Human papillomavirus vaccine practices in the USA

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STI Online First, published on April 21, 2012 as 10.1136/sextrans-2011-050437 Health services research

SHORT REPORT

Human papillomavirus vaccine practices in the USA: do primary care providers use sexual history and cervical cancer screening results to make HPV vaccine recommendations? Deanna Kepka,1 Zahava Berkowitz,2 K Robin Yabroff,1 Katherine Roland,2 Mona Saraiya2 1 Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, Maryland, USA 2 Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia, USA

Correspondence to Dr Deanna Kepka, Health Services and Economics Branch, Applied Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Executive Plaza North, Room 4017, 6130 Executive Boulevard, MSC 7344, Bethesda, MD 20892-7344, USA; [email protected] The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the National Cancer Institute or the Centers for Disease Control and Prevention. Accepted 28 March 2012

ABSTRACT Objectives Guidelines recommend against the use of Papanicolaou (Pap) or human papillomavirus (HPV) testing when determining eligibility for the HPV vaccine. Optimally, the HPV vaccine should be administered before sexual initiation. Guidelines recommend that ageeligible women with past exposure to HPV should still be vaccinated. Little is known about how primary care providers (PCPs) use sexual history and HPV and Pap tests in their HPV vaccine recommendations. Methods Data from the 2007 Cervical Cancer Screening Supplement (CCSS) administered with the National Ambulatory Medical Care Survey (NAMCS) and the National Hospital Ambulatory Medical Care Survey (NHAMCS) were used to assess HPV vaccination recommendations. The CCSS investigates cervical cancer screening practices, HPV testing and HPV vaccine recommendations among PCPs. A summary measure of compliance with guidelines was defined as rarely or never using the number of sexual partners and HPV tests and Pap tests to determine vaccine receipt. A total of 421 PCPs completed the CCSS in 2007. Results Among NAMCS and NHAMCS providers who recommend the HPV vaccine, only 53% (95% CI 42% to 63%) reported making guideline-consistent recommendations. The majority reported sometimes to always recommending the HPV vaccine to women with a history of an abnormal Pap result (85%; 95% CI 75% to 91%) and a positive HPV test (79%; 95% CI 70% to 86%). Conclusions A large proportion of providers report practices that are inconsistent with guidelines. Providers may also be recommending the vaccine to women who may receive little benefit from the vaccine. Provider and system-level efforts to improve guideline-consistent practices are needed.

Differences among guidelines may impact primary care provider (PCP) knowledge and recommendation practices for the human papillomavirus (HPV) vaccine. In 2006, the Advisory Committee on Immunization Practices (ACIP) recommended that girls aged 11 and 12 years receive the HPV vaccine and that girls and women aged 13e26 years who have not yet received the vaccine receive ‘catch up’ vaccination as part of cervical cancer prevention efforts to increase vaccine coverage in the USA.1 Similarly, the American Cancer Society also recomKepka D, Berkowitz Article Z, Yabroff KR, et al. Sex Transm Infect (2012). doi:10.1136/sextrans-2011-050437 Copyright author (or their employer) 2012. Produced by

mends HPV vaccination for girls aged 11 and 12 years with ‘catch-up’ vaccination for girls and women aged 13e18 years. However, the American Cancer Society differs from ACIP and recommends that HPV vaccination should be a part of informed decisions between a patient and her provider for women aged 19e26 years due to insufficient evidence that assesses vaccine benefit among women with more than four sexual partners and the lack of cost-effectiveness analyses evidence for vaccination for this age group.2 Optimally, the HPV vaccine should be administered before sexual initiation. However, ACIP and the American College of Obstetricians and Gynecologists recommend that age-eligible women with past exposure to HPV still be vaccinated (ie, regardless of whether they have an abnormal Papanicolaou (Pap) test or a positive HPV test).3 4 Guidelines recommend against the use of Pap or HPV testing to identify women for HPV vaccination4 and routine HPV testing for women under the age of 30 years.5 6 Little is known about how PCPs use sexual history and HPV and Pap testing in their recommendations for the HPV vaccine.

METHODS We used data from the 2007 Cervical Cancer Screening Supplement (CCSS) administered with the National Ambulatory Medical Care Survey (NAMCS) and the National Hospital Ambulatory Medical Care Survey (NHAMCS) to assess PCPs HPV vaccination recommendations for their patients. The CCSS investigates cervical cancer screening practices, HPV testing and HPV vaccine recommendations among PCPs. The questionnaire was administered in PCP offices and community health centres (NAMCS) and hospital outpatient departments (NHAMCS). NAMCS includes obstetricians/gynaecologists, general/family practice physicians, internists or mid-level providers and has a large range of sociodemographic characteristics of these providers; NHAMCS includes clinics specialising in obstetrics/gynaecology or general medicine and only has their geographical region of practice.7 8 Descriptive statistics and HPV vaccine recommendations were assessed for 407 NAMCS and NHAMCS respondents who provided information on their cervical cancer screening practices.7 Among providers who recommend the HPV vaccine and 1 of 3 BMJ Publishing Group Ltd under licence.


