The Journal – October 2012
Clinical Service Characteristics and Initiation of the Human Papillomavirus Vaccination Series in an Academic Clinic Setting
By Amanda M. Hinson-Enslin, MPH, RDH; Robert Cardarelli, DO, MPH; and Kathryn M. Cardarelli, PhD
Ms Hinson-Enslin, dental hygienist, Brown and Associates, DDS; Dr Roberto Cardarelli, associate professor of behavioral and community health and director of the Primary Care Research Center/Texas Prevention Institute, University of North Texas Health Science Center, Fort Worth, Texas; and Dr Kathryn Cardarelli, assistant professor of epidemiology and director of the Center for Community Health/Texas Prevention Institute, University of North Texas Health Science Center, Fort Worth, Texas. Send correspondence to Amanda M. Hinson-Enslin, MPH, RDH, at Marshall H. Brown, DDS & Associates, 8432 Hawks Nest Dr, Fort Worth, TX 76131; email: firstname.lastname@example.org.
This work was supported in part by R21CA126732 from the National Cancer Institute and by 5P20MD001633 from the National Center on Minority Health and Health Disparities to KMC. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCI or NCMHD.
Investigators examined billing records from 4 university-affiliated primary care clinics for encounters with females aged 8-26 years from October 2007 to May 2008 to determine clinical service characteristics of initiating the human papillomavirus (HPV) vaccination series. A total of 5538 services were rendered to 1365 patients within 2550 visits. Sixteen percent of those who received HPV vaccination were adults. Statistically significant predictors of initiating the vaccination series included type of visit (ie, nurse visit and preventive visit) and the patient being a minor.
In June 2006, the Food and Drug Administration (FDA) approved the first vaccination, Gardasil©, to help prevent human papillomavirus (HPV) types 6, 11, 16, and 18 among girls and women aged 9 to 26 years.1-5 Soon after FDA approval, the Centers for Disease Control and Prevention's Advisory Committee on Immunization Practices (ACIP) recommended the 3-dose vaccination for girls as young as 9 years but, ideally, at ages 11-12 years.6-8 The ACIP also suggested that unvaccinated girls and women between the ages of 13 and 26 years obtain the HPV vaccination to help prevent contracting HPV types 6, 11, 16 and 18.7,8 The administration of the HPV vaccination is intended to protect against contracting HPV strains that cause cervical cancer and genital warts. An estimated 6.2 million persons in the United States are infected annually by HPV, making it the most common sexually transmitted disease.9,10 Of the 120 possible strains, 12 are linked causally to cervical cancer.9 Cervical cancer is a worldwide epidemic that kills more than 250,000 women yearly, and estimates predict that half a million women will be given a new diagnosis annually.11 The lifetime probability of a woman developing cancer of the cervix in the United States in 2008 was 1 in 142, which improved from 1 in 138 in 2007, and 1 in 135 in 2006. Yet, cervical cancer has the second highest mortality rate among cancer cases worldwide.9,12-14 Girls between the ages of 15 to 25 years represent almost half of the reported HPV cases.15 At least 80% of women who reach age 50 years have been infected by at least a single strain of HPV.15
Attitudes and beliefs of the HPV vaccination vary, but according to a 2004 study by Davis et al, 75% of parents wanted their child to be vaccinated after educational material was presented.16 Previous studies have indicated that with education most parents, children, and college attendees prefer to have the vaccination.16,17 While most research has studied individual factors associated with vaccination perceptions and acceptance, little investigation has been conducted on clinical practice characteristics and attributes as potential predictors to HPV vaccination delivery. Our study examined which clinical service characteristics are associated with the initiation of the HPV vaccination series among females between the ages of 8 to 26 years at 4 academic primary care clinics. Such information may provide guidance to clinics and programs to increase HPV vaccination rates.
Deidentified insurance billing records were identified for all females aged 8-26 years who were seen at least once in any of 4 primary care academic clinics located in Fort Worth, Texas, from October 2007 to May 2008. This time frame was selected since the HPV vaccination was approved by the FDA in late 2006 and became available shortly after at the 4 academic clinics. A total of 2,550 encounters occurred during this period. Data were condensed at the individual level, removing duplicated entries that resulted from multiple visits during the study period and resulting in the final study sample of 1365. However, the total number of services, visits, and type of visits were tallied for each patient as described below. This study was approved by the University of North Texas Health Science Center's Institutional Review Board.
