Comparison of Patient- and Clinician-Collected Anal Cytology Samples to Screen for Human Papillomavirus–Associated Anal Intraepithelial Neoplasia in Men Who Have Sex with Men

  1. Peter V. Chin-Hong, MD;
  2. J. Michael Berry, MD;
  3. Su-Chun Cheng, DSc, MS;
  4. Joseph A. Catania, PhD;
  5. Maria Da Costa, MS;
  6. Teresa M. Darragh, MD;
  7. Fred Fishman, BS;
  8. Naomi Jay, NP, PhD;
  9. Lance M. Pollack, PhD; and
  10. Joel M. Palefsky, MD
  1. From the University of California, San Francisco, San Francisco, California, and Oregon State University, Corvallis, Oregon.

    Abstract

    Background: Human papillomavirus (HPV)–associated anal cancer is increasing in prevalence and is more common among men who have sex with men and HIV-positive individuals than cervical cancer is among women in the United States. Cytology screening can detect the anal cancer precursor, anal intraepithelial neoplasia (AIN). Little is known about self-collected samples for AIN screening, and few community-based AIN estimates exist.

    Objective: To compare the sensitivity of self-collected versus clinician-collected anal cytology specimens to detect biopsy-confirmed AIN and the prevalence estimate of AIN in a community sample.

    Design: Cross-sectional study. Participants were mailed anal cytology self-collection kits with instructions. Clinicians repeated anal cytology and performed high-resolution anoscopy with biopsies as the diagnostic reference standard.

    Setting: San Francisco, California.

    Patients: Community-based sample of men who have sex with men.

    Measurements: Prevalence of anal HPV and AIN. Sensitivity and specificity of self-collected and clinician-collected anal cytology specimens to diagnose AIN were calculated.

    Results: Biopsy-proven AIN was diagnosed in 57% of HIV-positive and 35% of HIV-negative participants (P = 0.04), and 80% provided adequate self-collected specimens for interpretation. The sensitivity of cytology to detect AIN in HIV-positive men was 75% (95% CI, 51% to 93%) when self-collected and 90% (CI, 68% to 99%) when clinician-collected; respective values in HIV-negative men were 48% (CI, 26% to 70%) and 62% (CI, 38% to 82%). The specificity of cytology to detect AIN in HIV-positive men was 50% (CI, 22% to 78%) when self-collected and 64% (CI, 36% to 86%) when clinician-collected; respective values in HIV-negative men were 86% (CI, 71% to 94%) and 85% (CI, 72% to 93%).

    Limitations: The study sample was from a narrowly defined geographical area. Participants self-reported HIV status.

    Conclusion: In a community-based sample, a high proportion of HIV-positive and HIV-negative men who have sex with men have AIN. The sensitivity of cytology to detect AIN is higher for clinician-collected versus self-collected specimens and for HIV-positive versus HIV-negative men. The specificity of cytology to detect AIN is higher in HIV-negative versus HIV-positive men. However, the probability of AIN in a patient with a negative cytology result may not be low enough (23% for HIV-negative men and 45% for HIV-positive men with a patient-collected specimen) for clinicians to be comfortable recommending no anoscopy for those with a negative cytology result if done as a one-time test. These data raise the question of whether the optimal population screening strategy is cytology screening with anoscopy only for those who test positive or whether anoscopy should be recommended for everyone in these risk groups. Given limited resources and the limited number of clinicians trained in anoscopy, cytology screening may be the best current approach to identifying disease in the at-risk population.

    Article and Author Information

    • Acknowledgment: The authors thank Dave Huebner for assistance with the anal cytology screening instructions and visual aids and Christopher Ambridge, Stacey Acton, and Jeff Henne of The Henne Group, San Francisco, for their committed outreach. They also thank all the study participants for their generosity.

