Abstract
Objective
To estimate changes in high risk women’s knowledge of cervical cancer prevention, human papillomavirus (HPV), and HPV vaccination since introduction and marketing of HPV vaccines.
Methods
At study visits in 2006 and 2008, women with the human immunodeficiency virus (HIV) and at-risk comparison women in a multicenter U.S. cohort study completed 44-item self-report questionnaires exploring their knowledge of cervical cancer prevention, HPV, and HPV vaccination. Results from 2006 were compared to those obtained in 2008. Knowledge scores were correlated with demographic variables, measures of education and attention, and medical factors. Significant associations were assessed in multivariable models.
Results
HIV-seropositive women had higher knowledge scores than seronegative women at baseline (13.2 +/− 5.7 vs 11.8 +/− 6.0, P = 0.0002) and follow-up (14.1 +/− 5.3 vs 13.2 +/− 5.5, P = 0.01), but the change in scores was similar (0.9 +/− 5.3 vs 1.5 +/− 5.5, P = 0.13). Knowledge that cervical cancer is caused by a virus rose significantly (P = 0.005), but only to 24%. Belief that cervical cancer is preventable only rose from 52% to 55% (P = 0.04), but more than 90% of women in both periods believed regular Pap testing was important. In ANCOVA models, higher baseline score, younger age, higher education level, higher income, and former- as opposed to never-drug users, but not HIV status, were associated with improved knowledge.
Conclusion
High-risk women’s understanding of cervical cancer and HPV has improved, but gaps remain. Improvement has been weakest for less-educated and lower-income women.
Introduction
Persistent infection by human papillomaviruses (HPVs) can lead to cervical cancer, but effective screening and treatment of cancer precursors can substantially reduce cancer risk. Women with the human immunodeficiency virus (HIV) face high prevalence rates of HPV and high incidence rates of cervical intraepithelial neoplasia, the precursor to cervical cancer (1-5). Cervical cancer prevention is a complex process, potentially including vaccination against highest risk HPV types before sexual debut, repeated Pap and HPV DNA screening, triage with HPV DNA assessment and colposcopy, and cervical therapy. Loss to follow-up can occur at each step, and noncompliance with cancer prevention protocols is common among women at highest cervical cancer risk, including minority and poor women and those with HIV (6, 7). Women with HIV, like HIV-uninfected women of similar background, have significant knowledge deficits related to HPV, cervical cancer prevention, and HPV vaccination (8-11), even in the face of repeated visits for management of abnormal Pap tests and cervical cancer precursors. This may be because underlying educational deficits are a barrier to understanding cancer prevention messages (11). Little is known about how women’s knowledge of cervical cancer causation and prevention has evolved recently, influenced by clinician-based and public health education about HPV as well as marketing campaigns for HPV vaccination, available since 2006. We set out to estimate how knowledge and attitudes about cervical cancer prevention, HPV, and HPV vaccination might have changed from 2006-8 before and after the 2006 U.S. commercial introduction of HPV vaccine.
Methods
This investigation was nested in the Women’s Interagency HIV Study (WIHS), an ongoing U.S. multicenter prospective cohort investigation of the course of HIV infection and related health conditions among HIV seropositive women and seronegative comparison women at risk for HIV. The protocols, recruitment processes, procedures, and baseline results of the WIHS have been described (12, 13). Enrollment began with 2,623 women in 1994-5 at 6 study consortia (Bronx, Brooklyn, Chicago, Los Angeles, San Francisco, and Washington, D.C.). The cohort was expanded to 3,766 women during 2001-2002 (13). Written informed consent was obtained after local human subjects committees approved study protocols. HIV serostatus was determined by ELISA with confirmatory testing at study entry for all participants and annually thereafter for those initially seronegative.
Follow up continues, but this analysis compares information from previously reported cross-sectional questionnaires administered first between April and October, 2006, and again between April and October, 2008 (11). Following initial administration, women were provided with an answer sheet containing correct answers and explanations and were encouraged to bring questions to their clinicians.