The primary outcome of interest was the initiation of the HPV vaccination series, defined as receiving at least 1 HPV vaccination. Completion of the series, which comprises 3 vaccinations over 6 months, was not chosen as an outcome of interest because of the short study period and the possibility that patients may complete the series beyond May 2008. Nonetheless, the study team believed that initiating the series was good proxy measure to eventually receiving the second and third immunization injections.
Categories for race or ethnicity were non-Hispanic white, African American, Hispanic, and other. Clinic site was dummy coded to maintain confidentiality, and insurance type (private, federal or state, and multiple sources) was also included in the study. Age was calculated using the date of birth and the date at the midpoint of the study period (January 15, 2008) and then categorized as younger than 18 years (minor) and 18 years or older (adult). As each patient may have had multiple services and visits, a total number of office visits, preventive visits, and nurse visits were tabulated for each patient during the study period. In addition, the number of other non-HPV immunizations was recorded during the same visit. A preventive visit was measured as a visit with a clinician and coded as a preventive visit (ie, well-child visit, preventive or yearly visit). A nurse visit was measured as a visit without a clinician but with a nursing staff member.
Descriptive counts and frequencies were computed for categorical data; means and standard deviations, for continuous variables. Independent sample t tests and chi-square analyses were performed to test for differences in independent variables between participants who initiated the HPV vaccination series and those who did not (Table 1). Logistic regression was performed, and crude and adjusted odds ratios and 95% confidence intervals were calculated (Tables 2 and 3). Statistical significance was assessed at the alpha = 0.05 level. The multiple logistic regression model assessed for potential collinearity and no collinear relationships were identified. Statistical Package for the Social Sciences (SPSS) Version 15.0 was used for analysis.
Study population characteristics are presented in Table 1. Those who initiated the HPV vaccinations were more likely to receive clinical services at 2 of the clinical sites, were younger than 18 years, had fewer office visits but a greater number of preventive and nurse visits, and received a higher number of other immunizations. No statistically significant differences were found between those who initiated the HPV vaccination series and those who did not by race or ethnicity and by insurance type.
Univariate logistic regression results are presented in Table 2. Hispanics were 1.53 times more likely (95% confidence interval [CI]: 1.05-2.22) to initiate the HPV vaccination series compared with whites. Patients with multiple forms of insurance were 42% more likely (95% CI: 1.02-1.96) to initiate the vaccination series compared with patients having only private insurance. In addition, those who received their clinical services at clinic site 4 and those 18 years or older were 50% (95% CI: 0.31-0.81) and 74% (95% CI: 0.16-0.43), respectively, less likely to initiate the vaccination series. Although we found a 25% reduction in odds (95% CI: 0.65-0.87) of initiating the HPV vaccination series for every clinic visit, we observed 3.50 (95% CI: 2.73-4.48) and 9.29 (95% CI: 5.98-14.45) times increased odds of initiating the vaccination series for every preventive and nurse visit, respectively. Moreover, the odds of initiating the series showed a 2-fold increase for every other immunization that was delivered in the encounter.
Multiple logistic regression results are presented in Table 3. In this model, we found no statistically significant associations with initiating the HPV vaccination series for race or ethnicity, insurance type, number of office visits, or number of other immunizations. In the adjusted model, clinic site 2 was 56% less likely (95% CI: 0.24-0.81) and clinic site 3 was 85% more likely (95% CI: 1.07-3.23) to initiate the vaccination series when compared with clinic site 1. Those aged 18 years and older remained 69% less likely (95% CI: 0.16-0.57) to initiate the series compared with those who were younger than 18 years. Moreover, every preventive and nurse visit increased the odds of initiating the HPV vaccination series by 3.85 (95% CI: 2.81-5.28) and 15.7 (95% CI: 8.89-27.65) times, respectively.
Previous research exploring barriers and enabling factors for HPV vaccination have used qualitative methods and survey-based study designs and have focused primarily on patients, caregivers, and clinicians.18-21 This study examined clinical practice characteristics that predict HPV vaccination by using billing records from primary care clinics in urban Texas. This objective evidence is important for clinics and health systems to leverage and strategically allocate resources to develop plans and protocols to successfully implement HPV vaccination programs.
