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Vaccine 31 (2012) 109–113

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Impact of human papillomavirus (HPV) vaccination on HPV 16/18-related prevalence in precancerous cervical lesions Suzanne E. Powell a,∗ , Susan Hariri a , Martin Steinau b , Heidi M. Bauer c , Nancy M. Bennett d , Karen C. Bloch e,f , Linda M. Niccolai g , Sean Schafer h , Elizabeth R. Unger b , Lauri E. Markowitz a a Division of STD Prevention, National Center for HIV, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road, NE MS-E02, Atlanta, GA 30333, USA b Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, NE MS-G41, Atlanta, GA 30333, USA c STD Control Branch, California Department of Public Health, 850 Marina Bay Parkway, Building P, 2nd Floor, Richmond, CA 94804, USA d Center for Community Health and Department of Medicine, University of Rochester School of Medicine and Dentistry, 46 Prince Street, Rochester, NY 14607, USA e Department of Medicine, Vanderbilt University Medical Center, A-2200 MCN, Nashville, TN 37232, USA f Department of Preventive Medicine, Vanderbilt University Medical Center, A-2200 MCN, Nashville, TN 37232, USA g Division of Epidemiology of Microbial Diseases, Yale School of Public Health, 60 College Street, P.O. Box 208034, New Haven, CT 06520, USA h HIV/STD/TB Program, Oregon Public Health Division, Center for Public Health Practice, Oregon Health Authority, 800 NE Oregon Street, Suite 1130, Portland, OR 97232, USA

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Article history: Received 23 August 2012 Received in revised form 22 October 2012 Accepted 25 October 2012 Available online 6 November 2012 Keywords: Human papillomavirus (HPV) Vaccine impact Cervical intraepithelial neoplasia (CIN)

a b s t r a c t Background: Vaccination against human papillomavirus (HPV) types 16 and 18 is recommended for girls aged 11 or 12 years with catch-up vaccination through age 26 in the U.S. Cervical intraepithelial neoplasia (CIN) grade 2 or 3 and adenocarcinoma in situ (CIN2+) are used to monitor HPV vaccine impact on cervical disease. This report describes vaccination status in women diagnosed with CIN2+ and examines HPV vaccine impact on HPV 16/18-related CIN2+. Methods: As part of a vaccine impact monitoring project (HPV-IMPACT), females 18–31 years with CIN2+ were reported from pathology laboratories in CA, CT, NY, OR, TN from 2008 to 2011. One diagnostic block was selected for HPV DNA typing with Roche Linear Array. Demographic, abnormal Papanicolaou (Pap) test dates and vaccine status information were collected. The abnormal Pap test immediately preceding the CIN2+ diagnosis was defined as the ‘trigger Pap’. Results: Among 5083 CIN2+ cases reported to date, 3855 had vaccination history investigated; 1900 had vaccine history documented (vaccinated, with trigger Pap dates, or unvaccinated). Among women who initiated vaccination >24 months before their trigger Pap, there was a significantly lower proportion of CIN2+ lesions due to 16/18 compared to women who were not vaccinated (aPR = .67, 95% CI: .48–.94). Among the 1900 with known vaccination status, 20% initiated vaccination on/after their trigger screening. Women aged 21–23 years were more likely to initiate vaccination on/after the trigger Pap compared to 24–26 year olds (29.0% vs. 19.6%, p = .001), as were non-Hispanic blacks compared to non-Hispanic whites (27.3% vs. 19.0%, p = .001) and publicly compared to privately insured women (38.1% vs. 17.4%, p < .0001). Conclusion: We found a significant reduction in HPV 16/18-related lesions in women with CIN2+ who initiated vaccination at least 24 months prior to their trigger Pap. These preliminary results suggest early impact of the HPV vaccine on vaccine-type disease, but further evaluation is warranted. Published by Elsevier Ltd.