The 44-item questionnaire included items related to knowledge of HPV, risk factors for cervical cancer, the HPV vaccine, and care following abnormal Pap smears. This analysis included only women who completed questionnaires in English. Responses were coded as correct or incorrect. McNemar’s test for correlated matched pairs was used to compare each woman’s baseline and follow-up responses, with further stratification by HIV status. A previous principal component analysis for item reduction was conducted, reducing the number of items to 24 items (11) that were used to compute a factor-based scale for knowledge score at baseline and follow-up (Cronbach’s alpha for follow-up data = 0.85). Each participant received a score of 1 for a correct and 0 for an incorrect response, with a maximum possible score of 24. A change score analysis, using the paired t-test, was conducted to assess whether and to what extent each individual’s knowledge score improved between baseline and follow-up.
Analysis of covariance (ANCOVA) models were used to examine change in knowledge between baseline and follow-up, where the follow-up score was the dependent variable. Independent variables included baseline score, HIV status, and other demographic and medical characteristics, including age at questionnaire administration, self-reported ethnicity, education attained by study entry, household income, abnormal Pap history, prior colposcopy, cervical disease treatment, reading level using the Wide Range Achievement Test-Version 3 (WRAT, 14), where scores can range from 0 to 42, and information processing and attentiveness using the Symbol Digit Modalities Test (15). For the initial model, each independent variable was evaluated for fit using the Type III SS value and p-value and were included in the analyses if they had a p-value <0.05. Raw symbol digit and WRAT score were added to subsequent models, as these had been shown to be significant in prior models assessing baseline knowledge (11). Final models are presented using the PROC Generalized Linear Models (GLM) procedure in SAS software 9.2 (SAS Institute Inc., Cary, NC).
Results
Of the 1,812 women completing study visits in 2006, 1,451 (80%) had completed questionnaires in English and are the focus of this study. Of these, 1,214 completed questionnaires again in 2008, but 93 were missing responses to at least one question and were excluded. Of the remaining 1,121 women included in this analysis, 773 (69%) were HIV seropositive and 348 (31%) were seronegative. The 93 women missing data on the follow-up questionnaire were slightly older (45.7 vs 43.1 years, P = 0.01 vs included patients), with lower education levels (P = 0.004) and lower WRAT scores (median 26 vs 29, P = 0.0009), were more likely to be a current or former intravenous drug users than those with complete questionnaire data (48.4% vs 23.2%, P< 0.0001), and were more likely to have CD4 counts <200/cmm (20% vs 13%, P = 0.04). Demographic and medical characteristics of included women are presented in Table 1. Of the women with HIV, 500 (65%) were using highly active antiretroviral therapy at the time of the first survey.
Table 1.
Baseline demographic and medical characteristics of women who completed questionnaires at baseline and follow-up (n=1121). N (%)
| HIV+ | HIV− | P-value1 | Missing | p-value | |
|---|---|---|---|---|---|
| N=773 | N=348 | ||||
| Age at interview (years) | |||||
| <30 | 44 (5.7) | 63 (18.1) | <0.0001 | ||
| 30-39 | 198 (25.6) | 113 (32.5) | |||
| 40-49 | 332 (43.0) | 111 (31.9) | |||
| 50+ | 199 (25.7) | 61 (17.5) | |||
| Ethnicity | |||||
| Non-Hispanic African American |
497 (64.3) | 219 (62.9) | 0.01 | ||
| Hispanic | 139 (18.0) | 84 (24.2) | |||
| Non-Hispanic White | 110 (14.2) | 30 (8.6) | |||
| Other | 27 (3.5) | 15 (4.3) | |||
| Average annual household income (n=1062) |
|||||
| <=$6,000 | 121 (16.4) | 79 (24.3) | 0.02 | ||
| $6,001-$12,000 | 216 (29.3) | 80 (24.6) | |||
| $12,001-$18,000 | 105 (14.3) | 41 (12.6) | |||
| $18,001+ | 295 (40.1) | 125 (38.5) | |||
| Education level (n=1119) | |||||
