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Human Papillomavirus Infection and Cervical Cytology in Women Screened for Cervical Cancer in the United States, 2003–2005

S. Deblina Datta, MD; Laura A. Koutsky, PhD; Sylvie Ratelle, MD; Elizabeth R. Unger, MD, PhD; Judith Shlay, MD, MSPH; Tracie McClain, MD; Beth Weaver, MD; Peter Kerndt, MD; Jonathan Zenilman, MD; Michael Hagensee, MD, PhD; Cristen J. Suhr, MPH, CHES; and Hillard Weinstock, MD, MPH
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From the Centers for Disease Control and Prevention, Atlanta, Georgia; University of Washington, Seattle, Washington; Massachusetts Department of Public Health, Boston, Massachusetts; Denver Public Health, Denver, Colorado; County of Los Angeles Department of Health Services, Los Angeles, California; Johns Hopkins University School of Medicine, Baltimore, Maryland; and Louisiana State University Health Sciences Center, New Orleans, Louisiana.

Acknowledgment: The authors thank Donna Felsenstein, Julie M. Freedman, Karen Gacicia, Rick Intres, Cindy Miller, Sheila Hart Nelson, Asuncion “Susie” Rivera, Laura Smock, Silvia Vernaza, Akhila Balasubramanian, Tara McPartland, Jim Braxton, Alicia Edwards, Rob Nelson, Ashley Sardella, David Swan, Ruth Ann Tucker, Akbar Zaidi, Mona Saraiya, Mark Foster, Xinyue Hou, Rebecca Rothbard, Julie Subiadur, Bita Amani, Kim Burtle, Sara R. Germann, Peter He, Evelyn Kim, Maxine Liggins, Lizzeth Romero, Nandini Sodhi, Angela H. Shin, Nicole D. Vick, Susan Walker, Sharon Webb, Evette Youssef, and the HSS project staff for their contributions toward the preparation of the manuscript. The authors dedicate this work to the memory of Dr. Sylvie Ratelle, whose scientific acumen, leadership, dedication to the field of STD prevention, and kind spirit were vital to the HSS project.

Potential Financial Conflicts of Interest:Consultancies: B. Weaver (Merck), M. Hagensee (Merck). Honoraria: B. Weaver (Merck). Grants received: L.A. Koutsky (Merck).

Reproducible Research Statement:Study protocol: Available on request from Dr. Datta (e-mail, ddatta@cdc.gov). Statistical code: Contact Dr. Datta (e-mail ddatta@cdc.gov) regarding availability. Data set: Contact Dr. Datta (e-mail, ddatta@cdc.gov) regarding availability.

Requests for Single Reprints: S. Deblina Datta, MD, Centers for Disease Control and Prevention, 1600 Clifton Road, MS E-02, Atlanta, GA 30333; e-mail, ddatta@cdc.gov.

Current Author Addresses: Drs. Datta, Unger, and Weinstock and Ms. Suhr: Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333.

Drs. Koutsky and Weaver: University of Washington, 1914 North 34th Street, Suite 300, Seattle, WA 98103.

Dr. Shlay: Denver Public Health, 605 Bannock Street, Denver, CO 80204.

Drs. McClain, Kerndt, and Zenilman: County of Los Angeles Department of Health Services, STD Program, 2615 South Grand Avenue, Room 500, Los Angeles, CA 90007.

Dr. Hagensee: Louisiana State University Health Sciences Center, 190 Perdido Street, New Orleans, LA 70112.

Author Contributions: Conception and design: S.D. Datta, L.A. Koutsky, E.R. Unger, J. Shlay, T. McClain, B. Weaver, P. Kerndt, J. Zenilman, M. Hagensee, H. Weinstock.

Analysis and interpretation of the data: S.D. Datta, L.A. Koutsky, E.R. Unger, J. Shlay, T. McClain, P. Kerndt, J. Zenilman, C.J. Suhr.

Drafting of the article: S.D. Datta, L.A. Koutsky, E.R. Unger.

Critical revision of the article for important intellectual content: S.D. Datta, L.A. Koutsky, E.R. Unger, J. Shlay, T. McClain, B. Weaver, P. Kerndt, J. Zenilman, M. Hagensee, H. Weinstock.