1. Introduction

∗ Corresponding author. Tel.: +1 404 639 6425; fax: +1 404 639 8610. E-mail addresses: [email protected] (S.E. Powell), [email protected] (S. Hariri), [email protected] (M. Steinau), [email protected] (H.M. Bauer), nancy [email protected] (N.M. Bennett), [email protected] (K.C. Bloch), [email protected] (L.M. Niccolai), [email protected] (S. Schafer), [email protected] (E.R. Unger), [email protected] (L.E. Markowitz). 0264-410X/$ – see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.vaccine.2012.10.092

Human papillomavirus (HPV) types 16 and 18 account for about 70% of cervical cancers and 50% of precancerous lesions. Two prophylactic vaccines against HPV types 16 and 18 are licensed for use in females in the United States (U.S.) [1,2]. In clinical trials, vaccine efficacy for the prevention of HPV 16 and 18-related precancerous lesions, cervical intraepithelial neoplasia grades 2 and 3 and adenocarcinoma in situ (CIN2+), was close to 100% for women naïve to the respective HPV vaccine types [3–5]. In contrast, efficacy ranged from 52% to 73% in the intent-to-treat (ITT) population

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that included women with prevalent HPV infections [3–5], as the vaccines are not therapeutic and do not prevent progression to disease among women infected with vaccine targeted HPV types at the time of vaccination. Since 2006, the U.S. Advisory Committee on Immunization Practices (ACIP) has recommended routine HPV vaccination for females aged 11 or 12 years, and for females aged 13–26 years if not previously vaccinated [6]. Monitoring trends in HPV type-specific CIN2+ could provide the earliest evidence of HPV vaccine impact on cervical disease, but population-based CIN2+ monitoring is challenging in the U.S. without national registries for cervical cancer screening or cervical precancerous lesions [7]. In Victoria, Australia, where vaccine coverage exceeds 80%, ecological data suggest vaccine impact on CIN2+ among females less that 18 years of age, but despite established registries, Pap and vaccine data linkage has been challenging, thus complicating interpretation of the data [8,9]. Furthermore, since vaccination is recommended through age 26 years, many women may be vaccinated after exposure to HPV through sexual activity. Information on vaccination history including dates of vaccination is important for vaccine effectiveness studies. Obtaining such data is challenging in the U.S. because adolescent and adult vaccination history is often missing, incomplete or not collected in state-based Immunization Information Systems (IIS) [10]. The primary objective of this analysis was to describe vaccination status in women diagnosed with CIN2+ and to examine the impact of HPV vaccination on precancerous cervical lesions caused by HPV types 16 and 18, using the indirect cohort study design [11,12]. This study design uses women with CIN2+ caused by nonHPV vaccine types as a comparison group to those infected with HPV vaccine types 16 and 18. 2. Methods 2.1. Population We used data collected from the HPV-IMPACT project (described in detail elsewhere [13]), which was established in 2007 to monitor the population impact of the HPV vaccine on CIN2+ and HPV types in U.S. women. Archived diagnostic tissue for HPV DNA typing, HPV vaccination, cervical cancer screening history and demographic data were collected for females aged 18–39 years residing in 5 catchment areas in California, Connecticut, New York, Oregon and Tennessee who were diagnosed with CIN2+ and reported to HPVIMPACT from 2008 to 2011. Due to reporting standards at some sites, partial data from 2011 was reported to the monitoring system as of May 2012, and was used for this analysis. Each of the 5 sites obtained approval from their Institutional Review Board or an exemption from review. 2.2. DNA typing Reporting laboratories prepared serial sections from one diagnostic formalin-fixed paraffin-embedded tissue block per case using precautions to prevent PCR contamination between cases as described in Gargano et al. [14]. Specimens were shipped to the Centers for Disease Control and Prevention (CDC) with cool packs to avoid high temperatures during transit. HPV DNA typing was performed only on specimens with at least one lesion present in hematoxylin and eosin (H&E) stained sections before and after extraction. Extraction and testing were performed as described in Gargano et al. [14] and Steinau et al. [15]. Briefly, extraction used high temperature (120 ◦ C) overnight external lysis with proteinase K and automated extraction with chemagic MSM (Chemagen, USA). Extracts were used in L1 consensus PCR (Linear Array (LA) HPV Genotyping Assay, Roche Diagnostics, Indianapolis,