| Less than high school | 249 (32.3) | 116 (33.4) | 0.26 | ||
| Completed high school | 234 (30.3) | 118 (34.0) | |||
| Some College/College degree |
289 (37.4) | 113 (32.6) | |||
| Site/Location | |||||
| Bronx | 116 (15.0) | 65 (18.7) | 0.0009 | ||
| Brooklyn | 215 (27.8) | 73 (21.0) | |||
| Washington DC | 124 (16.0) | 47 (13.5) | |||
| Los Angeles | 84 (10.9) | 62 (17.8) | |||
| San Francisco | 110 (14.3) | 60 (17.2) | |||
| Chicago | 124 (16.0) | 41 (11.8) | |||
| Alcohol use | |||||
| Abstainer | 462 (59.8) | 165 (47.4) | <0.0001 | ||
| Light (<3 drinks/wk) | 225 (29.1) | 111 (31.9) | |||
| Moderate/Heavy (3+ drinks/wk) |
86 (11.1) | 72 (20.7) | |||
| Current Smoker | 337 (43.6) | 171 (49.1) | 0.08 | ||
| Injection drug use status | |||||
| Current user | 13 (1.7) | 7 (2.0) | 0.003 | ||
| Former user | 187 (24.2) | 53 (15.2) | |||
| Never | 573 (74.1) | 288 (82.8) | |||
| Non-Injection drug use status |
|||||
| Current user | 177 (22.9) | 116 (33.3) | 0.0002 | ||
| Former user | 395 (51.1) | 171 (47.1) | |||
| Never | 201 (26.0) | 61 (17.5) | |||
| English WRAT2 score (number of words pronounced correctly) (n=898) |
|||||
| Mean | 28.9 | 28.7 | 0.803 | ||
| Median | 31.0 | 29.0 | 0.564 | ||
| Range | 3 - 42 | 8 - 42 | |||
| Lifetime nadir CD4 lymphocyte count (cells/cmm) (n=773) |
|||||
| <200 | 355 (45.9) | ||||
| 200-500 | 357 (46.2) | ||||
| >500 | 61 (7.9) | ||||
| CD4 lymphocyte count (cells/cmm) at visit (n=773) |
|||||
| <200 | 101 (13.1) | ||||
| 200-500 | 303 (39.2) | ||||
| >500 | 369 (47.7) |
P-value obtained by using the chi-square test unless otherwise specified.
Wide Range Achievement Test
P-value obtained by using the t-test for means.
P-value obtained using the Wilcoxon rank-sum test.
P-value comparing missing to all those who completed entire survey.
Summary knowledge scores increased modestly between baseline and follow-up (12.7 +/− 5.8 vs 13.8 +/− 5.3, P < 0.0001). HIV-seropositive women had higher scores than seronegative women. This was true both at baseline (13.2 +/− 5.7 vs 11.8 +/− 6.0, P = 0.0002) and follow-up (14.1 +/− 5.3 vs 13.2 +/− 5.5, P = 0.01). However, the change in scores was statistically similar for the two groups (0.94 +/− 5.3 vs 1.47 +/− 5.5, P = 0.13).
Knowledge of cervical cancer prevention improved across a range of questions during follow-up. Nevertheless, substantial knowledge deficits persisted. For example, while significantly more women at follow-up understood what part of the body a Pap test evaluated (P = 0.0002), the proportion rose only to 52%. Knowledge of risk factors, indicating understanding of the causal factors underlying cervical cancer, remained marginal, with substantial proportions of women not understanding the link between cervical cancer and sexual activity, screening compliance, and smoking. Knowledge that cervical cancer is caused by a virus rose significantly (P = 0.005), but only to 24%. Belief that cervical cancer is preventable only rose from 52% to 55% (P = 0.04). Despite this, more than 90% of women continued to believe that regular Pap testing was important for both HIV infected and uninfected women. The proportion of women who knew HPV is a sexually transmitted virus causing warts and cervical cancer rose from 66% to 71% (P < 0.0002). About a third believed incorrectly that HPV could be cured with medication and roughly half believed that individuals can tell when they are HPV infected, proportions that did not change significantly across time. Awareness of the availability of HPV vaccination rose between 2006 and 2008 among the 1,121 women completing follow-up questionnaires, from 505 (45%) to 739 (66%), (P < 0.0001). This increased awareness appeared to arise from multiple sources, as women’s recognition of most sources of information increased over baseline (doctors 18% in 2006 vs 20% in 2008, nurses 10% vs 19%, WIHS staff 16% vs 33%, and advertising 69% vs 79%, P <0.0001). The proportion of women citing news reports or not recalling their information source did not change significantly (63% vs 55% for news, 7% vs 6% for unknown, P >0.2).