Our study revealed higher rates of initiating the HPV vaccination series in 2 specific family medicine clinics that serve large numbers of pediatric and adolescent patients. Notwithstanding the unavailability of additional data to explore these differences, we believe they are a result of standardized protocols, standing orders, and workflows that have been designed for a full age-spectrum family medicine practice. This is consistent with other research that has found a higher likelihood to recommend the HPV vaccination if the practice saw a high number of adolescent patients.22 Because the HPV vaccination is more efficacious when given at early ages, we were encouraged to find that age (younger than 18 years) was a significant predictor of the HPV vaccination. Given that preventive visits decline significantly after age 14 years and again after 17 years,23 this is an important age group to target for HPV vaccination. Furthermore, vaccination rates among adults are diminished by multiple barriers.24,25
The study has several limitations that must be considered. Because our data were collected during a time when the HPV vaccination was introduced to the United States market, there may be some differences from our findings as a result of time. We used receiving at least one vaccination as a proxy measure to initiating the HPV vaccination series, as small numbers precluded analyses of assessing the completion of the vaccination series. In addition, because billing data were used, we could not ascertain whether one of the HPV vaccination dosages was provided in a different location. Although the FDA has recently approved the HPV vaccination for males, we only included females because male vaccinations were not approved at the time of our study. Whether results can be generalized to other parts of the country or to nonacademic clinics is unknown. Kahn et al found that academic clinics in Texas were more likely than nonacademic practices to recommend the HPV vaccine to adolescent girls.22 Finally, the cross-sectional nature of the analyses precludes any causal conclusions.
Current ACIP recommendations include universal HPV vaccination of adolescent girls. Targeting patients who present for a preventive visit or a nurse visit may be an efficient strategy to increase HPV vaccine uptake, particularly for adolescent patients. Many interventions can be designed to accommodate the resources and circumstances that are specific to any setting. However, future research will be needed to determine which interventions are more efficient and cost-effective.
Physicians could consider implementing interventions depending on the capability of clinics and their available resources to increase the completion of the HPV vaccination series. These include developing automated reminders using information technology products, such as population management software associated with electronic health records or developing macro programs using Microsoft Excel©. Another suggestion is to conduct vaccination-specific queries and invite patients who are due (ie, for their next HPV vaccination) to call and schedule a nurse visit appointment. An additional method is to place reminders in front of medical charts during preventive or any type of visit. These are simple examples of possible interventions that can be developed in any clinic setting.
Nurse visits were the single greatest predictor to initiating the HPV vaccination series in our study, followed by yearly preventive visits. On the basis of these findings, physicians can design effective strategies related to preventive and nurse visits to improve adherence to national vaccination recommendations within clinics and health systems. Physicians’ limited time constrains their opportunity to spend time with patients and parents to discuss the HPV vaccine, underscoring the contribution of support staff and nonphysician personnel in providing this role.21 Further research of these strategies and methods will need to study how effectively they retain patients to complete the HPV vaccination series.
- Centers for Disease Control and Prevention. HPV vaccine questions & answers. http://www.cdc.gov/vaccines/vpd-vac/faqs-vpd-vac.htm. Updated October 20, 2009. Accessed May 23, 2010.
- Herbert J, Coffin J. Reducing patient risk for human papillomavirus infection and cervical cancer. J Am Osteopath Assoc. 2008;108(2):65-70.
- US Food and Drug Administration. FDA licenses new vaccine for prevention of cervical cancer and other diseases in females caused by human papillomavirus [press release]. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/2006/ucm108666.htm. June 8, 2006. Updated June 18, 2009. Accessed May 23, 2010.
- US Food and Drug Administration. Human Papillomavirus (Types 6, 11, 16, 18) Recombinant Vaccine: Medical officer's review. http://www.fda.gov/downloads/BiologicsBloodVaccines/Vaccines/ApprovedProducts/UCM111287.pdf. Accessed May 23, 2010.
- US Food and Drug Administration. Gardasil. http://www.fda.gov/cber/products/gardasil.htm. Updated November 17, 2009. Accessed May 23, 2010.