IN) which detects 37 HPV types (6, 11, 16, 18, 26, 31, 33, 35, 39, 40, 42, 45, 51, 52, 53, 54, 55, 56, 58, 59, 61, 62, 64, 66, 67, 68, 69, 70, 71, 72, 73, 81, 82, 83, 84, 89, IS39). Samples with inadequate or HPV negative LA results were retested with INNO-LiPA® HPV Genotying Extra Assay (Innogenetics, Gent, Belgium). Samples negative for both the genomic control probe and HPV in LA and INNO-LiPA were considered inadequate and omitted [16]. 2.3. HPV vaccination history and cervical cancer screening data collection Detailed HPV vaccination information was investigated using various data sources among the 5 surveillance sites. Project staff conducted medical chart reviews of ordering and managing providers (which included obstetricians/gynecologists, family practitioners, and pediatricians) as the initial source for investigating HPV vaccination history. Where possible, state-based IIS were used to ascertain vaccination history [10]. Oregon, having the most complete and reliable IIS among the 5 surveillance sites, crosschecked vaccination status obtained from medical chart reviews against their state’s IIS. In Tennessee, CIN2+ cases were linked to the state’s Medicaid (TennCare) database to ascertain vaccination history in women continuously enrolled since June 2006. In California, project staff worked with providers to have vaccination history recorded on the colposcopy intake form for one of their largest public hospitals. Given the high awareness of HPV vaccination in New York [17], several large practices record HPV vaccination history on their intake form, which is administered at each visit. Since CIN2+ is reportable statewide in Connecticut, a telephone interview was conducted in addition to medical chart reviews on eligible women with reported CIN2+ [18]. If multiple data sources were available, information from the medical chart of the vaccine provider was used as it contained the most accurate information on vaccine doses, dates, and type of vaccine. Three mutually exclusive groups were used to categorize vaccination status. A woman was defined as ‘vaccinated’ if medical provider documentation or self-report data, such as an intakeform or interview, contained at least one date of vaccination or an approximate age of vaccination. A woman was determined ‘not vaccinated’ if she reported, or her medical records documented that no HPV vaccine was given. If no documentation was found using any of the data sources, the vaccination status was defined as ‘unknown vaccine history’. Demographic information including race/ethnicity and health insurance status as well as cervical cancer screening history was obtained on all women with HPV typing results. Laboratory and/or medical records were used to obtain demographic information. The abnormal Papanicolaou (Pap) test date immediately preceding the CIN2+ diagnosis, referred to as the ‘trigger Pap’, was collected primarily through pathology laboratory reports or medical chart reviews. 2.4. Analyses Statistical analysis was restricted to females aged 18–31 years at the time of CIN2+ diagnosis, since they were age-eligible for HPV vaccination prior to or during the study period. For descriptive analyses, diagnosis was categorized by grade and type (CIN 2, CIN 2/3, CIN 3, AIS/AIS + CIN). Age at vaccine initiation was stratified into 5-year age groups starting at 14 years, the earliest age that the women in this study could have received the HPV vaccine based on the date of vaccine licensure. Age at CIN2+ diagnosis was stratified into 3-year age groups. Race and ethnicity were classified as non-Hispanic white, non-Hispanic Black, Hispanic, Asian and Other. Other races included American Indian or Alaska native, native Hawaiian or Pacific Islander, and multiple races. Insurance

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5,083 18–31 year old women with CIN2+

1,827 Unknown vaccination history

3,855 Vaccination history

949 Vaccinated

1,079 Not vaccinated

821 Vaccination and Pap dates

1,900 Known vaccination status and Pap dates

1,226 Specimens sent for HPV DNA typing

19 HPV DNA negative

1,207 HPV DNA positive

Fig. 1. Flow chart of women studied from HPV-IMPACT project.