Health services research offer an HPV test (n¼308), the use of sexual history and HPV and Pap test results in making HPV vaccine recommendations were assessed by response category (rarely or never vs sometimes to always). A summary measure of compliance with guidelines was defined as rarely or never using the number of sexual partners and HPV tests and Pap tests to determine vaccine receipt (table 1). To account for the NAMCS and NHAMCS sampling weights and incorporate survey design and nonresponse, data were analysed using SUDAAN.

RESULTS A total of 421 providers completed the CCSS in 2007 (weighted CCSS response rates for NAMCS and NHAMCS, 27.6% and 54.4%, respectively). Among NAMCS providers, almost 50% were general/family practice physicians. The majority were men, aged 45 years and older, and working in smaller practices in metropolitan regions. In an additional weighted analysis, we found that of the subset of NAMCS providers who recommend the HPV vaccine (90%), 41% recommend it to girls aged 9e12 years, 80% to girls and women aged 13e26 years, and 21% to women aged 27 years and older. NHAMCS providers were mostly in general practice, with half affiliated with teaching hospitals (data not shown). Among NAMCS and NHAMCS providers who recommend the HPV vaccine, only 53% (95%; CI 42% to 63%) reported making guideline-consistent recommendations across all measures such that they rarely or never use the number of sexual partners, an HPV test or a Pap test to determine vaccine receipt (table 1). The majority of providers reported sometimes to always recommending the vaccine to women with a history of an abnormal Pap test result (85%; 95% CI 75% to 91%) and with a positive HPV test (79%; 95% CI 70% to 86%). Recommenda-

Table 1

tions for the vaccine did not differ by provider specialty (data not shown).

DISCUSSION This is the first national study to investigate compliance with guidelines related to the use of sexual history and HPV and Pap testing to determine HPV vaccine recommendations. We found that nearly half of PCPs made recommendations for HPV vaccination that were not consistent with all three of the measures used to assess guideline compliance. This includes the overuse of HPVand Pap testing and enquiry into sexual history to determine vaccine receipt, which may add additional unnecessary costs and barriers to the practice of vaccinating adult women. Furthermore, providers may be recommending the vaccine to women who may receive little benefit from HPV vaccination, and as a result they may also be overusing the HPV vaccine. Receipt of the HPV vaccine by women who may receive little benefit from HPV vaccination may not be accompanied by appropriate counselling on the relative decreased effectiveness of the vaccine. This could result in potential harm if the vaccine recipient and/or her parent feel that the vaccine recipient is protected against HPV types 16 and 18 when she may not be. However, receipt of the HPV vaccine among women aged 19e26 years with a history of abnormal Pap tests and/or a positive HPV test may occur as a result of an informed decision-making process with a medical provider. In addition to improving consistency across guidelines, provider and system-level efforts to improve HPV vaccine practices are needed. In 2010, only approximately 22% of women aged 19e26 years in the USA had received at least one dose of the HPV vaccine, suggesting that additional efforts are needed to increase vaccination in age-eligible women.9 However, the non-recommended use of HPV and Pap testing to determine

PCPs use of sexual history and HPV and Pap testing to recommend HPV vaccination (N¼308)*

For each row, numbers do not always add to 308 because unknown/not applicable/do not ask or missing responses were not included. Shaded areas represent guideline consistency. *Data from the 2007 Cervical Cancer Screening Supplement (CCSS), administered in conjunction with the National Ambulatory Medical Care Survey (NAMCS) and the National Hospital Ambulatory Medical Care Survey (NHAMCS), including only providers who recommend the human papillomavirus (HPV) vaccine and offer the HPV test as included in the skip patterns related to the survey design. The rate of inclusion is similar for NAMCS and NHAMCS providers. The percentages are population estimates. To account for the NAMCS and NHAMCS weights, sampling design and survey non-response, data were analysed using SUDAAN 10.0.1. yCenters for Disease Control and Prevention (CDC) Advisory Committee on Immunisation Practices, ‘Quadrivalent human papillomavirus vaccine’ (2007) and the American College of Obstetricians and Gynaecologists, committee opinion #344, ‘Human Papillomavirus Vaccination’ (2006). Guidelines are against the use of HPV testing, Papanicolaou (Pap) testing, and enquiry into sexual history to determine who should receive the HPV vaccination. Current guidelines support age-based recommendations. zSummary measure of guideline-consistent practices was defined rarely or never using the number of sexual partners, HPV tests, and Pap tests to determine who should receive the vaccine. xUnable to determine the age range of female patients. PCP, primary care provider.