- Advisory Committee on Immunization Practices. Quadrivalent human papillomavirus vaccine. MMWR Morb Mortal Wkly Rep. 2007;56:1-24.
- Markowitz LE, Dunne EF, Saraiya M, et al. Quadrivalent human papillomavirus vaccine: Recommendations of the Advisory Committee on Immunization Practices (ACIP) [electronic version]. MMWR Morb Mortal Wkly Rep. 2007;56(RR02):1-24. http://www.cdc.gov/mmwr/preview/mmwrhtml/rr5602a1.htm?s_cid=rr5602a1_e. Updated March 12, 2007. Accessed May 23, 2010.
- American Academy of Pediatrics, Committee on Infectious Diseases. Prevention of human papillomavirus infections: provisional recommendations for immunization of girls and women with quadrivalent human papillomavirus vaccine. Pediatrics. 2007;120(3):666-668.
- Steben M, Duarte-Franco E. Human papillomavirus infection: epidemiology and pathophysiology. Gynecol Oncol. 2007;107(2 Suppl 1):S2-S5.
- Weinstock H, Berman S, Cates W Jr. Sexually transmitted diseases in American youth: incidence and prevalence estimates, 2000. Perspect Sex Reprod Health. 2004;36(1):6-10.
- WHO. Preparing for the introduction of HPV vaccines: policy and programme guidance for countries. http://whqlibdoc.who.int/hq/2006/WHO_RHR_06.11_eng.pdf. Accessed May 23, 2010.
- American Cancer Society. Cancer Facts and Figures 2006. Atlanta, GA: American Cancer Society. http://www.cancer.org/docroot/PRO/content/PRO_1_1_Cancer_Statistics_2006_Presentation.asp. Accessed May 23, 2010.
- American Cancer Society. Cancer Facts and Figures 2007. Atlanta, GA: American Cancer Society. http://www.cancer.org/docroot/PRO/content/PRO_1_1_Cancer_Statistics_2007_Presentation.asp. Accessed May 23, 2010.
- American Cancer Society. Cancer Facts and Figures 2008. Atlanta, GA: American Cancer Society. http://www.cancer.org/docroot/PRO/content/PRO_1_1_Cancer_Statistics_2008_Presentation.asp. Accessed May 23, 2010.
- Saslow D, Castle PE, Cox JT, et al. American Cancer Society guidelines for human papillomavirus (HPV) vaccine use to prevent cervical cancer and its precursors. CACancer J Clin. 2007;57(1):7-28.
- Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. Obstet Gynecol Surv. 2004;59(12):820-822.
- Boehner CW, Howe SR, Bernstein DI, Rosenthal SL. Viral sexually transmitted disease vaccine acceptability among college students. Sex Transm Dis. 2003;30(10):774-778.
- Brewer NT, Fazekas KI. Predictors of HPV acceptability: a theory-informed, systematic review. Prev Med. 2007;(2-3)45:107-114.
- Gerend MA, Magloire ZF. Awareness, knowledge, and beliefs about human papillomavirus in a racially diverse sample of young adults. J Adolesc Health. 2008;42(3):237-242.
- Herzog TJ, Huh WK, Downs LS, Smith JS, Monk BJ. Initial lessons learned in HPV vaccination. Gynecol Oncol. 2008;109(2 Suppl):S4-S11.
- Jenson HB. Human papillomavirus vaccine: a paradigm shift for pediatricians. Curr Opin Pediatr. 2009;21(1):112-121.
- Kahn JA, Cooper HP, Vadaparampil ST, et al. Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to-12-year-old girls: a statewide survey of Texas physicians. Cancer Epidemiol Biomarkers Prev. 2009;18(8):2325-2332.
- Rand CM, Shone LP, Albertin C, Auinger P, Klein JD, Szilagyi PG. National healthcare visit patterns of adolescents: implications for delivery of new adolescent vaccines. Arch Pediatr Adolesc Med. 2007;161(3):252-259.
- Norwalk MP, Zimmerman RK, Feghali J. Missed opportunities for adult immunization in diverse primary care office settings. Vaccine. 2004;22(25-26):3457-3463.
- Johnson DR, Nichol KL, Lipczynski K. Barriers to adult immunization. Am J Med. 2008;121(7 Suppl 2):S28-S35.
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