type was grouped into private, public, uninsured, and other. Private insurance type included health maintenance and managed care organizations, while Medicaid/Medicare, Indian Health Service, and Military/Veterans Affairs were grouped into public insurance. The uninsured category included those documented as self-pay or no coverage, and multiple type insurance was classified as other. To determine time intervals, we assumed that the longer the time interval between vaccination and trigger Pap, the more likely infection with the type causing CIN2+ occurred after vaccination. Vaccinated women were classified into one of the following four categories: ≥1 dose on or after the trigger Pap, ≥1 dose 1–12 months before the trigger Pap, ≥1 dose 13–24 months before the trigger Pap, and ≥1 dose >24 months before the trigger Pap. Pearson’s X2 test for independence was used to examine bivariate associations between HPV vaccination status and study characteristics. We used a log binomial model to estimate the association of vaccination timing on HPV type 16/18-related CIN2+, adjusting for covariates. All analyses were conducted using SAS Enterprise 4.3. 3. Results From 2008 to 2011, 5083 women aged 18–31 years with CIN2+ were reported to the monitoring system. At the time of analysis, vaccine history was investigated on 3855 (75.8%) of the 5083 eligible women. A total of 949 (24.6%) were classified as having initiated vaccination (of which, 821 women also had a trigger Pap date); 1079 (28.0%) were not vaccinated and 1827 (47.4%) had unknown vaccination history (Fig. 1). The proportion of investigated cases for

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whom vaccination history was unknown varied by site; from 37.9% to 84.1%. The median age at CIN2+ diagnosis was 23 years among vaccinated women, and 25 among women not vaccinated and those with unknown vaccination history. In vaccinated women, the percentage completing the 3 dose series ranged from 50.0% in Oregon to 71.1% in Connecticut. Timing and status of vaccination by diagnosis and demographics are outlined in Table 1. Among the 1900 women with vaccination histories (either vaccinated, with trigger Pap dates, or unvaccinated), 23.2% initiated vaccination before the trigger Pap, 20.0% initiated vaccination on/after the trigger Pap, and 56.8% were not vaccinated. We found significant differences in the percentage of women who initiated vaccination on/after the trigger Pap result by demographic characteristics. Women aged 21–23 years were more likely than women aged 24–26 years to have initiated vaccination on/after the trigger Pap (29.0% vs. 19.6%, p = .001). Significant differences were also found for non-Hispanic black women compared with non-Hispanic whites (27.3% vs. 19.0%, p = .001) and women with public insurance compared to private insurance (38.1% vs. 17.4%, p < .0001). Specimens from 64.5% of women with information on vaccination history (1226/1900) were sent to CDC for HPV DNA typing, at the time of analysis. Of the 1226 specimens, 1207 (98.5%) were HPV DNA positive. There were no differences with respect to diagnosis grade/type, age at vaccination initiation, age at CIN2+ diagnosis, race/ethnicity, insurance and project site among CIN2+ cases for whom DNA typing was not done (data not shown). After controlling for race/ethnicity and project site, women with CIN2+ who initiated vaccination at least 24 months before their trigger Pap were less likely to have HPV16/18-related CIN2+ lesions (aPR = .67, 95% CI: .48–.94) compared to those who were not vaccinated (Table 2). Timing of vaccine initiation was not associated with the proportion of HPV 16/18-related lesions in women diagnosed with CIN3/AIS.

4. Discussion This analysis presents early data suggesting HPV vaccine impact on HPV 16/18-related CIN2+ lesions in women 18–31 years in the U.S. We used time interval between vaccination and abnormal Pap screening as a measure of the likelihood that the vaccination occurred prior to infection with the HPV type responsible for the lesion. Despite the small sample size, we found that among women who initiated vaccination at least 24 months before their trigger Pap, HPV 16/18 accounted for a significantly smaller proportion of CIN2+ related lesions compared to women who initiated vaccination closer to their trigger Pap and to women who were not vaccinated. These results are consistent with prelicensure clinical trial analyses in the intention-to-treat (ITT) populations, which found no evidence of early efficacy, but that efficacy became apparent starting at about 24 months after vaccination [4,19]. It should be noted that our current analysis is not designed to evaluate HPV-type replacement in CIN2+ lesions, although this project may provide insight into this important question with additional years of data. Our data did not demonstrate the same vaccine impact in women diagnosed with CIN3/AIS, the highest grade lesions; this lack of association may in part be due to the longer time needed for CIN 3 or AIS to develop [20]. In the present analysis, we were unable to examine time intervals longer than 24 months given the short timeframe after widescale vaccine introduction. Time interval between vaccination and abnormal Pap screening would likely need to be longer to see an impact on higher grade lesions, and will continue to be evaluated with more years of data. This study has some limitations. The use of different sources to obtain vaccination history may have biased our findings, as completeness and accuracy varied by source and project site. However,

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Table 1 Human papillomavirus (HPV) vaccination status/timing by selected characteristics.