    • Grant Support: By an American Cancer Society Institutional Research Award (Dr. Chin-Hong); grants K23 AI054157 (Dr. Chin-Hong), R01 CA54053 (Dr. Palefsky), R01 CA/AI 88739 (Dr. Palefsky), and R01 MH54320 (Dr. Catania) from the National Institutes of Health; the California Universitywide AIDS Research Program (ID04-SF-008, Dr. Catania); the General Clinical Research Center, with funds provided by the Division of Research Resources (5 M01-RR-00079, Dr. Palefsky); and CYTYC Corporation.

    • Potential Financial Conflicts of Interest:Grants pending: J.A. Catania (National Institutes of Health). Other: T.M. Darragh (CYTYC).

    • Reproducible Research Statement:Study protocol and statistical code: Available from Dr. Chin-Hong (phong{at}php.ucsf.edu). Data set: Not available.

    • Requests for Single Reprints: Peter V. Chin-Hong, MD, University of California, San Francisco, Box 0654, 513 Parnassus Avenue, Room S-380, San Francisco, CA 94143-0654; e-mail, phong{at}php.ucsf.edu.

    • Current Author Addresses: Dr. Chin-Hong: University of California, San Francisco, Box 0654, 513 Parnassus Avenue, Room S-380, San Francisco, CA 94143-0654.

    • Drs. Berry and Jay: University of California, San Francisco, 1600 Divisadero Street, San Francisco, CA 94115.

    • Dr. Cheng: University of California, San Francisco, 185 Berry Street, Suite 5700, San Francisco, CA 94107.

    • Dr. Catania: Oregon State University, 705 Northwest Elizabeth Drive, Corvallis, OR 97330.

    • Ms. Da Costa: University of California, San Francisco, 521 Parnassus Avenue, San Francisco, CA 94143.

    • Dr. Darragh: University of California, San Francisco, Department of Pathology, 1600 Divisadero Street, #B221, San Francisco, CA 94115.

    • Mr. Fishman: University of California, San Francisco, Mount Zion Medical Center, 1600 Divisadero Street, Box 1699, San Francisco, CA 94143.

    • Dr. Pollack: University of California, San Francisco, 50 Beale Street, Suite 1300, San Francisco, CA 94105.

    • Author Contributions: Conception and design: P.V. Chin-Hong, J.A. Catania, J.M. Palefsky.

    • Analysis and interpretation of the data: P.V. Chin-Hong, S.C. Cheng, M. Da Costa, T.M. Darragh, J.M. Palefsky.

    • Drafting of the article: P.V. Chin-Hong, J.M. Palefsky.

    • Critical revision of the article for important intellectual content: P.V. Chin-Hong, J.A. Catania, T.M. Darragh, L.M. Pollack, J.M. Palefsky.

    • Final approval of the article: P.V. Chin-Hong, J.M. Berry, J.A. Catania, N. Jay, L.M. Pollack, J.M. Palefsky.

    • Provision of study materials or patients: P.V. Chin-Hong, J.A. Catania, L.M. Pollack.

    • Statistical expertise: P.V. Chin-Hong, S.C. Cheng.

    • Obtaining of funding: P.V. Chin-Hong.

    • Administrative, technical, or logistic support: P.V. Chin-Hong, J.A. Catania, F. Fishman, L.M. Pollack.

    • Collection and assembly of data: P.V. Chin-Hong, J.M. Berry, F. Fishman, N. Jay, L.M. Pollack, J.M. Palefsky.

    Responses to this article

    • IN RESPONSE
      • Peter V Chin-Hong and
      • Nancy A. Hessol, Joel M. Palefsky
      Ann Intern Med published online October 26, 2009
    • Anal Cancer Screening: Taking a Step Back
      • Jeffrey D. Klausner and
      • Kenneth A. Katz, Christina A. Clarke, Kyle T. Bernstein, Mitchell H. Katz
      Ann Intern Med published online October 26, 2009

    Summary for Patients

    • Summaries for Patients:Comparison of Patient- and Physician-Collected Specimens to Screen for Anal Cancer Ann Intern Med September 2, 2008 149:I-38
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