Knowledge about HPV vaccination also improved dramatically between surveys (Table 2), although many women did not understand the utility of vaccination in preventing perianal lesions and many believed it prevented herpes infections. Women also failed to appreciate the importance of targeting young girls for vaccination and incorrectly considered older women as good vaccine candidates. The proportion of women who believed HPV vaccination was extremely or very important for cervical cancer prevention, as compared to those who considered it somewhat/not important or were unsure, rose from 70% to 78% (P < 0.0001). Compared to 2006, more women at follow-up in 2008 believed recommending HPV vaccination to female relatives and friends to be extremely or very important (61% vs 66%, P = 0.001).
Table 2.
Percentage of correct responses to questions about vaccination against the human papillomavirus (HPV) at baseline and follow-up. (n=1,121)
| Correct Answer | |||
|---|---|---|---|
| Question | Baseline | Follow-up | McNemar’s test p-value |
|
Have you heard about an HPV vaccine called
Gardasil? |
45.1% | 65.9% | <0.0001 |
|
What do you think the vaccine is meant to
prevent? |
|||
| Abnormal Pap tests, cervical cancer and precancer | 66.0% | 72.9% | <0.0001 |
| Lung infections | 63.8% | 71.0% | <0.0001 |
| Urine infections | 54.4% | 62.5% | <0.0001 |
| Warts around the genitals and anus | 34.4% | 38.8% | 0.01 |
| Genital herpes | 38.7% | 43.7% | 0.006 |
|
For women with HIV, what are
recommendations for HPV vaccination? |
74.2% | 71.4% | 0.09 |
|
Among women without HIV, who should get
the HPV vaccine? |
|||
| Girls as young as 9 years of age | 28.0% | 38.5% | <0.0001 |
| Teenage and young adult women | 67.1% | 79.0% | <0.0001 |
| Women over 25 years who are at high risk | 9.3% | 14.6% | <0.0001 |
| Women 50 years of age and older | 21.6% | 33.8% | <0.0001 |
Factors associated with an improvement in knowledge score are shown in Table 3. The first model demonstrated that higher baseline score, younger age, higher education level, higher income, and former as opposed to never drug use were associated with greater improvement in knowledge score. R2 for this model was 0.32, indicating that these factors explained about a third of the magnitude of change. HIV status was not significant after controlling for these factors. When added to the final model (model 3) WRAT reading level replaced education as a significant correlate (0.09, 95% C.I. 0.04-0.13, P < 0.001) and improved R2 to 0.35, suggesting that educational quality was a more important predictor of change in knowledge than the number of years in school.
Table 3.
Regression coefficients for ANCOVA models among participants completing questionnaires assessing cervical cancer prevention knowledge, assessing association between follow-up knowledge score and other factors.
