willingness for less frequent pap test screening intervals. Med Care 48(3):249–259CrossRefPubMedGoogle Scholar
  36. 36.
    Lee JW-Y, Berkowitz Z, Saraiya M (2011) Low-Risk human papillomavirus testing and other nonrecommended human papillomavirus testing practices among U.S. Health Care Providers. Obstetrics Gynecol 118(1):4–13CrossRefGoogle Scholar
  37. 37.
    FDA approves first human papillomavirus test for primary cervical cancer screening []
  38. 38.
    Huh WK, Ault KA, Chelmow D, Davey DD, Goulart RA, Garcia FAR, Kinney WK, Massad LS, Mayeaux EJ, Saslow D et al (2015) Use of primary high-risk human papillomavirus testing for cervical cancer screening: interim clinical guidance. Obstetr Gynecol. Google Scholar
  39. 39.
    Chronological History of ACS Recommendations for the Early Detection of Cancer in People Without Cancer Symptoms []
  40. 40.
    ACOG (2002) ACOG practice bulletin. Diagnosis and treatment of cervical carcinomas. Number 35., May 2002. Int J Gynaecol Obstet 78(1):79–91CrossRefGoogle Scholar
  41. 41.
    Davey DD, Austin RM, Birdsong G, Buck HW, Cox JT, Darragh TM, Elgert PA, Hanson V, Henry MR, Waldman J (2002) ASCCP patient management guidelines: Pap Test specimen adequacy and quality indicators. Am J Clin Pathol 118(5):714–718CrossRefPubMedGoogle Scholar
  42. 42.
    USPSTF (1996) Guide to Clinical Preventive Services: Report of the U.S. Preventive Services Task Force. 2nd edn. WIlliams & WIlkins, BaltimoreGoogle Scholar
  43. 43.
    USPSTF: U.S. Preventive Services Task Force (2003) Recommendations and rationale-screening for cervical cancer: recommendations and rationale. Am Fam Phys 67(8):1759–1766Google Scholar
  44. 44.
    ACOG Practice Bulletin no. 109 (2009) Cervical cytology screening. Obstet Gynecol 114(6):1409–1420CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature (outside the USA) 2017

Authors and Affiliations

  1. 1.Department of EpidemiologyJohns Hopkins Bloomberg School of Public HealthBaltimoreUSA
  2. 2.Clinical Genetics Branch, Division of Cancer Epidemiology and GeneticsNational Cancer InstituteRockvilleUSA
  3. 3.Department Global HealthGeorge Washington UniversityWashingtonUSA

Personalised recommendations