Overall Diagnosis CIN 2 CIN 2/3 CIN 3 AIS/AIS + CIN Age at vaccine initiation (yrs) 14–18b 19–23 24–26 27–31 Age at CIN2+ diagnosis (yrs) 18–20 21–23 24–26 27–31 Racec Non-Hispanic white Non-Hispanic black Hispanic Asian Other Insuranced Private Public Uninsured Other

Overalla N

≥1 dose before trigger Pap n (row %)

≥1 dose on/after trigger Pap n (row %)

Not vaccinated n (row %)

1900

441 (23.2)

380 (20.0)

1079 (56.8)

1096 251 526 27

273 (24.9) 56 (22.3) 107 (20.3) 5 (18.5)

230 (21.0) 40 (15.9) 105 (20.0) 5 (18.5)

593 (54.1) 155 (61.8) 314 (59.7) 17 (63.0)

68 489 261 3

58 (85.3) 256 (52.4) 125 (47.9) 2 (66.7)

10 (14.7) 233 (47.7) 136 (52.1) 1 (33.3)

– (–) – (–) – (–) – (–)

217 644 622 417

67 (30.9) 160 (24.8) 161 (25.9) 53 (12.7)

66 (30.4) 187 (29.0) 122 (19.6) 5 (1.2)

84 (38.7) 297 (46.1) 339 (54.5) 359 (86.1)

1116 275 202 31 42

276 (24.7) 49 (17.8) 34 (16.8) 8 (25.8) 10 (23.8)

212 (19.0) 75 (27.3) 35 (17.3) 3 (9.7) 8 (19.1)

628 (56.3) 151 (54.9) 133 (65.8) 20 (64.5) 24 (57.1)

1042 512 69 67

296 (28.4) 85 (16.6) 5 (7.3) 13 (19.4)

181 (17.4) 126 (38.1) 8 (11.6) 16 (23.9)

565 (54.2) 301 (58.8) 56 (81.2) 38 (56.7)

Trigger Pap: the abnormal Papanicolaou (Pap) test immediately preceding the CIN2+ diagnosis; CIN2+: cervical intraepithelial neoplasia, grade 2 or 3 or adenocarcinoma in situ. a Includes those that have vaccine dates and trigger Pap dates. b 14 years is the earliest age that cohort could have received vaccination based on date of vaccine licensure. c Excludes 12.4% missing/unknown race. d Excludes 11.2% missing/unknown insurance.

vaccination history was investigated without any prior knowledge of HPV typing data. Currently, adolescent vaccination is underreported to the California, New York and Tennessee IIS, and the Connecticut IIS contains only childhood vaccination records. IIS improvements that are expected with increased electronic reporting will help establish immunization systems as the primary source of vaccine information for future assessments. This analysis was based on a small sample size; thus, was not sufficiently powered to fully examine the relationship between vaccination, including series completion and diagnosis subgroups. Future analyses of the data will assess vaccine impact by demographics, number of doses and clinical characteristics. We found that some women with CIN2+ initiated HPV vaccination only after having an abnormal Pap or being diagnosed

with cervical disease. Similar data were previously reported from one of the sites in our project [21]. These data suggest that the abnormal test results may have led to patient request and/or provider recommendation for HPV vaccination. Significant differences were also found in vaccine initiation on/after the trigger Pap by age, race and insurance status. While the reasons are not clear, these differences in timing of vaccine initiation may be partially due to differential access to health care, differences in health seeking behavior or insurance coverage for vaccine. Although the vaccine may provide partial protection against future infection in women with an abnormal Pap test who are not infected with all types targeted by the HPV vaccines, vaccinating females at younger ages will provide maximum benefit of HPV vaccines.