| Model 1 N=1121 |
Model 2 N=1056 |
Model 3 N=897 |
|
|---|---|---|---|
| Adjusted R 2 | 0.32 | 0.33 | 0.35 |
| F-Value | 66.11 | 57.971 | 48.11 |
| Predictor variables | |||
| Intercept | 7.43 (6.00 – 8.87)1 | 4.95 (3.15 – 6.75)1 | 3.63 (1.64 – 5.62)1 |
| Total baseline score | 0.44 (0.40 – 0.49)1 | 0.42 (0.37 – 0.47)1 | 0.41 (0.36 – 0.46)1 |
| HIV seropositive (vs negative) | 0.35 (−0.23 – 0.93) | 0.34 (−0.25 – 0.93) | 0.52 (−0.10 – 1.15) |
| Age at visit | −0.03 (−0.06 - - 0.001)2 |
−0.01 (−0.04 – 0.02) | −0.007 (−0.04 – 0.02) |
| Education (vs less than High school) |
|||
| High school | 0.88 (0.22 – 1.53)3 | 0.74 (0.08 – 1.41)2 | 0.30 (−0.41 – 1.02) |
| College | 1.57 (0.89 – 2.24)1 | 1.22 (0.51 – 1.92)1 | 0.62 (−0.15 – 1.39) |
| Income > $18,000 (vs <$18,000) | 1.03 (0.46 – 1.60)1 | 0.78 (0.20 – 1.37)2 | 0.68 (0.07 – 1.29)2 |
| Drug use (vs never used) | |||
| Former user | 0.73 (0.06 – 1.39)2 | 0.66 (−0.01 – 1.34) | 0.55 (−0.16 – 1.25) |
| Current user | 0.75 (−0.01 – 1.50) | 0.63 (−0.14 – 1.40) | 0.28 (−0.53 – 1.09) |
| Symbol digit | 0.06 (0.03 – 0.08)1 | 0.04 (0.01 – 0.07)2 | |
| WRAT4 | 0.09 (0.04 – 0.13)1 |
P ≤ 0.001
P ≤ 0.05
P ≤ 0.01
Wide Range Achievement Test
Discussion
Between 2006 and 2008, knowledge of cervical cancer prevention rose significantly in a cohort of women at high risk for cervical cancer, yet substantial deficits remained. Although most women could not identify the cervix as the part of the body assessed by Pap testing, most understood the purpose of Pap testing as well as the meaning and appropriate follow-up for abnormal results, with improvement in these knowledge areas over time. In 2008, most women still did not appreciate risk factors for cervical cancer. Of greatest concern, despite these improvements in knowledge, barely half of study participants actually believed cervical cancer to be preventable, suggesting that understanding may not be sufficient to alter beliefs.
Knowledge of HPV and HPV vaccination also improved significantly, but again gaps remain, perhaps because advertising became an even more dominant information source during the study interval. Many women do not appreciate that the target vaccine population is young girls rather than adult women, since the vaccine is prophylactic rather than therapeutic and the efficacy of vaccination in preventing cervical precancer declines with age and sexual experience (17). In combination with study staff and clinicians’ efforts at education, media coverage of and advertising for HPV vaccination appears to have communicated effectively the importance of vaccinations, while the vaccines’ limitations are less well understood.
Our findings are broadly consistent with those of others, who have found that knowledge of cervical cancer prevention, HPV, and HPV vaccination has improved since the introduction of HPV vaccination in 2006. Media coverage of HPV vaccine has not emphasized basic cervical cancer prevention concepts, and focused education by WIHS staff may have contributed to improvements we identified in these areas. Media coverage is likely to have contributed strongly to improvements identified in HPV infection and vaccine knowledge, as reflected in the substantial proportion of women who described media and advertising as information sources.
Kelly and colleagues found that exposure to media coverage of HPV has been associated with improved knowledge of HPV and cervical cancer, although they along with Wallace and Ache did identify deficiencies in media messages, specifically that new reports often lack information about the importance of continued Pap testing for vaccinated women (18, 19). Habel and colleagues similarly found that media messages after vaccine introduction lacked information about vaccine safety and side effects or about HPV and cervical cancer (20). In a study from Belgium, Donders and associates found that understanding of the oncogenic potential of HPV had improved since vaccine introduction, especially among younger and less educated women, yet many remained reluctant to embrace vaccination because of cost (21). Kelly and colleagues found that U.S. media reports around the time of introduction of HPV vaccination were associated temporally with a persistent increase in awareness of the link between HPV and cervical cancer, although awareness did not rise among less educated and minority women (22). In contrast, in interviews conducted soon after vaccine introduction, Marlow, Waller, and Wardle found that although awareness of HPV as a cause of cervical cancer had tripled since 2002, it remained only 2.5%, and few women understood the sexually transmitted nature of HPV infection (23). Like us, Hughes and associates similarly found that minority women were less aware of HPV vaccine and that advertising played a large role in HPV vaccine awareness, but they also found that clinicians and internet were women’s preferred sources (24).