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Health services research

Key messages < Guidelines recommend against the use of Pap or HPV testing

when determining eligibility for the HPV vaccine. < A large proportion of US providers report practices that are

inconsistent with HPV vaccination guidelines. < Provider and system-level efforts to improve guideline-

consistent practices for HPV vaccine administration are needed. vaccine receipt is an unnecessary use of testing.5 Furthermore, providers who universally recommend the HPV vaccine to patients with pre-invasive cervical cancer and/or infection with HPV 16 and 18 may be overusing the vaccine. The low response rate was a limitation of our study, and NAMCS and NHAMCS respondents differed from non-respondents in demographic characteristics, practice size and geographical location. However, all estimates used sample weights that incorporated survey non-response. In sensitivity analysis, the majority of PCP characteristics that differed between NAMCS respondents and non-respondents were not related to recommendations for the vaccine. Therefore, our findings should be generalisable to the US population of PCPs performing cervical cancer screening. An additional limitation is that PCPs who specifically serve women under the age of 26 years were not targeted for the survey, although the majority reported treating patients aged 15e24 years (weighted percentage 76%). Questions about HPV and Pap testing and sexual history did not specify a particular patient age group. To ensure that all age-eligible women receive the HPV vaccine without enquiry into sexual history and overuse of HPV and Pap tests, as consistent with ACIP and American College of Obstetricians and Gynecologists guidelines, additional provider and system-level efforts, such as algorithms within electronic

medical records, to improve guideline-consistent practices are needed. Furthermore, providers should not overuse the vaccine among women who would receive little benefit from immunisation. Acknowledgements DLK acknowledges support from the Cancer Prevention Fellowship Program, Center for Cancer Training and the Health Services and Economics Branch, Applied Research Program, Division of Cancer Control and Population Sciences of the National Cancer Institute, Bethesda, MD. Contributors All authors conceived the research questions. DK led the data analysis and wrote the short report under the guidance of KRY and MS. ZB completed the statistical analyses, drafted the methods and edited the short report. KR helped design the study and edited the short report. KRY and MS contributed to the writing and editing of the short report. Competing interests None. Provenance and peer review Not commissioned; externally peer reviewed.

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Centers for Disease Control and Prevention. ACIP Recommends HPV Vaccination. 2006. http://www.cdc.gov/media/transcripts/t060629.htm (accessed 1 Jun 2011). Saslow D, Castle PE, Cox JT, et al. American Cancer Society guideline for human papillomavirus (HPV) vaccine use to prevent cervical cancer and its precursors. CA Cancer J Clin 2007;57:7e28. Committee on Adolescent Health Care; ACOG Working Group on Immunisation. ACOG committee opinion no. 344: human papillomavirus vaccination. Obstet Gynecol 2006;108:699e705. Markowitz LE, Dunne EF, Saraiya M, et al; Centers for Disease Control and Prevention. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). Morbidity Mortality Weekly Rep 2007;56:1e24. Solomon D, Papillo J, Davis Davey D. Statement on HPV DNA test utilization. J Low Genit Tract Dis 2009;13:135e6. US Preventive Services Task Force. Screening for cervical cancer: US Preventive Services Task Force draft recommendation statement. 2011. http://www. uspreventiveservicestaskforce.org/draftrec4.htm (accessed 11 Nov 2011). Centers for Disease Control and Prevention. About the Ambulatory Health Care Surveys. 2009. http://www.cdc.gov/nchs/ahcd/about_ahcd.htm (accessed 1 Jun 2011). Roland KB, Soman A, Benard VB, et al. Human papillomavirus and pap test screening interval recommendations in the United States. Am J Obstet Gynecol 2011;205:447. Centers for Disease Control and Prevention (CDC). Adult vaccination coveragedUnited States, 2010. MMWR Morb Mortal Wkly Rep 2012;61:66e72.

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Human papillomavirus vaccine practices in the USA: do primary care providers use sexual history and cervical cancer screening results to make HPV vaccine recommendations? Deanna Kepka, Zahava Berkowitz, K Robin Yabroff, et al. Sex Transm Infect published online April 21, 2012

doi: 10.1136/sextrans-2011-050437

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