Table 2 HPV 16/18 positivity in CIN2+ lesions by vaccination timing. Diagnosis/timing of vaccine initiation CIN2+ Not vaccinated On/after trigger Pap 1–12 months before trigger Pap 13–24 months before trigger Pap >24 months before trigger Pap CIN3/AIS Not vaccinated On/after trigger Pap 1–12 months before trigger Pap 13–24 months before trigger Pap >24 months before trigger Pap

N

HPV 16/18 n (%)

PR (95% CI)

aPRa (95% CI)

682 300 95 96 53

382 (56.0) 174 (58.0) 53 (55.8) 50 (52.1) 21 (39.6)

ref 0.98 (0.88–1.10) 1.00 (0.82–1.21) 0.93 (0.76–1.14) 0.71 (0.50–0.99)

ref 0.95 (0.85–1.07) 0.93 (0.77–1.13) 0.90 (.74–1.10) 0.67 (0.48–0.94)

211 93 29 25 19

158 (74.9) 66 (70.9) 24 (82.8) 18 (72.0) 13 (68.4)

ref 0.92 (0.80–1.07) 1.10 (0.91–1.33) 0.96 (0.74–1.25) 0.92 (0.67–1.25)

ref 0.91 (0.79–1.05) 1.03 (0.85–1.24) 0.91 (0.70–1.17) 0.87 (0.63–1.18)

HPV: human papillomavirus; CIN: cervical intraepithelial neoplasia; Trigger Pap: the abnormal Papanicolaou (Pap)test immediately preceding the CIN2+ diagnosis; PR: prevalence ratio; aPR: adjusted prevalence ratio; CI: confidence interval. a CIN2+: adjusted for race and site; CIN3/AIS: adjusted for race.

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In summary, we used data from a large population-based system for monitoring HPV vaccine impact on cervical disease in the U.S. to examine HPV vaccine effectiveness on HPV 16/18 types in CIN2+ lesions. We found that among women who were vaccinated at least two years prior to the abnormal cervical cancer screening test that led to a CIN2+ diagnosis, a significantly smaller proportion of CIN2+ lesions were related to HPV vaccine types 16 or 18 compared to those unvaccinated. These results, while encouraging, are preliminary and will be followed with more detailed analyses to fully evaluate vaccine effectiveness overall, by number of doses and in different racial/ethnic groups. Because HPV vaccination may be initiated in some women who have an abnormal Pap, accurate information on timing of vaccination is important for vaccine effectiveness determination. Acknowledgements

[4]

[5] [6]

[7]

[8]

[9] [10] [11]

The authors thank The HPV-IMPACT Working Group members for their dedication and contribution toward making this project successful: Ina Park, MD, MS, Erin Whitney, MPH, and Sharon McDonnell, MPH (California Department of Public Health, STD Control Branch); James Hadler, MD, Pamela Julian, MPH, James Meek, MPH (Yale University School of Medicine, Connecticut Emerging Infections Program) and Lynn Sosa, MD (Connecticut Department of Public Health); Mary Scahill and Denisse Licon, MPH (University of Rochester – New York Emerging Infections Program); Nasreen Abdullah MD, MPH, Rob Laing, MPH (Oregon Department of Human Services); Diane Levine, BS, RN, MPH, Manideepthi Pemmaraju, MBBS, MPH, Chasiety Turner, MPH (Vanderbilt University – Tennessee Emerging Infections Program). The authors gratefully acknowledge and thank Kathleen Hutchins (National Center for HIV, viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention) for her data management expertise and continuous support with this project. Disclosure statement: No conflict of interests.