Final approval of the article: S.D. Datta, L.A. Koutsky, E.R. Unger, J. Shlay, T. McClain, B. Weaver, P. Kerndt, J. Zenilman, H. Weinstock.

Provision of study materials or patients: S.D. Datta, L.A. Koutsky, J. Shlay, T. McClain, B. Weaver, J. Zanilman, M. Hagensee.

Statistical expertise: S.D. Datta, L.A. Koutsky.

Obtaining of funding: L.A. Koutsky, J. Shlay, B. Weaver, P. Kerndt, H. Weinstock.

Administrative, technical, or logistic support: L.A. Koutsky, E.R. Unger, T. McClain, B. Weaver, P. Kerndt, C.J. Suhr.

Collection and assembly of data: J. Zenilman.

Ann Intern Med. 2008;148(7):493-500. doi:10.7326/0003-4819-148-7-200804010-00004
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Our findings document the substantial number of high-risk HPV infections that Hybrid Capture 2 testing would detect among women presenting for cervical screening at STD, family planning, and primary care clinics in the United States. The overall prevalence of 23% shown by Hybrid Capture 2 testing and the large number of infections across demographic groups, clinic types, and cities is indicative of the high prevalence of high-risk HPV (although most infections will not result in cervical disease, particularly among adolescents [1011]). Of age, race, ethnicity, clinic type, and city categories, high-risk HPV prevalence differed most by age (range, 6% to 35%). The observed distribution of steadily decreasing high-risk HPV prevalence across increasing age groups is consistent with that observed in other studies in the United States and other developed countries with cervical screening programs (12). In contrast, other countries exhibited U-shaped prevalence curves or flat curves (that is, high HPV prevalence with no decrease in older groups). Observed variations are most likely due to differences in the availability of cervical screening programs, in incidence of HPV infections, and in sexual behaviors. In contrast to known epidemiologic associations between race and other sexually transmitted infections (1315), the age-adjusted prevalence of high-risk HPV infection did not vary substantially by race (range, 20% to 24%, excluding the prevalence of 32% observed among multiracial women) or ethnicity (range, 20% to 24%) but did vary more by clinic type (range, 17% to 26%, adjusted for age and city). The range in prevalence across cities was 19% to 28% (adjusted for age and clinic type). Analyses are planned to further evaluate these observed differences.

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Submit a Comment/Letter
Screening Tests for Cervical Cancer
Posted on April 25, 2008
Masaharu Tsubokura
Teikyo university chiba medical center
Conflict of Interest: None Declared

Datta et al. reported that high-risk HPV was widespread among women receiving cervical screening. (1) Surprisingly, the present study showed that the prevalence of cytology results with low-grade squamous intraepithelial lesion (LSIL), high-grade squamous intraepithelial lesion (HSIL) or adenocarcinoma in situ (AIS) was significantly higher among women younger than 30 years compared with those age 30 years or older (P<0.001), while the median age at diagnosis for cervical cancer was 48 years of age in the United States. (2) Although over 50 percent of women with HSIL have cervical intraepithelial neoplasia 2 or greater and 2 percent of women with HSIL have invasive carcinoma, LSIL is associated with a transient HPV infection in adolescents and both the infection and LSIL usually resolve over time. (3) A study involving 187 adolescents aged 13 to 22 years with LSIL showed that 61 percent of the lesions had regressed within one year and 91 percent regressed within three years. (4) Since the risk of CIN 2,3 in women with LSIL is different from that in women with HSIL, management of LSIL is different from that of HSIL. Clinicians will have difficulties in drawing a definite conclusion from this study because the number of women with LSIL, HSIL and AIS was not shown separately. We are grateful if the authors provide us the information on the number of enrollees and the prevalence of high-risk HPV among women with LSIL, HSIL and AIS separately.

1. Datta et al. Human Papillomavirus Infection and Cervical Cytology in Women Screened for Cervical Cancer in the United States, 2003-2005 Annals of internal medicine 2008;148:493.