Our study was limited by lack of a control group that did not receive education about cervical cancer risks and screening, omitted for ethical reasons in a population at high risk for cervical cancer with a history of noncompliance with colposcopy. We also could not determine whether improvements in knowledge were due to passive testing effects from repeated exposure to the same questions. However, the two-year lag between questionnaires may minimize testing effects. Our multivariable model, with an R2 of only 0.35, indicates that unmeasured factors accounted for 65% of the improvement in knowledge between 2006 and 2008. We could not determine the relative contribution of staff educational interventions, mass media coverage, advertising, and other sources. Finally, women who completed questionnaires at follow-up may have known more about cervical cancer prevention and HPV than those who did not, skewing scores upward in ways we cannot define.
Several years after the introduction of HPV vaccination, significant gaps persist in women’s understanding of cervical cancer prevention, HPV, and HPV vaccination. Clinician education, news and advertising messages, and our directed educational intervention have led to improvements in these areas, but improvements are weakest in knowledge about cervical cancer prevention in general. Low income women and those with lower reading skills may require specific targeted interventions, perhaps using nontraditional media such as video or internet based programs, and trials of interventions for these women are indicated.
Precis.
Between 2006 and 2008, women’s knowledge of cervical cancer prevention and human papillomavirus improved, although substantial gaps remain.
Acknowledgement
The authors thank the Women’s Interagency HIV Study (WIHS) Collaborative Study Group for data collection, with centers (Principal Investigators) at New York City/Bronx Consortium (Kathryn Anastos); Brooklyn, NY (Howard Minkoff); Washington DC Metropolitan Consortium (Mary Young); The Connie Wofsy Study Consortium of Northern California (Ruth Greenblatt); Los Angeles County/Southern California Consortium (Alexandra Levine); Chicago Consortium (Mardge Cohen); Data Coordinating Center (Stephen Gange).
The WIHS is funded by the National Institute of Allergy and Infectious Diseases (UO1-AI-35004, UO1-AI-31834, UO1-AI-34994, UO1-AI-34989, UO1-AI-34993, and UO1-AI-42590) and by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (UO1-HD-32632). The study is co-funded by the National Cancer Institute, the National Institute on Drug Abuse, and the National Institute on Deafness and Other Communication Disorders. Funding is also provided by the National Center for Research Resources (UCSF-CTSI Grant Number UL1 RR024131). H.D. Strickler was supported by NCI R01 CA85178-01.
The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of the NIH.
Footnotes
Financial Disclosure: The authors did not report any potential conflicts of interest.
Contributor Information
L. Stewart Massad, Washington University School of Medicine, St. Louis, MO
Charlesnika T. Evans, Department of Veterans Affairs Hines VA Medical Center and Northwestern University Feinberg School of Medicine, Chicago, IL
Kathleen M. Weber, The CORE Center at John H. Stroger Jr. Hospital of Cook County, Chicago, IL.
Johanna L. Goderre, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD
Nancy A. Hessol, University of California, San Francisco, CA.
Donna Henry, Montefiore Medical Center, Bronx, NY
Christine Colie, Georgetown University School of Medicine, Washington, DC
Howard D. Strickler, Albert Einstein College of Medicine, Bronx, NY
D. Heather Watts, Eunice Kennedy Shriver National Institute for Child Health and Human Development, Bethesda, MD
Tracey E. Wilson, State University of New York, Downstate Medical Center, Brooklyn, NY
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