[12]

[13]

[14]

[15]

[16]

[17]

[18]

References [19] [1] Centers for Disease Control. National vaccination coverage among adolescents aged 13–17 years – United States, 2006. MMWR Morb Mortal Wkly Rep 2007;56(August (34)):885–8. [2] Centers for Disease Control. 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). MMWR Morb Mortal Wkly Rep 2010;59(May (20)):626–9. [3] Hildesheim A, Herrero R, Wacholder S, Rodriguez AC, Solomon D, Bratti MC, et al. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine

[20]

[21]

113

among young women with preexisting infection: a randomized trial. JAMA 2007;298(August (7)):743–53. Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 2007;356(May (19)):1928–43. Group FIS. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 2007;356(May (19)):1915–27. Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger ER, et al. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2007;56(March (RR-2)):1–24. Markowitz LE, Hariri S, Unger ER, Saraiya M, Datta SD, Dunne EF. Postlicensure monitoring of HPV vaccine in the United States. Vaccine 2010;28(July (30)):4731–7. Brotherton JM, Fridman M, May CL, Chappell G, Saville AM, Gertg DM. Early effect of the HPV vaccination programme on cervical abnormalities in Victoria, Australia: an ecological study. Lancet 2011;377(June (9783)):2085–92. Saraiya M, Hariri S. HPV vaccine effect: is the glass half full or half empty? Lancet 2011;377(June (9783)):2057–8. Centers for Disease Control. Progress in immunization information systems – United States, 2010. MMWR Morb Mortal Wkly Rep 2012;61(June):464–7. Broome CV, Facklam RR, Fraser DW. Pneumococcal disease after pneumococcal vaccination: an alternative method to estimate the efficacy of pneumococcal vaccine. N Engl J Med 1980;303(September (10)):549–52. Andrews N, Waight PA, Borrow R, Ladhani S, George RC, Slack MP, et al. Using the indirect cohort design to estimate the effectiveness of the seven valent pneumococcal conjugate vaccine in England and Wales. PLoS ONE 2011;6(December (12)):e28435. Hariri S, Unger ER, Powell SE, Bauer HM, Bennett NM, Bloch KC, et al. The HPV vaccine impact monitoring project (HPV-IMPACT): assessing early evidence of vaccination impact on HPV-associated cervical cancer precursor lesions. Cancer Causes Control 2012;23(February (2)):281–8. Gargano JW, Wilkinson EJ, Unger ER, Steinau M, Watson M, Huang Y, et al. Prevalence of human papillomavirus types in invasive vulvar cancers and vulvar intraepithelial neoplasia 3 in the United States before vaccine introduction. J Low Genit Tract Dis 2012;16(October (4)):471–9. Steinau M, Patel SS, Unger ER. Efficient DNA extraction for HPV genotyping in formalin-fixed, paraffin-embedded tissues. J Mol Diagn 2011;13(July (4)):377–81. Hariri S, Steinau M, Rinas A, Gargano JW, Ludema C, Unger ER, et al. HPV genotypes in high grade cervical lesions and invasive cervical carcinoma as detected by two commercial DNA assays, North Carolina, 2001–2006. PLoS ONE 2012;7(3):e34044. Rand CM, Schaffer SJ, Humiston SG, Albertin CS, Shone LP, Heintz EV, et al. Patient–provider communication and human papillomavirus vaccine acceptance. Clin Pediatr 2011;50(February (2)):106–13. Niccolai LM, Mehta NR, Hadler JL. Racial/ethnic and poverty disparities in human papillomavirus vaccination completion. Am J Prev Med 2011;41(October (4)):428–33. Olsson SE, Kjaer SK, Sigurdsson K, Iversen OE, Hernandez-Avila M, Wheeler CM, et al. Evaluation of quadrivalent HPV 6/11/16/18 vaccine efficacy against cervical and anogenital disease in subjects with serological evidence of prior vaccine type HPV infection. Hum Vaccin 2009;5(October (10)):696–704. Castle PE, Rodriguez AC, Burk RD, Herrero R, Wacholder S, Alfaro M, et al. Short term persistence of human papillomavirus and risk of cervical precancer and cancer: population based cohort study. BMJ 2009;339:b2569. Mehta NR, Julian PJ, Meek JI, Sosa LE, Bilinski A, Hariri S, et al. Human papillomavirus vaccination history among women with precancerous cervical lesions: disparities and barriers. Obstet Gynecol 2012;119(March (3)):575–81.