2.http://seer.cancer.gov/csr/1975_2005/results_single/sect_01_table.11_2p gs.pdf

3. Wright et al. Cervical dysplasia in adolescents. Obstet Gynecol 2005;106:115.

4. Moscicki et al. Regression of low-grade squamous intra-epithelial lesions in young women Lancet 2004;364:1678

Conflict of Interest:

None declared

In Response
Posted on June 9, 2008
S. Deblina Datta
Centers for Disease Control and Prevention
Conflict of Interest: None Declared

Authors Reply:

The prevalence of HPV DNA in LSIL and HSIL is known to be very high, and therefore, management decisions are based on the presence of the cytologic abnormality alone. The management of LSIL (referral for colposcopy) and the management of HSIL (loop electrosurgical excision procedure, or LEEP) are similar in that procedural evaluations are needed (with the exception of special populations) and HPV DNA testing would not influence management. The management of ASC-US, however, is dependent upon the results of HPV DNA testing. [1] The ALTS trial demonstrated the utility of HPV DNA testing as a triage strategy in the management of ASC- US for all women (but not for LSIL), and the ASCCP recommended this strategy in their 2001 guidelines. [2,3] The 2006 ASCCP guidelines have been amended to exclude adolescent ASC-US cases (age <_21 years="years" from="from" hpv="hpv" dna="dna" triage="triage" due="due" to="to" the="the" high="high" prevalence="prevalence" of="of" infections="infections" and="and" low="low" risk="risk" cancer="cancer" in="in" this="this" age="age" group.="group." therefore="therefore" our="our" original="original" report="report" we="we" chose="chose" present="present" among="among" persons="persons" with="with" asc-us="asc-us" pap="pap" tests="tests" more="more" detail="detail" by="by" order="order" inform="inform" debate="debate" about="about" optimal="optimal" cutoffs="cutoffs" for="for" triage.="triage." encountered="encountered" relatively="relatively" few="few" lsil="lsil" hsil="hsil" cases="cases" resulting="resulting" combining="combining" categories.="categories." p="p" />Although we do not advocate managing LSIL and HSIL on the basis of HPV DNA testing, we report prevalence data for LSIL and HSIL Paps: HR-HPV prevalence (as measured by Hybrid Capture 2 testing) among those with LSIL and aged 14-20 years was 91% (156/171, 95% CI 86-95%) and those aged 21-29 years was 90% (198/219, 95% CI 86-94%). Other 5-year age categories had fewer than 20 cases and we do not report them. Prevalence was 71% (40/56, 95% CI 56-83%) for those aged 30 years and older. There were 54 cases of HSIL, with a HR-HPV prevalence of 93% (43/46, 95% CI 82-97%) among those aged less than 30 years and a prevalence of 75% (6/8, 95% CI 35-97%) among those aged 30 years and older. There was a single case of AIS in our study.

S. Deblina Datta, MD Hillard Weinstock, MD MPH


1. Wright TC Jr, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ, Solomon D; for the 2006 ASCCP-Sponsored Consensus Conference. 2006 consensus guidelines for the management of women with abnormal cervicalscreening tests. J Low Genit Tract Dis. 2007 Oct;11(4):201-22.

2. Human papillomavirus testing for triage of women with cytologic evidence of low-grade squamous intraepithelial lesions: baseline data from a randomized trial. The Atypical Squamous Cells of Undetermined Significance/Low-Grade Squamous Intraepithelial Lesions Triage Study (ALTS) Group. J Natl Cancer Inst. 2000 Mar 1;92(5):397-402.

3. Wright TC Jr, Cox JT, Massad LS, Twiggs LB, Wilkinson EJ; ASCCP- Sponsored Consensus Conference. 2001 Consensus Guidelines for the management of women with cervical cytological abnormalities. JAMA. 2002 Apr 24;287(16):2120-9.

Conflict of Interest:

None declared

Submit a Comment/Letter

Summary for Patients

Results of Pap Smears and Human Papillomavirus Tests during Cervical Cancer Screening

The summary below is from the full report titled “Human Papillomavirus Infection and Cervical Cytology in Women Screened for Cervical Cancer in the United States, 2003–2005.” It is in the 1 April issue of Annals of Internal Medicine (volume 148, pages 493-500). The authors are S.D. Datta, L.A. Koutsky, S. Ratelle, E.R. Unger, J. Shlay, T. McClain, B. Weaver, P. Kerndt, J. Zenilman, M. Hagensee, C.J. Suhr, and H. Weinstock.


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